Harmful Algal Blooms in Eutrophic Marine Environments: Causes, Monitoring, and Treatment

Abstract

Marine eutrophication, primarily driven by nutrient over input from agricultural runoff, wastewater discharge, and atmospheric deposition, leads to harmful algal blooms (HABs) that pose a severe threat to marine ecosystems. This review explores the causes, monitoring methods, and control strategies for eutrophication in marine environments. Monitoring techniques include remote sensing, automated in situ sensors, modeling, forecasting, and metagenomics. Remote sensing provides large-scale temporal and spatial data, while automated sensors offer real-time, high-resolution monitoring. Modeling and forecasting use historical data and environmental variables to predict blooms, and metagenomics provides insights into microbial community dynamics. Control treatments encompass physical, chemical, and biological treatments, as well as advanced technologies like nanotechnology, electrocoagulation, and ultrasonic treatment. Physical treatments, such as aeration and mixing, are effective but costly and energy-intensive. Chemical treatments, including phosphorus precipitation, quickly reduce nutrient levels but may have ecological side effects. Biological treatments, like biomanipulation and bioaugmentation, are sustainable but require careful management of ecological interactions. Advanced technologies offer innovative solutions with varying costs and sustainability profiles. Comparing these methods highlights the trade-offs between efficacy, cost, and environmental impact, emphasizing the need for integrated approaches tailored to specific conditions. This review underscores the importance of combining monitoring and control strategies to mitigate the adverse effects of eutrophication on marine ecosystems.

1. Introduction

Marine eutrophication refers to the excessive input of nutrients, such as nitrogen and phosphorus, into marine ecosystems [1]. These nutrients primarily come from sources like agricultural runoff, urban sewage, industrial discharge, and river inflow [2]. This excess nutrient load stimulates the overgrowth of phytoplankton, leading to HABs. The resulting excessive growth of algae can deplete oxygen levels in the water, cause hypoxia, harm ecosystem health, and produce toxins posing threats to human and animal health [3]. The dominant algae species of harmful algae outbreaks in sea areas are listed in Table 1.

Marine eutrophication poses significant threats to biodiversity, fisheries, aquaculture, and human health. Over the past two decades, significant progress has been made in understanding marine eutrophication (Figure 1). Scientists have focused on elucidating the mechanisms, influencing factors, and ecological consequences of eutrophication [4]. Additionally, researchers have developed new monitoring techniques and management strategies to address this challenge [5].

Table 1. The dominant algae species of harmful algae outbreaks in sea areas.

Sea Areas	Dominant Algae Species	Refs.
Gulf of Mexico	Karenia brevis Dinophysis ovum	[6,7,8]
North Atlantic Ocean	Alexandrium spp. Pseudo-nitzschia spp.	[9,10,11]
Pacific Ocean	Karenia spp. Alexandrium spp. Dinophysis spp.	[12,13,14]
North Sea and Baltic Sea	Alexandrium spp. Dinophysis spp.	[15]
Indian Ocean	Cochlodinium spp. Noctiluca scintillans	[16,17,18]
Arctic Ocean	Karlodinium spp. Heterosigma spp.	[19]
Mediterranean Sea	Alexandrium spp. Karenia spp.	[20]
Caribbean Sea	Karenia brevis	[21]
South China Sea	Alexandrium spp. Cochlodinium spp.	[22,23]
Black Sea	Alexandrium spp. Dinophysis spp.	[24,25]
Bay of Bengal	Dinoflagellate spp. Noctiluca scintillans Karenia brevis	[18,26]
East China Sea	Alexandrium spp. Prorocentrum spp.	[23,27]
East Siberian Sea	Karlodinium spp. Heterosigma spp.	[28,29,30]
Barents Sea	Alexandrium spp. Dinophysis spp.	[31,32,33]
Southern Ocean	Phaeocystis spp. Dinophysis spp.	[34,35]
South Atlantic Ocean	Alexandrium spp. Karenia spp.	[36,37]
Norwegian Sea	Alexandrium spp. Dinophysis spp.	[32,38]
Adriatic Sea	Alexandrium spp. Pseudo-nitzschia spp.	[39,40]
Tyrrhenian Sea	Alexandrium spp. Dinophysis spp.	[41]
Monterey Bay	Pseudo-nitzschia australis	[42]

Table 1. The dominant algae species of harmful algae outbreaks in sea areas.

Sea Areas	Dominant Algae Species	Refs.
Gulf of Mexico	Karenia brevis Dinophysis ovum	[6,7,8]
North Atlantic Ocean	Alexandrium spp. Pseudo-nitzschia spp.	[9,10,11]
Pacific Ocean	Karenia spp. Alexandrium spp. Dinophysis spp.	[12,13,14]
North Sea and Baltic Sea	Alexandrium spp. Dinophysis spp.	[15]
Indian Ocean	Cochlodinium spp. Noctiluca scintillans	[16,17,18]
Arctic Ocean	Karlodinium spp. Heterosigma spp.	[19]
Mediterranean Sea	Alexandrium spp. Karenia spp.	[20]
Caribbean Sea	Karenia brevis	[21]
South China Sea	Alexandrium spp. Cochlodinium spp.	[22,23]
Black Sea	Alexandrium spp. Dinophysis spp.	[24,25]
Bay of Bengal	Dinoflagellate spp. Noctiluca scintillans Karenia brevis	[18,26]
East China Sea	Alexandrium spp. Prorocentrum spp.	[23,27]
East Siberian Sea	Karlodinium spp. Heterosigma spp.	[28,29,30]
Barents Sea	Alexandrium spp. Dinophysis spp.	[31,32,33]
Southern Ocean	Phaeocystis spp. Dinophysis spp.	[34,35]
South Atlantic Ocean	Alexandrium spp. Karenia spp.	[36,37]
Norwegian Sea	Alexandrium spp. Dinophysis spp.	[32,38]
Adriatic Sea	Alexandrium spp. Pseudo-nitzschia spp.	[39,40]
Tyrrhenian Sea	Alexandrium spp. Dinophysis spp.	[41]
Monterey Bay	Pseudo-nitzschia australis	[42]

Eutrophication and water blooms, while intricately connected, are distinct phenomena within aquatic ecosystems [43]. Eutrophication is primarily characterized by nutrient enrichment and its subsequent effects on water quality and oxygen levels. In contrast, water blooms are defined by the visible proliferation of algal biomass, often accompanied by toxin production and significant fluctuations in oxygen levels [44]. The criteria for eutrophication and water bloom are summarized in

Table 2. The criteria for eutrophication and HABs.

Criteria	Eutrophication	HABs
Definition	Nutrient enrichment in water bodies, leading to excessive algal growth	Rapid and excessive growth of algae
Key Nutrients	Nitrogen, Phosphorus	Nitrogen, Phosphorus
Chlorophyll-a Concentration	>20 µg/L	>30 µg/L
Cell Density	N/A	>100,000 cells/mL [45]
Dissolved Oxygen	Hypoxia (DO < 2 mg/L) in bottom waters [46]	Significant diurnal fluctuation (supersaturation during day, hypoxia at night) [47]
Odor	N/A	Unpleasant odors due to volatile organic compounds (VOCs) [48]
Toxin Production	N/A	Presence of harmful algal toxins [49]

.

Table 3. Characteristics and environmental conditions of major HAB types.

HAB Type	Dominant Species	Characteristics	Conditions for Dominance	Refs.
Cyanobacterial Blooms (Blue-Green Algae)	Microcystis, Anabaena, Nodularia	Produces microcystins, nodularins; toxic to humans and animals; common in freshwater and brackish environments	High nutrient levels (especially phosphorus); warm, stagnant waters; low water flow	[51]
Dinoflagellate Blooms	Alexandrium, Karenia, Gymnodinium	Known for “red tides”; produces neurotoxins (e.g., saxitoxins, brevetoxins) causing shellfish poisoning	Nutrient-rich environments; presence of specific minerals (e.g., silica for diatoms); stratified water column	[52,53]
Diatom Blooms	Pseudo-nitzschia, Chaetoceros	Produces domoic acid leading to amnesic shellfish poisoning; common in colder waters	Presence of silica; low predation; cold, nutrient-rich waters	[54,55]
Haptophyte Blooms	Phaeocystis, Chrysochromulina	Forms gelatinous masses disrupting food webs; produces dimethyl sulfide influencing climate	High nutrient availability; low predation; stable, stratified waters	[56,57]
Raphidophyte Blooms	Heterosigma, Chattonella	Produces reactive oxygen species; associated with fish kills	High nutrient and iron levels; warm temperatures; low grazing pressure	[58,59]
Green Algae Blooms	Ulva, Enteromorpha	Forms thick surface mats leading to hypoxia; disrupts marine habitats	High light availability; shallow, nutrient-rich waters; limited grazing	[60,61]

provides an overview of the primary types of HABs, highlighting the dominant species, key characteristics, and the environmental conditions that favor their occurrence. Each type of bloom is associated with specific species of phytoplankton, such as cyanobacteria, dinoflagellates, and diatoms, among others [50]. These species exhibit distinct behaviors, from producing toxins to forming massive surface mats, which can have severe ecological and economic impacts. The dominance of these blooms is typically driven by environmental conditions such as nutrient enrichment, water temperature, light availability, and water column stratification. Understanding these factors is critical for predicting and managing the occurrence of HABs in marine ecosystems.

In this study, we aim to provide insights into the dominant algae species that are responsible in eutrophicated marine ecosystems; summarize monitoring techniques, management strategies, and treatment technologies from the past two decades; highlight areas where further research is needed to improve our understanding of eutrophication processes; and develop more effective treatment technologies.

2. Hazards of Marine Harmful Algal Blooms

Marine HABs pose significant hazards to marine ecosystems, affecting a wide range of biological, chemical, and physical aspects of the environment. The primary hazards include oxygen depletion, toxin production, habitat degradation, and biodiversity loss.

2.1. Oxygen Depletion

Oxygen depletion, also known as hypoxia (DO < 2 mg/L), is a significant environmental hazard associated with marine HABs [62,63]. Excessive nutrients, particularly nitrogen and phosphorus, enter marine environments from agricultural runoff, wastewater discharge, and atmospheric deposition. These nutrients fuel the rapid growth of phytoplankton, leading to algal blooms [64,65]. Certain conditions, such as warm water temperatures and ample sunlight, can further promote the rapid proliferation of algae [66,67]. During a bloom, the algal biomass increases substantially. While alive, these algae contribute to O₂ production through photosynthesis during the day and consume O₂ and produce CO₂ through respiration during the night. DO levels exhibit diurnal fluctuations, with higher levels during the day (due to photosynthesis) and lower levels at night (due to respiration and decomposition) [62,68,69]. Algal cells eventually die, and dead algal cells sink to the bottom layers of the water column. Bacteria and other microorganisms decompose the dead algal matter.

Table 4. Microbial communities involved in the decomposition of algal biomass in marine environments: species, decomposition methods, and resulting products.

Type of Microorganism	Species Name	Method of Decomposing Algal Biomass	Products after Decomposition	Refs.
Bacteria	Pseudomonas putida	Oxidizes organic matter in the presence of oxygen	CO2, H2O	[71,72]
Bacteria	Bacillus subtilis	Aerobic decomposition of proteins and polysaccharides	CO2, H2O	[73,74]
Bacteria	Desulfovibrio vulgaris	Anaerobic sulfate reduction, using sulfate as an electron acceptor	H2S, CO2	[75]
Archaea	Methanosarcina barkeri	Anaerobic decomposition of organic acids and alcohols	CH₄, CO2	[76]
Fungi	Aspergillus terreus	Breaks down complex polysaccharides (cellulose, hemicellulose)	Simpler organic molecules, CO2	[77,78]
Bacteria	Clostridium butyricum	Fermentation of organic matter under anaerobic conditions	Butyric acid, H2, CO2	[79]
Fungi	Penicillium chrysogenum	Decomposes polysaccharides and proteins, especially in low-oxygen environments	Organic acids, CO2	[80]

provides an overview of specific microbial species involved in the breakdown of algal biomass in marine ecosystems. These species belong to various groups, including bacteria, archaea, and fungi, each contributing to the decomposition through different metabolic pathways. The products of these processes range from carbon dioxide and water in aerobic conditions to hydrogen sulfide and methane in anaerobic environments. These microorganisms play a crucial role in nutrient cycling and influence oxygen levels, affecting the health and stability of marine ecosystems, particularly during HABs. The consumption of large amounts of DO from the surrounding water leads to a significant reduction in the DO levels in the water. As oxygen levels drop, hypoxic (DO < 2 mg/L) or anoxic (DO < 0.5 mg/L) conditions develop, particularly in the benthic (bottom) zones of the water body [62,70].

Environmental factors significantly impact oxygen consumption rates in microbial decomposition processes. Higher temperatures typically accelerate microbial metabolic rates, leading to increased decomposition and oxygen consumption, though this can also result in faster oxygen depletion, especially in poorly mixed water bodies [49]. Conversely, colder temperatures slow microbial activity, reducing both decomposition and oxygen use. Nutrient availability plays a dual role: nutrient-rich environments promote rapid microbial growth and higher oxygen consumption, while excessive nutrients can lead to algal blooms, increasing organic matter and exacerbating oxygen depletion [81]. Oxygen levels are critical; high oxygen supports efficient aerobic decomposition, while low oxygen shifts processes to less efficient anaerobic pathways, resulting in the accumulation of partially decomposed matter and production of compounds like hydrogen sulfide and methane. The composition of algal biomass also affects decomposition rates; algae with tough cell walls or harmful toxins may decompose more slowly, influencing microbial activity and oxygen consumption [82].

The impact of O₂ depletion on marine life includes the following: (1) Stress and mortality: marine organisms, especially those that are less mobile or sessile (e.g., benthic invertebrates), can experience stress or mortality due to low oxygen levels [83,84,85]. (2) Behavioral changes: fish and other mobile organisms may exhibit behavioral changes, such as moving to shallower waters or areas with higher oxygen levels to avoid hypoxia, which in turn alters food webs [83,86]. Hypoxic conditions can alter predator-prey dynamics and food web structures by affecting the abundance and distribution of various species [87,88,89].

2.2. Algal Toxin

Many marine algae can produce toxins, as shown in Table 5. The production of algal toxins during HABs poses significant hazards to marine ecosystems [90]. These hazards include direct and indirect effects on marine organisms [15,91], alterations in ecosystem dynamics [92], and long-term ecological impacts [93,94].

Those algal toxins can cause large-scale mortality of marine organisms. These toxins interfere with nervous system function, leading to paralysis and death [95]. Toxins can be transferred up the food web [96], affecting a wide range of marine organisms [95,97]. Predatory species, including marine mammals, birds, and larger fish, can be poisoned by consuming contaminated prey [96,98,99].

Table 5. The toxins produced during marine harmful algal blooms.

Toxins	Producers	Type	Refs.
Paralytic Shellfish Toxins	Alexandrium spp. Gymnodinium catenatum Pyrodinium bahamense	Neurotoxins	[100]
Amnesic Shellfish Toxins	Pseudo-nitzschia spp.	Neurotoxins	[101,102,103,104]
Neurotoxic Shellfish Toxins	Karenia brevis	Neurotoxins	[105,106,107]
Ciguatoxins	Gambierdiscus toxicus	Neurotoxins	[108,109]
Kalkitoxin	Lyngbya majuscula	Neurotoxins	[110,111]
Prymnesins	Prymnesium parvum	Hemolytic toxins and neurotoxins	[112]
Caulerpenyne	Caulerpa taxifolia	Cytotoxins	[113,114,115,116]
Aplysiatoxins	Lyngbya spp.	Cytotoxins	[112]
Pectenotoxins	Dinophysis spp.	Hepatotoxins and cytotoxins	[117,118]
Diarrhetic Shellfish Toxins	Dinophysis spp. Prorocentrum lima	Gastrointestinal toxins and cytotoxins	[107,119,120]
Azaspiracids	Azadinium spp. Mytilus edulis	Gastrointestinal toxins and cytotoxins	[121,122,123]
Yessotoxins	Protoceratium reticulatum Lingulodinium polyedrum Gonyaulax spinifera	Cardiovascular toxins	[124,125,126]
Azaspiracids	Azadinium spp. Mytilus edulis	Gastrointestinal toxins and cytotoxins	[121,122,123]
Cylindrospermopsin	Cylindrospermopsis raciborskii	Hepatotoxins and nephrotoxins	[127,128]
Microcystins	Microcystis spp., Anabaena spp., Planktothrix spp.	Hepatotoxins	[129,130,131]
Pectenotoxins	Dinophysis spp.	Hepatotoxins and cytotoxins	[132,133]

Table 5. The toxins produced during marine harmful algal blooms.

Toxins	Producers	Type	Refs.
Paralytic Shellfish Toxins	Alexandrium spp. Gymnodinium catenatum Pyrodinium bahamense	Neurotoxins	[100]
Amnesic Shellfish Toxins	Pseudo-nitzschia spp.	Neurotoxins	[101,102,103,104]
Neurotoxic Shellfish Toxins	Karenia brevis	Neurotoxins	[105,106,107]
Ciguatoxins	Gambierdiscus toxicus	Neurotoxins	[108,109]
Kalkitoxin	Lyngbya majuscula	Neurotoxins	[110,111]
Prymnesins	Prymnesium parvum	Hemolytic toxins and neurotoxins	[112]
Caulerpenyne	Caulerpa taxifolia	Cytotoxins	[113,114,115,116]
Aplysiatoxins	Lyngbya spp.	Cytotoxins	[112]
Pectenotoxins	Dinophysis spp.	Hepatotoxins and cytotoxins	[117,118]
Diarrhetic Shellfish Toxins	Dinophysis spp. Prorocentrum lima	Gastrointestinal toxins and cytotoxins	[107,119,120]
Azaspiracids	Azadinium spp. Mytilus edulis	Gastrointestinal toxins and cytotoxins	[121,122,123]
Yessotoxins	Protoceratium reticulatum Lingulodinium polyedrum Gonyaulax spinifera	Cardiovascular toxins	[124,125,126]
Azaspiracids	Azadinium spp. Mytilus edulis	Gastrointestinal toxins and cytotoxins	[121,122,123]
Cylindrospermopsin	Cylindrospermopsis raciborskii	Hepatotoxins and nephrotoxins	[127,128]
Microcystins	Microcystis spp., Anabaena spp., Planktothrix spp.	Hepatotoxins	[129,130,131]
Pectenotoxins	Dinophysis spp.	Hepatotoxins and cytotoxins	[132,133]

The environmental standards for algal toxins in water resources vary across countries and regions, reflecting differences in local conditions, risk assessments, and public health policies [134].

Table 6. Environmental standards for various algal toxins in water resources across major countries.

Country/Region	Algal Toxin	Standard (µg/L)	Water Type	Remarks	Ref.
United States	Microcystin-LR	1.6	Drinking Water	EPA’s Health Advisory level for infants and young children.	[135]
United States	Microcystin-LR	8	Drinking Water	EPA’s Health Advisory level for adults.	[136]
United States	Cylindrospermopsin	0.7	Drinking Water	EPA’s Health Advisory level for infants and young children.	[137]
United States	Cylindrospermopsin	3	Drinking Water	EPA’s Health Advisory level for adults.	[138]
United States	Anatoxin-a	20	Recreational Water	No federal standard for drinking water.	[139]
European Union	Microcystin-LR	1	Drinking Water	Set by the European Commission for safe drinking water.	[140]
Australia	Microcystin-LR	1.3	Drinking Water	Based on WHO guidelines for drinking water safety.	[141]
Canada	Microcystin-LR	1.5	Drinking Water	Guidelines set by Health Canada.	[142]
Brazil	Microcystin-LR	1	Drinking Water	Aligned with WHO recommendations.	[143]
New Zealand	Microcystin-LR	1	Drinking Water	Based on WHO guidelines for safe drinking water.	[144]
China	Microcystin-LR	1	Drinking Water	National standard for safe drinking water.	[145]
Japan	Microcystin-LR	1	Drinking Water	National guidelines for safe drinking water.	[146]
South Africa	Microcystin-LR	1	Drinking Water	Set by the Department of Water Affairs and Forestry.	[147]
WHO	Microcystin-LR	1	Drinking Water	International guideline value for safe drinking water.	[148]

is a summary of the key standards from major countries. The standards for algal toxins in water resources, particularly Microcystin-LR, are generally consistent across major countries, with a common guideline of 1 µg/L for drinking water. These standards reflect the need to protect public health from the potential harmful effects of algal toxins, which are prevalent in many freshwater bodies worldwide. Some countries also set different levels for recreational waters, recognizing the varying risks based on exposure type. The inclusion of algal toxin levels in environmental standards is crucial for the standardization and safety of water resources globally.

2.3. Habitat Degradation

HABs pose significant hazards to marine habitats, affecting their structure, function, and the organisms that depend on them [49,149]. HABs can lead to habitat degradation in marine ecosystems through several mechanisms. In addition to oxygen depletion and the release of toxins, the mechanisms of HABs that degrade marine habitats include the following: (1) Light limitation: Dense algal blooms can reduce light penetration in the water column due to high concentrations of phytoplankton and particulate matter. This reduction in light availability affects photosynthetic organisms, such as seagrasses and benthic algae [150,151]. (2) Physical smothering: Dense algal mats can form on the surface or bottom of water bodies during blooms. These mats can physically smother benthic habitats, including coral reefs, seagrass beds, and rocky substrates [90,152,153] (

Table 7. Contribution of pathways to habitat degradation by HABs.

Pathway	Contribution	Details	Refs.
Oxygen Depletion	High	Major driver of habitat degradation; leads to hypoxia or anoxia, causing widespread die-offs and loss of marine organisms.	[154,155]
Toxicity	High	Severe impact through poisoning of marine life and humans; disrupts health of various species and ecosystem balance.	[156]
Disruption of Food Webs	Moderate to High	Alters food web dynamics by outcompeting primary producers and reducing food availability for herbivores.	[157]
Light Reduction	Moderate	Reduces light penetration, affecting photosynthesis of submerged vegetation and causing habitat decline.	[149]
Physical Damage	Moderate	Causes direct harm to benthic habitats through smothering by mucilaginous or gelatinous substances.	[158]
Nutrient Imbalance	Moderate	Leads to persistent algal blooms by disrupting nutrient levels, exacerbating other degradation pathways.	[159,160]
Altered Community Structure	Variable	Shifts species composition, affecting biodiversity and ecosystem resilience; impact depends on specific species changes.	[161]

).

2.4. The Impact of Water Blooms on the Carbon Cycle and Carbon Accumulation Processes

Water blooms, particularly those caused by harmful algal species, play a significant role in the carbon cycle and carbon accumulation in aquatic ecosystems. During the rapid proliferation of phytoplankton, large quantities of carbon dioxide (CO₂) are absorbed from the atmosphere through photosynthesis, leading to the formation of organic carbon within algal biomass [162]. This process temporarily sequesters atmospheric carbon in aquatic systems, contributing to the short-term storage of carbon. However, the efficiency of this sequestration is influenced by the type of algae, the duration of the bloom, and the subsequent fate of the biomass [163].

As shown in Figure 2, once the bloom reaches its peak, the accumulation of organic matter can lead to complex feedback mechanisms in the carbon cycle. The decomposition of dead algal cells by microbial activity results in the release of CO₂ and methane (CH₄), potent greenhouse gasses, back into the atmosphere or water column, particularly in hypoxic or anoxic conditions [164]. This decomposition process not only negates some of the initial carbon sequestration but also exacerbates oxygen depletion in the water, contributing to further degradation of the ecosystem. Additionally, the sinking of algal biomass to the ocean floor can lead to long-term carbon burial, depending on the environmental conditions and the rate of sedimentation.

Moreover, the occurrence of water blooms can alter the overall carbon dynamics by shifting the balance between carbon fixation and respiration [165]. In some cases, the production of extracellular organic carbon compounds during bloom events can enhance the carbon flux to the deep ocean, potentially contributing to long-term carbon sequestration. However, the extent of this contribution varies with the bloom’s intensity, duration, and the specific characteristics of the algal species involved. Ultimately, the impact of water blooms on the carbon cycle is multifaceted, with both positive and negative effects on carbon accumulation processes during and after biomass formation [166].

3. Factors Leading to Marine Eutrophication

Marine eutrophication is driven by a range of natural and anthropogenic factors that lead to excessive nutrient enrichment in marine environments. Here are the primary factors contributing to marine eutrophication, as shown in Figure 3.

Additionally, the requirements of HABs for various elements such as nitrogen (N), phosphorus (P), and silicon (Si) vary depending on the specific algal species involved [167]. The ratio of these elements is crucial in determining which species will dominate in a given environment.

Table 8. The elemental requirements for various HAB species.

Algal Group/Species	Key Elemental Requirements	Optimal N:P:Si Ratio	Comments	Refs.
Pseudonitzschia spp. (Diatom)	High Si, Moderate N, Moderate P	15:01:16	Produces domoic acid, a neurotoxin causing amnesic shellfish poisoning (ASP).	[168]
Skeletonema costatum (Diatom)	High Si, Moderate N, Moderate P	14:01:16	Common in temperate regions; requires silicon for robust growth.	[169,170]
Alexandrium spp. (Dinoflagellate)	High N, Moderate P, Low Si	16:01:00	Thrives in nitrogen-rich environments; does not require silicon.	[171,172]
Karenia brevis (Dinoflagellate)	High N, Moderate P, Low Si	20:01:00	Produces brevetoxins, linked to “red tides” in the Gulf of Mexico.	[173]
Dinophysis spp. (Dinoflagellate)	High N, Moderate P, Low Si	18:01:00	Produces okadaic acid, causing diarrhetic shellfish poisoning (DSP).	[174]
Noctiluca scintillans (Dinoflagellate)	High N, Moderate P, Low Si	10:01:00	Non-toxic but can cause hypoxia; benefits from high N inputs.	[175]
Cylindrospermopsis raciborskii (Cyanobacterium)	High P, Moderate N, Low Si	05:01:00	Thrives in phosphorus-rich environments; produces cylindrospermopsin toxin.	[176]
Microcystis spp. (Cyanobacterium)	High N, High P, Low Si	20:01:00	Common in eutrophic freshwater; produces microcystins, toxic to humans and animals.	[177,178]
Heterosigma akashiwo (Raphidophyte)	High N, Moderate P, Low Si	25:01:00	Known for causing fish kills; thrives in high N, low Si environments.	[179]

is a summary of the elemental requirements for various HAB species, including the optimal elemental ratios between nitrogen, phosphorus, and silicon.

Nutrient contributions to HABs across marine ecosystems are shown in

Table 9. Nutrient contributions to HABs across various marine ecosystems.

Nutrient	Role in HABs	Ecosystem	Processes and Conditions	Dominant Algal Species	Refs.
N	Major driver of algal growth; often limiting nutrient	Coastal Waters	High inputs from agriculture, urban runoff	Dinoflagellates, Cyanobacteria	[152,159,180]
		Open Ocean	Upwelling, atmospheric deposition	Diatoms, Dinoflagellates
		Polar Regions	Seasonal nutrient release from ice melt	Diatoms, Phaeocystis
P	Key driver in phosphorus-limited systems	Estuaries and Coastal Lagoons	Runoff from agriculture, sewage discharge	Cyanobacteria, Dinoflagellates	[181,182,183]
		Freshwater-Influenced Marine Systems	High phosphorus inputs	Cyanobacteria, Diatoms
Si	Essential for diatom growth	Upwelling Zones	Nutrient-rich upwelled waters	Diatoms	[184,185,186]
		River-Influenced Systems	Abundant silicon from riverine inputs	Diatoms

. Nitrogen is often the limiting nutrient in marine environments, meaning that an increase in nitrogen levels can significantly boost algal growth. This is particularly true in coastal areas, where nitrogen inputs from agricultural runoff, urban wastewater, and atmospheric deposition are common. In these regions, HABs are frequently observed, especially near estuaries and river mouths. In contrast, open ocean ecosystems, which are typically nutrient poor, may experience HABs when nitrogen is introduced through processes such as upwelling or atmospheric deposition. Polar regions also exhibit seasonal blooms driven by nitrogen released from melting ice.

Phosphorus, another critical nutrient, plays a significant role in freshwater and some brackish environments. While it is less commonly a limiting factor in marine systems compared to nitrogen, phosphorus can still exacerbate HABs, particularly in coastal lagoons and estuaries where phosphorus inputs from agriculture and sewage are high. Freshwater-influenced marine systems are especially vulnerable to phosphorus-driven blooms when nitrogen levels are already elevated.

Silicon is essential for diatoms, a group of algae that require silica for their cell walls. In ecosystems where diatoms are dominant, such as coastal upwelling zones and river-influenced systems, silicon availability regulates diatom growth and influences the overall phytoplankton community structure. However, when silicon becomes depleted, other harmful algal species that do not require silicon, such as dinoflagellates or cyanobacteria, may dominate, leading to HABs.

The elemental requirements and ratios of N, P, and Si play a critical role in determining the composition and dominance of different algal species in HABs. Diatoms require a balanced supply of N, P, and Si, while dinoflagellates and cyanobacteria can thrive in environments with high N and P but low Si. Understanding these ratios helps in predicting which algal species are likely to bloom under different environmental conditions.

The formation of HABs is therefore a complex process that varies widely across different marine ecosystems. Coastal and estuarine ecosystems are particularly susceptible due to higher nutrient inputs from human activities, while the open ocean, polar regions, and tropical ecosystems experience HABs driven by natural processes such as upwelling, ice melt, and nutrient stratification. Understanding these variations is crucial for effectively predicting, managing, and mitigating the impacts of HABs in diverse marine environments.

3.1. Sources of Nutrient Inputs

3.1.1. Agricultural Runoff

The sources of nutrient inputs into marine environments are diverse and multifaceted. Agricultural runoff is a primary contributor, introducing substantial amounts of nitrogen and phosphorus derived from fertilizers and animal manure [64,180,187]. These nutrients are mobilized during rainfall events and transported via surface runoff into streams, rivers, and ultimately the coastal waters [154,188].

Global consumption of nitrogen and phosphorus fertilizers has generally been on the rise over the past decade [188,189,190,191,192,193] (Figure 4). This increase is largely attributed to the growing agricultural demands from developing countries in Asia, Latin America, and Africa, where the need to boost agricultural productivity is paramount [194]. According to the Food and Agriculture Organization (FAO), global nitrogen fertilizer consumption increased by approximately 1–2% annually, while phosphorus consumption saw a slightly slower growth rate [195,196,197]. The use of synthetic fertilizers in agriculture adds substantial amounts of nitrogen and phosphorus to the soil. Excess nutrients not taken up by crops are susceptible to being washed away by rainfall or irrigation. This runoff can travel through drainage systems, rivers, and streams, eventually reaching coastal marine environments.

The amount and type of nutrient runoff from agricultural fields are influenced by a combination of crop type, agricultural practices, and environmental factors. Cereal crops, with high nitrogen and phosphorus requirements, contribute significantly to nutrient runoff, particularly when fertilizers are over-applied or poorly timed. Leguminous crops, while reducing nitrogen runoff, still pose a risk for phosphorus loss. Additionally, practices such as excessive irrigation, conventional tillage, and improper timing of fertilizer applications exacerbate nutrient runoff, especially in regions with high rainfall and certain soil types (

Table 10. Influence of agricultural practices on nutrient runoff.

Factor	Description	Impact on Nutrient Runoff	Refs.
Over-application of Fertilizers	Applying fertilizers in amounts exceeding crop needs.	High risk of nutrient runoff, especially during heavy rain.	[198]
Timing of Fertilizer Application	Fertilizer applied during non-growing seasons or prior to heavy rainfall.	Increased nutrient loss to runoff.	[199]
Irrigation Practices	Excessive or inefficient irrigation methods.	Increases leaching and runoff, particularly of N.	[200]
Tillage Practices	Conventional tillage increases soil disturbance and erosion.	Higher erosion and surface runoff leading to nutrient loss.	[201,202]
Crop Rotation and Cover Cropping	Rotating crops with different nutrient needs and using cover crops to absorb residual nutrients.	Reduces nutrient buildup and runoff.	[203]

).

Developing countries face a multitude of challenges in managing fertilizer use, encompassing economic constraints, technical and knowledge gaps, infrastructural difficulties, environmental vulnerabilities, weak regulatory frameworks, and social and cultural barriers. High fertilizer costs and dependence on subsidies make it difficult for smallholder farmers to apply fertilizers efficiently, while limited access to soil testing and agricultural extension services leads to imbalanced fertilization. Poor infrastructure, such as inadequate transportation and storage, further complicates fertilizer distribution. Environmental factors, including vulnerability to extreme weather and soil degradation, exacerbate these issues. Additionally, weak regulations allow low-quality fertilizers to flood the market, and traditional practices often resist modern agricultural methods. Addressing these challenges requires a comprehensive approach that improves education, infrastructure, and regulation and promotes sustainable agricultural practices [204].

Livestock are also a source of nitrogen and phosphorus from agricultural runoff [205]. As shown in Figure 5, according to FAO statistics [206,207,208,209,210,211], the increase in global livestock production and the outbreak of marine eutrophication are highly positively correlated (Pearson correlation coefficient greater than 0.95), indicating that there is a certain correlation between livestock farming and marine eutrophication. Intensive and industrialized farming practices, such as concentrated animal feeding operations (CAFOs), have increased significantly, according to the FAO [212,213,214,215]. This intensification generates large amounts of manure, a major source of nitrogen and phosphorus, which can enter water bodies through surface runoff and leaching [205]. Heavy rainfall, improper manure storage, and over-application of manure exacerbate this process, ultimately transporting these nutrients to rivers and coastal waters and contributing to eutrophication [216].

The transition of agriculture to organic farming methods, along with the use of innovative nitrogen and phosphate fertilizers and mixed organo-mineral fertilizers, plays a crucial role in addressing the environmental challenges posed by conventional agricultural practices [217].

Organic farming emphasizes the use of natural inputs and ecological processes, reducing the dependence on synthetic nitrogen (N) and phosphorus (P) fertilizers, which are primary contributors to nutrient runoff into aquatic systems. By employing practices such as crop rotation, cover cropping, and the application of organic manure, organic farming enhances soil structure and increases its capacity to retain nutrients, thereby minimizing the leaching and runoff of N and P into marine environments. The reduced nutrient loading from organic farming helps to mitigate the occurrence of HABs and hypoxic conditions, which are often linked to excessive nutrient inputs in coastal waters [218].

Innovative fertilizers, including slow-release, controlled-release, and enhanced-efficiency fertilizers, are designed to synchronize nutrient release with crop demand, thus reducing the excess availability of N and P that often leads to runoff and leaching (

Table 11. Innovative fertilizer technologies for reducing eutrophication.

Fertilizer Technology	Nutrients Provided	Mechanism	Suitable Crops	Refs.
Slow-Release Fertilizers (SRFs)	Nitrogen, Phosphorus, Potassium	Gradual nutrient release aligned with crop uptake	Cereals, horticultural crops, turfgrass	[221,222]
Controlled-Release Fertilizers (CRFs)	Nitrogen, Phosphorus, Potassium	Coating controls nutrient release over time	Vegetables, fruits, ornamental plants	[223,224]
Nitrification Inhibitors	Nitrogen	Inhibits nitrification, reducing nitrate leaching	Maize, wheat, rice	[225,226]
Urease Inhibitors	Nitrogen (Urea-based)	Prevents rapid urea conversion, reducing ammonia loss	Rice, cereals, pasture	[227,228]
Enhanced Efficiency Fertilizers (EEFs)	Nitrogen, Phosphorus	Combines slow and controlled release with inhibitors	Various crops including cereals, fruits, vegetables	[229,230]
Polymer-Coated Fertilizers	Nitrogen, Potassium	Encapsulated nutrients in a polymer for controlled release	High-value crops like fruits, vegetables, ornamentals	[231,232]
Biochar-Enhanced Fertilizers	Nitrogen, Phosphorus, Potassium, micronutrients	Uses biochar to retain nutrients and reduce leaching	Cereals, legumes, vegetables	[233]
Struvite Fertilizers	Phosphorus, Nitrogen, Magnesium	Mineral compound with slow nutrient release	Horticultural crops, cereals	[234]

) [219]. These fertilizers typically incorporate inhibitors that slow down the conversion processes (e.g., nitrification inhibitors) or feature coatings that control nutrient release rates. By optimizing nutrient availability, these fertilizers reduce the risk of N and P entering water bodies in concentrations that could contribute to eutrophication. The effectiveness of these fertilizers in reducing nutrient losses has been demonstrated in various studies, showing potential in mitigating the anthropogenic impacts on marine environments [220].

Mixed organo-mineral fertilizers combine the advantages of organic materials with mineral nutrients, improving nutrient use efficiency and reducing the environmental footprint of fertilization (

Table 12. Mixed organo-mineral fertilizers for reducing eutrophication.

Fertilizer Name	Nutrients Provided	Principle	Suitable Crops	Refs.
Humic Acid-Enriched Fertilizers	N, P, K, Micronutrients	Enhances nutrient absorption and soil structure with humic acid.	Cereals, vegetables, fruits, legumes	[235]
Compost-Based Mineral Fertilizers	N, P, K, Organic Matter	Integrates compost with minerals to improve soil organic content and nutrient retention.	Vegetables, fruits, horticultural crops	[236,237]
Biochar-Integrated Fertilizers	N, P, K, Carbon	Uses biochar to enhance nutrient retention and reduce leaching.	Row crops, perennials, reclamation projects	[238,239]
Seaweed Extract-Based Fertilizers	N, P, K, Trace Elements	Combines seaweed extracts for growth promotion with minerals for nutrient availability.	Vegetables, fruits, ornamental plants	[240]
Poultry Manure-Enriched Fertilizers	N, P, K, Calcium	Combines poultry manure with minerals for balanced nutrient supply.	Grain crops, pasture, vegetables	[241]

). The organic components enhance soil organic matter, which supports soil microbial activity and the slow release of nutrients, while the mineral components ensure that crops receive adequate N and P. This combination reduces the immediate availability of nutrients that could otherwise be lost to runoff. Additionally, the presence of organic matter improves soil water retention and reduces erosion, further decreasing the potential for nutrient runoff into marine systems.

3.1.2. Aquaculture

Aquaculture, particularly marine aquaculture, can significantly contribute to nutrient inputs in marine environments [150,242]. This process involves the farming of fish, shellfish, and other aquatic organisms in controlled marine environments. Aquaculture significantly contributes to nutrient inputs in marine environments through several mechanisms [243]. Uneaten feed and excreta from farmed fish and shellfish release substantial amounts of nitrogen and phosphorus, which accumulate in surrounding waters and sediments, causing localized eutrophication [22]. Additionally, the use of fertilizers in some aquaculture practices, such as seaweed farming, introduces further nutrients into the water [216,242,244]. Effluents from aquaculture facilities, including water used for cleaning tanks and ponds, often contain high nutrient levels.

The distribution of major global aquaculture sites and eutrophication hotspots over the last decade is shown in Figure 6 [4,15,16,64,102,188,189,245,246,247,248,249,250,251]. It can be found that aquaculture sites and eutrophication hotspots have a high degree of overlap, so it can be considered that aquaculture is one of the causes of seawater eutrophication.

3.1.3. Urban Runoff

Urban runoff adds to this nutrient load through lawn fertilizers, pet waste, and leakage from faulty septic systems [252,253]. These inputs are particularly significant in heavily urbanized coastal regions where impervious surfaces facilitate rapid nutrient transport to marine environments [254,255].

Figure 7 exhibits the distribution of global marine eutrophication hotspots and coastal cities with a population of more than 3 million worldwide. As can be seen from Figure 7, there is a certain overlap between global marine eutrophication hotspots and large coastal cities. This indicates that urban runoff from large cities is one of the causes of marine eutrophication. Wastewater discharges, encompassing both municipal and industrial effluents, are significant sources of nitrogen and phosphorus [255,256]. Even after treatment, these effluents often contain residual nutrient loads that contribute to the overall eutrophication potential of receiving waters. The combustion of fossil fuels in large cities contributes to atmospheric deposition, where nitrogen compounds are deposited into the oceans through precipitation and dry deposition, further augmenting nutrient levels in marine systems [257,258].

Table 13. Overview of population and nitrogen and phosphorus discharge in major global cities.

City	Population	Nitrogen Discharge (tons/Year)	Phosphorus Discharge (tons/Year)	Sources of Nitrogen and Phosphorus Discharge	Ref.
New York	8,336,817	120,000	8500	Domestic sewage, agricultural runoff, industrial waste	[259]
Los Angeles	3,979,576	85,000	6000	Domestic sewage, urban runoff, industrial effluents	[260]
Miami	467,963	45,000	3200	Domestic sewage, urban runoff, aquaculture, agricultural runoff	[261]
Vancouver	631,486	55,000	4000	Domestic sewage, urban runoff, aquaculture	[262]
Sao Paulo	12,252,023	200,000	15,000	Domestic sewage, industrial waste, agricultural runoff	[263]
Rio de Janeiro	6,747,815	130,000	9500	Domestic sewage, industrial waste, agricultural runoff	[264]
Buenos Aires	15,153,729	180,000	12,500	Domestic sewage, urban runoff, industrial effluents, agricultural runoff	[265]
Caracas	2,939,000	75,000	5000	Domestic sewage, urban runoff, industrial waste	[266]
London	9,304,000	150,000	10,000	Domestic sewage, urban runoff, industrial effluents	[267]
Paris	11,017,000	160,000	11,000	Domestic sewage, urban runoff, agricultural runoff	[259]
Barcelona	5,575,000	85,000	6500	Domestic sewage, urban runoff, aquaculture, industrial waste	[268]
Antwerp	520,000	50,000	3000	Domestic sewage, industrial effluents, port activities	[269]
Cairo	20,900,000	300,000	22,000	Domestic sewage, agricultural runoff, industrial effluents	[270]
Lagos	15,388,000	270,000	20,000	Domestic sewage, urban runoff, industrial waste, aquaculture	[271]
Addis Ababa	5,228,000	90,000	7000	Domestic sewage, urban runoff, agricultural runoff	[272]
Abidjan	5,158,000	85,000	6500	Domestic sewage, urban runoff, industrial waste	[273]
Tokyo	14,043,000	320,000	25,000	Domestic sewage, urban runoff, industrial effluents, agricultural runoff	[274]
Shanghai	24,870,000	500,000	35,000	Domestic sewage, industrial effluents, aquaculture, agricultural runoff	[275]
Beijing	21,540,000	400,000	30,000	Domestic sewage, urban runoff, industrial waste, agricultural runoff	[276]
Hong Kong	7,474,200	150,000	10,000	Domestic sewage, urban runoff, aquaculture	[277]
Singapore	5,637,000	200,000	15,000	Domestic sewage, urban runoff, aquaculture	[278]
Mumbai	20,667,000	350,000	26,000	Domestic sewage, urban runoff, industrial waste	[279]
Sydney	5,367,000	90,000	7000	Domestic sewage, urban runoff, aquaculture, agricultural runoff	[280]
Melbourne	5,159,000	85,000	6500	Domestic sewage, urban runoff, aquaculture	[281]
Istanbul	15,519,000	250,000	18,000	Domestic sewage, urban runoff, industrial effluents	[282]
Jakarta	10,770,000	270,000	20,000	Domestic sewage, urban runoff, industrial waste, aquaculture	[283]
Manila	1,780,148	80,000	5500	Domestic sewage, urban runoff, aquaculture	[284]

provides a comparative analysis of key factors contributing to nutrient loading in various coastal and urban areas, including population, types of waste discharges, and primary sources of nitrogen and phosphorus pollution.

As shown in

Table 14. Summary of seasonal algal blooms in various sea areas.

Sea Area Name	Outbreak Time	Outbreak Cause	Outbreak Frequency	Dominant Species	Refs.
Black Sea	December–March	Nutrient loading, temperature inversion	Annually	Pseudo-nitzschia spp. Emiliania huxleyi	[288,289]
Baltic Sea	November–February	Low temperature, high nutrient levels	Biennially	Aphanizomenon spp.	[290,291]
Gulf of Maine	January–March	Cold water upwelling, nutrient input	Annually	Alexandrium fundyense	[292]
Bering Sea	December–April	Ice melt, nutrient upwelling	Annually	Chaetoceros spp.	[31,32,33]
Sea of Okhotsk	November–March	Ice edge upwelling, nutrient inflow	Annually	Pseudo-nitzschia spp.	[293]
Yellow Sea	December–February	Cold water mixing, agricultural runoff	Annually	Skeletonema costatum	[294]
Barents Sea	February–April	Temperature drops, nutrient influx	Biennially	Chaetoceros spp.	[29,30]
North Sea	December–March	Cold currents, high nutrient load	Annually	Phaeocystis globosa	[295,296]
Gulf of St. Lawrence	December–February	Cold water upwelling, river runoff	Annually	Alexandrium tamarense	[297]
Sea of Japan	January–March	Cold currents, nutrient inputs	Annually	Dinophysis spp.	[298]

, the phenomenon of “winter algal bloom” refers to the unusual growth of algae during the winter months, a period typically characterized by lower temperatures and reduced sunlight, which are generally less conducive to algal proliferation. Despite these conditions, certain sea areas around the world experience significant algal blooms in winter due to specific environmental factors [285]. These include the Black Sea, the Baltic Sea, the Gulf of Maine, the Bering Sea, the Sea of Okhotsk, and the Yellow Sea, among others [286]. The causes of winter algal blooms vary by region but commonly involve nutrient enrichment from agricultural runoff or urban discharge, cold water upwelling, and temperature inversions that trap nutrients near the surface [287]. In some areas, the melting of sea ice contributes to the influx of nutrients, while in others, the circulation of cold currents or the mixing of water layers during winter storms creates optimal conditions for algal growth. These blooms often involve species that are well-adapted to cold conditions and can sometimes produce harmful toxins, posing risks to marine ecosystems and human health.

3.2. CO₂ Emissions

Over the past decade, global carbon emissions have risen steadily from 33.1 Gt in 2010 to 36.6 Gt in 2019 and then experienced a significant 6.4% decline in 2020 due to the COVID-19 pandemic, before rebounding to 36.3 Gt by 2022 [299]. The COVID-19 pandemic led to a temporary reduction in CO₂ emissions due to decreased industrial activity, transportation, and energy consumption [300]. The temporary reduction in emissions during the pandemic slightly slowed the rate of ocean acidification and global warming, but these changes were short-lived and not substantial enough to reverse long-term trends. As a result, the overall impact on HABs was minimal, with no significant reduction in their frequency or intensity. For example, a study in the Gulf of Mexico reported a slight decrease in the intensity of HABs during the early stages of the pandemic, likely due to reduced nutrient inputs from agricultural runoff. However, blooms in other areas, such as the Baltic Sea, have persisted or even increased, which may be influenced by long-term environmental trends rather than short-term emissions changes [301].

Increased CO₂ emissions cause climate change, leading to a rise in sea temperatures and ocean acidification. CO₂ emissions contribute to HABs primarily through climate change and ocean acidification [302]. Increased CO₂ levels lead to global warming, which raises sea surface temperatures, creating favorable conditions for the growth and proliferation of harmful algal species. Additionally, ocean acidification, resulting from higher atmospheric CO₂ dissolving into seawater, can alter marine ecosystems and nutrient dynamics, often benefiting certain harmful algal species over others [303]. These changes in temperature and pH levels can disrupt marine ecosystems, leading to more frequent and intense HABs. The CO₂ emissions from 2010 to 2024 are shown in Figure 8.

3.2.1. Rising Sea Temperatures

Since the beginning of the 20th century, global sea surface temperatures (SSTs) have risen significantly. According to the Intergovernmental Panel on Climate Change (IPCC), the average rate of SST increase has been approximately 0.13 °C per decade from 1901 to 2020 [304]. However, the rate of increase has accelerated in recent decades. For instance, from 1990 to 2020, the SST increase has been closer to 0.18 °C per decade, reflecting an intensified warming trend in recent years. Climate-induced increases in sea temperatures create favorable conditions for the proliferation of many harmful algal species [305]. Warmer waters not only enhance algal metabolic rates but also extend the growing seasons, leading to more frequent and prolonged bloom events [306]. For instance, species such as Karenia brevis and Alexandrium spp. thrive in warmer conditions, resulting in intensified red tide events and paralytic shellfish poisoning outbreaks, respectively. The marine algae species that thrive as sea temperatures rise are listed in

Table 15. Marine algal species that thrive as sea temperatures rise.

Algal Species	Toxin Produced	Effects	Refs.
Karenia brevis	Brevetoxins	Causes red tides, respiratory irritation, fish kills	[307,308,309]
Alexandrium fundyense	Saxitoxins	Affects human health through contaminated shellfish	[310]
Dinophysis spp.	Okadaic acid	Causes gastrointestinal issues in humans	[311,312]
Ceratium furca	None specific	Disrupts marine ecosystems, depletes oxygen	[313]
Pseudo-nitzschia spp.	Domoic acid	Neurological effects in humans and marine animals	[314,315]
Gymnodinium catenatum	Saxitoxins	Affects human health through contaminated shellfish	[316,317]
Cochlodinium polykrikoides	None specific	Causes fish kills, disrupts marine ecosystems	[10,318]
Prorocentrum minimum	Yessotoxins	Affects marine life, potential human health impacts	[319,320]
Akashiwo sanguinea	Hemolysins	Fish kills, disrupts marine ecosystems	[321,322]
Chattonella spp.	Brevetoxins	Causes fish kills, respiratory irritation	[323,324]
Heterosigma akashiwo	Unknown toxins	Fish kills, disrupts marine ecosystems	[315]
Margalefidinium polykrikoides	Unknown toxins	Causes fish kills, disrupts marine ecosystems	[325]
Lingulodinium polyedrum	Yessotoxins	Causes red tides, bioluminescence, disrupts ecosystems	[326]
Scrippsiella trochoidea	None specific	Disrupts marine ecosystems, depletes oxygen	[327]
Ostreopsis spp.	Palytoxin-like compounds	Respiratory issues, skin irritation in humans, marine life effects	[328]

.

Rising sea temperatures trigger the intensification of HABs through several interconnected mechanisms that influence the growth, distribution, and toxicity of algal species. The underlying mechanisms are as follows:

(1).

Enhanced Growth Rates of Warm-Water Algal Species

Many harmful algal species, such as the species mentioned in Table 15, have optimal growth temperatures that are higher than those of other phytoplankton. As sea temperatures rise, these species can grow faster and outcompete other organisms, leading to more frequent and intense blooms. Additionally, warmer waters can extend the growing season for harmful algae, allowing them to thrive for longer periods each year, which increases the likelihood of blooms [329].

(2).

Altered Stratification of Water Columns

Rising sea temperatures increase the stratification of the water column, which reduces vertical mixing [329]. This leads to the formation of nutrient-rich surface layers where algae can proliferate. With limited nutrient exchange between surface and deeper waters, harmful algal species that can efficiently use available surface nutrients can dominate. Reduced mixing also means lower turbulence, which favors the growth of harmful algal species that thrive in stable, calm water conditions.

(3).

Changes in Nutrient Availability

Higher temperatures can accelerate the decomposition of organic matter in the water, leading to increased nutrient availability (e.g., nitrogen and phosphorus) in surface waters [306]. This nutrient enrichment supports the growth of harmful algal species, particularly in coastal regions where nutrient inputs from the land are already high. Additionally, warmer conditions may alter the ratio of nutrients, such as nitrogen to phosphorus, in a way that favors harmful algal species over other phytoplankton.

(4).

Increased Toxicity of Certain Algal Species

Enhanced Toxin Production: Some harmful algae produce more toxins when exposed to higher temperatures. For example, species like Alexandrium spp. and Cylindrospermopsis raciborskii are known to increase their toxin production in warmer waters [330]. This makes blooms not only more frequent but also more dangerous to marine life and humans.

(5).

Geographical Expansion of HABs

Rising sea temperatures enable harmful algal species to expand their range towards the poles, colonizing new areas that were previously too cold. This geographical shift increases the occurrence of HABs in regions that were not historically affected. On the other hand, warmer waters also create favorable conditions for the invasion of harmful algal species into new ecosystems, where they may encounter fewer predators or competitors, leading to more severe blooms [302].

(6).

Impacts on Predator–Prey Dynamics

Warmer sea temperatures can disrupt the balance of marine food webs, reducing the populations of grazers that feed on algae. This reduction in grazing pressure allows harmful algal species to proliferate unchecked [304].

3.2.2. Ocean Acidification

Global carbon dioxide emissions have generally increased in recent decades because of economic growth, industrialization, and population expansion. The energy sector, in particular the combustion of fossil fuels for power generation, heating, and transport, remains the largest source of emissions [303].

Elevated atmospheric CO₂ concentrations can lead to ocean acidification, which can affect algal species to varying degrees [331]. Certain harmful algae may produce more toxins because of ocean acidification, as shown in

Table 16. Algae that can bloom and produce toxicity under ocean acidification in existing studies.

Algal Species	Toxins	Distribution	Refs.
Alexandrium spp.	saxitoxins	Widely distributed in temperate and tropical coastal waters around the world.	[332,333]
Pseudo-nitzschia spp.	domoic acid	Found globally in both coastal and open ocean waters, with notable blooms along the west coast of North America (California and Alaska), the Gulf of Mexico, and parts of Europe (North Sea).	[334,335]
Dinophysis spp.	okadaic acid pectenotoxins	Found in coastal waters worldwide, including the North Atlantic, the Mediterranean Sea, and the coasts of South America and Asia.	[333]
Karenia brevis	brevetoxins	Primarily found in the Gulf of Mexico and along the southeastern coast of the United States, particularly in Florida.	[336,337]
Gambierdiscus spp.	ciguatoxins	Predominantly found in tropical and subtropical regions, including the Caribbean, the Pacific Islands, and the coasts of Australia and Southeast Asia.	[338]
Microcystis spp.	microcystins	Primarily found in freshwater, brackish, and marine environments, with occurrences in coastal regions worldwide, including the Baltic Sea and estuaries.	[339,340]
Lyngbya majuscula	lyngbyatoxin	Found in tropical and subtropical coastal waters, including the Caribbean, the Indian Ocean, and the Pacific Ocean, particularly around Australia and Southeast Asia.	[341,342]

.

3.3. The Influence of Alien Species

The introduction of alien species in marine environments can have significant, often detrimental, impacts on the ecosystem, particularly by exacerbating eutrophication and promoting harmful algal blooms. These species can modify nutrient cycles, outcompete native species, and introduce new challenges, creating conditions that favor the dominance of harmful algae (

Table 17. Case studies of alien species impacting eutrophication and HABs.

Alien Species	Impact Mechanism	Location of Occurrence	Dominant Species during Algal Outbreaks	Ref.
Caulerpa taxifolia	Outcompetes native seagrasses, alters nutrient cycling	Mediterranean Sea	Alexandrium minutum	[343]
Mnemiopsis leidyi	Disrupts zooplankton populations, leading to increased algal biomass	Black Sea	Prymnesium parvum	[344]
Didemnum vexillum	Biofouling on structures, altering local nutrient dynamics	New Zealand Coast	Karenia brevis	[345]
Undaria pinnatifida	Outcompetes native kelp, changes habitat structure	North Atlantic Ocean	Phaeocystis globosa	[346]
Perna viridis	Alters nutrient cycles through biofiltration	Gulf of Mexico	Microcystis aeruginosa	[347]
Mytilus galloprovincialis	Outcompetes native mussels, changes nutrient dynamics	South African Coast	Alexandrium catenella	[348]
Ctenophora (comb jellies)	Predation on zooplankton, reducing grazing pressure on phytoplankton	Caspian Sea	Gonyaulax spinifera	[349]
Codium fragile	Competes with native algae, modifies nutrient availability	Japan Sea	Prorocentrum minimum	[98]
Gracilaria vermiculophylla	Creates dense mats, alters local hydrodynamics and nutrient flow	Western Baltic Sea	Dinophysis acuminata	[350]
Sargassum muticum	Forms large floating mats, modifies nutrient dynamics	English Channel	Pseudo-nitzschia spp.	[351]
Ciona intestinalis	Biofouling, alters nutrient recycling in coastal areas	Scandinavian Coasts	Chaetoceros spp.	[352]
Littorina littorea	Alters sediment structure, impacting nutrient availability	North American East Coast	Heterosigma akashiwo	[353]
Spartina alterniflora	Invades and modifies coastal wetlands, alters nutrient dynamics	Pacific Coast of the US	Coscinodiscus spp.	[354]
Styela clava	Biofouling and competition, altering habitat complexity	South Korean Coast	Skeletonema costatum	[345]
Pterois volitans (Lionfish)	Predation on herbivorous fish, leading to overgrowth of algae	Caribbean Sea	Karenia brevis	[355]
Corbicula fluminea	Alters sediment and nutrient dynamics	Southeast Asian Coast	Cylindrospermopsis raciborskii	[356]
Carcinus maenas (Green Crab)	Preys on native species, modifies ecosystem structure	US Atlantic Coast	Alexandrium fundyense	[357]
Eriocheir sinensis (Chinese Mitten Crab)	Burrowing activity alters sediment and nutrient flow	European Rivers	Microcystis aeruginosa	[358]
Lepidochitona cinerea	Grazes on native algae, shifts competitive balance	Mediterranean Coast	Noctiluca scintillans	[359]
Halophila stipulacea	Competes with native seagrasses, changes nutrient dynamics	Caribbean Sea	Pyrodinium bahamense	[360]
Batillaria attramentaria	Alters sediment composition, impacts nutrient cycles	West Coast of North America	Lingulodinium polyedra	[361]
Ascophyllum nodosum	Changes in nutrient uptake dynamics	North Atlantic Ocean	Aureococcus anophagefferens	[362]
Charybdis japonica	Predation and competition, altering nutrient dynamics	New Zealand Estuaries	Akashiwo sanguinea	[363]
Melanoides tuberculata	Modifies sediment and nutrient availability	Florida Wetlands	Karlodinium veneficum	[364]
Rapana venosa	Predation on bivalves, impacting nutrient recycling	Black Sea	Alexandrium tamarense	[365]
Tunicata (Sea Squirts)	Filter feeding, changes nutrient dynamics	Scottish Coast	Prymnesium parvum	[366]
Clytia hemisphaerica	Alters plankton community dynamics	Northern Adriatic Sea	Karenia mikimotoi	[367]
Chthamalus stellatus	Changes intertidal nutrient flows	Portuguese Coast	Dinophysis acuta	[368]
Tricellaria inopinata	Biofouling on marine structures, altering local nutrient dynamics	Italian Coast	Pseudochattonella verruculosa	[366]
Balanus improvisus	Displaces native species, modifies nutrient availability	Baltic Sea	Aphanizomenon flos-aquae	[369]
Crassostrea gigas (Pacific Oyster)	Alters local nutrient cycles through biofiltration	Normandy Coast, France	Chattonella marina	[370]

). Understanding these interactions is critical for managing and mitigating the risks associated with both eutrophication and HABs in marine ecosystems.

3.4. Geographical Distribution of HABs

The impact of toxic bloom processes is heavily influenced by geographical distribution, as environmental conditions, oceanographic features, and human activities vary across regions. Warmer waters, coastal upwelling zones, and enclosed seas are more prone to HABs due to favorable conditions for algae growth. Areas with high nutrient runoff from agriculture and urbanization, such as the Gulf of Mexico and the East China Sea, experience frequent and intense blooms that disrupt ecosystems and harm local economies. The severity of HABs also depends on the region’s biodiversity and human activity, with regions like the Mediterranean and Southeast Asia facing significant public health and economic risks from toxin accumulation in seafood. Understanding these geographical influences is crucial for effective HAB management and mitigation strategies.

Table 18. Summary of the relationship between location, dominant algal species, toxin, geographical distribution, environmental factors, oceanographic features, and the mechanism of influence on toxic bloom processes.

Location	Dominant Algal Species	Toxin	Geographical Distribution	Environmental Factors	Oceanographic Features	Mechanism of Influence	Ref.
Gulf of Mexico, USA	Karenia brevis	Brevetoxins	Subtropical, coastal waters	Warm temperatures, high nutrient runoff	Seasonal stratification, riverine inputs	Warm waters and high nutrient runoff from agriculture promote bloom frequency and intensity.	[371]
East China Sea, China	Prorocentrum donghaiense	Okadaic acid	Coastal, heavily industrialized	High nutrient input from agriculture and urbanization	Strong currents, upwelling zones	Nutrient pollution and strong ocean currents promote frequent blooms.	[372]
Baltic Sea, Europe	Nodularia spumigena	Nodularin	Enclosed sea, brackish water	Eutrophication, limited water exchange	Stratification, low salinity	Limited water exchange and nutrient accumulation contribute to persistent cyanobacterial blooms.	[373]
Mediterranean Sea, Europe	Alexandrium minutum	Saxitoxins (Paralytic Shellfish Toxins)	Semi-enclosed sea, temperate	Variable nutrient sources, urban runoff	Complex circulation patterns, semi-enclosed nature	High nutrient input and complex circulation patterns enhance HAB development.	[374]
Great Lakes, USA	Microcystis aeruginosa	Microcystins	Freshwater, temperate region	Agricultural runoff, warm summers	Stratification, freshwater system	Agricultural runoff and warm summers lead to frequent cyanobacterial blooms.	[375]
Black Sea, Europe	Alexandrium tamarense	Saxitoxins (Paralytic Shellfish Toxins)	Enclosed sea, nutrient-rich	Nutrient input from rivers, limited circulation	Low salinity, poor water circulation	Limited circulation and high nutrient input exacerbate toxic bloom events.	[376]
South China Sea, Asia	Gymnodinium catenatum	Saxitoxins (Paralytic Shellfish Toxins)	Tropical, coastal waters	Marine traffic, coastal development, nutrient loading	Monsoon-driven circulation, coastal upwelling	High nutrient loading and monsoon-driven currents promote frequent toxic blooms.	[377]
Chesapeake Bay, USA	Dinophysis acuminata	Okadaic acid, Dinophysistoxins	Estuarine, temperate region	High nutrient input from agriculture and urban runoff	Stratification, tidal mixing	Nutrient pollution and stratification enhance bloom occurrences.	[378]
Arabian Gulf, Middle East	Cochlodinium polykrikoides	No specific toxin identified, but associated with fish kills	Arid, warm coastal waters	Desalination effluents, high salinity	High salinity, weak circulation	High salinity and nutrient input from desalination create favorable conditions for HABs.	[379]
Australian Coastal Waters	Noctiluca scintillans	Ammonia (indirectly harmful, not a toxin in the traditional sense)	Coastal, temperate to tropical	Upwelling, nutrient-rich waters	Coastal upwelling, strong currents	Upwelling and nutrient enrichment lead to frequent red tide events.	[380]

highlights the complex interplay between environmental factors, oceanographic features, and geographical distribution in shaping the occurrence and impact of HABs.

Overall, variation in HABs across marine ecosystems is influenced by local nutrient conditions. In coastal waters, high nutrient loads from land runoff lead to frequent and intense blooms, particularly of dinoflagellates and cyanobacteria, driven by high nitrogen and phosphorus levels. The open ocean typically has lower nutrient levels, but localized nutrient enrichment through upwelling or iron fertilization can trigger blooms, particularly of diatoms or other phytoplankton when iron or nitrogen is added. Estuaries experience fluctuating nutrient levels due to the mixing of freshwater and seawater, with high nitrogen and phosphorus inputs leading to diverse algal blooms, influenced by varying salinity and hydrodynamic conditions. In coral reefs, which are usually low in nutrients, excess nitrogen and phosphorus can shift ecosystems from coral-dominated to algal-dominated systems, where macroalgae and harmful algae outcompete corals and degrade the reef environment.

4. Monitoring Techniques and Management Strategies

Monitoring HABs in marine environments is crucial for early detection and management to mitigate their impacts on marine ecosystems, human health, and economies. Several monitoring techniques are used, ranging from traditional field-based methods to advanced technological approaches [100].

4.1. Field Sampling and Microscopy

Water sampling remains a fundamental technique for HAB monitoring. Traditional methods involve collecting samples using Niskin bottles at various depths and locations. Microscopy is used to identify and count algal cells in collected water samples. Traditional light microscopy requires expertise in algal taxonomy. Advances such as flow cytometry, combined with microscopy, enhance the speed and accuracy of identification and counting. Automated imaging flow cytometers like FlowCam provide high-resolution images and quantitative data on algal populations [381].

4.2. Molecular Techniques

4.2.1. DNA/RNA Analysis

PCR and qPCR are powerful molecular techniques utilized for detecting and quantifying specific algal species by targeting unique genetic markers, thereby ensuring precise identification and reducing the risk of misidentification [382]. The technology’s high sensitivity allows it to detect minute amounts of algae DNA early in the development of HABs, providing rapid results within hours, which is significantly faster than traditional methods [383]. Quantitative PCR (qPCR) further enhances this capability by enabling the precise quantification of algae DNA, which correlates with the severity of blooms and assists in evaluating their environmental impact [384]. The process of using PCR for HAB monitoring involves sampling water from affected areas, isolating algae DNA through cell lysis, and employing specific primers designed to amplify target DNA sequences unique to the species of interest. The application steps of PCR technology in monitoring HABs are shown in Figure 9. Recent advancements include digital PCR (dPCR) for achieving absolute DNA quantification without standard curves, Next-Generation Sequencing (NGS) for comprehensive genomic analysis beyond PCR’s scope, multiplex PCR for simultaneously detecting multiple algae species, portable Point-of-Care PCR devices for real-time monitoring in field settings, and integration with remote sensing and bioinformatics for precise spatial mapping and predictive modeling of HAB dynamics [385]. These innovations collectively enhance the effectiveness and versatility of PCR technology in monitoring and managing harmful algal blooms. The differences between traditional PCR, dPCR, and qPCR are shown in

Table 19. The differences between traditional PCR, dPCR, and qPCR.

Feature	Principle of Operation	Quantification Method	Sensitivity and Precision
Traditional PCR	Amplifies DNA for qualitative detection	Qualitative (presence/absence)	Less sensitive, suitable for detection only
qPCR	Quantifies DNA via fluorescence measurement	Relative quantification based on standard curves	Sensitive, but dependent on PCR efficiency and standard curves
dPCR	Partitions sample, performs PCR in each, and counts positive reactions	Absolute quantification using Poisson statistics	Highly sensitive and precise, minimal influence from PCR efficiency

.

dPCR achieves absolute quantification through the following steps:

(1)

Partitioning: The sample is diluted and then partitioned into thousands or millions of tiny individual reactions. Each partition ideally contains either zero or one DNA molecule of the target sequence.

(2)

PCR Amplification: Each partition undergoes PCR amplification independently. If a partition contains the target DNA, it will produce a positive (fluorescent) signal after amplification; if it does not, it will remain negative.

(3)

Counting Positive Partitions: After amplification, the number of positive partitions (those that fluoresce) is counted.

(4)

Poisson Statistics: The proportion of positive partitions is used to estimate the absolute number of target molecules in the original sample using Poisson distribution. This calculation accounts for the fact that not all partitions will contain exactly one DNA molecule due to the random distribution.

Digital PCR (dPCR) offers significant advantages in monitoring HABs due to its high sensitivity and precision [386]. It allows for the early detection of low-abundance algal species and the quantification of specific toxin-producing genes, providing direct insights into potential bloom toxicity [387]. Additionally, dPCR facilitates the monitoring of environmental DNA (eDNA) from harmful algae, even in the absence of visible cells, making it a powerful tool for predicting bloom events. Its ability to achieve absolute quantification without standard curves also enhances the reliability and standardization of data across laboratories, improving the consistency of HAB monitoring programs.

Remote sensing technology is highly effective in providing large-scale and continuous monitoring of HABs, especially in open and relatively clear waters. The ability to monitor blooms in near real-time allows for rapid response and management actions, such as closing shellfish beds or issuing public health warnings [388]. It also enables the tracking of bloom development and movement, which is critical for understanding and predicting HAB events. However, the effectiveness of remote sensing is limited in turbid or optically complex waters, where the presence of suspended sediments or colored dissolved organic matter can obscure the detection of algal blooms. Cloud cover and atmospheric conditions also pose challenges, as they can block satellite sensors and lead to gaps in data. Additionally, remote sensing may struggle to distinguish between different algal species, making it difficult to identify specific harmful species and differentiate them from non-toxic phytoplankton. This limitation is particularly problematic in regions with diverse phytoplankton communities.

In summary, while remote sensing is a powerful tool for monitoring HABs, its effectiveness varies depending on the ecological environment and regional characteristics. Continued advancements in sensor technology and data processing methods are essential for improving the accuracy and reliability of remote sensing for HAB monitoring.

4.2.2. Metagenomics

Metagenomics has revolutionized the study of HABs by analyzing the collective genetic material of microbial communities in environmental samples. This approach avoids the isolation of individual organisms, capturing the diversity and functional potential of algae species implicated in blooms [389]. Recent research has highlighted the role of metagenomics in elucidating complex interactions within microbial communities and uncovering new insights into HAB dynamics and toxin production.

Metagenomics for HAB monitoring begins with sample collection from bloom-affected areas, followed by DNA extraction to capture genetic material from diverse microbial populations. High-throughput sequencing technologies enable the comprehensive analysis of DNA without prior isolation of individual species. Bioinformatics tools process sequencing data, identify specific algae species, and quantify their abundance based on genetic markers [390]. This integrated approach facilitates the interpretation of bloom dynamics, species composition, and environmental influences. Practical examples of HAB surveillance using macrogenomics are shown in Table 20.

Metagenomics holds promise for advancing predictive modeling of HABs, integrating remote sensing technologies for real-time monitoring, and enhancing ecosystem management strategies. Future research directions include refining bioinformatics tools for faster data analysis, exploring microbial interactions within bloom communities, and developing portable sequencing platforms for field applications [391].

Table 20. Practical examples of HAB surveillance using macrogenomics.

Harmful Algal Species	Location	Toxins	Application of Genomic/Metagenomic Technologies	Refs.
Karenia brevis	Florida, USA	Brevetoxins	Metagenomics for monitoring bloom dynamics, toxin production, and environmental influences.	[392,393]
Dinophysis spp.	Europe	Okadaic acid	High-throughput sequencing to monitor species abundance and predict bloom events impacting shellfish harvesting.	[394]
Alexandrium spp.	Gulf of Maine, USA	Saxitoxins	Genomic surveillance to detect genetic markers specific to Alexandrium spp., facilitating early warning and management of paralytic shellfish poisoning outbreaks.	[395]
Microcystis spp.	Global freshwater systems	Microcystins	Metagenomics for tracking bloom dynamics, toxin production, and ecological impacts on freshwater ecosystems.	[396]
Pseudo-nitzschia spp.	California, USA	Domoic acid	Application of metagenomics to monitor bloom occurrence, toxin levels in shellfish, and issuance of public health advisories.	[397]
Gambierdiscus spp.	Pacific Islands	Ciguatoxins	Metagenomic surveillance to monitor species distribution and abundance in coral reef ecosystems, informing safe fish consumption practices.	[398]
Akashiwo sanguinea	Asian coastal waters	Unknown toxins	Genomic approaches for understanding genetic diversity and environmental responses of A. sanguinea blooms.	[399]
Heterosigma akashiwo	Pacific Northwest, USA	Ichthyotoxins	Metagenomics to study genetic variability, bloom initiation, and environmental factors influencing bloom formation.	[400]
Dinoflagellate spp.	Baltic Sea	Saxitoxins, Okadaic acid	Utilization of metagenomics to analyze species composition, toxin production dynamics, and microbial interactions within blooms.	[401,402]

Table 20. Practical examples of HAB surveillance using macrogenomics.

Harmful Algal Species	Location	Toxins	Application of Genomic/Metagenomic Technologies	Refs.
Karenia brevis	Florida, USA	Brevetoxins	Metagenomics for monitoring bloom dynamics, toxin production, and environmental influences.	[392,393]
Dinophysis spp.	Europe	Okadaic acid	High-throughput sequencing to monitor species abundance and predict bloom events impacting shellfish harvesting.	[394]
Alexandrium spp.	Gulf of Maine, USA	Saxitoxins	Genomic surveillance to detect genetic markers specific to Alexandrium spp., facilitating early warning and management of paralytic shellfish poisoning outbreaks.	[395]
Microcystis spp.	Global freshwater systems	Microcystins	Metagenomics for tracking bloom dynamics, toxin production, and ecological impacts on freshwater ecosystems.	[396]
Pseudo-nitzschia spp.	California, USA	Domoic acid	Application of metagenomics to monitor bloom occurrence, toxin levels in shellfish, and issuance of public health advisories.	[397]
Gambierdiscus spp.	Pacific Islands	Ciguatoxins	Metagenomic surveillance to monitor species distribution and abundance in coral reef ecosystems, informing safe fish consumption practices.	[398]
Akashiwo sanguinea	Asian coastal waters	Unknown toxins	Genomic approaches for understanding genetic diversity and environmental responses of A. sanguinea blooms.	[399]
Heterosigma akashiwo	Pacific Northwest, USA	Ichthyotoxins	Metagenomics to study genetic variability, bloom initiation, and environmental factors influencing bloom formation.	[400]
Dinoflagellate spp.	Baltic Sea	Saxitoxins, Okadaic acid	Utilization of metagenomics to analyze species composition, toxin production dynamics, and microbial interactions within blooms.	[401,402]

4.3. Remote Sensing

Remote sensing has become an indispensable tool for monitoring marine HABs, offering large-scale, real-time data. The process begins with satellite imagery acquisition, where modern satellites equipped with optical and multispectral sensors capture images across various wavelengths [403]. These images help detect algal blooms by identifying unique spectral signatures of chlorophyll-a, a pigment in algae. By distinguishing between blooming and non-blooming areas, remote sensing algorithms enable accurate detection and monitoring. Practical examples of HAB surveillance using remote sensing are shown in Table 21. These examples illustrate that remote sensing is a powerful tool for monitoring HABs across various regions and ecological contexts, providing critical data for timely responses to potential ecological and public health threats. However, the effectiveness of remote sensing technologies is influenced by factors such as sensor resolution, frequency of data acquisition, local environmental conditions, and the specific optical properties of the water body. While some regions benefit from high-frequency monitoring, others face challenges related to cloud cover, water turbidity, and the need for high spatial and spectral resolution. Thus, remote sensing is most effective when integrated with in situ observations and local knowledge to address these limitations and improve the accuracy of HAB detection and management.

Regular satellite passes allow for continuous monitoring of bloom dynamics, tracking changes in extent, density, and movement. These temporal data provide insights into the development stages of blooms. Remote sensing also incorporates environmental parameters such as sea surface temperature, salinity, and ocean currents, which influence bloom formation and propagation. The integration of satellite observations with in situ measurements, including buoy data and water sampling, enhances the accuracy and reliability of assessments [404]. Practical cases of satellite maps for remote sensing are shown in Figure 10.

Table 21. Practical examples of HAB surveillance using remote sensing.

Location	Algal Species	Technology	Application	Ref.
Florida, USA	Karenia brevis	MODIS, Sentinel-3	Detecting and monitoring red tides, tracking bloom dynamics, and issuing public health advisories.	[22]
Baltic Sea	Various dinoflagellates	MERIS, Sentinel-3	Monitoring algal bloom extents, identifying species composition, and assessing environmental impacts.	[405]
California, USA	Pseudo-nitzschia spp.	MODIS, Landsat, Sentinel-2	Tracking bloom development, assessing toxin levels in shellfish, and providing early warnings.	[406]
Gulf of Mexico	Karenia brevis	MODIS, VIIRS, Sentinel-3	Detecting bloom onset, monitoring spatial distribution, and guiding management decisions for fisheries and tourism.	[407]
Great Lakes, USA	Microcystis spp.	MODIS, Sentinel-2, Landsat	Monitoring cyanobacterial blooms, assessing water quality, and informing drinking water treatment processes.	[408]
East China Sea	Karenia mikimotoi	MODIS, Sentinel-3, Hyperspectral sensors	Tracking bloom dynamics, assessing environmental conditions, and supporting fisheries management.	[409]
Chesapeake Bay, USA	Prorocentrum minimum	Landsat, Sentinel-2	Monitoring bloom occurrence, species composition, and environmental influences.	[410]
Mediterranean Sea	Various dinoflagellates	MODIS, MERIS, Sentinel-3	Assessing bloom extent, species diversity, and ecological impacts on marine ecosystems.	[411]
Arabian Gulf	Cochlodinium polykrikoides	MODIS, Sentinel-3, Landsat	Detecting fish-killing algal blooms, tracking bloom movement, and mitigating impacts on aquaculture.	[412]
Australia	Nodularia spumigena	MODIS, Sentinel-2	Monitoring toxic cyanobacterial blooms, assessing water quality, and informing public health decisions.	[413]
Irish Coastal Waters	Karenia mikimotoi	MODIS, Sentinel-2, Landsat	Detecting bloom initiation, monitoring spatial distribution, and assessing impacts on marine life.	[414]
North Sea	Various dinoflagellates	Sentinel-3, MODIS	Monitoring bloom dynamics, species composition, and environmental influences.	[415]
South China Sea	Heterosigma akashiwo	MODIS, Hyperspectral sensors	Tracking bloom initiation and dynamics, assessing environmental conditions, and supporting fisheries management.	[22,23]
Gulf of Maine, USA	Alexandrium spp.	MODIS, Sentinel-2, Landsat	Detecting and monitoring blooms, assessing toxin production, and guiding management practices for shellfish harvesting.	[416]
Black Sea	Various algae	MODIS, Sentinel-3	Monitoring bloom extents, species diversity, and environmental factors influencing bloom formation and persistence.	[417]

Table 21. Practical examples of HAB surveillance using remote sensing.

Location	Algal Species	Technology	Application	Ref.
Florida, USA	Karenia brevis	MODIS, Sentinel-3	Detecting and monitoring red tides, tracking bloom dynamics, and issuing public health advisories.	[22]
Baltic Sea	Various dinoflagellates	MERIS, Sentinel-3	Monitoring algal bloom extents, identifying species composition, and assessing environmental impacts.	[405]
California, USA	Pseudo-nitzschia spp.	MODIS, Landsat, Sentinel-2	Tracking bloom development, assessing toxin levels in shellfish, and providing early warnings.	[406]
Gulf of Mexico	Karenia brevis	MODIS, VIIRS, Sentinel-3	Detecting bloom onset, monitoring spatial distribution, and guiding management decisions for fisheries and tourism.	[407]
Great Lakes, USA	Microcystis spp.	MODIS, Sentinel-2, Landsat	Monitoring cyanobacterial blooms, assessing water quality, and informing drinking water treatment processes.	[408]
East China Sea	Karenia mikimotoi	MODIS, Sentinel-3, Hyperspectral sensors	Tracking bloom dynamics, assessing environmental conditions, and supporting fisheries management.	[409]
Chesapeake Bay, USA	Prorocentrum minimum	Landsat, Sentinel-2	Monitoring bloom occurrence, species composition, and environmental influences.	[410]
Mediterranean Sea	Various dinoflagellates	MODIS, MERIS, Sentinel-3	Assessing bloom extent, species diversity, and ecological impacts on marine ecosystems.	[411]
Arabian Gulf	Cochlodinium polykrikoides	MODIS, Sentinel-3, Landsat	Detecting fish-killing algal blooms, tracking bloom movement, and mitigating impacts on aquaculture.	[412]
Australia	Nodularia spumigena	MODIS, Sentinel-2	Monitoring toxic cyanobacterial blooms, assessing water quality, and informing public health decisions.	[413]
Irish Coastal Waters	Karenia mikimotoi	MODIS, Sentinel-2, Landsat	Detecting bloom initiation, monitoring spatial distribution, and assessing impacts on marine life.	[414]
North Sea	Various dinoflagellates	Sentinel-3, MODIS	Monitoring bloom dynamics, species composition, and environmental influences.	[415]
South China Sea	Heterosigma akashiwo	MODIS, Hyperspectral sensors	Tracking bloom initiation and dynamics, assessing environmental conditions, and supporting fisheries management.	[22,23]
Gulf of Maine, USA	Alexandrium spp.	MODIS, Sentinel-2, Landsat	Detecting and monitoring blooms, assessing toxin production, and guiding management practices for shellfish harvesting.	[416]
Black Sea	Various algae	MODIS, Sentinel-3	Monitoring bloom extents, species diversity, and environmental factors influencing bloom formation and persistence.	[417]

Recent advancements in technology, such as high-resolution imagery from Sentinel-2 and Landsat satellites, have improved spatial and spectral resolution for detailed bloom monitoring. The accuracy of various remote sensing technologies used to monitor HABs is shown in

Table 22. Differences in resolution and typical accuracy of each remote sensing technology.

Technology	Resolution	Typical Accuracy	Refs.
MODIS	250–1000 m	Major blooms detected	[402]
Sentinel-1	10–20 m (SAR)	N/A	[402]
Sentinel-2	10–60 m	70–80%	[419]
Sentinel-3	300 m (OLCI)	70–80%	[420]
Landsat 8	30 m	80–90%	[421,422]
Hyperspectral Camera (Drones/Aircraft)	1–5 m	>90%	[423]
Multispectral Sensors (Drones)	1–5 m	80–90%	[424,425]

. Hyperspectral and thermal sensors further enhance the detection of subtle changes in water quality. Early warning systems developed by combining satellite data with predictive models and historical records enable timely mitigation measures [403]. Future research aims to refine algorithms for automated detection, integrate remote sensing with other monitoring techniques, and enhance data fusion methods for effective HAB management and prediction [418].

Hyperspectral cameras with effective detection ranges offer significant advantages in monitoring red tides by providing detailed spectral data that enhance species identification, detection sensitivity, and spatial–temporal mapping of algal blooms [426]. They enable accurate measurement of chlorophyll and other pigments, allowing for precise assessments of bloom density and water quality. These high-resolution data support early detection of low-concentration blooms, detailed impact assessments of aquatic ecosystems, and informed management strategies. By integrating hyperspectral data with other remote sensing and in situ measurements, these cameras improve overall monitoring, modeling, and response efforts for effective red tide management [427].

4.4. Automated In Situ Sensors

Automated in situ sensors, such as fluorometers, spectrophotometers, nutrient sensors, optical sensors, and DNA biosensors, provide continuous, real-time monitoring of marine environments for early detection and tracking of HABs (details are shown in

Table 23. Types of automated in situ sensors.

Sensor Type	Function	Deployment Examples	Applications	Refs.
Fluorometers	Measure chlorophyll fluorescence to estimate phytoplankton concentration.	Gulf of Maine	Monitoring Alexandrium spp. blooms for Paralytic Shellfish Poisoning prevention.	[428]
Spectrophotometers	Analyze water samples to detect specific pigments associated with harmful algae.	Chesapeake Bay, USA	Detecting and tracking Prorocentrum minimum blooms, aiding in shellfish safety management.	[429]
Nutrient Sensors	Monitor concentrations of nutrients like nitrate, phosphate, and silicate.	Great Lakes, USA	Monitoring Microcystis spp. blooms to protect drinking water sources.	[430]
Optical Sensors	Capture data on water clarity, turbidity, and light penetration.	Chesapeake Bay, USA	Detecting and tracking Prorocentrum minimum blooms, aiding in shellfish safety management.	[431,432]
DNA Biosensors	Detect and quantify specific genetic markers of harmful algae.	Great Lakes, USA	Monitoring Microcystis spp. blooms to protect drinking water sources.	[433]

). These sensors are deployed on buoys, moorings, or autonomous underwater vehicles, collecting data on parameters like chlorophyll fluorescence, nutrient levels, and water temperature. The data are integrated and analyzed using advanced algorithms to identify harmful algae, track bloom development, and predict future outbreaks. Regular calibration ensures accuracy, and continuous monitoring enables timely mitigation measures.

Automated in situ sensors offer several advantages for monitoring HABs. They provide real-time monitoring, delivering continuous data that enable prompt detection and response to outbreaks. These sensors offer high-resolution temporal and spatial data, significantly enhancing the understanding of bloom dynamics [434]. They are cost-effective, reducing the need for frequent manual sampling and laboratory analysis. Furthermore, their scalability allows for deployment in multiple locations, covering large geographic areas and improving the overall efficiency of HAB monitoring and management efforts.

Using automated in situ sensors to monitor HABs involves several key steps. First, water samples are collected from areas suspected or known to be affected by HABs, ensuring the samples are representative of the bloom area [425]. DNA is then extracted from these samples, retrieving genetic material from all organisms present. High-throughput sequencing is performed on the extracted DNA, allowing for the analysis of genetic material from complex environmental samples [382]. Bioinformatics tools process the sequencing data to identify and quantify specific harmful algae species based on their genetic markers [435]. This comprehensive analysis provides insights into bloom dynamics, species composition, and environmental factors influencing HAB outbreaks, enabling proactive monitoring and management strategies. The key steps in using automated in situ sensors are shown in Figure 11.

4.5. Modeling and Forecasting

Modeling and forecasting play a crucial role in monitoring marine HAB outbreaks by predicting their occurrence, movement, and potential impacts. The process involves collecting historical and real-time data on environmental parameters such as water temperature, salinity, nutrient levels, and ocean currents, as well as biological data on algal species [155]. These data are input into sophisticated computer models that simulate the complex interactions between physical, chemical, and biological factors influencing HABs. These models use algorithms and statistical methods to analyze patterns and trends, enabling the prediction of bloom development and dispersion [436]. Forecasting systems integrate model outputs with remote sensing data and in situ observations to provide timely and accurate predictions of HABs, aiding in early warning and mitigation strategies [437]. Predictive models used for monitoring HABs are shown in

Table 24. Predictive models used for monitoring HABs.

Predictive Model	Practical Example	Description	Ref.
Numerical Models	Gulf of Mexico: Predicting Karenia brevis blooms	Utilizes physical, chemical, and biological data to simulate bloom dynamics and predict outbreaks	[438,439]
Statistical Models	Chesapeake Bay: Forecasting Prorocentrum minimum blooms	Uses historical data and statistical methods to predict bloom occurrences	[440]
Machine Learning Models	Great Lakes: Forecasting cyanobacterial blooms	Employs machine learning algorithms to analyze large datasets and predict HABs	[441]
Hydrodynamic Models	North Sea: Predicting Phaeocystis globosa blooms	Integrates oceanographic data to model water movement and predict bloom dispersion	[442]
Biogeochemical Models	Baltic Sea: Forecasting Nodularia spumigena blooms	Combines nutrient cycling and algal growth dynamics to forecast blooms	[443]
Coupled Physical-Biological Models	California Coast: Predicting Alexandrium catenella blooms	Integrates physical oceanography and biological processes to predict bloom dynamics	[444]
Remote Sensing Integrated Models	Florida Coast: Predicting Karenia brevis blooms using satellite data	Combines satellite remote sensing with modeling to enhance bloom prediction accuracy	[402]
Ecosystem Models	Puget Sound: Forecasting harmful algal bloom impacts on marine ecosystems	Models interactions between HABs and marine ecosystems to predict ecological impacts	[445]
Bayesian Network Models	New Zealand: Forecasting Alexandrium minutum blooms	Uses probabilistic methods to integrate various data sources for bloom prediction	[445]
Lagrangian Particle Tracking Models	East China Sea: Predicting Dinophysis acuminata blooms	Tracks the movement of individual water parcels to predict the transport and spread of blooms	[446]
Artificial Neural Networks	Mediterranean Sea: Predicting Dinoflagellate blooms	Uses neural network algorithms to learn and predict complex bloom patterns	[447]
Ensemble Models	Black Sea: Forecasting Cyanobacteria blooms	Combines multiple model outputs to improve prediction reliability and accuracy	[448]
Time Series Models	Hong Kong Waters: Predicting Cochlodinium polykrikoides blooms	Analyzes time series data to identify trends and predict future bloom events	[449]
Spatial–Temporal Models	South Korea: Forecasting Cochlodinium polykrikoides blooms	Integrates spatial and temporal data to predict the occurrence and spread of blooms	[450]
Decision Support Systems	Norway: Forecasting Karenia mikimotoi blooms	Provides integrated tools for real-time monitoring, prediction, and decision-making support	[451]

.

4.6. Comparison of Monitoring Techniques for Eutrophic Oceans

Monitoring techniques for treating eutrophic oceans each have distinct advantages and disadvantages. Field Sampling and microscopy are well-established with extensive historical data but are labor-intensive and time-consuming [438]. Molecular techniques offer high sensitivity and rapid results but require specialized equipment and high initial costs. DNA/RNA analysis provides detailed genetic information and can identify multiple species but needs advanced bioinformatics and is costly. Metagenomics offers a comprehensive view of microbial communities but has very high costs and complex data interpretation. Remote sensing enables large-scale, real-time monitoring with minimal environmental impact but is limited to surface observations and has high setup costs. Automated in situ sensors provide continuous real-time data and reduce the need for frequent sampling but are expensive to install and maintain. Modeling and forecasting enable predictive analysis and proactive management but require accurate data, robust models, and high computational resources. Overall, the choice of technique depends on the specific monitoring needs, available resources, and long-term sustainability goals (

Table 25. Comparison of monitoring techniques for eutrophic oceans.

Technique	Advantages	Disadvantages	Cost	Sustainability	Refs.
Field Sampling and Microscopy	Direct observation, extensive historical data, low initial cost	Labor-intensive, time-consuming, requires skilled personnel	Moderate	Low	[452]
Molecular Techniques	High sensitivity and specificity, rapid results	Requires specialized equipment and personnel, high setup costs	High initial, moderate ongoing	Moderate	[453]
DNA/RNA Analysis	Detailed genetic information, multiple species identification	Advanced bioinformatics needed, high sequencing costs	High	Moderate to High	[454]
Metagenomics	Comprehensive view, identifies unknown species	High-throughput sequencing, complex data interpretation	Very High	High	[455]
Remote Sensing	Large-scale, real-time, non-invasive	Limited to surface, requires calibration, high setup cost	Moderate to High	High	[456,457]
Automated in situ Sensors	Continuous real-time monitoring, various parameter measurements	High setup and maintenance costs, limited to fixed locations	High initial, moderate to high maintenance	High	[458]
Modeling and Forecasting	Predictive, integrates multiple data sources, proactive management	Requires accurate data and robust models, high computational resources	High	High	[459]

).

5. Treatment Technologies for Eutrophication of Seawater

There are several treatment technologies used to address the eutrophication of seawater. These technologies aim to reduce nutrient levels, particularly nitrogen and phosphorus, which are primary contributors to eutrophication. The key treatment technologies are summarized in

Table 26. The key treatment technologies for eutrophication of seawater.

Technology Type	Example Methods	Description	Refs.
Chemical Treatments	Nutrient Binding Agents	Uses chemicals to precipitate or bind nutrients	[460,461]
Biological Treatments	Bioremediation, Aquatic Plants	Utilizes microorganisms or plants to remove nutrients	[462,463]
Physical Treatments	Dredging, Aeration and Oxygenation, Flocculation	Involves physical processes to remove or reduce nutrients	[464]
Constructed Wetlands	Natural Filtration	Mimics natural wetlands for nutrient removal	[465,466]
Advanced Technologies	Membrane Filtration, Electrochemical Treatment, Photocatalysis	Uses advanced methods to filter or degrade nutrients	[467]
Innovative Technologies	Biochar Application, Microbial Fuel Cells	Employs emerging technologies for nutrient removal and management	[468]

.

5.1. Chemical Treatments

Chemical treatments are commonly employed to manage eutrophication by targeting the reduction in nutrient levels, especially phosphorus, in aquatic systems.

Phosphorus precipitation involves the addition of chemicals that react with soluble phosphorus to form insoluble compounds, which then settle out of the water column and can be removed [469]. Table 27 provides a comprehensive overview of various phosphorus precipitation treatments, highlighting their mechanisms, applications, and specific examples where they have been effectively used to manage eutrophication in aquatic environments.

Phosphorus precipitation treatments offer effective solutions for reducing phosphorus levels in water bodies, crucial for managing eutrophication [470]. They vary in advantages, such as the high efficiency of aluminum sulfate (alum) and ferric chloride, the environmental friendliness of chitosan and biochar, and the long-lasting effects of lanthanum-modified clay. However, these treatments also have disadvantages, including potential toxicity to aquatic life from alum and ferric compounds, high costs associated with lanthanum-modified clay and lanthanum chloride, and handling difficulties with lime and magnesium hydroxide [471]. Additionally, some treatments may alter water pH or hardness, such as calcium nitrate and lime, while others like sodium sulfate may increase water salinity. The environmental impact of phosphorus precipitation chemicals is a critical factor in their selection. While highly effective options like lanthanum-modified clay and lanthanum chloride present minimal environmental risks, their high cost makes them suitable mainly for sensitive environments. Chemicals such as ferric chloride and ferric sulfate, though cost-effective, can lead to significant iron accumulation and potential acidification, posing risks to aquatic life. Eco-friendly alternatives like chitosan and biochar offer lower environmental impacts but may require optimization for enhanced phosphate removal. The choice of treatment must balance efficacy, cost, and environmental sustainability, with special consideration given to the specific ecological conditions of the affected water bodies (Table 27).

Table 27. Chemical reagents for phosphorus precipitation.

Chemical Treatment	Mechanism	Efficacy	Cost	Specific Environmental Impact	Considerations	Refs.
Aluminum Sulfate	Forms insoluble aluminum phosphate	High	Moderate	Potential aluminum toxicity to aquatic organisms; increases water acidity.	Effective at low pH; potential aluminum toxicity in aquatic environments.	[472,473]
Ferric Chloride	Forms insoluble ferric phosphate	High	Low	Iron accumulation in sediments; potential to lower pH significantly.	Effective across a wide pH range; can cause iron accumulation in sediments.	[474]
Calcium Hydroxide	Forms insoluble calcium phosphate	Moderate	Low	Minimal impact; may increase water hardness and pH.	Safe for the environment but less effective in cold temperatures.	[475,476]
Lanthanum-Modified Clay	Binds phosphate to form insoluble compound	Very High	High	Minimal environmental risks; low mobility of lanthanum in aquatic systems.	High selectivity for phosphate; expensive but highly effective.	[477,478]
Activated Alumina	Adsorbs phosphate ions	High	High	Disposal of spent media can lead to aluminum leaching; moderate environmental risk.	High adsorption capacity; disposal of spent material needs careful handling.	[479,480]
Zeolites	Adsorbs ammonium and phosphate ions	Moderate	Moderate	Low risk; naturally occurring, can be reused.	Environmentally friendly, reusable, but with moderate phosphate removal capacity.	[481]
Ferric Sulfate	Forms insoluble ferric phosphate	High	Low	Can cause iron overload in aquatic systems; potential for acidification.	Similar to ferric chloride; potential for iron overload in treated waters.	[482]
Poly Aluminum Chloride	Forms insoluble aluminum phosphate	High	Moderate	Potential for aluminum accumulation in water bodies; moderate sludge production.	Effective at low pH, lower sludge volume compared to alum; risk of aluminum accumulation.	[483]
Chitosan	Binds with phosphate ions	Moderate	High	Biodegradable with low environmental impact; safe for aquatic life.	Biodegradable, but less effective at high phosphorus concentrations.	[484]
Biochar	Adsorbs phosphorus and nitrogen	Low to Moderate	Low	Carbon-neutral; potential for organic contaminants based on feedstock.	Sustainable, but effectiveness varies depending on feedstock and activation.	[485,486]
Lanthanum Chloride	Forms insoluble lanthanum phosphate	Very High	High	Low environmental risk; high selectivity for phosphate; stable in water.	Highly effective but expensive; mainly used in sensitive environments like lakes.	[487,488]
Iron(III) Chloride	Forms insoluble iron phosphate	High	Low	Potential for iron accumulation and acidification; can harm aquatic life.	Common and cost-effective; environmental risks include iron build-up.	[489,490]
Calcium Nitrate	Increases oxygen levels, reducing phosphorus release	Moderate	Moderate	Low risk; dual function in promoting plant growth and phosphate binding.	Dual function as both nutrient and phosphorus binder; environmentally safe.	[491,492]
Magnesium Hydroxide	Precipitates phosphate as magnesium phosphate	Moderate	Low	Minimal impact; can increase water pH, making it more alkaline.	Safe and cost-effective but limited by pH dependency.	[475,493]
Ferric Aluminum Sulfate	Forms insoluble phosphorus compounds	High	Moderate	Increased sludge production; potential iron and aluminum toxicity.	Combines benefits of ferric and alum salts; increased sludge production.	[472]
Sodium Sulfate	Forms insoluble sodium phosphate	Low	Low	Least effective; minimal direct environmental impact.	Least effective for phosphorus removal; often used in conjunction with other chemicals.	[494]

Table 27. Chemical reagents for phosphorus precipitation.

Chemical Treatment	Mechanism	Efficacy	Cost	Specific Environmental Impact	Considerations	Refs.
Aluminum Sulfate	Forms insoluble aluminum phosphate	High	Moderate	Potential aluminum toxicity to aquatic organisms; increases water acidity.	Effective at low pH; potential aluminum toxicity in aquatic environments.	[472,473]
Ferric Chloride	Forms insoluble ferric phosphate	High	Low	Iron accumulation in sediments; potential to lower pH significantly.	Effective across a wide pH range; can cause iron accumulation in sediments.	[474]
Calcium Hydroxide	Forms insoluble calcium phosphate	Moderate	Low	Minimal impact; may increase water hardness and pH.	Safe for the environment but less effective in cold temperatures.	[475,476]
Lanthanum-Modified Clay	Binds phosphate to form insoluble compound	Very High	High	Minimal environmental risks; low mobility of lanthanum in aquatic systems.	High selectivity for phosphate; expensive but highly effective.	[477,478]
Activated Alumina	Adsorbs phosphate ions	High	High	Disposal of spent media can lead to aluminum leaching; moderate environmental risk.	High adsorption capacity; disposal of spent material needs careful handling.	[479,480]
Zeolites	Adsorbs ammonium and phosphate ions	Moderate	Moderate	Low risk; naturally occurring, can be reused.	Environmentally friendly, reusable, but with moderate phosphate removal capacity.	[481]
Ferric Sulfate	Forms insoluble ferric phosphate	High	Low	Can cause iron overload in aquatic systems; potential for acidification.	Similar to ferric chloride; potential for iron overload in treated waters.	[482]
Poly Aluminum Chloride	Forms insoluble aluminum phosphate	High	Moderate	Potential for aluminum accumulation in water bodies; moderate sludge production.	Effective at low pH, lower sludge volume compared to alum; risk of aluminum accumulation.	[483]
Chitosan	Binds with phosphate ions	Moderate	High	Biodegradable with low environmental impact; safe for aquatic life.	Biodegradable, but less effective at high phosphorus concentrations.	[484]
Biochar	Adsorbs phosphorus and nitrogen	Low to Moderate	Low	Carbon-neutral; potential for organic contaminants based on feedstock.	Sustainable, but effectiveness varies depending on feedstock and activation.	[485,486]
Lanthanum Chloride	Forms insoluble lanthanum phosphate	Very High	High	Low environmental risk; high selectivity for phosphate; stable in water.	Highly effective but expensive; mainly used in sensitive environments like lakes.	[487,488]
Iron(III) Chloride	Forms insoluble iron phosphate	High	Low	Potential for iron accumulation and acidification; can harm aquatic life.	Common and cost-effective; environmental risks include iron build-up.	[489,490]
Calcium Nitrate	Increases oxygen levels, reducing phosphorus release	Moderate	Moderate	Low risk; dual function in promoting plant growth and phosphate binding.	Dual function as both nutrient and phosphorus binder; environmentally safe.	[491,492]
Magnesium Hydroxide	Precipitates phosphate as magnesium phosphate	Moderate	Low	Minimal impact; can increase water pH, making it more alkaline.	Safe and cost-effective but limited by pH dependency.	[475,493]
Ferric Aluminum Sulfate	Forms insoluble phosphorus compounds	High	Moderate	Increased sludge production; potential iron and aluminum toxicity.	Combines benefits of ferric and alum salts; increased sludge production.	[472]
Sodium Sulfate	Forms insoluble sodium phosphate	Low	Low	Least effective; minimal direct environmental impact.	Least effective for phosphorus removal; often used in conjunction with other chemicals.	[494]

5.2. Biological Treatments

Biological treatments for marine eutrophication involve utilizing living organisms or natural processes to mitigate nutrient levels and control algal blooms [495]. Key methods include biomanipulation, which adjusts aquatic food webs by enhancing populations of species like zooplankton that consume algae; bioaugmentation, which introduces specific nutrient-degrading microorganisms to reduce excess nutrients; and phytoremediation, involving plants like water hyacinth to absorb and remove nutrients (Table 28).

In practical applications, the three are usually used together to form constructed wetlands or floating treatment wetlands [496]. Constructed wetlands use engineered systems of plants and microorganisms to treat nutrient-rich waters; floating treatment wetlands deploy floating mats of plants to uptake nutrients from the water. These treatments are generally environmentally friendly and sustainable but require careful management and ongoing maintenance to ensure effectiveness and avoid ecological imbalances [497].

Table 28. Key methods for biological treatments for marine eutrophication.

Treatment	Mechanism	Advantages	Disadvantages	Refs.
Biomanipulation	Altering food web to control algae	Environmentally friendly; sustainable	Requires careful management; potential ecological imbalance	[498]
Bioaugmentation	Adding nutrient-degrading microorganisms	Effective in targeted applications; quick results	Potential introduction of non-native species; cost of microbes	[499,500]
Phytoremediation	Using plants to absorb nutrients	Cost-effective; easy to implement	Potential plant disposal issues; variable effectiveness	[501,502]

Table 28. Key methods for biological treatments for marine eutrophication.

Treatment	Mechanism	Advantages	Disadvantages	Refs.
Biomanipulation	Altering food web to control algae	Environmentally friendly; sustainable	Requires careful management; potential ecological imbalance	[498]
Bioaugmentation	Adding nutrient-degrading microorganisms	Effective in targeted applications; quick results	Potential introduction of non-native species; cost of microbes	[499,500]
Phytoremediation	Using plants to absorb nutrients	Cost-effective; easy to implement	Potential plant disposal issues; variable effectiveness	[501,502]

5.2.1. Biomanipulation

Biomanipulation aims to control algal blooms and reduce eutrophication by modifying the structure of the food web within an aquatic ecosystem [503]. The primary mechanism involves manipulating the populations of key species to indirectly control algal populations. This can be achieved through two main strategies: (1) enhancing populations of herbivorous zooplankton; (2) modifying fish populations. Biomanipulation leverages natural ecological interactions to manage eutrophication and algal blooms [498]. By manipulating the populations of zooplankton, fish, or aquatic plants, these methods aim to restore balance to the aquatic ecosystem, reduce nutrient levels, and improve water quality.

In marine ecosystems, biomanipulation to control eutrophic algae involves the introduction of specific fish and herbivorous zooplankton that naturally feed on algae, helping to maintain ecological balance and water quality [504]. Species such as rabbitfish, parrotfish, and surgeonfish are effective in coastal and reef environments, where they graze on various algae and seaweeds. Herbivorous zooplankton, including marine copepods, rotifers, cladocerans, and mysid shrimp, play a crucial role in consuming phytoplankton and maintaining water clarity in coastal and estuarine systems [505]. These organisms have been successfully used in diverse marine environments, such as the Red Sea, Caribbean Sea, Hawaiian Islands, and coastal waters of Norway and Japan, demonstrating their effectiveness in managing marine eutrophication through natural biological processes [506].

5.2.2. Bioaugmentation

Bioaugmentation involves the introduction of specific strains of microorganisms into an aquatic environment to enhance the degradation of pollutants, including excess nutrients like nitrogen and phosphorus, which contribute to eutrophication [499]. The mechanism relies on selecting and introducing bacteria, fungi, or algae known for their ability to metabolize and remove these nutrients from the water [507]. By augmenting the natural microbial community, bioaugmentation accelerates the breakdown and removal of these compounds, thereby mitigating eutrophication and controlling harmful algal blooms. Key bacteria include Pseudomonas, Bacillus, Nitrosomonas, Nitrobacter, Rhodobacter, and Alcaligenes (

Table 29. Bacteria used in bioaugmentation for marine eutrophication.

Bacteria	Mechanism	Usage Scenarios	Refs.
Pseudomonas	Degrades organic matter and assimilates nutrients	Used in nutrient-rich water bodies to reduce nitrogen and phosphorus levels	[508,509]
Bacillus	Breaks down organic matter and assimilates nutrients	Applied in coastal areas to mitigate nutrient pollution	[510,511]
Nitrosomonas	Converts ammonia to nitrite (nitrification)	Used in aquaculture and wastewater treatment to manage ammonia levels	[512,513]
Nitrobacter	Converts nitrite to nitrate (nitrification)	Applied in marine environments to complete the nitrification process	[514,515]
Rhodobacter	Uptakes and removes phosphorus	Utilized in phosphorus-rich environments to reduce eutrophication	[516,517]
Alcaligenes	Degrades organic pollutants and nutrients	Applied in wastewater treatment and coastal waters	[518]

).

5.2.3. Phytoremediation

Phytoremediation involves using plants and algae to remove, stabilize, or degrade pollutants from water bodies. In marine environments, certain aquatic plants and algae can uptake excess nutrients, such as nitrogen and phosphorus, which are the primary causes of eutrophication [519]. These organisms absorb these nutrients through their roots or fronds, incorporating them into their biomass, thereby reducing the nutrient levels in the water. The process also enhances oxygen production and provides habitats for marine life, contributing to overall ecosystem health. Phytoremediation utilizes various plants and algae to mitigate marine eutrophication by absorbing, accumulating, and degrading excess nutrients [520]. As shown in Table 30, species such as seagrasses, kelps, mangroves, saltmarsh plants, microalgae, and macroalgae have been effectively used in different marine environments. Seagrasses and saltmarsh plants are commonly used in shallow coastal and intertidal zones to enhance water quality and provide habitats, while kelps and macroalgae are effective in nutrient-rich coastal areas due to their high growth rates and nutrient absorption capacities [521]. Mangroves stabilize coastlines and improve sediment quality in tropical regions, though they grow slowly. Microalgae are suitable for controlled aquaculture settings due to their rapid nutrient uptake. Each species offers unique benefits and challenges, making phytoremediation a versatile yet complex approach to managing marine eutrophication [519].

Phytoremediation may cause allelopathy. Allelopathy refers to the release of chemicals by plants to affect the growth and development of other plants or microorganisms. During the phytoremediation process, plants will release some chemicals that may affect other plants and microorganisms in the surrounding environment. The allelopathic plants used in marine eutrophication control are summarized in Table 31. Phytoremediation for marine eutrophication often involves plants that exhibit allelopathic properties, releasing substances that inhibit algal growth. Key examples include Sargassum sp. [522], which produces phlorotannins and polysaccharides to reduce nutrient availability and alter the microenvironment, and Ulva lactuca [522,523], which releases ulvan to compete for nutrients and modify local conditions. Zostera marina and Cymodocea nodosa use terpenoids and phenolic compounds to affect light penetration and nutrient dynamics [524,525,526]. Other examples include Gracilaria sp. [527,528], which releases phycobiliproteins and polysaccharides, and Caulerpa sp. [529,530], which produces caulerpenyne and polysaccharides to inhibit algae. These plants use various mechanisms such as nutrient competition, chemical inhibition, and environmental modification to manage algal blooms and improve water quality in coastal and marine ecosystems.

Table 30. Phytoremediation species for marine eutrophication.

Species	Mechanism	Usage Scenarios	Advantages	Disadvantages	Refs.
Zostera marina	Uptake and store nutrients in their tissues	Effective in shallow coastal waters	Enhances biodiversity, provides habitats	Sensitive to water quality changes	[531]
Rhizophora spp.	Absorb nutrients through root systems, stabilize sediments	Suitable for intertidal zones	Stabilizes shorelines, reduces erosion	Requires large areas, slow growth	[532]
Spartina alterniflora	Uptake nutrients, improve sediment quality	Effective in estuarine and coastal environments	Improves water quality, supports diverse fauna	Limited to specific habitats	[533,534]
Ulva spp.	Rapidly uptake nutrients through fronds	Suitable for nutrient-rich coastal waters	Fast-growing, easy to harvest	Can become invasive, requires management	[535,536]
Chlorella spp.	Absorb nutrients through cellular uptake, can be cultured easily	Effective in controlled environments	High nutrient uptake efficiency, potential biofuel source	Requires controlled conditions, potential for algal blooms	[537,538]
Phaeodactylum tricornutum	Absorb nutrients through frustules	Suitable for controlled environments	High nutrient uptake, potential biofuel source	Requires specific cultivation conditions	[539]
Anabaena spp.	Fix nitrogen, uptake phosphorus	Effective in nutrient-rich environments	High growth rate, potential biofertilizer source	Can produce harmful toxins, needs careful management	[540,541]
Eichhornia crassipes	Uptake nutrients through roots and leaves	Effective in various water bodies	High biomass production, enhances water quality	Can become invasive, requires management	[542,543]
Laminaria spp.	Uptakes nutrients and provides habitats for marine life	Effective in temperate marine environments	High growth rates and nutrient absorption capacity	Requires attachment substrate	[544]

Table 30. Phytoremediation species for marine eutrophication.

Species	Mechanism	Usage Scenarios	Advantages	Disadvantages	Refs.
Zostera marina	Uptake and store nutrients in their tissues	Effective in shallow coastal waters	Enhances biodiversity, provides habitats	Sensitive to water quality changes	[531]
Rhizophora spp.	Absorb nutrients through root systems, stabilize sediments	Suitable for intertidal zones	Stabilizes shorelines, reduces erosion	Requires large areas, slow growth	[532]
Spartina alterniflora	Uptake nutrients, improve sediment quality	Effective in estuarine and coastal environments	Improves water quality, supports diverse fauna	Limited to specific habitats	[533,534]
Ulva spp.	Rapidly uptake nutrients through fronds	Suitable for nutrient-rich coastal waters	Fast-growing, easy to harvest	Can become invasive, requires management	[535,536]
Chlorella spp.	Absorb nutrients through cellular uptake, can be cultured easily	Effective in controlled environments	High nutrient uptake efficiency, potential biofuel source	Requires controlled conditions, potential for algal blooms	[537,538]
Phaeodactylum tricornutum	Absorb nutrients through frustules	Suitable for controlled environments	High nutrient uptake, potential biofuel source	Requires specific cultivation conditions	[539]
Anabaena spp.	Fix nitrogen, uptake phosphorus	Effective in nutrient-rich environments	High growth rate, potential biofertilizer source	Can produce harmful toxins, needs careful management	[540,541]
Eichhornia crassipes	Uptake nutrients through roots and leaves	Effective in various water bodies	High biomass production, enhances water quality	Can become invasive, requires management	[542,543]
Laminaria spp.	Uptakes nutrients and provides habitats for marine life	Effective in temperate marine environments	High growth rates and nutrient absorption capacity	Requires attachment substrate	[544]

Table 31. The allelopathic plants used in marine eutrophication control.

Plant	Allelopathic Substances	Habitat	Principle of Algae Removal	Refs.
Sargassum spp.	Phlorotannins, polysaccharides	Marine coastal areas, tropical and subtropical waters	Inhibits algal growth by reducing nutrient availability and altering the microenvironment.	[522]
Ulva spp.	Ulvan, polysaccharides	Coastal marine environments, intertidal zones	Competes for nutrients and modifies the local chemical environment.	[522,523]
Zostera marina	Terpenoids, phenolic compounds	Subtidal areas, seagrass meadows	Reduces light penetration and competes for nutrients.	[524,525]
Cymodocea nodosa	Phenolic compounds, saponins	Seagrass meadows, coastal regions	Alters nutrient availability and creates unfavorable growth conditions.	[526]
Gracilaria spp.	Phycobiliproteins, polysaccharides	Tropical and subtropical waters, coral reefs	Inhibits algae through nutrient competition and altering local chemical environment.	[527,528]
Padina spp.	Phlorotannins, polysaccharides	Tropical and subtropical marine environments	Reduces algal growth by competing for nutrients and releasing inhibitory substances.	[545]
Fucus vesiculosus	Phlorotannins, polysaccharides	Temperate coastal regions	Alters the nutrient dynamics and inhibits algal growth through chemical release.	[546]
Chaetomorpha spp.	Algal acids, polysaccharides	Coastal and estuarine environments	Competes for nutrients and modifies the chemical environment to inhibit algal growth.	[547]
Ruppia maritima	Phenolic compounds, flavonoids	Shallow coastal and estuarine waters	Reduces nutrient availability and light penetration, affecting algae growth.	[548,549,550]
Caulerpa spp.	Caulerpenyne, polysaccharides	Tropical and subtropical marine environments	Competes for space and nutrients and releases toxins that inhibit algae.	[529,530]
Syringodium isoetifolium	Terpenoids, flavonoids	Seagrass meadows, coastal waters	Reduces nutrient availability and light penetration, inhibiting algae growth.	[551,552]
Enteromorpha spp.	Ulvan, phenolic compounds	Coastal and estuarine environments	Competes for nutrients and releases inhibitory substances affecting algae.	[523,553]
Corallina spp.	Calcified polysaccharides, phenolics	Coral reefs, rocky intertidal zones	Alters the chemical environment and reduces nutrient availability to inhibit algae.	[522]
Laminaria spp.	Fucoidan, phlorotannins	Temperate coastal areas, kelp forests	Reduces nutrient levels and alters the microenvironment to inhibit algal growth.	[554,555]

Table 31. The allelopathic plants used in marine eutrophication control.

Plant	Allelopathic Substances	Habitat	Principle of Algae Removal	Refs.
Sargassum spp.	Phlorotannins, polysaccharides	Marine coastal areas, tropical and subtropical waters	Inhibits algal growth by reducing nutrient availability and altering the microenvironment.	[522]
Ulva spp.	Ulvan, polysaccharides	Coastal marine environments, intertidal zones	Competes for nutrients and modifies the local chemical environment.	[522,523]
Zostera marina	Terpenoids, phenolic compounds	Subtidal areas, seagrass meadows	Reduces light penetration and competes for nutrients.	[524,525]
Cymodocea nodosa	Phenolic compounds, saponins	Seagrass meadows, coastal regions	Alters nutrient availability and creates unfavorable growth conditions.	[526]
Gracilaria spp.	Phycobiliproteins, polysaccharides	Tropical and subtropical waters, coral reefs	Inhibits algae through nutrient competition and altering local chemical environment.	[527,528]
Padina spp.	Phlorotannins, polysaccharides	Tropical and subtropical marine environments	Reduces algal growth by competing for nutrients and releasing inhibitory substances.	[545]
Fucus vesiculosus	Phlorotannins, polysaccharides	Temperate coastal regions	Alters the nutrient dynamics and inhibits algal growth through chemical release.	[546]
Chaetomorpha spp.	Algal acids, polysaccharides	Coastal and estuarine environments	Competes for nutrients and modifies the chemical environment to inhibit algal growth.	[547]
Ruppia maritima	Phenolic compounds, flavonoids	Shallow coastal and estuarine waters	Reduces nutrient availability and light penetration, affecting algae growth.	[548,549,550]
Caulerpa spp.	Caulerpenyne, polysaccharides	Tropical and subtropical marine environments	Competes for space and nutrients and releases toxins that inhibit algae.	[529,530]
Syringodium isoetifolium	Terpenoids, flavonoids	Seagrass meadows, coastal waters	Reduces nutrient availability and light penetration, inhibiting algae growth.	[551,552]
Enteromorpha spp.	Ulvan, phenolic compounds	Coastal and estuarine environments	Competes for nutrients and releases inhibitory substances affecting algae.	[523,553]
Corallina spp.	Calcified polysaccharides, phenolics	Coral reefs, rocky intertidal zones	Alters the chemical environment and reduces nutrient availability to inhibit algae.	[522]
Laminaria spp.	Fucoidan, phlorotannins	Temperate coastal areas, kelp forests	Reduces nutrient levels and alters the microenvironment to inhibit algal growth.	[554,555]

5.3. Physical Treatments

Physical treatments for marine eutrophication involve mechanical, hydrological, or structural methods to remove or mitigate excess nutrients and restore water quality [556]. These treatments typically aim to physically remove nutrient-rich sediments, control water flow, or introduce oxygen into the water. Physical treatments for marine eutrophication involve various mechanical and structural methods to manage excess nutrients and restore water quality [557]. As shown in

Table 32. Physical treatments for marine eutrophication.

Treatment	Mechanism	Usage Scenarios	Advantages	Disadvantages	Refs.
Dredging	Removes nutrient-rich sediments	Effective in areas with significant sediment buildup	Immediate reduction in internal nutrient loading	Expensive, disrupts benthic habitats	[558,562]
Aeration and Oxygenation	Introduces oxygen to enhance aerobic conditions and reduce nutrient release	Suitable for lakes, ponds, and enclosed coastal areas	Improves oxygen levels and water quality	Requires continuous operation and energy input	[559,563]
Flushing	Increases water circulation to dilute and remove nutrients	Effective in enclosed or semi-enclosed water bodies	Reduces nutrient concentrations and improves water movement	Dependent on tidal or external water sources	[560]
Constructed Wetlands	Filters and absorbs nutrients through plant uptake and sedimentation	Suitable for nutrient runoff areas	Provides habitats and improves water quality	Requires large areas and ongoing maintenance	[564,565]
Barriers and Curtains	Prevents spread of nutrients and algal blooms	Effective in localized bloom control	Immediate containment of algal blooms	Limited to small, contained areas	[566]
Sediment Capping	Covers nutrient-rich sediments with inert material to prevent nutrient release	Suitable for areas with high nutrient sediment loads	Prevents nutrient release and improves water quality	Can be expensive, may require repeated applications	[567,568]

, dredging removes nutrient-rich sediments, significantly reducing internal nutrient loading, but can be costly and disruptive to benthic habitats [558]. Aeration and oxygenation improve oxygen levels in hypoxic waters, promoting aerobic conditions and reducing nutrient release from sediments, though they require continuous energy input [559]. Flushing enhances water circulation, diluting nutrient concentrations and improving water movement, but depends on tidal or external water sources [560]. Constructed wetlands filter and absorb nutrients through plant uptake and sedimentation, providing habitats and improving water quality, but require large areas and ongoing maintenance. Barriers and curtains prevent the spread of nutrients and algal blooms, offering immediate containment, but are limited to small, contained areas. Sediment capping involves covering nutrient-rich sediments with an inert material, preventing nutrient release and improving water quality, but can be expensive and may need repeated applications. Each physical treatment has its advantages and limitations, making them suitable for different scenarios and degrees of eutrophication [561].

Sediment capping is a widely used physical treatment to control nutrient release from sediments and mitigate marine eutrophication [567,568,569]. Common materials used for sediment capping include sand, clay (e.g., bentonite), geotextiles, activated carbon, alum, and Phoslock (lanthanum-modified clay). Each of these materials has its own effectiveness and risks. For instance, sand is a basic and cost-effective capping material, but it may require frequent replenishment due to erosion. Clay offers a more stable, long-term barrier against nutrient release but can be disturbed by bioturbation. Geotextiles reinforce sediment caps, enhancing stability and reducing the need for frequent maintenance, while activated carbon is effective at adsorbing contaminants but may lose efficacy over time as it becomes saturated.

However, the application of sediment capping is not without risks. Repeated applications may be necessary due to erosion or disturbances, increasing the overall cost. Some materials, such as alum and Phoslock, can alter water chemistry, potentially leading to unintended environmental consequences like changes in pH or the release of other contaminants. The long-term stability of sediment caps can also be compromised by natural processes such as sedimentation and biological activity, which may necessitate ongoing monitoring and maintenance.

In summary, while sediment capping is an effective strategy for controlling nutrient release and managing eutrophication, it requires careful consideration of the materials used and the specific conditions of the water body. The choice of material should balance effectiveness, cost, and potential environmental impact to ensure sustainable long-term management.

5.4. Constructed Wetlands

Constructed wetlands are engineered systems designed to mimic natural wetland processes for treating various types of water pollution, including marine eutrophication [570,571]. The mechanisms underlying their effectiveness in treating marine eutrophication typically involve physical, chemical, and biological processes, including the following: (1) Physical processes: Constructed wetlands use the physical structure of wetland plants and substrates (soil or gravel) to slow down the flow of water. This allows suspended solids to settle, reducing turbidity and sedimentation. In the context of marine eutrophication, this helps trap organic matter and nutrients like nitrogen and phosphorus [464]. (2) Chemical processes: Wetland plants and their associated microorganisms facilitate chemical processes such as adsorption, precipitation, and ion exchange. These processes can help to remove or transform nutrients and pollutants. For instance, certain plants and bacteria can uptake and store nutrients like nitrogen and phosphorus, reducing their availability in the water column. (3) Biological processes: Microorganisms in the wetland substrate play a crucial role in breaking down organic matter through processes like decomposition and mineralization [572]. This degradation process consumes oxygen, creating an anaerobic (low oxygen) environment in parts of the wetland where denitrification can occur. Denitrification converts nitrate (NO₃⁻) to nitrogen gas (N₂), which is released harmlessly into the atmosphere, thereby reducing nitrogen levels in the water.

Constructed wetlands are employed to manage marine eutrophication through various technologies, each utilizing specific plant species. For instance, subsurface flow wetlands with Phragmites australis and Typha angustifolia are used in coastal regions of China and the USA [573,574,575,576], while surface flow wetlands with Scirpus validus and Juncus effusus are found in Europe and Australia [577]. Hybrid wetlands combining Carex spp. and Cyperus papyrus are used in North America and Europe [578,579]. Vertical flow wetlands with Canna indica and Phragmites australis are prevalent in Asia and the Mediterranean [580,581]. Free water surface wetlands using Eichhornia crassipes and Lemna minor are utilized in tropical regions [582,583], whereas constructed mangrove wetlands with Avicennia marina and Rhizophora stylosa are implemented in Southeast Asia and northern Australia [584,585]. Additionally, constructed seagrass beds with Zostera marina and Thalassia testudinum are present in the Mediterranean and Caribbean coasts [586]. Each system is tailored to its regional context to effectively reduce nutrient loads and manage eutrophication. Examples of constructed wetlands used in the management of marine eutrophication are shown in

Table 33. Examples of constructed wetlands used in the management of marine eutrophication.

Technology Used	Main Species Involved	Location	Refs.
Subsurface Flow Wetlands	Phragmites australis, Typha angustifolia	Coastal areas in China and the USA	[573,574,575,576]
Surface Flow Wetlands	Scirpus validus, Juncus effusus	Coastal regions in Europe, Australia	[577]
Hybrid Wetlands	Carex spp., Cyperus papyrus	Coastal regions in North America and Europe	[578,579]
Vertical Flow Wetlands	Canna indica, Phragmites australis	Coastal areas in Asia and the Mediterranean	[580,581]
Free Water Surface Wetlands	Eichhornia crassipes, Lemna minor	Tropical and subtropical regions worldwide	[582,583]
Constructed Mangrove Wetlands	Avicennia marina, Rhizophora stylosa	Southeast Asia and Northern Australia	[584,585]
Constructed Seagrass Beds	Zostera marina, Thalassia testudinum	Mediterranean and Caribbean coastal regions	[586]

.

5.5. Advanced Technologies

Advanced technologies for addressing marine eutrophication leverage cutting-edge methods to target and mitigate nutrient pollution and restore ecological balance, including nano-technology, electrocoagulation, and advanced oxidation processes (

Table 34. Advanced technologies for marine eutrophication.

Technology	Mechanism	Advantages	Disadvantages	Refs.
Nano-technology	Uses nanoparticles to target and adsorb nutrients	High precision in targeting specific contaminants	Potential ecological risks, high cost	[588,589]
Electrocoagulation	Uses electrical currents to coagulate and remove suspended particles	Effective in removing a wide range of contaminants	High energy consumption, maintenance requirements	[590,591,592]
Ultrasonic Treatment	Disrupts algal cells using high-frequency sound waves	Non-chemical, prevents algal bloom formation	Limited to small areas, high initial setup cost	[593,594]
Advanced Oxidation Processes	Uses strong oxidants to degrade organic pollutants and reduce nutrient levels	Effective in degrading a wide range of pollutants	High operational cost, potential formation of by-products	[595]

) [587]. Nano-technology employs nanoparticles to precisely target and remove specific contaminants, offering high precision but with potential ecological risks and high costs. Biochar adsorbs nutrients from water through specially processed organic material, providing a sustainable and long-term solution for nutrient binding but requiring large quantities and posing a risk of nutrient re-release. Electrocoagulation uses electrical currents to coagulate and remove suspended particles, effective for a wide range of contaminants but with high energy consumption and maintenance needs. Ultrasonic treatment disrupts algal cells with high-frequency sound waves, preventing bloom formation without chemicals, though it is limited to small areas and involves high initial costs. Robotic systems utilize autonomous or remotely operated vehicles for precise monitoring and treatment, ideal for coastal monitoring and inaccessible areas, but are costly and require advanced technical infrastructure. Advanced oxidation processes (AOPs) deploy strong oxidants to degrade organic pollutants and reduce nutrient levels, effective for a broad range of pollutants but with high operational costs and potential by-product formation. Each advanced technology offers unique benefits and challenges, making them suitable for various scenarios and degrees of eutrophication.

5.6. Resource Processing of Algae

Before algae cells can be used as resources, they need to be collected. Algae collection technologies from HABs encompass a range of methods, each designed to effectively remove and process algae from aquatic environments [596]. Mechanical harvesting provides immediate physical removal, while chemical flocculation aggregates algae for easier extraction. Algae resource technologies focus on transforming the collected algal biomass into valuable products while minimizing environmental impacts [597]. Methods like thermophilic fermentation and anaerobic digestion convert algae into renewable energy sources such as biogas, while pyrolysis produces bio-oil and biochar, both of which contribute to energy production and carbon sequestration (

Table 35. Summary of algae resource conversion technologies from HABs.

Method	Advantages	Disadvantages	Product after Treatment	Function of the Product	Refs.
Biological Treatment	Eco-friendly, can selectively target harmful species	Slow process, needs specific environmental conditions	Biogas, organic fertilizers	Renewable energy, nutrient recycling	[598,599]
Thermophilic Fermentation	High energy yield, effective pathogen destruction	Requires controlled conditions, infrastructure investment	Biogas, biochar	Renewable energy, soil enhancement	[600,601]
Dewatering and Drying	Simple technology, reduces volume of algae	Energy-intensive, potential loss of nutrients	Dried algae powder	Animal feed, fertilizer additive	[602]
Pyrolysis	Converts algae into energy-rich products, reduces biomass	High temperature requirement, complex setup	Bio-oil, biochar	Renewable energy, carbon sequestration	[603,604]
Anaerobic Digestion	Converts algae to biogas, reduces odor	Requires pretreatment, slow process	Biogas, digestate	Renewable energy, soil conditioner	[605]

). Mechanical dewatering and drying processes reduce the algae’s water content, facilitating its use as animal feed or fertilizer. These technologies not only offer solutions for managing algae blooms but also create opportunities for sustainable energy and resource recovery.

5.7. Comparison of Treatments for Eutrophic Oceans

The advantages and disadvantages of various treatments for eutrophic marine systems vary significantly in terms of cost and sustainability. Physical treatments offer immediate results but are expensive and unsustainable due to ongoing maintenance needs. Chemical treatments provide quick nutrient reduction but are temporary and potentially harmful, with low sustainability. This comparison highlights the need to balance effectiveness, cost, and long-term environmental impact when selecting a treatment for eutrophic marine conditions. Bioaugmentation enhances microbial diversity and is moderately sustainable but requires careful monitoring. Biomanipulation uses natural predators and is highly sustainable but complex and slow to show results. Constructed wetlands and phytoremediation are more natural and sustainable approaches; wetlands enhance biodiversity but need significant land and time, while phytoremediation is cost-effective but slower. Nano-technology is highly precise and effective but also costly and carries potential ecological risks. Electrocoagulation is effective and relatively fast but requires high energy and maintenance, with moderate sustainability. Advanced oxidation processes are highly efficient but come with high costs and the risk of harmful by-products, making them moderately sustainable (

Table 36. Comparison of treatments for eutrophic oceans.

Treatment	Advantages	Disadvantages	Cost	Sustainability
Physical Treatments	Immediate results, effective at removing algae and debris	High operational and maintenance costs, short-term solution	High	Low (temporary solution)
Nano-technology	High precision, effective at targeting specific contaminants	Potential ecological risks, high cost, limited large-scale application	Very High	Moderate (potential risks)
Electrocoagulation	Effective for a wide range of contaminants, relatively fast	High energy consumption, maintenance requirements, potential chemical by-products	High	Moderate
Advanced Oxidation	Effective in degrading various pollutants, non-selective	High operational cost, potential formation of harmful by-products	Very High	Moderate (risk of by-products)
Constructed Wetlands	Natural, sustainable, enhances biodiversity	Requires large land area, long establishment time	Moderate	High (long-term benefits)
Phytoremediation	Natural, cost-effective, enhances habitat	Limited to certain types of contaminants, slow process	Low to Moderate	High (natural process)
Bioaugmentation	Targets specific contaminants, enhances microbial diversity	Potential for non-native species introduction, monitoring required	Moderate	Moderate to High
Biomanipulation	Enhances ecosystem balance, uses natural predators	Complex to manage, slow process	Low to Moderate	High (natural balance)
Chemical Treatments	Fast-acting, effective for immediate nutrient reduction	Potential toxic effects, temporary solution, repeated applications needed	Low to Moderate	Low (temporary and potentially harmful)

).

An integrated approach to managing marine eutrophication combines multiple strategies to effectively address the complex and multifaceted nature of this environmental issue. This approach involves a combination of monitoring, prevention, and remediation techniques tailored to specific environmental contexts.

(1)

Comprehensive Monitoring Systems

Implement integrated monitoring systems that combine remote sensing for large-scale, real-time data with localized in situ measurements for detailed analysis [606]. dPCR can be used for precise detection of specific harmful algae species and toxin genes, allowing for early detection and rapid response to HABs. For example, the Baltic Sea, a region heavily impacted by eutrophication, utilizes a combination of remote sensing, in situ water sampling, and digital PCR (dPCR) for monitoring nutrient levels, phytoplankton biomass, and HABs.

(2)

Nutrient Management Practices

Employ best management practices (BMPs) alongside innovative nutrient management techniques, such as slow-release fertilizers or mixed organo-mineral fertilizers, to minimize nutrient inputs from agriculture [607]. In urban areas, enhancing wastewater treatment facilities to remove nitrogen and phosphorus before discharge into marine systems is crucial [608]. For example, in the Chesapeake Bay, the implementation of agricultural BMPs such as riparian buffer zones, cover cropping, and controlled fertilizer application has significantly reduced nutrient runoff.

(3)

Physical and Chemical Treatment Methods

Combine sediment capping with other methods, such as hypolimnetic oxygenation (oxygenation of bottom waters) or aeration, to prevent nutrient release from sediments [556]. Physical methods like dredging might be used in areas with severe sediment contamination, followed by capping to prevent recontamination. For example, in the Swan River Estuary, Australia, Phoslock (lanthanum-modified clay) has been used to cap sediments and bind phosphorus, reducing its availability for algal growth.

(4)

Ecosystem Restoration and Biomanipulation

Restore and protect coastal wetlands and seagrass beds, which act as natural nutrient filters, and provide habitats for species that can outcompete harmful algae [504]. In some cases, biomanipulation, such as the introduction of filter-feeding organisms like mussels, can help control algal populations. For example, in Lake Taihu, China, wetland restoration and the reintroduction of native aquatic vegetation have been implemented to absorb excess nutrients and reduce algal blooms.

An effective integrated approach to managing marine eutrophication involves combining advanced monitoring techniques with targeted nutrient management, physical and chemical remediation methods, ecosystem restoration, and strong policy frameworks. The specific combination of strategies will depend on the environmental context, including the sources of nutrients, the characteristics of the affected marine system, and the socio-economic conditions of the region.

6. Conclusions

Marine eutrophication, driven primarily by excessive inputs of nutrients such as nitrogen and phosphorus, has led to the proliferation of HABs across various coastal ecosystems. These blooms present significant ecological, economic, and public health risks. Effective monitoring is critical for predicting and managing HAB outbreaks. Technologies such as remote sensing, automated in situ sensors, and advanced modeling and forecasting play essential roles in early detection and real-time monitoring of HABs. Each of these methods has distinct advantages and limitations concerning cost, effectiveness, sustainability, and ecological impact, highlighting the need for a balanced approach to monitoring and management.

Addressing marine eutrophication also necessitates overcoming technical thresholds and exploring future research directions. One major challenge involves optimizing nutrient removal technologies to enhance their precision and efficiency while minimizing environmental impacts. Current methods, such as chemical precipitation and sediment capping, require advancements to better target nitrogen and phosphorus. Innovations in nanotechnology and advanced materials offer potential solutions for more effective nutrient capture and reduced need for repeated interventions.

The scalability of bioremediation techniques is another critical challenge. Although the use of specific microorganisms or engineered algae shows promise, scaling these methods while avoiding unintended ecological consequences remains a hurdle. Future research should focus on genetic engineering and synthetic biology to develop organisms capable of efficient and safe nutrient remediation on a larger scale. Additionally, closed-loop systems should be explored to prevent these organisms from escaping into the broader environment.

Further progress in remote sensing and monitoring technologies is needed to achieve higher resolution and accuracy. While hyperspectral cameras and satellite-based sensors have improved real-time monitoring capabilities, more localized and detailed data are essential for immediate management decisions. Integrating these tools with automated response systems could facilitate rapid interventions to prevent or mitigate eutrophic conditions.

A crucial future research direction is the development of integrated management frameworks that combine various treatment approaches into a cohesive, adaptive strategy. Such frameworks should consider the specific ecological, socio-economic, and geographical contexts of the affected regions, ensuring that interventions are both effective and sustainable. This may involve integrating nutrient source control measures, in situ remediation techniques, and long-term ecosystem restoration efforts. Adaptive management systems must be designed to respond flexibly to changing environmental conditions, including the impacts of climate change, which are expected to exacerbate eutrophication problems.

Sustainability must be integral to the selection and implementation of monitoring and treatment methods for marine eutrophication. Adopting ecosystem-based management practices, utilizing low-impact and energy-efficient technologies, and involving stakeholders are key to ensuring social and cultural acceptability. Emphasis should be placed on supporting biodiversity, using biodegradable materials, and minimizing secondary pollution to achieve sustainable outcomes. Continuous and adaptive monitoring is essential for adjusting interventions based on evolving environmental conditions, ensuring their long-term effectiveness.

In summary, effectively addressing marine eutrophication involves overcoming significant technical challenges, particularly in nutrient removal efficiency, bioremediation scalability, and monitoring accuracy. Future research should focus on these critical areas while developing integrated, adaptive management frameworks. This comprehensive approach will enhance our capacity to manage eutrophication and support the long-term health and sustainability of marine ecosystems.