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Article

Are Alexandrium catenella Blooms Spreading Offshore in Southern Chile? An In-Depth Analysis of the First PSP Outbreak in the Oceanic Coast

1
Centro i~mar, Universidad de Los Lagos, Casilla 557, Puerto Montt 5290000, Chile
2
CeBiB, Universidad de Los Lagos, Casilla 557, Puerto Montt 5290000, Chile
3
Programa de Doctorado en Biología y Ecología Aplicada, Universidad Católica del Norte, Coquimbo 1780000, Chile
4
Programa de Investigación Pesquera, Instituto de Acuicultura, Universidad Austral de Chile, Puerto Montt 5489001, Chile
5
Programa Integrativo, Centro Interdisciplinario para la Investigación Acuícola (INCAR), Concepción 4030000, Chile
6
Centro de Estudios del Desarrollo Regional y Políticas Públicas (CEDER), Universidad de Los Lagos, Osorno 5290000, Chile
7
Facultad de Medicina y Ciencia, Universidad San Sebastian, Puerto Montt 5501842, Chile
8
Centro Oceanográfico de Vigo, Instituto Español de Oceanografía (IEO-CSIC), Subida a Radio Faro 50, 36390 Vigo, Spain
9
WorldFish Headquarters, Jalan Batu Maung, Batu Maung, 11960 Bayan Lepas, Penang, Malaysia
10
Department of Integrative Agriculture, College of Agriculture and Veterinary Science, United Arab Emirates University, Abu Dhabi 15551, United Arab Emirates
11
Faculty of Marine Resources and Environment, Tokyo University of Marine Science and Technology, Tokyo 108-8477, Japan
12
SEREMI de Salud Región de Los Lagos, Puerto Montt 5480000, Chile
13
Centro de Estudios de Algas Nocivas (CREAN), Instituto de Fomento Pesquero (IFOP), Padre Harter 574, Puerto Montt 2361827, Chile
14
Facultad de Ciencias del Mar, Departamento de Acuicultura, Universidad Católica del Norte, Coquimbo 1780000, Chile
15
Centro de Investigación y Desarrollo Tecnológico en Algas (CIDTA), Facultad de Ciencias del Mar, Universidad Católica del Norte, Coquimbo 1780000, Chile
16
Center for Ecology and Sustainable Management of Oceanic Islands (ESMOI), Departamento de Biología Marina, Facultad de Ciencias del Mar, Universidad Católica del Norte, Coquimbo 1780000, Chile
17
Centro de Innovación Acuícola AQUAPACIFICO, Coquimbo 1780000, Chile
*
Author to whom correspondence should be addressed.
Fishes 2024, 9(9), 340; https://doi.org/10.3390/fishes9090340
Submission received: 1 August 2024 / Revised: 27 August 2024 / Accepted: 27 August 2024 / Published: 29 August 2024
(This article belongs to the Section Environment and Climate Change)

Abstract

The blooms of Alexandrium catenella, the main producer of paralytic shellfish toxins worldwide, have become the main threat to coastal activities in Southern Chile, such as artisanal fisheries, aquaculture and public health. Here, we explore retrospective data from an intense Paralytic Shellfish Poisoning outbreak in Southern Chile in Summer–Autumn 2016, identifying environmental drivers, spatiotemporal dynamics, and detoxification rates of the main filter-feeder shellfish resources during an intense A. catenella bloom, which led to the greatest socio-economic impacts in that area. Exponential detoxification models evidenced large differences in detoxification dynamics between the three filter-feeder species surf clam (Ensis macha), giant barnacle (Austromegabalanus psittacus), and red sea squirt (Pyura chilensis). Surf clam showed an initial toxicity (9054 µg STX-eq·100 g−1) around 10-fold higher than the other two species. It exhibited a relatively fast detoxification rate and approached the human safety limit of 80 µg STX-eq·100 g−1 towards the end of the 150 days. Ecological implications and future trends are also discussed. Based on the cell density evolution, data previously gathered on the area, and the biology of this species, we propose that the bloom originated in the coastal area, spreading offshore thanks to the resting cysts formed and transported in the water column.
Key Contribution: The first PSP outbreak in the oceanic coast of Southern Chile generated severe socio-economic impacts due to the high toxicities detected in filter-feeder species (~9000 µg STX-eq·100 g−1). Exponential detoxification models evidenced large differences in detoxification dynamics between the three filter-feeder species studied. The spatiotemporal patterns of A. catenella in NW Patagonia showed the origin of the bloom in the Aysén region since spring, and a new outbreak in the SW of Chiloé in April possibly generated by a fast cyst germination.

1. Introduction

Harmful algal blooms (HABs) have become one of the main threats to coastal aquatic activities worldwide, such as aquaculture, fishing, tourism and public and ecosystem health [1]. Recently, Díaz and Álvarez [2], based on the analyses of the IOC database of HAB events (IOC-HAEDAT) of the last 50 years, showed a significant increase in the total number of reports, mainly of paralytic shellfish poisoning (PSP). This exponential increase in PSP toxic events has been associated with the irrefutable contribution of anthropogenic factors such as agricultural runoff and also industrial and domestic waste [3,4].
Alexandrium is one of the most important HAB-producing genera in the world in terms of diversity, distribution and socio-economic and human health impacts [5]. This genus has drawn a lot of attention in recent decades as the main causative agent of PSP all over the world [5]. In southern Chile, HABs of Alexandrium catenella have been a recurrent problem since 1972, when the first episode of this species was recorded in the Magallanes region (56 °S) [6]. In the Aysén region (44 °S), the first records date back to 1992, generating important episodes from 1995 onwards, even reaching the Los Lagos region (43 °S) in 2002 [7] and Los Ríos region (39 °S) in 2016 [8,9]. This remarkable northward progression reached the Los Lagos region, the site where an intense Chilean mussel (Mytilus chilensis) aquaculture and artisanal shellfish fisheries exist [10], causing dramatic socio-economic impacts [11]. In addition, Paredes-Mella et al. [12] detected toxic A. catenella cells in the Bío-Bío region (36 °S), and Rodríguez-Villegas et al. [13], resting cysts of this species in surface sediments from that area, confirmed the northward expansion of this dinoflagellate observed in recent decades. PSP events have varied interannually, alternating years with little or rare occurrence to years with more than 1,000,000 cells L−1 of A. catenella and toxicities greater than 10,000 μg STX-eq·100 g−1 of meat recorded in natural beds [7,14,15]. The concentrations of these paralytic shellfish toxins (PSTs) have even reached record values worldwide, such as in 2018, where toxicities of up to 143,000 μg STX-eq·100 g−1 were recorded in mussels from Aysén region associated with an intense bloom of the same dinoflagellate [11]. These high toxicities (>10,000 μg STX-eq·100 g−1) generate extensive detoxification periods that, in some cases, can last up to two years [14,16].
The Los Lagos region’s economy is highly dependent on hydrobiological resources. More than 7% of the 2024 regional GDP is based on fisheries and aquaculture activities [17]. Most of the fish and shellfish consumed in Chile come from Los Lagos [18]. In addition, both industries provide important sources of direct and indirect employment sources for the regional population [19]. Regarding benthic resources, particularly those that are vulnerable to PSTs, they are exploited mainly by the artisanal fishery sector and the mussel aquaculture sector.
The regional artisanal fishery sector includes 35,870 registered resource fishers (i.e., gleaners, divers and boat skippers, men and women), representing more than 35% of the national sectoral workforce. They dwell in and operate from more than 215 fishing ‘caletas’ (i.e., coves) distributed throughout the region in urban and rural settings. In 2022, molluscs regional landings amounted to nearly 19,000 tons (15% of the national total) including ‘almeja’ (Ameghinomya antiqua), ‘cholga’ (Aulacomya atra), ‘choro’ (Choromytilus chorus), and ‘loco’ (Concholepas concholepas). The region is also the main producer of ‘piure’ (Pyura chilensis), with 1,538 tons landed in 2022 (i.e., 74% of the national produce) [10].
In terms of the aquaculture industry, more than 1,100 concessions are registered for mollusc farming in Los Lagos. The main farmed species is the mussel or ‘chorito’ (Mytilus chilensis), accounting for more than 427,000 tons landed in 2022 [10]. Mussel aquaculture has been a booming industry in Chile in recent decades [20]. The country is among the three main mussel-producing countries, with more than USD 270 million in sales in 2021. Nearly 90% of the national production is exported to 60 countries, including Spain, France, Italy and the USA [21]. The whole mussel production chain in Chile is established in the Los Lagos region, playing a key role in the regional economy. The industry involves more than 620 firms, mostly micro (65%), small (24%) and medium (4%) enterprises, including seed collection, growth centres and processing plants; and employs ca. 12,000 and 5000 direct and indirect people, respectively (4% of regional employment). Mussel processing plants are the most labour-intensive activity and provide jobs mainly for women workers.
The heavy socio-economic dependence of Los Lagos on wild and farmed shellfish resources defines a highly vulnerable context to HAB in general, and to A. catenella in particular. A better understanding of key environmental drivers, spatiotemporal dynamics and detoxification rates is required to inform sanitary and fishery policies and strategies.
Some authors suggest that such inter-annual trends in shellfish toxicity are associated with large-scale climate variability [22,23]. The Patagonian fjords system is subject to multidecadal fluctuations related to large-scale climate cycles, such as the El Niño Southern Oscillation (ENSO), Antarctic Circumpolar Wave (ACW) and Southern Annular Mode (SAM). These cycles affect systems directly through changes in local wind patterns and rainfall and probably through changes in the velocity of glacier melting, one of the main sources of freshwater (and water column stability) in these highly stratified systems. In Chile, Guzmán et al. [15] and Molinet et al. [7] suggested that events such as El Niño and the ACW, respectively, could modulate the variation in A. catenella blooms in Southern Chile. Furthermore, the effects of these large-scale climatic fluctuations over HAB species were highlighted during the summer of 2016, when an exceptional bloom of A. catenella developed in Southern Chile associated with high positive values of ENSO (+2) and SAM (+3 hPa) index that affected the Chilean Patagonia [24]. Until then, the combined effect of the positive phases of ENSO/SAM in southern South America and their environmental impacts had not been documented. Thus, in the summer of 2016, a favourable combination of meteorological and hydrographic processes of multiple scales created conditions that promoted the development of a widespread bloom of A. catenella [23,24].
This paper analysed the spatial–temporal patterns of A. catenella and PSTs, detoxification rates in different filter-feeding shellfish and socioeconomic impacts of the first PSP outbreak recorded in the oceanic coast of southern Chile and their relationship with extreme climate anomalies that occurred in the summer and early autumn of 2016. Finally, we proposed a hypothesis of the origin of the first PSP on the oceanic coast of Southern Chile.

2. Materials and Methods

2.1. Study Area

NW Patagonia, from 41 to 45 °S, is part of one of the most extensive fjord and channel systems in the world (Figure 1). This highly stratified system, due to heavy freshwater inflow from rivers and glacier melting, has a rugged bathymetry and a highly dissected coastline. This area is subject to heavy rainfall, exhibiting very seasonal and latitudinal patterns, with an average of 2700 mm y−1 and up to 5000 mm in exceptional years [25,26]. The presence of numerous islands in this large fjord system contributes to heterogeneity in terms of geomorphology and depth distribution. This region is directly influenced by oceanic waters from the adjacent Pacific Ocean [27,28,29,30] through the Chacao Channel and Corcovado Gulf but is also affected by estuarine inputs [31] and continental waters [32]. Meanwhile, the oceanic coast of southern Chile is characterised by strong oceanic water influence, with salinity >31 despite the freshwater inputs from some rivers (i.e., Rivers Chepu, Cucao and Medina) and other smaller tributaries (Figure 1). Water temperature ranges from 10 to 14 °C [33,34], and the area is subjected to semidiurnal tides with amplitudes ranging from 2 m (neap tides) to 4 m (spring tides) [35].

2.2. IFOP Monitoring Programme

Monthly reports of phytoplankton distribution at 117 sampling stations in the Aysén and Los Lagos regions (NW Patagonia) from January to April 2016 were obtained from the Chilean Monitoring Program at the Instituto de Fomento Pesquero (IFOP). Under the framework of this program, integrated water-column samples for quantitative analyses of phytoplankton are collected with a dividable hose sampler from 0 to 10 and 10 to 20 m [36], a method recommended by the ICES group of experts as the most suitable for monitoring HAB species with patchy distributions [37] and immediately fixed with acidic Lugol’s solution [38]. For quantitative analyses of phytoplankton, 10 mL of the hose-samples were left to sediment overnight and analysed under an inverted microscope (Olympus CKX41) using the method described in Utermöhl [39]. This time ensures that all the cells can settle to the bottom of the chamber. To enumerate large but less abundant species, such as A. catenella, the whole surface (or base) of the chamber was scanned at a magnification of ×100 so that the detection limit was 100 cells L−1.

2.3. Wind and Ekman Transport

The wind component at 10 m in was obtained from the global model ERA5 [40] database (https://cds.climate.copernicus.eu/cdsapp#!/dataset/reanalysis-era5-single-levels; accessed on 10 March 2024) to calculate the Ekman transport with the alongshore wind stress and turbulence as the wind magnitude cubed [41,42,43]. This information was complemented with daily satellite images of sea surface temperature and chlorophyll-a from MODIS Aqua with 4 km resolution (https://oceandata.sci.gsfc.nasa.gov/; accessed on 10 March 2024).

2.4. PST Toxicity Data

Toxicity data (µg STX-eq·100 g−1) in different shellfish species were obtained from the Health Ministry Monitoring Programme available at the website of the regional health centre (https://seremi10.redsalud.gob.cl/resultados-de-monitoreos/; accessed on 5 May 2024). This Chilean programme, established to safeguard the public health of local populations, coordinates activities at regional health centres. Under the framework of this program, PST toxicity (expressed in μg STX-eq·100 g−1) was evaluated by mouse bioassay following the AOAC Official Method 959.08 [44]. Thus, for toxin extraction, 100 g of homogenised raw tissue was mixed with 100 mL of HCl (0.1 N) using a blender and then boiled for 5 min. The sample was cooled at room temperature for 10 min, and the pH was corrected to 2–4. The resulting extract was then transferred to a 200 mL volumetric flask and filled up to the 200 mL mark with HCl (0.003 N). Aliquots (1 mL) of the final extract were intraperitoneally injected into three Swiss mice weighing 19–21 g following the official AOAC method 959.08, and their death times were recorded. If any mouse died in <5 min, the test was performed again using diluted samples until the time until death was 5–7 min. The toxicity was calculated and expressed as μg STX-eq·100 g−1 sample, using Sommer’s Table. Furthermore, detoxification of three different filter-feeder taxonomic groups was evaluated, which were selected considering their frequency of PSP records during 2016: the surf clam (Bivalvia: Mesodesma donacium), the giant barnacle (Crustacea: Austromegabalanus psittacus) and the red sea squirt (Ascidiacea: Pyura chilensis). These samples were collected on the oceanic coast of Chiloé island (M. donacium) and the north of Chiloé Island (Figure 1).

2.5. Modelling

Following Díaz et al. [14], we considered four alternative exponential decay models, defined by a maximum PST value at day 0 (PSTmax), an overall decay rate (k) and the presence or absence of two additional parameters: (i) a baseline toxin level (PSTbl), which represents the non-zero post bloom toxin level, and (ii) a power time exponent (m) that allows for a decreasing detoxification rate over time,
P S T t = P S T m a x · e k · t
P S T t = P S T m a x · e k 1 · t m
P S T t = P S T b l + P S T m a x P S T b l · e k · t
P S T t = P S T b l + P S T m a x P S T b l · e k · t m
All four parameters were estimated for each species using least-square non-linear models [45], assuming normal distribution and multiplicative errors. Data support for each model was assessed and compared within species by the second-order Akaike information criterion and its corresponding relative weight [46].
All analyses and graphic representations were performed using the statistical and programming software R 3.5.1 [47], packages “car”, “ggplot2”, “nlme”, “lme4” and “cluster”, available through the CRAN repository (www.r-project.org/; accessed on 1 March 2024).

3. Results

3.1. Alexandrium catenella Bloom Evolution

Data from the Chilean Monitoring Programme (IFOP) collected with an integrated hose-sampler in the Aysén and Los Lagos regions (117 stations) showed that A. catenella populations, with cell densities ranging from 100 to 500 cells L−1, were first detected in October 2015 (mid-spring) in the Aysén region at stations located in the Moraleda channel and Puyuhuapi Fjord (Figure 2A).
Between November and December (late spring), the presence was restricted to the Aysén region with cell densities ranging from 100 to 3500 cells L−1 (Figure 2B–C). A relevant increase in A. catenella cell densities was observed in January 2016 (early summer), in particular in Jacaf Channel and the head of Puyuhuapi Fjord, with a cell maximum of 92,500 cells L−1 (Figure 2D). During this month, A. catenella cells were recorded for the first time at stations located in the south of the island of Chiloe with a maximum of 400 cells L−1 (Figure 2D). In February, cell densities remained high in the Aysen region, with maximums of 68,700 cells L−1 at the confluence of the Jacaf and Moraleda channels (Figure 2E). Meanwhile, in the Los Lagos region, they increased to maximum densities of 4,900 cells L−1 at the mouth of the Guafo. Furthermore, the presence of this dinoflagellate was detected further north through the inland sea of Chiloe, reaching estuary Compu (Figure 2E).
March showed the bloom decrease in all stations of both regions, with a maximum of 12,500 cells L−1 on the islands most exposed to the Pacific Ocean in the Aysén region. In the Los Lagos Region, cell densities did not exceed 400 cells L−1, but did reach the Deserterores islands area in the middle of the Chiloe inland sea (Figure 2F). In April (early autumn), the population decline continued in the Aysén region and the maximum numbers did not exceed 1600 cells L−1. However, in the Los Lagos region and specifically the stations located in the SW of Chiloé Island, a significant increase was detected, reaching densities of 8000 cells L−1 (Figure 2F). May showed the presence of cells mainly in Aysen with a maximum of 2400 cells L−1 (Figure 2G), before the population dispersion in June and July.

3.2. Meteorological and Oceanographic Conditions

The monthly average of the satellite images showed that in February, the sea surface temperature (SST) in the north section of the inner sea exhibited higher values (18–20 °C), specifically in Reloncaví Sound and the Gulf of Ancud, together with a large part of the adjacent ocean. In contrast, the Gulf of Corcovado showed SST values close to 14 °C (Figure 3A). At the same time, higher chlorophyll-a concentrations (30–50 µg L−1) were detected in the Reloncaví Sound, the Gulf of Ancud and the Gulf of Corcovado and along an intense patch on the oceanic coast extending from the south of the island of Chiloé to the north of the Chacao channel (Figure 3E).
The winds at 10 m in the oceanic part were from the SW with an Ekman transport to the NW, while in the Gulf of Corcovado, the winds were from the west, withdrawing their intensity as flow to the inner sea, where the winds were much less intense with variable directions. March showed colder SST compared to February (Figure 3B). In the oceanic area, the winds were from the south and the transport of Ekman to the west with greater intensity. In the inner sea and the Gulf of Corcovado, the wind was less intense, as were the concentrations of chlorophyll-a (Figure 3F). However, high values of chlorophyll-a were detected in the oceanic coast of Chiloé and the north section of the inner sea (the Reloncavi Sound and the Gulf of Ancud). In April and May, the SST continued to descend (Figure 3C,D), and the wind rotated to E and reduced the Ekman transport. High concentrations of chlorophyll-a only remained in the area of Reloncaví Sound and Gulf of Ancud (Figure 3H).

3.3. Evolution of PSP Outbreak

The monthly evolution of PST concentrations in clams A. atiqua on the south coast of Chiloé Island showed significant increases towards the end of summer and early autumn 2016. January showed all stations on the south coast of Chiloé with non-detectable levels of PST (<30 µg STX-eq·100 g−1 meat) in clams, except for Isla Dolores, where a concentration of 34 µg STX-eq·100 g−1 was recorded on 23 January 2016 (Figure 4A). In February, PSP concentrations did not show a significant increase compared to January. However, detectable concentrations below the permissible level for human consumption (range 33–53 µg STX-eq·100 g−1 of meat) were recorded in seven sectors of the southeast coast of Chiloé (Figure 4B). Nevertheless, the beginning of March showed a significant increase in the PST in A. atiqua clams in all stations in this area, reaching a maximum of 657 µg STX-eq·100 g−1 of meat on the SE coast of Chiloé on 8 March 2016 (Figure 4C). In April, PST concentrations decreased in most of the stations located on the SE coast of Chiloé, while they remained high on the SW coast, mainly in the area of Guapiquilan islands, where a maximum concentration of 840 µg STX-eq·100 g−1 of meat was recorded on 25 April 2016 (Figure 4D).
The main areas affected during the PSP outbreak were Guapiquilán, Cucao and Carelmapu, where PST concentrations exceeded the permissible level for human consumption by one or two orders of magnitude (Figure 5). The PST concentrations in bivalves increased significantly between 20 and 25 April (max. 6614 µg STX-eq·100 g−1 of meat; Figure 5A) and 26 and 30 April 2016 (max. 9193 µg STX-eq·100 g−1 meat; Figure 5B). Thus, the highest PST concentrations were recorded in mussels (10,214 µg STX eq/100 g−1), surf clams (9059 µg STX eq/100 g−1), and ribbed mussels (7534 µg STX eq/100 g−1). Furthermore, high PST concentrations were detected in the giant barnacle Austromegabalanus psittacus (935 µg STX eq/100 g−1) and the red sea squirt Pyura chilensis (889 µg STX eq/100 g−1). In addition, a maximum PST concentration of 1185 µg STX eq/100 g−1 was detected in the Chilean abalone Concholepas concholepas (Figure 6).

3.4. Detoxification Rates

Large differences in detoxification dynamics were found between the three species scrutinised here. Most informative detoxification models for all three species corresponded to exponential decays to a baseline (Table 1). Constant instantaneous decay models (Equation (3)) were selected for the surf clam (AICw = 0.92) and red sea quirt (AICw = 0.69), while a time-dependant instantaneous decay (Equation (4)) showed much better data support than model 3 for the giant barnacle.
Surf clam showed an initial toxicity (PSTmax) around 10-fold higher than the other two species (Figure 7; Table 2). Nonetheless, this species also exhibited a relatively fast detoxification rate and approached the human safety limit of 80 μg STX-eq·100 g−1 towards the end of the 150-day observation period (Figure 7). Giant barnacles, on the other hand, exhibited the lowest initial toxicity and the fastest return to levels below the human safety threshold (Figure 7).

4. Discussion

4.1. Local Environmental Drivers

The formation, maintenance and dissipation of HAB populations in fjords and coastal embayments is subject to processes of multiple (macro-, meso-, micro-) scale processes [48]. Thus, the Patagonian Fjords are subject to multidecadal fluctuations related to large-scale climate cycles, such as the El Niño Southern Oscillation (ENSO), the Antarctic Circumpolar Wave (ACW) and Southern Annular Mode (SAM). These cycles affect systems directly through changes in local wind patterns, rainfall, and probably through changes in the velocity of glacier melting, one of the main sources of freshwater (and water column stability) in these highly stratified systems. The effects of these large-scale climatic fluctuations over HAB species were highlighted during the summer of 2016 when an exceptional bloom of A. catenella developed in Southern Chile associated with a high positive (+1.1 hPa) Southern Annular Mode (SAM) index that affected the northern half of Chilean Patagonia [24]. Thus, as indicated by Garreaud [24] and León-Muñoz et al. [49], the worse ever recorded HAB during 2016 in Western Patagonia could be favoured by the drought, and the unusual southernly winds offshore occurred in this Austral area. The drought substantially reduced the freshwater input and weakened the vertical stratification in the inner waters of Patagonia, thus increasing the upward intrusion of saline, nutrient-rich waters into the surface layer, while southerly winds contributed to more frequent upwelling of nutrient-rich, oceanic water masses. Under these altered hydro-biological conditions, the heightened solar radiation reaching the surface provided optimal conditions for the algal bloom. These climatic effects of different scales are coupled with local modulators of anthropogenic origin such as runoff and organic nutrient loading. These types of factors have been suggested as triggers for high-biomass HAB (HB-HAB) in the Patagonian fjord system [50,51], but have not been investigated in A. catenella.
What makes this event particularly important is that it became the first PSP bloom event in the oceanic zone of Southern Chile, leading to relevant economic consequences that forced the development of new monitoring and management measurements (discussed further below). Before, even if PSP blooms were confirmed to be spreading northwards in Chile, reaching latitudes where they never were reported before [12], they were restricted to the inner sea. What explains this blooming pattern change? Is this an isolated case, or could it be a more prevalent pattern in the future? This geographical area has been well-studied and monitored regarding A. catenella blooms, focusing this research on the environmental conditions triggering its formation and on the role of resting cyst deposits as a factor explaining bloom recurrence. The conclusions were clear and coincident in three key aspects: (i) there is no potential for the formation of large resting cyst beds in this area, and depletion of resting cysts from sediments is fast (<3 months), (ii) implying both a short physiologically determined dormancy period (69 days according to [52]), and (iii) environmental conditions allowing fast germination after dormancy is completed, with no evidence for high residence times of cysts in sediments that could explain the recurrence of bloom events that are distant in time [53]. On the other hand, resting cysts could be key to explaining the geographical spread pattern observed in Chile, as the transport and viable germination of low resting cyst loads could facilitate the dissemination of viable cells [54]. Interestingly, local circulation patterns and sediment characteristics seem to favour short-term deposits of resting cysts in some of the more oceanic and exposed areas [55,56]. Resting cysts have been reported to reach even very deep oceanic areas in Southern Chile, where conditions are inappropriate for germination and cell survival [56]. However, the forces of upwelling and the hydrodynamic conditions originated by the topography/bathymetry of the area could enable the resuspension and viable germination of cysts, which supported us to previously hypothesise that oceanic areas could become cyst reservoirs with the potential for seeding coastal blooms [56]. However, even if this possibility remains feasible, the cell density progression recorded in this specific bloom event (Figure 2) suggests the inverted pattern, i.e., that the bloom was initiated in the inner coastal area from which it spread—probably via the transport of vegetative cells and resting cysts—to the oceanic side. The apparent decline in the northern part of the Aysén region, during March, may reflect the impoverishment of environmental conditions for A. catenella population growth on the inner coast. However, its spread along the exposed coast may have been favoured by a combination of multi-scale meteorological and hydrographic processes. The dominance and intensity of the southerly wind during March and April would have promoted the transport of the bloom to the west coast of Chiloé and, subsequently, to more northerly localities. Once on this coast, the coastal upwelling conditions that prevailed in March 2016 (Figure 3) would have contributed to its intensification. Otherwise, even if the apparent population decline was effective, the time gap between cell density peaks in coastal and oceanic sites (less than three months, Figure 2) is coincident with the germination period of A. catenella cysts reported above. However, if A. catenella bloom declination in March occurred through sexual reproduction, i.e., differentiation into gametes by depaupering condition [57] and planozygote formation, new different nutritional circumstances could alter the trajectory to encystment and promote zygote division [58], amplifying the outcome of sexuality and restoring the vegetative cells.

4.2. Accumulation-Detoxification Patterns

The concentration of toxins recorded in different species has been associated with the habitat they occupy [16], their trophic position [59,60] and spatial variability [14]. All three species analysed in this work are active filter feeders [61], so the most probably route of accumulation of toxins could have been through the ingestion of A. catenella. The accumulation patterns of PST seem to be associated with the relative abundance of A. catenella where samples were collected (north of the Chiloé island for giant barnacles and red sea squirts) (Figure 2 and Figure 5), although data of A. catenella were not available where surf clam samples were collected. Also, the size of particles filtered by each species [61] must be considered in future studies, because it could explain differences in the accumulated concentrations between species. Ben-Gigirey et al. [62] reported a low record of PST in edible Ascideaceae after a bloom of Alexandrium minutum in the Ría de Vigo (NW Spain), which is in line with what was described by Roje-Busatt and Ujević [63] in the Adriatic Sea.
Molinet et al. [16] and Díaz et al. [14] described that natural detoxification processes in bivalves appeared to be mainly related to the elapsed time (after the bloom) and maximum PST concentration acquired by the shellfish, although effects from zone, temperature and salinity indicated likely environmental effects upon metabolic, ventilation or ingestion rates. Natural detoxification in surf clam followed a strong exponential decay curve, similar in shape to those observed in other species [14,16,64,65,66]. Also, the red sea squirt and the giant barnacle showed the same detoxification pattern, although starting from lower values.
Coinciding with the proposals by Díaz et al. [14], the mathematical model of detoxification presented for three different taxa in this work can be used to develop predictors of the safety of fishing grounds and, thus, improve their management, considering that all of them represent important incomes for artisanal fishers.

4.3. Socio-Economics Impacts

The profound regional embeddedness of shellfish production makes it difficult to estimate the real impact of the 2016 PST outbreak in Los Lagos. However, several studies have outlined major social, economic and political consequences [67]. Social impacts include mental health disorders [68] and the detriment of labour and economic wellbeing perceptions [69].
Economic impacts, which also include the January and February massive fish kills produced by Pseudochattonella verruculosa [11,70], represented an unprecedented shock for the region with an estimated total loss of 43,04 thousand tons in exported products [71]. In response to the economic crisis, the Chilean government implemented a subsidy program for the unemployed and their families in the affected areas [18].
The political consequences of the so-called “Chilotean May” included the raising of a social movement reacting against the state and private salmon aquaculture industry sector [72,73]. There was a crisis and controversy about the causes and drivers of the outbreak that challenged scientific knowledge and politicised the contested discourses. Social media coverage played a key role during the upheaval [74,75], which was based on the assumed State’s culpability and the pollution of coastal ecosystems by the salmon industry [67]. In addition, the crisis uncovered longstanding demands from the Chiloé island that had been neglected by the state [76].
The multidimensional and interconnected impacts outlined above highlight the risks and threats derived from the great regional dependency on seafood production and healthy ocean conditions [77]. The increased reliance on marine resources suggests the need for further development of both PSP-outbreak impacts evaluations and diverse adaptation and mitigation policies and management measures in fisheries and aquaculture [78].
This study sheds light on the drivers, dynamics and detoxification rates of the major 2016 PST bloom in the Chilean Patagonia. It also discusses the multiple and profound social, economic and political impacts of the event at the regional level, highlighting the importance of permanent monitoring and a deeper understanding of HAB as complex social–ecological perturbations. As the Chilean case has shown, the lack of socially validated and opportune scientific assessments—among other factors—led to sharp contention and challenges between different discourses regarding the causes of the bloom. The general conflictive social environment and the lack of trust among stakeholder groups has likely amplified some of the most negative impacts of the event. The development of reliable science-based knowledge about PST and other toxins can play a key role in responding, mitigating and adapting to HAB in Chile and elsewhere.

4.4. Future Perspectives and A. catenella Northward Expansion

The sexual life cycle of A. catenella includes a dormant benthic stage (resting cyst). Resting cysts play an important role in bloom initiation, termination and dispersal [57]. Local hydrographic and environmental factors greatly affect the strength and timing of sexual induction and, therefore, the success of encystment and germination, while hydrodynamic processes and sediment characteristics determine the location of cyst deposits [53,79,80]. Big cyst deposits (so-called cysts beds) are known to seed recurrent Alexandrium catenella blooms in some coastal systems [81], and indeed, cyst density and distribution are considered important metrics for predicting A. catenella bloom occurrence [82]. However, even rare, patchy and short-term resting cyst deposits can work as an effective strategy for species dispersal, and this seems to be how A. catenella is successfully spreading northwards in Chile [54]. This spreading mechanism works provided that appropriate environmental conditions for germination and cell growth are met, and it appears that climate change may be involved in fostering this geographical spreading pattern. Additionally, in the present study, we posit that living cysts were transported offshore and became the inoculum for the first bloom in the ocean coast of Southern Chile. Supporting our hypothesis, it was previously proved that A. catenella resting cysts are already formed in the water column, reaching maximum cyst numbers in there one month after the planktonic peak [53]. This life cycle strategy allows for a fast and effective cyst transport before the cysts reach the sediments. Additionally, the short physiological dormancy period of the species fits well with the time gap between the maximum cell density peaks observed in inshore and offshore areas, considering both the formation and mandatory dormancy periods. Given that offshore areas have high potential for resting cyst preservation in the sediments, but also for cyst resuspension and germination [56], we believe that offshore A. catenella blooms could become more frequent in the future and, therefore, that local monitoring and forecasting programs should include them as target areas.

5. Conclusions

Coastal regions around the world are recurrently threatened by harmful algal blooms. Historical records on each location allowed specific monitoring programs to be designed that target the identification of the most relevant local blooming species within important socio-economic geographical areas. However, blooming patterns can change, accelerated by human-induced factors, which could foster species dispersal and, therefore, novel blooming scenarios. Even though local conditions are crucial for understanding each of these episodes, the areas of the world where changes and impacts are the highest can give us extraordinarily scientific insights into how global tendencies, in relation to harmful algal blooms and climate change, may work. Southern Chile is one example of these significant modifications in blooming patterns. For example, PSP blooms are already known to be spreading northwards. Additionally, the present work shows that PSP blooms are also spreading out of the inner coastal areas and posits that the mechanism underlying both expansions could be the same, based on the formation of resting cysts in the water column, which are transported out of the traditional blooming areas, where they germinate quickly. Our work also investigates the impact on the local shellfish industry of the first PSP toxic outbreak in the oceanic coast of Southern Chile through the analysis of the detoxification rates of three local filter-feeding species. Showing relatively fast detoxification rates, the presented data also offer relevant information for forecasting and accurately assessing the economic impact of future PSP bloom events in the area.

Author Contributions

Conceptualisation, P.A.D., C.M., M.S., M.D., D.V., R.I.F. and C.H.; methodology, P.A.D., C.M., M.S., M.D., C.H., P.C. and G.Á.; software, P.A.D., S.A.R., E.J.N., M.D. and B.C.; validation, C.M., E.J.N., D.V., R.I.F., L.B. and G.Á.; formal analysis, P.A.D., S.A.R., C.M., E.J.N., A.M. and G.Á.; investigation, P.A.D., S.A.R., C.M., E.J.N., A.M., M.S., D.V., R.I.F., L.B. and G.Á.; resources, P.A.D., C.H. and R.I.F.; data curation, P.A.D., C.H. and P.C.; writing—original draft preparation, P.A.D., S.A.R., C.M., E.J.N., A.M., D.V., R.I.F., L.B. and G.Á.; writing—review and editing, P.A.D., S.A.R., C.M., E.J.N., A.M., M.S., M.D., D.V., R.I.F., L.B., C.H., P.C., B.C. and G.Á.; visualisation, P.A.D., S.A.R., E.J.N. and B.C.; supervision, C.M., E.J.N., R.I.F. and G.Á.; project administration, P.A.D. and C.H.; funding acquisition, C.H. and R.I.F. All authors have read and agreed to the published version of the manuscript.

Funding

Patricio A. Díaz was funded by the ANID-FONDECYT 1231220 and by the Centre for Biotechnology and Bioengineering (CeBiB) (PIA project FB0001, ANID, Chile), both from the Chilean National Agency for Research and Development (ANID). Carlos Molinet was partially funded by FONDAP Project No 1522A0004 (INCAR). Rosa I. Figueroa was funded by a grant for Galician Networks of Excellence (GPC-VGOHAB (IN607B 2023/11)) from the Innovation Agency of the Xunta de Galicia (GAIN) and BIOTOX (PID2021-125643OB-C22), AEI, Spanish Ministry of Science, Innovation and Universities.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The original contributions presented in this study are included in the article; further inquiries can be directed to the corresponding authors.

Acknowledgments

We thank the Red Tide Laboratory from the Chilean Heath Minister for reports on PST toxicity levels. This contribution to SCOR WG #165 MixONET was supported by grant OCE-214035 from the National Science Foundation to the Scientific Committee on Oceanic Research (SCOR) and contributions from SCOR National Committees.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Map of the study area showing the geographic extension of the shellfish harvesting closures (dashed area) during the 2016 PSP outbreak.
Figure 1. Map of the study area showing the geographic extension of the shellfish harvesting closures (dashed area) during the 2016 PSP outbreak.
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Figure 2. Spatial and temporal distributions of Alexandrium catenella cell density (cells L−1) recorded in a monthly monitoring program carried out by IFOP in the NW Patagonia from October 2015 to May 2016.
Figure 2. Spatial and temporal distributions of Alexandrium catenella cell density (cells L−1) recorded in a monthly monitoring program carried out by IFOP in the NW Patagonia from October 2015 to May 2016.
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Figure 3. Modis Aqua satellite images show the monthly average of the sea’s surface temperature (AD) and chlorophyll-a (EH) from February to May 2016.
Figure 3. Modis Aqua satellite images show the monthly average of the sea’s surface temperature (AD) and chlorophyll-a (EH) from February to May 2016.
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Figure 4. Monthly evolution of PST concentration (µg STX-eq·100 g−1 of meat) recorded in clams (Ameghinomya antiqua) from January to April 2016 in the southern area of Chiloé Island. ND: not detected.
Figure 4. Monthly evolution of PST concentration (µg STX-eq·100 g−1 of meat) recorded in clams (Ameghinomya antiqua) from January to April 2016 in the southern area of Chiloé Island. ND: not detected.
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Figure 5. Spatial distribution of PST concentration (µg STX-eq·100 g−1 of meat) recorded in filter-feeder species on (A): 20–25 April 2016 and (B) 26–30 April 2016, sampling stations located in the inner and oceanic coast of Chiloé Island. ND: not detected.
Figure 5. Spatial distribution of PST concentration (µg STX-eq·100 g−1 of meat) recorded in filter-feeder species on (A): 20–25 April 2016 and (B) 26–30 April 2016, sampling stations located in the inner and oceanic coast of Chiloé Island. ND: not detected.
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Figure 6. Maximum PST concentration (µg STX-eq·100 g−1 of meat) recorded in 20 shellfish species (bivalves, gastropods and other filter-feeder species) recorded during the first PSP outbreak on the oceanic coast of Chiloé in April 2016. The green line represents the regulatory limit (80 μg STX-eq·100 g−1). ND: not detected.
Figure 6. Maximum PST concentration (µg STX-eq·100 g−1 of meat) recorded in 20 shellfish species (bivalves, gastropods and other filter-feeder species) recorded during the first PSP outbreak on the oceanic coast of Chiloé in April 2016. The green line represents the regulatory limit (80 μg STX-eq·100 g−1). ND: not detected.
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Figure 7. Monthly evolution of PST concentration (µg STX-eq·100 g−1 of meat) recorded in clams (Ameghinomya antiqua) from January to April 2016 in the southern area of Chiloé Island. ND: not detected.
Figure 7. Monthly evolution of PST concentration (µg STX-eq·100 g−1 of meat) recorded in clams (Ameghinomya antiqua) from January to April 2016 in the southern area of Chiloé Island. ND: not detected.
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Table 1. Detoxification model comparisons for surf clam (Ensis macha), giant barnacle (Austromegabalanus psittacus) and red sea squirt (Pyura chilensis). The null model corresponds to a reference constant toxicity model. Equations 1 to 4 correspond to exponential decay models as detailed in materials and methods. AICc = second-order Akaike’s Information Criterion (Burnjam and Anderson, 2002); ΔAICc = difference in AICc relative to the most informative model; AICcw = Akaike weight, which represents the probability of each model to be the most suitable one among all models being compared. Most informative models are in bold.
Table 1. Detoxification model comparisons for surf clam (Ensis macha), giant barnacle (Austromegabalanus psittacus) and red sea squirt (Pyura chilensis). The null model corresponds to a reference constant toxicity model. Equations 1 to 4 correspond to exponential decay models as detailed in materials and methods. AICc = second-order Akaike’s Information Criterion (Burnjam and Anderson, 2002); ΔAICc = difference in AICc relative to the most informative model; AICcw = Akaike weight, which represents the probability of each model to be the most suitable one among all models being compared. Most informative models are in bold.
ModelΔAICcAICcw
Surf ClamGiant BarnacleRed Sea SquirtSurf ClamGiant BarnacleRed Sea Squirt
Null252.444.7683.73000
Equation (1)13.228.8413.630.0010.0110.001
Equation (2)4.375.613.690.0670.0560.109
Equation (3)08.7200.5930.0120.691
Equation (4)1.1202.490.3390.9210.199
Table 2. Detoxification model parameters estimated for surf clam (Ensis macha), giant barnacle (Austromegabalanus psittacus) and red sea squirt (Pyura chilensis). Values in parentheses represent standard errors. All models fit using a non-linear squares procedure. All equations correspond to exponential decay models described in the materials and methods.
Table 2. Detoxification model parameters estimated for surf clam (Ensis macha), giant barnacle (Austromegabalanus psittacus) and red sea squirt (Pyura chilensis). Values in parentheses represent standard errors. All models fit using a non-linear squares procedure. All equations correspond to exponential decay models described in the materials and methods.
SpeciesBest
Model
Maximum
PST
(PSTmax)
Baseline
PST
(PSTbl)
Instantaneous Decay Rate
(k)
Power Time Dependence Parameter
(m)
Surf clamEquation (3)7784 (170)195 (47)−0.07 (0.055)n.a.
Giant barnacleEquation (4)602 (72)50 (17)−4.7·10−6 (3.15·10−5)3.7 (2.12)
Red sea squirtEquation (3)813 (53)57 (13)−0.05n.a.
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Díaz, P.A.; Rosales, S.A.; Molinet, C.; Niklitschek, E.J.; Marín, A.; Varela, D.; Seguel, M.; Díaz, M.; Figueroa, R.I.; Basti, L.; et al. Are Alexandrium catenella Blooms Spreading Offshore in Southern Chile? An In-Depth Analysis of the First PSP Outbreak in the Oceanic Coast. Fishes 2024, 9, 340. https://doi.org/10.3390/fishes9090340

AMA Style

Díaz PA, Rosales SA, Molinet C, Niklitschek EJ, Marín A, Varela D, Seguel M, Díaz M, Figueroa RI, Basti L, et al. Are Alexandrium catenella Blooms Spreading Offshore in Southern Chile? An In-Depth Analysis of the First PSP Outbreak in the Oceanic Coast. Fishes. 2024; 9(9):340. https://doi.org/10.3390/fishes9090340

Chicago/Turabian Style

Díaz, Patricio A., Sergio A. Rosales, Carlos Molinet, Edwin J. Niklitschek, Andrés Marín, Daniel Varela, Miriam Seguel, Manuel Díaz, Rosa I. Figueroa, Leila Basti, and et al. 2024. "Are Alexandrium catenella Blooms Spreading Offshore in Southern Chile? An In-Depth Analysis of the First PSP Outbreak in the Oceanic Coast" Fishes 9, no. 9: 340. https://doi.org/10.3390/fishes9090340

APA Style

Díaz, P. A., Rosales, S. A., Molinet, C., Niklitschek, E. J., Marín, A., Varela, D., Seguel, M., Díaz, M., Figueroa, R. I., Basti, L., Hernández, C., Carbonell, P., Cantarero, B., & Álvarez, G. (2024). Are Alexandrium catenella Blooms Spreading Offshore in Southern Chile? An In-Depth Analysis of the First PSP Outbreak in the Oceanic Coast. Fishes, 9(9), 340. https://doi.org/10.3390/fishes9090340

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