Extreme harmful algal blooms, climate change, and potential risk of eutrophication in Patagonian fjords: Insights from an exceptional Heterosigma akashiwo fish-killing event

Abstract

The Patagonian fjords have experienced intense harmful algal blooms (HABs) in the last decade, affecting important aquaculture areas in southern Chile. Climatic anomalies have recently triggered ‘super blooms’ of opportunistic toxic microalgal genera, especially due to persistent thermal stratification which likely provides an optimal niche for HABs development in fjord systems. In March-April 2021, an intense and widespread bloom of the raphidophyte Heterosigma akashiwo caused high salmon mortalities (>6,000 t) in the Comau fjord, Los Lagos Region. A climate variability analysis showed the effects of the positive phase of the Southern Annular Mode (SAM > 1.2 hPa) overcame those of La Niña (Niño3.4 = -0.9 °C) leading to an intense drought on the northern part of Patagonia with record low rainfall (the 2nd driest summer in the last 70 years) and increased water temperature. A regional satellite analysis revealed an extreme and persistent shallow Mixed Layer Depth (MLD) during summer periods since 2019 within the inland seas. In situ vertical fine-resolution measurements during the bloom event showed high cell abundances in the first 3 m of the water column (max. ∼ 70,000 cells mL−1), associated with warmer water temperature (∼15.5 – 17.5 °C), low salinity (∼25–30 psu), moderate to high dissolved oxygen (5 – 8.5 mg/L) and extremely high fluorescence signals in dense superficial cell aggregations (max. 74.9 µg/L). A 18S rRNA metabarcoding analysis formally confirmed the presence of H. akashiwo and its almost monospecific bloom development at the water surface. HPLC pigment analysis showed the carotenoid fucoxanthin in high proportion (48.8 %) compared to other photosynthetic pigments, becoming a potential pigment biomarker for early satellite H. akashiwo detection. Cell growth and cytotoxic in vitro experiments revealed high phenotypic plasticity of Chilean H. akashiwo against sudden changes in salinity. An RTgill-W1 gill cell assay revealed high cytotoxic activity (viability down to ∼ 50 – 30 % of controls) only at high cell abundances (>40,000H. akashiwo cells mL−1), which was in accordance with histological examination of moribund salmon that showed gill damage and circulatory disorders mainly due to long-term exposure to hypoxic conditions and not to potent cytotoxic effects. The Party-MOSA particles dispersion model revealed a high retention of water masses within the Comau fjord during the H. akashiwo outbreak, a scenario that may have boosted fish kills due to enhanced cells patchiness, ichthyotoxins persistence and hypoxic conditions. A historical dissolved inorganic nutrient data analysis showed that inner Patagonian fjords maintain low N and P concentrations including those environments considered of high eutrophication risk. Low N:P (<16:1) ratios measured at Comau fjord during the 2021 suggests that toxic flagellates growth could be favored over diatoms; however, low N:Si (<1:1 – N deficiency) evidences a clear need for better understanding of the role of mixotrophy in the persistence of the 2021H. akashiwo bloom for several weeks. These results highlight the fact that HABs responses against climate drivers and potential eutrophication are not universal and need to be assessed yearly and locally, particularly because extreme droughts and intensive aquaculture in northern Patagonia are expected to continue throughout the 21st century.