Pelagic harmful algal blooms and climate change: Lessons from nature's experiments with extremes

Time series now have sufficient duration to determine harmful algal bloom (HAB) responses to changing climate conditions, including warming, stratification intensity, freshwater inputs and natural patterns of climate variability, such as the El Niño Southern Oscillation and Pacific Decadal Oscillation. Against the context of time series, such as those available from phytoplankton monitoring, dinoflagellate cyst records, the Continuous Plankton Recorder surveys, and shellfish toxin records, it is possible to identify extreme events that are significant departures from long-term means. Extreme weather events can mimic future climate conditions and provide a "dress rehearsal" for understanding future frequency, intensity and geographic extent of HABs. Three case studies of extreme HAB events are described in detail to explore the drivers and impacts of these oceanic outliers that may become more common in the future. One example is the chain-forming diatom of the genus Pseudo-nitzschia in the U.S. Pacific Northwest and its response to the 2014-16 northeast Pacific marine heat wave. The other two case studies are pelagic flagellates. Highly potent Alexandrium catenella group 1 dinoflagellate blooms (up to 150 mg/kg PST in mussels; 4 human poisonings) during 2012-17 created havoc for the seafood industry in Tasmania, south-eastern Australia, in a poorly monitored area where such problems were previously unknown. Early evidence suggests that changes in water column stratification during the cold winter-spring season are driving new blooms caused by a previously cryptic species. An expansion of Pseudochattonella cf. verruculosa to the south and A. catenella to the north over the past several years resulted in the convergence of both species to cause the most catastrophic event in the history of the Chilean aquaculture in the austral summer of 2016. Together, these two massive blooms were colloquially known as the "Godzilla-Red tide event", resulting in the largest fish farm mortality ever recorded worldwide, equivalent to an export loss of USD$800 million which when combined with shellfish toxicity, resulted in major social unrest and rioting. Both blooms were linked to the strong El Niño event and the positive phase of the Southern Annular Mode, the latter an indicator of anthropogenic climate change in the southeastern Pacific region. For each of these three examples, representing recent catastrophic events in geographically distinct regions, additional targeted monitoring was employed to improve the understanding of the climate drivers and mechanisms that gave rise to the event and to document the societal response. Scientists must be poised to study future extreme HAB events as these natural experiments provide unique opportunities to define and test multifactorial drivers of blooms.