A critical review on control methods for harmful algal blooms
有害藻華控制方法評述

Juan J. Gallardo-Rodríguez, Department of Chemical Engineering, Faculty of Engineering, University of Concepción, Víctor Lamas 1290, 160-C Concepción, Bio-Bio, Chile.
Juan J. Gallardo-Rodríguez, 化學工程系，康塞普西翁大學工程學院，Víctor Lamas 1290, 160-C Concepción, Bio-Bio, Chile.

Email: juangallardo@udec.cl
電子郵件： juangallardo@udec.cl

Received 11 July 2017; accepted 2 April 2018.
2017年7月11日收到；2018年4月2日接受。

Key words: algicides, clays, control, flocculation, harmful algal blooms.
關鍵字：殺菌劑、黏土、防治、絮凝、有害藻華。

Harmful algal blooms (HABs) have been defined as any toxic or harmful event associated with microalgae that adversely affects public health, fishing activities, aquaculture and tourism (Clément & Lembeye 1994). The best known HAB phenomenon is the red tide; however, it is not the only one. The toxicity degree and changes in sea coloration will vary depending on the species of phytoplankton micro-organism involved (Hallegraeff et al. 1995). These blooms occur commonly in coastal ecosystems, but can also occur in the open sea as well as brackish or freshwater ecosystems (Anderson et al. 2012). HABs are also a concern in reservoir waters and in desalinization plants (Anderson et al. 2017). These episodes interfere negatively in ecosystems directly affecting biota, due to a series of mechanisms. These include physical damages, such as gill obstruction in fish, reduction in available oxygen or production of toxins (Bower et al. 1981).
有害藻華（HABs）被定義為與微藻類有關的任何有毒或有害事件，會對公眾健康、漁業活動、水產養殖和旅遊業造成不利影響（Clément & Lembeye，1994 年）。最著名的有害藻類繁殖現像是赤潮，但這並不是唯一的現象。毒性程度和海水顏色的變化因涉及的浮游植物微生物種類而異（Hallegraeff 等，1995 年）。這些藻華通常發生在沿海生態系中，但也可能發生在公海以及鹹水或淡水生態系（Anderson 等，2012 年）。水庫水域和脫鹽工廠中的 HAB 也令人擔憂（Anderson 等，2017 年）。由於一系列機制，這些事件會對生態系統造成負面影響，直接影響生物群。這些機制包括物理損害，如魚鰓阻塞、可用氧氣減少或產生毒素（Bower 等，1981 年）。

Harmful algal blooms are often associated with variations in climatic and hydrographic conditions (Van
有害藻類大量繁殖通常與氣候和水文條件的變化有關（Van
Egmond & Speijers 1999; Navarro et al. 2006) and anthropomorphic activity, such as increased eutrophication, maritime transport and aquaculture. During the 70s, affected countries ran their own HAB programs in a zonal context, without considering the global perspective of this problem (Anderson et al. 2012). The first reports of global incidence of HABs were made by Anderson (1989) and Hallegraeff (1993) who showed the increase in frequency, magnitude and geographic extent of these events, allowing the implementation of programs such as GEOHAB. This program is aimed to improve the prediction of HAB events by encouraging cooperative research (Anderson 1989; Hallegraeff 1993). Current established HAB programs include activities for the detection and quantification of toxins and cells (harmful species) in the water column, development of bloom forecasts and early warnings (Anderson et al. 2001; Davidson et al. 2016; Hardy et al. 2016; Maguire et al. 2016). Predicting the appearance of these blooms is complex as many interrelated phenomena are involved. Last advances in prediction and simulation require considerable computing resources as the numerical models are fed with
Egmond & Speijers，1999 年；Navarro 等人，2006 年）以及人為活動，如富營養化、海上運輸和水產養殖的增加。在 1970 年代，受影響的國家在區域範圍內開展了各自的有害藻華計劃，而沒有從全球角度考慮這一問題（Anderson 等，2012 年）。 Anderson （1989 年）和 Hallegraeff（1993 年）首次報告了 HABs 的全球發生率，顯示了這些事件發生頻率、規模和地理範圍的增加，從而促成​​了 GEOHAB 等計劃的實施。該計劃旨在透過鼓勵合作研究來改進對 HAB 事件的預測（Anderson，1989 年；Hallegraeff，1993 年）。目前已建立的有害藻華計劃包括檢測和量化水體中的毒素和細胞（有害物種）、制定藻華預測和預警等活動（Anderson 等，2001 年；Davidson 等，2016 年；Hardy 等，2016 年； Maguire 等，2016 年）。由於涉及許多相互關聯的現象，預測這些水華的出現非常複雜。預測和模擬的最新進展需要大量的計算資源，因為數值模型需要輸入
data from satellite images, weather forecasts and monitoring programs (Anderson et al. 2012). However, despite this significant scientific effort, reliable models for bloom appearance and dynamics are limited by the number of samples gathered in the HAB monitoring programs. Instruments able to automatically sample water for the detection of HAB species and toxins will contribute to the development of better prediction systems in a near future (Anderson et al. 2012).
這些數據來自衛星影像、天氣預報和監測計畫（Anderson 等，2012 年）。然而，儘管做出如此巨大的科學努力，但由於 HAB 監測計畫收集的樣本數量有限，有關水華出現和動態的可靠模型仍然有限。能夠自動採樣檢測 HAB 物種和毒素的儀器將有助於在不久的將來開發出更好的預測系統（Anderson 等，2012 年）。

Harmful algal bloom countermeasures can be classified in prevention mitigation and control. HAB mitigation is driven to the lessening of harmful effects once the bloom has occurred. In this respect, avoiding contact between bloom and aquacultured animals and restoring environmental conditions are the two main approaches. HAB-control measures currently used are focused on limiting the impact of blooms by reducing the number of toxic microalgae or through the removal of toxins from the water column (Sengco 2009a,b). These methods are of a physical, chemical or biological nature and have been used in freshwater and marine systems to control HABs at small and large scale (Sengco et al. 2005; Zheng et al. 2013; Wang et al. 2014, 2015; Sun et al. 2015; Yuan et al. 2016). HAB prevention consists in acting against causes of bloom formation which basically is to avoid eutrophication.
有害藻華對策可分為預防、緩解和控制。緩解有害藻華的目的是在藻華發生後減少有害影響。在這方面，避免藻華與水產養殖動物接觸和恢復環境條件是兩種主要方法。目前使用的 HAB 控制措施主要是透過減少有毒微藻的數量或清除水體中的毒素來限制水華的影響（Sengco，2009a,b）。這些方法具有物理、化學或生物性質，已在淡水和海洋系統中用於控制大小規模的HAB（Sengco 等人，2005 年；Zheng 等人，2013 年；Wang 等人，2014 年、2015 年；Sun等人，2015 年；Yuan 等人，2016 年）。 HAB 的預防包括針對藻華形成的原因採取行動，從根本上避免富營養化。

Expecting climate changes in the next decades that will favour bloom formation and also an increase of human activity in coastal areas, HABs will be growing concern in a global context. HAB control methods' development is integrated in a complex and diverse field where multidisciplinary approaches should be taken. The objective of this review was to provide a critical overview of the methods currently employed for HAB control (physical, physicochemical and biological) and those that were considered for the task. The fundamentals of these approaches, together with a thorough revision of the state of art, are provided in this work. Additionally, the generated impact on the associated ecosystems is also considered.
預計未來幾十年的氣候變遷將有利於藻華的形成，而且沿海地區的人類活動也將增 加，因此，藻華將成為全球日益關注的議題。 HAB 控制方法的發展是一個複雜多樣的綜合領域，應採取多學科方法。本綜述的目的是對目前用於控制有害藻華的方法（物理、物理化學和生物方法）以及考慮用於此任務的方法進行重要概述。本報告介紹了這些方法的基本原理，並對最新技術進行了全面修訂。此外，也考慮了對相關生態系統所產生的影響。

Physical methods have been used to a greater extent in freshwater, although these methods are the same for both fresh and seawater systems. The subsequent use of water has made that physical be preferred to chemical methods for freshwater. Toxic cyanobacteria of genera Microcystis and Anabaena pose a serious problem for freshwater resources. Low -or absence of - flow exchange, together with high concentrations of nutrients, allows these organisms to bloom, deteriorating water quality. A proposed solution has been based on increasing the mixture to avoid stratification. Thus, competitive advantages of dinoflagellates and cyanobacteria against another type of phytoplankton are diminished. For example, hypolimnetic withdrawals and horizontal flushing in reservoirs improve water quality by releasing volumes from the lower and upper layers, respectively. In the USA, during four decades selective hypolimnetic withdrawals have been selectively carried out (Schneider et al. 2004). Water mixture can also be produced using mechanical (pumps), hydraulic or pneumatic mixers. Although solar-powered systems are now available, these equipments are expensive and logistic for large systems is complicated. The examples gathered in the literature reflect that the cost is only acceptable for drinking water (Cong et al. 2011). Another proposed solution is the use of floating covers to avoid the proliferation of photosynthetic organisms. Although there has been some field experience, costs and impacts have not been documented. However, this is a prevention method rather than a control measure. On the contrary, physical disruption can control a developed bloom if the volume of water to be treated is relatively small. For example, sonication is suited for water treatment systems but not for large waterbodies (Anderson et al. 2017). Its disadvantage is that by eliminating microalgae biomass through sonication, dissolved organic compounds are also released.
物理方法在淡水中的使用程度更高，儘管這些方法在淡水和海水系統中都是一樣的。在淡水系統中，水的後續使用使得物理方法比化學方法更受青睞。微囊藻屬（Microcystis）和赤藻屬（Anabaena）的有毒藍綠藻為淡水資源帶來了嚴重問題。水流交換量低或缺乏，再加上高濃度的營養物質，使得這些生物大量繁殖，導致水質惡化。建議的解決方案是增加混合物以避免分層。這樣，甲藻和藍綠藻對另一種浮游植物的競爭優勢就會減弱。例如，水庫中的下滲抽水和水平沖洗可分別從下層和上層釋放水量，從而改善水質。在美國，40 年來一直有選擇性地進行下滲抽水（Schneider 等人，2004 年）。也可使用機械（幫浦）、液壓或氣動混合器生產混合水。雖然現在有了太陽能供電系統，但這些設備價格昂貴，大型系統的物流也很複雜。文獻中收集的實例表明，只有飲用水的成本是可以接受的（Cong 等人，2011 年）。另一個建議的解決方案是使用浮動蓋來避免光合生物的擴散。雖然已有一些實地經驗，但成本和影響尚未記錄在案。不過，這是一種預防方法，而不是控制措施。相反，如果需要處理的水量相對較小，物理破壞可以控制已形成的水華。例如，超音波處理適用於水處理系統，但不適用於大型水體（Anderson 等人，2017 年）。其缺點是，透過超音波消除微藻生物量的同時，也會釋放出溶解的有機化合物。

Physical methods in coastal areas have been related to large mariculture facilities. Fish cultured in net pens are negatively affected by certain harmful or ichthyotoxic species. These species are not generally toxic to humans, but they can kill cultured fish massively. The mechanism of fish death is through several mechanisms including damage of gill tissue, blood hypoxia, toxigenic reactions to ichthyotoxic agents and gas bubble trauma from oxygen supersaturation (Rensel & Whyte 2004). Therefore, physical control methods have been based on creating a separation between fish and HAB and providing air to prevent hypoxia. Perimeters skirts can be useful, as long as they are accompanied by other measures. It usually requires aeration inside the cage to avoid hypoxia and ammonium accumulation. Aeration can be supplied by pumping water, pumping air or using surface agitators. Air is pumped from diffusers such as airstones or aspirators (horizontal, selfpowered units or nozzle types), used alone or in conjunction with water pumps. So far, airlift upwelling is the most used method in salmon farms (Jack Rensel, personal communication, August, 9, 2016). Airlift system pumps water from deep layers into the cage. This water is typically free of photosynthetic cells. Thus, it operates as a dilution method. When used with perimeter skirts, results are better. Although these methods can show certain efficiency, they have limitations. For example, they have proven unable to contain a bloom of Pseudochattonella in 2016 in Chilean salmon facilities (Clément et al. 2016). Towing net pens away from blooms to prevent fish death has been used in Canada, Norway and Japan for recurrent HABs of
沿海地區的物理方法與大型海產養殖設施有關。網箱養殖的魚類會受到某些有害魚類或魚毒物種的負面影響。這些魚種一般對人類無毒，但會使養殖的魚類大量死亡。魚類死亡的機制有幾種，包括鰓組織損傷、血液缺氧、對魚毒素的毒性反應以及氧氣過飽和造成的氣泡創傷（Rensel 和 Whyte，2004 年）。因此，物理控制方法的基礎是在魚類和 HAB 之間建立隔離，並提供空氣以防止缺氧。只要同時採取其他措施，圍裙是有用的。通常需要在網箱內通氣，以避免缺氧和氨累積。可以透過抽水、抽氣或使用表面攪拌器來通氣。空氣由擴散器泵送，如氣孔或吸氣器（水平、自供電裝置或噴嘴類型），可單獨使用或與水泵一起使用。到目前為止，氣舉上湧是鮭魚養殖場使用最多的方法（傑克-倫塞爾，個人通信，2016 年 8 月 9 日）。氣舉系統將水從深層泵入籠中。這種水通常不含光合作用細胞。因此，它是一種稀釋方法。如果與圍裙一起使用，效果會更好。雖然這些方法能顯示出一定的效率，但也有其限制。例如，2016 年在智利的鮭魚養殖設施中，這些方法已被證明無法遏制假尾柱蟲的繁殖（Clément 等人，2016 年）。加拿大、挪威和日本已將網箱拖離藻華，以防止魚類死亡。

Heterosigma, Karenia and Chattonella, respectively (Rensel & Whyte 2004). Alternatively, decked floating pens can submerge the cage. However, not all blooms are more densely concentrated on the surface. In the first years of mariculture, these systems were expensive, although new designs that integrate alert and airlift/aeration systems are nowadays available (e.g. decked floating pens by Kropf Industial, Toronto, Ontario, Canada; Aquapods by Innovasea, Boston, MA, USA, EE. UU.).
分別是 Heterosigma、Karenia 和 Chattonella（Rensel 和 Whyte，2004 年）。另外，有甲板的浮動圍欄可將籠子浸沒。不過，並非所有的水花都會更密集地集中在水面上。在海產養殖的最初幾年，這些系統價格昂貴，不過現在已有整合警報和氣舉/曝氣系統的新設計（例如加拿大安大略省多倫多市Kropf Industial 公司的甲板浮籠；美國馬薩諸塞州波士頓市Innovasea 公司的Aquapods ）。 UU.）。

Physical methods that were evaluated and discarded (reasons are discussed in NOWPAP CEARAC, 2007) include (i) magnetic separation of artificially magnetized planktonflocs; (ii) centrifugal separation; (iii) ultraviolet radiation; (iv) cavitation induced by ultrasound (Zhang et al. 2009); (v) flocculation by bubbling and skimming.
經評估後放棄的物理方法包括：(i) 人工磁化浮游生物絮團的磁分離；(ii) 離心分離；(iii) 紫外線輻射；(iv) 超音波誘導的空化作用（Zhang 等人，2009 年)；(v) 起泡和撇渣的絮凝作用。

The first reported control action for a HAB is attributed to the use of copper sulphate in the USA (Rounsefell & Evans 1958). In 1957, this algicidal was dispersed from airplanes over a K. brevis bloom. Although temporarily effective, the method did not terminate completely the bloom. To date, it is the only chemical control intervention in the sea registered in the literature. So far, many effective algicidals have been described; however, application in open systems (coastal or open sea areas) has not the preferred method due to environmental concerns (Sengco 2009a,b). Similarly to purely physical methods, when chemical or physical-chemical methods are described, a clear separation between fresh and seawater applications should be carried out. Water chemistry and turbulence, different bloom-forming species and, in some cases, legal considerations have caused that control actions had been different for fresh and seawater blooms.
據報導，對有害藻華的首次控制行動是在美國使用硫酸銅（Rounsefell 和 Evans，1958 年）。 1957 年，這種殺藻劑被從飛機上撒佈到 K. brevis 水華上。雖然暫時有效，但這種方法並沒有完全終止藻華。迄今為止，這是文獻中記載的唯一海洋化學控制干預措施。迄今為止，已描述了許多有效的藻類殺滅劑；然而，出於對環境的考慮，在開放系統（沿海或開放海域）中應用藻類殺滅劑並非首選方法（Sengco，2009 年a、b） 。與純物理方法類似，在介紹化學或物理化學方法時，也應明確區分淡水和海水的應用。水的化學性質和湍流、不同的水華形成物種，以及在某些情況下的法律考慮，都會導致對淡水和海水水華採取不同的控制措施。

In freshwater systems, such as lakes or lagoons, chemicals are regularly used (AWWA, 2004; Chen et al. 2011a,b). These interventions in freshwaters have been observed as less risky, not only for the existence of defined limits, but also for the fact that the natural habitats where chemicals are to be used are already considered contaminated/deteriorated. In other cases, as was noted for physical methods, the intervention is obliged as drinking-water supplies are affected. For an algicidal, the main feature should be, undoubtedly, that it does not create a secondary contamination. Short-life molecules such as chlorides or oxidants (copper sulphate, hydrogen peroxide, , etc.) fulfilled this requisite. Hydrogen peroxide is effective in freshwater at low concentration ) (Bauzá et al. 2014). Microcystis toxins (microcystins) are considered hepatotoxic, whereas anatoxin-a (produced by Anabaena spp.) is a neurotoxin. Consequently, they must be removed from the drinking or irrigation water. As advantage over other algicidals, hydrogen peroxide destroys microcystins helped by natural UV radiation (Bauzá et al. 2014). Similarly, photocatalytic degradation of microcystins is also possible (Shephard et al. 1998). Water electrolysis can create reactive oxygen species in situ without posing serious effects to other aquatic organisms. Xu et al. (2007) demonstrated the inhibitory effect of electrolysis on Microcystis aeruginosa and proposed further research on other species. As the mechanism of action of conventional algicidals was shown to affect the release of toxins in M. aeruginosa-treated populations, ethyl 2-methylacetoacetate (EMA) was preferred to copper sulphate, hydrogen peroxide or diuron as cell membrane remains its integrity longer (Zhou et al. 2013). However, despite the measures described, for drinking water resources, massive liberation of toxins has made that flocculating agents such as lime or alum had been suggested (Lam et al. 1995).
在湖泊或潟湖等淡水系統中，經常使用化學物質（AWWA，2004 年；Chen 等人，2011a,b）。據觀察，在淡水中採取這些幹預措施的風險較小，這不僅是因為存在明確的限制，還因為要使用化學物質的自然棲息地已被認為受到污染/惡化。在其他情況下，如物理方法一樣，由於飲用水供應受到影響，必須進行幹預。毫無疑問，殺藻劑的主要特徵是不會造成二次污染。氯化物或氧化劑（硫酸銅、過氧化氫、 等）等短效分子可以滿足此要求。過氧化氫在淡水中的低濃度 是有效的。 Bauzá 等人，2014 年）。微囊藻毒素（微囊藻毒素）被認為具有肝毒性，而 anatoxin-a（由 Anabaena 屬產生）則是一種神經毒素。因此，必須將它們從飲用水或灌溉水中去除。與其他殺藻劑相比，過氧化氫能在自然紫外線輻射的幫助下破壞微囊藻毒素（Bauzá 等人，2014 年）。同樣，光催化降解微囊藻毒素也是可行的（Shephard 等人，1998 年）。水電解可在原位產生活性氧，而不會對其他水生生物造成嚴重影響。 Xu 等人（2007 年）證實了電解對銅綠微囊藻的抑製作用，並建議進一步研究其他物種。由於傳統殺藻劑的作用機制被證明會影響銅綠微囊藻處理族群的毒素釋放，2-甲基乙醯乙酸乙酯（EMA）比硫酸銅、過氧化氫或雙脲更能維持細胞膜的完整性（Zhou 等，2013 年）。然而，儘管採取了上述措施，但對於飲用水資源而言，毒素的大量釋放使得人們建議使用石灰或明礬等絮凝劑（Lam 等，1995 年）。

Regarding seawater species, hydrogen peroxide was proved effective against cysts of G. catenatum (Bolch & Hallegraeff 1993), A. tamarense and A. catenella (Ichikawa et al. 1993) contained in ship's ballast waters. and require doses even lower and , respectively) (Lam et al. 1995). Ozonation of seawater oxidizes bromide, which is a weak but stable disinfectant. Its effect on several marine taxa of HAB has been tested through on several species such as K. brevis, Prorocentrum triestinum, Scrippsiella trochoidea, Karenia digitale and Amphidinium sp. . Due to the ozone use conditions, its use was recently recommended in ballast water tanks of ships. (Anderson et al. 2017). A good part of the research in this field was not published in international journals but registered in regional reports or journals (most of them not written in English). Especially relevant is the CEARAC report, which summarizes the initiatives carried out in the China-Korea-Japan-Russia region (NOWPAP CEARAC, 2007). In this report, the countermeasures evaluated up to 2007 were described. In China, a number of substances were assayed, for instance, hydroxyl radicals (against Gymnodinium mikimotoi), disinfectants such as quaternary ammonium compounds (against H. akashiwo), alkylpolyglycoside or chlorine dioxide (against Phaeoecystis globose), herbicides such as bromogeramine (against Prorocentrum micans) or tertbutyl triazine. These studies did not evaluate the impact on the environment, and most of them were conducted in laboratory assays. However, with hydroxyl radicals maritime enclosures were effectively used in the shore of Jiaozhou Gulf (Qingdao) (Xiyao et al. 2003). On the other hand, extensive work was carried out in Japan on the possibilities of hydrogen peroxide both in laboratory and enclosures (seawater and freshwater) although, as in the case of Chinese studies, not published in international journals. The inhibiting effect of peroxide was tested on vegetative cells and cysts of Chattonella marina
在海水物種方面，過氧化氫被證明對船舶壓載水中的 G. catenatum（Bolch 和 Hallegraeff，1993 年）、A. tamarense 和 A. catenella（Ichikawa 等人，1993 年）孢囊有效。 和 所需的劑量甚至分別低於 和 。 Lam等人，1995 年）。海水經臭氧處理後會氧化溴，溴是一種弱但穩定的消毒劑。透過對 K. brevis、Prorocentrum triestinum、Scrippsiella trochoidea、Karenia digitale 和 Amphidinium sp..由於臭氧的使用條件，最近建議在船舶壓載水艙中使用臭氧。 (安德森等人，2017 年）。該領域的大部分研究都沒有在國際期刊上發表，而是發表在地區報告或期刊上（其中大部分都不是用英文撰寫的）。其中特別重要的是中國-韓國-日本-俄羅斯區域海洋研究和培訓中心的報告，該報告總結了在中國-韓國-日本-俄羅斯區域開展的活動（NOWPAP CEARAC，2007 年）。該報告介紹了截至 2007 年所評估的因應措施。在中國，對許多物質進行了檢測，例如羥基自由基（針對米氏藻類）、消毒劑，如季銨鹽化合物（針對H. akashiwo）、烷基多醣苷或二氧化氯（針對球囊藻類） 、除草劑，如溴麥草畏（針對微囊藻類）或叔丁基三嗪。這些研究沒有評估對環境的影響，而且大多數研究都是在實驗室中進行的。不過，在膠州灣（青島）海岸有效地使用了羥基自由基海洋圍欄（Xiyao 等，2003 年）。另一方面，日本在實驗室和圍欄（海水和淡水）中對過氧化氫的可能性進行了廣泛的研究，但與中 國的研究一樣，這些研究並未在國際期刊上發表。對過氧化氫的抑製作用進行了測試，結果表明，過氧化氫對無性細胞和 Chattonella marina 的包囊有抑製作用。
and Gymnodinium mikimotoi, among others. Hydrogen peroxide was found to cause abnormal swimming behaviour and death to fish. This is in concordance with the recent findings of Dorantes-Aranda et al. (2015). Other products assayed were disinfectants (i.e. acrinol which also resulted toxic for fish) and copper sulphate (laboratory and offshore field experiment (1966)).
和 Gymnodinium mikimotoi 等。研究發現，過氧化氫會導致魚類游泳行為異常和死亡。這與 Dorantes-Aranda 等人（2015 年）最近的研究結果一致。其他化驗的產品包括消毒劑（即也會導致魚類中毒的丙烯醇）和硫酸銅（實驗室和近海實地實驗（1966 年））。

Recently, novel algicidals (more selective) for undesirable species have been found. In general, these molecules required less concentrations to be effective, have short persistence time and show low or no toxicity to other species. For example, an anthraquinone derivative was tested in limnocorrals against O. perornata (Schrader et al. 2003). Anthraquinone has a half-life of 19 h. and is nontoxic to other phytoplankton species nor cultured fish. For seawater species, several molecules have also been proposed. Short synthetic peptides ) were shown to be detrimental to . akashiwo and . minimum (seawater red tide organisms) and nontoxic to other species of interest in in vitro and in vivo assays (Park et al. 2016b). On the other hand, low molecular weight water-soluble chitosan disrupted red tide dinoflagellates and raphidophytes' membranes and its chloroplasts within at concentrations ranging (Park et al. 2016a). At these concentrations, nontoxic species were not affected. Algicidals such as TD49 (Baek et al. 2014) (algicidal thiazolidinedione derivative) and -[(3,4-dichlorophenyl)methyl]cyclohexanamine (DP92) (Cho et al. 2016) were shown to be selective even between seawater harmful species. These substances required cell-to-cell contact so water solubility poses a problem. Encapsulation in cationic liposomes of DP92 overcame this problem maximizing the cell removal (Cho et al. 2016).
最近，人們發現了對不良物種具有更強選擇性的新型殺藻劑。一般來說，這些分子所需的有效濃度較低，持續時間較短，對其他物種的毒性較低或沒有毒性。例如，一種蒽醌衍生物 在石灰華中對 O. perornata 進行了測試（Schrader 等人，2003 年）。蒽醌的半衰期為 19 小時，對其他浮游植物物種和養殖魚類均無毒性。對於海水物種，也提出了幾種分子。短合成勝肽 ) 對{{2}.akashiwo 和 ..minimum （海水紅潮生物）有害，而在體外和體內試驗中對其他相關物種無毒（Park 等人， 2016b）。另一方面，在 濃度範圍內，低分子量水溶性殼聚醣可在 內破壞赤潮甲藻和蚜藻的膜及其葉綠體（Park 等人，2016a）。 (Park 等人，2016a）。在這些濃度下，無毒物種不受影響。殺藻劑如TD49（Baek 等人，2014 年）（殺藻噻唑烷二酮衍生物）和 -[(3,4-二氯)-[（3,4-二氯苯基）甲基]環己胺(DP92) （Cho 等人，2016 年）已被證明甚至在海水有害物種之間也具有選擇性。這些物質需要細胞間的接觸，因此水溶性是個問題。將 DP92 封裝在陽離子脂質體中克服了這個問題，最大限度地清除了細胞（Cho 等人，2016 年）。

An alternative method consists in inducing flocculation and later sedimentation using flocculating agents. In the 'flocculation' control process, it is required that both coagulation-flocculation and sedimentation be produced.
另一種方法是使用絮凝劑誘導絮凝，然後進行沉澱。在 "絮凝 "控制過程中，需要同時產生混凝-絮凝和沈澱。

Adhesion process. The chemical nature of the substratum will determine the adhesion process of the target HAB species. The cell-cell and cell-substratum interactions have been comprehensively described by DLVO theory and more recently by the extended DLVO theory (XDVLO) (Van Oss & Giese 1995), which introduces the contribution of the electrostatic forces. The DLVO theory was first proposed for colloidal systems although its applicability for living cells seems to be generally accepted. This is as well the case of microalgae (Ozkan & Berberoglu 2013; Nabweteme et al. 2015; Ndikubwimana et al. 2015).
附著過程。基質的化學性質將決定目標 HAB 物種的黏附過程。 DLVO 理論全面描述了細胞-細胞和細胞-基質之間的相互作用，最近的擴展 DLVO 理論（XDVLO）（Van Oss & Giese，1995 年）則引入了靜電力的作用。 DLVO 理論最初是針對膠體系統提出的，但其對活細胞的適用性似乎已被普遍接受。微藻也是如此（Ozkan 和 Berberoglu，2013 年；Nabweteme 等人，2015 年；Ndikubwimana 等人，2015 年）。
According to the XDLVO theory, the total energy of interaction of two surfaces is comprised of three forces: (i) Lifshitz-Van de Waals (LVW), (ii) acid-base (AB) and (iii) electrostatic (EL). Van der Waals forces which account for asymmetrical distribution of electrons are typically attractive. However, Ozkan and Berberoglu predicted that LVW forces to be repulsive for the interaction of hydrophobic surfaces with various diatoms (Ozkan & Berberoglu 2013). On the other hand, EL forces depend on the surfaces' charge, showing a repulsive interaction for same-charge surfaces. Micro-organisms usually have a negatively charged surface due to amine, carboxyl and hydroxyl groups. Both freshwater and seawater microalgae have been shown to exhibit negative surface charge (Sengco 2001; Yu et al. 2004; Rosa et al. 2017). Although the charge magnitude is lower in seawater species. forces can be attractive or repulsive based on the surface free energy of the cell and the substratum. Consequently, hydrophobic cells will colonize easily a hydrophobic surface whereas hydrophilic surfaces will show more resistance to cell adhesion. Similarly, hydrophobic cells show greater tendency to form flocs than hydrophilic cells. The overall force of attraction (or repulsion) is the sum of three forces and depends on the distance. LVW and AB forces are of shorter range than EL. According to the XDLVO theory, the force balance allows calculating an energy and a distance of interaction. XDLVO forces can be reasonably well calculated for microalgae systems (Ozkan & Berberoglu 2013; Nabweteme et al. 2015). EL forces can be calculated using physicochemical properties (e.g. zeta potential, ), whereas LVW and AB are obtained by measuring the contact angle on different solvents (polar and nonpolar) and applying the Young's equation (Nabweteme et al. 2015). When this is carried out, the forces magnitude can be compared. In Figure 1, data calculated by Ozkan and Berberoglu (Ozkan & Berberoglu 2013) for different diatoms and microalgae (both hydrophobic and hydrophilic) have been averaged to illustrate the interaction forces' order of magnitude. However, it must be taken into account that the cell surfaces may change with time (for example, during growth phases, nutrient limiting conditions), resulting in lower flocculation efficiencies (Sengco et al. 2005).
根據 XDLVO 理論，兩個表面相互作用的總能量由三種力組成：(i) 利夫希茨-范德華力（LVW），(ii) 酸鹼力（AB）和 (iii) 靜電力（EL）。由於電子分佈不對稱，范德華力通常具有吸引力。然而，Ozkan 和 Berberoglu 預測，在疏水錶面與各種矽藻的相互作用中，范德華力是排斥力（Ozkan 和 Berberoglu，2013 年）。另一方面，EL 力取決於表面的電荷，顯示相同電荷表面的排斥相互作用。由於胺基、羧基和羥基的存在，微生物表面通常帶負電荷。淡水和海水微藻都表現出表面負電荷（Sengco，2001 年；Yu 等人，2004 年；Rosa 等人，2017 年）。雖然海水物種的電荷量較低。根據細胞和基質的表面自由能， 力可能是吸引的，也可能是排斥的。因此，疏水性細胞很容易在疏水性表面定殖，而親水性表面則對細胞黏附表現出更大的阻力。同樣，疏水細胞比親水細胞更容易形成絮狀物。總的吸引力（或排斥力）是三種力的總和，取決於距離。 LVW 力和 AB 力的作用距離比 EL 力短。根據 XDLVO 理論，力平衡可以計算相互作用的能量和距離。 XDLVO 力可以很好地計算微藻系統（Ozkan 和 Berberoglu，2013 年；Nabweteme 等，2015 年）。 EL 作用力可透過理化性質（如zeta 電位， ）計算得出，而LVW 和AB 則可透過測量不同溶劑（極性和非極性）上的接觸角並應用楊氏方程式計算得出（Nabweteme 等人，2015 年）。這樣就可以比較力的大小。在圖 1 中，對 Ozkan 和 Berberoglu（Ozkan 和 Berberoglu，2013 年）計算的不同矽藻和微藻（疏水性和親水性）的數據進行了平均，以說明相互作用力的大小順序。然而，必須考慮到細胞表面可能會隨著時間的推移而改變（例如，在生長階段、營養限制條件下），從而導致絮凝效率降低（Sengco 等人，2005 年）。

The surfaces can be attached in the so-called primary minimum (close contact; Fig. 1) or forming a weaker union at a greater distance. This last situation would imply repulsive and forces, resulting in an overall force of interaction one order of magnitude lesser than that calculated for the primary minimum (Ozkan & Berberoglu 2013). This was the case for hydrophilic green algae on hydrophilic surfaces (e.g. stainless steel or glass) (Ozkan & Berberoglu 2013). When EL forces are of greater importance, an energy barrier must be overcome to observe
這些表面可以以所謂的原最小值（緊密接觸；圖 1）相連，也可以在較遠的距離形成較弱的結合。最後一種情況意味著 和 的排斥力，導致總體交互作用力比計算出的原生最小值小一個數量級（Ozkan 和 Berberoglu，2013 年）。親水錶面（如不鏽鋼或玻璃）上的親水綠藻就是這種情況（Ozkan 和 Berberoglu，2013 年）。當 EL 力更為重要時，必須克服能量障礙才能觀察到

Figure 1 Averaged Energy of interaction of diatoms and microalgae over different surfaces. Data from: Ozkan & Berberoglu (2013). ITO, indium-tin oxide; PE, polyethylene; PS, polystyrene; PC, polycarbonate; SS, stainless steel. ( ) glass; ( ) ITO; PE; PS; PC; ( SS. AB, acid-base; EL, electrostatic; LW, Lifshitz-van der Waals.
圖 1 矽藻和微藻在不同表面上相互作用的平均能量。資料來自：Ozkan & Berberoglu（2013 年）。 ITO，氧化銦錫；PE，聚乙烯；PS，聚苯乙烯；PC，聚碳酸酯；SS，不銹鋼。 ( ) 玻璃；( ) ITO； PE； 不鏽鋼。 PE; PS； PC； ( SS.AB：酸鹼；EL：靜電；LW：Lifshitz-van der Waals。

adhesion at the primary minimum. Kinetic energy supplied to cells could be sufficient to get over this barrier. For diatoms, Ozkan and Berberoglu estimated an average velocity of (Ozkan & Berberoglu 2013), which is easily provided in natural conditions due to sea turbulence or, even, swimming behaviour (Peters & Marrase 2000).
黏附在初級最低點。提供給細胞的動能足以跨越此障礙。對於矽藻，Ozkan 和 Berberoglu 估計平均速度為 （Ozkan 和 Berberoglu，2013 年）。 （Ozkan 和 Berberoglu，2013 年），在自然條件下，由於海水湍流或游泳行為（Peters 和 Marrase，2000 年），這種速度很容易達到。

The fact that at very low the amine, carboxyl and hydroxyl groups are partially protonated has been used to induce flocculation in harvesting steps of microalgae cultures (Liu et al. 2014). At high pH, auto-flocculation is also produced, but attributed to cations insolubilization (Molina Grima et al. 2003). The electrostatic double layer is compressed in high ionic media reducing its contribution (Cui et al. 2014). Consequently, it has been suggested that, in seawater, a lesser contribution of the EL force will determine that adhesion be controlled by AB forces (Nabweteme et al. 2015). When flocculation is to be induced, addition of positive ions can destabilize the suspension by neutralizing negative charges. Indeed, a good number of flocculants are cationic polyelectrolytes (Granados et al. 2012). For microalgae, has been proposed as an indicative of the suspension's stability (Yu et al. 1999), as at low (absolute value), the repulsion of the double layer is minimum and surfaces are able to be close enough to sense LVW and AB forces (Henderson et al. 2008; Kwak & Kim 2015). Henderson et al. (2008) optimized algae and biomass removal with values between and . However, as described above it is the contribution of the three forces what determines the flocculation process. Billuri et al. (2015) showed that complete charge neutralization was not related to maximum flocculation. Liu et al. (2016a) showed that the positive value of zeta potential did not correlate with removal efficiency using aluminiummodified clays as flocculating agent. Besides charge neutralization, additional mechanisms affecting particles in suspension could contribute to flocculation when clays are modified (Li et al. 2015). Moreover, as is depicted in Figure forces determined the adhesion process as they are by far greater and the energy barrier of EL forces is easily overcome with kinetic energy.
在極低的 中，胺基、羧基和羥基會部分質子化，這一事實已被用於在微藻培養的收穫步驟中誘導絮凝（Liu 等人，2014 年）。在高 pH 值條件下，也會產生自動絮凝，但歸因於陽離子不會溶解（Molina Grima 等人，2003 年）。在高離子介質中，靜電雙層會被壓縮，從而降低其作用（Cui 等，2014 年）。因此，有人認為，在海水中，EL 力的貢獻較小，這將決定黏附由 AB 力控制（Nabweteme 等人，2015 年）。在誘導絮凝時，加入正離子可透過中和負電荷來破壞懸浮液的穩定性。事實上，許多絮凝劑都是陽離子聚電解質（Granados 等人，2012 年）。對於微藻來說， 被認為是懸浮液穩定性的指標（Yu 等，1999 年），因為在低 （絕對值）的情況下， 與 之間的斥力會增加。 (絕對值）時，雙層的斥力最小，表面能夠接近到足以感應到 LVW 和 AB 力（Henderson 等人，2008 年；Kwak & Kim，2015 年）。 Henderson 等人（2008 年）優化了 值在 和 之間的藻類和生物量去除效果。 .然而，如上所述，決定絮凝過程的是三種作用力的貢獻。 Billuri 等人（2015 年）的研究表明，電荷完全中和 與最大絮凝度無關。 Liu 等人（2016a）的研究表明，使用鋁改質黏土作為絮凝劑，zeta 電位的正值與去除效率無關。除了電荷中和之外，影響懸浮顆粒的其他機制也可能在改性黏土時促進絮凝（Li 等人，2015 年）。此外，如圖 所示，力決定了黏附過程，因為它們遠比電荷中和作用力大，而且電荷中和作用力的能量障礙很容易被動能克服。

Biofilm formation was shown to be related to the critical surface energy in biofouling studies (Baier 2006). A similar approach has also been employed for microalgae and tested with both fresh and seawater species (Cui & Yuan 2013). According to Baier, for surfaces with a critical surface energy of the adhesion is minimum, regardless of the material (Baier 2006). The critical surface energy accounts for the surface tension that provokes a zero degrees angle when liquid and solid are in contact (Baier 2006). For solids with a critical surface energy of , water is able to wet the surface completely. This value of surface tension and is very close to the dispersive component for water (Van de Waals forces) (Baier 2006). This concept is not only related to interaction forces between surfaces but also to the relative
在生物污損研究中，生物膜的形成與臨界表面能有關（Baier，2006 年）。微藻也採用了類似的方法，並對淡水和海水物種進行了測試（Cui & Yuan，2013 年）。根據 Baier 的觀點，對於臨界表面能為 的表面，無論材料如何，附著力都是最小的（Baier，2006 年）。臨界表面能是指液體和固體接觸時產生零度角的表面張力（Baier，2006 年）。對於臨界表面能為 的固體，水能夠潤濕其表面。的固體，水能夠完全潤濕其表面。這個表面張力值非常接近水的分散成分（范德華力）（Baier，2006 年）。這個概念不僅與表面之間的相互作用力有關，也與水的相對錶面張力有關。
interaction between these surfaces and the liquid medium. In reality, what is observed at this value of surface tension is a very hydrophilic surface. Certain controversy is arisen when the adhesion process is studied from different perspectives. In supported cultures or biofouling materials, the main concern is knowing whether a biofilm will develop on a surface and how strong will the adhesion be, whereas in flocculation, the focus is on the velocity of the process. Eventually, every surface is colonized trough physical or biological mechanisms. The latter could include a previous adhesion of proteins which alter the chemistry of the surface (Vladkova 2007) and the aid of pili, flagella, mucilage or exopolysaccharides production (Schuergers & Wilde 2015). Biological processes of adhesion need greater times (hours or days) than those required for a rapid flocculation of a stable suspension of cells. For the initial stage, when nonautoflocculating cells are involved, only thermodynamic mechanisms should be considered. The topography of a surface is other area of interest for the adhesion process. It has been shown that the surface texture tends to increase biological adhesion of microalgae to a substratum (Gross et al. 2016), which is of paramount relevance in supported biofilm reactors. A specific topography can provoke that the cells form a more stable biofilm that resists turbulence (Hoipkemeier-Wilson et al. 2004). With respect to flocculation of harmful microalgae and cyanobacteria, not only is desirable a rapid coagulation and sedimentation but also it is crucial the conformation of a stable biofilm that avoid cells detachment under the turbulence levels found in natural systems. In principle, roughness scales of the size of the cells are more favourable to biological adhesion (Hoipkemeier-Wilson et al. 2004).
這些表面與液體介質之間的相互作用。實際上，在此表面張力值下觀察到的是非常親水的表面。從不同角度研究黏附過程會產生一些爭議。在支持培養物或生物污垢材料中，主要關注的是生物膜是否會在表面上形成以及黏附力有多強；而在絮凝過程中，關注的焦點則是黏附過程的速度。最終，每個表面都會透過物理或生物機制形成菌落。後者可能包括改變表面化學性質的蛋白質先前附著（Vladkova，2007 年），以及纖毛、鞭毛、黏液或外多醣的產生（Schuergers & Wilde，2015 年）。與細胞穩定懸浮液快速絮凝所需的時間相比，生物黏附過程需要更長的時間（數小時或數天）。在初始階段，當涉及非自動絮凝細胞時，只需考慮熱力學機制。表面形貌是黏附過程中另一個值得關注的面向。研究表明，表面紋理往往會增加微藻對基質的生物黏附性（Gross 等人，2016 年），這在支撐生物膜反應器中至關重要。特定的地形可促使細胞形成更穩定的生物膜，從而抵禦湍流（Hoipkemeier-Wilson 等人，2004 年）。對於有害微藻和藍藻的絮凝，不僅需要快速的凝結和沈澱，還需要形成穩定的生物膜，以避免細胞在自然系統中的湍流水平下脫落。原則上，與細​​胞大小相當的粗糙度更有利於生物黏附（Hoipkemeier-Wilson 等人，2004 年）。

Flocculating agents. For the sedimentation process, the particle-cells floccule must have a mass that allow settling in natural waters where a certain level of turbulence is always present. Sand or clay particles have been used as ballast to improve sedimentation properties of floccules. That fact, together with the availability (and biocompatibility) of clays, has made that these materials had been used almost exclusively to HAB control especially in seawater. Van Oss and Giese studied the surface thermodynamic properties of clay minerals establishing an interfacial free energy of interaction between clay particles and water (Van Oss & Giese 1995). A typical clay material is in the boundary between hydrophobicity and hydrophilicity (Van Oss & Giese 1995). In consequence, they are not ideal substratum for adhesion. As natural clays are besides negatively charged, they do not seem to be the ideal flocculant (Sengco 2001). So far, there is not a uniform description of clays. Since antiquity, these materials have been used and studied from different perspectives giving rise to different and sometimes contradictory terminology. An integrating definition was proposed by the joint nomenclature committees (JNCs) of the Association Internationale pour l'Etude des Argiles (AIPEA) and the Clay Minerals Society (CMS). In such a definition clays were described according to its size, physical plasticity, behaviour under fire and its natural origin. On the other hand, clay minerals are phyllosilicate minerals which confers clays its characteristic properties (examples of mineral clay are kaolinite, vermiculite, rectorite, montmorillonite, etc.). In most of laboratory assays, the mineral clays used have been mainly comprised of kaolinite and montmorillonite. However, the terms clays and mineral clays have been used indistinctly in several applied fields including this one. Mineral clays show an anisotropic layered structure and are easily modified both internally and superficially by adsorption, ion exchange or grafting (Bergaya et al. 2006). Defining a characteristic behaviour for the group is troublesome due to the heterogeneity and diversity of the group and the effect that impurities and the environment could have on clays. Natural clays are typically a mix of different mineral clays, associated minerals, humic mater, water and heterogeneous impurities (Carrado et al. 2006). Surface properties of mineral clays are determined by oxygen atoms involved in bonds, unless isomorphous substitutions exist. This could confer the clay a hydrophobic character. Hydrated cations (e.g. in smectites or vermiculites), defects on surface or exposure of hydroxyl groups (as in kaolinite) may create hydrophilic areas (or even overall hydrophilicity) on the material surface (Nulens et al. 1998). In contrast to 2:1 phyllosilicates (e.g. montmorillonite), 1:1 phyllosilicates (e.g. kaolin) show tightly packed layers and an overall neutral layer charge. On the other hand, 2:1 phyllosilicates exhibit negative charge in the unmodified form, but a greater porosity and absorptivity makes that, in the practice, these clays can have a positive charge (Bergaya et al. 2006). Sengco demonstrated that negative charge of montmorillonites and zeolites is totally neutralized in seawater (Sengco 2001). Moreover, pH and ionic strength were shown to have effect on zeta potential ( ) (Yu et al. 2004; Liu et al. 2016a) and on hydrophilic/ hydrophobic character (Nulens et al. 1998). For example, using a modified natural clay and PAC), Liu et al. (Liu et al. 2016a) obtained zeta potentials more positive on distilled water than on seawater when was below 7.5. Greater values resulted in a slight positive charge in SW and negative values for DW (Liu et al. 2016a). Consequently, if we consider that in flocculation studies, natural clays were used, then it is unavoidable that irreproducible or even contradictory results have been produced (Sengco & Anderson 2004).
絮凝劑。在沉澱過程中，絮凝體的顆粒細胞必須具有一定的質量，以便在始終存在一定湍流的自然水域中沉澱。沙子或黏土顆粒被用作壓艙物，以改善絮凝體的沉澱特性。這一事實，再加上粘土的可用性（和生物相容性），使得這些材料幾乎專門用於控制有害藻類繁殖，尤其是海水中的有害藻類繁殖。 Van Oss 和 Giese 研究了黏土礦物的表面熱力學特性，確定了黏土顆粒與水之間相互作用的界面自由能（Van Oss 和 Giese，1995 年）。典型的黏土材料介於疏水性和親水性之間（Van Oss 和 Giese，1995 年）。因此，它們不是理想的黏附基質。天然黏土除了帶負電之外，似乎也不是理想的絮凝劑（Sengco，2001 年）。到目前為止，對黏土還沒有統一的描述。自古以來，人們從不同的角度使用和研究這些材料，從而產生了不同的術語，有時甚至是相互矛盾的術語。國際黏土研究協會（AIPEA）和黏土礦物協會（CMS）的聯合命名委員會（JNCs）提出了一個統一的定義。在這個定義中，黏土是根據其大小、物理可塑性、在火中的表現及其天然來源來描述的。另一方面，黏土礦物是植物矽酸鹽礦物，它賦予了黏土特有的性質（礦物黏土的例子有高嶺石、蛭石、雷打石、蒙脫石等）。在大多數實驗室化驗中，使用的礦物黏土主要包括高嶺石和蒙脫石。不過，在包括本領域在內的多個應用領域中，黏土和礦物黏土這兩個術語的使用並不一致。礦物黏土具有各向異性的層狀結構，很容易透過吸附、離子交換或接枝等方式對其內部和表面進行改質（Bergaya 等人，2006 年）。由於黏土的異質性和多樣性，以及雜質和環境可能對黏土產生的影響，要確定該類黏土的特徵行為非常困難。天然黏土通常由不同的礦物黏土、伴生礦物、腐殖質、水和雜質混合而成（Carrado 等人，2006 年）。礦物黏土的表面特性由參與 鍵的氧原子決定，除非有同構替代。這可能會使粘土具有疏水特性。水合陽離子（如 如高嶺石），表面缺陷或羥基暴露可能會在材料表面形成親水性區域（甚至整體親水性）（Nulens 等人，1998 年）。與 2:1 的植矽體（如蒙脫石）相比，1:1 的植矽體（如高嶺土）顯示出緊密的堆積層和整體的中性層電荷。另一方面，2:1 植物矽酸鹽在未經改性的情況下顯示負電荷，但由於孔隙率和吸收性較大，在實際應用中，這些黏土可能帶有正電荷（Bergaya 等人， 2006 年）。 Sengco 證實，蒙脫石和沸石的負電荷在海水中會被完全中和（Sengco，2001 年）。此外，pH 值和離子強度對 zeta 電位（ ）（Yu 等人，2004 年；Liu 等人，2016a）和親水/疏水特性（Nulens 等人，1998 年）也有影響。例如，Liu 等人（Liu et al. 2016a）使用改質天然黏土 和 PAC，當 低於 7.5 時，蒸餾水的 zeta 電位比海水的 zeta 電位更更正。 值越大，海水中的電荷就越正，而蒸餾水中的電荷就越負（Liu 等，2016a）。因此，如果我們考慮到在絮凝研究中使用的是天然黏土，那麼不可避免地會產生不可重複甚至矛盾的結果（Sengco 和 Anderson，2004 年）。

The mechanism of flocculation enhancement of biopolymers has been explained in several works (Zou
生物聚合物增強絮凝作用的機制在一些著作中已有解釋（Zou

Figure 2 Mechanisms of flocculation in microalgae control strategies.
圖 2 微藻控制策略中的絮凝機制。

et al. 2006; Li & Pan 2013; Ndikubwimana et al. 2015; Wang et al. 2015), although different terminology has been used so far. When a flocculant acts as a bridge between cells, the mechanism is called 'bridging,' but if the entire cell surface is covered, then it is named 'patching' (Ndikubwimana et al. 2015). 'Netting' stands for the process of entrapment in a floccule. Miao et al. (2013) distinguished between chemical bonding and 'netting' (chemical or physical entrapment). On the other hand, 'sweeping' is produced when the ballast (or floccule) in its way down, sweep along a target cell. Terms such as 'netting,' 'sweeping' or 'patching' are ambiguous. Moreover, in our opinion, these terms do not illustrate the actual mechanism that ultimately controls the cell removal. In Figure 2, the flocculation processes described so far are illustrated in an integrating scheme. The steps required to cell removal are (i) encounter (cell-cell; cell-ballast; cell-biopolymer; cell-floccule); (ii) physical-chemical attraction (cation-aided, acid-base interaction); (iii) sedimentation (floccule, ballast-driven). The first step is often vital as a low encountering probability would result in low flocculation efficiency. For this reason, delivery method should be carefully studied. Flocculation agents could autoflocculate (depending, among other factors, on and salinity). To avoid this, flocculants are typically delivered forming a slurry and/or sprayed over the bloom-forming species (Pan et al. 2006b). Yu et al. hypothesized that interparticle encounters are favoured under mixing and, hence, greater in turbulent waters ( et al. 2004). A certain chemical or biomolecule could improve the cell removal acting on one or more of the steps. For instance, a 'bridging' effect between small flocs produces greater flocs with different sedimentation properties and greater 'netting' effect. In that sense, and Pan found that flocculation produced by cation addition (electrostatic interactions) resulted in 'fluffy' flocs with worse sedimentation, whereas the addition of polyelectrolytes formed greater flocs (Li & Pan 2013). In addition, it has been shown that environmental parameters (e.g. pH) during floc formation can influence floc stability with effects on algae resuspension (Shi et al. 2016).
等人，2006 年；Li & Pan，2013 年；Ndikubwimana 等人，2015 年；Wang 等人，2015 年），但迄今為止使用的術語有所不同。當絮凝劑在細胞之間起橋樑作用時，這種機制被稱為 "橋接"，但如果整個細胞表面都被覆蓋，則被稱為 "修補"（Ndikubwimana 等人，2015 年）。網狀"代表的是絮團中的夾帶過程。Miao 等人（2013 年）對化學鍵和"網狀"（化學或物理夾帶）進行了區分。另一方面，當壓艙物（或絮凝體）在下行過程中沿著目標細胞掃動時，就會產生"掃動"。網狀"、"橫掃"或"修補"等術語都是模棱兩可的。此外，我們認為這些術語並不能說明最終控制細胞去除的實際機制。圖 2 以整合方案的形式展示了迄今為止所描述的絮凝過程。細胞去除所需的步驟是：(i) 遭遇（細胞-細胞；細胞-壓載物；細胞-生物聚合物；細胞-絮凝體）；(ii) 物理化學吸引（陽離子輔助、酸鹼相互作用） ；(iii) 沉澱物（絮凝體、壓載物驅動）。第一步通常至關重要，因為相遇機率低會導致絮凝效率低。因此，應仔細研究投放方法。絮凝劑可能會自動絮凝（除其他因素外，還取決於 和鹽度）。為避免這種情況，絮凝劑通常以漿液形式投放和/或噴灑在形成藻華的物種上（Pan 等人，2006b）。 Yu 等人提出的假設是，在混合狀態下，粒子間的相遇更有利，因此，在湍流水域中，粒子間的相遇會更頻繁（ 等人，2004 年）。某種化學物質或生物大分子可以改善對一個或多個步驟的細胞清除作用。例如，小絮凝體之間的 "橋接 "效應會產生沉積特性不同的大絮凝體，並產生更大的 "網狀 "效應。從這個意義上說， 和潘發現，陽離子添加（靜電相互作用）產生的絮凝會導致沉降性較差的"蓬鬆"絮凝體，而添加聚電解質則會形成更大的絮凝體（李和潘，2013 年）。此外，研究表明，絮凝體形成過程中的環境參數（如 pH 值）會影響絮凝體的穩定性，進而影響藻類的再懸浮（Shi 等人，2016 年）。

For freshwater species, conventional all-purpose flocculants and clays have been assayed. Wang et al. (2012) presented a two-step protocol to remove in the field a bloom of colonial Microcystis where was first added to inactivate the cells and then polyferric sulphate (PFS) and sediments were used to flocculate and induce sedimentation. Despite adding PFS , the dry sediment concentration required was as high as (Wang et al. 2012). Clays showed better results, although removal was shown to be species specific. Bentonite was more efficient than kaolinite against Microcystis spp. in static or flow (Couette) experiments (Verspagen et al. 2006). Moreover, different natural strains of Microcystis showed dissimilar results (Verspagen et al. 2006). In various works of a same series (Pan et al. 2006a; Zou et al. 2006), several clays with and without modifications (ferric oxide and chitosan) were assayed with M. aureginosa. Sepiolite was selected due to best performance flocculating M. aureginosa (Pan et al. 2006a). This mineral clay has a 2:1 phyllosilicate structure lacking continuous octahedral sheets that results in a fibrous habit with high surface (Galan 1996). Local charge and the netting/ bridging properties of this fibrous clay were assumed to cause the flocculation (Pan et al. 2006a). Clays in freshwater are less effective than in seawater. This is attributed to the adsorption of ions and humics on clay's surface, which has been shown to reduce the double layer thickness in natural seawater (Sengco 2001). As was demonstrated by Pan et al. (Pan et al. 2006a), independently of , in freshwater, cyanobacteria and clays present overall negative charge. Therefore, the addition of an electrolyte or a biopolymer (e.g. chitosan) that acts as a bridge between cell and clay could enhance the flocculation process. In a field enclosure of Taihu Lake, Pan et al. (2006b) tested the effectivity of the use of chitosan-modified clays to remove a M. aureginosa bloom. Besides of controlling blooms, these methods contribute to the ecological restoration of in eutrophic shallow lakes (Pan et al. 2011a,b).
對於淡水物種，已對傳統的通用絮凝劑和粘土進行了評估。 Wang 等人（2012 年）提出了一種分兩步驟在野外清除大量繁殖的微囊藻的方案，首先加入 使細胞失活，然後使用聚合硫酸鐵（PFS）和沈積物進行絮凝和誘導沉積。儘管加入了 PFS {{1}所需的乾燥沉積物濃度高達 （Wang 等人，2012 年）。 (Wang 等人，2012 年）。黏土的去除效果較好，但也顯示出了物種特異性。在靜態或流動（Couette）實驗中，膨潤土比高嶺石對微囊藻屬更有效（Verspagen 等，2006 年）。此外，不同的天然微囊藻菌株也顯示出不同的結果（Verspagen 等人，2006 年）。在同一系列的多項研究中（Pan 等人，2006 年a；Zou 等人，2006 年），對幾種經過或未經過改性（氧化鐵和殼聚醣）的粘土進行了奧氏微囊藻檢測。之所以選擇海泡石，是因為它對 M. aureginosa 的絮凝效果最好（Pan 等人，2006a）。這種礦物黏土具有 2:1 的植矽體結構，缺乏連續的八面體片，因此具有高表面的纖維狀習性（Galan，1996 年）。這種纖維狀黏土的局部電荷和網狀/架橋特性被認為是造成絮凝的原因（Pan 等人，2006a）。淡水中的黏土不如海水中的有效。這是因為黏土表面吸附了離子和腐殖質，這已被證明會降低天然海水中的雙層厚度（Sengco，2001 年）。正如 Pan 等人（Pan et al. 2006a）所證實的那樣，與 無關，在淡水中，藍藻也會吸附 。在淡水中，藍藻和粘土總體上帶負電荷。因此，添加電解質或生物聚合物（如殼聚醣）作為細胞與黏土之間的橋樑，可增強絮凝過程。 Pan 等人（2006b）在太湖的實地圍堰中測試了使用殼聚醣改性的 粘土去除水華的效果。除了控制水華，這些方法還有助於富營養化淺水湖泊的生態恢復（Pan 等，2011a,b）。

Many biopolymers such as chitosan or exopolysaccharides have been tested for HAB control in the last years. Although there are recent studies dealing with chitosan's use with HAB species, its use as flocculant was postulated many years ago (Axberg et al. 1980). It was also proven useful for flocculating conventional microalgae (Lubián 1989; Molina Grima et al. 2003). Indeed, different agents acting as flocculation core (sediments, mineral clays, ashes, etc.) supplemented with chitosan were effective against freshwater cyanobacteria (Zou et al. 2006; Pan et al. 2006b; Li & Pan 2015; Wang et al. 2015; Yuan et al. 2016). Doseeffectivity curves can show an optimum from which a decrease is observed (Yuan et al. 2016). Auto-flocculation is the most probable cause, as was demonstrated for several coagulants-flocculants (Sengco 2001). Chitosan-clay flocculation effective concentrations ranged from 0.011 to with . Chitosan, which is also a known adsorbent (Wan Ngah et al. 2011), could additionally remove toxins. A composite from cellulose and chitosan was used as adsorbent for microcystins showing better results than other materials such as activated carbon (Tran et al. 2013).
在過去幾年中，許多生物聚合物（如殼聚醣或外多醣）都曾被測試用於控制有害藻華。儘管最近有研究涉及殼聚醣在 HAB 物種中的應用，但殼聚醣作為絮凝劑的用途早在多年前就已提出（Axberg 等人，1980 年）。事實證明，殼聚醣也可用於絮凝傳統微藻（Lubián，1989 年；Molina Grima 等人，2003 年）。事實上，作為絮凝核心的不同製劑（沉積物、礦物粘土、灰燼等）輔以殼聚醣可有效抑制淡水藍藻（Zou 等人，2006 年；Pan 等人，2006 年b；Li 和Pan，2015年；Wang 等人，2015 年；Yuan 等人，2016 年）。藥效曲線可以顯示出一個最佳值，從該值開始，藥效會逐漸降低（Yuan 等，2016 年）。自絮凝是最可能的原因，這一點在幾種混凝劑-絮凝劑中都得到了證實（Sengco，2001 年）。殼聚醣-黏土絮凝的有效濃度範圍為0.011 到 ，其中 ..殼聚醣也是已知的吸附劑（Wan Ngah 等人，2011 年），它還可以去除毒素。纖維素和殼聚醣的複合材料被用作微囊藻毒素的吸附劑，其效果優於活性碳等其他材料（Tran 等人，2013 年）。

In addition to 'bridging' biopolymers, other biomolecules have been assayed to improve HAB species' removal. For instance, M. oleifera seed extract as modifier of sand (Li & Pan 2013) or exopolysaccharides (EPS) from Pseudomonas aureginosa (Sun et al. 2015). Although in this second case, the much higher concentration required (e.g. Miao et al. 2013; Gu et al. 2015; Li & Pan 2015) puts in question the utility of EPS for flocculating harmful species. On the other hand, bacterial EPS could have other synergistic effects in the HAB termination, like microalgae inhibition or lysis (see Biological control methods). Another known way of improving flocculation is the use of surfactants which could increase the acid-base attraction between cells (or cell-floccule). Liu et al. (Liu et al. 2010) successfully added hexadecyl trimethyl ammonium bromide (a common surfactant) to natural clays targeting Microcystis aeruginosa. As was discussed, for freshwater species, use of mixes including cationic substances and surfactants is obliged due to a low ionic medium and unfavourable particle's surface properties.
除了 "橋接 "生物聚合物外，還對其他生物大分子進行了檢測，以改善有害藻華物種的清除。例如，油橄欖樹籽萃取物作為沙子的改良劑（Li 和 Pan，2013 年）或來自假單胞菌（Pseudomonas aureginosa）的外多醣（EPS）（Sun 等，2015 年）。雖然在第二種情況下，所需的濃度較高（例如Miao 等人，2013 年；Gu 等人，2015 年；Li 和Pan，2015 年），但EPS 在絮凝有害物種方面的效用卻受到質疑。另一方面，細菌 EPS 可在 HAB 終止過程中產生其他協同效應，如抑製或溶解微藻（請參閱生物控制方法）。另一種已知的改善絮凝效果的方法是使用界面活性劑，以增加細胞（或細胞-絮凝體）之間的酸鹼吸引力。 Liu 等人（Liu et al. 2010 年）成功地在針對銅綠微囊藻的天然黏土中添加了十六烷基三甲基溴化銨（一種常見的界面活性劑）。如上文所述，對於淡水物種，由於離子介質含量低和顆粒表面性質不利，必須使用包括陽離子物質和表面活性劑的混合物。

Another evaluated option consists in chemically modifying the clay surface. Acid treatment of clays has been shown to chemically modify the clay structure. For example, treatment of vermiculite was shown to destroy the chemical bonds of Si-O, Si-O-Si and Al-O groups (Miao et al. 2013). As a result, acid-treated vermiculite effectively removed freshwater M. aeruginosa cells in minutes trough charge neutralization (Miao et al. 2013). measures were used to argue that electrostatic neutralization was the main mechanism. However, as was discussed above, an overall negative potential in clay do not necessarily imply inability to flocculate cells (Billuri et al. 2015; Liu et al. 2016b). Tang et al. (2011), on the other hand, related the improvement with the amorphous silica surface structure produced after acid treatment . -treated clay (attapulgite) showed an increase in removal effectivity (Tang et al. 2011). Notwithstanding, Zou et al. found that chemical modification followed by cation addition was less effective than the use of chitosan (Zou et al. 2006). In the work of Dai et al. (2015), acid treatment and later addition of cationic polymers (poly(epichlorohydrin-dimethylamine) and polymeric ferric sulphate) to natural soils were shown to be effective against Microcystis cells in laboratory assays (Dai et al. 2015). A different approach, consisting in fabrication of a new flocculant based on clays, was followed by Gu et al. (2015). These authors synthesized a flocculant
另一種經過評估的方法是對黏土表面進行化學改質。將黏土進行酸處理可對黏土結構進行化學改質。例如，蛭石進行 處理可破壞Si-O、Si-O-Si和Al-O基團的化學鍵（Miao等人，2013年）。因此，經過酸處理的蛭石 能在幾分鐘內透過電荷中和有效去除淡水銅綠微囊藻細胞（Miao 等人，2013 年）。 措施用來論證靜電中和是主要機制。然而，如上文所討論的，黏土中的整體負 電位並不一定意味著無法絮凝細胞（Billuri等人，2015年；Liu等人，2016年b）。另一方面，Tang 等人（2011 年）將 電位的改善與酸處理 後產生的無定形二氧化矽表面結構相關聯。 . -經處理的黏土（attapulgite）的去除效果也有所提高（Tang 等人，2011 年）。儘管如此，Zou 等人發現化學改質後添加陽離子的效果不如使用殼聚醣（Zou 等人，2006 年）。在Dai 等人（2015 年）的研究中，酸處理以及隨後在天然土壤中添加陽離子聚合物（聚（環氧氯丙烷-二甲胺）和聚合硫酸鐵）在實驗室試驗中被證明對微囊藻細胞有效（Dai 等人，2015 年）。 Gu 等人（2015 年）採用了一種不同的方法，即基於黏土製造一種新的絮凝劑。這些作者合成了一種絮凝劑

(ZnO-montmorillonite) where dispersed or embedded nanoparticles produced inhibiting reactive oxygen species on Microcystis aeruginosa cultures. However, in their study, the effects of alone were similar to the synthesized clay and only chlorophyll reduction - instead of flocculated biomass - was determined (Gu et al. 2015). Another example of multipurpose flocculant with excellent results is the licensed clay Phoslock (van Oosterhout & Lürling 2013). This clay binds of phosphorus species reducing one of the triggers of bloom formation. However, required doses are higher than for other modified clays (around ) (Lürling & van Oosterhout 2013; Seger et al. 2015) and its cost is significantly higher ( US ton ) (Blázquez Pallí 2015). Flocculant modifiers (e.g. PAC, chitosan, etc.) could reduce the load although its large-scale application is limited by the costs. Recently, low-cost cationic starch has been proposed as soil modifier to control M. aeruginosa blooms. Application costs for this species were estimated at , which is an important reduction over other solutions such as PAC-clay, whose costs were quantified at (Shi et al. 2016).
(ZnO-蒙脫石），其中分散或嵌入的 奈米粒子對銅綠微囊藻培養物產生抑制活性氧的作用。然而，在他們的研究中，僅 的效果與合成黏土相似，而且只測定了葉綠素減少量，而不是絮凝生物量（Gu 等人，2015 年）。另一個效果極佳的多用途絮凝劑實例是許可使用的粘土Phoslock （van Oosterhout & LL.(van Oosterhout 和Lürling 2013）。這種粘土能與磷結合，減少水華形成的誘因之一。然而，所需劑量高於其他改性粘土（約 ）（Lürling 和van Oosterhout，2013 年；Seger 等人，2015 年），成本也高出許多（ 美 噸 ）（Blázquez Pallí ，2015 年）。絮凝劑改質劑（如PAC、殼聚醣等）可降低負荷，但其大規模應用受到成本的限制。最近，有人提出以低成本的陽離子澱粉作為土壤改良劑來控制銅綠微囊藻藻華。該物種的應用成本估計為 。與其他解決方案（如PAC-粘土，其成本被量化為 ）相比，此成本大大降低（Shi 等人，2016 年）。(Shi 等人，2016 年）。

In field applications in the sea, there are only examples of successful implementation only in Japan (Shirota 1989), Korea (Park et al. 2013) and China (Yu et al. 2017). Despite that, it is believed that the use of clays for marine control through flocculation is the most promising method currently used (Sengco & Anderson 2004; Anderson 2009; Park et al. 2013). In Korea, yellow clay application has become a standardized practice with regional and governmental support. When excessive concentration of HAB species (e.g. Cochlodinium polykrikoides) is found, clay slurry is dispersed from vessels at concentrations of (at least ; Park et al. 2013). This concentration implies a cost of . Park et al. calculated a minimum of 192 US$ per treated hectare with the current methodologies in use (Park et al. 2013). However, clay costs only represent around of total clay treatment costs. For instance, clay dispensers and ships account for the of the total amount (Park et al. 2013). Clay was first used in the field in 1996, after dramatic economic losses in 1995 (Park et al. 2013). Since then, losses due to HABs have been importantly reduced, although it cannot be exclusively attributed to clay dispersal. Other mitigation methods are also used. For example, since 1999, in a good number of facilities, chlorophyll sensors are linked to alarm systems that initiate bubbling on inland and marine aquaculture facilities (Park et al. 2013). Indeed, modern aquaculture centres count on early warning systems that allow activating countermeasures around or in the net pens. For instance, pumping water and feeding are stopped and air is bubbled in the cages. These systems and protocols are described in Physical methods.
在海洋中的實地應用方面，只有日本（Shirota 1989）、韓國（Park 等人，2013 年）和中國（Yu 等人，2017 年）有成功實施的實例。儘管如此，人們認為透過絮凝作用使用黏土控制海洋 是目前最有前途的方法（Sengco 和 Anderson，2004 年；Anderson，2009 年；Park 等人，2013 年）。在韓國，在地區和政府的支持下，施用黃粘土已成為一種標準化做法。當發現 HAB 物種（如 Cochlodinium polykrikoides）濃度過高時，從容器中撒下濃度為 （至少 ）的黏土漿。 (至少 ；Park 等人，2013 年）。這一濃度意味著 的成本。 .Park 等人根據目前使用的方法計算出，每處理一公頃土地的成本至少為 192 美元（Park 等人，2013 年）。然而，黏土成本僅佔黏土處理總成本的 左右。例如，黏土分配器和運輸船佔總費用的 （Park 等，2013 年）。在 1995 年遭受巨大經濟損失之後，黏土於 1996 年首次被用於現場處理（Park 等人，2013 年）。此後，有害藻華造成的損失顯著減少，但這不能完全歸因於黏土的擴散。另外也採用了其他緩解方法。例如，自 1999 年以來，在許多設施中，葉綠素感測器與警報系統相連，啟動內陸和海洋水產養殖設施中的氣泡（Park 等，2013 年）。事實上，現代水產養殖中心依靠預警系統來啟動網箱周圍或內部的應對措施。例如，停止抽水和餵食，並在網箱中鼓氣。物理方法》中介紹了這些系統和規程。

The Korean control system has been revised in two occasions to reduce the quantity of used clay. In a second-generation method, grinded clay was produced with better results, although introducing an unacceptable cost increase. The third-generation-clay-dispersal equipment hydrolyses the seawater previous mixing with the clay. The mixture contains that is an effective algicidal (Jeong et al. 2002). Even with the system, thousands of tons are dumped to the sea every year, and therefore, it exists certain concern about the environmental impact. Since 1996, from 1000 to 97000 tons have been used yearly (NFRDI, 2010). The Korean clay program is designed and followed by NFRDI (National Fisheries Research & Development Institute). The NFRDI produces a report that summarizes the main conclusion of the experimental assays carried out in laboratory and in the field. In the report of 2010, it was pointed out that clay size is important and almost every clay assayed was adequate for control C. polykrikoides (NFRDI, 2010). Even, dredged sediments showed acceptable removal efficiencies for . polykrikoides (Song et al. 2010).
韓國的控制系統已經過兩次修改，以減少使用黏土的數量。在第二代方法中，碾磨黏土的效果更好，但成本增加得令人難以接受。第三代粘土分散設備在與粘土混合之前會對海水進行水解。混合物中含有有效殺藻的 （Jeong 等人，2002 年）。即使有了 系統，每年仍有數千噸被傾倒入海，因此對環境影響有一定的擔憂。自 1996 年以來，每年的使用量從 1000 噸到 97,000 噸不等（NFRDI，2010 年）。韓國的粘土計劃由 NFRDI（國家漁業研究與發展研究所）設計和實施。 NFRDI 編寫的報告總結了在實驗室和實地進行的實驗檢測的主要結論。 2010 年的報告指出，黏土的大小很重要，幾乎所有化驗過的黏土都足以控制 C. polykrikoides（NFRDI，2010 年）。甚至，疏浚沉積物對 .polykrikoides 的去除率（Song 等人，2010 年）。

In Japan, similar methodology was also evaluated around fish enclosures. Suspensions of pure montmorillonite and/ or kaolinite were sprayed onto the surface of Cochlodinium sp. blooms at (Shirota 1989). Although there is scarce record of scientific papers (in international journals) on the matter, Chinese authorities have employed clay (modified) to control HABs. These treatments have been regularly carried out in aquafarms and occasional in recreational waters. For instance, for the Olympic Games in August of 2008, HAB control was carried out in waters at the sailing venue. Other examples of treatments have been recently discussed (Yu et al. 2017). A successful field implementation of clays Phoslock ) was carried out to control blooms of Prymnesium parvum in fish aquaculture ponds in Tasmania (Body 2011). However, comparative evaluation of Phoslock and other clays in laboratory assays showed for . parvum different effectivities in cell flocculation which did not correlate with ichthyotoxicity removal (Seger et al. 2015).
日本也在魚類圍欄周圍評估了類似的方法。將純蒙脫石和/或高嶺石懸浮液噴灑到 藻華表面（Shirota 1989 年）。 （Shirota，1989 年）。雖然有關這方面的科學論文（國際期刊）記錄很少，但中國當局已採用粘土（改性）來控制有害藻華。這些處理方法經常在水產養殖場使用，偶爾也在休閒水域使用。例如，在 2008 年 8 月的奧運會上，就在帆船比賽場地水域進行了 HAB 控制。最近也討論了其他處理實例（Yu 等，2017 年）。黏土 的成功實地應用Phoslock {{2})，以控制塔斯馬尼亞魚類養殖池塘中的副藻華（Body，2011 年）。然而，在實驗室試驗中對Phoslock {{3} 和其他黏土進行的比較評估顯示，對於 .parvum的細胞絮凝效果不同，這與去除魚毒並不相關（Seger等人，2015年）。

Having other target species, research and pilot experiences with several clays were carried out in the USA (Sengco & Anderson 2004). Sengco et al. (2001) proved 25 clays from different suppliers on several seawater HAB species from USA. The main conclusions were that the total clay composition (and not the main component of the product) determines the overall effect and that clay flocculation is highly species specific. Also, in a later study, Sengco and Anderson obtained different removal abilities for the clays assayed (Sengco & Anderson 2004). In this case, phosphatic clay, which showed promising perspectives for its
針對其他目標物種，美國對幾種黏土進行了研究並取得了試點經驗（Sengco 和 Anderson，2004 年）。 Sengco 等人（2001 年）對來自不同供應商的 25 種黏土進行了試驗，試驗對像是美國的幾種海水 HAB 物種。主要結論是，黏土的總成分（而不是產品的主要成分）決定了整體效果，而且黏土的絮凝作用具有高度的物種特異性。此外，在後來的研究中，Sengco 和 Anderson 發現所檢測的黏土具有不同的去除能力（Sengco 和 Anderson，2004 年）。在這種情況下，磷酸鹽粘土因其
practical use against Karenia brevis and others, was selected (Anderson et al. 2004; Hagström et al. 2010). Phosphatic clay is a natural occurring sediment whose main clay component is montmorillonite (Sengco 2001). This clay is effective with several species investigated: Karenia brevis, Aureococcus anophagefferens and Heterosigma akashiwo (Sengco et al. 2001; Sengco & Anderson 2004), Gymnodinium breve (Beaulieu et al. 2005) and Prymnesium parvum (Hagström et al. 2010). With phosphatic clay, assays were conducted up the mesocosmos scale (thousands of litres) and required doses ranged from 0.025 to (Sengco 2009a,b). However, field implementation in the USA was never undertaken for environmental concerns.
Anderson 等人，2004 年；Hagström 等人，2010 年）。磷酸鹽黏土是一種天然沉積物，其主要黏土成分是蒙脫石（Sengco，2001 年）。這種黏土對調查的多個物種都有效：Karenia brevis、Aureococcus anophagefferens 和Heterosigma akashiwo（Sengco 等人，2001 年；Sengco 和Anderson，2004 年）、Gymnodinium breve（Beaulieu 等人，2005 年）和Prymnesbreveium parymnes（ Hagström 等人，2010 年）。對於磷質黏土，進行了中觀尺度（數千公升）的測定，所需劑量從 0.025 到 不等（Sengco，2009 年 a、b）。 （Sengco，2009a,b）。然而，出於對環境的考慮，從未在美國進行實地實施。

Clay modification and prospects in seawater flocculants. The most serious drawback of clays in open waters is the low efficiency. The first intends to improve mineral clays had seawater species as targets. Probably, the first contribution was that of Maruyama et al. (1987). In their work, acid-treated clay proved to be equally efficient flocculant as aluminium hydroxide with seawater red tide species (Maruyama et al. 1987). As was discussed for freshwater countermeasures, polyelectrolytes addition has also been shown to drastically improve flocculation of seawater species. In a pioneering work, Yu et al. (1999) used polyaluminium chloride (PAC) and to modify clay properties. In their work, montmorillonite was modified and zeta potential was correlated with the improvement in removal of Heterosigma akashiwo (Yu et al. 1999). Preparations of with different degrees of inclusion were shown to increase the removal efficiency. With this modifications, clay dosage was reduced from 100-400 ton to ton (Yu et al. 1999, 2004). PAC-modified clays were tested with several seawater species showing a fivefold dose reduction, for instance, with the brown tide organism Aureococcus anophagefferens (Sengco et al. 2001; Yu et al. 2004) and the marine cyanobacterium Synechococcus (Sengco 2001). Recently, PAC and kaolin clay (1:5) were proven suitable to remove Alexandrium tamarense, its toxins and nutrients from sediments (Gu et al. 2015). In the cell-clay flocs, the adsorbed toxin was degraded to less toxic forms (Gu et al. 2015). In a parallel study, the PACkaolin mix was also proved valid for the seawater diatom seawater Skeletonema costatum (Lu et al., 2015b). PAC, however, not always improve the cell removal. PAC was shown to reduce the required dose of phosphatic clay by a factor of 5 but requiring an improved application protocol, as it could induce auto-flocculation of clay (Sengco et al. 2001). Similar conclusions for Prymnesium parvum (Haptophyceae) can be extracted from Sengco et al. (2005). In seawater tests under moderate flow speeds , Beaulieu et al. (2005) registered lower removal efficiencies for PAC-clay mix due to a higher floc porosity that eventually resulted in an increased floc erodibility and lower settling speed. Wang et al. observed other properties of PACmodified kaolin (Wang et al. 2014). The mixture was shown to induce encystment in flocculated S. trochoidea. Additionally, cysts were of temporary type and had lower germination rates after treatment with the clay (Wang et al. 2014). Additionally, inhibition of photosynthesis and oxidative stress was observed in nonflocculated Amphidinium cells after treatment with PAC-modified clays (0.25 g L (Liu et al. 2017). In consequence, modified clays would have a positive effect on preventing HAB reappearance.
海水絮凝劑中的黏土改質和前景。粘土在開放水域中最嚴重的缺點是效率低。改良礦物黏土的最初打算是以海水物種為目標。最早做出貢獻的可能是 Maruyama 等人（1987 年）。在他們的研究中，經酸處理的黏土被證明是與氫氧化鋁同樣有效的絮凝劑，可用於海水赤潮物種（Maruyama 等人，1987 年）。正如在淡水對策中討論的那樣，添加聚電解質也被證明能顯著改善海水物種的絮凝效果。在一項開創性的研究中，Yu 等人（1999 年）使用聚合氯化鋁 (PAC) 和 來改變黏土的性質。在他們的研究中，蒙脫石被改性，zeta 電位與 Heterosigma akashiwo 的去除率相關（Yu 等人，1999 年）。研究表明，含有不同程度 的{{1}製劑可提高去除效率。透過這種改良，黏土用量從 100-400 噸 減少到 噸 （Yu 等人，1999 年，2004 年）。 (Yu 等人，1999 年，2004 年）。 PAC 改質黏土在多個海水物種中進行了測試，結果表明劑量減少了五倍，例如褐潮生物Aureococcus anophagefferens（Sengco 等人，2001 年；Yu 等人，2004 年）和海洋藍藻Synechococcus（Sengco， 2001 年）。最近，PAC 和高嶺土（1:5）被證明適用於去除沉積物中的 Alexandrium tamarense、其毒素和營養物質（Gu 等，2015 年）。在細胞-黏土絮凝物中，吸附的毒素被降解為毒性較低的形式（Gu 等人，2015 年）。在一項平行研究中，PACkaolin 混合物也被證明對海水矽藻 Skeletonema costatum 有效（Lu 等人，2015b）。然而，PAC 並不總是能提高細胞去除率。研究表明，PAC 可將磷化黏土的所需劑量減少 5 倍，但需要改進施用方案，因為它可能誘發黏土自絮凝（Sengco 等人，2001 年）。 Sengco 等人（2005 年）也得出了類似的結論。在中等流速的海水試驗中 ，Beaulieu 等人（2005 年）也得出了類似的結論。 Beaulieu 等人（2005 年）發現，PAC-黏土混合物的去除率較低，原因是絮狀物孔隙率較高，最終導致絮狀物可侵蝕性增加，沉降速度降低。 Wang 等人觀察了 PAC 改質高嶺土的其他特性（Wang 等人，2014 年）。研究表明，該混合物可誘導絮凝的特洛喬氏藻發生包囊。此外，經黏土處理後，囊腫為臨時型，發芽率較低（Wang 等，2014 年）。此外，在使用 PAC 改質黏土（0.25 g L {{7} ）處理後，未絮凝的兩棲動物細胞出現了光合作用抑制和氧化壓力現象（Liu 等人，2017 年）。 (Liu等人，2017）。 因此，改質黏土將對防止有害藻類繁殖再現產生正面影響。

When the ionic strength is high, biopolymers tend to fold. In seawater, chitosan is much less effective due to the effects of ionic strength and (Molina Grima et al. 2003). In addition, it presents another problem during application because of its low solubility. Notwithstanding, chitosan was effective against the dinoflagellate . carterae, although only when polyaluminium chloride (Pan et al. 2011a,b) or M. oleifera extract (Li & Pan 2013) were added. Chitosan and PAC (as modifiers) were also shown effective against . carterae when yellow sea beach sand was used instead of clay (Pan et al. 2011a,b). Required sand concentrations to induce flocculation were similar to clay.
離子強度高時，生物聚合物容易摺疊。在海水中，由於離子強度和 的影響，殼聚醣的效果要差得多（Molina Grima 等人，2003 年）。 (Molina Grima 等人，2003 年）。此外，由於殼聚醣的溶解度低，在應用過程中還會遇到另一個問題。儘管如此，殼聚醣對甲藻 ..carterae，但只有在添加聚合氯化鋁（Pan 等人，2011a,b）或油橄欖萃取物（Li 和Pan，2013 年）時才有效。殼聚醣和 PAC（作為改質劑）也被證明對 ..terae的效果（Pan 等人，2011a,b）。誘導絮凝所需的沙子濃度與黏土相似。

Biopolymers of greater molecular mass or higher charge density are more stable in seawater and show better flocculating ability (Molina Grima et al. 2003). Combination of clay, xanthan (an extracellular heteropolysaccharide) and allowed eliminating . carterae in experiments carried out in seawater with xanthan 'bridging' and the clay acting as a ballast (Chen & Pan 2012). In this work, clay alone was unable of removing cells ( of removal). Xanthan with showed a certain degree of flocculation but significantly lower than with the clay (or soils) (Chen & Pan 2012). Alginate, in low concentrations (50 ), increased floccule cohesion and size, resulting in better flocculation than clay alone (Lin et al. 2013). However, concentrations of this anionic polysaccharide higher than showed a decrease in the coagulation rate (Lin et al. 2013). In seawater, chemically synthesized or natural surfactants have also been evaluated, however, most of them not along with clay (as a flocculation improver), but as algicidals (Baek et al. 2003; Sun et al. 2004). The surfactants screened were proven to be both effective and selective against seawater species (Sun et al. 2004). Apparently, in a work not available in English, hexadecyltrimethyleamine bromide (HDTMAB), a cationic organo-surfactant, was able to increase the Prorocentrum donghaiense cells removal rate of kaolin clay. The effect was attributed to cytotoxicity and to surface ionic charge reversal (Cao & Yu 2003). Despite the fact that flocculants reduce the toxin release (compared to algicidals), a
分子質量越大或電荷密度越高的生物聚合物在海水中越穩定，絮凝能力越強（Molina Grima 等人，2003 年）。將黏土、黃原膠（一種細胞外雜多醣）和 結合使用，可以消除 .在海水中進行的實驗中，黃原膠起到了"橋接"作用，粘土起到了壓艙物的作用（Chen 和Pan，2012 年）。在這項工作中，僅靠黏土無法去除細胞（ 去除）。含有 的黃原膠有一定程度的絮凝作用，但明顯低於黏土（或土壤）（Chen 和 Pan，2012 年）。低濃度（50 ）的海藻酸可增加絮凝體的凝聚力和尺寸，使絮凝效果優於單獨使用黏土（Lin 等人，2013 年）。然而，當這種陰離子多醣的濃度高於 時，混凝速率就會下降（Lin 等人，2013 年）。在海水中，也對化學合成或天然界面活性劑進行了評估，但其中大多數界面活性劑都沒有與粘土（作為絮凝改進劑）一起使用，而是作為藻類活性劑（Baek 等人，2003年；Sun 等人，2004 年）。經證明，篩選出的界面活性劑對海水物種既有效又有選擇性（Sun 等人，2004 年）。顯然，在一項沒有英文版本的研究中，陽離子有機界面活性劑十六烷基三甲基溴胺（HDTMAB）能夠提高高嶺土對 Prorocentrum donghaiense 細胞的去除率。這種效應歸因於細胞毒性和表面離子電荷反轉（Cao 和 Yu，2003 年）。儘管絮凝劑能減少毒素的釋放（與藻酸鹽相比），但高嶺土中的一種絮凝劑卻能減少毒素的釋放。
variable part of cells are lysed during the process or time after. Consequently, it is desirable that both toxins and nutrients be removed from the water column. The ability of some clays of adsorb toxins has been observed with different toxins (Pierce et al. 2004; Gu et al. 2015; Seger et al. 2015). In a recent study, Seger et al. (2015) found that bentonites (unmodified) were best suited for removing ichthyotoxins than kaolinites or Phoslock , which showed overall best cell removal.
在此過程中或之後的一段時間內，細胞的可變部分會被裂解。因此，最好能同時從水體中去除毒素和營養物質。有些黏土具有吸附不同毒素的能力（Pierce 等人，2004 年；Gu 等人，2015 年；Seger 等人，2015 年）。在最近的一項研究中，Seger 等人（2015 年）發現，膨潤土（未改性）比高嶺土或 Phoslock 更適合去除魚毒素。的細胞去除率最高。

Clays are nontoxic and a much safer alternative to algicidals. Notwithstanding, most focus has been put on their possible environmental impact due to their better prospects. Only sand or local soils could imply less ecological risk (Pan et al. 2011a,b). Although flocculants or modifiers could have detrimental impacts, the combined used has been shown to reduce the clay loading resulting in overall lower environmental impact (Wang et al. 2016a,b). Notwithstanding, application methods should be carefully considered as cultured fish could be sensitive to these substances. For instance, acidified chitosan has been shown to kill rainbow trout at concentration (Bullock et al. 2000). So far, the impact assessments in the biota, associated with the use of clays for HAB control, have been made up considering freshwater, marine and estuarine environments, both in planktonic and benthic species (Table 1). These studies have considered various taxa because of their biology (habitat, feeding strategies and/or reproduction) or commercial importance. In most cases, a variety of functional groups have been included, such as autotrophic (micro- and macroalgae), heterotrophic filtering and/or suspension-feeding organisms (crustaceans, bivalves) and fish. The common hypothesis is that clays and additives that increase their flocculating power, as well as the floc formed with microalgae, can directly affect those organisms. This effect can be attributed directly to the toxicity or, indirectly, by an alteration of their physiology, such as by reducing feed filtration rates (Shumway et al. 2003).
黏土無毒，是一種比藻酸安全得多的替代品。儘管如此，由於前景較好，大多數人還是將重點放在黏土可能對環境造成的影響。只有沙子或當地土壤的生態風險較低（Pan 等人，2011a,b）。儘管絮凝劑或改質劑可能會產生不利影響，但結合使用已被證明可減少黏土負荷，從而降低對環境的整體影響（Wang 等人，2016a,b）。儘管如此，由於養殖魚類可能對這些物質敏感，因此應仔細考慮施用方法。例如，酸化殼聚醣在 濃度下可殺死虹鱒（Bullock 等人，2000 年）。 (Bullock 等人，2000 年）。迄今為止，與使用黏土控制有害藻類繁殖相關的生物群影響評估已考慮到淡水、海洋和河口環境中的浮游生物和底棲物種（表 1）。這些研究考慮了各種分類群，因為它們具有生物學特性（棲息地、攝食策略和/或繁殖）或商業重要性。在大多數情況下，研究對象包括各種功能類群，例如自養生物（微藻和大型藻類）、異養過濾和/或懸浮取食生物（甲殼類、雙殼類）以及魚類。共同的假設是，黏土和添加劑如果能增強其絮凝能力，以及與微藻形成的絮凝體，就能直接影響這些生物。這種影響可直接歸因於毒性，也可間接歸因於改變生物的生理機能，如降低飼料過濾率（Shumway 等人，2003 年）。

The toxicity assessment of these compounds has been performed mostly using bioassays, and the results have shown no lethal effects induced by the clays in the range of concentrations recommended for HAB control, regardless of the taxa evaluated. This fact has been demonstrated for both benthic (Lewis et al. 2003) and planktonic species
對這些化合物的毒性評估主要是透過生物測定進行的，結果表明，在建議用於控制有害藻華的濃度範圍內，黏土不會誘發致死效應，無論評估的類群是什麼。對底棲生物（Lewis 等人，2003 年）和浮游生物物種都證明了這一事實。

Table 1 Studies of clays' impact on ecosystems
表 1 有關黏土對生態系影響的研究

(Stauber 2000; Orizar et al. 2013). Regarding the sublethal effects assessment, the reported data range from absence of alterations, for example in oxygen consumption and filtration rates in bivalves (Seo et al. 2008), to alterations in reproductive aspects that lead to lower production of progeny in cladocerans (Stauber 2000). However, it is important to note that variability of the responses is related to the type of flocculant tested (clay, modified clay), and very importantly, to the specific sensitivity of each species to this type of compound. Shumway et al. (2003) observed interspecific differences in the impact on filtration rates by phyical interference of the clay particles in the feeding process, even between members of the same taxonomic group. This antecedent is consistent with the work of Strachan and Kingston (2012), who observed a reduction in filtration rates as well as damage at the gill level in two species of Mytilidae (Bivalvia) exposed to bentonite.
(Stauber 2000 年；Orizar 等人 2013 年）。關於亞致死效應評估，所報告的數據範圍很廣，從沒有變化（例如雙殼類動物的耗氧量和過濾率）（Seo 等人，2008 年）到生殖方面的變化（導致橈足類後代產量降低）（Stauber，2000 年）。不過，必須注意的是，反應的變化與測試的絮凝劑類型（粘土、改性粘土）有關，而且非常重要的是，與每個物種對這類化合物的特定敏感性有關。 Shumway 等人（2003 年）觀察到，即使在同一分類群的成員之間，黏土顆粒在進食過程中的物理幹擾對過濾率的影響也存在種間差異。這項前因後果與 Strachan 和 Kingston（2012 年）的研究結果一致，他們觀察到兩種接觸膨潤土的貽貝科（雙殼類）魚類的過濾率降低，鰓部受損。

On the other hand, there are field studies which compared the composition of the planktonic communities either between sites with or without flocculant application (Ni et al. 2010) or pre- and post -dispersal of the flocculant in a certain area (Lee et al. 2008). While Ni et al. (2010) did not find negative effect on the composition of the zooplankton community; Lee et al. (2008) showed a significant effect on the abundances of certain planktonic components. Specifically, a reduction in protists biomass (21-41%) and zooplankton is reported within a few minutes after application of flocculants (clays alone and/or in combination with sophorolipid, respectively). However, the authors do not rule out that this decrease could be attributable to the evasion of these organisms from the areas in which the flocculants were applied. On the other hand, Park and Lee (2006) evaluated the impact on benthic community composition through qualitative comparison between sites with or without clays application. It was evidenced the exclusion of certain species from the impacted habitats, with the consequent alteration of the diversity in these sites.
另一方面，一些實地研究比較了施用或未施用絮凝劑地點的浮游生物群落組成（Ni 等人，2010 年），或某一地區絮凝劑撒佈前後的浮游生物群落組成（Lee 等人，2008 年）。 Ni 等人（2010 年）沒有發現對浮游動物群落組成的負面影響；而 Lee 等人（2008 年）則發現對某些浮游生物成分的豐度有顯著影響。具體而言，在施用絮凝劑（單獨使用黏土和/或與槐脂混合使用）後幾分鐘內，原生動物生物量（21-41%）和浮游動物 都有所減少。不過，作者並不排除這種減少可能是由於這些生物逃離了施用絮凝劑的區域。另一方面，Park 和 Lee（2006 年）透過對施用或未施用黏土的地點進行定性比較，評估了對底棲生物群落組成的影響。結果表明，某些物種被排除在受影響的生境之外，從而改變了這些地點的多樣性。

The frequency of HABs has increased in the last years, and for this reason, the use of flocculants may have been increased. This would result in a change from acute to a rather chronic exposure. It is already documented, for example, that the effects on respiration of filtering organisms are a function of both the concentration of flocculants and the duration of exposure (Seo et al. 2008). This aspect is relevant as the majority of experimental studies consider the effects of acute expositions. Field studies performed after massive application of flocculants suggest the recovery time of planktonic communities could be months, recommending massive applications of these clays on a biannual frequency (Ni et al. 2010). It is also important to consider the physical characteristics of the impacted area, as there is evidence that equivalent concentrations of clays can have a greater impact in areas with higher flow on the sediment, which produces the resuspension of particles preventing an adequate feed and therefore lower growth rates of suspension-feeding organisms (Archambault et al. 2004).
近年來，有害藻華的發生頻率上升，因此，絮凝劑的使用量可能增加。這將導致從急性接觸轉變為慢性接觸。例如，已有文獻表明，對過濾生物呼吸的影響是絮凝劑濃度和接觸時間長短的函數（Seo 等，2008 年）。這一點很重要，因為大多數實驗研究都考慮了急性接觸的影響。大量施用絮凝劑後進行的實地研究表明，浮游生物群落的恢復時間可能為 個月，因此建議每半年施用一次這些黏土（Ni 等人，2010 年）。考慮受影響區域的物理特徵也很重要，因為有證據表明，在沉積物流量較大的區域，同等濃度的黏土可能會產生更大的影響，這將導致顆粒重新懸浮，從而阻礙充足的進食，進而降低懸浮進食生物的生長率（Archambault 等人，2004 年）。

The most recent information regarding the effect of modified clays such as Phoslock (clay plus lanthanum) (Lürling & Tolman 2010; Lürling & Faassen 2012) is mainly used in the control of eutrophication given their ability to remove phosphorus, present in the water column and released from the sediments (Sun et al. 2015; Liu et al. 2016a; Noyma et al. 2016). The Phoslock effectiveness in the control of microalgae and cyanobacteria blooms in freshwater was demonstrated by an experimental approach. In a range of concentrations (including those used in the control of eutrophication in the field), a concentrationdependent reduction in the growth rates was observed. At the same time, this clay also shows the same negative effect on growth rates in small suspension-feeders, such as Brachionus (van Oosterhout & Lürling 2013) and Daphnia (Lürling & Tolman 2010). Additionally, it has been experimentally shown that the lanthanum included in the Phoslock formulation is bioaccumulated in organisms such as shrimp (Procarmabarus), in proportional concentrations while being exposed to this modified clay (Van Oosterhout et al. 2014). Herrmann et al. (2016), in an extensive review, showed varied toxicity data of lanthanum in water, sediments, and marine and freshwater species; the aim of this review was to define water and sediment quality criteria as there are no regulatory concentration limits for this metal. However, the authors only achieve this goal for freshwater, given the scarcity of information related to marine environment, neither in sediment nor results from chronic bioassays. The available information regarding the possible side effects from using these clays, both in the biota and the environment in which these species are, still is insufficient for adequate decisions about using clays for HAB control.
有關改性黏土（如Phoslock （黏土加鑭））效果的最新資訊（Lürling 和Tolman，2010 年；Lürling 和Faassen，2012 年）主要用於控制富營養化，因為它們能夠去除水中的磷。 (黏土加鑭）（Lürling和Tolman，2010年；Lürling和Faassen，2012年）主要用於控制富營養化，因為它們能夠去除水體中存在並從沉積物中釋放出來的磷（Sun等人，2015年；Liu等人，2016年a；Noyma等人，2016年）。實驗證明了 Phoslock {{1} 在淡水中控制微藻和藍藻藻華的有效性。在一定濃度範圍內（包括在實地富營養化控制中使用的濃度），觀察到生長速率的降低與濃度有關。同時，這種黏土也對小型懸浮取食者的生長速率產生了同樣的負面影響，如 Brachionus（van Oosterhout 和 Lürling，2013 年）和 Daphnia（Lürling 和 Tolman，2010 年）。此外，實驗表明，Phoslock 配方中的鑭會在蝦類（Procarmabarus）等生物體內進行生物累積，其濃度與接觸這種改性粘土時的濃度成正比（Van Oosterhout等人，2014年）。 Herrmann 等人（2016 年）在一篇內容廣泛的綜述中展示了鑭在水、沉積物、海洋和淡水物種中的各種毒性數據；該綜述的目的是確定水和沈積物的品質標準，因為這種金屬沒有規定濃度限值。然而，由於缺乏與海洋環境有關的信息，既沒有沉積物中的信息，也沒有慢性生物測定的結果，因此作者只針對淡水實現了這一目標。關於使用這些黏土對生物群和這些物種所處環境可能產生的副作用，現有的資訊仍不足以讓我們就使用黏土控制有害藻華做出適當的決定。

In the same direction, several chemical compounds have been considered for prevention and management of cyanobacterial blooms, via either growth inhibition of phytoplankton species or a decrease in nutrient concentration. Within these chemicals, there are some metals ( , and photosensitizers as hydrogen peroxide. Literature information about suitable use of hydrogen peroxide in microalgae bloom control is scarce, probably by their recognized toxicity in invertebrates and fish and fast degradation to water and oxygen (Jančula & Maršálek 2011). A field evaluation in the shallow Lake Koetshuis (Netherlands) showed that a diluted concentration of (2 ) had a high efficiency in algal removal (99%) while eukaryotic phytoplankton, zooplankton and macrofauna had a mild negative impact (Matthijs et al. 2012). Using a similar methodology and a higher concentration of
同樣，一些化學物質也被認為可以透過抑制浮游植物的生長或降低營養濃度來預防和管 理藍藻藻華。在這些化學物質中，有一些金屬（ 、{{1、 和過氧化氫等光敏劑。有關過氧化氫在微藻藻華控制中的適當使用的文獻資料很少，這可能是因為過氧化氫對無脊椎動物和魚類具有公認的毒性，而且會快速降解為水和氧氣（Jančula 和Maršálek 2011 年）。在淺水湖Koetshuis（荷蘭）進行的一項實地評估顯示，稀釋濃度的 （2 )2 ）對藻類的去除效率很高（99%），而真核浮游植物、浮游動物和大型底棲動物則有輕微的負面影響（Matthijs 等人，2012 年）。使用類似的方法和更高濃度的
hydrogen peroxide ( ), a harmful marine bloom (Alexandrium ostenfeldii) was controlled in the Ouwerkerkse brackish Kreek (Netherlands). The treatment achieved a decrease in both vegetative cells and pellicle cysts by within , but the total abundance of zooplankton decreased and some lethal and sublethal effects were quantified in fish and crustaceans (Burson et al. 2014). Despite these tests, the authors, based on their fast degradation, recommend the use of as an effective emergency treatment in the short term when the rapid and complete termination of is required in a relatively closed area.
過氧化氫（ ），控制了 Ouwerkerkse 鹹水溪（荷蘭）中的有害海洋水華（Alexandrium ostenfeldii）。在 內，無性細胞和星狀囊腫的數量都減少了 。但浮游動物的總豐度下降，對魚類和甲殼類動物也產生了一些致死和亞致死效應（Burson 等人，2014 年）。儘管進行了這些測試，但基於 的快速降解，作者建議在相對封閉的區域內需要快速、徹底地終止 時，使用 作為短期內有效的應急處理方法。

At worldwide scale, copper sulphate has been the most used metallic compound to manage cyanobacterial blooms, despite its reported nonspecific toxicity and capacity to cumulate in sediments. Considering these antecedents, some countries, such as Netherlands, Sweden, Czech Republic, have replaced copper by aluminium and iron, which can act also as phosphorus removal agents and thus slow down the recovery of blooms in the water body after application (Jančula & Maršálek 2011). Also, addition of iron as and has been used as a lake restoration tool; if iron binds to the excess of phosphorus in the system, a shift towards clear water and macrophyte dominated state is expected; notwithstanding toxic effects have been observed in the rest of lake biota at higher concentrations. Bakker et al. (2016) provided a review of iron impact on aquatic organisms and shallow lake ecosystems on the basis of ten studies where iron was used as restoration measure in the field. In most cases, a positive decrease in chlorophyll concentration was observed, although no assessment of the rest of biota was included. In relation to aluminium (e.g. polyaluminium chloride), there are no data at field scale; however, a negative impact in zooplankton has been observed several days after the addition of aluminium to water (Jančula et al. 2011).
在全球範圍內，硫酸銅一直是用於治理藍藻水華最常用的金屬化合物，儘管據報道它具有 非特異性毒性和在沉積物中累積的能力。考慮到這些前因後果，荷蘭、瑞典、捷克共和國等一些國家已用鋁和鐵取代銅，因為鋁和鐵也可作為除磷劑，從而減緩施用後水體中藻華的恢復速度（Jančula 和Maršálek，2011年）。此外，以 和 的形式添加鐵也被用作一種湖泊恢復工具；如果鐵能與系統中過量的磷結合，預計水體將轉向清澈和以大型水生植物為主的狀態；儘管在較高濃度下已觀察到對湖泊其他生物群的毒性影響。 Bakker 等人（2016 年）根據十項在實地使用鐵作為修復措施的研究，回顧了鐵對水生生物和淺水湖泊生態系統的影響。在大多數情況下，葉綠素濃度都出現了正向下降，但並未對生物群的其他部分進行評估。關於鋁（如聚合氯化鋁），沒有實地數據；不過，在水中添加鋁幾天后，浮游動物受到了負面影響（Jančula 等人，2011 年）。

In general, during the implementation and assessment of restoration projects, costs, response time and ecotoxicological consequences at field scale are not adequately considered, even though a large number of studies highlight the toxicity of metals and photosensitizers, which depend on dose concentration, the sensitivity of the species and environmental conditions such as , oxygen concentration , irradiance intensity and conductivity (Jančula & Maršálek 2011). This is why recent literature emphasizes the need for studies to evaluate the environmental complexity of the area to be impacted before applying a recommended control tool (Bakker et al. 2016; Stroom & Kardinaal 2016).
儘管大量研究強調了金屬和光敏劑的毒性取決於劑量濃度、物種的敏感性和環境條件，如 、氧氣濃度 、溫度 和濕度{{3 }} 。氧氣濃度 {{1}輻照強度 和電導率 。 (Jančula 和 Maršálek 2011）。因此，最近的文獻強調，在應用建議的控制工具之前，需要對受影響區域的環境複雜性進行評估研究（Bakker 等人，2016 年；Stroom & Kardinaal，2016 年）。

A recent approach considers a more environmentally friendly control of cyanobacterial HABs using modified local soil (MLS technology), which induces a decrease in cellular density through phosphorus arrest. The operation principle is similar to Phoslock , but with the advantage to use local soil supplemented with a biopolymer as chitosan (Wang et al. 2016a,b). In China, its implementation in the natural environment at mesocosm scale showed a change in microplankton community, with an increase in diversity (multi-algae coexistence) together with a decrease of nutrients in the water column and diminished release of nutrients from the sediments (Dai et al. 2015). At larger scale in the same lake, the impact was similar, showing restoration of submerged vegetation (Macrophyte) suggesting that nutrient limitation can be manipulated using the MLS technology and secondarily that ecological recovery can be promoted (Wang et al. 2016a,b). However, successful manipulation of biogeochemical processes requires a comprehensive understanding of physical, chemical and biological conditions, which could lead to contrasting results (Spears et al. 2016). Currently, no studies of ecotoxicological effects and alteration of coupled biogeochemical cycles (e.g. carbon and nitrogen) have been carried out, which should be considered previously to implement an eutrophication management tool.
最近的一種方法考慮使用改良的本地土壤（MLS 技術）對藍藻有害藻華進行更環保的控制，該技術透過磷捕獲誘導細胞密度下降。其工作原理與 Phoslock 相似，但其優勢在於使用了當地土壤中的磷酸鹽。的工作原理類似於 Phoslock {{0} ，但其優點是使用當地土壤，並輔以殼聚醣等生物聚合物（Wang 等人，2016a,b）。在中國，該方法在中觀尺度的自然環境中實施後，微浮游生物群落發生了變化，多樣性增加（多種藻類共存），同時水體中的營養物質減少，沉積物中的營養物質釋放減少（Dai 等，2015 年）。在同一湖泊的更大範圍內，影響也是類似的，顯示沈水植物（大型藻類）的恢復，這表明使用MLS 技術可以控制營養限制，其次還可以促進生態恢復（Wang 等人，2016a,b ）。然而，成功操縱生物地球化學過程需要全面了解物理、化學和生物條件，這可能會導致截然不同的結果（Spears 等，2016 年）。目前，尚未進行生態毒理效應和耦合生物地球化學循環（如碳和氮）改變的研究，在實施富營養化管理工具之前應考慮這一點。

Biological control is considered a valuable tool in pest control, mainly due to its 'environmentally friendly' quality. There are several examples of biological control in terrestrial systems, especially in the agricultural area, where it has been used successfully in the control of insect pests. An example is the use of sterile insect males (modified) and the use of pheromones (Heikki Hokkanen 1995). However, this practice presents certain long-term complications on nontarget organisms (Suckling 2013), difficulty in handling the biocontrol and other impacts on the intervened ecosystem (Simberloff 2011). These consequences in open systems regrettably reinforce the feared concept of irreversibility, making it a highly risky strategy that could only be considered by virtue of its benefits (Suckling 2013). We have included in this review reports suggesting different organisms that could 'theoretically' serve as biological controllers for HABs (Table 2). So far, the data collected have restricted its application mainly to controlled systems (laboratory). Although samples collected from the environment were used in many cases, the main limitation remains which is the uncertainty of the effect of introducing the controlling species. The organisms considered for the biological control of HAB include species that feed, infect or decompose HAB (called top-down control). Control methods suggested include the use of predators such as copepods (plankton grazers), ciliates or microalgae (mixotrophs dinoflagellates; Kamiyama & Arima 2001; Kamiyama et al. 2005; Chang 2011; Lim et al. 2017) and pathogenic micro-
生物防治被認為是害蟲防治的重要工具，主要是因為它具有 "環境友善 "的特性。在陸地系統中，特別是在農業領域，有幾個生物防治的例子，生物防治已被成功地用於控制害蟲。其中一個例子是使用昆蟲雄性不孕體（改良）和費洛蒙（Heikki Hokkanen，1995 年）。然而，這種做法會對非目標生物造成某些長期併發症（Suckling，2013 年）、生物控制處理困難以及對介入生態系統的其他影響（Simberloff，2011 年）。令人遺憾的是，開放系統中的這些後果強化了人們所擔心的不可逆概念，使其成為一種風險極高的策略，只能透過其益處加以考慮（Suckling，2013 年）。我們在本篇綜述中納入了一些報告，這些報告提出了 "理論上 "可作為有害藻華生物控製劑的不同生物（表 2）。到目前為止，收集到的數據主要限制其在受控系統（實驗室）中的應用。雖然在許多情況下使用了從環境中採集的樣本，但主要的限制仍然存在，即引入控制物種的效果不確定。考慮用於對有害藻華進行生物控制的生物包括以有害藻華為食、感染或分解有害藻華的物種（稱為自上而下控制）。建議的防治方法包括利用掠食者，如橈足類（浮游生物食草動物）、纖毛蟲或微藻類（混養雙鞭毛藻；Kamiyama & Arima 2001；Kamiyama 等人，2005；Chang 2011；Lim 等人，2017）和致病性微生物，如橈足類、纖毛蟲或微藻類（混養雙鞭毛藻；Kamiyama & Arima 2001；Kamiyama 等人，2005；Chang 2011；Lim 等人，2017）。

Table 2 Biological control methods assayed for HABs
表 2 對有害藻華進行化驗的生物防治方法

organisms. For the last group, there are several examples in literature. For example, control methods have been proposed using parasites (Park et al. 2004; Alacid et al. 2016), fungi (Jia et al. 2010b), lytic bacteria (Skerratt et al. 2002; Mayali & Azam 2004; Amaro et al. 2005; Gumbo et al. 2008; Su et al. 2011; Bibak & Hosseini 2013; Guan et al. 2014) and viruses (Suttle 1994; Baudoux & Brussaard 2005; Table 2).
生物。關於最後一類生物，文獻中有多個實例。例如，有人提出了利用寄生蟲（Park 等人，2004 年；Alacid 等人，2016 年）、真菌（Jia 等人，2010 年b）、裂解細菌（Skerratt 等人，2002 年；Mayali & Azam，2004年；Amaro 等人，2005 年；Gumbo 等人，2008 年；Su 等人，2011 年；Bibak & Hosseini，2013 年；Guan 等人，2014 年）和病毒（Suttle，1994 年；Baudoux & Brussaard，2005年；表2）進行控制的方法。

Lethal effects of toxins produced by harmful microalgae on predators (Chang 2011), which were reflected in changes in swimming behaviour, reduction in ingestion, decrease in growth and even death of the predator (Kamiyama & Arima 1997; Rosetta & McManus 2003), have been observed systematically. However, certain planktonic
有害微藻產生的毒素會對捕食者造成致命影響（Chang，2011 年），表現為捕食者游泳行為改變、攝食減少、生長下降甚至死亡（Kamiyama 和Arima，1997 年；Rosetta 和McManus，2003 年） 。然而，某些浮游生物
organisms are able to coexist, predate and feed on toxic microalgae. For example, heterotrophic dinoflagellates and ciliates have been shown to generate dinoflagellate mortalities over , being able to collapse a bloom in a matter of hours (Kamiyama & Arima 2001; Kamiyama et al. 2005). An example is the heterotrophic dinoflagellate Stoeckeria algicida, with an estimated removal rate of the dinoflagellate Heterosigma akashiwo of per minute (Jeong et al. 2005). In this context, several species of ciliates (Tintinnids and Aloricate) are able to feed on toxic dinoflagellates or another harmful phytoplankton. Several studies suggested their participation in the natural biological control of toxic microalgae bloom (Jeong et al. 1999; Kamiyama & Arima 2001; Rosetta & McManus 2003; Kamiyama et al. 2005). Previous reports have found the ciliate Favella taraikaensi capable of effectively terminate toxic strains of Alexandrium tamarense and Heterocapsa circularisquama in culture (Kamiyama & Arima 2001; Kamiyama et al. 2005).
生物能夠與有毒微藻共存、捕食並以其為食。例如，異養甲藻和纖毛蟲已被證明能使甲藻死亡率超過 ，並能在數小時內使水華崩潰（Kamiyama & Arima 2001；Kamiyama et al. ，能在數小時內使藻華崩潰（Kamiyama 和Arima，2001 年；Kamiyama 等，2005 年）。例如，異養甲藻Stoeckeria algicida 對甲藻Heterosigma akashiwo 的清除率估計為每分鐘 （Jeong 等，2005 年）。在這種情況下，有幾種纖毛蟲（Tintinnids 和Aloricate）能夠捕食有毒甲藻或其他有害浮游植物。一些研究表明，它們參與了有毒微藻藻華的自然生物防治（Jeong 等人，1999 年；Kamiyama 和Arima，2001 年；Rosetta 和McManus，2003 年；Kamiyama 等人，2005 年）。先前的報告發現，纖毛蟲(Favella taraikaensi)能夠有效地終止培養的有毒亞歷山大藻（Alexandrium tamarense）和圓環異藻（Heterocapsa circularisquama）（Kamiyama & Arima 2001; Kamiyama et al.

Although previous reports strengthen the supposed potential of various organisms as HAB biological control agents (Jinhui 2005), based on their efficiency and potential, it is important to take into account certain disadvantages that should be considered before their use in the field. For example, some plankton grazers such do not present specificity for strains or species, being able to prey on dinoflagellates of small size without discriminating between toxic and nontoxic (Jeong et al. 2004), including Amphidinium carterae and H. akashiwo (Jeong et al. 1999). On the other hand, it is important to consider that the presence of a predator could induce an increase in the toxicity or even modify the toxic profile of the harmful species.
儘管先前的報告加強了各種生物作為有害藻華生物控製劑的假設潛力（Jinhui，2005 年），但基於其效率和潛力，在實地使用之前必須考慮到某些缺點。例如，一些浮游生物食肉動物對菌株或物種不具有特異性，它們能夠捕食小體積的甲藻，而不區分有毒和無毒（Jeong 等人，2004 年），這些食肉動物中包括Amphidinium carterae 和H . akashiwo（Jeong 等人，1999 年）。另一方面，必須考慮到捕食者的存在可能會增加毒性，甚至改變有害物種的毒性特徵。

Another group that could be considered within the predators are the marine rotifers and copepods, which are abundant components of zooplankton and among their alimentary preferences can include toxic phytoplankton (Lacerot et al. 2013). This group has been shown to be highly species-specific. The rotifer Brachionus plicatilis was shown able to feed on the toxic dinoflagellate Pfiesteria piscicida, apparently without adverse effects in terms of fertility reduction or increased mortality (Hare et al. 2005). However, on the contrary, the same species failed to maintain its growth when its diet includes the harmful microalgae Aureoumbra lagunensis (Texas brown tide alga) (Turner & Tester 1997). Likewise, there are examples of copepods and rotifers with the ability to regulate the growth of certain toxic microalgae directly in a mesocosm (Vadstein et al. 2004; Granéli & Turner 2006). On the other hand, and similarly to rotifers and other potentially predatory microalgae, toxins from some harmful microalgae have shown deleterious effects on the physiology or fertility of copepods in laboratory and field studies (Solé et al. 2006a,b).
海洋輪蟲和橈足類是捕食者中的另一類，它們是浮游動物的重要組成部分，其食物偏好包括有毒浮游植物（Lacerot 等，2013 年）。研究表明，這類浮游動物具有高度的物種特異性。研究表明，輪蟲 Brachionus plicatilis 能夠以有毒甲藻 Pfiesteria piscicida 為食，顯然不會造成繁殖力下降或死亡率上升（Hare 等，2005 年）。但相反，當食物中包括有害的微藻類 Aureoumbra lagunensis（德克薩斯州褐潮藻）時，同一物種無法維持生長（Turner 和 Tester，1997 年）。同樣，也有例子表明，橈足類和輪蟲有能力在中觀宇宙中直接調節某些有毒微藻的生長（Vadstein 等，2004 年；Granéli 和 Turner，2006 年）。另一方面，與輪蟲和其他潛在的掠食性微藻類似，在實驗室和實地研究中，一些有害微藻的毒素也對橈足類的生理或繁殖力產生了有害影響（Solé 等，2006a ,b）。
Despite the interesting nature of this alternative biocontrol, the antecedents collected increase the uncertainty of its use in natural or field conditions. In addition, logistic difficulties in the application of the predator and difficulties in scaling the culture to obtain enough of this type of zooplankton predators limit their potential use outside the laboratory.
儘管這種替代性生物防治方法很有趣，但收集到的前因後果增加了其在自然或野外條件下使用的不確定性。此外，在應用捕食者方面的後勤困難，以及在擴大培養規模以獲得足夠的浮游動物捕食者方面的困難，都限制了它們在實驗室外的潛在用途。

A pathogenic biological agent is defined as any species which can produce disease or damage to the biology of a host, whether human, animal or plant, including parasites, bacteria, fungi and viruses. Marine microbial interactions involving eukaryotes and their parasites are part of the structural conformation of phytoplankton communities. These interactions can regulate the population densities of the main host, which in turn may have a relevant role in the natural control of toxic phytoplankton. Consequently, it has been proposed as a potential strategy to control HABs (Park et al. 2004; Alacid et al. 2016). Unlike the alternatives suggested above, the relationship between generalist parasitoids is strongly dependent on the specificity degree with the host. For example, flagellates, such as Amoebophrya ceratii and Parvilucifera infectans, are well-known intracellular parasites of free-living dinoflagellates, including species of the Alexandrium genus (Park et al. 2004; Alacid et al. 2016). In relation to this mechanism, an allelopathic molecule dependent on culture density has been identified, which acts as an activating signal for the infectious stage, but not for selection. The parasitoids contact the host at random, the possibility of penetrating inside the host cell and developing the infection strongly depends on the degree of susceptibility of the host (Alacid et al. 2016). Despite the interesting and promising use of this type of biocontrol, current knowledge is scarce and more research is needed before its use in the field for the control and mitigation of HAB.
病原生物製劑的定義是任何能對宿主（無論是人類、動物或植物）的生物學特性產生疾病或損害的物種，包括寄生蟲、細菌、真菌和病毒。涉及真核生物及其寄生蟲的海洋微生物相互作用是浮游植物群落結構構型的一部分。這些相互作用可以調節主要宿主的族群密度，進而在有毒浮游植物的自然控制中發揮相關作用。因此，有人提出將其作為控制有害藻華的潛在策略（Park 等人，2004 年；Alacid 等人，2016 年）。與上述替代方法不同，通性寄生蟲之間的關係在很大程度上取決於寄主的特定性。例如，鞭毛蟲（如 Amoebophrya ceratii 和 Parvilucifera infectans）是自由生活的甲藻（包括亞歷山大屬物種）的著名胞內寄生蟲（Park 等人，2004 年；Alacid 等人，2016 年）。與此機制有關的是，已經發現了一種依賴培養密度的等位病理分子，它是感染階段的活化訊號，但不是選擇訊號。寄生蟲隨機接觸宿主，能否穿透宿主細胞並形成感染在很大程度上取決於宿主的易感程度（Alacid 等人，2016 年）。儘管這種生物控制方法很有趣，使用前景也很廣闊，但目前的知識還很匱乏，在將其用於實地控制和緩解有害藻華之前，還需要進行更多的研究。

Although fungi have been infrequently reported as potential biological controllers, there are parasitic associations between freshwater microalgae and Chytridiomycetes fungi (called chytrids; Ibelings et al. 2004; Gerphagnon et al. 2013) and with biflagellate fungi belonging to Oomycetes. However, this latter association occurs to a lesser extent (Mountfort et al. 1996; Elbrächter & Schnepf 1998). Both groups have received considerable attention because of their occurrence in lakes and reservoirs in Europe, Asia, North and South America in the early 1990s (Van Donk & Ringelberg 1983; Heaney et al. 1988; Holfeld 1998). This fungal infection in planktonic diatoms has been associated with mortality of host organisms, suppression or retardation of phytoplankton blooms and changes in the size, distribution, and composition of planktonic populations and
雖然真菌作為潛在生物控制者的報導並不多見，但淡水微藻與糜狀真菌（稱為糜菌；Ibelings 等人，2004 年；Gerphagnon 等人，2013 年）以及與屬於卵菌綱的雙鞭毛真菌之間存在寄生關係。不過，後者的關聯程度較低（Mountfort 等，1996 年；Elbrächter & Schnepf，1998 年）。由於這兩類真菌在20 世紀90 年代初出現在歐洲、亞洲、北美和南美的湖泊和水庫中，因此受到了廣泛關注（Van Donk 和Ringelberg，1983 年；Heaney 等人，1988 年；Holfeld，1998 年）。浮游矽藻中的真菌感染與宿主生物的死亡、浮游植物繁殖的抑製或延緩以及浮游生物種群的大小、分佈和組成的變化有關。
communities (Canter & Lund 1953; Van Donk & Ringelberg 1983; Kudoh & Takahashi 1990; Sime-Ngando 2012). The dispersion of this type of parasites is through freeswimming flagellated zoospores. In contact with host cells, these micro-organisms penetrate hosts using their flagella forming an intracellular rhizoid through which the zoospore is fed outside the host. The zoospore becomes a sporangium that matures and produces new zoospores (Van Donk 1989). Regarding the association of marine microalgae and pathogenic fungi, it is still unknown whether their association dynamics acts in a similar way to that of freshwater clusters (Granéli & Turner 2006). However, there are studies in marine organisms which may suggest this. For example, the fungal pathogen Lagenisma coscinodisci was found able to colonize diatoms of the genus Coscinodiscus (Schnepf et al. 1978). In other study, the fungus Vertidllium lecanii ability to release algicidal substances causing mortality in specific dinoflagellates (Karenia mikimotoi and Akashiwo sanguinea) was observed (Mountfort et al. 1996). On the other hand, as in the case of the association of marine microalgae with fungi, there is scarce information concerning the relationship between freshwater toxic microalgae and pathogenic fungi. Notwithstanding, Canter (1972) reported that cyanobacteria of genus Microcystis and Anabaena (both toxic) are potential hosts to fungal parasites.
Canter & Lund 1953; Van Donk & Ringelberg 1983; Kudoh & Takahashi 1990; Sime-Ngando 2012）。這類寄生蟲透過自由遊動的鞭毛蟲孢子傳播。與宿主細胞接觸時，這些微生物利用鞭毛穿透宿主細胞，形成細胞內根瘤，透過根瘤將子孢子輸送到宿主體外。動物孢子變成孢子囊，孢子囊成熟後產生新的動物孢子（Van Donk，1989 年）。關於海洋微藻與病原真菌的結合，目前還不清楚它們的結合動態是否與淡水菌叢的結合動態相似（Granéli 和 Turner，2006 年）。不過，對海洋生物的一些研究可能顯示了這一點。例如，研究發現真菌病原體 Lagenisma coscinodisci 能夠在 Coscinodiscus 屬矽藻中定植（Schnepf 等人，1978 年）。另一項研究發現，真菌 Vertidllium lecanii 能夠釋放殺藻物質，導致特定甲藻（Karenia mikimotoi 和 Akashiwo sanguinea）死亡（Mountfort 等人，1996 年）。另一方面，與海洋微藻與真菌的關係一樣，有關淡水有毒微藻與致病真菌之間關係的資訊也很少。儘管如此，Canter（1972 年）報告說，微囊藻屬（Microcystis）和赤藻屬（Anabaena）藍藻（均有毒）是真菌寄生蟲的潛在宿主。

Indisputable evidences of bloom declining caused by algicidal bacteria are still missing (Mayali & Azam 2004). Despite this, probably algicidal and growth inhibitory bacteria (GIB) are the more promising bottom-up biocontrol-micro-organisms because of their abundance in marine systems, their ability to replicate rapidly and, in some cases, their highly host specificity (Bibak & Hosseini 2013). Several research studies have reported the identification and isolation from the environment of host-specific algicidal bacteria. Lytic bacteria were isolated in Northern Hiroshima Bay in the Seto Inland Sea that specifically affect harmful microalgae, such as C. antiqua and . akashiwo (Imai et al. 1991; Imai 2015). Yoshinaga et al. (1997) showed that a strain of Flavobacterium sp. (C49 strain) effectively and specifically inhibits . akashiwo, without affecting dinoflagellates or diatoms (Yoshinaga et al. 1997). Another strain of Pseudoalteromonas isolated from the environment (class Proteobacteria, gamma subdivision, identified as Y strain) is able to rapidly swell in toxic microalgae such as Gymnodinium and Gyrodinium, which precedes imminent cell lysis after ; a similar reaction was observed on species of raphidophytes, Chattonella and Heterosigma, which are severely damaged by the same strain, with evident lysis within of exposure (Lovejoy et al. 1998). However, in those dinoflagellates which possess theca, the effects of Y strain are less severe, although they manage to affect the thecal plate, even inducing detachment and evident signs of swelling (rounding up), they do not become lethal. So we assume the presence of the theca offers protection against lytic bacterial compounds that could be produced in particular by this strain of Pseudoalteromonas sp. (Lovejoy et al. 1998).
殺藻細菌導致水華減少的確鑿證據仍然缺失（Mayali 和 Azam，2004 年）。儘管如此，殺藻細菌（ ）和生長抑制細菌（GIB）可能是更有前景的自下而上的生物控制微生物，因為它們在海洋系統中數量眾多，具有快速複製能力，在在某些情況下還具有高度的宿主特異性（Bibak 和Hosseini，2013 年）。有幾項研究報告了從環境中鑑定和分離宿主特異性殺藻細菌的情況。在瀨戶內海的廣島灣北部分離出的溶藻細菌專門影響有害微藻，如 C. antiqua 和 .akashiwo 等（Imai 等，1991 年；Imai，2015 年）。 Yoshinaga 等人（1997 年）的研究表明，一株黃桿菌（C49 菌株）能有效、特異地抑制 ..akashiwo，而不影響甲藻或矽藻（Yoshinaga 等人，1997 年） 。從環境中分離出的另一株假交替單胞菌（蛋白質細菌類，γ 亞種，被鑑定為Y 菌株）能使有毒微藻（如Gymnodinium 和Gyrodinium）迅速膨脹， 後細胞即將溶解；在虹彩藻類Chattonella 和Heterosigma 上也觀察到類似的反應，它們受到同一菌株的嚴重破壞，在接觸後 內明顯溶解（Lovejoy 等人，1998 年）。然而，對於那些具有鱗甲的甲藻來說，Y 菌株的影響並不那麼嚴重，雖然它們能夠影響鱗甲板，甚至導致鱗甲板脫落和明顯的腫脹（變圓）跡象，但並不致命。因此，我們認為葉口的存在提供了對溶解性細菌化合物的保護，尤其是這種假交替單胞菌產生的溶解性細菌化合物（Lovejoy 等，1998 年）。

Alpha proteobacteria are frequently associated with dinoflagellates and diatoms, regardless of their toxicity (e.g. Roseobacter clade) (Granéli & Turner 2006). However, rather than mitigating , they appear to promote the formation of blooms and increase the toxin production. By small subunit ribosomal DNA (SSU rDNA) analysis, most of the ABs and GIBs have been classified as Gram-negative bacteria, belonging to the alpha- and gamma-proteobacteria group (mainly of the genera Alteromonas, Pseudoalteromonas, Pseudomonas and Vibrio) or Phylum Bacteroides (mainly of the genera Cytophaga and Saprospira) (Imai 2015; Ohtsuka et al. 2015).
α-蛋白細菌經常與甲藻和矽藻伴生，無論其毒性如何（如玫瑰桿菌支系）（Granéli 和 Turner，2006 年）。然而，它們並不能減輕 ，反而會促進 的形成。它們似乎會促進藻華的形成並增加毒素的產生。透過小亞基核醣體DNA（SSU rDNA）分析，大多數ABs 和GIBs 都被歸類為革蘭氏陰性菌，屬於α-和γ-蛋白菌群（主要是Alteromonas 屬、Pseudoalteromonas 屬、Pseudomonas 屬和Vibrio 屬）或菌門（主要是Cytophaga 屬和Saprospira 屬）（Imai，2015 年；Ohtsuka 等，2015 年）。

Algicidal mechanisms have been classified based on their direct or indirect nature (Lovejoy et al. 1998; Mayali & Azam 2004; Su et al. 2011). An example of direct effect is produced by the marine bacterium, Cytophaga sp., which is lethal to both diatoms and raphidophytes when added to algal cultures (Imai et al. 2001). Regarding indirect attacks, they are mediated by metabolites, which in many cases appear to be species-specific. Some examples of this type of indirect attack include peptides or enzymes (Imamura et al. 2000; Lee et al. 2008; Chen et al. 2011a,b; Wang et al. 2012), biosurfactants (Wang et al. 2005), pigments (Nakashima et al. 2006; Sakata et al. 2011) and antibiotic-like compounds (Dakhama et al. 1993; Lin et al. 2014). Compared with the number of algicidal bacterial strains which have been isolated and identified, there are less algicidal compounds successfully extracted, purified and identified. This is probably due to the difficulties in the purification of this type of compounds (Lin et al. 2014). Despite numerous examples of bacterial strains with strong algicidal and apparently specific activity, their use has not yet been attempted in the field. Further studies on the mechanisms of action associated with these bioactive compounds are required. The environmental impacts of the release of community organisms should be considered and discussed before considering to use biological control against HAB.
殺藻機制可根據其直接或間接性質進行分類（Lovejoy 等人，1998 年；Mayali 和 Azam，2004 年；Su 等人，2011 年）。直接作用的一個例子是海洋細菌 Cytophaga sp.，當其加入藻類培養物中時，對矽藻和蚜藻都有致死作用（Imai 等人，2001 年）。至於間接攻擊，它們是由代謝物介導的，在許多情況下似乎具有物種特異性。這類間接攻擊的一些例子包括勝肽或酵素（Imamura 等人，2000 年；Lee 等人，2008 年；Chen 等人，2011a,b；Wang 等人，2012 年）、生物表面活性劑（Wang 等人，2005 年）、色素（Nakashima 等人，2006 年；Sakata 等人，2011 年）和抗生素類化合物（Dakhama 等人，1993 年；Lin 等人，2014 年）。與已分離和鑑定的殺藻細菌菌株數量相比，成功萃取、純化和鑑定的殺藻化合物較少。這可能是由於純化此類化合物有困難（Lin 等人，2014 年）。儘管有許多例子表明細菌菌株具有很強的殺藻活性和明顯的特異性，但在實際應用中還沒有嘗試過。需要進一步研究與這些生物活性化合物相關的作用機制。在考慮使用生物防治技術防治有害藻華之前，應考慮並討論釋放群落生物對環境的影響。

There are a several studies linking the widespread abundance of viruses in the marine environment with their ecological importance (Proctor & Fuhrman 1990; Suttle 1994; Wommack & Colwell 2000; Brussaard 2005; Nagasaki 2008). However, the ecological role of the virus and, specifically, their relationship with eukaryotic microalgae has not been sufficiently investigated (Suttle 1994; Baudoux & Brussaard 2005; Nagasaki 2008). Algae viruses were initially
有多項研究將病毒在海洋環境中的廣泛存在與其生態重要性聯繫起來（Proctor & Fuhrman 1990；Suttle 1994；Wommack & Colwell 2000；Brussaard 2005；Nagasaki 2008）。然而，人們對病毒的生態作用，特別是它們與真核微藻的關係還沒有充分的研究（Suttle，1994 年；Baudoux & Brussaard，2005 年；Nagasaki，2008 年）。藻類病毒最初
(and almost completely) described as double-stranded DNA viruses of the family Phycodnaviridae (Suttle 1994; Mizumoto et al. 2007). Subsequently, new antecedents about RNA viruses capable of infecting marine photosynthetic protists have been published; for example, HaRNAV (Lawrence et al. 2001; Mizumoto et al. 2007) and RsRNAV (Shirai et al. 2006; Mizumoto et al. 2007) are positive-sense single-stranded RNA viruses that infect Heterosigma akashiwo microalgae (Raphidophyceae) and diatom Rhizosolenia setiger (Bacillariophyceae). Additionally, MpRNAV is a double-stranded RNA virus in the family Reoviridae that infects the cosmopolitan photosynthetic protist Micromonas pusilla (Prasinophyceae). However, the genomes of HaRNAV and RsRNAV have some characteristics similar to viruses of the order Picornavirales, based on phylogenetic analysis. The amino acidic sequence of the domain of the RNA-dependent RNA polymerase (RdRP) suggests that both viruses possess independent lineages, suggesting that they evolved from a deep internal branch in Picornavirales (Mizumoto et al. 2007). The interesting aspect about this type of biocontrol is its abundance in marine systems, great capacity, ease of replication and its high specificity for the host. However, this latter characteristic could in turn be considered a disadvantage, as this characteristic will make them unable to infect different genetic strains to the host species. As HABs are typically genetically heterogeneous, only a part of the population would be affected, limiting their application.
(幾乎完全）描述為 Phycodnaviridae 科的雙股 DNA 病毒（Suttle，1994 年；Mizumoto 等，2007 年）。例如，HaRNAV（Lawrence 等人，2001 年；水本等人，2007 年）和 RsRNAV（Shirai 等人，2006 年；水本等人，2007 年）。例如，HaRNAV（Lawrence 等人，2001 年；Mizumoto 等人，2007 年）和RsRNAV（Shira 等人，2006 年；Mizumoto 等人，2007 年）是正義單股RNA 病毒，可感染Heterosigma akashiwoidophyceae（Raph ）和矽藻Rhizosolenia setiger（Bacillariophyceae）。此外，MpRNAV 是 Reoviridae 科的一種雙股 RNA 病毒，感染世界性光合原生動物 Micromonas pusilla（Prasinophyceae）。然而，根據系統演化分析，HaRNAV 和 RsRNAV 的基因組具有一些與短小病毒目病毒相似的特徵。 RNA 依賴性RNA 聚合酶（RdRP）結構域的胺基酸序列表明，這兩種病毒都擁有獨立的品系，表明它們是從Picornavirales 的一個較深的內部分支演化而來的（Mizumoto 等人，2007 年） 。這類生物防治的有趣之處在於其在海洋系統中的大量存在、強大的能力、易於複製以及對宿主的高度特異性。不過，後一個特徵也可能被認為是一個缺點，因為這個特徵會使它們無法感染宿主物種的不同基因菌株。由於有害藻華通常具有基因異質性，因此只有部分族群會受到影響，這限制了其應用。

Finally, another proposed strategy for the control of introduced or exotic species is the genetic control using genetic engineering tools in species that allow to modify environmental tolerances, reproduction or other processes in undesired species. The issues associated with this kind of control strategy are similar in many ways to those associated with biological controversies about the potential negative impacts of introducing a nonnative manipulated organism into an open area. There are numerous examples in which genetic approaches have been successfully used in terrestrial agriculture, such as engineering plant crops so that they can produce their own insecticides. Similar genetic manipulations could be used in marine pests such as HABs. A HAB species that does not produce toxin could be produced. Alternatively, a bacterial strain or viral particles modified to achieve a greater pathogenicity towards HAB cells. However, the biosafety and ethical concerns associated with this issue are so far insurmountable.
最後，另一個控制引進或外來物種的建議策略是利用物種基因工程工具進行基因控制，從而改變不受歡迎物種的環境耐受性、繁殖或其他過程。與這種控制策略相關的問題在許多方面都與生物界關於將非本地受控生物引入開放區域的潛在負面影響的爭議相似。遺傳方法成功應用於陸地農業的例子不勝枚舉，例如對植物作物進行工程改造，使其能夠自行生產殺蟲劑。類似的基因操縱也可用於海洋害蟲，如有害藻華。可以培育出不產生毒素的 HAB 物種。或者，改造細菌菌株或病毒顆粒，使其對 HAB 細胞具有更強的致病性。然而，與此問題相關的生物安全和倫理問題迄今仍無法解決。

Although new generation of chemical algicides with greater specificity and lesser persistence have been described in recent years, the cost and environmental concerns have meant that they have not been tested at sea. In freshwater, both algicides and combinations of flocculants and other molecules have been effective in removing cyanobacteria blooms, although clays may also remove nutrients and toxins from the water column. Physical methods (airlift upwelling, perimeter skirts, etc.) for mariculture facilities are nowadays implemented. Despite of being useful and costeffective, these methods cannot control extense or persistent blooms. The only completely effective measure for control in the sea has been the use of clays to induce bloom flocculation. To achieve that, considerable quantities of clay are needed (from 100 to ). Although numerous studies have showed important improvements in clays that resulted in considerable reduction in the quantity required (e.g. PAC), the cost of the overall process has not been made public so far. Chinese examples of application suggest that this methodology could be extended to other affected areas. As clays are not toxic nor have important ecologic impacts, the use of clays (modified or not) is restricted to its cost of application. Despite the fact that promising biological mechanism for controlling HAB species has been described (mainly using algicidal bacteria), more research is needed to fully implement any of these methods in the field.
儘管近年來出現了特異性更強、持久性更低的新一代化學殺藻劑，但由於成本和環境問題，這些殺藻劑尚未在海上進行測試。在淡水中，殺藻劑以及絮凝劑和其他分子的組合都能有效去除藍藻藻華，儘管黏土也能去除水體中的營養物質和毒素。如今，海產養殖設施已採用實體方法（氣流上湧、圍裙等）。儘管這些方法有用且成本效益高，但無法控制大規模或持續的水華。唯一完全有效的海洋 控制措施是使用黏土來誘導藻華絮凝。要做到這一點，需要大量的黏土（從 100 到 ）。儘管大量研究表明，粘土的重要改進大大減少了所需數量（如 PAC），但整個過程的成本至今尚未公佈。中國的應用實例表明，這種方法可以推廣到其他受影響的地區。由於粘土沒有毒性，也不會對生態產生重大影響，因此粘土（無論是否經過改良）的使用僅限於其應用成本。儘管已經描述了控制有害藻華物種的有前途的生物機制（主要使用殺藻細菌），但要在實地全面實施這些方法，還需要更多的研究。

This research was supported by the University of Concepción (Chile) through the Program COPAS Sur-Austral (PFB-31/2007) and the Research Project VRID 216.096.067-1.0IN. We also thank funding from Conicyt, Chile (Fondecyt 2017, ref. 1170515).
本研究得到了智利康塞普西翁大學（University of Concepción）透過南澳 COPAS 計畫（PFB-31/2007）和研究計畫 VRID 216.096.067-1.0IN 提供的支持。我們也要感謝智利 Conicyt 公司的資助（Fondecyt 2017，編號 1170515）。

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