An Unprecedented Bloom of Oceanic Dinoflagellates (Karenia spp.) Inside a Fjord within a Highly Dynamic Multifrontal Ecosystem in Chilean Patagonia.

At the end of summer 2020, a moderate (~105 cells L-1) bloom of potential fish-killing Karenia spp. was detected in samples from a 24 h study focused on Dinophysis spp. in the outer reaches of the Pitipalena-Añihue Marine Protected Area. Previous Karenia events with devastating effects on caged salmon and the wild fauna of Chilean Patagonia had been restricted to offshore waters, eventually reaching the southern coasts of Chiloé Island through the channel connecting the Chiloé Inland Sea to the Pacific Ocean. This event occurred at the onset of the COVID-19 lockdown when monitoring activities were slackened. A few salmon mortalities were related to other fish-killing species (e.g., Margalefidinium polykrikoides). As in the major Karenia event in 1999, the austral summer of 2020 was characterised by negative anomalies in rainfall and river outflow and a severe drought in March. Karenia spp. appeared to have been advected in a warm (14-15 °C) surface layer of estuarine saline water (S > 21). A lack of daily vertical migration patterns and cells dispersed through the whole water column suggested a declining population. Satellite images confirmed the decline, but gave evidence of dynamic multifrontal patterns of temperature and chl a distribution. A conceptual circulation model is proposed to explain the hypothetical retention of the Karenia bloom by a coastally generated eddy coupled with the semidiurnal tides at the mouth of Pitipalena Fjord. Thermal fronts generated by (topographically induced) upwelling around the Tic Toc Seamount are proposed as hot spots for the accumulation of swimming dinoflagellates in summer in the southern Chiloé Inland Sea. The results here provide helpful information on the environmental conditions and water column structure favouring Karenia occurrence. Thermohaline properties in the surface layer in summer can be used to develop a risk index (positive if the EFW layer is thin or absent).

Small and patchy is enough: An example about how toxic HAB events can spread through low resting cyst loads.

The frequency of harmful algal blooms (HABs) has increased over the last two decades, a phenomenon enhanced by global climate change. However, the effects of climate change will not be distributed equally, and Chile has emerged as one important, vulnerable area. The Chilean Patagonian region (41‒56°S) hosts two marine ecoregions that support robust blue economies via wild fisheries, aquaculture, and tourism. However, the harmful algal bloom-forming dinoflagellate Alexandrium catenella, a causative agent of paralytic shellfish poisoning outbreaks, threatens the viability of blue industries in this region and others worldwide. Despite the proliferation of A. catenella blooms over the last few decades, the role of sedimentary resting cysts in the recurrence of harmful algal blooms and the species' northward expansion across Chilean Patagonia is not well understood. As a resting cyst-producing species, the sediment-cyst dynamics of A. catenella likely contribute to the geographical expansion and bloom recurrence of this species. For this purpose, we analyzed a decade of A. catenella surface sediment cyst records across the two ecoregions of the Chilean Patagonian System that were further stratified into five subregions based on water temperature, salinity, dissolved oxygen, and nutrient characteristics. We also analyzed spatio-temporal cyst dynamics in a pre-, during-, and post-bloom scenario of the Chiloense ecoregion (more northern) of the Magellanic province. Our results indicated highly variable A. catenella resting cyst abundances, with a maximum of 221 cysts cm-3 recorded in 2002 after an intense bloom. Generalized linear mixed models and linear mixed models found that sampling season, subregion, and Total Organic Matter (%) explained resting cyst presence and density. The results also demonstrated the presence of A. catenella cysts in northern subregions, evidencing the northward geographical expansion observed during the last few decades. The risks of A. catenella bloom recurrence from small, patchy resting cyst distributions across broad geographical areas and under changing environmental conditions are discussed.

Dinophysis acuminata or Dinophysis acuta: What Makes the Difference in Highly Stratified Fjords?

Dinophysis acuminata and D. acuta, which follows it seasonally, are the main producers of lipophilic toxins in temperate coastal waters, including Southern Chile. Strains of the two species differ in their toxin profiles and impacts on shellfish resources. D. acuta is considered the major cause of diarrhetic shellfish poisoning (DSP) outbreaks in Southern Chile, but there is uncertainty about the toxicity of D. acuminata, and little information on microscale oceanographic conditions promoting their blooms. During the austral summer of 2020, intensive sampling was carried out in two northern Patagonian fjords, Puyuhuapi (PUY) and Pitipalena (PIT), sharing D. acuminata dominance and D. acuta near detection levels. Dinophysistoxin 1 (DTX 1) and pectenotoxin 2 (PTX 2) were present in all net tow samples but OA was not detected. Although differing in hydrodynamics and sampling dates, D. acuminata shared behavioural traits in the two fjords: cell maxima (>103 cells L-1) in the interface (S ~ 21) between the estuarine freshwater (EFW)) and saline water (ESW) layers; and phased-cell division (µ = 0.3-0.4 d-1) peaking after dawn, and abundance of ciliate prey. Niche analysis (Outlying Mean Index, OMI) of D. acuta with a high marginality and much lower tolerance than D. acuminata indicated an unfavourable physical environment for D. acuta (bloom failure). Comparison of toxin profiles and Dinophysis niches in three contrasting years in PUY-2020 (D. acuminata bloom), 2018 (exceptional bloom of D. acuta), and 2019 (bloom co-occurrence of the two species)-shed light on the vertical gradients which promote each species. The presence of FW (S < 11) and thermal inversion may be used to provide short-term forecasts of no risk of D. acuta blooms and OA occurrence, but D. acuminata associated with DTX 1 pose a risk of DSP events in North Patagonian fjords.

The role of physico-chemical interactions in the seasonality of toxic dinoflagellate cyst assemblages: The case of the NW Patagonian fjords system.

Harmful algal blooms (HABs) are recurrent in the NW Patagonia fjords system and their frequency has increased over the last few decades. Outbreaks of HAB species such as Alexandrium catenella, a causal agent of paralytic shellfish poisoning, and Protoceratium reticulatum, a yessotoxins producer, have raised considerable concern due to their adverse socioeconomic consequences. Monitoring programs have mainly focused on their planktonic stages, but since these species produce benthic resting cysts, the factors influencing cyst distributions are increasingly gaining recognition as potentially important to HAB recurrence in some regions. Still, a holistic understanding of the physico-chemical conditions influencing cyst distribution in this region is lacking, especially as it relates to seasonal changes in drivers of cyst distributions, as the characteristics that favor cyst preservation in the sediment may change through the seasons. In this study, we analyzed the physico-chemical properties of the sediment (temperature, pH, redox potential) and measured the bottom dissolved oxygen levels in a "hotspot" area of southern Chile, sampling during the spring and summer as well as the fall and winter, to determine the role these factors may play as modulators of dinoflagellate cyst distribution, and specifically for the cysts of A. catenella and P. reticulatum. A permutational analysis of variance (PERMANOVA) showed the significant effect of sediment redox conditions in explaining the differences in the cyst assemblages between spring-summer and fall-winter periods (seasonality). In a generalized linear model (GLM), sediment redox potential and pH were associated with the highest abundances of A. catenella resting cysts in the spring-summer, however it was sediment temperature that most explained the distribution of A. catenella in the fall-winter. For P. reticulatum, only spring-summer sediment redox potential and temperature explained the variation in cyst abundances. The implications of environmental (physico-chemical) seasonality for the resting cysts dynamics of both species are discussed.

Interannual variability in mesoscale distribution of Dinophysis acuminata and D. acuta in Northwestern Patagonian fjords.

Dinophysis acuminata and D. acuta, which produce diarrheogenic toxins and pectenotoxins in southern Chile, display site-specific differences in interannual variability (2006 - 2018) in Reloncaví, Pitipalena and Puyuhuapi fjords (41 - 46 °S), Chilean Patagonia. Linear Models show decreasing trends in rainfall and river discharge. Latitudinal decreasing gradients in SST temperature and vertical salinity gradients were observed. A brackish water layer (FW salinity <11 psu), permanently present in Reloncaví, decreased in thickness with time in Pitipalena and was usually absent in Puyuhuapi, the only fjord where D. acuta reached bloom (>103 cells L‒1) densities every season. Dinophysis acuminata, associated with toxin profiles in shellfish that include only pectenotoxins, bloomed everywhere with a poleward increasing gradient. Absence of the FW layer provides a possible index of risk for D. acuta blooms. An apparent poleward shift of D. acuta populations, responsible for DSP outbreaks in Reloncaví in the 1970s, and the recent EU deregulation of pectenotoxins will have a positive impact on the mussel industry in Los Lagos Region. Changes to ongoing monitoring protocols to improve risk assessment capabilities are suggested.

Latitudinal Variation in the Toxicity and Sexual Compatibility of Alexandrium catenella Strains from Southern Chile.

The bloom-forming toxic dinoflagellate Alexandrium catenella was first detected in southern Chile (39.5-55° S) 50 years ago and is responsible for most of the area's cases of paralytic shellfish poisoning (PSP). Given the complex life history of A. catenella, which includes benthic sexual cysts, in this study, we examined the potential link between latitude, toxicity, and sexual compatibility. Nine clones isolated from Chilean Patagonia were used in self- and out-crosses in all possible combinations (n = 45). The effect of latitude on toxicity, reproductive success indexes, and cyst production was also determined. Using the toxin profiles for all strains, consisting of C1, C2, GTX4, GTX1, GTX3, and NeoSTX, a latitudinal gradient was determined for their proportions (%) and content per cell (pg cell-1), with the more toxic strains occurring in the north (-40.6° S). Reproductive success also showed a latitudinal tendency and was lower in the north. None of the self-crosses yielded resting cysts. Rather, the production of resting cysts was highest in pairings of clones separated by distances of 1000-1650 km. Our results contribute to a better understanding of PSP outbreaks in the region and demonstrate the importance of resting cysts in fueling new toxic events. They also provide additional evidence that the introduction of strains from neighboring regions is a cause for concern.

Niche differentiation of Dinophysis acuta and D. acuminata in a stratified fjord.

Dinophysis acuta and D. acuminata are associated with lipophilic toxins in Southern Chile. Blooms of the two species coincided during summer 2019 in a highly stratified fjord system (Puyuhuapi, Chilean Patagonia). High vertical resolution measurements of physical parameters were carried out during 48 h sampling to i) explore physiological status (e.g., division rates, toxin content) and ii) illustrate the fine scale distribution of D. acuta and D. acuminata populations with a focus on water column structure and co-occurring plastid-bearing ciliates. The species-specific resources and regulators defining the realized niches (sensu Hutchinson) of the two species were identified. Differences in vertical distribution, daily vertical migration and in situ division rates (with record values, 0.76 d-1, in D. acuta), in response to the environmental conditions and potential prey availability, revealed their niche differences. The Outlying Mean Index (OMI) analysis showed that the realized niche of D. acuta (cell maximum 7 × 103 cells L-1 within the pycnocline) was characterized by sub-surface estuarine waters (salinity 23 - 25), lower values of turbulence and PAR, and a narrow niche breath. In contrast, the realized niche of D. acuminata (cell maximum 6.8 × 103 cells L-1 just above the pycnocline) was characterized by fresher (salinity 17 - 20) outflowing surface waters, with higher turbulence and light intensity and a wider niche breadth. Results from OMI and PERMANOVA analyses of co-occurring microplanktonic ciliates were compatible with the hypothesis of species such as those from genera Pseudotontonia and Strombidium constituting an alternative ciliate prey to Mesodinium. The D. acuta cell maximum was associated with DSP (OA and DTX-1) toxins and pectenotoxins; that of D. acuminata only with pectenotoxins. Results presented here contribute to a better understanding of the environmental drivers of species-specific blooms of Dinophysis and management of their distinct effects in Southern Chile.