The impact of local and climate change drivers on the formation, dynamics, and potential recurrence of a massive fish-killing microalgal bloom in Patagonian fjord.

Harmful algal blooms (HABs) in southern Chile are a serious threat to public health, tourism, artisanal fisheries, and aquaculture in this region. Ichthyotoxic HAB species have recently become a major annual threat to the Chilean salmon farming industry, due to their severe economic impacts. In early austral autumn 2021, an intense bloom of the raphidophyte Heterosigma akashiwo was detected in Comau Fjord, Chilean Patagonia, resulting in a high mortality of farmed salmon (nearly 6000 tons of biomass) within 15 days. H. akashiwo cells were first detected at the head of the fjord on March 16, 2021 (up to 478 cells mL-1). On March 31, the cell density at the surface had reached a maximum of 2 × 105 cells mL-1, with intense brown spots visible on the water surface. Strong and persistent high-pressure anomalies over the southern tip of South America, consistent with the positive phase of the Southern Annular Mode (SAM), resulted in extremely dry conditions, high solar radiation, and strong southerly winds. A coupling of these features with the high water retention times inside the fjord can explain the spatial-temporal dynamics of this bloom event. Other factors, such as the internal local physical uplift process (favored by the north-to-south orientation of the fjord), salt-fingering events, and the uplift of subantarctic deep-water renewal, likely resulted in the injection of nutrients into the euphotic layer, which in turn could have promoted cell growth and thus high microalgal cell densities, such as reached by the bloom.

Oceanography time series reveals annual asynchrony input between oceanic and estuarine waters in Patagonian fjords.

The postglacial Patagonian fjord system along the west coast of southern South America is one of the largest stretches of the southern hemisphere (SH) fjord belt, influenced by the SH westerly wind belt and continental freshwater input. This study reports a 3-year monthly time series (2017-2020) of physical and biogeochemical parameters obtained from the Reloncaví Marine Observatory (OMARE, Spanish acronym) at the northernmost embayment and fjord system of Patagonia. The main objective of this work was to understand the land-atmosphere-ocean interactions and to identify the mechanisms that modulate the density of phytoplankton. A key finding of this study was the seasonally varying asynchronous input of oceanic and estuarine water. Surface lower salinity and warmer estuarine water arrived in late winter to summer, contributing to water column stability, followed by subsurface higher salinity and less warmer oceanic water during fall-winter. In late winter 2019, an interannual change above the picnocline due to the record-high polarity of the Indian Ocean Dipole inhibited water column stability. The biogeochemical parameters (NO3-, NO2-, PO43-, Si(OH)4, pH, and dissolved oxygen) responded to the surface annual salinity variations, and oceanic water mass contributed greatly to the subsurface inorganic nutrient input. The water column N/P ratio indicated that no eutrophication occurred, even under intense aquaculture activity, likely because of the high ventilation dynamics of the Reloncaví Sound. Finally, a shift in phytoplankton composition, characterized by surface chlorophyll-a maxima in late winter and deepening of spring-summer blooms related to the physicochemical conditions of the water column, was observed. Our results support the ecosystem services provided by local oceanography processes in the north Patagonian fjords. Here, the anthropogenic impact caused by economic activities could be, in part, chemically reduced by the annual ventilation cycle mediated by the exchange of oceanic water masses into Patagonian fjords.

Multiscale physical background to an exceptional harmful algal bloom of Dinophysis acuta in a fjord system.

Dinophysis acuta produces diarrhetic shellfish poisoning (DSP) toxins and pectenotoxins (PTX). It blooms in thermally-stratified shelf waters in late summer in temperate to cold temperate latitudes. Despite its major contribution to shellfish harvesting bans, little effort has been devoted to study its population dynamics in Chilean Patagonia. In 2017-2018, mesoscale distribution of harmful algal species (75 monitoring stations) revealed the initiation (late spring) and seasonal growth of a dense D. acuta population in the Aysén region, with maximal values at Puyuhuapi Fjord (PF). Vertical phytoplankton distribution and fine-resolution measurements of physical parameters along a 25-km transect in February 16th identified a 15-km (horizontal extension) subsurface thin layer of D. acuta from 4 to 8 m depth. This layer, disrupted at the confluence of PF with the Magdalena Sound, peaked at the top of the pycnocline (6 m, 15.9 °C, 23.4 psu) where static stability was maximal. By February 22nd, it deepened (8 m, 15.5 °C; 23.62 psu) following the excursions of the pycnocline and reached the highest density ever recorded (664 × 103 cells L-1) for this species. Dinophysis acuta was the dominant Dinophysis species in all microplankton net-tows/bottle samples; they all contained DSP toxins (OA, DTX-1) and PTX-2. Modeled flushing rates showed that Puyuhuapi, the only fjord in the area with 2 connections with the open sea, had the highest water residence time. Long term climate variability in the Southern hemisphere showed the effects of a Southern Annular Mode (SAM) in positive mode (+1.1 hPa) overwhelming a moderate La Niña. These effects included positive spring precipitation anomalies with enhanced salinity gradients and summer drought with positive anomalies in air (+1 °C) and sea surface (+2 °C) temperature. Locally, persistent thermal stratification in PF seemed to provide an optimal physical habitat for initiation and bloom development of D. acuta. Thus, in summer 2018, a favourable combination of meteorological and hydrographic processes of multiple scales created conditions that promoted the development of a widespread bloom of D. acuta with its epicentre at the head of Puyuhuapi fjord.

Disentangling the environmental processes responsible for the world's largest farmed fish-killing harmful algal bloom: Chile, 2016.

The dictyochophyte microalga Pseudochattonella verruculosa was responsible for the largest farmed fish mortality ever recorded in the world, with losses for the Chilean salmon industry amounting to US$ 800 M in austral summer 2016. Super-scale climatic anomalies resulted in strong vertical water column stratification that stimulated development of a dynamic P. verruculosa thin layer (up to 38 µg chl a L-1) for several weeks in Reloncaví Sound. Hydrodynamic modeling (MIKE 3D) indicated that the Sound had extremely low flushing rates (between 121 and 200 days) in summer 2016. Reported algal cell densities of 7000-20,000 cells mL-1 generated respiratory distress in fish that was unlikely due to low dissolved oxygen (permanently >4 mg L-1). Histological examination of salmon showed that gills were the most affected organ with significant tissue damage and circulatory disorders. It is possible that some of this damage was due to a diatom bloom that preceded the Pseudochattonella event, thereby rendering the fish more susceptible to Pseudochattonella. No correlation between magnitude of fish mortality and algal cell abundance nor fish age was evident. Algal cultures revealed rapid growth rates and high cell densities (up to 600,000 cells mL-1), as well as highly complex life cycle stages that can be easily overlooked in monitoring programs. In cell-based bioassays, Chilean P. verruculosa was only toxic to the RTgill-W1 cell line following exposures to high cell densities of lysed cells (>100,000 cells mL-1). Fatty acid profiles of a cultured strain showed elevated concentrations of potentially ichthyotoxic, long-chain polyunsaturated fatty acids (PUFAs) (69.7% ± 1.8%)- stearidonic (SDA, 18:4ω3-28.9%), and docosahexaenoic acid (DHA, 22:6ω3-22.3%), suggesting that lipid peroxidation may help to explain the mortalities, though superoxide production by Pseudochattonella was low (< 0.21 ± 0.19 pmol O2- cell-1 h-1). It therefore remains unknown what the mechanisms of salmon mortality were during the Pseudochattonella bloom. Multiple mitigation strategies were used by salmon farmers during the event, with only delayed seeding of juvenile fish into the cages and towing of cages to sanctuary sites being effective. Airlift pumping, used effectively against other fish-killing HABs in the US and Canada was not effective, perhaps because it brought subsurface layers of Pseudochattonella to the surface, or and it also may have lysed the fragile cells, rendering them more lethal. The present study highlights knowledge gaps and inefficiency of contingency plans by the fish farming industry to overcome future fish-killing algal blooms under future climate change scenarios. The use of new technologies based on molecular methods for species detection, good farm practices by fish farms, and possible mitigation strategies are discussed.