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Review

Perceived Intensification in Harmful Algal Blooms Is a Wave of Cumulative Threat to the Aquatic Ecosystems

1
Research Center of Microbial Diversity and Sustainable Utilization, Chiang Mai University, Chiang Mai 50200, Thailand
2
College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China
3
Department of Biological Sciences, Faculty of Applied Sciences, Rajarata University of Sri Lanka, Mihintale 50300, Sri Lanka
4
Center for Yunnan Plateau Biological Resources Protection and Utilization, College of Biological Resource and Food Engineering, Qujing Normal University, Qujing 655011, China
*
Authors to whom correspondence should be addressed.
Biology 2022, 11(6), 852; https://doi.org/10.3390/biology11060852
Received: 24 April 2022 / Revised: 20 May 2022 / Accepted: 28 May 2022 / Published: 2 June 2022
(This article belongs to the Special Issue Impact of Natural and Anthropogenic Pollution on Aquatic Ecosystems)

Abstract

:

Simple Summary

Harmful algal blooms (HABs) are a serious threat to aquatic environments. The intensive expansion of HABs across the world is a warning signal of environmental deterioration. Global climatic change enforced variations in environmental factors causing stressed environments in aquatic ecosystems that favor the occurrence, distribution, and persistence of HABs. Perceived intensification in HABs increases toxin production, affecting the ecological quality as well as serious consequences on organisms including humans. This review outlines the causes and impacts of harmful algal blooms, including algal toxicity, grazing defense, management, control measures, emerging technologies, and their limitations for controlling HABs in aquatic ecosystems.

Abstract

Aquatic pollution is considered a major threat to sustainable development across the world, and deterioration of aquatic ecosystems is caused usually by harmful algal blooms (HABs). In recent times, HABs have gained attention from scientists to better understand these phenomena given that these blooms are increasing in intensity and distribution with considerable impacts on aquatic ecosystems. Many exogenous factors such as variations in climatic patterns, eutrophication, wind blowing, dust storms, and upwelling of water currents form these blooms. Globally, the HAB formation is increasing the toxicity in the natural water sources, ultimately leading the deleterious and hazardous effects on the aquatic fauna and flora. This review summarizes the types of HABs with their potential effects, toxicity, grazing defense, human health impacts, management, and control of these harmful entities. This review offers a systematic approach towards the understanding of HABs, eliciting to rethink the increasing threat caused by HABs in aquatic ecosystems across the world. Therefore, to mitigate this increasing threat to aquatic environments, advanced scientific research in ecology and environmental sciences should be prioritized.

1. Introduction

Over the last few decades, there has been an escalating and worrisome trend in the incidence of phenomena known as “Harmful Algal Blooms” (HABs). This term is very broad, covering the diverse nature of blooms, but, most specific, HAB is the word related mostly to the entities that cause harm, either by toxin production or cell accumulation in larger masses altering the normal food web dynamics [1,2]. Freshwater, brackish water, and marine ecosystems are usually inhabited by a diverse set of algal species including diatoms, flagellates, dinoflagellates, cyanobacteria, and chrysophyte that can cause the harmful blooms and may produce toxins that can harm other inhabiting organisms and human beings. With exposure to certain environmental conditions, such as rising temperature and nutrient accumulation (e.g., nitrates and phosphates), various phytoplankton species can grow excessively and create larger masses of algal blooms [3,4,5,6]. The events of HABs are characterized by the explosion and sporadic dominance of toxic or harmful algal species. In some cases, these cell masses gained higher abundances and their pigments discolor the freshwater, commonly called a “red tide” or “brown tide” [7,8]. However, among these blooms, many species do not have dominant cell numbers and cannot cause water discoloration but are still harmful because of potent toxin production leading to devastating effects [1].
Harmful algal blooms (HABs) especially cover the algal species that grow extensively on a global scale and can cause substantial damage while producing toxic or harmful effects on humans, fish, shellfish, marine animals, and birds [9,10]. Most of the harmful bloom-forming species belong to six different cyanobacterial and algal groups including cyanophytes, diatoms, dinoflagellates, haptophytes, raphidophytes, and pelagophytes, that widely differ in their morphological, physiological, and ecological characteristics [11]. Cyanobacterial bloom-forming species include Dolicho spermum, Aphanizomenon, Cylindrospermopsis, Gloeotrichia, Microcystis, Nodularia, Planktothrix, Pseudanabaena, Synechococcus, Trichodesmium, Woronichinia, and benthic HABs Lyngbya, Oscillatoria, Phormidium, and Scytonema [12]. Some of these genera thrive in both fresh and brackish water while some are widespread in marine ecosystems. Recurring cyanobacterial harmful algal blooms (cHABs) are evident in some of the world’s largest inland freshwater ecosystems, Lake Victoria (Africa), Lake Erie and Lake Michigan (USA–Canada), Lake Okeechobee (Florida, USA), Lake Pontchartrain (Louisiana, USA), and Lake Taihu (China) [13,14]. Whereas, species succession from small to large diatoms and dinoflagellates usually dominates the aquatic bodies over the spring to summer seasons [15,16]. However, some of the dinoflagellates Dinophysis acuminata, Prorocentrum minimum, and the diatom Pseudo-nitzschia multiseries expand aquatic ecosystems in late spring or summer seasons [13,17].
Increased amounts of nutrients (e.g., eutrophication) together with several other factors, such as suitable temperature, light intensity, and movement of species can contribute to HAB formation [18,19]. Eutrophication and other physical, biological, and chemical factors are responsible for modulating the effects of increased nutrient loading in aquatic environments, influencing HAB population dynamics [6]. The climatic changes including regional and global warming may also favor the initiation, magnitude, duration, and distribution of HABs by disturbing dynamics of programmed algal cell death [20]. The spatial variations in climatic patterns are expected to expand the geographic ranges of benthic harmful algal blooms (BHABs) [21,22,23]. Whereas, the strong alterations of atmospheric and oceanic circulation dynamics in the southeastern Pacific Ocean were also linked to massive HABs in 2016 [24]. It is assumed that the surface temperatures in the world’s oceans are projected to warm by 0.4–1.4 °C by the mid-21st century, causing many tropical and sub-tropical harmful dinoflagellate genera such as Gambierdiscus, Fukuyoa, and Ostreopsis BHABs to exhibit higher growth rates over much of their current geographic range, resulting in higher population densities [25]. Moreover, the coastal waters have experienced progressive warming, acidification, and deoxygenation that will intensify this century, at the same time the impacts on the ecosystem from HABs have all increased over the past few decades [26]. Therefore, the wave of increasing threat by HABs in aquatic environments is accelerating and it needs to be explored at a larger scale for aquatic environment sustainability.
Expansion of global HABs has gained enough recognition; however, the bloom formation events were not sufficiently studied even though many countries were facing the bewildering array of their impacts [27,28]. Various bloom-forming dinoflagellate species have been documented as common species such as Prorocentrum minimum expanding throughout the world coastlines with escalating eutrophication [29]. Likewise, in the US HABs significantly increased their frequency and abundance leading to high aquatic contamination and bewildering effects in various parts from the 1980s to 2018 [30,31,32,33]. Similarly, in Europe and Asia, algal bloom formation is increasing with more potent toxic effects than in previous decades [34]. Whereas, in the past decade Arabian regions also faced the massive expansion of HABs [35]. However, these challenges are mirrored globally with recent examples, including an expansion of various harmful algal species such as Pseudochattonella cf. verruculosa in the south and Alexandrium catenella in the north in Chile, leading to massive fishery cessations in 2016, and disruption by Alexandrium catenella in Tasmania, southeastern Australia, from 2012 to 2017 of the fishing industry in poorly monitored coastal waters [24,33,36]. HABs significantly affect the water quality, by damaging its aesthetic value, causing oxygen deficiency, aquatic toxification, and affecting the biodiversity by higher mortalities of marine biota [37,38,39,40,41]. Apart from the toxic effects, HABs have also stressed socio-economic infrastructure including food trade, recreation, tourism, and sports [42]. The high degree of spatio-temporal heterogeneity in species composition, non-point source factors responsible for HABs formation, and imperfect biomass–toxicity relationships have caused a major challenge in understanding, forecasting, mitigating, and controlling the events of HABs across the aquatic environments. The most critical component in predicting, understanding, and addressing the substantial socio-economic, ecological, and human health concerns posed by HABs lies in research studies and management or monitoring communities capable of: (a) understanding the general and specific factors and mechanisms contributing to the formation of HABs, (b) vigorously detecting the biomass changes, especially most dominant and hazardous taxa, and (c) indicating the early toxicity information and possible remedies of mitigation to minimize the economic losses. To highlight the threat of HABs to aquatic environments, however, this review summarizes some major factors influencing the formation of HABs, toxicity, economic and ecological impacts, human health impacts, grazing defense, and management of HABs.

2. Factors Influencing the Formation of Harmful Algal Blooms (HABs)

There is a growing body of scientific literature focused on the influence of factors such as climatic change and eutrophication individually. However, due to the lack of literature, there is a concern for climatic change and its associated factors to be summarized along with other factors in one study. Therefore, in this review, an extensive effort was made to summarize the literature about various exogenous factors influencing the formation of HABs.

2.1. Interaction between Climatic Changes and Other Stressors

Griffith and Gobler [43] discussed climate change as a co-stressor to HABs, causing warming, acidification, and deoxygenation to provoke intensifying impacts of HABs in aquatic ecosystems. For deep understanding, the authors demonstrated the co-occurrence of climate change in coastal zones and co-effects of climate change stressors and HABs on aquatic life. Their review discussed the ecological and physiological framework for considering HABs as a climate change co-stressor and considers the consequences of their combined occurrence for coastal ecosystems. It also emphasized the importance of the inclusion of HAB species in experiments and monitoring programs that take into account the effects of multiple climate change stressors, as this will provide a more ecologically relevant perspective of the ecosystem structure and function of climate-altered systems in the future.
Wells et al. [44] demonstrated linkages between fisheries and aquaculture with experimental work specifically highlighting the application of experimental and field studies, extended observational programs, and retrospective studies, for an in-depth understanding of the socio-economic effects of HABs and climate change. Further, temperature variations, nutrient availability, precipitation, ocean acidification, and the physical structure of the water column, all influence the composition, productivity, and global range of phytoplankton accumulations. However, large uncertainty remains about how these climate drivers’ integration strengthens the shape of HABs in the future. They also mentioned that cyanobacterial HABs, benthic HABs, and HAB effects on fisheries are all concerned with the effects of temperature, light, stratification, salinity, storm severity, ocean acidification, nutrients, and grazer drivers on microalgae. Gobler [45] demonstrated that HABs displayed range expansion since 1980 and increased frequency in response to climatic change. These changes have brought increasing trends in HABs, which are partly due to the effects of thermal stress in marine ecosystems, particularly marine heatwaves, oxygen loss, ocean warming, increasing pollution intensity, and eutrophication. Consequently, these diversified HAB trends have negative impacts on human health, the local economy, tourism, and food security issues as well. Furthermore, the report outlined a number of connections between thermal waves and HABs. However, it has also been documented that anthropogenic interventions, climatic change, and individual events driven by regional, local, and global drivers promoted the trends of HABs globally. Ralston and Moore [46] discussed the utility of statistical models as well as the strengths and weaknesses of these models to model the HAB responses to climatic changes. They evaluate the HAB models with extensive observations and formulate suggestions for researchers to move forward in developing models that are more robust to project the impacts of climate change on HABs. Suggestions to assess the prolonged trends of HABs associated with climatic changes were also drawn from this work. Their review outlined that the statistical models widely employed for forecasting the near-term HABs and resource management, according to their analysis, are not well adapted for longer-term projections since forcing circumstances may differ from previous observations. Process-based models, on the other hand, are difficult to parameterize, require extensive calibration, and are more complicated, but they may predict the HAB response mechanistically under varying conditions. However, process-based models are vulnerable to failure if crucial processes emerge because of climate change that was not recognized during the development of the model. Furthermore, as resource managers and policymakers demand more forecasts of HAB consequences for both short and long time periods, modeling research based on HAB response to climate change will certainly expand. Such HAB models will be critical in informing the development of solution strategies to minimize the public health and socioeconomic impacts as well as build socio-ecological system resilience to future HABs.
Hennon and Dyhrman [47] discussed that during the last 20 years omics techniques such as transcriptomics, metabolomics, omics, genomics, and proteomics transformed the landscape data of several fields including HABs studies. Technological advancements have provided a breakthrough to create many omics datasets that are complementary and publicly available and provide new insights on HAB formation and toxin production. Genomic analysis on the other hand has been utilized to uncover the differences in nutritional requirements and toxicity mechanisms. Whereas, proteomics and transcriptomics have been employed to explore the responses of HAB species to environmental stressors while metabolomics can reveal toxicity and allelopathy mechanisms. The omics data, however, could be leveraged for improvements in predictions on how climate change will impact the dynamics of HABs. For a better and deeper understanding, the co-occurrence or interaction between climatic changes and temperature variations with other stressors are also summarized in this section. As climate change is considered as an important factor in HABs formation, associated changes such as increasing temperature and precipitation are of wide ranges and no certainties exist regarding their effects on flow and stratification [13]. Climatic change causes spatio-temporal variations in the hydrological aspects and rainfall patterns, which have increasing effects on the over-enrichment of nutrients modulating the HABs [48]. Therefore, the variability in patterns of rainfall significantly impacts sediment and nutrient delivery. Flushing, water residence time, metabolism, sediment-water exchange, and vertical stratification, may affect the persistence and dominance of HABs [12,49,50]. Some of the species such as rhodophytes and dinoflagellates increased rapidly while some are mostly dominating, for example, Dinophysis acuminata, Prorocentrum minimum, Chattonella antiqua, and Fibrocapsa japonica were favored by these factors in coastal zones of the North Sea [13].
The interaction between climatic change and temperature variations is directly correlated with the growth of phytoplankton, because their growth increased rapidly with increased temperature [51]. Numerous studies have reported the higher algal biomass in temperature ranges of 25–30°C [52]. However, variations in temperature affect the cyclic patterns of water that may change the physiological structure of water by elongating the stratification period in turn, which favors the HAB formation [11]. Similarly, global warming is associated with temperature changes, which significantly affect aquatic ecosystems. If the average value of temperature increases, this might have a direct effect on algal blooms. Globally, increased temperature up to 1.5–5 °C is direct evidence of increased bloom formation during this century [53]. At this rate, if the temperature reaches or exceeds 20 °C, it will have an inverse relation with eukaryotic phytoplankton whose growth will be stopped or decreased while giving a competitive benefit to cyanobacteria by increasing their growth [13]. On the other hand, relationships between temperature, growth rate, and toxin production are highly strain-specific and species-specific. Like temperature increases (up to 25 °C), generally, the growth of Dinophysis spp. is promoted [54]. For other toxin-producing species, inverse relationships between toxin production and growth rate have been described. Specifically, the growth of Alexandrium spp. increases with temperature in a strain-specific manner. Toxin content is generally greater among slower-growing cells maintained at lower temperatures [55,56]. Similarly, toxin content (per cell) of yessotoxin-producing dinoflagellates within the genera Protoceratium is greater within slowly dividing cells [57,58].
Drastic climate change and increasing temperature also cause an imbalance in photosynthetic activities and phosphorylation mechanisms. Atmospheric carbon dioxide was previously increased at a rate of 1% per year, while it reaches 3% annually now and up to 800 ppm is expected at the end of this century [59]. Due to the rise in CO2, the chemical composition of water will alter with declining pH and carbonate ions, and it is understandable that cyanobacteria are favored by low dissolved inorganic carbon [60]. Alternatively, it competes with eukaryotic algae under high pH and low carbon dioxide conditions [61]. Under high CO2 the toxin production including saxitoxins by several harmful algae (e.g., Alexandrium spp.) increases [62]. However, species-specific responses always do not follow the common trends. For example, growth and toxin production by A. catenella and A. ostenfeldii are expected to increase under high CO2 levels [63,64]. Furthermore, low pH may decrease the rate of cell division in some cyanobacteria species that promote bloom formation [65]. Strain-specific differences have been reported for P. multiseries, with some groups reporting an increase in growth and toxin production at low pH [66,67]. For harmful cyanobacteria, the responses to acidification are phenotype-specific. Some toxic strains lose their competitive advantages over non-toxic ones at low pH, and others become more competitive [68,69,70]. While some cyanobacteria decrease the rates of their cell division in response to low pH conditions [65,71,72]. However, laboratory and field studies demonstrated that other cyanobacteria respond to increase CO2 with increased cell division and carbon fixation, or both [73,74,75,76,77].
Climatic changes may also affect the salinity in estuaries and freshwater systems due to rising sea levels, an increase in drought frequency and duration in some regions and a concomitant increase in desiccation, or in other areas, increases in precipitation due to storms [78,79]. Although many phytoplankton species have no tolerance to salinity changes, however, some species, such as Lyngbya and Trichodesmium are able to survive in environments with euryhaline patterns [80]. Thus, changes in salinity may cause the shifts in phytoplankton communities and it may affect the composition of the community and potentially toxic concentrations [81]. Overall, warmer temperatures are beneficial for some HABs with expanded realized niche and accelerated growth [26,28,82,83,84]. A species-specific relationship exists between temperature, growth rate, and toxicity in some algal species. For example, the promoted growth and increased diarrhetic shellfish poisoning in Dinophysis spp. observed with increasing temperature up to 25 °C [43,54]. For some other toxin-producing species, there is an inverse relationship between growth and toxin production such as Alexandrium spp. which has increased growth at the optimum temperature of 15 °C, and increased toxin production at a higher temperature of 22 °C [55,56]. However, for other species, the relationship between temperature, growth, and toxin production is variable [85]. A number of studies investigated the impacts of warming/temperature on the growth rate and toxin profile of HABs. However, some of them have summarized the important interactions between marine and freshwater HABs with other stressors and toxin activity. In summary, the interaction between climatic patterns and other environmental stressors is a diverse phenomenon; critically, rainfall patterns may alter the population dynamics of HABs.

2.2. Nutrient Flooding and Eutrophication

Heisler et al. [5] in a scientific consensus on eutrophication and HABs revealed that degraded water quality from increased nutrient pollution promotes the development and persistence of many HABs. The composition, not just the total quantity of the nutrient pool affects the HABs, both chronic and episodic nutrient delivery promotes the HAB development [5]. O’Neil et al. [18] highlighted that eutrophication may promote proliferation and expansion of cHABs, particularly cyanobacterial genera from freshwater (Microcystis, Anabaena, Cylindrospermopsis), estuarine (Nodularia, Aphanizomenon), and marine ecosystems (Lyngbya, Synechococcus, Trichodesmium). Zohdi and Abbaspour [42] demonstrated that in eutrophic regions, the growth rate of HABs is maximum due to the entry of contaminated river flow and organic wastewater, which includes more than 10 ng/L of vitamin B12 concentration. Furthermore, among the potential drivers contributing to HAB events, the role of nutrient inputs has gained the most attention worldwide. Overpopulation of human beings enhanced the cultural nutrient loading which tracks their way and empties into the aquatic resources causing larger and fast bloom formation [5,29,86]. As freshwater bodies get enriched with nutrients, mainly phosphorus, a community shift may occur leading to the dominance of phytoplankton biomasses [18,82]. in the same way, phosphorus may promote akinete production in Anabena spp. as well, in limited nutrient conditions, P also favors the growth of Microcystis [18,87]. These changes are best exemplified by dense bloom formation in newly eutrophic rivers, lakes, and reservoirs that were previously devoid of cHABs [18]. For example, Pampulha reservoir in Brazil and Taihu lake in China faced dense and persistent cyanobacterial blooms [88,89].
Intensified anthropogenic interventions in the form of industrial waste and sewage disposal in aquatic ecosystems containing nitrates, ammonia, and phosphates also favor the HAB formation [90]. A higher quantity of phosphates in coastal water increased the ratio of nutrients that highly influenced the growth of harmful and nontoxic blooms. Some species are usually nontoxic but if they are exposed to different nutrient concentrations, they become toxic in cultural nutrient loading [91]. Evidence suggests that N may be equally or more important than P in the occurrence of toxic, non-diazotrophic cyanobacteria blooms such as Microcystis. Further, laboratory investigations demonstrated that increasing N concentrations generally increase the Microcystis growth and toxicity [18]. Thus, as nutrient loading increases the ratio of phosphorous and nitrogen to silicates, it favors the growth of harmful algal species including some non-diatoms. For example, in the Black Sea, silicate concentration decreases causing an escalation in blooms of flagellates and diatoms [11]. It is also believed that low nitrogen to phosphate ratios, or higher phosphate ratios could favor cyanobacterial blooms [92,93]. In addition, micronutrients such as trace metals also favor phytoplankton growth and have a critical role in the assimilation of essential macronutrients, photosynthesis, and toxicity of some algal species. The phenomenon of eutrophication produced HABs, which in turn produces harmful toxins and the activities of these toxins ultimately affect the vulnerability of aquatic organisms (Table 1).
Table 1. Summary of known interactions between marine and freshwater harmful algal blooms and other stressors.
Table 1. Summary of known interactions between marine and freshwater harmful algal blooms and other stressors.
FactorsStressorHABs SpeciesStrainToxic MechanismTest OrganismEffects or ObservationsReference
Climate changesThermal stressMicrocystis aeruginosaUV-006MicrocystinMus musculus (Mouse)Diminished toxicity at warmer temperatures[94]
Climate changesThermal stressMicrocystis aeruginosaM228MicrocystinMus musculus (Mouse)Higher LD50 at a warmer temperature[95]
Climate changesThermal stressCochlodinium polykrikoidesCP1Reactive oxygen species (ROS)Argopecten irradians
(bay scallop)
Increased toxicity (i.e., inhibited swimming by larval scallops) at cold temperature[96]
Climate changesThermal stressCochlodinium polykrikoidesCP1Reactive oxygen species (ROS)Mercenaria mercenaria
(hard clam, northern quahog)
Increased lethality at cold temperature[96]
Climate changesThermal stressCochlodinium polykrikoidesCP1, field samplesReactive oxygen species (ROS)Menidia berrylina (inland silverside)Increased lethality at cold temperature[96]
Climate changesThermal stressMicrocystis aeruginosaCP1,
CPSB-1 G
MicrocystinCyprinodon variegatus (sheephead minnow)Increased lethality at cold temperature[96]
Climate changesThermal stressMicrocystis aeruginosaPurified toxins-MCLRMicrocystinDanio rerio (zebrafish)Increased toxicity at warmer temperatures[97]
Climate changesThermal stressHeterosigma akashiwoPurified toxins-MCLRNAMoina macrocopa (freshwater daphnids)Increased toxicity at warmer temperatures[98]
EutrophicationAcidificationAureococcus anophagefferensCCMP 2393Unidentified toxinsNAIncreased swimming speed and net-down movement of algal cells in high pCO2 environments[99]
EutrophicationAcidificationAureococcus anophagefferensCCMP 1984Unidentified toxinsArgopecten irradiansIncreased lethality in low pH treatments[100]
EutrophicationAcidificationCochlodinium polykrikoidesCCMP 1984Unidentified toxinsCrassostrea virginica
(eastern oyster)
Increased lethality in low pH treatments[100]
EutrophicationAcidificationCochlodinium polykrikoidesCP1Reactive oxygen species (ROS)Mercenaria mercenariaIncreased mortality by larvae in acidification treatments[101]
EutrophicationAcidificationMicrocystis aeruginosaCP1Reactive oxygen species (ROS)Argopecten irradiansIncreased mortality by larvae in acidification treatments[96]
UpwellingHypoxiaMicrocystis aeruginosaFACHB-905MicrocystinHyriopsis cumingii
(sail mussel)
Reduced scope for growth among mussels within hypoxic treatments[102]
UpwellingHypoxiaMicrocystis aeruginosaFACHB-905MicrocystinHyriopsis cumingii
(sail mussel)
Diminished immune response among mussels within hypoxic treatments[103]
UpwellingHypoxiaMicrocystis aeruginosaFACHB-905MicrocystinHyriopsis cumingii
(sail mussel)
Increase cellular damage among mussels within hypoxic treatments[104]
UpwellingHypoxiaStephanopyxis palmerianaNAUnidentified toxinsNAIncreased seasonal toxicity[105]
Organic fertilizers from animal farming flushed out into the seawater are the major contributors to eutrophication in coastal regions. Vertical nutrient mixing can form heavy biomass, causing anoxia and detriment to the ecosystem [11]. Flushing of rainwater into the sea also increases the nutrients and algal biomass, as reported in the regions of the Black Sea and the Caspian Sea. On the Texas coast in 1935, heavy rainfall caused excessive phytoplankton blooms [106,107]. Whereas, the unusual rainfall in other places also caused events of L. polyedrum blooms, e.g., in Santa Barbara and south of the Mexican border due to enriched coastal water [1]. Garcia-Hernandez et al. [108] reported that increased shrimp farming activity might drastically change the Rhaphidophytes, diatoms, and dinoflagellate blooms, which may occur because of heavy discharge of nutrients ultimately leading to the increased eutrophication that triggers algal bloom formation. Interactive effects of eutrophication/nutrient flooding and HABs are diverse and complex; however, much of the current knowledge provides insights into these processes which seems to enhance the frequency and magnitude of these events in the future.

2.3. Events of Upwelling

The vertical or upward movement that causes circulation and increases productivity in the photic zone, which in turn changes the environmental conditions and nutrient content is termed upwelling [10]. Upwelling zones are considered the world’s best productive areas, whereas some researchers reported that upwelling could halt the occurrence of red tide. The phenomenon of upwelling that occurred between 1998 and 2004 was associated with HAB events in Hong Kong during summer, which occurred in conjunction with Manson winds and river water runoff [106,107]. Some studies in India were conducted along Dakshina Kannada coast and reported the occurrence of upwelling from March to October in that region, which was associated with HABs on the southwest coast of India [105]. Kun Kaak Bay in the south of Sonora, Mexico and northwest of Kino Bay have high productivity suggesting the upwelling of currents, and in the past, the diatom blooming species (e.g., Stephanopyxis palmeriana) were more common blooms. Similarly, red tide nontoxic blooms are commonly found in the Gulf of California. Mesodinium rubrum is a more common red tide algal species that was also associated with upwelling in these regions [108]. Events of upwelling mostly influenced the mixing of water layers, producing an imbalance in the mixture of water and gases; particularly, hypoxic conditions lead to the development of blooms and might cause serious toxicity to organisms [42,102,103,104]. However, the events of upwelling interact with climatic changes. HAB dynamics have traditionally been challenging to quantify, however, continuous efforts can push through this emerging challenge.

2.4. Wind Pressure/Strength and Dust Storms

Wind can contribute to the upwelling of deeper water layers rich with nutrients, which enhances the opportunity for HAB formation. Similarly, dust storms rich with iron increased nutrients in the sea when blowing through large desert areas such as the Sahara. In east coastal regions of North America, iron is considered a contributing factor to red tides [106]. The University of South Florida reported in their satellite-based observations, that clouds of dust blowing over the Sahara Desert and across the Gulf of Mexico and the Atlantic Ocean are the major factors responsible for red tides and the water of West Florida is provided with iron from these giant clouds [109]. Trichodesmium, a cyanobacterial genus, utilizes this iron from dust to fix atmospheric N2 that makes the environment of the Gulf of Mexico productive for toxic algae forming the red tides [109]. Albert et al. [3] reported some factors responsible in coastal Queensland (Australia) for Lyngbya majuscula blooming. During rainfall, water carried phosphorous, iron, and other organic contaminants to the coastal region. The combination of iron and phosphorous is required for L. majuscula to enhance its photosynthetic activity which expands its population and forms larger blooms. Iron is considered an important source for nitrogen acquisition and when the iron is highly available there is a high chance of brown tides, for example, brown tide bloom produced by Aureococcus anophagefferens is associated with high iron availability. The events that occurred in the Peconic estuary, New York, USA, may be explained by these observations [110]. Additionally, higher concentrations of heavy metals such as Pd and Cd in untreated nutrient-rich effluents originating from aquacultural practices is also a good example of increasing metal toxicity in oceans leading to the formation of HABs [108].

2.5. Discharge of Ships/Ballast Waters

It is estimated that the ballast waters of ships’ tanks can transfer approximately 300 billion dinoflagellates [42]. In the Persian Gulf during 2008, the occurrence of a red tide was predicted to be caused by the ballast water of ships along the Qatar and Kuwait routes [111]. Noctiluca dinoflagellate growth has increased, causing red tides as a result of oil spills from ships [96]. Wastewater containing pathogens and nutrients discharged from ships results in increased eutrophication, algal growth, and a decrease in soluble oxygen in water [112]. Anil et al. [113] observed that the spreading of harmful algal species via ballast water is very limited; however, ballast water may serve as a vector for the dispersal of harmful algal bloom species. For example, Monostroma oxyspermum, an algal species, was introduced from the northwest pacific and northeast Atlantic to India’s west coast due to the discharge of ballast waters [114]. The bloom formation by shipping from other oceans increases the susceptibility of HABs; however, large-scale studies are required to explore the causes of fast-spreading HAB species [114].

2.6. Other Factors Involved

Photosynthetic characteristics of phytoplankton indicated that their growth required enough light penetration, light intensity, and day/night durations. Mostly, the arousal of red tides was observed during warm sunny periods, which indicated the importance of light factors for these tidal formations [42]. Among other factors, one prominent cause of red tide algal blooming is also favored by their lower consumption by consumers and their grazers [106]. Unhealthy corals also favor bloom formation because the deposition of sediments makes the corals unhealthy or dead, whereas other zooplankton and fish death in the food web later covers the crust with calcareous matter and algae leading to bloom formation [115]. Volcanos and earthquakes on the seabed cause heat generation due to earth layer friction and increase the possibility of dissolving materials such as iron and mineral compounds in water. For example, in 2010, iron-dissolved ash from the Eyjafjallajökull volcano created an algal bloom in the North Atlantic [42]. Collectively, whatever the causes or reasons, globally aquatic resources especially in the coastal regions are now subjected to an unprecedented variety and frequency of HAB events.

3. Impacts of Harmful Algal Blooms (HABs)

HABs have large ecological and socioeconomic costs, affecting agriculture, real estate, food web resilience, water quality, fisheries, drinking water, tourism, and habitats, contributing to fish death and anoxia [116]. These effects can result in fish death involving thousands of fish and other marine life, leading to the degradation of the ecosystem [117]. Major impacts of HABs are summarized in the sections below.

3.1. Shellfish Poisoning

When toxic blooms are filtered by shellfish as their food source, the shellfish accumulate toxins in them up to dangerous levels for humans and other consumers. These toxicity events lead to poisoning syndromes such as amnesic shellfish poisoning (ASP), neurotoxic shellfish poisoning (NSP), paralytic shellfish poisoning (PSP), Ciguatera fish poisoning (CFP), diarrhetic shellfish poisoning (DSP), and cyanobacterial toxin poisoning. Besides these, there are many species that cause water discoloration, some are non-toxic to humans but lethal for invertebrates. Marine microalgae are important food for the inhabiting fauna from their early life stages, particularly mussels, clams, oysters, scallops, finfish, protozoans, and crustaceans. However, more than 5000 species of these microalgae have been identified [117], and out of these, only 300 contribute to the formation of red tides in marine ecosystems [118].
More than 50 species or so have been identified to produce toxins and cause human physiological mechanisms by fish or shellfish poisoning. Globally important harmful algal bloom species that cause paralytic shellfish poisoning (PSP) are Alexandrium catenella, A. cohorticula, A. fundyense, A. fraterculus, A. minutum, A. tamarense, Gymnodinium catenatum, Pyrodinium bahamense, and Lyngbya spp. Some calcareous macroalgae; those that cause diarrhetic shellfish poisoning (DSP) include: Dinophysis acuta, D. acuminate, D. caudata, D. fortii, D. norvegica, D. mitra, D. rotundata, D. sacculus, and Prorocentrum lima. Amnesic shellfish poisoning (ASP); Pseudo-nitzschia australis, P. delicatissima, P. multiseries, P. pseudodelicatissima, P. pungens, and P. seriata. Ciguatera fish poisoning (CFP): Gambierdiscus toxicus, Coolia monotis, and Fukuyoa spp. Neurotoxic shellfish poisoning (NSP): Karenia brevis, K. papilionacea, K. selliformis, and K. bicuneiformis. Cyanobacterial toxin poisoning: Anabaena circinalis, Microcystis aeruginosa, Nodularia spumigena, Pfiesteria piscicida, and P. shumwayae. Those producing harmless water discolorations are: Akashiwo sanguinea, Gonyaulax polygramma, Noctiluca scintillans, Scrippsiella trochoidea, and Trichodesmium erythraeum. While, some notorious species which are harmful to invertebrates and fish, but non-toxic to humans include: Chaetoceros concavicorne, C. convolutes, Karenia mikimotoi, K. brevisulcata, Karlodinium micrum, Chrysochromulina polylepis, Prymnesium parvum, P. patelliferum, Heterosigma akashiwo, Chattonella antiqua, C. marina, and C. verruculosa [1,118,119].

3.2. Human Health Impacts and Toxin Production by HABs

Marine toxin diseases are categorized based on their trans-vector types. For example, shellfish carry toxins that lead to paralytic shellfish poisoning. Paralytic shellfish poisoning is caused by the shellfish that carried potential toxins of the disease. Whereas, poisoning through mollusks also occurred during algal bloom episodes. However, fish poisoning is regional and usually associated with fish or specific reefs. Bloom episodes of Pfiesteria dinoflagellate in estuaries of the Southern Atlantic coast and middle suggest that anthropogenic pressure on the aquatic environment aggravated the existing conditions. Consequently, this anthropogenic stress resulted in fish death and human health hazards [120]. Additionally, humans could be exposed to the toxins directly released into the air or water. This phenomenon occurs naturally or through human activities such as water treatment causing turbulence in the water and leading to the direct release of toxins by cell disruption. Toxins can enter the body through inhalation, causing associated respiratory symptoms such as irritation, coughing, and other ailments [117]. However, the phenomenon of algal toxicity and the interaction of human health hazards to this toxicity is very diverse and complex. Some major categories of algal toxins more commonly causing human health concerns are summarized in this section.
Furthermore, the production of phycotoxins changes with geographical location, and novel toxins are detected with spatial variation leading to serious toxic events. Variations in temporal patterns and fluctuations in environmental factors also influence the rates of toxin production within blooms [12,28,121,122]. Phycotoxins including cyanotoxins produced by cyanobacteria, and marine biotoxins produced by various harmful algal blooms species, can be lethal to a variety of organisms and human beings [123,124]. Some of the important phycotoxins are summarized in Table 2.

3.3. Ecological and Economic Impacts of HABs

The complex phenomenon of chemical signaling from HAB species can make it more complicated and difficult to comprehend the important and variable effects of HABs on organisms and ecosystems. HAB species have a variety of poisonous, noxious, or allelochemical qualities that allow them to escape from some effects and predation [125]. Micro-zooplankton and meso-zooplankton members could not consume the toxic HAB species often; however, these deterrent properties may be highly species-specific or condition-specific [33,126,127]. Toxins and allelochemicals of HABs may have potential impacts on the communities of organisms elsewhere in the food chain or food web, such as microbial food web alteration, especially when grazing pressures are low [128]. Such large-scale ecological problems of HABs have been notoriously difficult to evaluate and quantify.
The economic effects of HABs are variable and highly diversified, and the accurate costs of HABs are difficult to assess. However, some studies reported their conclusions, for example, Hoagland et al. [129] estimated the annual economic effects of HABs in the USA between 1987 and 1992. At that time, the economic effects were valued at USD 50.0 million per year. Anderson et al. [130] reported approximately the effect of USD 50 million on the US economy per year. These losses were mostly due to the commercial fisheries and human health impacts on marine ecosystems. Whereas, in freshwater ecosystems estimated losses in the US were USD 4.6 billion per year, related to the potential eutrophication [131]. Most of the studies have focused on the events of HABs in the US; however, exact costs are still difficult to assess [132]. Few other exceptions also exist. In Canada, the human health costs were (670,000 CAD/year), in the UK up to 118,00 GBP/year due to the impacts on commercial fisheries [133], whereas in other European countries the costs for monitoring and management range from EUR 30,000 to over EUR 7 billion/year [134,135]. In Australia, the estimated cost was AUD 1–8.7 million AUD/year [136], and in New Zealand approximately 50,000/quarter NZD [33].
The dire need to predict and minimize the above-mentioned HAB incidents offers a powerful impetus for the investment in research and management measures. Furthermore, Bernard et al. [137] assessed that the annual economic losses by HABs in freshwater and marine ecosystems as of 2014 could be at USD ±10 billion. However, based on this calculation and using the typical value of information (VOI), the estimate of the resource is 1% [138]. Whereas, a comprehensive system for detecting and forecasting the HAB information would represent the value of USD ±100 million annually. This would be the first and most reasonable estimate for the assumption of “how much and how should” be capitalized in the monitoring efforts for HABs [33].

3.4. Other Negative Impacts of HABs

3.4.1. Effects on Aquaculture Food Production and Water Supply

HABs have negative effects on aquaculture and shellfish aquaculture because the shellfish have the ability to accumulate phycotoxins in their body by filtering during feeding, which also impacts their survival, life, history, and body structure [119,139]. Despite the large geographical distribution and negative impacts of HABs on aquaculture, accurate calculations for the estimated loss are difficult; however, some studies rigorously provided insights on this issue. According to FAO (2006), certain HABs constitute serious threats to aquaculture food production, that are linked to decreasing wild fish stocks, which have become a major protein source for coastal human populations [140]. The most effective strategy to protect humans from seafood poisoning related to HABs in farming and wild harvest of shellfish is to monitor the HAB species and biotoxins to implement the periodic closures of recreational, harvesting, growing, or commercial areas [141]. Moreover, the contamination of seafood items and products can result in financial losses in shellfish collection and cultivation, as well as certain finfish aquaculture. Besides these, other losses in auxiliary industries may be the distribution, processing, retailing, and wholesaling of seafood [142,143].
Zohdi and Abbaspour [140] found that HABs discolor coastal waters and harm the water quality. This issue results in damaging desalination systems and equipment, ships, and shore facilities. For instance, the Toledo water treatment plant could not treat the water to a safe level in 2014, so authorities gave hints to its 500,000 residents not to drink tap water. Kenya in 2004, China in 2007, and Australia in 2016 experienced similar incidents.

3.4.2. Effects on Other Organisms

Mostly the presence of HABs is associated with large mortalities of fish, sea turtles, seabirds, mammals, and marine organisms. The whole cycle of toxin transfer can be considered as HABs release toxins that can be accumulated by oysters (shellfish), accumulating the toxin in their body and transferring it to other fish that consume oysters as food. Furthermore, as the food web continues these toxins enter human bodies by consuming seafood; however, this phenomenon can cause economic loss and also severe illness. Paradigms of ecological risk that attempt to determine the toxic effects of harmful algal blooms on the coastal ecosystem are actually analogous to, and also evolved from, the human health risk assessment context [144]. HABs also cause acute/chronic effects in mammals and other organisms including humans worldwide by producing harmful toxins [116]. Moreover, the toxin production of harmful algal blooms such as Alexandrium tamarense and Gymnodinium catenatum at high concentrations decreased the growth of protozoan communities [145]. Naturally occurring toxins within the HABs have the potential to kill fish, shellfish, and other microorganisms directly, or they may be retained in the bodies of these organisms and later could be transferred to the food webs [146,147]. Currently, ecological risk assessment has some limitations. Human health risk assessments posed by toxin production associated with algal species are definite but their mode of action and their respective classes are still speculative. Interacting populations of many algal species vary according to the spatio-temporal patterns and their toxin profile is also influenced by location and time duration [144]. However, we summarized the important harmful phycotoxins classes with clinical implications on humans.

3.5. Grazing Defense by HABs

3.5.1. Defense of Phytoplankton against Grazers

During favorable nutrient loading conditions, the phytoplankton biomass increases. If certain factors depress the abundance of zooplankton the balance between phytoplankton and zooplankton biomasses is disturbed; then, phytoplanktons ultimately increase their population and cause blooms. Consequently, it is difficult for grazers to graze the density of these blooms on a normal ratio. As a result, some density-dependent toxins and extracellular polysaccharides might be present in the blooms causing harmful effects on the grazers. The best example of such a defense is shown by Aureococcus anophagefferens and Aureoumbra lagunensis during the 1985 and 1990–1997 blooms in Narragansett Bay at low grazer abundance periods [7,148]. This phenomenon makes it risky for the grazers to feed on the toxic phytoplankton at higher biomass and they show less grazing response to these toxic species [8,149]. However, if the algal population is low or normal, the growth rate of protozoans increases with an increase in food density until it reaches a specific maximum level [150,151,152].
Feeding by zooplanktons on harmful algal species also puts them into the category of HAB predators [153,154,155,156]. The population density of microzooplankton and their prey phytoplankton have equivalent growth rates [157]. Therefore, it is possible that grazing on HABs might result in optimal reproduction and growth in protozoan communities [158,159]. However, some grazers including protozoans and copepods successfully graze on some toxic dinoflagellates such as Alexandrium, Gymnodinium, Prorocentrum minimum, or Heterocapsa circularisquama without any apparent harm [156,158,159]. In a recent bioassay experiment on two harmful algal blooms, Alexandrium tamarense and Gymnodinium catenatum, increased feeding of periphytic ciliates on these blooms up to the algal concentrations of 102 to 104 cells mL−1 was reported [145]. Additionally, Favella ehrenbergii is a protozoan considered a voracious grazer of (Alexandrium tamarense) blooms [160].
During blooms, an increase in phytoplankton biomass will lead to an increase in respiration rates and total oxygen demand by both autotrophs and heterotrophs and this may lead to hypoxic conditions. In eutrophic bays, estuaries, and coastal lagoons, high photosynthetic activity and heavy phytoplankton biomass may lead to an increased pH and reduction in CO2 in marine water. Under highly eutrophic conditions, the grazers face different exposure circumstances of low oxygen at night and high pH during the daytime [161]. On the other hand, the hypoxic conditions are lethal for copepods causing increased mortality and reduced reproduction rates in female copepods [162,163]. Whereas, both hypoxic and anoxic conditions affect the distribution of planktonic protozoa. Some species are well adapted for anoxic conditions, some can flourish in normoxic environments, and others can dominate in hypoxic conditions [164]. An example is the Texas Laguna Madre dominated by the uninterrupted Aureoumbra lagunesis blooms. The density of A. lagunesis was higher and inversely proportional when compared to the protozoan’s grazer densities [165]. One possible reason for the difficulty of protozoa to feed and grow on high densities of A. lagunensis cells is the thick polysaccharide layer that surrounds cells, referred to as the extracellular polymeric substance or EPS [166]. Another reason for the suppression of natural populations of microzooplankton that feed on HABs depends on the size range of algal species [164]. For example, the cell diameter of A. laguensis is 4–5 μm, which does not fall in the preferred size ranges of the dominant copepod in Laguna Madre [167]. Moreover, the other suppression in the zooplankton population under the bloom condition could have been due to the high pH and hypoxic conditions. Based on these results, it seems that the initial grazer disruption, along with the nutrient pulse that allowed for rapid initial growth, was essential for the bloom to reach high densities of up to several million cells mL−1 within a few months [161]. Once this density of algal biomass reached a very high level, the planktonic grazers were suppressed for the duration of the A. laguensis bloom [165]. However, on the other hand, the algal defense theory suggested that a decrease in the density of edible algae by overgrazing leads to its replacement by slow-growing resistant species [168,169]. A study by McCauley and Briand is supporting the idea that the number of resistant species can be controlled by a reduction in grazing. The resistant species are defined as algae larger than 50 μm and almost all are cyanobacteria. However, low grazing conditions may be favoring some resistant species, for example, the Synedra a needle-like, unicellular diatom [169,170]. Therefore, this assumption would not contradict the fact that an increasing population of diverse nature of harmful algae leads to a higher resistance towards their predators, posing a serious threat to the aquatic environments.

3.5.2. Threshold Effects of HABs on Grazers

Disruption in grazer populations (top to down controls) can be a contributing factor to phytoplankton blooms. The imbalance in zooplankton–phytoplankton interactions or if there is a lag between zooplankton populations and growth of phytoplankton, or some other factor depresses the abundance of potential grazers, phytoplankton populations may be temporarily released from grazer control and reach bloom densities [161]. When HABs reach higher densities, threshold levels also reach maximum levels, for example, the initiation of the brown tide bloom Aureoumbra lagunensis in Texas during 1985 and the Rhode Island bloom of Aureococcus anophagefferens in Narragansett Bay, arising during the low grazer abundance periods [7]. Once these blooms have originated, the zooplankton show reduced grazing often on these unpalatable species eventually leading to the extension and persistence of HABs [8]. This decrease in zooplankton grazing may impair nutrient regeneration, resulting in phytoplankton nutrient limitation [171]. Reduction or limitation in nutrient supply or altered nutrient ratios could be a potential increase in the toxicity of HAB species [172]. Although it has yet been demonstrated, it could be interesting to determine if anything analogous to quorum sensing in bacteria in toxic phytoplankton, perhaps the high-density blooms, could release chemicals that induce the additional production of toxins [161].
Table 2. The scientific consensus on phycotoxins by harmful algal blooms (HABs), the toxicity mechanism, diagnosis, and negative effects on human health.
Table 2. The scientific consensus on phycotoxins by harmful algal blooms (HABs), the toxicity mechanism, diagnosis, and negative effects on human health.
Biological CategoryTypesToxicity MechanismDiagnosisSymptomsReference
HapatotoxinsMicrocystin MCsCarcinogenesis, genotoxicity, inhibition of protein phosphatases, repeated low-level exposureExposure; drinking water, contaminated dialysis fluid, soft water recreational environmentsLiver hemorrhage, diarrhea, abdominal pain, vomiting, shock, jaundice, dyspnea, weakness, multiple organ failure, respiratory distress[173]
NodularinInhibition of protein phosphatasesDrinking water, recreationGoose bumps, diarrhea, liver hemorrhage, vomiting, weakness[123]
CylindrospermopsinGlutathione and protein synthesis as well as cytochrome P450. Repeated low level exposure; carcinogenesis, genotoxicityChronic exposure linked to cancerGastroenteritis abdominal pain, bloody diarrhea, vomiting, acute liver inflammation. Liver and kidney failure, asthma, hay fever[123]
NeurotoxinsAnatoxin-a/Homoanatoxin-aNicotinic receptors: irreversible link to the nicotinic receiver S of acetylcholine in neuromuscular junctionCould be lethalMuscle twitching, staggering, cramping, convulsions, paralysis, respiratory failure, gasping, death by suffocation[116]
Anatoxin-a (S)Irreversible inhibitor acetylcholinesteraseMuscle twitching, salivation, paralysis, cramping[174]
SaxitoxinsNeurotoxic, target the peripheral nervous system. Selective high affinity block sodium conductance in voltage-gated sodium channelsDeath can occur within 2–12 h after exposure. Good prognosis after 24 h, requiring good medical support systemNausea, perioral burning ataxia, vomiting, drowsiness, muscular paralysis, paraesthesia, tachycardia, fever, respiratory failure, death[175]
beta-Methylamino L-alanine (BMAA)Experimentally acts predominantly on motor neuron-excitotoxic through glutamate receptorsChronic exposure linked to chronic neurodegenerative conditions: Amyotrophic Lateral SclerosisNot fully elucidated. Implicated in chronic neurodegenerative diseases[40]
DermatoxinsAplysiatoxinsPotent tumor promoters Potentiation of protein kinase CAsthma-like symptoms, skin irritation[176]
LyngbyatoxinPotent tumor promoters Potentiation of protein kinase CSkin irritation, contraction in smooth muscles[177]
Biotoxins [Amnesic]Domoic acid and isomersProduction of excessive gastric juice increased the acidityConsumption of shellfish (possibly, fish)Diarrhoea, nausea, vomiting, dizziness, headache, confusion, short-term memory deficits, motor weakness, disorientation. Severe cases result in cardiac arrhythmia, seizures, coma, respiratory distress, and possibly death[178,179]
Domoic acidGastroentritis and neurotoxicConsumption of infected clams oysters, crabs, anchovies, and sardinesGastroenteritis, nausea, diarrhoea, vomiting, abdominal cramps within 24 h. Neurological symptoms such as headache, dizziness, respiratory problems, seizures, short-term memory loss and coma usually appear within 48 h[10,180]
[Azaspiracid]Azaspiracid and its derivativesNAConsumption of shellfishDiarrhoea, nausea, vomiting, severe abdominal cramps; effects on mice include severe damage to the intestine, spleen, and liver tissues in animal tests[181,182,183]
[Ciguatera]CiguatoxinGastrointestinal acidificationConsumption of coral reef fishNausea, diarrhoea, vomiting, numbness of mouth and extremities. Neurological symptoms may persist for several months[184,185]
Ciguatoxins/maitotoxinNAConsumption of small-algae eating fishParesthesias, pain in urination, pain in the teeth, temperature reversal, blurred vision, gastrointestinal effects; diarrhoea, vomiting, abdominal cramps. Cardio-vascular symptoms; arrhythmias and heart block[10,180]
[Diarrhetic]DinophysistoxinsNAConsumption of shellfishAbdominal cramps, nausea, severe diarrhoea, vomiting, respiratory distress[186]
Okaidic acidNATransferable through mussels, scallops, clamNausea, diarrhoea, abdominal cramps, vomiting, and chills within 30 min to 12 h of ingestion[1]
[Neurotoxic]BrevetoxinsSuppress the functioning of the nervous system slowlyConsumption of shellfish (and fish at least for marine mammals); inhalation of marine aerosols during active bloomsTemperature sensation, nausea, muscle weakness, reversals, and vertigo. Exposure to aerosols related to respiratory and eye irritation, particularly for asthmatics[187,188]
[Palytoxicosis]Palytoxin, Ostreocin, OvatotoxinNACosumption of seafood; inhalation of marine aerosols; direct contact with waterNausea, abdominal cramps, vomiting, severe diarrhoea, lethargy, tingling of the lips, mouth, face and neck, lowered heart rate, skeletal muscle breakdown, muscle spasms and pain, lack of sensation, myalgia and weakness, hypersalivation, and difficulty breathing. Exposure to aerosols; eye and nose irritation, rhinorrhoea, general malaise, fever. Cutaneous irritations in beach swimmers[189,190]
[Paralytic]Saxitoxin and derivativesNAConsumption of shellfish, crustaceans, fishDiarrhoea, vomiting, nausea, numbness and tingling of the lips, mouth, face and neck. Severe cases can result in paralysis of the muscles of the chest and abdomen leading to death[191]

4. Management of Harmful Algal Blooms (HABs)

The diversity and impacts of harmful algal blooms are an increasing challenge for their management. Although various efforts have been directed towards managing HABs, nevertheless, strategies are needed to protect the fisheries sector, minimize economic losses as well as ecosystem deterioration, and foremost protect public health; these have varied considerably on large spatial scales, and among HAB types. Anderson [192] highlighted strategies used by various countries and commercial sectors across the world for the monitoring and management of HABs in coastline waters. A few strategies have been discussed in the sections below.

4.1. Current Trends

Over the last three decades, the nature of the HAB problem has changed considerably across the world. In recent years, a dramatic expansion has occurred in the areas affected by PSP toxins. However, a similar pattern also applies to various other types of HABs. Events of toxic blooms, resources affected, economic losses by them, a variety of toxins, and the emergence of toxic species have increased all over the world [192,193,194]. However, the sole point of contention is about the motives for the growth of HABs [192,195]. Mostly it is immediately assumed that anthropogenic activities and pollution are involved, and in some cases, this is true [194]. A variety of HAB species flourish on nitrogen and phosphorus present in industrial effluents, sewage, and agriculture waste. However, closer examination has revealed that some extended or newly born HAB issues have arisen in the waters where pollution is not the main influence. For thousands, if not millions of years, HAB species have been on the planet. During this extensive time period, they have had sufficient opportunities to expand, aided by climate change, movement in tectonic plates, and other global scenarios. As a result of improved detection technologies and more observers, certain new bloom episodes may reflect indigenous populations that have been detected [192].
The anthropogenic intervention has also aided the global growth of HAB by carrying hazardous species in ship ballast water [195]. Extensive aquaculture practices in many countries are another factor driving the global expansion of HABs. This leads to better product quality and safety monitoring, uncovering indigenous hazardous algae that were most likely always there [193]. Anderson (2009) also highlighted that the construction of aquaculture facilities has placed fish and shellfish resources in areas where toxic algal species occur but were previously unknown, leading to mortality events or toxicity outbreaks that would not have been noticed had the aquaculture facility not been placed there. It is now clear that the global spread of HAB phenomena is due in part to our ability to better identify the problem’s boundaries, the nature and breadth of poisonous or hazardous species, as well as their consequences. However, HABs are a major and widespread problem that is far larger than previously realized [192].

4.2. Management Issues of HABs

Those in charge of managing coastal resources endangered by HABs have a huge challenge because of the range of blooms and their effects are diverse in nature. The solutions required to protect the fisheries sectors, limit the economic losses, and environmental deterioration, and protect public health vary greatly depending on where you are and what form of HAB you have [192]. Various strategies have come across and been adopted by different countries and several of them are discussed here.

4.3. Mitigation of HABs

Enormous management actions taken against the distribution and expansion of HABs can be termed as mitigation. These actions include dealing with the prevailing or current bloom, and necessary steps taken to reduce the possible negative impacts [192]. Routine monitoring programs, which are now being carried out in more than 50 countries, are aimed at detecting harmful levels of the HAB toxins in shellfish [192]. These types of studies will lead to harvesting restrictions to keep the contaminated products off the market. Another common mitigation strategy is dragging away the fish net pens from intense HAB sites [192]. Various other traditional approaches including a reduction in nutrient load and experimental methods (e.g., omnivorous fish removal, flushing, and artificial mixing) have been used to reduce the expansion of HABs [196]. Furthermore, recently Paerl et al. [196] reviewed several mitigation strategies for cyanobacterial HABs (cHABs) including their control within water and airsheds and within water bodies. Although a wide range of measures has been employed to deal with HABs, however, there is still little information available on how climate change and temporal patterns will influence the efficacy of all strategies within water bodies.

4.4. Prevention of HABs

Steps or actions performed to prevent HABs from occurring or having a direct impact on a certain resource can be summed up as prevention [192]. Increased use of chemical fertilizers in agriculture, as well as increased combustion of fossil fuels, have all contributed to a rapid increase in the inflow of plant nutrients, notably nitrogen compounds, into the coastal seas around the world [86]. Controlling sewage or waste disposal has the potential to avert certain types of HABs, as demonstrated by legislation or policy measures adopted in Seto Inland Sea and other sites [197]. Several countries are executing sewage reduction plans, which is a positive trend that should be supported [192].

4.5. Control of HABs

Harmful algal blooms can be controlled by wise management and the best time to control these entities is at their initial growth before their development. Apart from this, many other preventive measures can be used to avoid them, such as preventing the direct disposal of sewage and animal waste to the aquatic resources, proper handling of wastewater treatment, and establishing an equipped refinery to control the nitrogen-to-phosphorus ratios, the rectification of agricultural methods, utilization of fertilizers at proper times to decrease potential runoff, the establishment of barrier areas of wetlands and bush to ensure maximum removal of phosphorus before release to the water bodies, and application of conservation tillage to decrease runoff for preventing the HABs. Other detailed physical, chemical, and biological methods are discussed in the sections below and summarized in Table 3.
Table 3. Summary of methods for controlling HABs.
Table 3. Summary of methods for controlling HABs.
Control MeasureTarget Algal SpeciesAction/MechanismReference
Physical Control
Hypolimnetic withdrawl and horizontal flushingDinoflagellates and Cyanobacterial species particualry (Microcystis and Dolichospermum)Mechanical pumps, pneumatic or hydraulic mixtures are used to produce water mixture which improves water quality and avoids stratification.[198,199,200]
FlocculationCyanobacterial bloomsThrough adhesion and repeated collision, large, rapidly sinking aggregates (or flocs) of algae and clay are formed and settle on the ocean floor.[201,202]
Sediment resuspension, burial, and removalAll bloom-forming species (dinoflagellates, cyanobacteria)To resuspend sediments in an area thought to be a seedbed for algal cysts (thick-walled dormant cells of algae) with the objective of burying cysts in deeper oxygen-depleted sediments where they are unable to germinate and, to resuspend sediments that would act as a natural flocculant to remove algal cells from the water column. Burial can be achieved by the placement of offsite material over the treatment area. All offsite material would be clean and free of toxins and of similar grain size and composition to sediments of the treatment area. Burial is also achievable through hydraulic suction dredging, where dredged material is removed from one area and discharged over the treatment area.[202]
AerationAll bloom-forming species (dinoflagellates, cyanobacteria)Aerators operate by pumping air through a diffuser near the bottom of a water body, resulting in the formation of plumes that rise to the surface and create vertical circulation cells as they propagate outwards from the aerator. This mixing of the water column disrupts the behavior of algal cells to migrate vertically in addition to limiting the accessibility of nutrients by internal loading.[203]
Hydrologic manipulationsAll bloom-forming species (dinoflagellates, cyanobacteria)Manipulation of inflow/outflow of water in the system to disrupt stratification and control HABs.[203]
Mechanical mixing (circulation)Cyanobacterial bloomsMechanical mixers are usually surface-mounted to disrupt the algal growth to migrate vertically in addition to limiting the accessibility of nutrients.[203]
Reservoir drawdown/desiccationCyanobacterial bloomsReservoirs and other controlled waterbodies can draw down the water level to the point where algal accumulations are exposed above the waterline. Subsequent desiccation and/or scraping to remove the layer of algal blooms attached to sediment or rock is required, in addition to the reinjection of water into the system.[203]
Surface skimmingCyanobacterial bloomsOil-spill skimmers have been used to remove cyanobacterial bloom surface scums. This technique is often coupled with the implementation of some coagulant or flocculent.[203]
UltrasoundCyanobacterial bloomsAn ultrasound device is used to control HABs by emitting ultrasonic waves of a particular frequency such that the cellular structure of algal species is destroyed by rupturing internal gas vesicles used for buoyancy control.[203]
Chemical Control
Algaecides/Algaestats applied prior to bloom to resist bloom formationCyanobacterial bloomsAlgaecides are chemical compounds applied to a waterbody to kill cyanobacteria and destroy the bloom. Several examples are copper-based algaecides (copper sulphate, copper II alkanolamine, copper citrate, etc.), potassium permanganate, chlorine, lime.[203]
BiosurfactantsSpecies specific (depends on specific bacteria or yeast used to produce surfactants)Surfactants break down algal cell membranes, making them non-functional, often resulting in cell lysis.[202]
Barley strawCyanobacterial bloomsBarley straw bales are deployed around the perimeter of the waterbody. Barley straw, when exposed to sunlight and in the presence of oxygen, produces a chemical that inhibits algae growth. Field studies suggest significant algistatic effects. Several causes for the observed effects have been suggested; however, the exact mechanism of this process is not well understood.[203]
CoagulationCyanobacterial bloomsCoagulants are used to facilitate the sedimentation of cyanobacteria cells to the anoxic bottom layer of the water column or below the photic zone. Unable to access light, oxygen, and other critical resources, the cells do not continue to multiply and eventually die.[203]
Biological Control
Bacteria as Bio Controllers
Bacillus cereusMicrocystis aeruginosaSecretion of cyanobacteriolytic substances[204]
Bacillus sp.Aphanizomenon flos-aquaeCell-to-cell contact mechanism[205]
Bacillus sp.Microcystis aeruginosaProduction of an extracellular product[206]
Bacillus sp.Phaeocystis globosaSecretion of algalytic substance[207]
Bdellovibrio-like sp.Microcystis aeruginosa (lake)Penetration[208]
Brachybacterium sp.Alexandrium catenellaProduce secondary metabolites[209]
CytophagaMicrocystis aeruginosaDirect contact[210]
Flexibacter flexilis, F. sanctiOscillatoria williamsiiInhibition of the photosynthetic electron transport reactions, and glycolate dehydrogenase and nitrogenase activity[211]
Myxococcus fulvus BGO2Phormidium lucidumEntrapment[212]
Myxococcus xanthus PCO2NAEntrapment[213]
Pseudomonas fluorescensHeterosigma akashiwoIndirect attack by alga-lytic substances[214]
Pseudomonas putidaMicrocystis aeruginosaInhibit the synthesis of the photosynthetic apparatus.[215]
Pedobacter sp. MaI11-5Microcystis aeruginosaMucous-like secretion from cyanobacteria for self-defense[216]
Raoultella sp. R11NADissolved microbial metabolites and humic acid[217]
Rhodobacteraceae PD-2Prorocentrum donghaienseProduce N-acyl-homoserine lactone signals[218]
Streptomyces neyagawaensisMicrocystis aeruginosaSecretion of extracellular antialgal substances[219]
Saprospira albidaMicrocystis aeruginosaParasitic lysis[220]
Streptomyces sp.Microcystis aeruginosaIndirect attack by producing algicidal compounds[221]
Agrobacterium vitisMicrocystis aeruginosaQuorum sensing[222]
Rhizobium sp.Microcystis aeruginosaLysis[223]
Methylobacterium zatmanii,
Sandaracinobactor sibiricus,
Halobacillus sp.
Microcystis aeruginosaBioflocculation[224]
Algicidal bacteria (Pseudoalteromonas sp.)Chattonella sp., Gymnodinium sp.,
Heterosigma sp.
Indirect/Algicidal effect[225]
Algicidal bacteria
(Bacillus sp. LP10)
Phuphania globosaIndirect/Active compounds lytic[226]
Algicidal bacteria
(Vibrio sp., Flavobacterium sp., Pseudoaltero sp., Acinetobacter sp.)
Gymnodinium mikimotoiDirect/Growth inhibition[227]
Algicidal bacteria
(Bacillus sp. AB-4)
Chattonella marina, Akashiwo sanguinea, Fibrocapsa japonica, Heterosigma akashiwo,
Scrippsiella trochoidea
Indirect/Algicidal effect[228]
Algicidal bacteria (Vibrio sp. DHQ25)Alexandrium tamarenseIndirect/Algicidal effect[229]
Algicidal bacteria (Pseudoalteromonas sp., Zobellia sp., Cellulophaga lytica, Planomicrobium sp., Bacillus cereus)Gymnodinium catenatumIndirect/Active compounds lytic[230]
Biosurfactant bacteria (Pseudomonas aeruginosa)Alexandrium minutum, Karenia brevis,
Pseudo-nitzschia sp.,
Gonyostomum semen, Microcystis aeruginosa
Indirect/Surfactant[231]
Algicidal bacteria
(Shewanella sp. IRI-160)
Prorocentrum piscicida, Prorocentrum minimum,
Gyrodinium uncatenum
Indirect/Algicidal effect[232]
Zooplankton as biocontroller
Daphnia ambiguaMicrocystis aeruginosaGrazing[233]
Daphnia hyalineChlorella sp.Grazing[234]
D. galeata, Cyclops sp.Scenedesmus sp.Grazing[234]
Poterioochromonas sp.Microcystis aeruginosaGrazing[235]
Strombidinopsis jeokjoCochlodinium polykrikoidesDirect/Grazing[236]
Favella taraikaensi, F. azoticaAlexandrium tamarenseDirect/Grazing[237]
Algae as bio controller
Dinoflagellate heterotrophic
(Stoeckeria algicida)
Heterosigma akashiwoDirect/Grazing[238]
Ankistrodesmus falcatusChlorella vulgarisBio-flocculation[239]
Scenedesmus obliquusChlorella vulgarisBio-flocculation[239]
Tetraselmis suecicaNeochloris oleoabundansBio-flocculation[239]
Fungi as bio controller
Fungus Trichaptum abietinumMicrocystis aeruginosa, M. flos-aquae, Oocystis borgeiDirect/Preying ability[240]
Fungus Trichaptum abietinumMicrocystis aeruginosa, M. flos-aquae, O. borgeiDirect/Preying ability[240]
Irpex lacteus, Trametes hirsute, Trametes versicolor, Bjerkandera adustaMicrocystis aeruginosaDirect attack[241]
Fish as bio controller
Silver carpMicrocystis aeruginosaGrazing[235]
Bighead carpMicrocystis aeruginosaGrazing[235]
Tilapia
(Oreochromisni loticus)
Microcystis aeruginosaIngestion and digestion[242]
Virus as bio controller
Virus HaVHeterosigma akashiwoDirect/Lysis infection[243]
HaNIVHeterosigma akashiwoDirect/Induction of cell death or apoptosis[244]
HcRNAVHeterocapsa circularisquamaDirect/Induction of cell lysis[245]

4.5.1. Physical Control

Physical methods include control of sources or levels of nutrients entering from industrial or urban sewage, treating wastewater, reduction in ecosystem salinity, preventing water rotation to avoid algal spreading, control of untreated ship ballast water discharge and preventing oil spills at sea, removing deceased fish from coastal water, and filtering the contaminated water by suctioning and returning back the purified water. Mechanical control includes the removal of algal cells by dispersion of clay on the water surface. In Korea and other countries of the world, fish farming is a valued industry, threatened by harmful algal blooms, and the clay method has been widely adopted for the removal of these algal blooms [42].

4.5.2. Biological Control

Living organisms such as microorganisms, aquatic birds, domestic animals, viruses, and bacteria are used as biological control measures to limit populations of phytoplankton [42]. Different microorganisms including bacteria, protozoa, viruses, algae, yeasts, molds, and Rickettsia have been used as biocontrollers for HABs [66,246]. In highly nutrient-loaded lakes, some strains of bacteria control cyanobacterial blooms by producing allelochemicals [247]. The SSZ01 strain of bacteria produced highly toxic β-carbolines (e.g., harmine and norharmane) and showed significant anti-algal activity [248]. Besides bacteria, fungi also secrete some inhibiting agents such as extracellular compounds, which control HABs. White rot Lopharia spadicea fungus has been shown to significantly inhibit Microcystis aeruginosa, Glenodinium spp., and Cryptomonas ovata [240].
Myxobacteria are an example of having the potential to kill unicellular filamentous Cladophora by having close contact. Mostly algicidal bacteria secrete algicidal compounds which lyse algae [249]. Palmitoleic acid is produced by a marine Vibrio bacterium which is vital for terminating harmful algal blooms in marine ecosystems. It is also reported that BS02 bacteria has an inhibiting effect on A. tamarense, showing selective control in algal blooms [247]. However, some fungi are algicidal and can directly kill the algal species, Han et al. pointed out four species of fungi, including Trametes hirsuta T24, Irpex lacteus T2b, Bjerkandera adusta T1. and Trametes versicolor F21a, that can degrade algae by attacking them directly. Globally, some important bacterial species are used as biological control of harmful algal blooms; for example, Microcystis aeruginosa can be controlled by Halobacillus sp. [131], Streptomyces sp. [221], Pedobacter sp. (MaI11-5) [249], Pseudomonas putida [215], Sandaracinobactor sibiricus [223], Agrobacterium vitis [222], and Sandaracinobactor neyagawaensis [219], while Rhodobacteraceae Strain PD-2 can control the Prorocentrum donghaiense [218], and Pseudomonas fluorescens can control Heterosigma akashiwo [214]. Although biological control of HABs is diverse, enormous studies have demonstrated various methods of controlling the HABs using biological applications.
Besides these, some other important strategies opted as biological control include fish species that graze on these blooms and fungi that can decompose by direct attack on them. Viruses have the ability to reproduce quickly and can specifically interact with HAB species and cause their destruction in larger masses. Zooplankton are also voracious grazers of HABs, some of the algae can control HABs by bio-flocculation and various bacterial strains, as discussed in previous sections in detail, can also additionally control HABs by producing secondary metabolites, a cell-to-cell contact mechanism, and by producing antagonistic volatiles, respectively.

4.5.3. Chemical Control

Various chemicals are used to control cyanobacterial harmful algal blooms (cHABs), CuSO4 is effective against HABs; however, it is toxic to other plants and animals and its residues are found in sediments and are considered legacy pollutants. Hydrogen peroxide is selectively used against cyanobacteria and possesses no severe side effects on the ecosystem [14,250]. These treatments can be used for limited small areas, whereas, hydrogen peroxide is degraded rapidly by different physio-chemical and biotic activities; thus, its treatment should be applied many times throughout the blooming period. The multiple treatments used for effective results have become costly. Therefore, cautionary measurements for cHABs that produce toxins should be considered because endotoxins released by dead organisms contaminate drinking and irrigation water. Hydrogen peroxide usage is more reliable than copper sulfate because its oxidation stimulant is light and breaks microcystins into peptide residue [250]. It would therefore detoxify water that is affected by microcystin-producing HABs. Phosphorous is immobilized in sediments by chemical precipitation. However, it is not effective because its repeated treatments are expensive. All available forms of nitrogen are soluble in water so no techniques can be used to immobilize it [14]. As the research studies and advanced technologies have revolutionized, however, HAB control is still hampered by several research gaps and effective control measures are immediately required for the mitigation of HABs.

4.5.4. Molecular Approaches

Advanced “-omic” technologies such as proteomics, transcriptomics, metabolomics, and genomics offer a platform to study the HAB species and community dynamics [121]. However, exploring this is still limited because primers are lacking for many important species. However, genomic tools can extend to obtain standard practices and find out the functioning of some genes [218]. Furthermore, identifying the gene regulatory mechanisms for the production of toxins in HAB species is a difficult goal to achieve.

4.6. Constraints of HAB Controlling Methods

The effectiveness of controlling methods has some limitations that do not allow these preventive measures to work more precisely. From a brief literature survey, some important limitations are drawn in this section.

4.6.1. Physical Methods

Generally, some of the physical methods (e.g., aeration) are more effective in deep-water columns. However, it highly depends on the rate of airflow and the degree of stratification, and the size of the water body, the larger the water body, the less effective and more costly the methods are. Whereas, hydrologic manipulation needs a sufficient volume of water and a capability for controlling the flow. Oftentimes it can be expensive and unintentional consequences towards other aquatic organisms are expected. Similarly, mechanical mixing has a limited range as operating with individual devices may be away from targeted regions; thus, providing a suitable environment for algal growth in those areas. Desiccation or reservoir drawdown is likely to have a significant impact on other aquatic biota in the system. It could be expensive, as it needs many input resources, especially water to refill the water body. Surface skimming is ineffective until the later stages of bloom. At the later stages of bloom, a lot of harmful aspects have materialized. Therefore, proper equipment is required before the implementation. Ultrasound may be lethal to green algae and zooplankton can disrupt the cellular masses, but the effectiveness depends on the geometry of the species.

4.6.2. Chemical Methods

Algaecides have risks of cell lysis and the direct release of harmful toxins into the targeted environment; therefore, these are usually used at the earlier stages of bloom formation. Some algaecides on the other hand are potentially toxic to other organisms such as fish, invertebrates, and zooplanktons. Barley straw is only effective against new algal species as it can inhibit their growth rather than killing the existing algal species. While, after 2–8 weeks barley straw is seriously harmful to the waterbody as its decay produces harmful chemicals and can cause fish death by deoxygenation. Coagulation processes are limited by depth because the lysis of coagulated cells over time releases the toxins directly into the aquatic ecosystem. Whereas, flocculation is also subject to depth limitations.

4.6.3. Biological Methods

Most of the biological methods including microorganisms and fungi are species-specific, whereas the fish species also cannot kill the toxicant species. In open systems, the application of biological methods may regrettably reinforce the fear of irreversibility. Therefore, this makes it a highly risky strategy. Nevertheless, it could be under consideration only by virtue of its positive outputs. However, the main limitation of introducing the controlling species remains the uncertain conditions. In addition, logistic difficulties in the application of predators, such as the scaling of cultures to obtain a high number of predators and the limitations in their potential use outside the laboratory conditions are also considerable.

5. Emerging Technologies and Limitations in Their Application

Harmful algal blooms have sparked a lot of studies around the world. Consequently, numerous emerging advanced technologies are providing breakthroughs to solve the management issues of HABs we are dealing with.
Methods for detecting and quantifying toxins are critical in this regard, and progress has been rapid. For all major HAB toxins, classical analytical techniques combining chromatography and mass spectrometry (e.g., LC-MS) have developed significantly. They are now replacing many older approaches, such as the commonly used but socially unpopular bioassays on mice. Simple kits, on the other hand, that are similar to home pregnancy kits have been produced. These allow for low-cost, quick toxin testing and show a tremendous aptitude for application in the sample screening; thus, eliminating the expensive analysis for large samples in monitoring programs [192]. Bloom detection and tracking are other significant management requirements. At a larger scale, satellite remote sensing is being utilized to detect HABs in the Gulf of Mexico, and forecasts of impending landfall or exposure are now being made using simple transport models [251]. Because the existing blooms identified are mono-specific and dense in nature, hence have a chlorophyll property that shows their existence, that capability is difficult to transmit to other HABs. Remote sensing applications for other HABs, for example, depending on the detection of water masses using the temperature of the sea surface are promising [252]. Satellite-based remote sensing has some limitations: (a) data is limited to the ocean surface, which is typically <15 m but much shallower in coastline waters. This is a serious issue if HABs are intense in distinct subsurface layers; (b) landmasses and cloud cover, limiting its utility in shoreline waters, where the HABs originate; (c) different groupings of phytoplankton are resolved in a limited way from complicated, dynamic communities. For at least the last decade, researchers have been attempting to clarify the pigment-based functional categories or size of phytoplankton with mixed results [253,254,255]. Single or multi-spectral fluorometers, particle size analyzers, absorption, and backscatter sensors are the in-situ methods for quantifying phytoplankton biomass. However, these technologies provide size-based signals in bulk that are not specific to the HAB taxa [256]. Optical, chemical, and molecular technologies are used in other in situ sensing systems on moored and mobile platforms. The Optical Plankton Discriminator (OPD), also known as the Brevebuster, was developed in the late 1990s to detect optical signals of toxic dinoflagellate K. brevis, based on its unique pigment signature in mixed phytoplankton communities [257]. The Environmental Sample Processor (ESP), which was designed for moored deployments, detects and quantifies HAB species and toxins using immuno- or molecular probe-based tests [258,259,260]. Over the last decade, a number of field studies based on portable image technologies and various lab methods have been developed. Several of them are now frequently employed in HAB monitoring projects, the best known are FlowCAM and IFCB. FlowCAM detects and monitors the presence of HAB species using the principles of fluidics based on the flow cytometry and the optics of the light microscope. Whereas, to generate the high-resolution images of <10–150 μm particle sizes, IFCB combines flow cytometry and video technology [261]. However, despite progress, accurate and precise identification of phytoplankton species using automated algorithms remains a bottleneck in their use, which frequently needs human assistance [262]. Furthermore, for many HAB species, “molecular probes” have been produced at the lowest scale, allowing algal cells to be identified and counted more readily and quickly than the standard microscopy allows [263]. Biologically unknown toxins, cryptic species, congeners, and pathways might stymie the development of widely used test kits or sensors for poisons and species, as well as the creation of ground-truthing standard sets. Precisely, what defines a “bloom” differs greatly amongst the species of HAB, and many toxin-producers may persist in small numbers. Whereas a toxic “event” is generally derived by regulatory authorities concerned with humans and food safety measures, this metric may not be relevant for researchers and managers working to understand and control HABs before they become intensely dangerous [33]. The availability of more affordable instruments has increased the usage of observation systems, but long-term expenses associated with maintenance, and purchasing proprietary chemicals might be a barrier that is generally unshared among users [33]. In conclusion, the choice of the right technology may necessitate the coordinated employment of complementary techniques, which is useful in management efforts to mitigate and control HABs.

6. Conclusions

Harmful algal blooms present a wide range of problems and consequences including their causes and control. Aquatic pollution and anthropogenic interventions in coastal areas have increased their populations drastically and the emergence of novel toxic species. Recently, due to the extensive and steady events of HABs that cause deleterious impacts on aquaculture, human health, tourism, and foremost the entire coastal economy, there is an increasing need for the scientific community to realize the phenomenon, much greater than in the past. Furthermore, changes in global climatic patterns have significantly influenced their persistence and toxicity which is further aggravating the environmental sustainability. In many parts of the world, well-managed fisheries and aquaculture industries, as well as other resources, have been seriously threatened by HABs and this wave of danger will expand for those countries that have not recognized this problem or struggle to encounter it. Although, technological advancements have developed the abilities in ocean monitoring and have opened spaces for the identification of blooms, as well as to explore the chemical, physical, and biological parameters that cause the emergence, expansion, and disappearance of these algal blooms. There are still many loopholes that should be necessarily filled through mutual coordination by research organizations. However, the innovation and creativeness of explorers for future improvements are highly dependent on the collaboration and cooperation of biological and physical researchers who are struggling with these bloom populations.

Author Contributions

Conceptualization, S.S.U.H.K., N.Y., S.C.K., N.S.; writing—original draft preparation, S.S.U.H.K.; writing—review and editing, S.S.U.H.K., N.Y., S.C.K., N.S.; funding acquisition, S.C.K., N.S. All authors have read and agreed to the published version of the manuscript.

Funding

This work was funded by Chiang Mai University, Thailand.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declared no conflict of interest.

References

  1. Horner, R.A.; Garrison, D.L.; Plumley, F.G. Harmful algal blooms and red tide problems on the U.S. west coast. Limnol. Oceanogr. 1997, 42, 1076–1088. [Google Scholar] [CrossRef]
  2. Sha, J.; Xiong, H.; Li, C.; Lu, Z.; Zhang, J.; Zhong, H.; Zhang, W.; Yan, B. Harmful algal blooms and their ecoenvironmental indication. Chemosphere 2021, 274, e129912. [Google Scholar] [CrossRef]
  3. Albert, S.; O’Neil, M.J.; Udy, J.W.; Ahern, S.K.; O’Sullivan, C.M.; Dennison, W.C. Blooms of the cyanobacterium Lyngbya majuscula in coastal Queensland, Australia: Disparate sites common factors. Mar. Pollut. Bull. 2005, 51, 428–437. [Google Scholar] [CrossRef]
  4. Curren, E.; Yoshida, T.; Kuwahara, V.S.; Leong, S.C.Y. Rapid profiling of tropical marine cyanobacterial communities. Reg. Stud. Mar. Sci. 2019, 25, e100485. [Google Scholar] [CrossRef]
  5. Heisler, J.P.; Gilbert, J.; Burkholder, J.; Anderson, D.; Cochlan, W.; Dennison, W.; Dortch, Q.; Gobler, C.J.; Heil, C.; Humphries, E.; et al. Eutrophication and harmful algal blooms: A scientific consensus. Harmful Algae 2008, 8, 3–13. [Google Scholar] [CrossRef][Green Version]
  6. Cira, E.K.; Wetz, M.S. Spatialtemporal distribution of Aureoumbra lagunensis (“brown tide”) in Baffin Bay, Texas. Harmful Algae 2019, 89, e101669. [Google Scholar] [CrossRef]
  7. Buskey, E.J.; Montagna, P.A.; Amos, A.F.; Whitledge, T.E. Disruption of grazer populations as a contributing factor to the initiation of the Texas brown tide algal bloom. Limnol. Oceanogr. 1997, 42, 1215–1222. [Google Scholar] [CrossRef]
  8. Caron, D.A.; Gobler, C.J.; Lonsdale, D.J.; Cerrato, R.M.; Schaffner, R.A.; Rose, J.M.; Buck, N.J.; Taylor, G.; Boissonneault, K.R.; Mehran, R. Microbial herbivory on the brown tide alga, Aureococcus anophagefferens: Results from natural ecosystems, mesocosms and laboratory experiments. Harmful Algae 2004, 3, 439–457. [Google Scholar] [CrossRef]
  9. Chattopadhyay, J.; Sarkar, R.R.; Pal, S. Mathematical modelling of harmful algal blooms supported by experimental findings. Ecol. Complex. 2004, 1, 225–235. [Google Scholar] [CrossRef]
  10. Sonak, S.; Patil, K.; Devi, P.; D’Souza, L. Causes, human health impacts and control of harmful algal blooms: A comprehensive review. Environ. Pollut. Protect. 2018, 3, 40–55. [Google Scholar] [CrossRef]
  11. Zingone, A.; Enevoldsen, H.O. The diversity of harmful algal blooms: Challenge for science and management. Ocean Coast. Manag. 2000, 43, 725–748. [Google Scholar] [CrossRef]
  12. Paerl, H.W. Mitigating harmful cyanobacterial blooms in a human- and climatically-impacted world. Life 2014, 4, 988–1012. [Google Scholar] [CrossRef][Green Version]
  13. Peperzak, L. Climate change and harmful algal blooms in the North Sea. Acta Oecologica 2003, 24, 139–144. [Google Scholar] [CrossRef]
  14. Paerl, H.W. A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis spp. Harmful Algae 2016, 54, 4–20. [Google Scholar]
  15. Bakker, C.; Herman, P.M.J.; Vink, M. Changes in seasonal succession of phytoplankton induced by the stormsurge barrier in the Oosterschelde (SW Netherlands). J. Plankton Res. 1990, 12, 947–972. [Google Scholar] [CrossRef]
  16. Hofstraat, J.W.; van Zeijl, W.J.M.; de Vreeze, M.E.J.; Peeters, J.C.H.; Peperzak, L.; Colijn, F.; Rademaker, M. Phytoplankton monitoring by flow cytometry. J. Plankton Res. 1994, 16, 1197–1224. [Google Scholar] [CrossRef]
  17. Vrieling, E.G.; Koeman, R.P.T.; Nagasaki, K.; Ishida, Y.; Peperzak, L.; Gieskes, W.W.C.; Veenhuis, M. Chattonella and Fi-brocapsa (Raphidophyceae): First observations of, potentially harmful, red tide organisms in Dutch coastal waters. Neth. J. Sea Res. 1995, 33, 183–191. [Google Scholar] [CrossRef][Green Version]
  18. O’Neil, J.M.; Davis, T.W.; Burford, M.A.; Gobler, C.J. The rise of harmful cyanobacteria blooms: The potential roles of eutrophication and climate change. Harmful Algae 2012, 14, 313–334. [Google Scholar] [CrossRef]
  19. Shriwastav, A.; Thomas, J.; Bose, P. A comprehensive mechanistic model for simulating algal growth dynamics in photobioreactors. Bioresour. Technol. 2017, 233, 7–14. [Google Scholar] [CrossRef]
  20. Durand, P.M.; Choudhury, R.; Rashidi, A.; Michod, R.E. Programmed death in a unicellular organism has species-specific fitness effects. Biol. Lett. 2014, 10, e20131088. [Google Scholar] [CrossRef]
  21. Tester, P.A.; Vandersea, M.W.; Buckel, C.A.; Kibler, S.R.; Holland, W.C.; Davenport, E.D.; Clark, R.D.; Edwards, K.F.; Taylor, J.C.; Vander Pluym, J.L.; et al. Gambierdiscus (Dinophyceae) species diversity in the Flower Garden Banks National Marine Sanctuary, northern Gulf of Mexico, USA. Harmful Algae 2013, 29, 1–9. [Google Scholar] [CrossRef]
  22. Nishimura, T.; Sato, S.; Wittaya, T.; Sakanari, H.; Uehara, K.; Shah, M.M.R.; Suda, S.; Yasumoto, T.; Taira, Y.; Yamaguchi, H.; et al. Genetic diversity and distribution of the ciguatera causing dinoflagellate Gambierdiscus spp. (Dinophyceae) in coastal areas of Japan. PLoS ONE 2013, 8, e60882. [Google Scholar] [CrossRef][Green Version]
  23. Birchenough, S.N.; Reiss, H.; Degraer, S.; Mieszkowska, N.; Borja, Á.; Buhl Mortensen, L.; Braeckman, U.; Craeymeersch, J.; De Mesel, I.; Kerckhof, F. Climate change and marine benthos: A review of existing research and future directions in the North Atlantic. Wires Clim. Change 2015, 6, 203–223. [Google Scholar] [CrossRef][Green Version]
  24. Trainer, V.L.; Moore, S.K.; Hallegraeff, G.; Kudela, R.M.; Clement, A.; Mardones, J.I.; Cochlan, W.P. Pelagic harmful algal blooms and climate change: Lessons from nature’s experiments with extremes. Harmful Algae 2020, 91, e101591. [Google Scholar] [CrossRef]
  25. Tester, P.A.; Litaker, R.W.; Berdalet, E. Climate change and harmful benthic microalgae. Harmful Algae 2020, 91, e101655. [Google Scholar] [CrossRef]
  26. Gobler, C.J.; Doherty, O.M.; Hattenrath-Lehmann, T.K.; Griffith, A.W.; Kang, Y.; Litaker, R.W. Ocean warming since 1982 has expanded the niche of toxic algal blooms in the North Atlantic and North Pacific oceans. Proc. Natl. Acad. Sci. USA 2017, 114, 4975–4980. [Google Scholar] [CrossRef][Green Version]
  27. Hallegraeff, G.M. A review of harmful algal blooms and their apparent global increase. Phycologia 1993, 32, 79–99. [Google Scholar] [CrossRef][Green Version]
  28. Glibert, P.M.; Icarus Allen, J.; Artioli, Y.; Beusen, A.; Bouwman, L.; Harle, J.; Holmes, R.; Holt, J. Vulnerability of coastal ecosystems to changes in harmful algal bloom distribution in response to climate change: Projections based on model analysis. Glob. Change Biol. 2014, 20, 3845–3858. [Google Scholar] [CrossRef]
  29. Glibert, P.M.; Anderson, D.A.; Gentien, P.; Grane’li, E.; Sellner, K.G. The global, complex phenomena of harmful algal blooms. Oceanography 2005, 18, 136–147. [Google Scholar] [CrossRef]
  30. Parsons, M.L.; Okolodkov, Y.B.; Aké-Castillo, J.A. Diversity and morphology of the species of Pseudonitzschia (Bacillariophyta) of the National Park Sistema Arrecifal Veracruzano, SW Gulf of Mexico. Acta Bot. Mex. 2012, 98, 51–72. [Google Scholar]
  31. Kramer, B.J.; Davis, T.W.; Meyer, K.A.; Rosen, B.H.; Goleski, J.A.; Dick, G.J.; Oh, G.; Gobler, C.J. Nitrogen limitation, toxin synthesis potential, and toxicity of cyanobacterial populations in Lake Okeechobee and the St. Lucie River Estuary, Florida, during the 2016 state of emergency event. PLoS ONE 2018, 13, e0196278. [Google Scholar] [CrossRef][Green Version]
  32. Davis, T.W.; Stumpf, R.; Bullerjahn, G.S.; Mckay, R.M.; Chaffin, J.D.; Bridgeman, T.B.; Winslow, C. Science meets policy: A framework for determining impairment designation criteria for large waterbodies affected by cyanobacterial harmful algal blooms. Harmful Algae 2019, 81, 59–64. [Google Scholar] [CrossRef]
  33. Stauffer, B.A.; Bowers, H.A.; Buckley, E.; Davis, T.W.; Johengen, T.H.; Kudela, R.; McManus, M.A.; Purcell, H.; Smith, G.J.; Woude, A.V.; et al. Considerations in harmful algal bloom research and monitoring: Perspectives from a consensusbuilding workshop and technology testing. Front. Mar. Sci. 2019, 6, e399. [Google Scholar] [CrossRef][Green Version]
  34. Kudela, R.M.; Gobler, C.J. Harmful dinoflagellate blooms caused by Cochlodinium sp.: Global expansion and ecological strategies facilitating bloom formation. Harmful Algae 2012, 14, 71–86. [Google Scholar] [CrossRef]
  35. do Rosario Gomes, H.; Goes, J.I.; Matondkar, S.P.; Parab, S.G.; Al-Azri, A.R.; Thoppil, P.G. Blooms of Noctiluca miliaris in the Arabian Sea—An in situ and satellite study. Deep Sea Res. Part I Oceanogr. Res. Pap. 2008, 55, 751–765. [Google Scholar] [CrossRef]
  36. Sakamoto, S.; Lim, W.; Lu, D.; Dai, X.; Orlova, T.; Iwataki, M. Harmful algal blooms and associated fisheries damage in East Asia: Current status and trends in China, Japan, Korea and Russia. Harmful Algae 2021, 102, e101787. [Google Scholar] [CrossRef]
  37. Capuzzo, E.; Stephens, D.; Silva, T.; Barry, J.; Forster, R.M. Decrease in water clarity of the southern and central North Sea during the 20th century. Glob. Change Biol. 2015, 21, e2206. [Google Scholar] [CrossRef][Green Version]
  38. Mitra, A.; Flynn, K.J. Promotion of harmful algal blooms by zooplankton predatory activity. Biol. Lett. 2006, 2, e194. [Google Scholar] [CrossRef]
  39. Mu, D.; Ruan, R.; Addy, M.; Mack, S.; Chen, P.; Zhou, Y. Life cycle assessment and nutrient analysis of various processing pathways in algal biofuel production. Bioresour. Technol. 2017, 230, 33–42. [Google Scholar] [CrossRef]
  40. Azevedo, S.M.F.O.; Carmichael, W.W.; Jochimsen, E.M.; Rinehart, K.L.; Lau, S.; Shaw, G.R.; Eaglesham, G.K. Human intoxication by microcystins during renal dialysis treatment in Caruaru-Brazil. Toxicology 2002, 182, 441–446. [Google Scholar] [CrossRef]
  41. Nasri, H.; El, H.S.; Bouaïcha, N. First reported case of turtle deaths during a toxic Microcystis spp. bloom in Lake Oubeira, Algeria. Ecotoxicol. Environ. Saf. 2008, 71, 535–544. [Google Scholar] [CrossRef] [PubMed]
  42. Zohdi, E.; Abbaspour, M. Harmful algal blooms (red tide): A review of causes, impacts and approaches to monitoring and prediction. Int. J. Environ. Sci. Technol. 2019, 16, 1789–1806. [Google Scholar] [CrossRef]
  43. Griffith, A.W.; Gobler, C.J. Harmful algal blooms: A climate change costressor in marine and freshwater ecosystems. Harmful Algae 2020, 91, e101590. [Google Scholar] [CrossRef] [PubMed]
  44. Wells, M.L.; Karlson, B.; Wulff, A.; Kudela, R.; Trick, C.; Asnaghi, V.; Trainer, V.L. Future HAB science: Directions and challenges in a changing climate. Harmful Algae 2020, 91, e101632. [Google Scholar] [CrossRef]
  45. Gobler, C.J. Climate change and harmful algal blooms: Insights and perspective. Harmful Algae 2020, 91, e101731. [Google Scholar] [CrossRef] [PubMed]
  46. Ralston, D.K.; Moore, S.K. Modeling harmful algal blooms in a changing climate. Harmful Algae 2020, 91, e101729. [Google Scholar] [CrossRef]
  47. Hennon, G.M.M.; Dyhrman, S.T. Progress and promise of omics for predicting the impacts of climate change on harmful algal blooms. Harmful Algae 2020, 91, e101587. [Google Scholar] [CrossRef]
  48. Moss, B.; Kosten, S.; Meerhoff, M.; Battarbee, R.W.; Jeppesen, E.; Mazzeo, N.; Havens, K.; Lacerot, G.; Liu, Z.; De Meester, L.; et al. Allied attack: Climate change and eutrophication. Inland Waters 2011, 1, 101–105. [Google Scholar] [CrossRef][Green Version]
  49. Elliott, J.A. The seasonal sensitivity of cyanobacteria and other phytoplankton to changes in flushing rate and water temperature. Glob. Change Biol. 2010, 16, 864–876. [Google Scholar] [CrossRef]
  50. Zhu, M.; Paerl, H.W.; Zhu, G.; Wu, T.; Li, W.; Shi, K.; Zhao, L.; Zhang, Y.; Qin, B.; Caruso, A.M. The role of tropical cyclones in stimulating Cyanobacteria (Microcystis spp.) blooms in hypertrophic Lake Taihu, China. Harmful Algae 2014, 39, 310–321. [Google Scholar] [CrossRef]
  51. Polat, S.; Akiz, A.; Olgunoglu, M.P. Daily variation of coastal phytoplankton assemblages in summer condition of the North Eastern Mediterranean (Bay of Iskenderun). Pak. J. Bot. 2005, 37, 715–724. [Google Scholar]
  52. Sadeghi Mazidi, S.; Ahmadi, M.R.; Taherizadeh, M.R. The seasonal changes in phytoplankton population and environmental factors in winter and spring in Bandar Abbas coastal waters. Fish. Aquat. J. 2011, 5, 13–21. [Google Scholar]
  53. Houghton, J.T.; Ding, Y.; Griggs, D.J.; Noguer, M.; Van der Linden, P.J.; Dai, X.; Maskell, K.; Johnson, C.A. Climate Change 2001: The Scientific Basis; Cambridge University Press: Cambridge, UK, 2001; p. 881. [Google Scholar]
  54. Kamiyama, T.; Nagai, S.; Suzuki, T.; Miyamura, K. Effect of temperature on production of okadaic acid, dinophysistoxin-1, and pectenotoxin-2 by Dinophysis acuminata in culture experiments. Aquat. Microb. Ecol. 2010, 60, 193–202. [Google Scholar] [CrossRef][Green Version]
  55. Hamasaki, K. Variability in toxicity of the dinoflagellate Alexandrium tamarense isolated from Hiroshima Bay, Western Japan, as a reflection of changing environmental conditions. J. Plankton Res. 2001, 23, 271–278. [Google Scholar] [CrossRef][Green Version]
  56. Etheridge, S.M.; Roesler, C.S. Effects of temperature, irradiance, and salinity on photosynthesis, growth rates, total toxicity, and toxin composition for Alexandrium fundyense isolates from the Gulf of Maine and Bay of Fundy. Deep Sea Res. Part II Top. Stud. Oceanogr. 2005, 52, 2491–2500. [Google Scholar] [CrossRef]
  57. Guerrini, F.; Ciminiello, P.; Dell’Aversano, C.; Tartaglione, L.; Fattorusso, E.; Boni, L.; Pistocchi, R. Influence of temperature, salinity and nutrient limitation on yessotoxin production and release by the dinoflagellate Protoceratium reticulatum in batchcultures. Harmful Algae 2007, 6, 707–717. [Google Scholar] [CrossRef]
  58. Röder, K.; Hantzsche, F.M.; Gebühr, C.; Miene, C.; Helbig, T.; Krock, B.; Hoppenrath, M.; Luckas, B.; Gerdts, G. Effects of salinity, temperature and nutrients on growth, cellular characteristics and yessotoxin production of Protoceratium reticulatum. Harmful Algae 2012, 15, 59–70. [Google Scholar] [CrossRef][Green Version]
  59. Fussel, H.M. An updated assessment of the risks from climate change based on research published since the IPCC Fourth Assessment Report. Clim. Change 2009, 97, 469–482. [Google Scholar] [CrossRef]
  60. Cao, L.; Caldeira, K. Atmospheric CO2 stabilization and ocean acidification. Geophys. Res. Lett. 2008, 35, e19609. [Google Scholar] [CrossRef]
  61. Qui, B.; Gao, K. Effects of CO2 enrichment on the bloomforming cyanobacterium Microcystis aeruginosa (Cyanophyceae): Physiological responses and relationships with the availability of dissolved inorganic carbon. J. Phycol. 2002, 38, 721–729. [Google Scholar]
  62. Tatters, A.O.; Flewelling, L.J.; Fu, F.; Granholm, A.A.; Hutchins, D.A. High CO2 promotes the production of paralytic shellfish poisoning toxins by Alexandrium catenella from Southern California waters. Harmful Algae 2013, 30, 37–43. [Google Scholar] [CrossRef]
  63. Kremp, A.; Godhe, A.; Egardt, J.; Dupont, S.; Suikkanen, S.; Casabianca, S.; Penna, A. Intraspecific variability in the response of bloomforming marine microalgae to changed climate conditions: Phenotypic variability and climate conditions. Ecol. Evol. 2012, 2, 1195–1207. [Google Scholar] [CrossRef] [PubMed]
  64. Hattenrath-Lehmann, T.K.; Smith, J.L.; Wallace, R.B.; Merlo, L.R.; Koch, F.; Mittelsdorf, H.; Gobler, C.J. The effects of elevated CO2 on the growth and toxicity of field populations and cultures of the saxitoxin-producing dinoflagellate, Alexandrium fundyense. Limnol. Oceanogr. 2015, 60, 198–214. [Google Scholar] [CrossRef] [PubMed][Green Version]
  65. Czerny, J.; Barcelos e Ramos, J.; Riebesell, U. Influence of elevated CO2 concentrations on cell division and nitrogen fixation rates in the bloomforming cyanobacterium Nodularia spumigena. Biogeosciences 2009, 6, 1865–1875. [Google Scholar] [CrossRef][Green Version]
  66. Sun, J.; Hutchins, D.A.; Feng, Y.; Seubert, E.L.; Caron, D.A.; Fu, F.X. Effects of changing pCO2 and phosphate availability on domoic acid production and physiology of the marine harmful bloom diatom Pseudonitzschia multiseries. Limnol. Oceanogr. 2011, 56, 829–840. [Google Scholar] [CrossRef][Green Version]
  67. Tatters, A.O.; Fu, F.X.; Hutchins, D.A. High CO2 and silicate limitation synergistically increase the toxicity of Pseudonitzschia fraudulenta. PLoS ONE 2012, 7, e32116. [Google Scholar] [CrossRef][Green Version]
  68. Van de Waal, D.B.; Verspagen, J.M.; Finke, J.F.; Vournazou, V.; Immers, A.K.; Kardinaal, W.E.A.; Tonk, L.; Becker, S.; Van Donk, E.; Visser, P.M.; et al. Reversal in competitive dominance of a toxic versus non-toxic cyanobacterium in response to rising CO2. ISME J. 2011, 5, 1438–1450. [Google Scholar] [CrossRef][Green Version]
  69. Sandrini, G.; Matthijs, H.C.P.; Verspagen, J.M.H.; Muyzer, G.; Huisman, J. Genetic diversity of inorganic carbon uptake systems causes variation in CO2 response of the cyanobacterium Microcystis. ISME J. 2014, 8, 589–600. [Google Scholar] [CrossRef][Green Version]
  70. Yu, L.; Kong, F.; Shi, X.; Yang, Z.; Zhang, M.; Yu, Y. Effects of elevated CO2 on dynamics of microcystin-producing and non-microcystin-producing strains during Microcystis blooms. J. Environ. Sci. 2015, 27, 251–258. [Google Scholar] [CrossRef]
  71. Shapiro, J.; Wright, D.I. Current beliefs regarding dominance by blue-greens: The case for the importance of CO2 and pH. Verh. IVTLAP 1990, 24, 38–54. [Google Scholar] [CrossRef]
  72. Whitton, B.A.; Potts, M. Introduction to the Cyanobacteria. In The Ecology of Cyanobacteria; Whitton, B.A., Potts, M., Eds.; Kluwer Academic Publishers: Dortrecht, NL, USA, 2000; pp. 1–11. [Google Scholar]
  73. Barcelos e Ramos, J.; Biswas, H.; Schulz, K.G.; LaRoche, J.; Riebesell, U. Effect of rising atmospheric carbon dioxide on the marine nitrogen fixer Trichodesmium. Glob. Biogeochem. Cycl. 2007, 21, GB2028. [Google Scholar] [CrossRef][Green Version]
  74. Fu, F.-X.; Mulholland, M.R.; Garcia, N.S.; Beck, A.; Bernhardt, P.W.; Warner, M.E.; Sanudo-Wilhelmy, S.A.; Hutchins, D.A. Interactions between changing pCO2, N2 fixation, and Fe limitation in the marine unicellular cyanobacterium Crocosphaera. Limnol. Oceanogr. 2008, 53, 2472–2484. [Google Scholar] [CrossRef][Green Version]
  75. Hutchins, D.A.; Fu, F.-X.; Zhang, Y.; Warner, M.E.; Feng, Y.; Fortune, K.; Bernhardt, P.W.; Mulholland, M.R. CO2 control of Trichodesmium N2 fixation, photosynthesis, growth rates, and elemental ratios: Implications for past, present, and future ocean biogeochemistry. Limnol. Oceanogr. 2007, 52, 1293–1304. [Google Scholar] [CrossRef][Green Version]
  76. Riebesell, U.; Schulz, K.G.; Bellerby, R.G.; Botros, M.; Fritsche, P.; Meyerhofer, M.; Neill, C.; Nondal, G.; Oschlies, A.; Wohlers, J.; et al. Enhanced biological carbon consumption in a high CO2 ocean. Nature 2007, 450, 545–548. [Google Scholar] [CrossRef] [PubMed]
  77. Kranz, S.A.; Sultemayer, D.; Richter, K.U.; Rost, B. Carbon acquisition by Trichodesmium: The effect of pCO2 and diurnal changes. Limnol. Oceanogr. 2009, 54, 548–559. [Google Scholar] [CrossRef]
  78. Moisander, P.H.; McClinton, E.; Paerl, H.W. Salinity effects on growth, photosynthetic parameters, and nitrogenise activity in estuarine planktonic cyanobacteria. Microb. Ecol. 2002, 43, 432–442. [Google Scholar] [CrossRef]
  79. Bordalo, A.A.; Vieira, M.E.C. Spatial variability of phytoplankton, bacteria and viruses in the mesotidal salt wedge Douro Estuary (Portugal). Estuar. Coast Shelf. Sci. 2005, 63, 143–154. [Google Scholar] [CrossRef]
  80. Orr, P.T.; Jones, G.J.; Douglas, G.B. Response of cultured Microcystis aeruginosa from the Swan River, Australia, to elevated salt concentration and consequences for bloom and toxin management in estuaries. Mar. Freshw. Res. 2004, 55, 277–283. [Google Scholar] [CrossRef]
  81. Tonk, L.; Bosch, K.; Visser, P.M.; Huisman, J. Salt tolerance of the harmful cyanobacterium Microcystis aeruginosa. Aquat. Microb. Ecol. 2007, 46, 117–123. [Google Scholar] [CrossRef]
  82. Paerl, H.W.; Huisman, J. Blooms like it hot. Science 2008, 320, 57–58. [Google Scholar] [CrossRef][Green Version]
  83. Fu, F.X.; Tatters, A.O.; Hutchins, D.A. Global change and the future of harmful algal blooms in the ocean. Mar. Ecol. Prog. Ser. 2012, 470, 207–233. [Google Scholar] [CrossRef][Green Version]
  84. Wells, M.L.; Trainer, V.L.; Smayda, T.J.; Karlson, B.S.; Trick, C.G.; Kudela, R.M.; Ishikawa, A.; Bernard, S.; Wulff, A.; Anderson, D.M.; et al. Harmful algal blooms and climate change: Learning from the past and present to forecast the future. Harmful Algae 2015, 49, 68–93. [Google Scholar] [CrossRef] [PubMed][Green Version]
  85. Zhu, Z.; Qu, P.; Fu, F.; Tennenbaum, N.; Tatters, A.O.; Hutchins, D.A. Understanding the blob bloom: Warming increases toxicity and abundance of the harmful bloom diatom Pseudonitzschia in California coastal waters. Harmful Algae 2017, 67, 36–43. [Google Scholar] [CrossRef]
  86. Anderson, D.M.; Glibert, P.M.; Burkholder, J.M. Harmful algal blooms and eutrophication: Nutrient sources, composition and consequences. Estuaries 2002, 4B, 704–726. [Google Scholar] [CrossRef]
  87. Olli, K.; Kangro, K.; Kabel, M. Akinete production of Anabaena lemmermannii and A. cylindrica (Cyanophyceae) in natural populations of N- and P-limited coastal mesocosms. J. Phycol. 2005, 41, 1094–1098. [Google Scholar] [CrossRef]
  88. Figueredo, C.C.; Pinto-Coelho, R.M.; Lopes, A.M.M.B.; Lima, P.H.; Gücker, B.; Giani, A. From intermittent to persistent cyanobacterial blooms: Identifying the main drivers in an urban tropical reservoir. J. Limnol. 2016, 75, 445–454. [Google Scholar] [CrossRef][Green Version]
  89. Ma, J.; Qin, B.; Paerl, H.W.; Brookes, J.D.; Hall, N.S.; Shi, K.; Long, S. The persistence of cyanobacterial (Microcystis spp.) blooms throughout winter in Lake Taihu, China. Limnol. Oceanogr. 2016, 61, 711–722. [Google Scholar] [CrossRef][Green Version]
  90. Heller, U.; Struss, P.; Guerrin, F.; Roque, W. A qualitative modeling approach to algal bloom prediction. In Proceedings of the IJCAI-95 Workshop on Artificial Intelligence and the Environment, Montreal, QC, Canada, 20–25 August 1995; pp. 21–26. [Google Scholar]
  91. Bates, S.S.; de Freitas, A.S.W.; Milley, J.E.; Pocklington, R.; Quilliam, M.A.; Smith, J.G.; Worms, J. Controls on domoic acid production by the diatom Nitzschia pungens f. multiseries in culture: Nutrients and irradiance. Can. J. Fish. Aquat. Sci. 1991, 48, 1136–1144. [Google Scholar] [CrossRef][Green Version]
  92. Smith, V.H. Low nitrogen to phosphorus ratios favor dominance by blue-green algae in Lake Phytoplankton. Science 1983, 221, 669–671. [Google Scholar] [CrossRef][Green Version]
  93. Preece, E.P.; Hardy, F.J.; Moore, B.C.; Bryan, M. A review of microcystin detections in estuarine and marine waters: Environmental implications and human health risk. Harmful Algae 2017, 61, 31–45. [Google Scholar] [CrossRef][Green Version]
  94. van der Westhuizen, A.J.; Eloff, J.N. Effect of temperature and light on the toxicity and growth of the bluegreen alga Microcystis aeruginosa (UV-006). Planta 1985, 163, 55–59. [Google Scholar] [CrossRef] [PubMed]
  95. Watanabe, M.F.; Oishi, S. Effects of environmental factors on toxicity of a cyanobacterium (Microcystis aeruginosa) under culture conditions. Appl. Environ. Microbiol. 1985, 49, 1342–1344. [Google Scholar] [CrossRef] [PubMed][Green Version]
  96. Griffith, A.W.; Gobler, C.J. Temperature Controls the toxicity of the icthyotoxic dinoflagellate, Cochlodinium polykrikoides. Mar. Ecol. Prog. Ser. 2016, 545, 63–76. [Google Scholar] [CrossRef]
  97. Kim, J.; Seo, J.-K.; Yoon, H.; Kim, P.-J.; Choi, K. Combined effects of the cyanobacterial toxin microcystin-LR and environmental factors on lifehistory traits of indigenous cladoceran Moina macrocopa: Combined toxicity of MC-LR and water environmental factors. Environ. Toxicol. Chem. 2014, 33, 2560–2565. [Google Scholar] [CrossRef] [PubMed]
  98. Zhang, X.; Ji, W.; Zhang, H.; Zhang, W.; Xie, P. Studies on the toxic effects of microcystin-LR on the zebrafish (Danio rerio) under differenttemperatures. J. Appl. Toxicol. 2011, 31, 561–567. [Google Scholar] [CrossRef]
  99. Kim, H.; Spivack, A.J.; Menden-Deuer, S. pH alters the swimming behaviors of the raphidophyte Heterosigma akashiwo: Implications for bloom formation in an acidified ocean. Harmful Algae 2013, 26, 1–11. [Google Scholar] [CrossRef]
  100. Talmage, S.C.; Gobler, C.J. Effects of CO2 and the harmful alga Aureococcus anophagefferens on growth and survival of oyster and scallop larvae. Mar. Ecol. Prog. Ser. 2012, 464, 121–134. [Google Scholar] [CrossRef][Green Version]
  101. Griffith, A.W.; Gobler, C.J. Transgenerational exposure of North Atlantic bivalves to ocean acidification renders offspring more vulnerable to low pH and additional stressors. Sci. Rep. 2017, 7, e11394. [Google Scholar] [CrossRef][Green Version]
  102. Hu, M.; Wu, F.; Yuan, M.; Li, Q.; Gu, Y.; Wang, Y.; Liu, Q. Antioxidant responses of triangle sail mussel Hyriopsis cumingii exposed to harmful algae Microcystis aeruginosa and hypoxia. Chemosphere 2015, 139, 541–549. [Google Scholar] [CrossRef] [PubMed]
  103. Hu, M.; Wu, F.; Yuan, M.; Liu, Q.; Wang, Y. Combined effects of toxic cyanobacteria Microcystis aeruginosa and hypoxia on the physiological responses of triangle sail mussel Hyriopsis cumingii. J. Hazard. Mater. 2016, 306, 24–33. [Google Scholar] [CrossRef]
  104. Wu, F.; Kong, H.; Shang, Y.; Zhou, Z.; Gul, Y.; Liu, Q.; Hu, M. Histopathological alterations in triangle sail mussel (Hyriopsis cumingii) exposed to toxic cyanobacteria (Microcystis aeruginosa) under hypoxia. Aquaculture 2017, 467, 182–189. [Google Scholar] [CrossRef]
  105. Ramana, T.V.; Reddy, M.P.M. Upwelling and sinking in the Arabian sea along Dakshina Kannada coast. Environ. Ecol. 2006, 24, 379–384. [Google Scholar]
  106. Malaei Tavana, H.; Behpoor, S.; Changizi, M.; Karimi, H. Investigate the reinforcing factors in forming and occurrence of harmful algal bloom. In Proceedings of the National Conference on Human, Environment and Sustainable Development, Hamedan, Iran; 2008. [Google Scholar]
  107. Taghavi, L.; Abbaspour, M. The determinative factors for modeling and management of red tide in the Persian Gulf. In Proceedings of the First International Conference of Environmental and Geopolitical Persian Gulf, Qeshm Island, Iran; 2012. [Google Scholar]
  108. Garcia-Hernandez, J.; Garcia-Rica, L.; Jara-Marini, E.E.; Barraza-Guaradado, R.; Weaver, A.H. Concentrations of heavy metal in sediments and organism during a harmful algal bloom (HAB) at Kun Kaak Bay, Sonora, Mexico. Mar. Pollut. Bull. 2005, 50, 733–739. [Google Scholar] [CrossRef] [PubMed]
  109. News Report number PII: S2225-326X (01) 00229-6. Red tides and dust storms. Mar. Pollut. Bull. 2001, 42, e796. [CrossRef]
  110. Gobler, C.J.; Donat, J.R.; Consolvo, J.A.; Sanudo-wilhemy, S.A. Physicochemical speciation of iron during coastal algal blooms. Mar. Chem. 2002, 77, 71–89. [Google Scholar] [CrossRef]
  111. Anderson, M.D. Red tides. Sci. Am. J. 1994, 271, 52–58. [Google Scholar] [CrossRef] [PubMed]
  112. Ospar Commission. Assessment of the Impacts of Shipping on the Marine Environment; Ospar Commission: London, UK, 2009; ISBN 978-1-906840-80-8. [Google Scholar]
  113. Anil, A.C.; Venkat, K.; Sawant, S.S.; Dileepkumar, M.; Dhargalkar, V.K.; Ramaiah, N.; Harkantra, S.N.; Ansari, Z.A. Marine bioinvasion: Concern for ecology and shipping. Curr. Sci. 2002, 83, 214–218. [Google Scholar]
  114. Untawale, A.G.; Agadi, V.V.; Dhargalkar, V.K. Mahasagar: Bulletin National Institute of Oceanography; National Institute of Oceanography: Goa, India, 1980; Volume 23, pp. 179–181. [Google Scholar]
  115. Waldichuk, M. Marine biotoxins and human activity. Mar. Pollut. Bull. 1990, 21, 215–216. [Google Scholar] [CrossRef]
  116. Carmichael, W.W.; Boyer, G.L. Health impacts from cyanobacteria harmful algae blooms: Implications for the North American Great Lakes. Harmful Algae 2016, 54, 194–212. [Google Scholar] [CrossRef]
  117. Sournia, A.; Chretiennotdinet, M.J.; Ricard, M. Marine phytoplankton: How many species in the world ocean? J. Plankton Res. 1991, 13, 1093–1099. [Google Scholar] [CrossRef]
  118. Hallegraef, G.M.; Anderson, D.M.; Cembella, C.D. Manual on Harmful Marine Microalgae; United Nations Educational, Scientific and Cultural Organization (UNESCO): Paris, France, 2003; p. 770. [Google Scholar]
  119. Shumway, S.E. A review of the effects of algal blooms on shellfish and aquaculture. J. World Aquat. Soc. 1990, 21, 65–104. [Google Scholar] [CrossRef]
  120. Silbergeld, E.K.; Grattan, L.; Oidach, D.; Morris, J.G. Pfiesteria: Harmful algal blooms as Indicator of Human: Ecosystem interactions. Environ. Res. Sec. A 2000, 82, 97–105. [Google Scholar] [CrossRef] [PubMed][Green Version]
  121. Anderson, D.M.; Cembella, A.D.; Hallegraeff, G.M. Progress in understanding harmful algal blooms: Paradigm shifts and new technologies for research, monitoring, and management. Ann. Rev. Mar. Sci. 2012, 4, 143–176. [Google Scholar] [CrossRef] [PubMed][Green Version]
  122. Ianora, A.; Bentley, M.G.; Caldwell, G.S.; Casotti, R.; Cembella, A.D.; EngströmÖst, J.; Halsband, C.; Sonnenschein, E.; Legrand, C.; Llewellyn, C.A.; et al. The relevance of marine chemical ecology to plankton and ecosystem function: An emerging field. Mar. Drugs 2011, 9, 1625–1648. [Google Scholar] [CrossRef] [PubMed][Green Version]
  123. Ibelings, B.W.; Backer, L.C.; Kardinaal, W.E.; Chorus, I. Current approaches to cyanotoxin risk assessment and risk management around the globe. Harmful Algae 2015, 49, 63–74. [Google Scholar] [CrossRef] [PubMed][Green Version]
  124. Lawrence, J.; Loreal, H.; Toyofuku, H.; Hess, P.; Karunasagar, I.; Ababouch, L. Assessment and management of biotoxin risks in bivalve molluscs. FAO Fisher. Aquacult. Tech. Paper. 2011, 551, 1–337. [Google Scholar]
  125. Turner, J.T.; Granéli, E. “Top-down” predation control on marine harmful algae”. In Ecology of Harmful Algae; Granéli, E., Turner, J.T., Eds.; Springer: Berlin, Germany, 2006; pp. 355–366. [Google Scholar]
  126. Turner, J.T. Zooplankton community grazing impact on a bloom of Alexandrium fundyense in the Gulf of Maine. Harmful Algae 2010, 9, 578–589. [Google Scholar] [CrossRef]
  127. Davis, T.W.; Gobler, C.J. Grazing by mesozooplankton and microzooplankton on toxic and non-toxic strains of Microcystis in the Transquaking River, a tributary of Chesapeake Bay. J. Plankton Res. 2011, 33, 415–430. [Google Scholar] [CrossRef][Green Version]
  128. Weissbach, A.; Rudstrom, M.; Olofsson, M.; Bechemin, C.; Icely, J.; Newton, A.; Tillmann, U.; Legrand, C. Phytoplankton allelochemical interactions change microbial food web dynamics. Limnol. Oceanogr. 2011, 56, 899–909. [Google Scholar] [CrossRef]
  129. Hoagland, P.; Anderson, D.M.; Kaoru, Y.; White, A.W. The economic effects of harmful algal blooms in the United States: Estimates, assessment issues, and information needs. Estuaries 2002, 25, 677–695. [Google Scholar] [CrossRef]
  130. Anderson, D.; Hoagland, P.; Kaoru, Y.; White, A.W. Estimated Annual Economic Impacts from Harmful Algal Blooms (HABs) in the United States. In Woods Hole Oceanographic Institution Technical Report: WHOI-2000–2011; Woods Hole Oceanogr Inst.: Woods Hole, MA, USA, 2000. [Google Scholar]
  131. Dodds, W.K.; Bouska, W.W.; Eitzmann, J.L.; Pilger, T.J.; Pitts, K.L.; Riley, A.J.; Schloesser, J.T.; Thornbrugh, D.J. Eutrophication of U.S. Freshwaters: Analysis of potential economic damages. Environ. Sci. Technol. 2009, 43, 12–19. [Google Scholar] [CrossRef] [PubMed][Green Version]
  132. Sanseverino, I.; Conduto, D.; Pozzoli, L.; Dobricic, S.; Lettieri, T. Algal Bloom and its Economic Impact. In EUR 27905 EN; European Union: Luxembourg, 2016. [Google Scholar]
  133. Pretty, J.N.; Mason, C.F.; Nedwell, D.B.; Hine, R.E.; Leaf, S.; Dils, R. Environmental costs of freshwater eutrophication in England and Wales. Environ. Sci. Technol. 2003, 37, 201–208. [Google Scholar] [CrossRef] [PubMed][Green Version]
  134. Anderson, D.M.; Andersen, P.; Bricelj, V.M.; Cullen, J.J.; Rensel, J.E. Monitoring and management strategies for harmful algal blooms in coastal waters, APEC #201-MR-01.1. In Asia Pacific Economic Program, Singapore, and Intergovernmental Oceanographic Commission Technical Series; Intergovernmental Oceanographic Commission: Paris, France, 2001; 268p. [Google Scholar]
  135. Ahlvik, L.; Hyytiäinen, K. Value of adaptation in water protection—Economic impacts of uncertain climate change in the Baltic Sea. Ecol. Econ. 2015, 116, 231–240. [Google Scholar] [CrossRef]
  136. Steffensen, D.A. Economic cost of cyanobacterial blooms. Adv. Exp. Med. Biol. 2008, 619, 855–865. [Google Scholar] [PubMed]
  137. Bernard, S.; Kudela, R.; Velo-Suárez, L. Developing global capabilities for the observation and prediction of harmful algal blooms. In Oceans and Society: Blue Planet; Djavidnia, S., Cheung, V., Ott, M., Seeyave, S., Eds.; Cambridge Scholars Publishing: Cambridge, UK, 2014; pp. 46–52. [Google Scholar]
  138. Macauley, M.K. The value of information: Measuring the contribution of space-derived earth science data to resource management. Space Policy 2006, 22, 274–282. [Google Scholar] [CrossRef]
  139. Landsberg, J.H. The effects of harmful algal blooms on aquatic organisms. Rev. Fish. Sci. 2002, 10, 113–390. [Google Scholar] [CrossRef]
  140. FAO. State of world aquaculture, 2006. In FAO Fisheries Technical Report Paper No. 500; Inland Water and Aquaculture Service, Fishery Resources Division, FAO Fisheries Department: Rome, Italy, 2006. [Google Scholar]
  141. Berdalet, E.; Fleming, L.E.; Gowen, R.; Davidson, K.; Hess, P.; Backer, L.C.; Enevoldsen, H. Marine harmful algal blooms, human health and wellbeing: Challenges and opportunities in the 21st century. J. Mar. Biol. Assoc. UK 2016, 96, 61–91. [Google Scholar] [CrossRef][Green Version]
  142. Larkin, S.; Adams, C. Harmful algal blooms and coastal business: Economic consequences in Florida. Soc. Nat. Resour. 2007, 20, 849–859. [Google Scholar] [CrossRef]
  143. Morgan, K.; Larkin, S.L.; Adams, C.M. Red tides and participation in marine-based activities: Estimating the response of Southwest Florida residents. Harmful Algae 2010, 9, 333–341. [Google Scholar] [CrossRef]
  144. Dolah, M.; Roelke, D.; Greene, R.M. Health and Ecological Impacts of Harmful Algal Blooms: Risk Assessment Needs. Hum. Ecol. Risk Assess. An Int. J. 2001, 7, 1329–1345. [Google Scholar] [CrossRef]
  145. Kazmi, S.S.U.H.; Xu, G.; Xuexi, T.; Xu, H. Insights into identifying the effect of harmful algae on ecological quality status using periphytic ciliates in marine ecosystems. Ecol. Ind. 2020, 117, e106581. [Google Scholar] [CrossRef]
  146. Harmful Algal Research and Response. A National Environmental Science Strategy 2005–2015; Ramsdell, J.S.; Anderson, D.M.; Glibert, P.M. (Eds.) Ecological Society of America: Washington, DC, USA, 2005; p. 96. [Google Scholar]
  147. Fleming, L.E.; Easom, J.; Baden, D.; Rowan, A.; Levin, B. Emerging harmful algal blooms and human health: Pfiesteria and related organisms. Toxicol. Pathol. 1999, 27, 573–581. [Google Scholar] [CrossRef] [PubMed]
  148. Smayda, T.J.; Villareal, T.A. The 1985 ‘brown-tide’and the open phytoplankton niche in Narragansett Bay during summer. In Novel Phytoplankton Blooms; Springer: Berlin/Heidelberg, Germany, 1989; pp. 159–187. [Google Scholar]
  149. Buskey, E.J.; Hyatt, C.J. Effects of the Texas “brown tide” alga on planktonic grazers. Mar. Ecol. Prog. Ser. 1995, 126, 285–292. [Google Scholar] [CrossRef]
  150. Heinbokel, J.F. Studies of the functional role of tintinnids in the Southern California Bight. I. Grazing and growth rates in laboratory cultures. Mar. Biol. 1978, 47, 177–189. [Google Scholar] [CrossRef]
  151. Jonsson, P.R. Particle size selection, feeding rates and growth dynamics of marine planktonic oligotrichous ciliates (Ciliophora: Oligotrichina). Mar. Ecol. Prog. Ser. 1986, 33, 265–277. [Google Scholar] [CrossRef]
  152. Buskey, E.J.; Coulter, C.J.; Brown, S.L. Feeding, growth and bioluminescence of the heterotrophic dinoflagellate Protoperidinium huberi. Mar. Biol. 1994, 121, 373–380. [Google Scholar] [CrossRef]
  153. Gifford, D.J. The protozoanmetazoan trophic link in pelagic ecosystems. J. Protozool. 1991, 38, 81–86. [Google Scholar] [CrossRef]
  154. Cyr, H.; Pace, M.L. Grazing by zooplankton and its relationship to community structure. Can. J. Fish. Aquat. Sci. 1992, 49, 1455–1465. [Google Scholar] [CrossRef]
  155. McManus, G.B.; Ederington-Cantrell, M.C. Phytoplankton pigments and growth rates, and microzooplankton grazing in a large temperate estuary. Mar. Ecol. Prog. Ser. 1992, 87, 77–85. [Google Scholar] [CrossRef]
  156. Montagnes, D.J.S.; Lessard, E.J. Population dynamics of the marine planktonic ciliate Strombidinopsis multiaris: Its potential to control phytoplankton blooms. Aquat. Microb. Ecol. 1999, 20, 167–181. [Google Scholar] [CrossRef]
  157. Strom, S.L.; Morello, T.A. Comparative growth rates and yields of ciliates and heterotrophic dinoflagellates. J. Plankton Res. 1998, 20, 571–584. [Google Scholar] [CrossRef]
  158. Kamiyama, T. Growth and grazing responses of tintinnid ciliates feeding on the toxic dinoflagellate Heterocapsa circularisquama. Mar. Biol. 1997, 128, 509–515. [Google Scholar] [CrossRef]
  159. Jeong, H.J.; Shim, J.H.; Lee, C.W.; Kim, J.S.; Koh, S.M. Growth and grazing rates of the marine planktonic ciliate Strombidinopsis sp. on red-tide and toxic dinoflagellates. J. Euk. Microbiol. 1999, 46, 69–76. [Google Scholar] [CrossRef]
  160. Needler, A.B. Paralytic shellfish poisoning and Gonyaulax tamarensis. J. Fish. Res. Bd. Can. 1949, 7, 490–504. [Google Scholar] [CrossRef]
  161. Buskey, E.J. How does eutrophication affect the role of grazers in harmful algal bloom dynamics? Harmful Algae 2008, 8, 152–157. [Google Scholar] [CrossRef]
  162. Roman, M.; Gauzens, A.L.; Rhinehart, W.K.; White, J. Effects of low oxygen water on Chesapeake Bay zooplankton. Limnol. Oceanogr. 1993, 38, 1603–1614. [Google Scholar] [CrossRef]
  163. Marcus, N.M.; Richmond, C.; Sedlacek, C.; Miller, G.A.; Oppert, C. Impact of hypoxia on the survival, egg production and population dynamics of Acartia tonsa Dana. J. Exp. Mar. Biol. Ecol. 2004, 301, 111–128. [Google Scholar] [CrossRef]
  164. Fenchel, T.; Kristensen, L.D.; Rasmussen, L. Water column anoxia: Vertical zonation of planktonic protozoa. Mar. Ecol. Prog. Ser. 1990, 62, 1–10. [Google Scholar] [CrossRef]
  165. Buskey, E.J.; Liu, H.; Collumb, C.; Bersano, J.G.F. The decline and recovery of a persistent Texas Brown Tide algal bloom in the Laguna Madre (TX, USA). Estuaries 2001, 24, 337–346. [Google Scholar] [CrossRef]
  166. Liu, H.; Buskey, E.J. Hypersalinity enhances the production of extracellular polymeric substance (EPS) in the Texas brown tide alga, Aureoumbra lagunensis (Pelagophyceae). J. Phycol. 2000, 36, 71–77. [Google Scholar] [CrossRef]
  167. Buskey, E.J.; Stockwell, D.A. Effects of a persistent “brown tide” on zooplankton populations in the Laguna Madre of South Texas, toxic phytoplankton blooms in the sea. In Toxic Phytoplankton Blooms in the Sea; Smayda, T.J., Shimizu, Y., Eds.; Elsevier: Amsterdam, The Netherlands, 1993; pp. 659–666. [Google Scholar]
  168. Gliwicz, Z.M. Why do cladocerans fail to control algal blooms? Hydrobiologia 1990, 200, 83–97. [Google Scholar] [CrossRef]
  169. Sarnelle, O. Herbivore effects on phytoplankton succession in a eutrophic lake. Ecol. Monogr. 1993, 63, 129–149. [Google Scholar] [CrossRef]
  170. McCauley, E.; Briand, F. Zooplankton grazing and phytoplankton species richness: Field tests of the predation hypothesis 1. Limnol. Oceano. 1979, 24, 243–252. [Google Scholar] [CrossRef]
  171. Glibert, P.M. Interactions of top-down and bottom-up control in planktonic nitrogen cycling. Hydrobiologia 1998, 363, 1–12. [Google Scholar] [CrossRef]
  172. Johansson, N.; Graneli, E. Influence of different nutrient conditions on cell density, chemical composition and toxicity of Prymnesium parvum (Haptophyta) in relation to different N:P supply ratios. Mar. Ecol. Prog. Ser. 1999, 239, 243–258. [Google Scholar]
  173. Wood, R. Acute animal and human poisonings from cyanotoxin exposure—A review of the literature. Environ. Int. 2016, 91, 276–282. [Google Scholar] [CrossRef]
  174. Banack, S.A.; Caller, T.; Henegan, P.; Haney, J.; Murby, A.; Metcalf, J.S.; Powell, J.; Cox, P.A.; Stommel, E. Detection of Cyanotoxins, Beta-N-methylamino-L-alanine and Microcystins, from a Lake Surrounded by Cases of Amyotrophic Lateral Sclerosis. Toxins 2015, 7, 322–336. [Google Scholar] [CrossRef][Green Version]
  175. Koreiviene, J.; Anne, O.; Kasperoviciene, J.; Burskyte, V. Cyanotoxin management and human health risk mitigation in recreational waters. Environ. Monit. Assess. 2014, 186, 4443–4459. [Google Scholar] [CrossRef]
  176. Chen, Y.; Shen, D.; Fang, D. Nodularins in poisoning. Clin. Chim. Acta. 2013, 425, 18–29. [Google Scholar] [CrossRef]
  177. Yuan, M.; Carmichael, W.W.; Hilborn, E.D. Microcystin analysis in human sera and liver from human fatalities in Caruaru, Brazil 1996. Toxicon 2006, 48, 627–640. [Google Scholar] [CrossRef]
  178. Scholin, C.A.; Gulland, F.; Doucette, G.J.; Benson, S.; Busman, M.; Chavez, F.P.; Cordaro, J.; DeLong, R.; De Vogelaere, A.; Harvey, J.; et al. Mortality of sea lions along the central California coast linked to a toxic diatom bloom. Nature 2000, 403, 80–84. [Google Scholar] [CrossRef] [PubMed]
  179. Fehling, J.; Davidson, K.; Bolch, C.J.; Bates, S.S. Growth and domoic acid production by Pseudonitzschia seriata (Bacillariophyceae) under phosphate and silicate limitation. J. Phycol. 2004, 40, 674–683. [Google Scholar] [CrossRef]
  180. Weiss, K.R. Paying a price for paradise: Sea breeze carries arsenal of toxins ashore during red tide outbreaks. Los Angeles Times, 1 August 2006. [Google Scholar]
  181. Klontz, K.C.; Abraham, A.; Plakas, S.M.; Dickey, R.W. Musselassociated azaspiracid intoxication in the United States. Annal. Inter. Med. 2009, 150, 361. [Google Scholar] [CrossRef] [PubMed][Green Version]
  182. Twiner, M.; Hess, P.; Doucette, G.J. Azaspiracids: Toxicology, pharmacology, and risk assessment. In Seafood and Freshwater Toxins. Pharmacology, Physiology and Detection, 3rd ed.; Botana, L.M., Ed.; CRC Press: Boca Raton, FL, USA, 2014; pp. 823–855. [Google Scholar]
  183. Hess, P.; McCarron, P.; Krock, B.; Kilcoyne, J.; Miles, C.O. Azaspiracids: Chemistry, biosynthesis, metabolism and detection. In Seafood and Freshwater Toxins. Pharmacology, Physiology and Detection, 3rd ed.; Botana, L., Ed.; CRC Press: Boca Raton, FL, USA, 2014; pp. 799–821. [Google Scholar]
  184. Litaker, R.W.; Vandersea, M.W.; Faust, M.A.; Kibler, S.R.; Nau, A.W.; Holland, W.C.; Chinain, M.; Holmes, M.J.; Tester, P.A. Global distribution of ciguatera causing dinoflagellates in the genus. Gamb. Toxicon 2010, 56, 711–730. [Google Scholar] [CrossRef] [PubMed]
  185. Tester, P.A.; Kibler, S.R.; Holland, W.C.; Usup, G.; Vandersea, M.W.; Leaw, C.P.; Lim, P.T.; Jacob Larsen, J.; Mohammad-Noor, N.; Faust, M.A.; et al. Sampling harmful benthic dinoflagellates: Comparison of artificial and natural substrate methods. Harmful Algae 2014, 39, 8–25. [Google Scholar] [CrossRef]
  186. Reguera, B.; Riobo, P.; Rodriguez, F.; Diaz, P.A.; Pizarro, G.; Paz, B.; Franco, J.M.; Blanco, J. Causative organisms, distributions and fate in shellfish. Mar. Drugs 2014, 12, 394–461. [Google Scholar] [CrossRef]
  187. Watkins, S.M.; Reich, A.; Fleming, L.E.; Hammond, R. Neurotoxic shellfish poisoning. Mar. Drugs 2008, 6, 431–455. [Google Scholar] [CrossRef][Green Version]
  188. Fleming, L.E.; Kirkpatrick, B.; Backer, L.C.; Walsh, C.J.; Nierenberg, K.; Clark, J.; Reich, A.; Hollenbeck, J.; Benson, J.; Cheng, Y.S.; et al. Review of Florida red tide and human health effects. Harmful Algae 2011, 20, 224–233. [Google Scholar] [CrossRef][Green Version]
  189. Vila, M.; Arin, L.; Battocchi, C.; Bravo, I.; Fraga, S.; Penna, A.; Reñé, A.; Riobó, P.; Rodriguez, F.; Sala, M.M.; et al. Management of Ostreopsis blooms in recreational waters along the Catalan coast (NW Mediterranean Sea): Cooperation between a research project and a monitoring program. Cryptogam. Algol. 2012, 33, 143–152. [Google Scholar] [CrossRef]
  190. Ciminiello, P.; Dell’Aversano, C.; Dello Iacovo, E.; Fattorusso, E.; Forino, M.; Tartaglione, L.; Yasumoto, T.; Battocchi, C.; Giacobbe, M.; Amorim, A.; et al. Investigation of toxin profile of Mediterranean and Atlantic strains of Ostreopsis cf. siamensis (Dinophyceae) by liquid chromatography–high resolution mass spectrometry. Harmful Algae 2013, 23, 19–27. [Google Scholar] [CrossRef]
  191. Anderson, D.M.; Keafer, B.A.; Geyer, W.R.; Signell, R.P.; Loder, T.C. Toxic Alexandrium blooms in the western Gulf of Maine: The plume advection hypothesis revisited. Limnol. Oceanogr. 2005, 50, 328–345. [Google Scholar] [CrossRef][Green Version]
  192. Anderson, D.M. Approaches to monitoring, control and management of harmful algal blooms (HABs). Ocean Coast. Manag. 2009, 52, 342–347. [Google Scholar] [CrossRef] [PubMed][Green Version]
  193. Anderson, D.M. Toxic algal blooms and red tides: A global perspective. In Red Tides: Biology, Environmental Science and Toxicology; Okaichi, T., Anderson, D.M., Nemoto, T., Eds.; Elsevier: Amsterdam, The Netherlands, 1989; pp. 11–16. [Google Scholar]
  194. Smayda, T.J. Primary production and the global epidemic of phytoplankton blooms in the sea: A linkage? In Novel Phytoplankton Blooms: Causes and Impacts of Recurrent Brown Tide and Other Unusual Blooms; Cosper, E.M., Carpenter, E.J., Bricelj, V.M., Eds.; Springer: New York, NY, USA, 1989; pp. 213–222. [Google Scholar]
  195. Hallegraeff, G.M.; Bolch, C.J. Transport of diatom and dinoflagellate resting spores via ship’s ballast water: Implications for plankton biogeography and aquaculture. J. Plankton Res. 1992, 1, 67–84. [Google Scholar]
  196. Paerl, H.W.; Gardner, W.S.; Havens, K.E.; Joyner, A.R.; McCarthy, M.J.; Newell, S.E.; Scott, J.T. Mitigating cyanobacterial harmful algal blooms in aquatic ecosystems impacted by climate change and anthropogenic nutrients. Harmful Algae 2016, 54, 213–222. [Google Scholar] [CrossRef][Green Version]
  197. Okaichi, T. Red tides in the Seto Inland Sea. In Sustainable Development in the Seto Inland Sea, Japan—From the Viewpoint of Fisheries; Okaichi, T., Yanagi, Y., Eds.; Terra Scientific Publishing Company: Tokyo, Japan, 1997; pp. 251–304. [Google Scholar]
  198. Schneider, M.L.; Wilhelms, S.C.; Yates, L.I. SELECT Version 1.0 Beta: A One-Dimensional Reservoir Selective Withdrawal Model Spreadsheet; Engineer Research and Development Center, U.S. Army Corps of Engineers: Washington, DC, USA, 2004. [Google Scholar]
  199. Cong, H.B.; Huang, T.L.; Chai, B.B. Research on applying a water-lifting aerator to inhibit the growth of algae in a sourcewater reservoir. Int. J. Environ. Pollut. 2011, 45, 166–175. [Google Scholar] [CrossRef]
  200. Gallardo-Rodríguez, J.J.; Astuya-Villalón, A.; Llanos-Rivera, A.; Avello-Fontalba, V.; Ulloa-Jofré, V. A critical review on control methods for harmful algal blooms. Rev. Aquac. 2019, 11, 661–684. [Google Scholar] [CrossRef]
  201. Pierce, R.H.; Henry, M.S.; Higham, C.J.; Blum, P.; Sengco, M.R.; Anderson, D.M. Removal of harmful algal cells (Karenia brevis) and toxin from seawater culture by clay flocculation. Harmful Algae 2004, 3, 141–148. [Google Scholar] [CrossRef][Green Version]
  202. Kidwell, M.D. Prevention, Control, and Mitigation of Harmful Algal Blooms Program; National Ocean Service National Oceanic and Atmospheric Administration: Silver Spring, MD, USA, 2015; pp. 1–60. [Google Scholar]
  203. NEIWPCC (New England Interstate Water Pollution Control Commission). Harmful Algal Bloom Control Methods Synopses; NEIWPCC: Lowell, MA, USA, 2015; pp. 1–28. [Google Scholar]
  204. Nakamura, N.; Nakano, K.; Sugiura, N.; Matsumura, M. A novel control process of cyanobacterial bloom using cyanobacteriolytic bacteria immobilized in floating biodegradable plastic carriers. Environ. Technol. 2003, 24, 1569–1576. [Google Scholar] [CrossRef]
  205. Shunyu, S.; Liu, Y.D.; Shen, Y.W.; Li, G.B.; Li, D.H. Lysis of Aphanizomenon flosaquae (Cyanobacterium) by a bacterium Bacillus cereus. Biol. Contr. 2006, 39, 345–351. [Google Scholar] [CrossRef]
  206. Pei, H.; Hu, W. Lytic characteristics and identification of two algalysing bacterial strains. J. Ocean Univ. China 2006, 5, 368–374. [Google Scholar] [CrossRef]
  207. Gerphagnon, M.; Macarthur, D.J.; Latour, D.; Gachon, C.M.; Van Ogtrop, F.; Gleason, F.H.; Sime-Ngando, T. Microbial players involved in the decline of filamentous and colonial cyanobacterial blooms with a focus on fungal parasitism. Environ. Microbiol. 2015, 17, 2573–2587. [Google Scholar] [CrossRef]
  208. Caiola, M.G.; Pellegrini, S. Lysis of Microcystis aeruginosa (kütz.) by bdellovibrio-like bacteria1. J. Phycol. 1984, 20, 471–475. [Google Scholar] [CrossRef]
  209. Kim, Y.S.; Son, H.J.; Jeong, S.Y. Isolation of an algicide from a marine bacterium and its effects against the toxic dinoflagellate Alexandrium catenella and other harmful algal bloom species. J. Microbiol. 2015, 53, 511–517. [Google Scholar] [CrossRef] [PubMed]
  210. Rashidan, K.K.; Bird, D.F. Role of predatory bacteria in the termination of a cyanobacterial bloom. Microb. Ecol. 2001, 41, 97–105. [Google Scholar] [CrossRef]
  211. Sallal, A.K. Lysis of cyanobacteria with Flexibacter spp. isolated from domestic sewage. Microbios 1993, 77, 57–67. [Google Scholar]
  212. Burnham, J.C.; Collart, S.A.; Daft, M.J. Myxococcal predation of the cyanobacterium Phormidium luridum in aqueous environments. Arch. Microbiol. 1984, 137, 220–225. [Google Scholar] [CrossRef]
  213. Burnham, J.C.; Collart, S.A.; Highison, B.W. Entrapment and lysis of the cyanobacterium Phormidium luridum by aqueous colonies of Myxococcus xanthus PCO2. Arch. Microbiol. 1981, 129, 285–294. [Google Scholar] [CrossRef]
  214. Kim, J.D.; Kim, B.; Lee, C.G. Algalytic activity of Pseudomonas fluorescens against the red tide causing marine alga Heterosigma akashiwo (Raphidophyceae). Biol. Control. 2007, 41, 296–303. [Google Scholar] [CrossRef]
  215. Zhang, H.; Yu, Z.; Huang, Q.; Xiao, X.; Wang, X.; Zhang, F.; Hu, C. Isolation, identification and characterization of phyto-planktonlytic bacterium CH-22 against Microcystis aeruginosa. Limnologica 2011, 41, 70–77. [Google Scholar] [CrossRef][Green Version]
  216. Yang, L.; Maeda, H.; Yoshikawa, T.; Zhou, G.Q. Algicidal effect of bacterial isolates of Pedobacter sp. against cyanobacterium Microcystis aeruginosa. Water Sci. Eng. 2012, 5, 375–382. [Google Scholar]
  217. Su, J.F.; Shao, S.C.; Ma, F.; Lu, J.S.; Zhang, K. Bacteriological control by Raoultella sp. R11 on growth and toxins production of Microcystis aeruginosa. Chem. Eng. J. 2016, 293, 139–150. [Google Scholar] [CrossRef]
  218. Zheng, L.; Cui, Z.; Xu, L.; Sun, C.; Powell, R.J.; Hill, R.T. Draft genome sequence of Rhodobacteraceae strain PD-2, an algi-cidal bacterium with a quorum-sensing system, isolated from the marine microalga Prorocentrum donghaiense. Genome Announc. 2015, 3, e01549. [Google Scholar] [CrossRef] [PubMed][Green Version]
  219. Choi, H.J.; Kim, B.H.; Kim, J.D.; Han, M.S. Streptomyces neyagawaensis as a control for the hazardous biomass of Microcystis aeruginosa (Cyanobacteria) in eutrophic freshwaters. Biol. Control. 2005, 33, 335–343. [Google Scholar] [CrossRef]
  220. Ashton, P.J.; Robarts, R.D. Apparent predation of Microcystis aeruginosa Kütz. Emend elenkin by a Saprospira-like bacterium in a hypertrophic lake (Hartbeespoort Dam, South Africa). J. Limnol. Soc. S. Afr. 1987, 13, 44–47. [Google Scholar]
  221. Luo, J.; Wang, Y.; Tang, S.; Liang, J.; Lin, W.; Luo, L. Isolation and identification of algicidal compound from Streptomyces and algicidal mechanism to Microcystis aeruginosa. PLoS ONE 2013, 8, e76444. [Google Scholar] [CrossRef]
  222. Imai, I.; Kido, T.; Yoshinaga, I.; Ohgi, K.; Nagai, S. Isolation of Microcystis-killer bacterium Agrobacterium vitis from the biofilm on the surface of the water plant Egeria densa. Kalliopi A Pagou. 2010, 150, 150–152. [Google Scholar]
  223. Pal, M.; Pal, S.; Qureshi, A.; Sangolkar, L.N. Perspective of cyanobacterial harmful algal bloom (HAB) mitigation: Microcystis toxin degradation by bacterial consortia. Indian J. Exp. Biol. 2018, 56, 511–518. [Google Scholar]
  224. Danyang, Z.; Qian, Y.; Fuxing, Z.; Xueping, S.; Yongxiang, F.; Xiaoying, Z.; Hong, X. Flocculating properties and potential of Halobacillus sp. strain H9 for the mitigation of Microcystis aeruginosa blooms. Chemosphere 2019, 218, 138–146. [Google Scholar]
  225. Lovejoy, C.; Bowman, J.P.; Hallegraeff, G.M. Algicidal effects of a novel marine Pseudoalteromonas isolate (class Proteobacteria, Gamma subdivision) on harmful algal bloom species of the genera Chattonella, Gymnodinium, and Heterosigma. Appl. Environ. Microbiol. 1998, 64, 2806–2813. [Google Scholar] [CrossRef][Green Version]
  226. Guan, C.; Guo, X.; Cai, G.; Zhang, H.; Li, Y.; Zheng, W.; Zheng, T. Novel algicidal evidence of a bacterium Bacillus sp. LP-10 killing Phaeocystis globosa, a harmful algal bloom causing species. Bio. Control 2014, 76, 79–86. [Google Scholar] [CrossRef]
  227. Yoshinaga, I.; Kawai, T.; Ishida, Y. Analysis of algicidal ranges of the bacteria killing the marine dinoflagellate Gymnodinium mikimotoi isolated from Tanabe Bay, Wakayama Pref, Japan. Fish. Sci. 1997, 63, 94–98. [Google Scholar] [CrossRef][Green Version]
  228. Kim, Y.S.; Lee, D.S.; Jeong, S.Y.; Lee, W.J.; Lee, M.S. Isolation and characterization of a marine algicidal bacterium against the harmful raphidophyceae Chattonella marina. J. Microbiol. 2009, 47, 9–18. [Google Scholar] [CrossRef] [PubMed]
  229. Wang, B.X.; Zhou, Y.Y.; Bai, S.J.; Su, J.Q.; Tian, Y.; Zheng, T.L.; Yang, X. A novel marine bacterium algicidal to the toxic dino-flagellate Alexandrium tamarense. Lett. Appl. Microbiol. 2010, 51, 552–557. [Google Scholar] [CrossRef]
  230. Skerratt, J.H.; Bowman, J.P.; Hallegraeff, G.; James, S.; Nichols, P.D. Algicidal bacteria associated with blooms of a toxic dinoflagellate in a temperate Australian estuary. Mar. Ecol. Prog. Ser. 2002, 244, 1–15. [Google Scholar] [CrossRef][Green Version]
  231. Gustafsson, S.; Hultberg, M.; Figueroa, R.I.; Rengefors, K. On the control of HAB species using low biosurfactant concentrations. Harmful Algae 2009, 8, 857–863. [Google Scholar] [CrossRef]
  232. Hare, C.E.; Demir, E.; Coyne, K.J.; Craig Cary, S.; Kirchman, D.L.; Hutchins, D.A. A bacterium that inhibits the growth of Pfiesteria piscicida and other dinoflagellates. Harmful Algae 2005, 4, 221–234. [Google Scholar] [CrossRef]
  233. Urrutia-Cordero, P.; Ekvall, M.K.; Hansson, L.A. Controlling harmful cyanobacteria: Taxaspecific responses of cyanobacteria to grazing by largebodied Daphnia in a biomanipulation scenario. PLoS ONE 2016, 11, e0153032. [Google Scholar] [CrossRef]
  234. Knisely, K.; Geller, W. Selective feeding of four zooplankton species on natural lake phytoplankton. Oecologia 1986, 69, 86–94. [Google Scholar] [CrossRef]
  235. Görgényi, J.; Boros, G.; Vitál, Z.; Mozsár, A.; Várbíró, G.; Vasas, G.; Borics, G. The role of filter-feeding Asian carps in algal dispersion. Hydrobiologia 2016, 764, 115–126. [Google Scholar] [CrossRef][Green Version]
  236. Jeong, H.J.; Kim, J.S.; Yoo, Y.D.; Kim, S.T.; Song, J.Y.; Kim, T.H.; Seong, K.A.; Kang, N.S.; Kim, M.S.; Kim, J.H.; et al. Control of the harmful alga Cochlodinium polykrikoides by the naked ciliate Strombidinopsis jeokjo in mesocosm enclosures. Harmful Algae 2008, 7, 368–377. [Google Scholar] [CrossRef]
  237. Kamiyama, T.; Tsujino, M.; Matsuyama, Y.; Uchida, T. Growth and grazing rates of the tintinnid ciliate Favella taraikaensis on the toxic dinoflagellate Alexandrium tamarense. Mar. Biol. 2005, 147, 989–997. [Google Scholar] [CrossRef]
  238. Jeong, H.J.; Jae, S.K.; Jong, H.K.; Seong, T.K.; Kyeong, A.S.; Tae, H.K.; Jae, Y.S.; Soo, K.K. Feeding and grazing impact of the newly described heterotrophic dinoflagellate Stoeckeria algicida on the harmful alga Heterosigma akashiwo. Mar. Ecol. Prog. Ser. 2005, 295, 69–78. [Google Scholar] [CrossRef]
  239. Salim, S.; Bosma, R.; Vermuë, M.H.; Wijffels, R.H. Harvesting of microalgae by bio-flocculation. J. Appl. Phycol. 2011, 23, 849–855. [Google Scholar] [CrossRef][Green Version]
  240. Jia, Y.; Du, J.J.; Fang, H.; Zhao, G.Y.; Tian, X.J. Inhibition of freshwater algal species by co-culture with two fungi. Mat. Sci. Eng. C-Mater. 2013, 33, 2451–2454. [Google Scholar] [CrossRef] [PubMed]
  241. Han, G.M.; Feng, X.G.; Jia, Y.; Wang, C.Y.; He, X.B.; Zhou, Q.Y.; Tian, X.J. Isolation and evaluation of Terrestrial fungi with algicidal ability from Zijin Mountain, Nanjing, China. J. Microbiol. 2011, 49, 562–567. [Google Scholar] [CrossRef] [PubMed]
  242. Salazar Torres, G.; Silva, L.H.; Rangel, L.M.; Attayde, J.L.; Huszar, V.L. Cyanobacteria are controlled by omnivorous filter-feeding fish (Nile tilapia) in a tropical eutrophic reservoir. Hydrobiologia 2016, 765, 115–129. [Google Scholar] [CrossRef]
  243. Nagasaki, K.; Yamaguchi, M. Isolation of a virus infectious to the harmful bloom causing microalga Heterosigma akashiwo (Raphidophyceae). Aquat. Microb. Ecol. 1997, 13, 135–140. [Google Scholar] [CrossRef]
  244. Lawrence, J.E.; Chan, A.M.; Suttle, C.A.; British, I. A novel virus (HaNIV) causes lysis of the toxic bloom-forming alga heterosigma akashiwo (raphidophyceae). J. Phycol. 2001, 37, 216–222. [Google Scholar] [CrossRef]
  245. Mizumoto, H.; Tomaru, Y.; Takao, Y.; Shirai, Y.; Nagasaki, K. Intraspecies host specificity of a single-stranded RNA virus infecting a marine photosynthetic protist is determined at the early steps of infection. J. Virol. 2007, 81, 1372–1378. [Google Scholar] [CrossRef][Green Version]
  246. Backer, L.C.; Manassarambaptiste, D.; Leprell, R.; Bolton, B. Cyanobacteria and algae blooms: Review of health and environmental data from the Harmful Algal Bloom-Related Illness Surveillance System (HABISS) 2007–2011. Toxins 2015, 7, 1048–1064. [Google Scholar] [CrossRef][Green Version]
  247. Li, H.; Pan, G. Simultaneous removal of harmful algal blooms and microcystins using microorganism- and chitosan-modified local soil. Environ. Sci. Technol. 2015, 49, 6249–6625. [Google Scholar] [CrossRef] [PubMed][Green Version]
  248. Alamri, S.A.; Mohamed, Z.A. Selective inhibition of toxic cyanobacteria by β-carboline-containing bacterium Bacillus flexus isolated from Saudi freshwaters. Saudi J. Biol. Sci. 2013, 20, 357–363. [Google Scholar] [CrossRef] [PubMed][Green Version]
  249. Yang, X.; Li, X.; Zhou, Y.; Zheng, W.; Yu, C.; Zheng, T. Novel insights into the algicidal bacterium DH77-1 killing the toxic dinoflagellate Alexandrium tamarense. Sci. Total Environ. 2014, 482–483, 116–124. [Google Scholar] [CrossRef] [PubMed]
  250. Matthijs, H.C.P.; Visser, P.M.; Reeze, B.; Meeuse, J.; Slot, P.C.; Wjin, G.; Talens, R.; Huisman, J. Selective suppression of harmful cyanobacteria in an entire lake with hydrogen peroxide. Water Res. 2012, 46, 1460–1472. [Google Scholar] [CrossRef]
  251. Stumpf, R.P.; Culver, M.E.; Tester, P.A.; Tomlinson, M.; Kirkpatrick, G.J.; Pederson, B.A.; Truby, E.; Ransibrahmanakul, V.; Soracco, M. Monitoring Karenia brevis blooms in the Gulf of Mexico using satellite ocean color imagery and other data. Harmful Algae 2003, 2, 147–160. [Google Scholar] [CrossRef]
  252. Luerssen, R.M.; Thomas, A.C.; Hurst, J. Relationships between satellite-measured thermal features and Alexandrium-imposed toxicity in the Gulf of Maine. Deep. Sea Res. Part II 2005, 52, 2656–2673. [Google Scholar] [CrossRef]
  253. McManus, M.A.; Kudela, R.M.; Silver, M.W.; Steward, G.F.; Donaghay, P.L.; Sullivan, J.M. Cryptic blooms: Are thin layers the missing connection? Estuar. Coasts 2008, 31, 396–401. [Google Scholar] [CrossRef]
  254. Ryan, J.P.; Gower, J.F.R.; King, S.A.; Bissett, W.P.; Fischer, A.M.; Kudela, R.M.; Kolber, Z.; Mazzillo, F.; Rienecker, E.V.; Chavez, F.P. A coastal ocean extreme bloom incubator. Geophys. Res. Lett. 2008, 35, e12602. [Google Scholar] [CrossRef]
  255. Mouw, C.B.; Hardman-Mountford, N.J.; Alvain, S.; Bracher, A.; Brewin, R.J.W.; Bricaud, A.; Ciotti, A.M.; Devred, E.; Fujiwara, A.; Hirata, T.; et al. A consumer’s guide to satellite remote sensing of multiple phytoplankton groups in the Global Ocean. Front. Mar. Sci. 2017, 4, e41. [Google Scholar] [CrossRef][Green Version]
  256. Lombard, F.; Boss, E.; Waite, A.M.; Vogt, M.; Uitz, J.; Stemmann, L.; Sosik, H.M.; Schulz, J.; Romagnan, J.-B.; Picheral, M.; et al. Globally consistent quantitative observations of planktonic ecosystems. Front. Mar. Sci. 2019, 6, 196. [Google Scholar] [CrossRef][Green Version]
  257. Shapiro, J.; Dixon, L.K.; Schofield, O.M.; Kirkpatrick, B.; Kirkpatrick, G.J. New sensors for ocean observing: The optical phytoplankton discriminator. In Coastal Ocean Observing Systems; Liu, Y., Kerkering, H., Weisberg, R.H., Eds.; Academic Press: Boston, MA, USA, 2015; pp. 326–350. [Google Scholar]
  258. Scholin, C.; Massion, E.I.; Wright, D.K.; Cline, D.E.; Mellinger, E.; Brown, M. Aquatic Autosampler Device. U.S. Patent No. 6187530, 2001. [Google Scholar]
  259. Doucette, G.J.; Mikulski, C.M.; Jones, K.L.; King, K.L.; Greenfield, D.I.; Marin, R.; Jensen, S.; Roman, B.; Elliott, C.T.; Scholin, C.A. Remote, subsurface detection of the algal toxin domoic acid onboard the environmental sample processor: Assay development and field trials. Harmful Algae 2009, 8, 880–888. [Google Scholar] [CrossRef]
  260. Bowers, H.A.; Marin, R., III; Birch, J.M.; Scholin, C.A. Sandwich hybridization probes for the detection of Pseudonitzschia (Bacillariophyceae) species: An update to existing probes and a description of new probes. Harmful Algae 2017, 70, 37–51. [Google Scholar] [CrossRef] [PubMed]
  261. Harred, L.B.; Campbell, L. Predicting harmful algal blooms: A case study with Dinophysis ovum in the Gulf of Mexico. J. Plankt. Res. 2014, 36, 1434–1445. [Google Scholar] [CrossRef]
  262. Benfield, M.C.; Grosjean, P.; Culverhouse, P.F.; Irigoien, X.; Sieracki, M.E.; Lopez-Urrutia, A.; Dam, H.; Hu, Q.; Davis, C.; Hanson, A.; et al. RAPID: Research on automated plankton identification. Oceanography 2007, 20, 172–187. [Google Scholar] [CrossRef]
  263. Anderson, D.M. Identification of harmful algal species using molecular probes: An emerging perspective. In Harmful Marine Algal Blooms Technique et Documentation; Lassus, P., Arzul, G., Erard, E., Gentien, P., Marcaillou, C., Eds.; Intercept Ltd.: Paris, France, 1995; pp. 3–13. [Google Scholar]
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Kazmi, S.S.U.H.; Yapa, N.; Karunarathna, S.C.; Suwannarach, N. Perceived Intensification in Harmful Algal Blooms Is a Wave of Cumulative Threat to the Aquatic Ecosystems. Biology 2022, 11, 852. https://doi.org/10.3390/biology11060852

AMA Style

Kazmi SSUH, Yapa N, Karunarathna SC, Suwannarach N. Perceived Intensification in Harmful Algal Blooms Is a Wave of Cumulative Threat to the Aquatic Ecosystems. Biology. 2022; 11(6):852. https://doi.org/10.3390/biology11060852

Chicago/Turabian Style

Kazmi, Syed Shabi Ul Hassan, Neelamanie Yapa, Samantha C. Karunarathna, and Nakarin Suwannarach. 2022. "Perceived Intensification in Harmful Algal Blooms Is a Wave of Cumulative Threat to the Aquatic Ecosystems" Biology 11, no. 6: 852. https://doi.org/10.3390/biology11060852

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