Spatial Temporal Expansion of Harmful Algal Blooms in Chile: A Review of 65 Years Records

Abstract

Harmful Algal Blooms (HABs) have been classified depending on the causative organism and its impacts: non-toxic HAB (microalgae capable of affecting tourism and causing oxygen deficiency, which generates mortality of marine organisms), toxic HAB (microalgae capable of transferring toxins to the food chain), and ichthyotoxic HAB (microalgae capable of generating mechanical damage in fish). HABs represent a worldwide problem and have apparently increased in frequency, intensity, and geographic distribution at different latitudes. This review details the occurrence of HAB events in the Southeast Pacific, Chile, over a 65-year period, analysing two of the three types of HAB described: toxic and ichthyotoxic HABs. For this, we conducted a review from many different scientific sources and from the written press and social media, that have mentioned HAB events in the country. In Chile, the microalgae involved in HAB events are dinoflagellate (52%), diatoms (33%) and silicoflagellate (10%), with a total of 41 species and/or genera described in the literature. A total of 501 HAB events were recorded in Chile between 1956 and 2021, where 240 (47.9%), 238 (47.5%), 14 (2.7%), 8 (1.5%) and 1 (0.2%) event were caused by diatoms, dinoflagellate, silicoflagellate, raphidophycean and haptophyte, respectively. An apparent increase in the frequency of HAB events is observed since the first record in 1956, with a maximum of 46 events during the years 2017 and 2019. The highest incidence in fish is caused by the group of silicoflagellate, raphidophycean and haptophyte (23 events), where 10 events caused mortalities in salmon with an incidence rate of 43.4%. Unlike what is observed with diatoms and dinoflagellate, the events associated with these groups are less frequent, but hold a much higher salmon mortality rate. During the last 65 years, HAB’s geographic extent shows an apparent trend to increase south-to-north. However, the identification of events is closely linked to the areas where much of the country’s aquaculture is located and, therefore, it could be biased. In turn, it is observed that the apparent increase in HAB events could be associated with a greater monitoring effort after major events (e.g., after the 2016 HAB event). On the other hand, it is also recognized a lack of knowledge about harmful algae throughout the Chilean Humboldt Current system, particularly in the northern regions, such as Atacama and Coquimbo. Therefore, the total number of blooms that have occurred in fjords and channels, particularly those that have caused minor economic impacts for artisanal fishermen and the salmon and mussel farming sector, might be underestimated.

1. Introduction

Phytoplankton are the base of the food chain in the marine environment, being the fundamental food for filtering organisms (bivalves), mollusc larvae and fish [1,2,3,4]. In the sea, phytoplankton develops on various temporal and spatial scales, being able to cause natural events such as algal blooms, defined as the intense proliferation of microalgae (millions of cells per litter), capable of changing the colour of the water in some instances [5,6]. These algal blooms are beneficial to filter-feeding marine organisms and therefore favour aquaculture and fishing activities [4,5,7].

In some cases, algal blooms can produce negative effects, potentially causing health, economic and environmental impacts [8]. These phenomena are known as Harmful Algal Blooms (HABs) also commonly known as red tides [9], and the natural phenomena produced by microalgae cause harm or damage to public health, tourism, fishing resources and aquaculture activities [10,11,12,13]. Within the 5000 species of phytoplankton described, about 200 are harmful species (0.4%), including taxa of cyanobacteria, dinoflagellate, raphidophycean, haptophyte and diatoms [13,14,15], which can have devastating effects on marine environments and inland waters, and on the economies of the coastal communities that depend on the extraction and cultivation of marine organisms [6,16,17,18].

HABs have been classified according to the causative organisms and their impacts, into three different types: (1) non-toxic HABs: microalgae capable of affecting tourism and causing oxygen deficiency, which generates mortality of marine organisms; (2) toxic HABs: microalgae capable of transferring toxins to the food chain; and (3) ichthyotoxic HABs: microalgae capable of generating mechanical damage in gills and other toxigenic reactions in fish [4,12,19,20]. These three types of HAB represent a worldwide problem [21] and there is an apparent increase in frequency, intensity, and geographic distribution at different latitudes [22,23,24].

Among the species of microalgae capable of generating HABs, some can produce chemical compounds of high toxicity, that are heat resistant and that can interfere, even in low concentrations, in physiological processes, such as the conduction of nerve impulses, the absorption of water and food in the intestine, or memory processing [25]. These types of toxic events represent serious concern for human health, animal health and the local economies, requiring constant monitoring [26].

The toxins of the microalgae that cause HABs are concentrated in marine organisms due to their feeding behaviour and they can act as transvectors of the toxins [27,28,29]. The most common transvectors are primary filter-feeding consumers such as mussels, oysters, clams, and razor clams, among others [13]. However, other organisms are also capable of accumulating marine toxins, and therefore, gastropods, cephalopods, crustaceans, and echinoderms have been included in routine monitoring [13,30]. The effect of direct human consumption of toxic marine organisms can be variable, depending on the type of toxin and its concentration [31]. However, the greatest concern is the group of saxitoxins (associated with the genus Alexandrium in Chile) for causing a paralysing syndrome in humans that can lead to death.

The factors related to the apparent increase in HABs worldwide are numerous, namely: (i) transport and release of ballast water from affected oceanic or coastal areas, (ii) anthropogenic activities that increase the availability of nutrients causing coastal eutrophication, and (iii) influence of climate change and large-scale phenomena such as the El Niño Southern Oscillation (ENSO), the North Atlantic Oscillation (NAO) and the Pacific Decadal Oscillation (PDO) [2,5,7,12,23,32,33,34,35,36,37,38].

Recently Hallegraeff et al. [15], through a meta- analysis on databases of HAB between 1985 and 2018, showed a trend of increased frequency and global distribution of HABs in Latin America and the Caribbean. However, he mentions that this tendency could also be attributed to the intensification of sampling efforts through scientific and monitoring activities, which are associated with the increment in aquaculture production.

There is a global trend of increased consumption of marine products [39]. One of the alternatives to meet the worldwide protein requirements is aquaculture, but fishing continues to contribute to this task [40]. The geographical characteristics of southern Chile have been suitable for the development of intensive industrial aquaculture and the extractive fishery of marine organisms for many years [41]. In Chile, 69% of the aquaculture industry farmed salmonid species with harvests above 989,000 t during 2019. The main species were Atlantic salmon (Salmo salar) with 71%, coho salmon (Oncorhynchus kisutch) with 21% and rainbow trout (Oncorhynchus mykiss) with 8% [42]. This sets Chile as the world’s second largest producer after Norway [41,43]. On the other hand, molluscs exports represent 29.3% of the national aquaculture production and is mainly represented by the harvest and farming of mussels (Mytilus chilensis) with a total of 380,000 t exported in 2019. This, which represents 76.7% of the production of molluscs at the national level, places Chile as the second largest world producer. Therefore, an important part of the Chilean economy depends on the marine environment and its resources, which are not exempt from the impacts of HABs and their health, environmental and socioeconomic consequences [41,43].

In 2016, in part due to the strong HAB event recorded that year caused by Alexandrium catenella, the losses on molluscs’ production were estimated at approximately USD 30–40 million. That same year, the losses due to the outbreak of Pseudochattonella cf. verruculosa affected between 18 and 20% of Chilean salmon production, equivalent to USD800 million [12]. These HAB phenomena coincided with a strong El Niño event and the positive phase of the Southern Annular Mode (SAM), which caused lower rainfall and higher solar radiation than those usually recorded in the affected areas. The same year the lowest supply of fresh water from the rivers in southern Chile was recorded for the last 66 years. Climate conditions generated much warmer and more stable sea water masses with unusual strong stratification in the region, favouring the occurrence and maintenance of the Pseudochattonella cf. verruculosa HAB event [40]. Mardones et al. [44], mentioned that the advection of more saline waters from marine areas could have been a key factor in the abundance and persistence of the P. verruculosa bloom. The increase in salinity and the significant reduction of fresh water from the Puelo River, could have favoured the development of this microalgae [40]. This is consistent with results obtained in the laboratory, where the maximum cell abundance of this species was significantly higher at salinities of 30 psu [17].

Currently, weekly monitoring of marine toxins is carried out in the framework of the Bivalve Mollusc Health Program (PSMB) of the Servicio Nacional de Pesca y Acuicultura (SERNAPESCA), whose objective is to monitor mollusc harvesting areas to ensure food safety for exports. There are currently 159 sampling stations for marine toxins and phytoplankton. PSMB results are updated daily by an Early Warning System for Red Tides (mr-SAT), providing real-time information for fast decision-making. In addition, regional laboratories of the Ministry of Health monitor shellfish harvesting areas from natural beds.

This review analyses the occurrence of historical HAB events in Chile, focusing on two of the three HAB types [20]: First, toxic HAB events, and ichthyotoxic HAB events or events capable of causing damage to fish.

2. Materials and Methods

A bibliographic search was carried out in the ISI Web of Science database using as keywords HABs and the combinations of HABs + Events and HABs + Events + Chile in all fields, with the aim of carrying out an historical reconstruction of HABs occurrences and events in Chile. When the HABs term was searched individually, the database returned 1328 publications, from 2010 to date, with a maximum of 199 publications (15%) in 2019 (Figure 1). When the HABs + Events keyword combination was used, the search dropped to 222 articles and when the HABs + Events + Chile combination was used, the search dropped to just 7 matches. The abstracts of the articles were read to prioritize the publications of studies associated with HABs.

Concomitantly, the search included the analyses of government monitoring programs such as the National Program for Surveillance and Control of Harmful Algal Phenomena—Ministry of Health; databases of the “Management and Monitoring of Red Tides in the Los Lagos, Aysén and Magallanes regions” of the Instituto de Fomento Pesquero (IFOP), including information from 2006 to 2020; toxin databases of the Laboratory of Marine Toxins of the Universidad de Chile; databases from the Instituto Tecnológico del Salmón (INTESAL) and bulletins generated by Servicio Nacional de Pesca (SERNAPESCA), regarding salmon farming centres monitoring.

Complementarily, a search was carried out in the written press and social media which mentioned HAB events in Chile.

The criteria for classifying a bloom or HAB event, were as follows: (1) To be qualified as a HAB event in the scientific literature; (2) in the case of toxic HAB, to have toxin concentrations above the regulatory limits (

Table 1. Thresholds for marine toxins in exported bivalve molluscs (PSP = Paralytic shellfish poison, ASP = Amnesic shellfish poisoning, DSP = Diarrhetic shellfish poison) regulated by the Bivalve Mollusc Health Program (PSMB) in Chile [46].

Toxin Syndrome	Toxin	Thresholds Limits
PSP	Saxitoxin (equivalent)	≥80 µg eq. STX/100 g
ASP	Domoic acid	≥20 mg/Kg
DSP (Lipophilic toxins)	Okadaic acid (OA) and Dinophysistoxins (DTX1 and DTX2)	≥160 µg/kg
	Pectenotoxins (PTX1 and PTX2)
	Azaspiracids (AZA1, AZA2 and AZA3)	≥160 µg eq. AZA/kg
	Yesotoxins (YTX, 45-OH-YTX, homo-YTX, 45-OH-homo-YTX)	≥3.75 mg eq. YTX/kg

), or microalgal abundance higher than the levels pre-established by SERNAPESCA to trigger contingency plans; and (3) in the case of non-toxic HABs, to have microalgal abundance above the harm threshold established by SERNAPESCA or have an abundance equal to or higher than the first recorded incidence of the species [39,45] (

Table 2. List of harmful microalgae monitored in salmon farms in Chile and their threshold limits [45]. n.i = no information.

Microalgae	Threshold Limits (Cell × mL−1)	Mechanism of Action
Alexandrium catenella	>300	Ichthyotoxic
Azadinium spp.	Unknown	n.i
Chaetoceros convolutus	>5	Mechanic
Chaetoceros cryophilus	>5	Mechanic
Octactis speculum	>75	Mechanic
Eucampia zodiacus	>400	Mechanic
Gymnodinium spp.	Unknown	n.i.
Heterosigma akashiwo	>20	Ichthyotoxic
Karenia mikimotoi	>40	Ichthyotoxic
Karenia spp.	>40	Ichthyotoxic
Leptocylindrus danicus	>2500	Mechanic
Leptocylindrus minimus	>2000	Mechanic
Pseudochattonella cf. verruculosa	>50	Ichthyotoxic
Rhizosolenia aff. setigera	>500	Mechanic
Thalassiosira pseudonana	>3000	Rheotoxicity
Haptophyte	Unknown	n.i.

).

Based on the collected information, tables were generated by genus and/or species, incorporating the following data for each event: year, month, locality, region, species, maximum recorded abundance (cell mL⁻¹), main impact, maximum concentration of toxins and the bibliographic reference. This information is available in Supplementary Materials as Tables S1–S6.

3. Results and Discussion

3.1. Occurrences and Events of HABs in Chile

HABs are caused by different microalgae phyla: Bacillariophyta (class Bacillariophyceae), Haptophyta, Miozoa (class Dinophyceae), and Ochrophyta (class Dictyophyceae and Raphidophyceae). In the text and figures, the species belonging Haptophyta are named by phyla. The Bacillariophyceae are nominated henceforth by the vernacular name diatoms, the Dictyophyceae as silicoflagellate and the Dinophyceae as dinoflagellate. In Chile, the species that causes HABs are mainly dinoflagellate (51%), diatoms (34%) and silicoflagellate (10%) (Figure 2A), with a total of 41 species and/or genera described in the literature.

Representatives of the dinoflagellate group are 21 taxa: Alexandrium catenella; Alexandrium spp.;) Amphidoma sp.; Azadinium sp.; Dinophysis acuminata; Dinophysis acuta; Dinophysis spp.; Gonyaulax spinifera; Gonyaulax taylorii; Gymnodinium spp.; Karenia mikimotoi; Karenia selliformes; Karenia spp.; Karlodinium australe; Kryptoperidinium triquetrum; Lepidodinium chlorophorum; Lepidodinium spp.; Margalefidinium polykrikoides; Prorocentrum lima; Prorocentrum micans; Protoceratium reticulatum.

In the case of diatoms, 14 taxa were registered: Chaetoceros convolutus; Chaetoceros cryophilus; Eucampia zodiacus; Leptocylindrus danicus; Leptocylindrus minimus; Pseudo-nitzschia australis; Pseudo-nitzschia calliantha; Pseudo-nitzschia delicatissima; Pseudo-nitzschia pseudodelicatissima; Pseudo-nitzschia seriata; Pseudo-nitzschia spp.; Pseudo-nitzschia subfraudulenta; Rhizosolenia setigera; Thalassiosira pseudonana.

There are four silicoflagellate species: Octactis speculum; Pseudochatonella verruculosa; Pseudochatonella spp; Vicicitus globosus, raphidophycean represented by Heterosigma akashiwo; and the haptophyte by undetermined species (

Table 3. Species that caused HABs events in the different regions of Chile, from south to north.

	Magallanes	Aysén	Los Lagos	Biobío	Coquimbo	Atacama	Antofagasta	Tarapacá	Arica- Parinacota
Dinophyceae (Dinoflagellate)
Alexandrium catenella	x	x	x				x *
Alexandrium spp.					x		x
Amphidoma sp.	x *
Azadinium sp.	x
Dinophysis acuminata	x	x	x	x	x	x			x
Dinophysis acuta		x	x
Dinophysis spp.		x	x
Gonyaulax spinifera			x
Gonyaulax taylorii							x
Gymnodinium spp.	x	x	x
Karenia mikimotoi	x	x
Karenia selliformes	x		x
Karenia spp.		x
Karlodinium australe	x
Kryptoperidinium triquetrum	x	x	x
Lepidodinium chlorophorum			x
Lepidodinium spp.		x	x
Margalefidinium polykrikoides			x
Prorocentrum lima						x
Prorocentrum micans			x					x	x
Protoceratium reticulatum	x	x	x				x
Bacillariophyceae (Diatoms)
Chaetoceros convolutus	x	x	x
Chaetoceros criophilus		x	x
Eucampia zodiacus	x	x	x
Leptocylindrus danicus		x	x
Leptocylindrus minimus	x	x	x
Pseudo-nitzschia australis	x	x	x		x	x	x
Pseudo-nitzschia calliantha					x	x
Pseudo-nitzschia delicatissima		x
Pseudo-nitzschia pseudodelicatissima	x	x	x		x	x
Pseudo-nitzschia seriata		x
Pseudo-nitzschia spp		x	x		x	x
Pseudo-nitzschia subfraudulenta					x	x
Rhrizosolenia setigera	x	x	x
Thalassiosira pseudonana		x	x
Dictyophyceae (Silicoflagellate)
Octactis speculum		x	x
Pseudochatonella spp.			x
Pseudochatonella verruculosa		x	x			x
Vicicitus globosus			x
Raphidophyceae
Heterosigma akashiwo			x
Haptophyta			x

* Species identification not verified.

).

A total of 501 HAB events has been recorded in Chile in 65 years, where 240 (47.9%), 238 (47.5%), 14 (2.7%), 8 (1.5%) and 1 (0.2%) event were caused by diatoms, dinoflagellate, silicoflagellate, raphidophycean and haptophyte, respectively (Figure 2B).

The regions with a greater number of species that have caused HAB events in Chile are, in decreasing order, Los Lagos, Aysén, Magallanes, Atacama, Coquimbo and Antofagasta with 29, 23, 16, 8, 7 and 5 HAB species, respectively. The Arica-Parinacota region have two HAB-species, while the Biobío and Tarapacá regions have one species that causes HAB events. The regions of La Araucanía, Ñuble, Maule, O’Higgins and Valparaíso do not present species that cause HAB events (Figure 3, Table 3).

In Chile, an apparent increase in the frequency of HAB events has been registered since the first record in 1956, with a maximum of 46 events observed during 2017 and 2019 (Figure 4).

The number of events per region amounted a total of 201, 147, 101, 14, 12, 10 and 2 events in the regions of Aysén (41%), Los Lagos (30%), Magallanes (21%), Atacama (2.8%), Coquimbo (2.4%), Antofagasta (2%) and Arica (0.4%), respectively. The regions of Tarapacá and Biobío registered only one event each (Figure 5).

3.2. Toxic HAB in Chile

In Chile, three types of marine biotoxins have been described according to their toxic effects and have been classified as: (1) PSP (Paralytic Shellfish Poison; saxitoxins). (2) DSP (Diarrhetic Shellfish Poison) (associated with 4 groups of toxins: (a) Okadaic Acid (OA) and Dinophysistoxins (DTX1 and DTX2); (b) Pectenotoxins (PTX1 and PTX2); (c) Yesotoxins (YTX, homo YTX, 45-OH-YTX and 45-OH-homo-YTX and d) Azaspiracids (AZA1, AZA2 and AZA3) (From these groups only OA, Dinophysistoxins and Azaspiracids have been shown to produce diarrhoea in humans). (3) ASP (Amnesic Shellfish Poison associated with domoic acid) [9,47]. The microalgae responsible for toxic HAB events are the dinoflagellate Alexandrium catenella (PSP), Dinophysis spp. and Protoceratium reticulatum (DSP) and Pseudo-nitzschia spp. (ASP) [25]. The PSP is the most worrying toxin due to its lethal effects on humans. In 2009, the Undersecretary of Fisheries and Aquaculture (SUBPESCA) declared A. catenella as a plague in the area from parallel 43°22′ S to 55° S [31]. A. catenella was classified as a “population of a hydrobiological species that, due to its abundance or density, can cause negative effects on human health, on hydrobiological species or on the environment, causing detriment and economic losses to activities such as extractive fisheries or aquaculture”. Due to this, SERNAPESCA maintains a surveillance program for the vegetative form (cysts) of A. catenella [48].

Toxic HAB events in Chile are mainly caused by the PSP syndrome, with 41% of occurrences, followed by DSP and ASP syndrome, with 35% and 24% of occurrences, respectively (Figure 6).

3.2.1. Paralytic Shellfish Poison in Chile (PSP)

The dinoflagellate of the genus Alexandrium is the producer of paralytic shellfish toxins (PSP) made up of more than 40 saxitoxin analogues, including saxitoxin itself (STX), neoSTX, gonyautoxins (GTX), decarbamoyl-gonyaulatoxins (dcGTXs) and the sulfocarbamoyl-saxitoxins (C1-C4) [49,50]. These neurotoxins specifically block voltage-gated sodium channels, causing muscle paralysis by blocking nerve impulses in a large variety of species including vertebrates [51]. Symptoms starts between 15 and 60 min after ingestion of contaminated shellfish, and the severity of the poisoning depends on the toxicity and quantity of the shellfish consumed and the susceptibility of the patient (children, women, men, in that order). A sample is classified as toxic, according with the Chilean regulation, when the paralyzing toxin levels are ≥80 µg of equivalent STX per 100 g of shellfish meat. In that case, the authorities close the aquaculture and fishing areas, forbid the extraction, marketing, and distribution of shellfish.

Currently, the PSP syndrome has a wide geographical distribution in Chile, presenting events associated with the Alexandrium genus in at least 6 regions throughout the country, from south to north: Magallanes, Aysén, Los Lagos, Coquimbo, and Antofagasta (Figure 2, Table 3 and Table S1 [12,30,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78]). In the north of the country (Coquimbo and Antofagasta), only the presence of Alexandrium ostenfeldii has been confirmed as a probable producer of paralyzing toxins [79]. However, in the two registered events, it was not possible to correctly define the microalgae species responsible for the toxic events [67]. On the other hand, paralyzing toxins are present in northern Chile in concentrations below the regulatory limits, from the Arica and Parinacota to the Coquimbo region, which could be associated with the presence of A. ostenfeldii [79]. It has also been shown that strains of A. ostenfeldii isolated from southern Chile are producers of GTX and STX [80].

Also noteworthy is an event of A. catenella (then known as Gonyaulax catenella) recorded in the spring of 1982 in San Jorge Bay, in the Antofagasta region, with an abundance of 339 cells mL⁻¹ [54], although the presence of this species in that event is challenged by other experts (Guzmán, personal communication).

A total of 67 HAB events associated with Alexandrium spp were recorded, with 36 fatalities and 497 intoxications. The events occur mainly in the spring–summer months, with some exceptions in the far south of the country. The most toxic events occurred in the years 1996, 1997, 1998, 2000, 2002, 2003, 2005, 2006, 2009, 2016 and 2017, and were associated with a greater number of intoxications and fatalities (Table S1). In some cases (1972, 2002, 2016), PSP toxicity exceeded 10,000 µg STX eq./100 g.

Of the 67 events identified from 1972 to 2021, the highest number of occurrences happened during 2002 with a total of six events (Figure 7). Considering the distribution by geographic zones, the Aysén region had 45% of the events, followed by the Magallanes and Los Lagos regions, with 31% and 18%, respectively. The Antofagasta region had 4% of the events, while the Coquimbo region had 2% of the occurrences (Figure 8).

The first record of a A. catenella bloom occurred in October 1972 in the southern area of Magallanes, with abundances of 600 cells mL⁻¹ and estimated toxin concentrations of 17,289 µg STX eq./100 g of shellfish. This first event caused three fatalities [52]. Subsequently, blooms of this species were recorded in 1981 and 1989, with 34 intoxicated and 2 fatalities [30,55,56]. From 1991 to 2021, the blooms of A. catenella are constant and almost permanent in the Magallanes region, presenting closures or prolonged bans in some sectors.

In 1992, the presence of A. catenella in the Aysén region was confirmed; however, the first toxic event was recorded in 1994 [30]. In May 1995, another event in the Aysén region caused, for the first time, the closure of fishing areas for bivalve molluscs, and one fatality and 12 intoxications were recorded [56]. The blooms of A. catenella in the Aysén region, as in Magallanes, are now constant, registering various events since then (Table S1). This was the beginning of an apparent expansion of the geographic distribution of A. catenella from south to north, encompassing other regions of the country. In 2002, the presence of A. catenella was confirmed in the south of the Chiloé province, in the Los Lagos region. This province, characterized by the production and harvest of both salmon and mussels, was strongly affected by this event, which left 50 intoxicated and three fatalities, in addition to economic losses due to salmon mortalities and the closure of areas for mussel harvesting [12,57].

One of the strongest toxic events in Chile was recorded between January and May 2016 in the Chiloé Archipelago, reaching toxicity values up to 10,410 µg STX eq./100 in the Punta Queler sector in the inner sea of Chiloé (PSMB regulatory analyses were registered by the Laboratory of Marine Toxins of the Universidad de Chile). This event surpassed the area coverage compared to the one recorded in 2002, which only covered the southern end of the Isla Grande de Chiloé, but nevertheless recorded a maximum value of 29,544 µg STX eq./100 [9]. This mega-event intoxicated 12 people and caused the death of marine invertebrates and vertebrates on the west coast of the Chiloé Archipelago [72]. The authorities decided on the closure of fishing areas for bivalve molluscs from natural stocks and mussel farming [12]. (In some areas of the inner sea of Chiloé, the clearance to subtoxic levels (≤80 STX eq. 100 g⁻¹) in some of the bivalve species took more than a year (LABTOX pers. comm.). This mega-event involved 3 regions of the country, (from 39 to 45° S), expanding the distribution of A. catenella to the Los Ríos Region [81].

While the highest impact of Alexandrium blooms is the risk of human life due to PSP, this species is also recognized as ichthyotoxic and produces economic losses due to massive salmon mortalities in farms. The years in which salmon mortalities occurred due to events associated with A. catenella were 2002, 2006, 2009 and 2018 (Table S1).

3.2.2. Lipophilic Marine Toxins

Lipophilic toxins encompass a wide group of marine toxins derived from different agents, all of which are dinoflagellate. Some toxins from this group cause gastrointestinal effects in humans. Because of this, lipophilic toxins were first labelled as Diarrheic Shellfish Poisoning (DSP) syndrome. Species of the genus Dinophysis produce okadaic acid (OA) and the dinophysistoxins derivatives (DTXs 1 and 2) and are also involved in the production of pectenotoxins (PTX-1 and 2). Dinoflagellate such as Protoceratium reticulatum, Lingulodinium polyedrum and Gonyaulax spinifera have been described as being responsible for producing yessotoxins (YTXs) [82]. Finally, the dinoflagellates of the genus Azadinium produce a complex set of more than 40 azaspiracids. The congeners AZA1, AZA2 and AZA3, among others, cause diarrhoeal poisoning with symptoms like those produced by OA and its derivatives. Of the four groups mentioned, only OA and its derivatives, and AZA, have diarrheic effects, while PTXs and YTXs have hepatotoxic and cardiotoxic effects, respectively [83,84,85]. The European community has recently excluded PTX as a toxin to be monitored, and in Japan, PTX and YTX are not considered among toxins that cause risk to public health.

In Chile, the events associated with these lipophilic toxins have occurred frequently since the first record produced by the dinoflagellate Dinophysis acuta in 1970 in the Reloncaví Estuary [52], affecting more than 200 people, who suffered gastrointestinal disorders after consuming mussels (Aulacomya atra) and no fatal cases were reported [30] (Table S2). Intoxications by lipophilic toxins could be underestimated because people do not always go to health centres upon intoxication or due to confusion regarding the identification of the causative agent. In order to truly define intoxication by lipophilic toxins, a detailed clinical history of the patient and a record of the foods recently ingested are necessary [47]. Currently, lipophilic toxins have a wide geographic distribution in Chile, with events associated with the genus Dinophysis and the species Protoceratium reticulatum, Gonyaulax taylorii, Gonyaulax spinifera, Azadinium sp. and Amphidoma sp. in 8 regions throughout the country: Magallanes, Aysén, Los Lagos, Biobío, Coquimbo, Antofagasta, Atacama and Arica-Parinacota over 4000 km of coast (Table 3 and Table S2). A total of 99 events have been recorded, 77 associated with the genus Dinophysis, 11 produced by Protoceratium reticulatum, 5 by Azadinium sp and 1 event associated with Gonyaulax taylorii, Gonyaulax spinifera and Amphidoma sp. These events produced in total 254 intoxications, altsshough some authors described over 500, but without specifying the years [30]. In general, the events occur in spring–summer, with some exceptions in Aysén (Table S2, [12,30,52,58,65,70,75,83,84,86,87,88,89,90,91,92,93,94,95,96,97,98,99,100,101,102,103,104,105,106,107,108,109,110,111]).

Of the events identified from 1970 to date, the highest number of events occurred during 2019 with a total of 12 records during that year (Figure 9). The species that account for the highest proportion of occurrences of lipophilic toxins in Chile were, in decreasing order, D. acuminata (49%), D. acuta (27%), P. reticulatum (12%), Azadinium sp (5 %), Dinophysis spp (4%), Gonyaulax taylorii (1%), Gonyaulax spinifera (s1%) and Amphidoma sp. (1%) (Figure 10 A). Regarding the geographical distribution, the Aysén region represented 53% of the events, followed by the Los Lagos and Magallanes regions, with 24% and 17%, respectively. The regions of Antofagasta, Coquimbo, Atacama, Biobío and Arica-Parinacota, showed a low percentage of occurrences, with less than 10% of the total (Figure 10B).

Since the first record in 1970, outbreaks of lipophilic toxins have occurred in the southernmost regions of the country. The Aysén Region has been affected since 1980 and the Magallanes Region since 1998 [83,84,85,92]. During P. reticulatum blooms, in 2015 and 2016, precautionary closures were adopted due to the presence of YTX (Table S2) detected for the first time in Chile by mass spectrometry and associated with the Bivalve Mollusc Health Program (PSMB) that authorizes the export of bivalve molluscs [12,94,100,112].

The production of OA, DTX and PTX by species of Dinophysis has been described by various authors [93,94,99,100,105,112,113]. D. acuminata has been associated with the production of DTX-1 in the Magallanes region [114] and with PTX-2 in samples obtained from the Reloncaví Estuary in Los Lagos region [112]. In northern Chile, during the summer of 2007/2008, PTX-2, PTX-11, PTX-2sa and YTX were identified in fractionated plankton samples from the Bay of Arica, being the first report of these toxins in Chilean coastal waters [98]. In the central coast of Chile, the presence of PTX-2 has been confirmed in samples of razor clams (Tagelus dombeii) associated with a spring event by D. acuminata in Bahía Tubul in the Biobío region [97]. On the other hand, D. acuta has been associated with the production of okadaic acid (OA) and PTX in Chile [91].

In the Chonos Archipelago in southern Chile (Aysén region), YTX was identified for the first time in samples of mussels (Mytilus chilensis) obtained during January 1991 [115]. Years later, in the Arica Bay in northern Chile, Krock et al. (2009) [98] identified, also for the first time, PTX and YTX, associated with a D. acuminata bloom and P. reticulatum cysts, respectively. After that, in Bahía Mejillones in northern Chile (Antofagasta region), Álvarez et al. [84] confirmed the presence of YTX in phytoplankton samples obtained from a P. reticulatum bloom. The same authors [84] identified the presence of YTX, associated with the dinoflagellate Gonyaulax taylorii, establishing this species for the first time as a source of YTX. During the summer of 2019, strandings of marine invertebrates were observed in the north coast of Chile, in the regions of Tarapacá, Atacama and Coquimbo, and included the death of starfish, clams, sea urchins and squids, with analysis revealing concentrations of 0.1–0.45 mg/kg of YTXs [111].

In the Los Lagos and Aysén region, the presence of P. reticulatum was positively correlated with the detection of YTXs in shellfish [99,116]. The presence of subtoxic levels of YTX represented 80.1% of the samples detected, during a study from October 2015 to September 2018, where in some sectors, the presence of YTX coincide with the presence of P. reticulatum [112]. The mortality of marine fauna attributed to YTX has been reported in other geographical areas around the world. For example, in 2011, a mortality event associated with the presence of the dinoflagellate Gonyaulax spinifera and YTX levels below 0.1 mg kg⁻¹ was reported in Sonoma County, California, affecting different marine invertebrates such as red and purple sea urchins, starfish and abalone. Additionally, in 2017, a mass mortality of 250 t of abalone was reported in different aquaculture centres along the South African coast associated with a Gonyaulax spinifera bloom [91,117]. These suggest that YTXs may have been the main cause of marine invertebrate mortality in Chile, however, more research is needed to understand the mechanisms and the effects of the toxins on the tissues and cells of the affected species. The mechanism of action of YTX in molluscs is poorly understood; however, immunochemical studies have shown the effect of YTX in the immune system, digestive functions, and calcium homeostasis. King et al. [118] exposed juvenile oysters to a P. reticulatum bloom causing strong feeding rejection and complete shell closure.

Other toxins have been detected in Chilean waters. Trefault et al. [85] identified gymnodimines (GYM) for the first time, with a distribution from Puerto Aysén to Temuco (Aysén to Araucania region), and also off the coast of Copiapó (Atacama region). It has been shown that this toxin is produced by the microalgae Alexandrium ostenfeldii and Karenia selliformes (previously known as Gymnodinium selliforme) [85]; however, the latter was rejected as a producer of GYM in Chile in laboratory cultivation experiments [119]. Trace levels of AZAs have been identified in shellfish samples [66,84,120] and the species Azadinium poporum was identified in Caleta Chañaral (Atacama region) in northern Chile as a possible producer of this toxin [121]. The microalgae of the genus Azadinium, which causes AZAs, are smaller (<15 µm) than the usual phytoplankton nets mesh size, which makes sampling difficult. On the other hand, the production of AZAs has also been attributed to the genus Amphidoma. In this sense, Campodonico & Guzmán [52], registered a bloom of Amphidoma sp. in the Strait of Magellan in 1973, with a maximum of 678 cells mL⁻¹. During that event, human poisoning was observed with no fatal cases; however, due to the lack of a specialized testing laboratory, the toxin could not be identified. Currently, the presence of Amphidoma sp. in Chile has not been confirmed, so the specific determination made in 1973 is still in doubt (Guzmán, pers. comm.).

Other emerging lipophilic toxins not subject to regulation correspond to previously described as “fast-acting” toxins or FATs, including spirolides (SPX) [97], the aforementioned GYMs [85] and pinnatoxins (PnTXs), produced by Alexandrium ostenfeldii, Karenia sp and Vulcanodinium rugosum, respectively.

3.2.3. Amnesic Shellfish Poison in Chile (ASP)

Diatoms of the genus Pseudo-nitzschia produce domoic acid (DA), a potent neurotoxin that acts as a glutamate agonist and is excitotoxic in the central nervous system [66,86]. This toxin is responsible for amnesic shellfish poisoning (ASP), which produces gastrointestinal and neurological problems, such as short-term memory loss [85,122]. These effects were described for the first time in 1987 in eastern Canada, where the ingestion of farmed mussels caused the intoxication of at least 250 people and 3 fatalities, determining DA as a toxin and the diatom Pseudo-nitzschia multiseries (ex Nitzschia pungens) as the causative agent [123].

Of the events identified from 1994 to date, the highest number of occurrences happened during 2016 with a total of 15 events during that year (Figure 11). Currently, amnesic toxins have a limited geographical distribution in Chile, with events associated with the Pseudo-nitzschia occurring in 5 regions throughout the country: Magallanes, Aysén, Los Lagos, Coquimbo, and Atacama (Table 3 and Table S3, [12,58,66,69,70,75,95,96,101,102,103,104,107,109,110,122,124,125,126,127]). A total of 118 events were recorded, without associated human intoxications. In general, the events occurred in the spring-summer, with small exceptions in northern Chile, where the events have occurred in late winter (Table S3). The events associated with Pseudo-nitzschia spp. have occurred in the resgions of Aysén (36%), Los Lagos (29%) and Magallanes (16%). Despite this, ASP has been particularly relevant in the northern zone of Chile, 19% of the events happening in the Atacama (10%) and Coquimbo (9%) regions (Figure 12).

In Chile, DA was detected for the first time in 1997 in shellfish from aquaculture farms in southern Chile [122]. Pseudo-nitzschia spp. blooms had been previously identified in 1994–1995, but without establishing the toxicity of the event [89]. ASP events have occurred with toxin levels exceeding the regulatory limit (20 µg/g), even with values over 300 µg/g, which have caused precautionary closures of fishing areas for bivalve molluscs (Table S3). On the other hand, it has been reported that the toxin is rapidly cleared by molluscs, both mussels and oysters, so once the number of cells of the causing agent decreases, clearance is achieved in a few days [12,122,128].

Within the species that produce DA in Chile, P. australis, P. pseudodelicatissima and P. calliantha have been identified [31,124]. In other species such as P. subfraudulenta, the production of DA has not been confirmed; however, they are described as part of a complex of toxin-producing species in Bahía Inglesa in Atacama region [124](Table S3).

One of the most extensive and intense events occurred in the spring of 2006 in Bahía Inglesa. This event was characterized by the dominance of P. australis, reaching an abundance of up to 1700 cells mL⁻¹, with toxin concentrations in scallops never recorded for this area (103 µg/g) [12]. Years later, and due to the growing concern of ASP events in the northern zone, public health monitoring programs detected another intense event in the Atacama region in December 2008, with toxin concentrations in shellfish of 198.5 µg/g (Table S3). In the Los Lagos region, one of the most severe events was recorded in 2014, triggering precautionary closures in several mollusc farming areas, with maximum concentrations of DA that exceeded 300 µg/g in mussels in November 1999 (LABTOX). Recently, two events in the Los Lagos region were recorded during December 2020 [129] and from January to March 2021, in the Huenquillahue and Chiloé areas, respectively. These events, apparently unrelated, had durations not previously recorded for this area (2 to 3 months). In Chiloé, the event happened mainly in the Quinchao Island, with values exceeding 130 µg/g of DA. Precautionary closures remained for several weeks, affecting many farming centres that at the time were in their harvest season (Table S3).

Similarly, to DSP and PSP the most common ASP transvector are filter-feeding bivalves such as mussels, clams, scallops, and oysters, but the presence of DA has also been registered in the tunicate Pyura chilensis, also a filter-feeder [129] with a high landing (over 2500 t in 2019) [42].

3.3. HABs: Ichthyotoxic or Capable of Causing Damage to Fish

The HABs that affect fish act through three main mechanisms: (a) oxygen depletion in the water column, (b) mechanical damage and/or (c) by toxicity of dinoflagellate metabolites [12]. The harmful effects of HABs on fish include: mortalities, stress, hypoxia, trauma due to oxygen supersaturation, mechanical damage (physical damage or irritation of the gills) and reactions to ichthyotoxic agents. These effects represent economic costs to companies and are often not reported in the scientific literature, being handled exclusively by salmon farming centres. Although in some cases there have not been mortalities, the harmful effects of HAB on fish represent a gateway to other pathogens (INTESAL).

In southern Chile, HABs have affected the salmon farming industry since 1983, causing significant mortality throughout the geographic area where this activity occurs, especially in the Chiloé inland sea. One of the first known blooms in Chile that have affected this industry, was the one recorded as “brown tide” caused by the raphidophycean Heterosigma akashiwo, which produced high mortality in the incipient salmon industry in Chile in September of 1988. This event killed nearly 2000 t of fish in the Los Lagos region, with economic losses of USD11 million (Table S6). The microalgae concentrations reached values over 100,000 cells mL⁻¹ [30]. In 1999, HABs associated with Karenia selliformis (identified at that time as Gymnodinium spp) reached a maximum concentration of 4000 cells mL⁻¹ extended for about a month and killing around 1125 t of fish in the Chiloé Archipelago. The outbreak happened from mid-March to mid-April of 1999 [130] (Table S5). During the summer of 2002 and the spring of 2009, A. catenella outbreaks were recorded; however, it was during 2009 that the concentrations reached up to 5000 cells mL⁻¹, ranging from the Aysén region to the south of Isla Grande de Chiloé in the Los Lagos region, generating losses of at least USD10 M to the salmon industry [12,131] (Table S1).

In 2014, a great mortality of salmonids due to HAB was recorded for the first time in the Magallanes region associated with the dinoflagellate Karlodinium cf. australe, not previously registered as harmful to salmon in Chile [132] (Table S5).

During the summer of 2016, an outbreak of Pseudochattonella cf. verruculosa caused high economic losses. The presence of the microalgae was recorded in at least 45 salmon centres in southern Chile, which killed 39,942 t of fish, with losses of up to M$800 USD. The 2016 ENSO, promoted conditions for the proliferation of P. verruculosa and other HAB species such as A. catenella recorded in the following months, which also generated mortalities in molluscs and fish [12,43]. Although Pseudochattonella sp. had been associated with several salmon mortality events in January–February 2005, 2009, and 2011, the last event in 2016 turned out to be the most massive and aggressive, spreading over large areas in the interior of fjords and channels in southern Chile. On the other hand, P. verruculosa is a species recently reported in Chile, so the study of its ecology is a topic yet to be addressed [17] (Table S6).

The HABs with fish mortality in Chile are mostly associated with dinoflagellate (46%), diatoms (29%) and silicoflagellate (17%) (Figure 13A), with a total of 24 species and/or genera. On the other hand, of the 220 events registered in Chile, 122 (56.2%), 72 (33.2%), 14 (6.45%), 8 (3.7%) and 1 (0.5%) event were caused by diatoms, dinoflagellate, silicoflagellate, raphidophycean, and haptophyte, in that order (Figure 13B). The species with the most recorded events are Chaetoceros convolutus (18%), Kryptoperidinium triquetrum (18%), Leptocylindrus minimus (10%), Eucampia zodiacus (9%), Rhrizosolenia setigera (8%), Leptocylindrus danicus (6 %), Gymnodinium spp. (6%) and Prorocentrum micans (5%), with 80% of the total events (Figure 14).

The regions that have a higher number of HAB events associated with fish mortality in Chile are, in decreasing order, Los Lagos, Aysén, Magallanes, Antofagasta and Atacama, with 37%, 37%, 22%, 2% and 1% of occurrences, respectively. The Tarapacá and Arica-Parinacota regions presented a percentage of less than 1% of the occurrences (Figure 15).

On the other hand, of the events identified from 1956 to date, the highest number of occurrences happened during 2019 with a total of 26 events (Figure 16).

The first event associated with fish mortality was observed in 1956 in the Arica-Iquique area [30]. Of the total number of events identified, 27 caused mortality in salmon and another 11 events killed other marine organisms. However, cases of blooms of harmful species have also been observed without fish damage and mortality (Tables S4–S6).

In the final phase of the “La Niña” during the summer of 2021, an intense positive phase of the Southern Annular Mode (SAM), atmospheric pressures greater than 1.2 h Pa were observed (unpublished IFOP data, presented at a FAN workshop). The SAM values reflect variations in winds, which change the behaviour of precipitations and local conditions in the Western Patagonian zone [133,134]. In summer 2021, the flows of large rivers in Patagonia strongly decreased, due to the low rainfall registered during that season. The influence of less fresh water determines changes in environmental conditions such as circulation, stratification, as well as changes in chemical conditions such as oxygenation, nutrient composition, and carbonate concentrations. The decrease in river flows caused less circulation, a weakly stratified water column with higher salinities, greater stability of the water column and therefore, a higher water temperature [40]. The lower circulation in fjords with low or almost zero water exchange could have favoured the algal blooms recorded during the summer of 2021 in Chile, similarly to what occurred during 2016 [45,133]. The three events associated with fish mortalities observed during the summer of 2021 were associated with the presence of Lepidodinium chlorophorum, Heterosigma akashiwo, Leptocylindrus minimus and L. danicus (INTESAL).

In most HABs associated with fish mortality the affected fish present lethargy, superficial swimming, increased opercular frequency, evident respiratory distress, loss of balance and death, the latter being caused by asphyxia with severe gill damage or by the action of haemolytic substances. The massive mortality of fish is, therefore, associated with severe stress and even when the surviving fish present a good productive/sanitary prognosis, prolonged exposures over time can generate a significant deterioration in the gill tissue. This will depend on the harmful microalgae species, its abundance, the number of events and the time of exposure [39,45,96,133].

3.3.1. Harmful Diatom Species

In general, diatoms that have a cell wall made of silica and covered by setae can mechanically damage and irritate the gill membranes, causing a cascade of events that affect the osmoregulatory capacity of fish. Within the diatom species described in Chile that affect fish, Chaetoceros cf. convolutus and genus Leptocylindrus have setae and triangular silica spines, respectively. The contact of the setae and spines with the gills produce a mechanical effect [135], generated vascular alterations, inflammatory conditions, and lamellar hyperplasia[136].

The HABs of Leptocylindrus minimus and L. danicus recorded in salmon farms in the Aysén region during the summer of 2021 generated blood hypoxia due to oxygen depletion in the water, which caused acute physiological stress in the fish (INTESAL). The effects of these species have been recorded previously [133] and exposed fish may show behavioural changes, including increased ventilation rates in response to physiological and osmotic stress [136]. Leptocylindrus is a harmful species to farmed salmon due to two factors: the morphology of the algae and the effects on oxygen depletion. The main effect is mechanical with mucus production, stress and higher susceptibility to pathogens.

Of the total registered events caused by diatoms (n = 122), 13 produced mortalities in salmon with an incidence rate of 10.7%. On the other hand, four events generated mortalities to marine organisms with an incidence rate of 3.3%. In general, despite exceeding the established harmful limits, the events did not necessarily produce direct mortality to the organisms, but they did cause harmful effects that could be associated with economic losses due to decreased growth or secondary infections (Table S4, [30,58,70,73,74,76,95,96,101,106,107,109,110,126,137,138,139,140]).

3.3.2. Dinoflagellates

Alexandrium catenella and Chatonella marina produce similar amounts of superoxide that increase with cell lysis [141,142,143]. Mardones, Dorantes-Aranda, Nichols et al. [142], found that the damage caused by A. catenella in fish under different environmental conditions was highly variable and strongly dependent on the strains involved. In addition, fish damage was correlated with cell abundance and with the number of lysed cells, producing greater gill damage than intact cells. On the other hand, gill cells exposed to paralytic toxin fractions exhibited very a low viability loss (<30%), even at concentrations equivalent to those naturally detected in southern Chile. This suggests that fish gill damage during A. catenella events might not only be explained by the presence of paralytic toxins, but rather by the synergistic interaction between ROS, DHA and potentially other PUFAs [142]. Another factor to be considered in A. catenella blooms is the high densities of resting cysts in the fjords. Mardones et al. [144], describes a short latency of 69 days, playing a relevant role in its abiotic factors such as salinity, irradiance, temperature and nutrients, which may modulate the germination of the cyst and the cell growth rates. Mardones, Müller et al. [144], also mentioned the ability of Chilean strains of A. catenella to adapt to space–time fluctuations of pCO₂/pH in Chilean fjords, which may imply some resistance to climate change.

The dinoflagellate Karlodinium cf. austral causes hemolytic, ichthyotoxic and cytotoxic effects produced by the activity of karlotoxins. Fish affected by these microalgae show shallow swimming, lethargy, increased mucus secretion, and massive mortalities. Histologically, diffuse necrosis of the lamellar epithelium is observed, which can affect the exchange of ions and gases in the gills [136].

In the dinoflagellate Karenia spp., toxicity could be related to haemolytic and cytotoxic mechanisms which are caused by PUFAs and specific toxins. Hyperplasia, hypertrophy, lamellar fusions, and aneurysm have been observed in gills. Multifocal coagulative necrosis occurs in the liver and can sometimes cause enteritis and focal hepatic necrosis [136]. Mardones et al. [119] provided evidence of significant genetic and phenotypic variability among isolates from around the world, indicating the existence of a “species complex” of K. selliformis. In addition, it is mentioned that the massive mortality of fauna during K. selliformis events in Chile cannot be explained by the presence of GYM or brevetoxins, instead, it can be largely attributed to the high production of long-chain PUFAs and/or highly toxic compounds not yet characterized [119].

Recently, the dinoflagellate Lepidodinium spp., and specifically Lepidodinium chlorophorum, generated losses of USD3.5 million in mortalities of salmonids in Chiloé in Los Lagos region, the cause described was a depletion of oxygen in the water column (Table S5) [140].

Of the registered events caused by dinoflagellates (n = 72), eight caused mortalities in salmon with an incidence rate of 11.1%, and six events generated mortalities in other marine organisms with an incidence rate of 8.3%. In general, similar to diatom blooms, regardless of exceeding the established limits of harmfulness, the events do not necessarily produce direct mortality, but they do when combined with other harmful effects. Still, the blooms can be associated with economic losses due to their impact on decreased growth rates or secondary infections (Table S5, [30,41,43,54,70,74,75,95,101,104,107,108,109,110,126,130,132,137,140,145,146]).

3.3.3. Silicoflagellate, Raphidophyceae and Haptophyte

The silicoflagellate Pseudochattonella cf. verruculosa has caused great damage in recent years, having mucocystic structures through which it discharges mucus. However, the ichthyotoxic mechanism of these species has not yet been fully described [17]. For the genus Pseudochattonella, production of ROS and osmotic stress have been described, which could be the main factor for cell lysis. Fish affected by the presence of this microalgae show high mortalities, surface swimming, lethargy, and the presence of petechiae (small red lesions) on the gill surface. Histologically, lamellar telangiectasia can be found, diffuse lamellar thrombosis, necrosis of the lamellar epithelium, and branchial hyperplasia, in addition to multifocal hepatic necrosis. Finally, salmonids are also harmed through hypoxia due to the respiration of the microalgae and the decomposition of the phytoplankton bloom [131].

Recently, another silicoflagellate, Vicicitus globosus, caused the mortality of 150 t of salmonids in Chiloé in Los Lagos region. These microalgae have been mentioned as highly cytotoxic for fish and also to other species of microalgae [135,147].

The raphidophycean Heterosigma akashiwo was one of the first microalgae that affected farmed fish in Chile [148].This species causes oedema and hypertrophy of epithelial cells in salmonids, in addition to an increase in mucus and fusion of filaments. In gills, there is a detachment of the epithelium from the basement membrane and eosinophilic content is observed in histological slides. It has been suggested that free fatty acids (FFA), possibly in a synergistic effect with ROS, may be the main mechanism of toxicity. ROS such as hydroxyl (OH) and superoxide (O⁻) radicals, in addition to hydrogen peroxide (H₂O₂) are formed naturally as by-product of oxygen metabolism, but which, under environmental stress (such as oxygen depletion or the presence of HAB), can increase their levels causing significant damage to cellular structures through oxidative stress. The blooms of H. akashiwo have been characterized by low toxicity, however, the production of fatty acids with cytotoxic characteristics, as well as the potential to produce exopolymers would contribute to the ichthyotoxicity [143]. Similar to P. cf. verruculosa this species forms a mucilage-like structure, causing circulatory disorders due to hypoxic exposure. Some of these molecules can cause respiratory and/or cardiac paralysis and abnormal behaviour, so the influence of mucocysts and the role they play in fish mortality should be studied [17,134]. Recently, Gallardo-Rodríguez et al. [107] observed a constant production of anaesthetic bioactives in cell cultures of H. akashiwo.

H. akashiwo was first detected in the years 1993–1994 in the Los Lagos region, it bloomed with maximum abundances of only 18 cells mL⁻¹, in Hornopirén/Reloncaví/Calbuco in 1993 and Chiloé in 1994. Many years later, in 2021, the events caused by H. akashiwo presented maximum concentrations of 200,000 cells mL⁻¹, causing the mortality of over 6000 t of salmon in the Comau fjord (Table S6). As in A. catenella, the presence of resistance cysts has been demonstrated in H. akashiwo, so the determination and isolation of the cysts is required to identify and monitor the areas prone to being affected by this harmful species [149].

Of the registered events caused by silicoflagellate, raphidophycean and haptophyte (n = 23), 10 caused mortalities in salmon with an incidence rate of 43.4%. Two events generated mortalities to other marine organisms with an incidence rate of 8.7%. Unlike what was observed in diatoms and dinoflagellates blooms, the events associated with these groups were less frequent, but with a much higher incidence on mortality (Table S6, [17,30,71,73,74,76,137,138,140,150]).

4. Conclusions and Perspectives

This review shows that harmful algal blooms in Chile are diverse in species, occurrences, distributions, and impacts. It also requires keeping a close eye, since in addition to the effects on public health and in the ecosystems, these events affect aquaculture and fishing, two of the most relevant socio-economic activities in the country. This requires the continuation of devoting efforts to the understanding and monitoring HABs in Chile. With this revision, we have been able to confirm that, during the last 65 years, HABs have shown an apparent trend of extending the distribution from south to north. We cannot ignore, however, that the identification of events is closely associated with the areas where a large part of the country’s aquaculture is located, and they are under more intense monitoring. Here, we also recognized that there is a strong lack of knowledge about harmful algae in the entire Humboldt Current system and more monitoring is needed in the northern regions of the country such as Atacama and Coquimbo. Moreover, what is currently documented might very likely underestimate the number of blooms that have occurred in fjords and channels, particularly those that caused minor economic impacts for artisanal fishermen and the salmon and mussel farming sector.

Climate change is affecting rainfall, wind regime, temperatures, freshwater flows, melting glaciers, which would generate a different scenario in the estuarine system, which could favour a greater proportion of harmful blooms. The only way to assess this hypothesis is to work on long term time series, to predict future events changes in frequency and intensity in space and time

Finally, the recent appearance of new toxins including spirolides (SPX) [114], gymnodimines (GYMs) [66] and pinnatoxins (PnTXs), pose challenges for the country, both socioeconomically and to avoid human poisoning. The presence of new taxa requires greater concern, where scientific research should be prioritized. Therefore, in our opinion, the following species should be included in the monitoring: Lepidodinium spp., Lepidodinium chlorophorum, Karlodinium australe, Kryptoperidinium triquetrum, Prorocentrum micans and Vicicitus globosus, Azadinium poporum and Vulcanodinium rugosum, either because of the production of new toxins or because they generate mortality in marine organisms.