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Methods to control harmful algal blooms: a review

Article in Environmental Chemistry Letters June 2022
環境化學通訊》上的文章 2022 年 6 月
DOI: 10.1007/s10311-022-01457-2
7 authors, including: 7 位作者,包括
Balaji Prasath Barathan 巴拉吉-普拉薩特-巴拉坦
Bharathidasan University
16 篇著作 155 次引用
Yong Zhang 張勇
College of Environmental Science and Engineering
33 篇著作 352 次引用

Methods to control harmful algal blooms: a review

Barathan Balaji-Prasath Ying Wang Yu Ping Su - David P. Hamilton Hong Lin Luwei Zheng
巴拉坦-巴拉吉-普拉薩特 王穎蘇玉萍- David P. Hamilton林虹鄭路偉
Yong Zhang  張勇

Received: 3 February 2022 / Accepted: 27 April 2022
收到:2022 年 2 月 3 日 / 接受:2022 年 4 月 27 日收到:2022 年 2 月 3 日 / 接受:2022 年 4 月 27 日
(c) The Author(s), under exclusive licence to Springer Nature Switzerland AG 2022
(c) 作者獨家授權施普林格-自然瑞士股份公司 2022 年

Abstract 摘要

The recent rise of red tide harmful algal blooms has induced ecosystem degradation, economic losses, and aquaculture damage, yet little is known on prevention and mitigation of red tides. Actual control methods involve physical, chemical, and biological processes, with varying success. Here, we review physical, chemical, and biological control methods applicable to red tide species in marine and estuarine water bodies. We discuss mechanisms of algal blooms outbreak and their applications to prevent outbreaks.

Keywords Algae bloom Algicide Dinoflagellate Red tide
關鍵字 藻華 殺藻劑 {{1}甲藻 {{2}紅潮

Introduction 導言

Harmful algal blooms emerge as "red tides" of algal cells that change the color of surface water with their red or brown pigmentation. Proliferations of microalgae in marine or brackish waters can cause fish kills, contaminate seafood with toxins, and alter ecosystems in ways humans perceive as harmful. Harmful algal blooms also cause water quality to deteriorate, making it unsuitable for potable water use (e.g., via desalination), as well as industrial use (Panagopoulos 2021, 2022). A broad classification of harmful algal blooms distinguishes two groups of organisms: the toxin producers, which can contaminate seafood or kill fish, and the high-biomass producers, which can cause anoxia and indiscriminately kill marine life in dense concentrations. Some harmful algal blooms have characteristics of both
有害藻類的大量繁殖表現為藻類細胞的 "紅潮",它們的紅色或棕色色素改變了地表水的顏色。海洋或鹹水中的微藻類大量繁殖會導致魚類死亡,使海鮮受到毒素污染,並以人類認為有害的方式改變生態系統。有害藻類大量繁殖也會導致水質惡化,使其不適合飲用水(如透過海水淡化)和工業用水(Panagopoulos,2021 年,2022 年)。有害藻華的大致分類將生物分為兩類:一類是毒素生成者,它們會污染海鮮或殺死魚類;另一類是高生物量生成者,它們會導致缺氧,並在密集的情況下不加區分地殺死海洋生物。有些有害藻華同時具有以下兩種特徵
Yu Ping Su
1 College of Environmental Science and Engineering, Fujian Normal University, Fuzhou 350007, People's Republic of China
1 福建師範大學環境科學與工程學院,中華人民共和國福州 350007
2 Fujian Key Laboratory of Pollution Control and Resource Recycling, Fuzhou 350007, People's Republic of China
2 福建省污染控制與資源循環利用重點實驗室,中華人民共和國福州 350007
3 Fujian Key Laboratory of Special Marine Bio-Resources Sustainable Utilization-Fujian Normal University, Fujian, China
3 福建省特種海洋生物資源永續利用重點實驗室-福建師範大學,福建,中國
4 Australian Rivers Institute, Griffith University, Nathan, QLD 4111, Australia
4 澳洲格里菲斯大學澳洲河流研究所,澳洲昆士蘭州內森 4111

(Du et al. 2017; Hu et al. 2018; Zohdi and Abbaspour 2019; Hallegraeff et al. 2021). Although the best-known harmful algal blooms phenomenon is the so-called red tide, it is not the only harmful algal blooms type, and others have caused damage to fisheries, threatened the coastal environment, and even harmed human health (Inaba et al. 2017; Kouakou and Poder 2019; Belin et al. 2021).
(Du 等人,2017 年;Hu 等人,2018 年;Zohdi 和 Abbaspour,2019 年;Hallegraeff 等人,2021 年)。雖然最著名的有害藻華現像是所謂的赤潮,但它並不是唯一的有害藻華類型,其他類型的藻華也對漁業造成了破壞,威脅了沿海環境,甚至損害了人類健康(Inaba 等, 2017 年;Kouakou 與Poder,2019 年;Belin 等,2021 年)。
There are about 300 species of phytoplankton that cause harmful algal blooms, although it should be noted that only a quarter of these are deemed harmful. Approximately 50% of the algal blooms species are dinoflagellates, and many of the more toxic species have a complex life cycle (Huang et al. 2018). Over the past few decades, many studies have been conducted to classify the organisms that cause harmful algal blooms and consider the effects of the outbreaks (Liu et al. 2013; Suzuki 2016; Wang et al. 2016; Sakamoto et al. 2021; Zingone et al. 2020) and sea coloration changes vary depending on the species of phytoplankton involved, such as from, common algal blooms species such as Karenia mikimotoi, Prorocentrum minimum, Karlodinium veneficum, Levanderina fissa, Chattonella antiqua, Heterosigma akashiwo, and Alexandrium catenella (Isabel et al. 2018). These species are usually poisonous and are also known to kill farmed fish in large numbers. The blooms commonly occur in coastal ecosystems, but they can also occur in the open sea, brackish water, or freshwater ecosystems (Anderson et al. 2012; Sunesen et al. 2021).
造成有害藻華的浮游植物約有 300 種,但需要注意的是,其中只有四分之一被認為是有害的。約 50%的藻華物種是甲藻,許多毒性較強的物種具有複雜的生命週期(Huang 等,2018 年)。在過去幾十年中,許多研究對引起有害藻華的生物進行了分類,並考慮了藻華爆發的影響(Liu 等,2013 年;Suzuki,2016 年;Wang 等,2016 年;Sakamoto 等,2021年;Zingone 等,2020 年)。 2020),海水顏色的變化因涉及的浮游植物種類而異,如來自Karenia mikimotoi、Prorocentrum minimum、Karlodinium v​​eneficum、Levanderina fissa、Chattonella antiqua、Heterosigma akashiwo 和Alexandrium catenella 等常見,2018 年),2018 年) 。這些物種通常有毒,已知會導致大量養殖魚類死亡。藻華通常發生在沿海生態系中,但也可能發生在公海、鹹水或淡水生態系(Anderson 等,2012 年;Sunesen 等,2021 年)。
In recent decades, scientists have made a concerted effort to prevent harmful algal blooms and mitigate the damage

by employing several methods to kill harmful species and suppress harmful algal blooms formation. Although trials of these methods suggest that harmful algal blooms are often preventable, algal blooms develop in areas that may cover many hundreds of square kilometers. Furthermore, there is potential for adverse secondary effects related to other components of the ecosystem, and for legacy pollution from persistent effects of algicides. This paper focuses on current harmful algal blooms control measures to limit their occurrence and remove toxins from the water column. Several studies concerning the development of strategies for controlling harmful algal blooms (Yang et al. 2015a, b; Yu et al. 2017) support these measures, which can be classified into three methods-physical (Lu et al. 2016; Tian et al. 2014; Zhang et al. 2018a, b), chemical (Baek et al. 2013, 2014; Wu et al. 2014; Yang et al. 2015a, b), and biological (Cai et al. 2016; Garces et al. 2013; Lee et al. 2015; Pokrzywinski et al. 2017; Sun et al. 2017, 2018; Wang et al. 2017; Zhang et al. 2018a, b; Shang et al. 2020; Zhang et al. 2020; BalajiPrasath et al. 2022).
採用多種方法殺死有害物種,抑制有害藻華的形成。儘管對這些方法的試驗表明,有害藻華通常是可以預防的,但藻華發生的區域可能覆蓋數百平方千米。此外,藻華也可能對生態系的其他組成部分產生不利的次要影響,以及殺藻劑的持久性影響造成的遺留污染。本文重點介紹目前的有害藻華控制措施,以限制其發生並清除水體中的毒素。有關有害藻華控制策略發展的多項研究(Yang 等,2015a,b;Yu 等,2017)支持這些措施,這些措施可分為三種方法--物理方法(Lu 等,2016;Tian 等,2014 ;Zhang 等,2018a,b)、化學方法(Baek 等,2013,2014;Wu 等,2018a,b)。 2013,2014;Wu 等人,2014;Yang 等人,2015a,b)和生物方法(Cai 等人,2016;Garces 等人,2013;Lee 等人,2015;Pokrzywinski 等人,2017;Sun 等人, 2017,2018;Wang 等人,2017;Zhang 等人,2018a,b;Shang 等人,2020;Zhang 等人,2020;BalajiPrasath 等人,2022)。
However, because of adverse ecological effects, high cost, or poor field operability, the application of most approaches is admittedly limited. As a result, few methods for dealing with harmful algal blooms damage can be administered on a large scale in the field; therefore, multiple measuresincluding physical, chemical, and biological methods-need to be considered. In the following systematic review, we propose that the current methodology for harmful algal blooms control needs further clarification through more thorough observation and prediction.

Physical methods 物理方法

For classification purposes, methods such as air pumping, magnetic separation, centrifugal separation, and ultrasonic destruction will be considered physical processes. If the volume of algal blooms-affected water to treat is limited, physical treatment can offer some containment; however, it should be considered a preventative measure rather than a control measure. An example of physical treatment is pumping seawater through a centrifugal separator to remove Karenia mikimotoi, Gyrodinium sp. and Cochlodinium polykirkoides (Cearace 2007). The centrifugal separator has attracted much attention because it avoids chemical controls. A magnetic separation method uses mechanical power and a mixture of iron oxide and chloride powder to separate, an effective method for removing red tide plankton. It then pumps the seawater through a magnetic separator to remove harmful algal blooms plankton. This method has proven to be effective for removing Chattonella sp. from the seawater column and is effective for small harmful algal blooms.
就分類而言,氣泵、磁分離、離心分離和超音波破壞等方法將被視為物理過程。如果需要處理的受藻華影響的水量有限,物理處理可以提供一定的遏製作用;但應將其視為預防措施而非控制措施。物理處理的一個例子是用離心分離器抽取海水,以去除 Karenia mikimotoi、Gyrodinium sp.和 Cochlodinium polykirkoides(Cearace,2007 年)。離心分離器避免了化學控制,因此備受關注。磁力分離法利用機械動力和氧化鐵與氯化物粉末的混合物分離,是去除紅潮浮游生物的有效方法。然後將海水抽入磁性分離器,去除有害的藻華浮游生物。事實證明,這種方法能有效清除海水中的 Chattonella sp.

Another proposed algal blooms control method is to use ultraviolet radiation. Chattonella marina was killed with radiation for , while other harmful algal blooms species, such as . akashiwo, and K. mikimotoi, were killed at lower ultraviolet radiation dose (Cearace 2007). As found in a study by Li et al. (2018), UV irradiation can induce damage in microalgal cells on multiple levels, including adverse effects on nucleic acids, light harvesting through electron transfer, nitrogen fixation and assimilation, toxin synthesis, settle ability, oxidative pressure, antioxidative capacity, and overall cell integrity. An air extraction method introduces fine bubbles into harmful algal blooms so that microbubbles adhere to the algae and cause the plankton to float to the surface for removal. This physical control method allows the separation of fish and harmful algal blooms by providing oxygen in the form of fine bubbles to prevent fish hypoxia. However, its application may be limited where there are extensive harmful algal blooms that require very large mechanical bubblers. Dispersed air bubbles are formed when air is introduced into the system and vigorously agitated, or when airflow is continuously passed through certain porous materials. These air bubbles become highly buoyant when they interact with negatively charged microalgae cells and the cells can be readily collected at the water surface (Zhan et al. 2021).
另一種控制藻華的方法是使用紫外線輻射。在輻射 下, 的藻類被殺死,而 等其他有害藻類則被殺死。而其他有害藻華物種,如 .akashiwo 和 K. mikimotoi,在較低的紫外線輻射劑量下就會被殺死(Cearace,2007 年)。 Li 等人(2018 年)的研究發現,紫外線照射會對微藻細胞造成多層面的損傷,包括對核酸、透過電子傳遞的光收集、固氮和同化作用、毒素合成、沉降能力、氧化壓力、抗氧化能力和整體細胞完整性產生不利影響。空氣萃取法將細小氣泡引入有害藻類繁殖區,使微氣泡附著在藻類上,使浮游生物浮出水面,以便清除。這種物理控制方法透過以微小氣泡的形式提供氧氣,防止魚類缺氧,從而將魚類和有害藻華分離開來。不過,在有害藻類大量繁殖,需要使用大型機械氣泡器的地方,這種方法的應用可能會受到限制。將空氣引入系統並大力攪拌,或氣流持續通過某些多孔材料時,就會形成分散的氣泡。當這些氣泡與帶負電荷的微藻細胞相互作用時,就會產生很強的浮力,細胞很容易被收集到水面上(Zhan 等,2021 年)。
Ultrasonication is another method that applies sound waves to the water column to generate a cyclic expansion and compression phase leading to vibration that affects algae buoyancy and causes cells to sink to the bottom of the water column. The use of ultrasound is being promoted for harmful algal blooms control by some distributors of ultrasound equipment. Research and reviews have been carried out overseas on ultrasound (Lürling and Tolman 2014; Ohtani 2003). These devices are purported to produce collapse of gas vesicles and inhibit photosynthesis in harmful algal blooms, with lysis and damage of cells. The most authoritative and scientifically based research on ultrasound indicates, however, that it is highly unlikely to have any control effect on harmful algal blooms in natural systems unless extremely high-intensity ultrasound is applied within a very small body of water. Such high-intensity ultrasound has been found to kill zooplankton grazers (Ohtani 2003) and could potentially affect fish populations and behavior. Because they cannot photosynthesize, the algal blooms does not reform.
超音波是另一種方法,它將聲波應用於水體,產生循環膨脹和壓縮階段,從而產生振動,影響藻類浮力,使細胞沉入水體底部。一些超音波設備經銷商正在推廣使用超音波來控制有害藻華。國外對超音波進行了研究和評論(Lürling 和 Tolman,2014 年;Ohtani,2003 年)。據稱,這些設備能使有害藻華的氣泡崩潰並抑制光合作用,同時裂解和破壞細胞。不過,最權威、最有科學依據的超音波研究表明,除非在極小的水體中使用極高強度的超音波,否則超音波不太可能對自然系統中的有害藻華產生任何控制效果。研究發現,這種高強度的超音波會殺死浮游動物中的食草動物(Ohtani,2003 年),並可能影響魚類的數量和行為。由於它們無法進行光合作用,藻華也無法恢復。
In the future, the frequency, power, and exposure time used to control algal blooms of different initial densities in different types of water bodies should be examined. This effort could improve treatment efficiency and reduce energy consumption. At the same time, the impact of ultrasound on water quality, other aquatic organisms, and the release of algal toxins from bloom-forming algae should remain of concern (Park et al. 2017). Most physical methods are slow and expensive, so they are challenging to use for large
今後,應研究用於控制不同類型水體中不同初始密度藻華的頻率、功率和照射時間。這樣做可以提高處理效率,降低能耗。同時,超音波對水質、其他水生生物以及藻華形成藻類毒素釋放的影響仍應引起關注(Park 等,2017 年)。大多數物理方法既緩慢又昂貴,因此在大型水處理中使用這些方法具有挑戰性。

blooms. Moreover, physical methods are not always practical, so they are primarily used as algal blooms emergency measures rather than as a preventative strategy. Due to limited field experience with physical methods of harmful algal blooms mitigation, there is limited information about the cost and impact.

Chemical methods 化學方法

The well-established and most promising mitigation strategy against harmful algal blooms that is classified as a chemical method is coagulated flocculation. Most harmful algal blooms control research has focused on flocculation using different clays (Lu et al. 2015). Many studies have been conducted to explore the viability of using charged beach sand/ sediments (Li and Pan 2013; Pan et al. 2011), biopolymers, and other naturally occurring substances, such as chitosan, as flocculants (Burns et al. 2009). The bonding process induces flocculation and then uses the flocculant to precipitate biopolymers. This process creates larger harmful algal blooms plankton aggregates that are easier to separate. Process control is important to produce coagulated flocculation and sedimentation simultaneously, i.e., a physicochemical process.
混凝絮凝法是一種行之有效、最有前景的緩解有害藻華的化學方法。大多數有害藻華控制研究都專注於使用不同黏土進行絮凝(Lu 等人,2015 年)。許多研究都在探索使用帶電海灘沙/沉積物(Li 和Pan,2013 年;Pan 等人,2011 年)、生物聚合物和其他天然物質(如殼聚醣)作為絮凝劑的可行性(Burns 等人,2009 年)。黏合過程會誘發絮凝,然後利用絮凝劑沉澱生物聚合物。此過程可產生較大的有害藻華浮游生物聚集體,且較容易分離。製程控制對於同時產生混凝絮凝和沈澱(即物理化學過程)非常重要。
The consequences of chemical algaecides lingering in water environments and their effects on human health should also be considered. Due to the widespread application of chemical algaecides, some of those that enter the algae cells eventually remain in the water. To minimize potential harm to human health and aquatic environments, chemical algaecides should be selected with special consideration of their potential toxicity to other organisms and ability to release minimal residue into the environment. The chemical nature of the matrix also determines the adhesion process of the target harmful algal blooms species. For further reference, the Derjaguin-Landau-Verwey-Overbeek theory describes the forces between two charged surfaces in a liquid medium. In this theory, two main interactions, the Lifshitz-van der Waals (attractive) and the electrostatic (repulsive) interactions explain the overall interaction between a cell and a substrate (Nabweteme et al. 2015).
也應考慮化學除藻劑在水環境中的殘留後果及其對人類健康的影響。由於化學除藻劑的廣泛應用,一些進入藻類細胞的化學除藻劑最終會殘留在水中。為了盡量減少對人類健康和水生環境的潛在危害,在選擇化學除藻劑時應特別考慮其對其他生物的潛在毒性以及向環境中釋放最少殘留物的能力。基質的化學性質也決定了目標有害藻華物種的附著過程。作為進一步參考,Derjaguin-Landau-Verwey-Overbeek 理論描述了液體介質中兩個帶電錶面之間的作用力。在該理論中,兩種主要的相互作用,即Lifshitz-van der Waals(吸引力)和靜電(排斥力)相互作用,解釋了細胞與基質之間的整體相互作用(Nabweteme 等人,2015 年) 。

Flocculation 絮凝

Clay flocculation to mitigate harmful algal blooms has also been studied and applied to coastal waters. Flocculants are added to water to create a "floc," which removes particles by binding and condensing them together; the resulting floc then promotes the rapid sinking of the aggregate, including algal blooms species, to the seafloor (Shirota 1989; Yu et al. 1994). This technique is convenient for field applications (Park et al. 2013). On the other hand, natural clays have low coagulation efficiency and poor flexibility, which can result in large deposition loads on the sediments, which may cause risks to benthic marine life due to the size of clay particles, their zeta potential and potential for smothering (Padilla et al. 2010). Therefore, efforts to identify newer and more productive clay modifiers that produce less secondary pollution (Pan et al. 2011) are still needed. Cell surfaces may change over time, resulting in a decrease in flocculation efficiency. At present the only obvious and fully effective measure to control harmful algal blooms in the ocean is to use clay to induce flocculation (Shirota 1989).
人們也研究了黏土絮凝法,並將其應用於沿海水域,以減輕有害藻華。在水中添加絮凝劑可形成"絮凝體",透過將顆粒結合併凝結在一起來去除顆粒;由此產生的絮凝體可促進包括藻華物種在內的集合體快速沉入海底(Shirota,1989 年;Yu 等,1994 年)。這種技術便於實地應用(Park 等人,2013 年)。另一方面,天然黏土的凝結效率低、柔韌性差,可能會在沉積物上造成較大的沉積負荷,由於黏土顆粒的大小、zeta 電位和窒息潛能,可能會對底棲海洋生物造成傷害(Padilla等,2010 年)。因此,仍需努力尋找更新、更有效的黏土改質劑,以減少二次污染(Pan 等,2011 年)。細胞表面可能會隨時間變化,導致絮凝效率下降。目前,控制海洋中有害藻類大量繁殖的唯一明顯且完全有效的措施是使用黏土誘導絮凝(Shirota,1989 年)。

Modified clays 改性黏土

Many studies have shown that modified clay produces cationic hydrolysis products that suppress growth of algal blooms cells in two ways-through direct action from collisions inducing cell flocculation and through indirect mechanisms that remove soluble nutrients or lead to shading (Balaji-Prasath et al. 2021a). Modified clay technology has been widely used in Southeast Asia for over two decades because of its favorable characteristics, such as being nontoxic, inexpensive, and controlling harmful algal blooms et al. 2016; Yu et al. 2017). Notably, some researchers have found that this technique inhibits the germination of cysts (Wang et al. 2014). Cyst germination is a critical factor in the formation of harmful algal blooms, so modified clay may provide a means for prolonged reduction in harmful algal blooms and minimizing environmental impacts.
許多研究表明,改性粘土產生的陽離子水解產物可通過兩種方式抑制藻華細胞的生長--通過碰撞誘導細胞絮凝的直接作用和通過去除可溶性營養物質或導致遮光的間接機制(Balaji-Prasath 等,2021a)。二十多年來,改性黏土技術因其無毒、廉價、可控制有害藻類大量繁殖等優點在東南亞得到了廣泛應用 等人,2016;Yu等人,2017)。值得注意的是,一些研究人員發現這種技術會抑制包囊的發芽(Wang 等人,2014 年)。孢囊萌發是形成有害藻華的關鍵因素,因此改性黏土可能為長期減少有害藻華和最大限度地減少對環境的影響提供了一種手段。
Recent research has explored the viability of using sand, natural polymers, and other naturally occurring substances as flocculants. This newly developed strategy improves the harmful algal blooms removal efficiency and reduces the amount of clay used. Clay mixed with poly aluminum chloride, calcium hydroxide, and chitosan reduced the required clay loading by fivefold (Sengco et al. 2005; Song et al. 2010). As an additive for clay dispersion, cationic poly aluminum chloride, or chitosan, plays a role in bridging and promoting particle formation. Pan et al (2011) found that removing harmful algal blooms species using poly aluminum chloride/chitosan modified sand was significantly enhanced. However, the efficacy of sand/local soil is reduced in marine systems due to increased salinity in seawater. When soil particles are altered through a bi-component mechanism of surface charge and network bridge modification using biodegradable modifiers (e.g., Moringa oleifera and chitosan), a higher algal blooms removal rate can be achieved (Li and Pan 2013).
最近的研究探討了使用沙子、天然聚合物和其他天然物質作為絮凝劑的可行性。這種新開發的策略提高了去除有害藻華的效率,並減少了黏土的用量。與聚合氯化鋁、氫氧化鈣和殼聚醣混合的黏土可將所需的黏土用量減少五倍(Sengco 等人,2005 年;Song 等人,2010 年)。作為粘土分散的添加劑,陽離子聚合氯化鋁或殼聚醣在架橋和促進顆粒形成方面發揮作用。 Pan 等人(2011 年)發現,使用聚合氯化鋁/殼聚醣改質砂去除有害藻華物種的效果顯著增強。然而,在海洋系統中,由於海水鹽度增加,沙子/當地土壤的功效會降低。當使用生物可降解改質劑(如Moringa oleifera 和殼聚醣)透過表面電荷和網橋改性的雙組分機制改變土壤顆粒時,可實現更高的藻華去除率(Li 和Pan,2013年)。
Secondary metabolites of other natural substances from plants, such as glycoside, polyphenol, polysaccharide, terpene, flavone, and alkaloid, are ecologically safe and biodegradable; they could also be potential resources for new modifiers that make sand or clay more efficient for algal

blooms mitigation (Nabweteme et al. 2015). Although few investigators have identified the source of algal blooms inhibitory effects from traditional Chinese herb-modified clay, this low-cost measure also has negligible environmental impacts (Tian et al. 2014). Different benign types of clay also provide options for controlling harmful algal blooms (Zhou et al. 2007). Table 1 summarizes different modified clays that have been developed to control red tide harmful algal blooms.
Nabweteme 等人,2015 年)。雖然很少有研究人員確定了傳統中草藥改質黏土抑制藻華的作用來源,但這種低成本措施對環境的影響也可以忽略不計(Tian 等,2014 年)。不同類型的良性黏土也為控制有害藻華提供了選擇(Zhou 等,2007 年)。表 1 總結了為控制赤潮有害藻華而開發的不同改質黏土。

Surfactants 界面活性劑

Surfactants are surface-active compounds that reduce the surface tension and interfacial tension between liquids, solids, and gases (Wang et al. 2017). Two types of surfactants have been tested as algicides: chemically synthesized (synthetic) and those produced by microorganisms (biosurfactants). Ideally, surfactants containing clay could act synergistically to improve algae removal efficiency. Cocamidopropyl betaine, a synthetic surfactant, has removal efficiency of A. tamarense, while Gemini surfactants (ethylene bis (dodecyl dimethyl ammonium bromide) exhibited the highest removal rate of Chattonella marina, with removal rate close to (Wang et al. 2017). According to Sun et al. (2004a, b), bio-surfactants are highly biodegradable in natural seawater. For example, sophorolipids and rhamnolipids are a group of glycolipids produced by microbes that have high biodegradability and ecological acceptability (Haba et al. 2000; Wang et al. 2005). Bi-component modification of sophorolipid-yellow clay mixture has removal efficiency on marine plankton (Liu 2016).
界面活性劑是一種界面活性化合物,可降低液體、固體和氣體之間的表面張力和界面張力(Wang 等人,2017 年)。有兩類界面活性劑曾經作為殺藻劑進行測試:化學合成的界面活性劑(合成界面活性劑)和微生物產生的界面活性劑(生物表面活性劑)。理想情況下,含有黏土的界面活性劑可發揮協同作用,提高除藻效率。合成界面活性劑椰油醯胺丙基甜菜鹼對塔瑪琳藻的去除率為 ,而Gemini 界面活性劑(乙烯雙(十二烷基二甲基溴化銨))對海洋水蚤的去除率最高,接近 。 (Wang 等人,2017 年)。根據 Sun 等人(2004a, b)的研究,生物界面活性劑在天然海水中具有很高的生物降解性。例如,sophorolipids 和 rhamnolipids 是一類由微生物產生的醣脂,具有很高的生物降解性和生態可接受性(Haba 等,2000 年;Wang 等,2005 年)。雙組分改質槐脂-黃色黏土混合物對海洋浮游生物具有 的去除效率(Liu,2016 年)。
The bio-surfactant affects the clay particles' chemical affinity, resulting in higher binding rates and improved cell removal ability. Bio-surfactants show promising algicidal effects and biodegradation efficiency. However, the modification of clays with surfactants (Gemini, Cocamidopropyl betaine, rhamnolipid, sophorolipid) or flocculants (poly aluminum chloride) can improve cell removal rate and reduce the required clay concentration by an order of magnitude or so (Lee et al. 2008; Wang et al. 2017; Wu et al. 2010).
生物界面活性劑會影響黏土顆粒的化學親和力,從而提高結合率和細胞去除能力。生物表面活性劑具有良好的殺藻效果和生物降解效率。然而,使用界面活性劑(Gemini、椰油酰胺丙基甜菜鹼、鼠李醣脂、槐脂)或絮凝劑(聚合氯化鋁)改性黏土可以提高細胞去除率,並將所需的黏土濃度降低一個數量級左右(Lee 等,2008 年;Wang 等,2017 年;Wu 等,2010 年)。

Cationic substances for algicidal efficacy

The cationic particles of biodegradable materials loaded with algicides may significantly enhance algicidal effect. Usually, the algal cell wall is made up of glycocalyx and a plasma membrane. However, most of the dinoflagellate cell wall consists of thick cellulosic thecal plates (Bogus et al. 2014), making identifying the algicidal agent difficult. However, plasma membranes have an amphipathic character and can interact electrically with the surface of cationic liposomes and peptides delivered through the cell wall. They combat algal blooms species through membrane penetration and affect the chloroplast membrane containing sulfoquinothiodiacyl glycerol and phosphatidyl glycerol (Gibbs 1981).
可生物降解材料的陽離子顆粒負載殺藻劑,可顯著增強殺藻效果。通常,藻細胞壁由糖萼和質膜組成。然而,大多數甲藻細胞壁都由厚厚的纖維素鈣板組成(Bogus 等人,2014 年),因此很難識別殺藻劑。不過,質膜具有兩親性,可與透過細胞壁輸送的陽離子脂質體和勝肽表面產生電相互作用。它們透過膜滲透對抗藻華物種,並影響含有磺基喹硫基甘油和磷脂酰甘油的葉綠體膜(Gibbs,1981 年)。
Additionally, cationic substances damage negatively charged lipids (Park et al. 2011). Thus, they represent a promising avenue of research for maximizing algicidal efficiency. Research has identified that cationic peptides HPA 3 and Helicobacter pylori-derived synthetic antimicrobial peptide work against . akashiwo and . marina by causing pore formation in the plasma membrane (Park et al. 2011). Harmful algal blooms cells motility destroys the plasma membrane and induces the outflow of intracellular components. Other studies show that a designer liposome delivery system for TD53 (1,2-dimyristoyl-sn-glycerol 3-phosphocholine) improves its delivery and efficacy against algal blooms species such as . marina, . akashiwo, and C. polykrikoides (Han et al. 2011).
此外,陽離子物質會破壞帶負電荷的脂質(Park 等人,2011 年)。因此,它們是最大限度提高殺藻效率的一個有前景的研究途徑。研究發現,陽離子勝肽HPA 3 和幽門螺旋桿菌衍生的合成抗菌肽對 .akashiwo 和 .akashiwo 和 marina 起作用,因為它們會在質膜上形成孔隙(Park 等人,2011 年)。有害藻華細胞的移動會破壞質膜,誘導細胞內成分外流。其他研究表明,為TD53 設計的脂質體遞送系統(1,2-二肉荳蔻基-sn-甘油-3-磷酸膽鹼)提高了其遞送能力和對藻華物種(如 ..marina、 .akashiwo 和C. polykrikoides(Han 等人,2011 年)。
Novel and natural cationic polymeric flocculants grafted from quaternary ammonium monomer -(3-chloro-2-hydroxypropyl) trimethylammonium chloride are also effective at removing A. tamarense. Studies show that cationic modified flocculants reduce the adverse effects of harmful algal blooms in seawater (Cho et al. 2016; Pang et al. 2013) have encapsulated cationic liposomes in a new algicide, dichlorophenyl)methyl] cyclohexylamine (DP92). Electrostatic interaction between the negatively charged cell walls of harmful algal blooms and DP92 facilitates electrostatic interaction. Four synthetic peptides such as Del, Hn-Mc-DRW, and Hn-Mc-DWR variants have a robust inhibitory effect on marine algae that may be suitable for marine ecosystems (Park et al. 2016).
由季銨鹽單體 -(3-氯-2-羥基丙基三甲基氯化銨)接枝而成的新型天然陽離子聚合物絮凝劑也能有效去除金龜子。 -(3-氯-2-羥基丙基)三甲基氯化銨也能有效去除金目藻。研究表明,陽離子改質絮凝劑可減少海水中有害藻類大量繁殖的不利影響(Cho 等人,2016 年;Pang 等人,2013 年)。有害藻類帶負電荷的細胞壁與 DP92 之間的靜電相互作用促進了靜電作用。四種合成勝肽,如 Del、Hn-Mc-DRW 和 Hn-Mc-DWR 變體對海洋藻類有很強的抑製作用,可能適用於海洋生態系(Park 等,2016 年)。
Modified clay algicides induce the lysis of harmful algal blooms in two ways. One is direct action through collisions and flocculation with target cells, followed by sedimentation and death (Saxena and Harish 2018). The second is through indirect mechanisms that remove soluble nutrients (e.g., phosphate), and reduces the light available for photosynthesis. Oxidative stress occurs via the overproduction of reactive oxygen species and significantly damages or alters the function and structure of target cells (Park et al. 2011). Modified clay effectiveness is enhanced with certain chemicals or biomolecules used for flocculation enhancement, such as cations, surfactants, coagulants, and biopolymers, which act as a bridge between cells. This bridging effect produces progressively larger flocs that increase the 'net' effect and sedimentation rate.
改質黏土殺藻劑透過兩種方式誘導有害藻類大量繁殖。一種是透過與目標細胞的碰撞和絮凝直接作用,然後沉澱和死亡(Saxena 和 Harish,2018 年)。第二種是透過間接機制去除可溶性營養物質(如磷酸鹽),並減少光合作用所需的光照。氧化壓力透過過度產生活性氧而發生,並嚴重損害或改變目標細胞的功能和結構(Park 等,2011 年)。使用某些用於增強絮凝效果的化學物質或生物分子(如陽離子、界面活性劑、凝結劑和生物聚合物)可增強改質黏土的效果,這些化學物質或生物分子在細胞之間起到橋樑作用。這種橋接效應可產生逐漸增大的絮團,從而提高 "淨 "效應和沈降速度。

Engineered nanoparticles

Recent advances in engineered nanoparticles have led to the development a series of nanomaterials with algicidal properties. It is well known that engineered nanoparticles can
Table 1 Modified clays used to remove red-tide harmful algal blooms
表 1 用於清除赤潮有害藻華的改質黏土
Tested algal bloom species
time 時間
Inhibition rate 抑制率 Modified clay 改性黏土 References 參考資料
Inorganic modified clays
Skeletonema costatum, and
Skeletonema costatum,以及
Olisthodiscus . Olisthodiscus ..
Acid-treated modified clay-
modified clay 改性黏土
Maruyama et al. (1987)
丸山等人(1987 年)
Phaeocystis globosa and 球囊藻和
Aureococcus anophagef-
ferens 渡鴉
44.6 and  44.6 和
Aluminum sulfate-modified
clay; 粘土;
Aluminum chloride-modified
clay; 粘土;
Poly aluminum chloride-mod-
ified clay 倘泥
Liu (2016), Liu et al. (2016)
Liu(2016),Liu 等人(2016)
Heterosigma akashiwo and
Heterosigma akashiwo 和
Alexandrium tamarense 檉柳
Mixed Metal Layered Hydrox-
ide Positive Electrosol-mod-
ified clay; 粘土;
Polysilicate metal salt-modi-
fied clay 
Sun et al.  Sun et al.
costatum, H. akashiwo and
costatum、H. akashiwo和
A. tamarense
Poly aluminum chloride-mod-
ified clay 黏土
Yu et al. (2006)
Yu 等人(2006 年)
Prorocentrum minimum - -
Poly aluminum chloride- 聚合氯化鋁
modified clay 改性黏土
Yu et al. (1999)
Yu 等人(1999 年)
Organic modified clays 有機改質黏土
Prorocentrum donghaiense
H. akashiwo
Cetyltrimethylammonium 十六烷基三甲基銨
bromide-modified clay 溴改質粘土
Cao (2004), Cao et al. (2004)
Cao(2004),Cao 等人(2004)
P. donghaiense
bromide-modifiedclay 溴化改質粘土
Cao and  曹和
P. globosa
Dodecyl dimethyl benzyl 十二烷基二甲基芐基
ammonium bromide-modi- 溴化銨
fied clay; 粘土;
Cetyltrimethylammonium 十六烷基三甲基銨
bromide-modified clay 溴改質粘土
Amphidinium carterae, Amphidinium carterae、
Scrippsiella trochoidea, P.
donghaiense, H. akashiwo
90 to  90 到
Dialkyl polyoxyethylene 二烷基聚氧乙烯
triquat-modified clay; 三酸酯改性粘土;
Trialkyl polyoxyethylene
triquat-modified clay; 三酸酯改性粘土;
C8 alkyl polyglycoside quater-
C8 烷基聚醣苷季化合物
nary ammonium salt-modi-
fied clay; 粘土;
C12 alkyl polyglycoside C12 烷基聚醣苷
quaternary ammonium salt-
modified clay 改性黏土
Song et al. (2003)
宋等人(2003 年)
Composite modified clays
P. globosa
85 to  85 到
chloride-modified clay; 氯化改質粘土;
Polydimethyldiallyl ammo-
nium chloride/polyaluminum
chloride-modified clay; 氯化改質粘土;
Cetyltrimethylammonium 十六烷基三甲基銨
bromide/polyaluminum chlo-
ride-modified clay; 改性粘土;
Dodecyl dimethyl benzyl 十二烷基二甲基芐基
ammonium bromide/polya- 溴化銨/聚亞安酯
luminum chloride-modified
clay 黏土
Liu (2016)
S. trochoidea, A. carterae and  
Sodium salt/poly 鈉鹽/聚
aluminum salt-modified clay
Song et al. (2003)
宋等人(2003 年)
Synthetic Surfactant 合成界面活性劑
A. tamarense
Cocamidopropyl betaine- 椰油醯胺丙基甜菜鹼
modified clay 改性黏土
Liu et al. (2016)
Liu 等人(2016 年)
Table 1 (continued) 表 1(續)
Tested algal bloom species
time 時間
Inhibition rate 抑制率 Modified clay 改性黏土 References 參考資料
Chattonella marina 沼澤鱂
Ethylene bis (dodecyl dime-
thyl ammonium bromide)- 乙基溴化銨)-
modified clay 改性黏土
Wang et al. (2017)
Biosurfactant 生物表面活性劑
Cochlodinium polykrikoides
clay 黏土
Lee et al. (2008)
李等人(2008 年)
The clays are considered in terms of harmful algal bloom species impacted, concentration and cultivation time (i.e., exposure to the clay), inhibition rate, the name of the modified clay, and relevant references
induce cell stress through the formation of reactive oxygen species (ROS), causing damage to organelles, high rates of consumption of nutrients, and reduced rates of photosynthesis (Saxena and Harish 2018). Different nanomaterials have been used in titanium dioxide, zinc oxide, cerium oxide, coral-like structured barium titanate, yttrium oxide, and aluminum oxide; these have all proven to be effective algicides. The phytoplankton cell wall comprises protein, polysaccharide, and uric acid and has high adhesion to engineered nanoparticles. Functional groups present on the cell wall form a negatively charged surface, enhancing the electrostatic attraction with positively charged engineered nanoparticles (Chen et al. 2019). The enormous surface area of engineered nanoparticles improves cell entrapment while reducing nutrient uptake and photosynthesis of cells (Li et al. 2015a, b; Li et al. 2018).
透過形成活性氧(ROS)誘導細胞應激,導致細胞器受損、營養物質消耗率高以及光合作用速率降低(Saxena 和 Harish,2018 年)。不同的奈米材料已被用於二氧化鈦、氧化鋅、氧化鈰、珊瑚狀結構的鈦酸鋇、氧化釔和氧化鋁;這些都被證明是有效的殺藻劑。浮游植物細胞壁由蛋白質、多醣體和尿酸組成,對工程奈米粒子有很高的附著力。細胞壁上的官能基形成帶負電的表面,增強了與帶正電的工程奈米粒子的靜電吸引(Chen 等,2019 年)。工程奈米粒子巨大的表面積提高了細胞吸附能力,同時降低了細胞的營養吸收和光合作用(Li 等人,2015a, b;Li 等人,2018)。
Chiu et al. showed that marine phytoplankton responds to different engineered nanoparticles through the calcium signaling pathway (Chiu et al. 2017). Minor changes in intracellular levels in the presence of nanomaterialinduced toxicity causes phytoplankton mortality, but the mechanisms are not yet fully understood (Kadar et al. 2012). Different dinoflagellate species need to be studied further, especially those that produce the harmful algal blooms, and this requires detailed physiological responses for the mitigation of blooms in the field (Li et al. 2018). Although very few types of engineered nanoparticles have been developed and used in laboratory experiments, the results for algal blooms removal are encouraging (Table 2). Risk assessment studies are required to better understand the efficacy of engineered nanoparticles for mitigating harmful algal blooms.
Chiu等人的研究表明,海洋浮游植物透過鈣信號通路 對不同的工程奈米粒子做出反應(Chiu等人,2017)。 (Chiu等人,2017)。在奈米材料誘導的毒性作用下,細胞內 水平的微小變化會導致浮游植物死亡,但其機制尚未完全明了(Kadar等人,2012)。需要進一步研究不同的甲藻種類,尤其是那些產生有害藻華的甲藻,這需要詳細的生理反應,以便在現場緩解藻華(Li 等人,2018 年)。儘管已開發並在實驗室實驗中使用的工程奈米粒子種類很少,但用於清除藻華的結果令人鼓舞(表 2)。需要進行風險評估研究,以便更好地了解工程奈米粒子在緩解有害藻華的功效。

Algicidal chemicals 殺菌劑

Use of algicidal chemicals is a standard method for mitigation and control of harmful algal blooms, but limitations exist due to toxicity to other aquatic organisms (Grattan et al. 2016). Therefore, significant efforts have been made to identify new chemical compounds that are environmentally friendly and specifically target harmful algae (Anderson 2009). Chemical oxidants such as ozone, chlorine, permanganate, copper sulfate, sodium hypochlorite, and hydrogen peroxide are often used for the inactivation of harmful algal blooms (Ebenezer et al. 2014). Use of ozone has proven effective for the inactivation of different algal species such as K. brevis, Amphidinium sp. and C. polykrikoides (Oemcke and Hans van Leeuwen 2005; Schneider et al. 2003; Shin et al. 2017). Ozone has been shown to rapidly oxidize ten different algal blooms species through lipid peroxidation and cell membrane rupture (Ebenezer and Ki 2013) and disruption of gene structure. Ozone has been effective in the laboratory and was also recently recommended for treatments of ship ballast water.
使用殺藻化學物質是緩解和控制有害藻華的標準方法,但由於對其他水生生物具有毒性,因此存在局限性(Grattan 等人,2016 年)。因此,人們一直在努力尋找既環保又能專門針對有害藻類的新型化合物(Anderson,2009 年)。臭氧、氯、高錳酸鹽、硫酸銅、次氯酸鈉和過氧化氫等化學氧化劑經常被用於滅活有害藻類(Ebenezer 等,2014 年)。事實證明,臭氧可有效滅活不同種類的藻類,如 K. brevis、Amphidinium sp.和 C. polykrikoides(Oemcke 和 Hans van Leeuwen,2005 年;Schneider 等人,2003 年;Shin 等人,2017 年)。研究表明,臭氧可透過脂質過氧化、細胞膜破裂(Ebenezer 和 Ki,2013 年)和基因結構破壞,迅速氧化十種不同的藻華物種。臭氧在實驗室中效果顯著,最近也被推薦用於處理船舶壓艙水。
Moreover, recent studies have also demonstrated that when tiny ozone bubbles called "nanobubbles" burst in the water, they produce hydroxyl radicals and peroxides, so ozone levels must be carefully monitored for effects on marine life. Many of the results with ozone were delineated
此外,最近的研究還表明,當被稱為 "奈米氣泡 "的微小臭氧氣泡在水中破裂時,會產生羥基自由基和過氧化物,因此必須仔細監測臭氧濃度對海洋生物的影響。許多與臭氧有關的結果都被描述為
Table 2 Engineered nanoparticles used to remove red tide harmful algal blooms species
表 2 用於清除赤潮有害藻華的工程奈米顆粒 物種
Engineered nanoparticles
Tested HAB cells 經測試的 HAB 細胞
time 時間
Inhibition rate 抑制率 References 參考資料
Titanium dioxide 二氧化鈦 Karenia brevis 卡倫氏菌 Li et al. (2015a, b)
Titanium dioxide 二氧化鈦 A. tamarense - Li et al. (2018)
Silver nanoparticles 銀奈米粒子 P. minimum P. 最低限度 Butz et al. (2019)
Zinc oxide 氧化鋅 A. tamarense Castro-Bugallo et al. (2014)
Castro-Bugallo 等人(2014 年)
Yttrium(III) oxide 氧化釔(III) A. tamarense Castro-Bugallo et al. (2014)
Castro-Bugallo 等人(2014 年)
in regional reports but have not been recorded in international academic articles. The oxidative biocide chlorine produces a marked physiological and biochemical response in P. minimum (Ebenezer and Ki 2013) sodium hypochlorite and copper sulfate, when used as algicides, may significantly inhibit the growth, metabolism, and photosynthesis of algae, destroy the plasma membrane of cells, and produce reactive oxygen species. They are also highly effective in removing C. polykrikoides by promoting cell stress (Ebenezer et al. 2014).
但在國際學術文章中還沒有記錄。次氯酸鈉和硫酸銅用作殺藻劑時,可顯著抑制藻類的生長、新陳代謝和光合作用,破壞細胞質膜,並產生活性氧。它們還能透過促進細胞壓力反應來高效去除多殺藻類(Ebenezer 等人,2014 年)。
Copper sulfate is considered too expensive to control marine harmful algal blooms and is toxic to many marine organisms so is not considered further here. Kwon et al. found that 1,4 naphthoquinone with benzothiazole derivatives is a potent inhibitor of . akashiwo and . polykrikoides (Kwon et al. 2013) Thiazolidinediones, also called glitazones, have shown potent algicidal activity of species such as . circularisquama, C. marina, H. akashiwo, and C. polykrikoides (Baek et al. 2012, 2014). In photosynthetic organisms, the compound locks electron transfer in photosystem II though its exact mode of action is not fully clear (Kim et al. 2010). Because the compound is hydrophobic, it may damage the cell membrane, including the thylakoid membrane structure, resulting in photosynthetic damage and cell lysis (Baek et al. 2012, 2013, 2014; Kim et al. 2010, 2012).
硫酸銅被認為在控制海洋有害藻華方面過於昂貴,對許多海洋生物有毒,因此在此不再贅述。 Kwon 等人發現,含有苯並噻唑衍生物的 1,4-萘醌對 .akashiwo 和 ..polykrikoides(Kwon 等人,2013 年)。噻唑烷二酮類,又稱格列酮類,對 ..circularisquama、C. marina、H. akashiwo 和 C. polykrikoides(Baek 等人,2012 年,2014 年)。在光合生物中,該化合物可鎖定光合系統 II 中的電子傳遞,但其確切的作用模式尚不完全清楚(Kim 等,2010 年)。由於該化合物具有疏水性,它可能會破壞細胞膜,包括類木質膜結構,導致光合作用損傷和細胞溶解(Baek 等人,2012 年、2013 年、2014 年;Kim 等人,2010 年、2012 年) 。
Different chemical compounds have been developed and used in experiments involving the removal of various types of harmful algal blooms cells (Table 3). The mechanism by which chemical algicides induce the cell lysis. The algicide most probably ruptures or is transferred through the cell wall and cell membrane by specific transporters, and then enters the cytoplasm and encounters organelles, including chloroplasts, the endoplasmic reticulum, and mitochondria. This process stimulates the overproduction of reactive oxygen species (Ebenezer and Ki 2013). Strong oxidants like ozone increase levels reactive oxygen species within cells, interfering with cell function and resulting in cell lysis (Zhang et al. 2003). Hydroxyl radicals and hydrogen peroxide are reactive oxygen species that are by-products of photosynthesis and respiration. Hydroxyl radicals and oxygen can produce hydroxide, a highly damaging reactive oxygen species. The excess reactive oxygen species activities of antioxidant enzymes, such as superoxide dismutase, catalase, reduced glutathione, peroxidase, are responsible for scavenging reactive oxygen species.
在清除各類有害藻華細胞的實驗中,已經開發並使用了不同的化合物(表 3)。化學殺藻劑誘導細胞裂解的機制。殺藻劑很可能會破裂細胞壁和細胞膜,或透過特定的轉運體轉移到細胞壁和細胞膜上,然後進入細胞質並遇到細胞器,包括葉綠體、內質網和粒線體。這個過程會刺激活性氧的過度產生(Ebenezer 和 Ki,2013 年)。臭氧等強氧化劑會增加細胞內的活性氧水平,幹擾細胞功能並導致細胞溶解(Zhang 等人,2003 年)。羥自由基和過氧化氫是活性氧,是光合作用和呼吸作用的副產品。羥自由基和氧會產生氫氧化物,這是一種破壞性很強的活性氧。超氧化物歧化酶、過氧化氫酶、還原型穀胱甘肽、過氧化物酶等抗氧化酶具有清除過量活性氧的活性。
These enzymes are localized in different cell compartments and activated to various extents upon exposure to stress. The remaining reactive oxygen species initiate lipid peroxidation, leading to an increase in malondialdehyde content, often used as a biomarker of oxidative stress and loss of membrane integrity; the lack of intracellular malondialdehyde ultimately leads to cell death. In addition, the chloroplast membrane is damaged, and the grana lamellae of the thylakoid membranes are destroyed, creating interfering with photosynthetic system II and I (plastoquinone, plastocyanin, and ferredoxin activity), decreasing chlorophyll and protein content (cytochrome b6-f complex), eventually leading to photosynthesis being down-regulated upon. Excessive reactive oxygen species can also cause mitochondrial disfunction, which may affect cell metabolism and clump nuclear chromatin through binding nucleotides. The disruption of the metabolic process damages the DNA, affecting gene expression and cell reproductive (Shin et al. 2017; Zhang et al. 2003).
這些酵素定位於不同的細胞區,在受到壓力時會被不同程度地活化。剩餘的活性氧引發脂質過氧化,導致丙二醛含量增加,丙二醛通常被用作氧化壓力和膜完整性喪失的生物標記;細胞內丙二醛的缺乏最終導致細胞死亡。此外,葉綠體膜受損,類囊體膜的顆粒層被破壞,幹擾光合作用系統II 和I(質醌、質花青素和鐵氧還蛋白活性),降低葉綠素 和蛋白質含量(細胞色素b6-f 複合物),最終導致光合作用下調。過多的活性氧也會導致粒線體功能失調,進而影響細胞的新陳代謝,並透過結合核苷酸使核染色質凝集。代謝過程的破壞會損害 DNA,影響基因表現和細胞繁殖(Shin 等人,2017 年;Zhang 等人,2003 年)。

Biological methods 生物方法

Biological methods of algal blooms control are environmentally friendly and may provide a cost-effective alternative strategy to physical and chemical methods. Generally,
Table 3 Chemical oxidants used to remove red tide harmful algal blooms
表 3 用於清除赤潮有害藻華的化學氧化劑
Oxidants 氧化劑
Concentration/cultiva- 集中/培養
tion time 時間
Inhibition rate 抑制率 Tested algal bloom species
Reference 參考資料
Ozone 臭氧
H. akashiwo; Heterocapsa triquetra, .
polykrikoides; K. mikimotoi
Honjo et al. (2004)
本莊等人(2004 年)
Potassium permanganate 高錳酸鉀 Karlodinium micrum; P. minimum Deeds et al. (2002)
Deeds 等人(2002 年)
Ozone 臭氧 Gymnodinium breve 魴魚 Schneider et al. (2003)
施奈德等人(2003 年)
Hydrogen peroxide 過氧化氫 C. polykrikoides Ryu et al. (1998)
Ryu 等人(1998 年)
Ozone 臭氧 C. polykrikoides Schneider et al. (2003)
施奈德等人(2003 年)
Chlorine  P. globose Zhang et al. (2003)
張等人(2003 年)
Ozone 臭氧 A. tamarense; S. trochoidea Yang et al.  Yang et al.
Chlorine  C. polykrikoides Ryu et al. (1998)
Ryu 等人(1998 年)
Chlorine  - C. polykrikoides Ebenezer and Ki (2013)
埃比尼澤和基(2013 年)
The oxidants are considered in terms of the type of oxidant, concentration and cultivation time (i.e., exposure to the clay), inhibition rate, harmful algal bloom species impacted, and relevant references

biological algicides kill algae through direct or indirect contact. For example, various microorganisms are used, such as bacteria, viruses, actinomycetes, parasitic pathogens, grazers, plants, and animals, which produce other secondary metabolite chemicals (Xiao et al. 2019; Xu et al. 2019; Zhu et al. 2019). Several different organisms can theoretically act as biological controllers of harmful algal blooms. For algal bloom control, biological methods rely primarily on predator-prey methods that mostly rely on controls by zooplankton populations.
生物殺藻劑透過直接或間接接觸殺死藻類。例如,可使用各種微生物,如細菌、病毒、放線菌、寄生病原體、食草動物、植物和動物,它們會產生其他次級代謝物化學物質(Xiao 等,2019 年;Xu 等,2019 年;Zhu 等,2019 年)。理論上,幾種不同的生物都可以作為有害藻華的生物控制者。對於藻華控制,生物方法主要依靠捕食者-被捕食者方法,這種方法主要依靠浮游動物族群的控制。

Algicidal bacteria 殺藻細菌

Bacteria-algae-based approaches for algal blooms control represent a research hotspot. This method can lyse algae directly or indirectly, attacking cells (Zhang et al. 2018a, b). A direct attack mode requires that the algicidal bacteria contact and invade the algal cells' surface to inhibit the growth and cause cell lysis. Researchers have found that most cytophages, including Flavobacterium and Bacteroidetes, show algicidal activity through direct contact with algal cells. An indirect attack mode mainly comprises the competition between bacteria and algae or the secretion of extracellular metabolites leading to algal death (Meyer et al. 2017). For example, deinoxanthin produced by Deinococcus xianganeasis has a robust anti-algal effect on . tamarense (Li et al. 2015a, b). Prodigiosin produced by Hahella KA22 has produced high algicidal activity against H. akashiwo, Phaeocystis globosa, and Prorocentrum donghaiense (Zhao et al. 2014). Besides, -acetylhistamine, o-tyrosine, L-histidine, and urocanic acid produced by Bacillus sp. strain B1 can kill H. akashiwo, P. globosa, and . donghaiense (Zhao et al. 2014). These and other active microbial metabolites are highly effective algicides, but their ecological impact on other aquatic organisms has not been well tested, severely hindering development of this promising harmful algal blooms treatment.
基於細菌-藻類的藻華控制方法是一個研究熱點。此方法可以直接或間接裂解藻類,攻擊細胞(Zhang 等,2018a, b)。直接攻擊模式要求殺藻細菌接觸並侵入藻類細胞表面,抑制其生長並導致細胞裂解。研究人員發現,大多數的細胞噬菌體(包括黃桿菌和類桿菌)都是透過與藻類細胞直接接觸而表現出殺藻活性。間接攻擊模式主要包括細菌與藻類之間的競爭或分泌胞外代謝物導致藻類死亡(Meyer 等,2017 年)。例如,Deinococcus xianganeasis 產生的脫氧黃素對 ..tamarense(Li 等人,2015a, b)。 Hahella KA22 產生的原薯蕷皂苷對 H. akashiwo、Phaeocystis globosa 和 Prorocentrum donghaiense 具有很高的殺藻活性(Zhao 等,2014 年)。此外, -乙醯組胺-菌株B1 產生的-乙醯組胺、鄰酪胺酸、L-組胺酸和尿氨酸能殺死H. akashiwo、P. globosa 和{{3} } ..donghaiense(趙等人,2014 年)。這些和其他活性微生物代謝產物是高效的殺藻劑,但它們對其他水生生物的生態影響尚未得到很好的測試,嚴重阻礙了這種有前景的有害藻華處理方法的發展。
Bacteria have a complicated relationship with bloomforming species, and bacteria with algicide activity should be first isolated and identified (Li et al. 2015a, b). The algicide activity of bacteria can be divided into two categories: a single microorganism responsible for suppressing harmful algal blooms species or a multi-species community (Sun et al. 2018). Microbial aggregates are a multi-species community of algae that include microorganisms and macroorganisms growing on solid substrates. Multispecies communities comprise aggregates embedded in the mucus matrix of extracellular polymeric substances and have relatively high mechanical stability and cell density. These aggregates comprise phototrophic and heterotrophic biofilms (Sun et al. 2018). Heterotrophic biofilms control harmful algal blooms by producing anti-algae compounds. For example, the growth-inhibiting bacteria isolated from seagrass
細菌與形成藻華的物種關係複雜,應先分離鑑定具有殺藻活性的細菌(Li 等,2015a,b)。細菌的殺藻活性可分為兩類:一類是負責抑制有害藻華物種的單一微生物,另一類是多物種群落(Sun 等,2018 年)。微生物聚集體是一種多物種藻類群落,包括生長在固體基質上的微生物和大型生物。多物種群落由嵌入胞外聚合物物質黏液基質的聚集體組成,具有相對較高的機械穩定性和細胞密度。這些聚集體包括光養生物膜和異養生物膜(Sun 等,2018 年)。異養生物膜透過產生抗藻化合物來控制有害藻類的大量繁殖。例如,從海草中分離出的生長抑制細菌

(Zostera sp.) leaves show inhibitory activity against the toxic dinoflagellate A. tamarense (Onishi et al. 2014). Therefore, growth-inhibiting bacteria in the microbial aggregates provide an attractive possibility for biological control of toxic blooms.
(Zostera sp.)葉片對有毒甲藻 A. tamarense 具有抑制活性(Onishi 等人,2014 年)。因此,微生物聚集體中的生長抑制細菌為有毒水華的生物控制提供了一種極具吸引力的可能性。
In the past few decades, many studies have reported that algal inhibition by bacteria involves cell destruction, subcellular structure changes, photosynthesis inhibition, enzyme activity effects, and functional gene expression changes, showing that these may negatively affect algae and cause cell death (Cai et al. 2016; Lu et al. 2016; Zhang et al. 2018a, b; Zhang et al. 2016). Most algicide bacteria and their compounds are algae species-specific, making them an environmentally friendly method of harmful algal blooms control. The bacterial genera Cytophaga sp., Saprospira sp., Alteromonas sp., Pseudoalteromonas sp., Vibrio sp., Shewanella sp., Bacillus sp., Planomicrobium sp., and Micrococcus sp., target specific algal cells (Kim et al. 2015a, b; Meyer et al. 2017; Park et al. 2010; Pokrzywinski et al. 2012). Before considering the use of biological control for harmful algal blooms, the environmental impact of biological releases on ecosystems needs careful consideration.
在過去幾十年中,許多研究報告了細菌對藻類的抑製作用涉及細胞破壞、亞細胞結構變化、光合作用抑制、酶活性影響和功能基因表現變化,表明這些可能對藻類產生負面影響並導致細胞死亡(Cai 等,2016 年;Lu 等,2016 年;Zhang 等,2018a,b;Zhang 等,2016 年)。大多數殺藻細菌及其化合物對藻類物種具有特異性,因此是控制有害藻華的環境友善方法。細菌屬Cytophaga sp.、Saprospira sp.、Alteromonas sp.、Pseudoalteromonas sp.、Vibrio sp.、Shewanella sp.、Bacillus sp.、Planomicrobium sp.和Micrococcus sp.針對特定的藻類細胞(Kim 等,2015a,b; Meyer 等,2017;Park 等,2010;Pokrzywinski 等,2012)。在考慮使用生物控制有害藻華之前,需要仔細考慮生物釋放對生態系統的環境影響。

Actinomycetes as an algicide

There are relatively few studies on algicidal actinomycetes and their bioactive compounds (Bai et al. 2011; Zhang et al. 2014; Zheng et al. 2013). The first report is on Micrococcus sp., which killed the harmful dinoflagellate, C. polykrikoides (Kim et al. 2008). To the best of our knowledge, only four lysing actinomycetes have been described, including Brevibacterium sp., S. malaysiensis, S. alboflavus, and Micrococcus sp., which can kill the harmful dinoflagellates . polykrikoides, A. tamarense, P. globosa, and H. akashiwo (Bai et al. 2011; Yu et al. 2018; Zhang et al. 2015; Zheng et al. 2013). These actinomycetes exhibit high-strength algicidal activity through inhibition of electron flow in the PS II reaction center and interference with photosynthetic pigments. Any inhibition of physiological activity can induce reactive oxygen species production in algal cells that may ultimately lead to oxidative damage. As previously noted, secondary metabolites produced by actinomycetes, such as proteases, peptides, amino acids, and antibiotic, can also be strong algicidal compounds.
關於殺藻放線菌及其生物活性化合物的研究相對較少(Bai 等人,2011 年;Zhang 等人,2014 年;Zheng 等人,2013 年)。第一份報告是關於微球菌(Micrococcus sp.)的,它殺死了有害的甲藻 C. polykrikoides(Kim 等,2008 年)。據我們所知,目前只描述了四種裂解放線菌,包括Brevibacterium sp.、S. malaysiensis、S. alboflavus 和Micrococcus sp.,它們可以殺死有害甲藻 ..polykrikoides、A . tamarense、P. globosa 和H. akashiwo(Bai 等人,2011 年;Yu 等人,2018 年;Zhang 等人,2015 年;Zheng 等人,2013 年)。這些放線菌透過抑制 PS II 反應中心的電子流和乾擾光合色素,表現出高強度的殺藻活性。對生理活動的任何抑制都會誘導藻類細胞產生活性氧,最終導致氧化損傷。如前所述,放線菌產生的次級代謝物,如蛋白酶、勝肽、胺基酸和抗生素等,也可以成為強烈的殺藻化合物。

Algicidal parasitic pathogens

The dynamics of algal parasites and their role in harmful algal blooms termination are not well understood. Parasites can proliferate in marine dinoflagellate hosts, causing death (Chen et al. 2018). For example, Amoebophrya ceratii infection spreads rapidly in dense dinoflagellate populations, reducing host reproduction rates. Parasitic infections provide
藻類寄生蟲的動態及其在有害藻華終止中的作用尚不十分清楚。寄生蟲可在海洋甲藻宿主體內增殖,導致死亡(Chen 等,2018 年)。例如,Amoebophrya ceratii 感染會在密集的甲藻族群中迅速擴散,降低宿主的繁殖率。寄生蟲感染提供了

opportunities for biological control of harmful algal blooms (Siano et al. 2011; Velo-Suarez et al. 2013) and ability to eliminate entire host populations in a few days potentially makes them more effective as control agents that zooplankton. The parasite identifies and attaches to the host's surface, penetrates the host cytoplasm and even the nucleoplasm, and then regulates host defense mechanisms, including host toxins (Padilla et al. 2010). Recent studies have found that galactolipid in the chloroplast membrane of A. tamarase can be infected by Amoebophrya sp (Leblond and Dahmen 2012). So far, two types of parasites-Amoebophrya ceratii and Parvilucifera infectans-are well-known intracellular parasites of free-living dinoflagellates that have received particular attention as a biological methods algal blooms species inhibition (Chambouvet et al. 2008; Li et al. 2014).
這些寄生蟲能夠在幾天內消滅整個宿主種群,這可能使它們成為更有效的浮游動物控製劑,從而為有害藻華的生物控制提供了機會(Siano 等,2011 年;Velo-Suarez 等,2013年)。寄生蟲會辨識並附著在宿主表面,穿透宿主細胞質甚至核質,然後調節宿主防禦機制,包括宿主毒素(Padilla 等,2010 年)。最近的研究發現,檉柳甲葉綠體膜中的半乳脂可被嗜水阿米巴蟲感染(Leblond 和 Dahmen,2012 年)。迄今為止,有兩類寄生蟲--Amoebophrya ceratii 和Parvilucifera infectans--是眾所周知的自由生活甲藻的胞內寄生蟲,作為抑制藻華物種的生物方法受到特別關注(Chambouvet 等,2008 年;Li 等,2014 年)。

Algicidal viruses 殺菌病毒

The use of algicidal viruses has great potential as a biological control method for harmful algal blooms. Over 40 viruses that can infect algae have been identified and isolated (Nagasaki and Tomaru 2009). Among these is cell lysis of the bloom-forming dinoflagellate, . circularisquama by HaRNAV, a single-stranded RNA virus, observed in Ago Bay (Mizumoto et al. 2008). Another study found the double-stranded RNA virus lysed . circularisquama (Tarutani et al. 2001). Hemolytic HaV 01 has been used to infect . akashiwo harmful algal blooms (Nagasaki et al. 1999), while HcDNAV, a large double-stranded DNA virus, lyses cells of the bloom-forming of . circularisquama (Takano et al. 2018). The most exciting aspects of this control method is the natural abundance and variety of viruses in marine systems, and their large capacity, easy replication, and high specificity to the host. Further work is required to understand the specificity of viruses to different genetic strains in their host species.
使用殺藻病毒作為生物控制有害藻華的方法具有巨大潛力。目前已發現並分離出 40 多種可感染藻類的病毒(Nagasaki 和 Tomaru,2009 年)。在這些病毒中, .circularisquama 被 HaRNAV(一種單股 RNA 病毒)溶解(Mizumoto 等人,2008 年)。另一項研究發現,雙股 RNA 病毒 能裂解 .circularisquama (Tarutani 等,2001 年)。溶血HaV 01 已被用於感染 .akashiwo 有害藻華(Nagasaki 等,1999 年),而大型雙股DNA 病毒HcDNAV 則能裂解 .circularisquama 的細胞(高野等人, 2018 年)。這種控制方法最令人興奮的地方在於海洋系統中病毒的天然豐富性和多樣性,以及它們的大容量、易複製性和對宿主的高度特異性。要了解病毒對宿主物種中不同基因株的特異性,還需要進一步的工作。

Protistan grazers 原生動物草食動物

Meta-zooplankton grazing may be a significant loss factor for harmful algal blooms, even resulting in their termination (Calbet et al. 2003). These grazing meta-zooplankton include copepods, cladocerans, larvae of invertebrates, and hydrozoans (Lee et al. 2014). An example includes the grazing ciliate Strombidinopsis jeokjo, which reduced a large population of . ploykrikoides to insignificant levels within a few days (Jeong et al. 2008). Mixotrophic dinoflagellates are potentially prolific grazers. For example, Alexandrium pohangense population lyse . polykrikoides cells (Lim et al. 2017), while P. lebourae feeds on Amphidinium sp., Thecadinium kofoidii, and Prorocentrum fukuyoi (Kim et al. 2015a, b). Experiments involving the removal of harmful algal blooms cells by protistan grazers in summarized in
捕食元浮游動物可能是有害藻華的重要損失因素,甚至會導致藻華終止(Calbet 等人,2003 年)。這些吃草的元浮游動物包括橈足類、櫛水母、無脊椎動物幼蟲和水螅(Lee 等,2014 年)。其中一個例子是食草纖毛蟲 Strombidinopsis jeokjo,它將大量 .ploykrikoides 在幾天內就減少到微不足道的水平(Jeong 等,2008 年)。混養甲藻是潛在的多產食草動物。例如,Alexandrium pohangense族群會裂解 .polykrikoides 細胞(Lim 等人,2017 年),而P. lebourae 則以Amphidinium sp.、Thecadinium kofoidii 和Prorocentrum fukuyoi 為食(Kim 等人,2015a, b) 。原生動物食肉動物清除有害藻華細胞的實驗摘要如下

Table 4. But while this biological method appears to be a safe and effective way of controlling harmful algal blooms populations, there are few ecosystem-scale applications.
表 4.不過,雖然這種生物方法似乎是一種安全有效的控制有害藻華數量的方法,但在生態系範圍內的應用卻很少。
Different biological agents have been developed and used in experiments involving the removal of various types of harmful algal blooms cells (Table 4). Biological agents, including bacteria (Pokrzywinski et al. 2017; Zhang et al. 2018a, b), actinomycete (Cai et al. 2016; Yu et al. 2018), viruses (Takano et al. 2018; Tarutani et al. 2001), parasitic pathogens and protistan grazers (Jeong et al. 2011; Kim et al. 2015a, b; Yoo et al. 2013a, b), should also be considered as potential inhibitors for controlling the outbreak of harmful algal blooms. However, logistics difficulties in the predator's application and scaling the culture to get enough zooplankton predators limit their potential use outside the laboratory.
在清除各類有害藻華細胞的實驗中,已經開發並使用了不同的生物製劑(表 4)。包括細菌(Pokrzywinski 等人,2017 年;Zhang 等人,2018a, b)、放線菌(Cai 等人,2016 年;Yu 等人,2018 年)、病毒(Takano 等人,2018 年;Tarutani 等人,2001 年)、寄生病原體和原生動物捕食者(Jeong 等人,2011 年;Kim 等人,2015a, b;Yoo 等人,2013a, b)在內的生物製劑也應被視為控制有害藻華爆發的潛在抑制劑。然而,捕食者應用的後勤困難以及擴大培養規模以獲得足夠的浮游動物捕食者限制了它們在實驗室外的潛在用途。

Micro- and macro-algae algicides

Many recent studies have focused on separating anti-algae active substances from micro-algae and macro-algae to inhibit harmful algal blooms species (Ben Gharbia et al. 2017; Calbet et al. 2003). Secondary metabolites from micro- and macro-algae play an important role in inhibiting growth of algal blooms species and stopping formation of harmful algal blooms and are generally non-toxic to other organisms (Jeong et al. 2008; Lee et al. 2014). Relationships between micro- and macro-algae and harmful algal blooms have been studied intensively over the last two decades (Jeong et al. 2011; Kim et al. 2015a, b; Lim et al. 2017), including examining terpenoids, glycerolipids, and various other secondary compounds (Ben Gharbia et al. 2017).
最近的許多研究著重於從微藻和大型藻類中分離抗藻活性物質,以抑制有害藻華物種(Ben Gharbia 等人,2017 年;Calbet 等人,2003 年)。微藻和大型藻類中的次級代謝物在抑制藻華物種的生長和阻止有害藻華的形成方面發揮著重要作用,而且一般對其他生物無毒(Jeong 等人,2008 年;Lee 等人, 2014 年)。在過去二十年中,人們對微藻和大型藻類與有害藻華之間的關係進行了深入研究(Jeong 等人,2011 年;Kim 等人,2015a, b;Lim 等人,2017 年),包括研究萜類、甘油脂類和其他各種次級化合物(Ben Gharbia 等人,2017 年)。
Several chemicals have been extracted from marine macro-algae (seaweed) which can inhibit many other microalgae, potentially even red tide dinoflagellates (Sahu et al. 2020; Wang et al. 2021). Previous reports have shown that these bioactive compounds directly attack the permeability of target cell membranes and affect photosynthetic activity by inhibiting the growth and survival of algae. These findings may contribute to novel ways to improve algicide substances for emergency control of algal blooms (Yoo et al. 2013a, b), for example, using extracts or bioactive compounds from micro- and macro-algae. Different metabolites from micro- and macro-algae have used in experiments involving the removal of various types of algal blooms cells, with encouraging results (Table 5).
從海洋大型藻類(海藻)中提取的一些化學物質可抑制許多其他微藻,甚至可能抑制赤潮甲藻(Sahu 等,2020 年;Wang 等,2021 年)。先前的報告顯示,這些生物活性化合物直接攻擊目標細胞膜的滲透性,並透過抑制藻類的生長和存活來影響光合作用活性。這些發現可能有助於以新穎的方式改進用於緊急控制藻華的殺藻物質(Yoo 等,2013a, b),例如,利用微藻和大型藻類的萃取物或生物活性化合物。在清除各種類型藻華細胞的實驗中,使用了來自微藻和大型藻類的不同代謝物,結果令人鼓舞(表 5)。

Inhibitory effects of allelochemicals

Allelopathy from harmful algal blooms involves biochemical compounds produced from secondary metabolism of plants and microorganisms, which influence growth and reproduction of algal blooms species (Chen et al. 2013; Xiao et al.
有害藻華產生的同化作用涉及植物和微生物二次代謝產生的生化化合物,這些化合物會影響藻華物種的生長和繁殖(Chen 等,2013 年;Xiao 等,2007 年)。
Table 4 Biological agents used to remove red tide harmful algal blooms
表 4 用於消除赤潮有害藻華的生物製劑
Algicide 殺藻劑 Mode of action 作用方式 Tested algal bloom species
Reference 參考資料
Bacteria 細菌
Joostella sp. Indirect/Active compounds lytic
A. tamarense Yang et al.  楊等人
Bacillus sp. Indirect/Active compounds lytic
P. globose Li et al. (2014)
李等人(2014 年)
Paracoccus sp. Indirect/Active compounds lytic
P. donghaiense Zhang et al.  Zhang et al.
Mangrovimonas sp. Indirect/Algicidal effect
A. tamarense Li et al. (2014)
李等人(2014 年)
Pseudoalteromonas sp. 假交替單胞菌 Indirect/Algicidal effect
A. tamarense Su et al. (2007)
蘇等人(2007 年)
Tenacibaculum sp. Direct/Growth inhibition
A. tamarense Li and Pan (2013)
Cytophaga sp. Direct/Algicidal effect 直接/殺藻作用 G. breve Doucette et al. (1998)
杜塞特等人(1998 年)
Brachybacterium sp. Indirect/Algicidal effect
A. tamarense Kim et al.  Kim 等人 {{0}
Cytophaga sp. Indirect/Growth inhibition
K. brevis Mayali and Doucette (2002)
Mayali 與 Doucette(2002 年)
Altererythrobacter sp. Indirect/Algicidal effect
A. tamarense Li et al. (2016)
Shewanella sp. Indirect/Algicidal exudate
間接: 藻類滲出物
P. minimum, Karlodinium veneficum; Gyrodinium
P. minimum, Karlodinium v​​eneficum; Gyrodinium
instriatum 引信
Pokrzywinski et al. (2017)
Pokrzywinski 等人(2017 年)
Deinococcus sp. Indirect/Algalytic substance
A. tamarense Li et al.  李等人 {{0}
Alteromonas sp. Indirect/Active compounds lytic
tamarense; H. akashiwo Cho et al. (2016)
Cho 等人(2016 年)
Alteromonas sp. Indirect/Algicidal exudate
間接: 藻類滲出物
P. donghaiense Shi et al. (2018)
Shi 等人(2018)
Vibrio sp. 弧菌 Indirect/Growth inhibition
A. tamarense Fu et al. (2011)
Fu 等人(2011 年)
Actinomycetes 放線菌
Brevibacterium sp. Indirect/Lysis 間接/溶解 A. tamarense Bai et al. (2011)
Bai 等人(2011 年)
malaysiensis 馬來西亞 Indirect/Algicidal effect
P. globosa Zheng et al. (2013)
S. alboflavus Indirect/Algicidal effect
P. globosa Zhang et al. (2014)
Streptomyces sp. JSO1 鏈黴菌 JSO1 Algicidal activity 殺藻活性 P. globosa Zhang et al. (2015)
S. alboflavus Indirect/Lysis 間接/溶解 P. globosa Cai et al. (2016)
Streptomyces sp. U3 鏈黴菌 U3 Indirect/Algicidal effect
H. akashiwo Yu et al. (2018)
Yu 等人(2018)
Parasites 寄生蟲
Amoebophrya sp. Direct/grazing 直接/放牧 A. tamarense 112
Parvilucifera infectans Direct/grazing 直接/放牧 A. minutum Cai et al. (2016)
Amoebophrya sp. Direct/grazing 直接/放牧 A. sanguinea Mazzillo et al. (2011)
Mazzillo 等人(2011 年)
Amoebophrya ceratii 陶瓷嗜阿米巴原蟲 Direct/grazing 直接/放牧 G. catenatum Nishitani et al. (1985)
Nishitani 等人(1985 年)
Viruses 病毒
HcDNAV Direct/Lysis infection 直接/溶解感染 Heterocapsa circularisquama Takano et al. (2018)