Warmer, deeper and greener mixed layers in the north Atlantic subpolar gyre over the last 50 years.

Shifts in global climate resonate in plankton dynamics, biogeochemical cycles, and marine food webs. We studied these linkages in the North Atlantic subpolar gyre (NASG), which hosts extensive phytoplankton blooms. We show that phytoplankton abundance increased since the 1960s in parallel to a deepening of the mixed layer and a strengthening of winds and heat losses from the ocean, as driven by the low frequency of the North Atlantic Oscillation (NAO). In parallel to these bottom-up processes, the top-down control of phytoplankton by copepods decreased over the same time period in the western NASG, following sea surface temperature changes typical of the Atlantic Multi-decadal Oscillation (AMO). While previous studies have hypothesized that climate-driven warming would facilitate seasonal stratification of surface waters and long-term phytoplankton increase in subpolar regions, here we show that deeper mixed layers in the NASG can be warmer and host a higher phytoplankton biomass. These results emphasize that different modes of climate variability regulate bottom-up (NAO control) and top-down (AMO control) forcing on phytoplankton at decadal timescales. As a consequence, different relationships between phytoplankton, zooplankton, and their physical environment appear subject to the disparate temporal scale of the observations (seasonal, interannual, or decadal). The prediction of phytoplankton response to climate change should be built upon what is learnt from observations at the longest timescales.

Effects of a harmful algal bloom on the community ecology, movements and spatial distributions of fishes in a microtidal estuary

Harmful algal blooms can adversely affect fish communities, though their impacts are highly context-dependent and typically differ between fish species. Various approaches, comprising univariate and multivariate analyses and multimetric Fish Community Indices (FCI), were employed to characterise the perceived impacts of a Karlodinium veneficum bloom on the fish communities and ecological condition of the Swan Canning Estuary, Western Australia. The combined evidence suggests that a large proportion of the more mobile fish species in the offshore waters of the bloom-affected area relocated to other regions during the bloom. This was indicated by marked declines in mean species richness, catch rates and FCI scores in the bloom region but concomitant increases in these characteristics in more distal regions, and by pronounced and atypical shifts in the pattern of inter-regional similarities in fish community composition during the bloom. The lack of any significant changes among the nearshore fish communities revealed that bloom impacts were less severe there than in deeper, offshore waters. Nearshore habitats, which generally are in better ecological condition than adjacent offshore waters in this system, may provide refuges for fish during algal blooms and other perturbations, mirroring similar observations of fish avoidance responses to such stressors in estuaries worldwide.

Effects of a harmful algal bloom on the community ecology, movements and spatial distributions of fishes in a microtidal estuary

Harmful algal blooms can adversely affect fish communities, though their impacts are highly context-dependent and typically differ between fish species. Various approaches, comprising univariate and multivariate analyses and multimetric Fish Community Indices (FCI), were employed to characterise the perceived impacts of a Karlodinium veneficum bloom on the fish communities and ecological condition of the Swan Canning Estuary, Western Australia. The combined evidence suggests that a large proportion of the more mobile fish species in the offshore waters of the bloom-affected area relocated to other regions during the bloom. This was indicated by marked declines in mean species richness, catch rates and FCI scores in the bloom region but concomitant increases in these characteristics in more distal regions, and by pronounced and atypical shifts in the pattern of inter-regional similarities in fish community composition during the bloom. The lack of any significant changes among the nearshore fish communities revealed that bloom impacts were less severe there than in deeper, offshore waters. Nearshore habitats, which generally are in better ecological condition than adjacent offshore waters in this system, may provide refuges for fish during algal blooms and other perturbations, mirroring similar observations of fish avoidance responses to such stressors in estuaries worldwide.

Distribution, occurrence and biotoxin composition of the main shellfish toxin producing microalgae within European waters: A comparison of methods of analysis.

Harmful algal blooms (HABs) are a natural global phenomena emerging in severity and extent. Incidents have many economic, ecological and human health impacts. Monitoring and providing early warning of toxic HABs are critical for protecting public health. Current monitoring programmes include measuring the number of toxic phytoplankton cells in the water and biotoxin levels in shellfish tissue. As these efforts are demanding and labour intensive, methods which improve the efficiency are essential. This study compares the utilisation of a multitoxin surface plasmon resonance (multitoxin SPR) biosensor with enzyme-linked immunosorbent assay (ELISA) and analytical methods such as high performance liquid chromatography with fluorescence detection (HPLC-FLD) and liquid chromatography–tandem mass spectrometry (LC–MS/MS) for toxic HAB monitoring efforts in Europe. Seawater samples (n = 256) from European waters, collected 2009–2011, were analysed for biotoxins: saxitoxin and analogues, okadaic acid and dinophysistoxins 1/2 (DTX1/DTX2) and domoic acid responsible for paralytic shellfish poisoning (PSP), diarrheic shellfish poisoning (DSP) and amnesic shellfish poisoning (ASP), respectively. Biotoxins were detected mainly in samples from Spain and Ireland. France and Norway appeared to have the lowest number of toxic samples. Both the multitoxin SPR biosensor and the RNA microarray were more sensitive at detecting toxic HABs than standard light microscopy phytoplankton monitoring. Correlations between each of the detection methods were performed with the overall agreement, based on statistical 2 × 2 comparison tables, between each testing platform ranging between 32% and 74% for all three toxin families illustrating that one individual testing method may not be an ideal solution. An efficient early warning monitoring system for the detection of toxic HABs could therefore be achieved by combining both the multitoxin SPR biosensor and RNA microarray.

Distribution, occurrence and biotoxin composition of the main shellfish toxin producing microalgae within European waters: A comparison of methods of analysis.

Harmful algal blooms (HABs) are a natural global phenomena emerging in severity and extent. Incidents have many economic, ecological and human health impacts. Monitoring and providing early warning of toxic HABs are critical for protecting public health. Current monitoring programmes include measuring the number of toxic phytoplankton cells in the water and biotoxin levels in shellfish tissue. As these efforts are demanding and labour intensive, methods which improve the efficiency are essential. This study compares the utilisation of a multitoxin surface plasmon resonance (multitoxin SPR) biosensor with enzyme-linked immunosorbent assay (ELISA) and analytical methods such as high performance liquid chromatography with fluorescence detection (HPLC-FLD) and liquid chromatography–tandem mass spectrometry (LC–MS/MS) for toxic HAB monitoring efforts in Europe. Seawater samples (n = 256) from European waters, collected 2009–2011, were analysed for biotoxins: saxitoxin and analogues, okadaic acid and dinophysistoxins 1/2 (DTX1/DTX2) and domoic acid responsible for paralytic shellfish poisoning (PSP), diarrheic shellfish poisoning (DSP) and amnesic shellfish poisoning (ASP), respectively. Biotoxins were detected mainly in samples from Spain and Ireland. France and Norway appeared to have the lowest number of toxic samples. Both the multitoxin SPR biosensor and the RNA microarray were more sensitive at detecting toxic HABs than standard light microscopy phytoplankton monitoring. Correlations between each of the detection methods were performed with the overall agreement, based on statistical 2 × 2 comparison tables, between each testing platform ranging between 32% and 74% for all three toxin families illustrating that one individual testing method may not be an ideal solution. An efficient early warning monitoring system for the detection of toxic HABs could therefore be achieved by combining both the multitoxin SPR biosensor and RNA microarray.

Diversity of luciferase sequences and bioluminescence production in Baltic Sea Alexandrium ostenfeldii

The toxic dinoflagellate Alexandrium ostenfeldii is the only bioluminescent bloom-forming phytoplankton in coastal waters of the Baltic Sea. We analysed partial luciferase gene (lcf) sequences and bioluminescence production in Baltic A. ostenfeldii bloom populations to assess the distribution and consistency of the trait in the Baltic Sea, and to evaluate applications for early detection of toxic blooms. Lcf was consistently present in 61 Baltic Sea A. ostenfeldii strains isolated from six separate bloom sites. All Baltic Sea strains except one produced bioluminescence. In contrast, the presence of lcf and the ability to produce bioluminescence did vary among strains from other parts of Europe. In phylogenetic analyses, lcf sequences of Baltic Sea strains clustered separately from North Sea strains, but variation between Baltic Sea strains was not sufficient to distinguish between bloom populations. Clustering of the lcf marker was similar to internal transcribed spacer (ITS) sequences with differences being minor and limited to the lowest hierarchical clusters, indicating a similar rate of evolution of the two genes. In relation to monitoring, the consistent presence of lcf and close coupling of lcf with bioluminescence suggests that bioluminescence can be used to reliably monitor toxic bloom-forming A. ostenfeldii in the Baltic Sea.

Diversity of luciferase sequences and bioluminescence production in Baltic Sea Alexandrium ostenfeldii

The toxic dinoflagellate Alexandrium ostenfeldii is the only bioluminescent bloom-forming phytoplankton in coastal waters of the Baltic Sea. We analysed partial luciferase gene (lcf) sequences and bioluminescence production in Baltic A. ostenfeldii bloom populations to assess the distribution and consistency of the trait in the Baltic Sea, and to evaluate applications for early detection of toxic blooms. Lcf was consistently present in 61 Baltic Sea A. ostenfeldii strains isolated from six separate bloom sites. All Baltic Sea strains except one produced bioluminescence. In contrast, the presence of lcf and the ability to produce bioluminescence did vary among strains from other parts of Europe. In phylogenetic analyses, lcf sequences of Baltic Sea strains clustered separately from North Sea strains, but variation between Baltic Sea strains was not sufficient to distinguish between bloom populations. Clustering of the lcf marker was similar to internal transcribed spacer (ITS) sequences with differences being minor and limited to the lowest hierarchical clusters, indicating a similar rate of evolution of the two genes. In relation to monitoring, the consistent presence of lcf and close coupling of lcf with bioluminescence suggests that bioluminescence can be used to reliably monitor toxic bloom-forming A. ostenfeldii in the Baltic Sea.

Individual-based modelling of the development and transport of a Karenia mikimotoi bloom on the North-West European continental shelf

In 2006, a large and prolonged bloom of the dinoflagellate Karenia mikimotoi occurred in Scottish coastal waters, causing extensive mortalities of benthic organisms including annelids and molluscs and some species of fish ( Davidson et al., 2009). A coupled hydrodynamic-algal transport model was developed to track the progression of the bloom around the Scottish coast during June–September 2006 and hence investigate the processes controlling the bloom dynamics. Within this individual-based model, cells were capable of growth, mortality and phototaxis and were transported by physical processes of advection and turbulent diffusion, using current velocities extracted from operational simulations of the MRCS ocean circulation model of the North-west European continental shelf. Vertical and horizontal turbulent diffusion of cells are treated using a random walk approach. Comparison of model output with remotely sensed chlorophyll concentrations and cell counts from coastal monitoring stations indicated that it was necessary to include multiple spatially distinct seed populations of K. mikimotoi at separate locations on the shelf edge to capture the qualitative pattern of bloom transport and development. We interpret this as indicating that the source population was being transported northwards by the Hebridean slope current from where colonies of K. mikimotoi were injected onto the continental shelf by eddies or other transient exchange processes. The model was used to investigate the effects on simulated K. mikimotoi transport and dispersal of: (1) the distribution of the initial seed population; (2) algal growth and mortality; (3) water temperature; (4) the vertical movement of particles by diurnal migration and eddy diffusion; (5) the relative role of the shelf edge and coastal currents; (6) the role of wind forcing. The numerical experiments emphasized the requirement for a physiologically based biological model and indicated that improved modelling of future blooms will potentially benefit from better parameterisation of temperature dependence of both growth and mortality and finer spatial and temporal hydrodynamic resolution.

Individual-based modelling of the development and transport of a Karenia mikimotoi bloom on the North-West European continental shelf

In 2006, a large and prolonged bloom of the dinoflagellate Karenia mikimotoi occurred in Scottish coastal waters, causing extensive mortalities of benthic organisms including annelids and molluscs and some species of fish ( Davidson et al., 2009). A coupled hydrodynamic-algal transport model was developed to track the progression of the bloom around the Scottish coast during June–September 2006 and hence investigate the processes controlling the bloom dynamics. Within this individual-based model, cells were capable of growth, mortality and phototaxis and were transported by physical processes of advection and turbulent diffusion, using current velocities extracted from operational simulations of the MRCS ocean circulation model of the North-west European continental shelf. Vertical and horizontal turbulent diffusion of cells are treated using a random walk approach. Comparison of model output with remotely sensed chlorophyll concentrations and cell counts from coastal monitoring stations indicated that it was necessary to include multiple spatially distinct seed populations of K. mikimotoi at separate locations on the shelf edge to capture the qualitative pattern of bloom transport and development. We interpret this as indicating that the source population was being transported northwards by the Hebridean slope current from where colonies of K. mikimotoi were injected onto the continental shelf by eddies or other transient exchange processes. The model was used to investigate the effects on simulated K. mikimotoi transport and dispersal of: (1) the distribution of the initial seed population; (2) algal growth and mortality; (3) water temperature; (4) the vertical movement of particles by diurnal migration and eddy diffusion; (5) the relative role of the shelf edge and coastal currents; (6) the role of wind forcing. The numerical experiments emphasized the requirement for a physiologically based biological model and indicated that improved modelling of future blooms will potentially benefit from better parameterisation of temperature dependence of both growth and mortality and finer spatial and temporal hydrodynamic resolution.

Characterisation of algicidal bacterial exometabolites against the lipid-accumulating diatom Skeletonema sp.

Microalgae are of increasing interest due to their occurrence in the environment as harmful algal blooms and as a source of biomass for the production of fine and bulk chemicals. A method for the low cost disruption of algal biomass for environmental remediation or bioprocessing is desirable. Naturally-occurring algal lytic agents from bacteria could provide a cost-effective and environmentally desirable solution. A screen for algal lytic agents against a range of marine microalgae has identified two strains of algicidal bacteria isolated from the coastal region of the Western English Channel. Both strains (designated EC-1 and EC-2) showed significant algicidal activity against Skeletonema sp. and were identified as members of Alteromonas sp. and Maribacter sp. respectively. Characterisation of the two bioactivities revealed that they are small extracellular metabolites displaying thermal and acid stability. Purification of the EC-1 activity to homogeneity and initial structural analysis has identified it as a putative peptide with a mass of 1266. amu.

Characterisation of algicidal bacterial exometabolites against the lipid-accumulating diatom Skeletonema sp.

Microalgae are of increasing interest due to their occurrence in the environment as harmful algal blooms and as a source of biomass for the production of fine and bulk chemicals. A method for the low cost disruption of algal biomass for environmental remediation or bioprocessing is desirable. Naturally-occurring algal lytic agents from bacteria could provide a cost-effective and environmentally desirable solution. A screen for algal lytic agents against a range of marine microalgae has identified two strains of algicidal bacteria isolated from the coastal region of the Western English Channel. Both strains (designated EC-1 and EC-2) showed significant algicidal activity against Skeletonema sp. and were identified as members of Alteromonas sp. and Maribacter sp. respectively. Characterisation of the two bioactivities revealed that they are small extracellular metabolites displaying thermal and acid stability. Purification of the EC-1 activity to homogeneity and initial structural analysis has identified it as a putative peptide with a mass of 1266. amu.

A role for diatom-like silicon transporters in calcifying coccolithophores.

Biomineralization by marine phytoplankton, such as the silicifying diatoms and calcifying coccolithophores, plays an important role in carbon and nutrient cycling in the oceans. Silicification and calcification are distinct cellular processes with no known common mechanisms. It is thought that coccolithophores are able to outcompete diatoms in Si-depleted waters, which can contribute to the formation of coccolithophore blooms. Here we show that an expanded family of diatom-like silicon transporters (SITs) are present in both silicifying and calcifying haptophyte phytoplankton, including some globally important coccolithophores. Si is required for calcification in these coccolithophores, indicating that Si uptake contributes to the very different forms of biomineralization in diatoms and coccolithophores. Significantly, SITs and the requirement for Si are absent from highly abundant bloom-forming coccolithophores, such as Emiliania huxleyi. These very different requirements for Si in coccolithophores are likely to have major influence on their competitive interactions with diatoms and other siliceous phytoplankton.

A role for diatom-like silicon transporters in calcifying coccolithophores.

Biomineralization by marine phytoplankton, such as the silicifying diatoms and calcifying coccolithophores, plays an important role in carbon and nutrient cycling in the oceans. Silicification and calcification are distinct cellular processes with no known common mechanisms. It is thought that coccolithophores are able to outcompete diatoms in Si-depleted waters, which can contribute to the formation of coccolithophore blooms. Here we show that an expanded family of diatom-like silicon transporters (SITs) are present in both silicifying and calcifying haptophyte phytoplankton, including some globally important coccolithophores. Si is required for calcification in these coccolithophores, indicating that Si uptake contributes to the very different forms of biomineralization in diatoms and coccolithophores. Significantly, SITs and the requirement for Si are absent from highly abundant bloom-forming coccolithophores, such as Emiliania huxleyi. These very different requirements for Si in coccolithophores are likely to have major influence on their competitive interactions with diatoms and other siliceous phytoplankton.

Haptophyta

Haptophyta are predominantly planktonic and phototrophic organisms that have their main distribution in marine environments worldwide. They are a major component of the microbial ecosystem, some form massive blooms and some are toxic. Haptophytes are significant players in the global carbonate cycle through photosynthesis and calcification. They are characterized by the haptonema, a third appendage used for attachment and food handling, two similar flagella, two golden-brown chloroplasts, and organic body scales that serve in species identification. Coccolithophores have calcified scales termed coccoliths. Phylogenetically Haptophyta form a well-defined group and are divided into two classes Pavlovophyceae and Coccolithophyceae (Prymnesiophyceae). Currently, about 330 species are described. Environmental DNA sequencing shows high haptophyte diversity in the marine pico- and nanoplankton, of which many likely represent novel species and lineages. Haptophyte diversity is believed to have peaked in the past and their presence is documented in the fossil record back to the Triassic, approximately 225 million years ago. Some biomolecules of haptophyte origin are extraordinarily resistant to decay and are thus used by geologists as sedimentary proxies of past climatic conditions.

Haptophyta

Haptophyta are predominantly planktonic and phototrophic organisms that have their main distribution in marine environments worldwide. They are a major component of the microbial ecosystem, some form massive blooms and some are toxic. Haptophytes are significant players in the global carbonate cycle through photosynthesis and calcification. They are characterized by the haptonema, a third appendage used for attachment and food handling, two similar flagella, two golden-brown chloroplasts, and organic body scales that serve in species identification. Coccolithophores have calcified scales termed coccoliths. Phylogenetically Haptophyta form a well-defined group and are divided into two classes Pavlovophyceae and Coccolithophyceae (Prymnesiophyceae). Currently, about 330 species are described. Environmental DNA sequencing shows high haptophyte diversity in the marine pico- and nanoplankton, of which many likely represent novel species and lineages. Haptophyte diversity is believed to have peaked in the past and their presence is documented in the fossil record back to the Triassic, approximately 225 million years ago. Some biomolecules of haptophyte origin are extraordinarily resistant to decay and are thus used by geologists as sedimentary proxies of past climatic conditions.