Emerging phylogeographic perspective on the toxigenic diatom genus Pseudo-nitzschia in coastal northern European waters and gateways to eastern Arctic seas: Causes, ecological consequences and socio-economic impacts.

The diatom Pseudo-nitzschia H. Peragallo is perhaps the most intensively researched genus of marine pennate diatoms, with respect to species diversity, life history strategies, toxigenicity, and biogeographical distribution. The global magnitude and consequences of harmful algal blooms (HABs) of Pseudo-nitzschia are particularly significant because of the high socioeconomic impacts and environmental and human health risks associated with the production of the neurotoxin domoic acid (DA) among populations of many (although not all) species. This has led to enhanced monitoring and mitigation strategies for toxigenic Pseudo-nitzschia blooms and their toxins in recent years. Nevertheless, human adaptive actions based on future scenarios of bloom dynamics and proposed shifts in biogeographical distribution under climate-change regimes have not been implemented on a regional scale. In the CoCliME (Co-development of climate services for adaptation to changing marine ecosystems) program these issues were addressed with respect to past, current and anticipated future status of key HAB genera such as Pseudo-nitzschia and expected benefits of enhanced monitoring. Data on the distribution and frequency of Pseudo-nitzschia blooms in relation to DA occurrence and associated amnesic shellfish toxin (AST) events were evaluated in a contemporary and historical context over the past several decades from key northern CoCliME Case Study areas. The regional studies comprised the greater North Sea and adjacent Kattegat-Skagerrak and Norwegian Sea, eastern North Atlantic marginal seas and Arctic gateways, and the Baltic Sea. The first evidence of possible biogeographical expansion of Pseudo-nitzschia taxa into frontier eastern Arctic gateways was provided from DNA barcoding signatures. Key climate change indicators, such as salinity, temperature, and water-column stratification were identified as drivers of upwelling and advection related to the distribution of regional Pseudo-nitzschia blooms. The possible influence of changing variables on bloom dynamics, magnitude, frequency and spatial and temporal distribution were interpreted in the context of regional ocean climate models. These climate change indicators may play key roles in selecting for the occurrence and diversity of Pseudo-nitzschia species within the broader microeukaryote communities. Shifts to higher temperature and lower salinity regimes predicted for the southern North Sea indicate the potential for high-magnitude Pseudo-nitzschia blooms, currently absent from this area. Ecological and socioeconomic impacts of Pseudo-nitzschia blooms are evaluated with reference to effects on fisheries and mariculture resources and coastal ecosystem function. Where feasible, effective adaptation strategies are proposed herein as emerging climate services for the northern CoCLiME region.

Forecasting harmful algae blooms: Application to Dinophysis acuminata in northern Norway.

Dinophysis acuminata produces Diarrhetic Shellfish Toxins (DST) that contaminate natural and farmed shellfish, leading to public health risks and economically impacting mussel farms. For this reason, there is a high interest in understanding and predicting D. acuminata blooms. This study assesses the environmental conditions and develops a sub-seasonal (7 - 28 days) forecast model to predict D. acuminata cells abundance in the Lyngen fjord located in northern Norway. A Support Vector Machine (SVM) model is trained to predict future D. acuminata cells abundance by using the past cell concentration, sea surface temperature (SST), Photosynthetic Active Radiation (PAR), and wind speed. Cells concentration of Dinophysis spp. are measured in-situ from 2006 to 2019, and SST, PAR, and surface wind speed are obtained by satellite remote sensing. D. acuminata only explains 40% of DST variability from 2006 to 2011, but it changes to 65% after 2011 when D. acuta prevalence reduced. The D. acuminata blooms can reach concentration up to 3954 cells l-1 and are restricted to the summer during warmer waters, varying from 7.8 to 12.7 °C. The forecast model predicts with fair accuracy the seasonal development of the blooms and the blooms amplitude, showing a coefficient of determination varying from 0.46 to 0.55. SST has been found to be a useful predictor for the seasonal development of the blooms, while the past cells abundance is needed for updating the current status and adjusting the blooms timing and amplitude. The calibrated model should be tested operationally in the future to provide an early warning of D. acuminata blooms in the Lyngen fjord. The approach can be generalized to other regions by recalibrating the model with local observations of D. acuminata blooms and remote sensing data.

Apparent biogeographical trends in Alexandrium blooms for northern Europe: identifying links to climate change and effective adaptive actions.

The marine dinoflagellate Alexandrium Halim represents perhaps the most significant and intensively studied genus with respect to species diversity, life history strategies, toxigenicity, biogeographical distribution, and global magnitude and consequences harmful algal blooms (HABs). The socioeconomic impacts, environmental and human health risks, and mitigation strategies for toxigenic Alexandrium blooms have also been explored in recent years. Human adaptive actions based on future scenarios of bloom dynamics and shifts in biogeographical distribution under climate-change parameters remain under development and not yet implemented on a regional scale. In the CoCliME (Co-development of climate services for adaptation to changing marine ecosystems) project these issues were addressed with respect to past, current and anticipated future status of key HAB genera and expected benefits of enhanced monitoring. Data on the distribution and frequency of Alexandrium blooms related to paralytic shellfish toxin (PST) events from key CoCliME Case Study areas, comprising the North Sea and adjacent Kattegat-Skagerrak, Norwegian Sea, and Baltic Sea, and eastern North Atlantic marginal seas, were evaluated in a contemporary and historical context over the past several decades. The first evidence of possible biogeographical expansion of Alexandrium taxa into eastern Arctic gateways was provided from DNA barcoding signatures. Various key climate change indicators, such as salinity, temperature, and water-column stratification, relevant to Alexandrium bloom initiation and development were identified. The possible influence of changing variables on bloom dynamics, magnitude, frequency and spatial and temporal distribution were interpreted in the context of regional ocean climate models. These climate change impact indicators may play key roles in selecting for the occurrence and diversity of Alexandrium species within the broader microeukaryote communities. For example, shifts to higher temperature and lower salinity regimes predicted for the southern North Sea indicate the potential for increased Alexandrium blooms, currently absent from this area. Ecological and socioeconomic impacts of Alexandrium blooms and effects on fisheries and aquaculture resources and coastal ecosystem function are evaluated, and, where feasible, effective adaptation strategies are proposed herein as emerging climate services.

Spatial and biological oceanographic insights into the massive fish-killing bloom of the haptophyte Chrysochromulina leadbeateri in northern Norway.

A bloom of the fish-killing haptophyte Chrysochromulina leadbeateri in northern Norway during May and June 2019 was the most harmful algal event ever recorded in the region, causing massive mortalities of farmed salmon. Accordingly, oceanographic and biodiversity aspects of the bloom were studied in unprecedented detail, based on metabarcoding and physico-chemical and biotic factors related with the dynamics and distribution of the bloom. Light- and electron-microscopical observations of nanoplankton samples from diverse locations confirmed that C. leadbeateri was dominant in the bloom and the primary cause of associated fish mortalities. Cell counts by light microscopy and flow cytometry were obtained throughout the regional bloom within and adjacent to five fjord systems. Metabarcoding sequences of the V4 region of the 18S rRNA gene from field material collected during the bloom and a cultured isolate from offshore of Tromsøy island confirmed the species identification. Sequences from three genetic markers (18S, 28S rRNA gene and ITS region) verified the close if not identical genetic similarity to C. leadbeateri from a previous massive fish-killing bloom in 1991 in northern Norway. The distribution and cell abundance of C. leadbeateri and related Chrysochromulina species in the recent incident were tracked by integrating observations from metabarcoding sequences of the V4 region of the 18S rRNA gene. Metabarcoding revealed at least 14 distinct Chrysochromulina variants, including putative cryptic species. C. leadbeateri was by far the most abundant of these species, but with high intraspecific genetic variability. Highest cell abundance of up to 2.7 × 107 cells L - 1 of C. leadbeateri was found in Balsfjorden; the high cell densities were associated with stratification near the pycnocline (at ca. 12 m depth) within the fjord. The cell abundance of C. leadbeateri showed positive correlations with temperature, negative correlation with salinity, and a slightly positive correlation with ambient phosphate and nitrate concentrations. The spatio-temporal succession of the C. leadbeateri bloom suggests independent initiation from existing pre-bloom populations in local zones, perhaps sustained and supplemented over time by northeastward advection of the bloom from the fjords.

Harmful algal blooms and their effects in coastal seas of Northern Europe.

Harmful algal blooms (HAB) are recurrent phenomena in northern Europe along the coasts of the Baltic Sea, Kattegat-Skagerrak, eastern North Sea, Norwegian Sea and the Barents Sea. These HABs have caused occasional massive losses for the aquaculture industry and have chronically affected socioeconomic interests in several ways. This status review gives an overview of historical HAB events and summarises reports to the Harmful Algae Event Database from 1986 to the end of year 2019 and observations made in long term monitoring programmes of potentially harmful phytoplankton and of phycotoxins in bivalve shellfish. Major HAB taxa causing fish mortalities in the region include blooms of the prymnesiophyte Chrysochromulina leadbeateri in northern Norway in 1991 and 2019, resulting in huge economic losses for fish farmers. A bloom of the prymesiophyte Prymnesium polylepis (syn. Chrysochromulina polylepis) in the Kattegat-Skagerrak in 1988 was ecosystem disruptive. Blooms of the prymnesiophyte Phaeocystis spp. have caused accumulations of foam on beaches in the southwestern North Sea and Wadden Sea coasts and shellfish mortality has been linked to their occurrence. Mortality of shellfish linked to HAB events has been observed in estuarine waters associated with influx of water from the southern North Sea. The first bloom of the dictyochophyte genus Pseudochattonella was observed in 1998, and since then such blooms have been observed in high cell densities in spring causing fish mortalities some years. Dinoflagellates, primarily Dinophysis spp., intermittently yield concentrations of Diarrhetic Shellfish Toxins (DST) in blue mussels, Mytilus edulis, above regulatory limits along the coasts of Norway, Denmark and the Swedish west coast. On average, DST levels in shellfish have decreased along the Swedish and Norwegian Skagerrak coasts since approximately 2006, coinciding with a decrease in the cell abundance of D. acuta. Among dinoflagellates, Alexandrium species are the major source of Paralytic Shellfish Toxins (PST) in the region. PST concentrations above regulatory levels were rare in the Skagerrak-Kattegat during the three decadal review period, but frequent and often abundant findings of Alexandrium resting cysts in surface sediments indicate a high potential risk for blooms. PST levels often above regulatory limits along the west coast of Norway are associated with A. catenella (ribotype Group 1) as the main toxin producer. Other Alexandrium species, such as A. ostenfeldii and A. minutum, are capable of producing PST among some populations but are usually not associated with PSP events in the region. The cell abundance of A. pseudogonyaulax, a producer of the ichthyotoxin goniodomin (GD), has increased in the Skagerrak-Kattegat since 2010, and may constitute an emerging threat. The dinoflagellate Azadinium spp. have been unequivocally linked to the presence of azaspiracid toxins (AZT) responsible for Azaspiracid Shellfish Poisoning (AZP) in northern Europe. These toxins were detected in bivalve shellfish at concentrations above regulatory limits for the first time in Norway in blue mussels in 2005 and in Sweden in blue mussels and oysters (Ostrea edulis and Crassostrea gigas) in 2018. Certain members of the diatom genus Pseudo-nitzschia produce the neurotoxin domoic acid and analogs known as Amnesic Shellfish Toxins (AST). Blooms of Pseudo-nitzschia were common in the North Sea and the Skagerrak-Kattegat, but levels of AST in bivalve shellfish were rarely above regulatory limits during the review period. Summer cyanobacteria blooms in the Baltic Sea are a concern mainly for tourism by causing massive fouling of bathing water and beaches. Some of the cyanobacteria produce toxins, e.g. Nodularia spumigena, producer of nodularin, which may be a human health problem and cause occasional dog mortalities. Coastal and shelf sea regions in northern Europe provide a key supply of seafood, socioeconomic well-being and ecosystem services. Increasing anthropogenic influence and climate change create environmental stressors causing shifts in the biogeography and intensity of HABs. Continued monitoring of HAB and phycotoxins and the operation of historical databases such as HAEDAT provide not only an ongoing status report but also provide a way to interpret causes and mechanisms of HABs.

Summer mortalities and detection of ostreid herpesvirus microvariant in Pacific oyster Crassostrea gigas in Sweden and Norway.

The Pacific oyster Crassostrea gigas has recently expanded its range in Scandinavia. The expansion is presumably a result of northwards larval drift. Massive settlements were recorded in many areas along the Swedish west coast and southern Norway in 2013 and 2014. After the spawning season in 2014, the temperature of the surface water peaked at 24-26°C. After this period, high and sudden mortalities occurred in a Swedish hatchery and in wild populations along the Swedish west coast and south coast of Norway. Surveys and collected data showed that mortalities mainly occurred during 3 wk in September. All size classes were affected, and affected populations displayed a patchy distribution with heavily affected and unaffected populations in close proximity. Flat oysters Ostrea edulis and blue mussels Mytilus edulis were unaffected. Ostreid herpesvirus (OsHV) was detected in moribund Pacific oyster spat as well as in surviving adults. The virus was identified as OsHV-1 µvar. This is the first detection of this variant in Scandinavia, showing that OsHV-1 µvar is present in areas with recent establishments of Pacific oysters, and where there is no aquaculture of this species.

A novel pectenotoxin, PTX-12, in Dinophysis spp. and shellfish from Norway.

Two novel pectenotoxins (PTXs) were detected by LC-MS in solid phase extracts of net hauls taken at Flødevigen, Norway, in June 2002 that were dominated by Dinophysis acuminata and Dinophysis norvegica. The new compounds were isolated as minor components from a large collection of a Dinophysis acuta-dominated bloom obtained from Skjer, Sognefjorden, Norway, in October 2002. LC-MS and NMR analyses revealed that the new components, 36S-PTX-12 and 36R-PTX-12, occurred as a pair of equilibrating diastereoisomers differing from PTX-2 in that they contained an exocylic olefinic methylene rather than a methyl group at C-38. Analyses of shellfish extracts revealed that PTX-12 accumulated in Norwegian blue mussels (Mytilus edulis) and cockles (Cerastoderma edule), along with PTX-12 seco acids occurring as a complex mixture of diastereoisomers. LC-MS analysis of algal cells picked from the net haul from Flødevigen revealed that PTX-12 predominated in D. acuta and D. norvegica, whereas PTX-2 was the predominant pectenotoxin in D. acuminata. Preliminary observations indicate that the relative contents of PTX-2 and PTX-12 vary between sites and years in Norway, even within a single species of Dinophysis. Our data also suggest that heterotrophic dinoflagellates may accumulate toxins from their prey.