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Changing wind patterns linked to unusually high Dinophysis blooms around the Shetland Islands, Scotland
Harmful Algae 39 (2014) 365–373
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Changing wind patterns linked to unusually high Dinophysis blooms around the Shetland Islands, Scotland Callum Whyte *, Sarah Swan 1,2, Keith Davidson 1,2 Microbial and Molecular Biology Department, Scottish Association for Marine Science, Scottish Marine Institute, Oban, Argyll PA37 1QA, United Kingdom
A R T I C L E I N F O
A B S T R A C T
Article history: Received 9 May 2014 Received in revised form 16 September 2014 Accepted 17 September 2014 Available online
During the summer of 2013, 70 people received Diarrhetic Shellfish Poisoning following consumption of mussels harvested in the Shetland Islands, Scotland. At this time, large numbers of the biotoxinproducing phytoplankton genus Dinophysis was observed around the Shetland Islands. Analysis indicated this increase was not due to in situ growth but coincided with a change in the prevalent wind direction. A previous large bloom of Dinophysis during 2006 also coincided with a similar change in the prevalent wind patterns. Wind direction and speed in the North East Atlantic and the North Sea is strongly influenced by the North Atlantic oscillation (NAO) with a positive relationship between it and wind direction. It has been noted that a positive trend in the NAO is linked to climate change and predictions suggest there will be an increasingly westward component to prevalent wind directions in the North Sea which could lead to an increase in the occurrence of these harmful algal blooms. Analysis of wind patterns therefore offers a potential method of early warning of future bio-toxicity events. ß 2014 Published by Elsevier B.V.
Keywords: Dinophysis Harmful algal bloom Dinophysistoxins Advection Wind pattern Shetland Islands
1. Background In July 2013 there was an outbreak of Diarrhetic Shellfish Poisoning (DSP) in the South East of England. Although it is not known how many people were actually affected, 70 people sought medical advice after consuming mussels which, they had been served in several prominent restaurants in London. They were later found to be suffering the symptoms of DSP. The shellfish had been supplied by a farm in the coastal waters of the Shetland Islands (Fig. 1). Although the numbers of Dinophysis had been slowly increasing during the preceding few weeks, analysis did not indicate that the concentration of toxins in the shellfish was high. However three days after the farmer had harvested the shellfish an unusually high level of toxins was detected by the Food Standards Agency (FSA) weekly monitoring programme (FSA, 2013), accom-
Abbreviations: ASIMUTH, Applied Simulations and Integrated Modelling for the Understanding of Toxic and Harmful Algal Blooms; BADC, British Atmospheric Data Centre; DSP, Diarrhetic Shellfish Poisoning; DTX (1–3), dinophysistoxins; GDP, Gross Domestic Product; FSA, Food Standards Agency; NAO, North Atlantic Oscillation; OA, okadaic acid; SAMS, Scottish Association for Marine Science. * Corresponding author. Tel.: +44 01631 559 226. E-mail addresses: [email protected], [email protected] (C. Whyte), [email protected] (S. Swan), [email protected] (K. Davidson). 1 These authors contributed equally to this work. 2 Tel: +44 01631 559 226. http://dx.doi.org/10.1016/j.hal.2014.09.006 1568-9883/ß 2014 Published by Elsevier B.V.
panied by a very rapid accumulation of Dinophysis cells. The area was closed and commercial harvesting was suspended, unfortunately too late for the luckless consumers of the affected mussels. This paper investigates the possibility that the unusually large blooms of Dinophysis observed around the coast of Shetland during 2013, and another large bloom event during 2006, were not due to high in situ growth rates, but rather to changes in the annual pattern of prevalent wind direction. We discuss the possibility that an analysis of wind patterns could be used to provide an early warning of biotoxic events. Yasumoto et al. (1980) was among the first to suggest that gastro-intestinal pain, accompanied by diarrhoea, nausea and vomiting, following the consumption of mussels (Mytilus edulis) was linked to the presence of dinoflagellates in the water column, in particular Dinophysis fortii. This link was confirmed after outbreaks of severe gastro-intestinal shellfish poisoning in Japan during 1976 and 1977 and led to the identification of a new set of toxins associated with the genus Dinophysis (Reguera et al., 2012). Identified as Diarrhetic Shellfish Poisoning (DSP) causative toxins, these lipophilic compounds are comprised principally of Okadaic Acid (OA) and its derivatives DTX-1, DTX-2 and DTX-3 (Smayda, 2006; Taylor et al., 2013). They have been found to bind with protein phosphatase receptors in the body, leading to an accumulation of phosphorylated proteins with symptoms of lethargy, general weakness, vomiting, cramps and diarrhoea,
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symptoms that can appear from 30 min to several hours after ingestion of the contaminated shellfish (Gerssen et al., 2010). The Dinophysis species most commonly found in Scottish waters are D. acuminata, D. acuta, and D. norvegica, all of which have been confirmed to produce toxins with particular emphasis on D. acuminata and D. acuta (Bresnan et al., 2005; Hart et al., 2007). While contamination of both farmed and wild shellfish by OA and DTX’s is sporadic, it is widespread and has been reported from eleven countries across Europe including Denmark, France, Germany, Ireland, Italy, Norway, Portugal, Spain, Sweden and the Netherlands (Smayda, 2006). Perhaps the severest outbreak occurred in Spain during 1981 when an outbreak of DSP affected approximately 5000 people, mostly from Madrid (Fraga et al., 1984, 1988; Gestal-Otero, 2000). While unrecorded cases are likely to have occurred, the first reliable record of Diarrhetic Shellfish Poisoning in the UK was in 1997 when 49 people became ill after eating shellfish in two London restaurants (Hinder et al., 2011; Scoging and Bahl, 1998). Since then the frequency of closures due to DSP around the UK appears to be increasing. This may simply be due to a better understanding of the underlying causes of shellfish poisoning, a greater awareness of the problem and a more rigorous monitoring programme. Unlike some species of harmful algae, Dinophysis does not need to be present in large numbers to cause toxicity in shellfish. A few hundred cells/l can be enough to lead to the closure of a harvesting area. In 2000, DSP toxins were found in shellfish in areas on the East coast of Scotland, Orkney, the Outer Hebrides, the Shetland Islands and the Firth of Clyde. In all, closures of the various shellfish harvesting areas amounted to 24 weeks (Howard et al., 2001). In 2002, DSP toxins were found throughout Scotland with the majority of the closures lasting between four to six weeks, although some areas were closed for up to seven months. Between 2008 and 2009, thirteen areas were closed in the Shetland Islands and seven areas in Argyll and Bute (Hinder et al., 2011) and most recently, large areas of Shetland were closed for several weeks during 2013. In addition to the extremely distressing effects contaminated shellfish can have on anyone who consumes them, a DSP outbreak can have far reaching consequences for the shellfish industry. While there is an obvious detrimental effect on farmers, processors and distributors, the impact can extend well outside the closed harvesting area. In what is sometimes referred to as a ‘‘halo’’ effect (Rural Affairs Committee, 1999) consumer confidence is often lost, not only in the closed fishery, but in shellfish products in general, regardless of the area where they were harvested. This loss of confidence can easily outlast the closure itself and, as much of Scotland’s production is destined for overseas markets, can have serious economic impacts for the country’s GDP (Rural Affairs Committee, 1999). DSP events are particularly damaging to aquaculture in the South West of Ireland, an area responsible for 80% of the rope grown blue mussel (Mytilus edulis) and 50% of the pacific oyster (Crassostrea gigas) cultivated in Ireland. Production in this area suffers from a history of harmful algal events; often closing the area for months at a time (Raine et al., 2010). The frequency of shellfish harvesting area closures due to DSP events in Southern Ireland, particularly in the large bays of Bantry, Dunmanus and Long Island, would suggest that these areas are particularly suited for the growth of Dinophysis. However the hydro-dynamic processes, in particular, the exchange of substantial fractions of the bay volume during thermal stratification, present in these bays suggests that they are unsuited to the development of indigenous phytoplankton populations (Raine et al., 2010). Instead, it is believed to be wind driven water exchange between the Irish coast and the continental shelf that is responsible for these events (Raine et al., 2010). Similarly, Escalera et al. (2010) have confirmed that
accumulations of Dinophysis species in Galician rı´as during October and November were due not to intrinsic growth but to physical transport from other areas. In Scottish waters Dinophysis are widely distributed, usually in low numbers (Tett and Edwards, 2002; Davidson and Bresnan, 2009) and are generally found in offshore waters. Once advected onshore, however, they can accumulate in semi-enclosed areas where in the right conditions they may thrive. Given their widespread distribution, outbreaks of DSP can occur almost anywhere around the Scottish coast. Responsible for 54% of the mussel production in Scotland with 105 businesses involved in shellfish production (Shetland in Statistics, 2011), Shetland plays an important role in the Scottish economy. Given its geographical location and its topography, comprised of numerous fjords and embayments, it provides an ideal environment for shellfish aquaculture. However, as the closures due to an exceptionally large bloom of Dinophysis experienced during the summer of 2013 illustrate, it is also vulnerable to blooms of these harmful algae. The Scottish Government has called for an increase in shellfish production from 6,525 tonnes in 2012 to a proposed 13,000 tonnes by 2020. It is important therefore to understand the mechanism underlying this unusual event and try to estimate its likelihood of recurrence. 2. Methods Following the FSA guidelines, seawater samples integrated over a depth of 10 m were collected by Lund tube as part of the FSA phytoplankton monitoring programme for Scottish waters. The samples were gently mixed and 500 ml sub-samples transferred to brown, Nalgene bottles and immediately treated with acidified Lugol’s solution to obtain a final concentration of 1% by volume. Samples were collected weekly from nine distinct sites around Shetland between April and October. From November to March the frequency of sampling was reduced to one sample per month. After collection, these samples were sent to the Scottish Association for Marine Science (SAMS) where 50 ml aliquots were settled using the Utermo˝ hl sedimentation method as outlined in Lund et al. (1958). Following FSA protocols the phytoplankton was allowed to settle for a minimum of 20 h before examination. Full chamber counts at 200 magnification were carried out using Carl Zeiss Axiovert inverted microscopes. While regulatory biotoxin phytoplankton surveillance and monitoring has occurred in Scotland since 1991, early sampling was spatially and temporally variable. However, since 2006 a more structured collection regime has been used, with FSA-funded sampling officers collecting waters samples from designated representative monitoring points within classified shellfish production areas. Hence, to determine whether the number of Dinophysis cells recorded in Shetland during 2013 had changed significantly, a plot of all the Dinophysis counts made between 2006 and 2013 was created. The median was calculated for each day of the year between 2006 and 2013 and was drawn onto this plot (see Fig. 2 solid line) along with the 5th and 95th percentiles. These are represented in the figure by the dashed lines and form an envelope encompassing 90% of the observations made. The individual datum points have been omitted for clarity. Counts of Dinophysis recorded during 2013 were then plotted against this median and a Chi square test was performed, making the assumption that values recorded during 2013 would be equally distributed around the median. Using the same envelope for counts made between 2006 and 2013 this method was used to investigate Dinophysis counts made during 2006 (see Fig. 3). Active phytoplankton growth in Scottish waters occurs mostly between spring and autumn when light, water temperature and nutrients are sufficient (Davidson et al., 2011). As the monitoring
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Fig. 1. Map of location showing sampling sites mentioned in the text.
summer counts, making them appear more significant than they are. To counter this, counts were transformed using Log10(X + 0.5z), where X = the number of Dinophysis cells counted and z = the detection limit, in this case 20 cells/l. To ascertain wind direction, data were downloaded from the British Atmospheric Data Centre (BADC) (BADC, 2012) for Lerwick, Shetland (BADC station identifier src-id 9). The BADC provided hourly wind direction and wind speed for each day of the year. These data were then averaged to obtain a mean daily scalar wind speed and direction for each year between 2006 and 2013. A ‘‘climatology’’ was then created by calculating the mean values for each day of the year between 2006 and 2013. To generate the monthly wind roses these mean daily values were binned into sixteen 22.5 degree bins and plotted in Microsoft Excel. 2.1. Growth rates
Fig. 2. (A) Dinophysis counts recorded in Shetland during 2013 (circles) plotted against median values of Dinophysis recorded in Shetland between 2006 and 2013 (solid black line). Dashed lines represent the 5th and 95th percentiles of the data collected between 2006 and 2013. (B) Dinophysis counts recorded in Shetland during 2006 (circles) plotted against median values of Dinophysis recorded in Shetland between 2006 and 2013 (solid black line). Dashed lines represent the 5th and 95th percentiles of the data collected between 2006 and 2013.
programme takes place throughout the year, albeit at a reduced frequency during the winter months, many of the observations made in the early and late parts of the year consist of zero counts. This has the tendency to drag the median down and can bias
Any significant changes in the number of Dinophysis recorded could potentially be due to natural, inter-annual differences in growth rates. In situ and cultured growth rates for Dinophysis species grown at different temperatures vary widely in the literature. In an attempt to choose a realistic value, only those growth rates found from in situ studies involving those species of Dinophysis growing in Scottish waters and at the temperatures found in the waters around Shetland were used. To estimate the exponential growth rates of Dinophysis around Shetland, a mean value of 0.32 d 1 calculated from the values shown in Table 1 was used. In situ growth rates cover a wide range of values and the value chosen can have a marked effect on the outcome. To address this, growth rates were also calculated for one standard deviation from the mean. As with growth rates, loss rates can also vary widely in the literature. Zhai et al. (2010) working in the North-west Atlantic calculated loss rates between 10% and 60%, while Kozlowsky-Suzuki et al., 2006 estimated 25% losses from copepod grazing in the Baltic Sea. Again taking a conservative approach, the lowest of these loss rates, i.e. 10% was chosen. Dinophysis is a mixotroph, requiring light, nutrients and live prey to thrive. Unfortunately, suitable data on nutrient levels, irradiance and the availability of prey that would allow a detailed growth model to be constructed for the sites in question were not available. Nevertheless taking a conservative approach, and assuming idyllic growth conditions existed at the sites, a simple
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Fig. 3. Dinophysis numbers recorded at (A) Braewick Voe, (B) Ronas Voe, (C) East of Linga and (D) Busta Voe, Shetland during July and August 2013 (solid line) plotted alongside the numbers of Dinophysis that would be expected from a simple exponential growth model with 10% losses (dashed line). The exponential growth rates for one standard deviation are represented by the lighter shaded lines. Diagrams (E) Basta Voe Cove and (F) Scarvar Ayre, both located on the East coast of Shetland, are shown as a comparison.
model of exponential growth with 10% losses was used to predict the numbers of Dinophysis (N) that could be expected to be present during the bloom, i.e. dN/dt = rmN (0.9), where rm = 0.32 d 1. Table 1 Dinophysis growth rates used in calculations (see text). Growth rate (1/d)
Species
Authors
0.11 0.22 0.63
Dinophysis acuta Dinophysis acuminata Dinophysis norvegica
Stolte and Garce´s (2006)
0.40 0.45
Dinophysis acuminata Dinophysis caudata
Velo-Sua´rez et al., 2009
0.11 0.23
Dinophysis acuminata Dinophysis acuminata
Tong et al. (2010)
0.47 0.57
Dinophysis acuta Dinophysis acuta
Farrell et al. (2013)
0.10 0.17 0.40
Dinophysis norvegica Dinophysis norvegica Dinophysis norvegica
Gisselson et al. (2002)
3. Results 3.1. Increase in Dinophysis spp. Fig. 2A shows the distribution of Dinophysis counts made between 2006 and 2013. Counts of Dinophysis made in 2013 have been plotted over this envelope providing a graphic illustration of the year’s distribution. It is obvious from Fig. 2A that 2013 had exceptionally high levels of Dinophysis. Indeed a Chi squared test carried out, making the assumption that the 2013 observations should be equally distributed along the median, showed a significant change, x2 = 42.13, p < 0.001 in Dinophysis numbers. Fig. 2B was constructed in a similar way to Fig. 2A. In this case the situation is not quite as visually clear as that in 2013. Nevertheless carrying out a Chi square test, again making the assumption that the 2006 observations should be equally
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Table 2 Chi square values for Dinophysis numbers recorded between 2006 and 2013. When calculating the Chi square value for the whole year 2006, 2007, 2008 and 2010 and 2013 all showed a significant difference in Dinophysis numbers. However when the growth period between May and August was considered only 2006 and 2013 showed a significant change (see text for further explanation). Year
Significant
Higher
2006 2007 2008 2009 2010 2011 2012 2013
x
x
x
Lower
x
x
x
x
x
Chi square 29.57 2.22 33.94 0.12 5.23 2.49 1.66 42.13
distributed along the median, still shows that there was a significant change in the numbers of Dinophysis observed in 2006 relative to the 2006–2013 median, x2 = 29.57, p < 0.001. The results of calculating Chi square tests for each of the years between 2006 and 2013 can be found in Table 2. Although not as large as that found during 2006 and 2013, a significant increase in annual Dinophysis numbers was also observed in 2010. In Shetland the highest numbers of Dinophysis occur in the summer between May and August. A Chi square test carried out on each year for this period reveals that only 2006 and 2013 show a significant increase in Dinophysis numbers relative to the 2006–2013 median.
p < 0.001 p < 0.001 p < 0.05
p < 0.001
Month
Significant
Chi square
May–August May–August May–August May–August May–August May–August May–August May–August
x
8.17 1.31 1.33 2.27 0.55 1.36 0.17 36.5
x
p < 0.01
p < 0.001
while the prevalent wind directions observed in August 2006 were similar to those in 2013, the southerly wind speeds were lower than those in 2013 and represented a smaller percentage of the days during August when the wind blew from the south. This may account for the difference in the Dinophysis densities in the two years (Fig. 2). While the Dinophysis bloom observed during 2013 ended rather abruptly at the end of July, corresponding to the change in wind direction, the bloom observed during 2006 peaked again in August of that year before gradually declining during September and October. 4. Discussion
3.2. Net growth rates Fig. 3 shows the result of plotting the actual numbers of Dinophysis cells counted per litre (solid line) in (A) Braewick Voe, (B) Ronas Voe, (C) Vaila Sound and (D) Busta Voe, Shetland, during July 2013, against the numbers that would be expected, assuming exponential growth of Dinophysis, at these sites (represented by dashed line, exponential growth 1 standard deviation represented by lighter shaded lines). It can be seen that in each case the numbers of Dinophysis observed exceeded the numbers that would be expected. As a comparison the actual numbers of Dinophysis cells counted per litre (solid line) from two additional sites (E) Basta Voe and (F) Dales Voe, both located on the east coast of the Shetland Islands, are also shown. In these two locations the accumulation of Dinophysis is less than that expected from exponential growth. 3.3. Wind Patterns Fig. 5 was produced after constructing a climatology for the period between 2006 and 2013 then extracting the mean prevalent wind directions for June, July and August, shown in diagrams (A), (C) and (E). It can be seen that the mean wind direction for the period is mostly from the South (S) or South, South East (SSE). Any surface water movement induced by wind from this direction would tend to move water northwards towards Shetland from the North Sea. In contrast during 2013 the prevalent wind direction changed dramatically to the West (Fig. 4B, D, F) particularly during June and July (Fig. 4B, D) when the unusually high numbers of Dinophysis were observed. Interestingly, as the wind patterns began to move back towards a more Southerly direction in August (Fig. 4F) the numbers of Dinophysis began to return to more usual densities. Fig. 5 shows the same mean prevalent wind direction observed between 2006 and 2013 at Lerwick, Shetland but in this case it is compared with the mean wind direction observed during June, July and August, 2006 (Fig. 5B, D, F). While the bloom during 2006 did not reach the same densities as that observed during 2013 the increase in numbers of Dinophysis observed was still significant. Again it can be seen that there was a major change in wind direction during June, July and August. It is interesting to note that
It is apparent from Fig. 2 that significantly more Dinophysis was observed in Shetland during 2006 and 2013. Although there appeared to be significant increases in annual Dinophysis numbers during 2007, 2008 and 2010 (see Table 2), these are not reflected in the changes observed during the summer months when numbers of Dinophysis are expected to be at their highest. This appears to be an artefact of the large amount of zero values in the dataset. These tend to accrue towards the beginning and end of the year when Dinophysis is scarce. Occasional observations of Dinophysis cells, albeit in low densities at these times of the year, strongly affect the results of a Chi square test when median values are inevitably zero. Analysis of the data for the period between May and August of each year reveals that only 2006 and 2013 show a significant increase in Dinophysis numbers. The information presented in Fig. 3 suggests that, rather than ideal growing conditions accounting for the rapid increase in Dinophysis numbers, the increase was due in part to some mechanical means. Diaz et al. (2013) found that changes to local wind patterns affected upwelling events offshore and speculate that this increased the availability of suitable prey, sustaining large Dinophysis populations which were then advected into the Galician Rı´as Baixas. The experience from the bays of the west coast of Ireland (Raine et al., 2010) is that rapid increases in Dinophysis numbers are again associated with wind driven water advection. Our analyses suggest a similar process may occur in the voes of Shetland. During 2013 unusual wind patterns were observed during June, July and August that, in contrast to the normally prevalent Southerly winds, blew from the West. Edwards et al. (2006) note that over the last four decades the centre for distribution of Dinophysis in the North Sea has moved eastwards towards the coast of Norway. They also observe that there appears to have been a Northwards shift in the distribution of Dinophysis. In this case it could be expected that the usual southerly winds would advect water from the Eastern side of the North Sea which as Edwards et al. (2006) have observed, now contains relatively fewer cells of Dinophysis. Instead, Westerly winds would advect water originating on the edges of the Faroe-Shetland channel. Smayda and Reynolds (2001), classify Dinophysis as a type VII dinoflagellate life-form, adapted to survive in coastal currents and to grow in
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Fig. 4. A series of wind roses illustrating the mean prevalent wind direction observed during (A) June, (C) July and (E) August between 2006 and 2013 compared with the prevalent wind direction observed during (B) June, (D) July and (F) August 2013 at Lerwick, Shetland. Higher wind speeds are shown by darker shades. The percentage of days during the month when the wind blew from a given direction is represented by the length of the diamond.
weak frontal systems. The conditions to the west of Shetland along the edges of this channel which, experience regular upwelling events, followed by periods of relaxation, could be expected to provide ideal conditions for the growth of Dinophysis.
It is interesting to note that the two sites shown that were located on the East coast of Shetland did not show any great increase in Dinophysis numbers during the same period nor did the rates of accumulation of Dinophysis exceed that predicted by
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Fig. 5. [A series of wind roses illustrating the mean prevalent wind direction observed during 2006]. A series of wind roses illustrating the mean prevalent wind direction observed during (A) June, (C) July and (E) August between 2006 and 2013 compared with the prevalent wind direction observed during (B) June, (D) July and (F) August 2006 at Lerwick, Shetland. Higher wind speeds are shown by darker shades. The percentage of days during the month when the wind blew from a given direction is represented by the length of the diamond.
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exponential growth. This conclusion is given strength by the observations made during the summer of 2006, when unusually high numbers of Dinophysis were again accompanied by a change in the prevailing winds from South to West. The changes in Dinophysis distribution reported by Edwards et al. (2006) appear to be related to higher temperatures during winter. A similar change has been found by Wasmund et al. (1998). Working in the Baltic Sea, they observed a change from diatom to dinoflagellate dominance and also connected this to milder winters. Given that dinoflagellates make up the biggest proportion of toxic algae, rising sea temperatures could have serious consequences for outbreaks of harmful algal blooms around our coasts. These impacts will only be acerbated by changes in the prevalent wind patterns. Evidence that winds in the North Sea are becoming stronger and that they increasingly have a west or southwesterly component is growing (Siegismund and Schrum, 2001; Brown, 2009; Christensen et al., 2007). Large scale bipolar patterns such as the NAO are known to influence both the speed and the direction of winds in the North East Atlantic and the North Sea (Phillips et al., 2013) and as these are positively linked with climate change (Gillett et al., 2003) the incidence of changing wind patterns in Shetland may be set to increase and with them the possibility of more prevalent bio-toxic events connected to those species such as Karenia mikimotoi (Davidson et al., 2009), and Dinophysis spp. that are influenced by Westerly, wind advected currents. Predicting harmful algal blooms is fraught with difficulties. Rigorous monitoring is still the safest way to ensure that consumers can eat shellfish with confidence and without worrying about food poisoning. However, as the recent event in London illustrates, the possibility for contaminated shellfish to enter the food supply still exists. Models, such as those developed in the EU project ASIMUTH (ASIMUTH, 2014), that predict harmful algal blooms are gaining in accuracy and sophistication, although there is no room for complacency. As the frequency of harmful algal blooms around the globe is perceived to be on the increase, and as the levels of investment in aquaculture rise, an understanding of their underlying causes, accompanied by tools to help mitigate their impact is more important than ever. Competing interests None. Authors contributions CW has contributed in generation of data, analysis and paper writing. SS has contributed in generation of data and paper writing. KD has contributed in analysis and paper writing. Author’s information For the past nine years SS has been the manager of the monitoring programme for the presence of toxin producing plankton in shellfish production areas in Scotland. Her interests lie in the distribution and development of harmful algal blooms and the taxonomy of potentially toxic phytoplankton. KD is the head of the Microbial and Molecular Biology Department at the Scottish Association for Marine Science. His current interests lie in the processes governing the initiation of harmful algal blooms and the influences that bathymetry and physical drivers play in phytoplankton distribution and productivity. CW is a member of the Department of Microbial and Molecular Biology and deputy manager of the monitoring programme for the
presence of toxin producing plankton in Scottish shellfish production areas. His research interests lie in phytoplankton ecology; specifically those few species that produce bio-toxins. He is trying to understand the drivers that lead to blooms of harmful algae, with the eventual goal of developing tools and methods that help to identify and predict their occurrence. Acknowledgements The authors would like to acknowledge the NERC PURE research programme and the EU FP7 project ASIMUTH who supplied the funding for this study. They would like to thank the following for their assistance in identifying and enumerating the phytoplankton samples: Deborah Brennan, Christine Campbell, Eilidh Cole, Joanne Fielding, Sharon McNeill, Elaine Mitchell and Rachel Saxon. They would also like to thank the British Atmospheric Data Centre and the Food Standards Agency for the generous use of their data.[TS]
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Harmful Algae journal homepage: www.elsevier.com/locate/hal
Changing wind patterns linked to unusually high Dinophysis blooms around the Shetland Islands, Scotland Callum Whyte *, Sarah Swan 1,2, Keith Davidson 1,2 Microbial and Molecular Biology Department, Scottish Association for Marine Science, Scottish Marine Institute, Oban, Argyll PA37 1QA, United Kingdom
A R T I C L E I N F O
A B S T R A C T
Article history: Received 9 May 2014 Received in revised form 16 September 2014 Accepted 17 September 2014 Available online
During the summer of 2013, 70 people received Diarrhetic Shellfish Poisoning following consumption of mussels harvested in the Shetland Islands, Scotland. At this time, large numbers of the biotoxinproducing phytoplankton genus Dinophysis was observed around the Shetland Islands. Analysis indicated this increase was not due to in situ growth but coincided with a change in the prevalent wind direction. A previous large bloom of Dinophysis during 2006 also coincided with a similar change in the prevalent wind patterns. Wind direction and speed in the North East Atlantic and the North Sea is strongly influenced by the North Atlantic oscillation (NAO) with a positive relationship between it and wind direction. It has been noted that a positive trend in the NAO is linked to climate change and predictions suggest there will be an increasingly westward component to prevalent wind directions in the North Sea which could lead to an increase in the occurrence of these harmful algal blooms. Analysis of wind patterns therefore offers a potential method of early warning of future bio-toxicity events. ß 2014 Published by Elsevier B.V.
Keywords: Dinophysis Harmful algal bloom Dinophysistoxins Advection Wind pattern Shetland Islands
1. Background In July 2013 there was an outbreak of Diarrhetic Shellfish Poisoning (DSP) in the South East of England. Although it is not known how many people were actually affected, 70 people sought medical advice after consuming mussels which, they had been served in several prominent restaurants in London. They were later found to be suffering the symptoms of DSP. The shellfish had been supplied by a farm in the coastal waters of the Shetland Islands (Fig. 1). Although the numbers of Dinophysis had been slowly increasing during the preceding few weeks, analysis did not indicate that the concentration of toxins in the shellfish was high. However three days after the farmer had harvested the shellfish an unusually high level of toxins was detected by the Food Standards Agency (FSA) weekly monitoring programme (FSA, 2013), accom-
Abbreviations: ASIMUTH, Applied Simulations and Integrated Modelling for the Understanding of Toxic and Harmful Algal Blooms; BADC, British Atmospheric Data Centre; DSP, Diarrhetic Shellfish Poisoning; DTX (1–3), dinophysistoxins; GDP, Gross Domestic Product; FSA, Food Standards Agency; NAO, North Atlantic Oscillation; OA, okadaic acid; SAMS, Scottish Association for Marine Science. * Corresponding author. Tel.: +44 01631 559 226. E-mail addresses: [email protected], [email protected] (C. Whyte), [email protected] (S. Swan), [email protected] (K. Davidson). 1 These authors contributed equally to this work. 2 Tel: +44 01631 559 226. http://dx.doi.org/10.1016/j.hal.2014.09.006 1568-9883/ß 2014 Published by Elsevier B.V.
panied by a very rapid accumulation of Dinophysis cells. The area was closed and commercial harvesting was suspended, unfortunately too late for the luckless consumers of the affected mussels. This paper investigates the possibility that the unusually large blooms of Dinophysis observed around the coast of Shetland during 2013, and another large bloom event during 2006, were not due to high in situ growth rates, but rather to changes in the annual pattern of prevalent wind direction. We discuss the possibility that an analysis of wind patterns could be used to provide an early warning of biotoxic events. Yasumoto et al. (1980) was among the first to suggest that gastro-intestinal pain, accompanied by diarrhoea, nausea and vomiting, following the consumption of mussels (Mytilus edulis) was linked to the presence of dinoflagellates in the water column, in particular Dinophysis fortii. This link was confirmed after outbreaks of severe gastro-intestinal shellfish poisoning in Japan during 1976 and 1977 and led to the identification of a new set of toxins associated with the genus Dinophysis (Reguera et al., 2012). Identified as Diarrhetic Shellfish Poisoning (DSP) causative toxins, these lipophilic compounds are comprised principally of Okadaic Acid (OA) and its derivatives DTX-1, DTX-2 and DTX-3 (Smayda, 2006; Taylor et al., 2013). They have been found to bind with protein phosphatase receptors in the body, leading to an accumulation of phosphorylated proteins with symptoms of lethargy, general weakness, vomiting, cramps and diarrhoea,
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symptoms that can appear from 30 min to several hours after ingestion of the contaminated shellfish (Gerssen et al., 2010). The Dinophysis species most commonly found in Scottish waters are D. acuminata, D. acuta, and D. norvegica, all of which have been confirmed to produce toxins with particular emphasis on D. acuminata and D. acuta (Bresnan et al., 2005; Hart et al., 2007). While contamination of both farmed and wild shellfish by OA and DTX’s is sporadic, it is widespread and has been reported from eleven countries across Europe including Denmark, France, Germany, Ireland, Italy, Norway, Portugal, Spain, Sweden and the Netherlands (Smayda, 2006). Perhaps the severest outbreak occurred in Spain during 1981 when an outbreak of DSP affected approximately 5000 people, mostly from Madrid (Fraga et al., 1984, 1988; Gestal-Otero, 2000). While unrecorded cases are likely to have occurred, the first reliable record of Diarrhetic Shellfish Poisoning in the UK was in 1997 when 49 people became ill after eating shellfish in two London restaurants (Hinder et al., 2011; Scoging and Bahl, 1998). Since then the frequency of closures due to DSP around the UK appears to be increasing. This may simply be due to a better understanding of the underlying causes of shellfish poisoning, a greater awareness of the problem and a more rigorous monitoring programme. Unlike some species of harmful algae, Dinophysis does not need to be present in large numbers to cause toxicity in shellfish. A few hundred cells/l can be enough to lead to the closure of a harvesting area. In 2000, DSP toxins were found in shellfish in areas on the East coast of Scotland, Orkney, the Outer Hebrides, the Shetland Islands and the Firth of Clyde. In all, closures of the various shellfish harvesting areas amounted to 24 weeks (Howard et al., 2001). In 2002, DSP toxins were found throughout Scotland with the majority of the closures lasting between four to six weeks, although some areas were closed for up to seven months. Between 2008 and 2009, thirteen areas were closed in the Shetland Islands and seven areas in Argyll and Bute (Hinder et al., 2011) and most recently, large areas of Shetland were closed for several weeks during 2013. In addition to the extremely distressing effects contaminated shellfish can have on anyone who consumes them, a DSP outbreak can have far reaching consequences for the shellfish industry. While there is an obvious detrimental effect on farmers, processors and distributors, the impact can extend well outside the closed harvesting area. In what is sometimes referred to as a ‘‘halo’’ effect (Rural Affairs Committee, 1999) consumer confidence is often lost, not only in the closed fishery, but in shellfish products in general, regardless of the area where they were harvested. This loss of confidence can easily outlast the closure itself and, as much of Scotland’s production is destined for overseas markets, can have serious economic impacts for the country’s GDP (Rural Affairs Committee, 1999). DSP events are particularly damaging to aquaculture in the South West of Ireland, an area responsible for 80% of the rope grown blue mussel (Mytilus edulis) and 50% of the pacific oyster (Crassostrea gigas) cultivated in Ireland. Production in this area suffers from a history of harmful algal events; often closing the area for months at a time (Raine et al., 2010). The frequency of shellfish harvesting area closures due to DSP events in Southern Ireland, particularly in the large bays of Bantry, Dunmanus and Long Island, would suggest that these areas are particularly suited for the growth of Dinophysis. However the hydro-dynamic processes, in particular, the exchange of substantial fractions of the bay volume during thermal stratification, present in these bays suggests that they are unsuited to the development of indigenous phytoplankton populations (Raine et al., 2010). Instead, it is believed to be wind driven water exchange between the Irish coast and the continental shelf that is responsible for these events (Raine et al., 2010). Similarly, Escalera et al. (2010) have confirmed that
accumulations of Dinophysis species in Galician rı´as during October and November were due not to intrinsic growth but to physical transport from other areas. In Scottish waters Dinophysis are widely distributed, usually in low numbers (Tett and Edwards, 2002; Davidson and Bresnan, 2009) and are generally found in offshore waters. Once advected onshore, however, they can accumulate in semi-enclosed areas where in the right conditions they may thrive. Given their widespread distribution, outbreaks of DSP can occur almost anywhere around the Scottish coast. Responsible for 54% of the mussel production in Scotland with 105 businesses involved in shellfish production (Shetland in Statistics, 2011), Shetland plays an important role in the Scottish economy. Given its geographical location and its topography, comprised of numerous fjords and embayments, it provides an ideal environment for shellfish aquaculture. However, as the closures due to an exceptionally large bloom of Dinophysis experienced during the summer of 2013 illustrate, it is also vulnerable to blooms of these harmful algae. The Scottish Government has called for an increase in shellfish production from 6,525 tonnes in 2012 to a proposed 13,000 tonnes by 2020. It is important therefore to understand the mechanism underlying this unusual event and try to estimate its likelihood of recurrence. 2. Methods Following the FSA guidelines, seawater samples integrated over a depth of 10 m were collected by Lund tube as part of the FSA phytoplankton monitoring programme for Scottish waters. The samples were gently mixed and 500 ml sub-samples transferred to brown, Nalgene bottles and immediately treated with acidified Lugol’s solution to obtain a final concentration of 1% by volume. Samples were collected weekly from nine distinct sites around Shetland between April and October. From November to March the frequency of sampling was reduced to one sample per month. After collection, these samples were sent to the Scottish Association for Marine Science (SAMS) where 50 ml aliquots were settled using the Utermo˝ hl sedimentation method as outlined in Lund et al. (1958). Following FSA protocols the phytoplankton was allowed to settle for a minimum of 20 h before examination. Full chamber counts at 200 magnification were carried out using Carl Zeiss Axiovert inverted microscopes. While regulatory biotoxin phytoplankton surveillance and monitoring has occurred in Scotland since 1991, early sampling was spatially and temporally variable. However, since 2006 a more structured collection regime has been used, with FSA-funded sampling officers collecting waters samples from designated representative monitoring points within classified shellfish production areas. Hence, to determine whether the number of Dinophysis cells recorded in Shetland during 2013 had changed significantly, a plot of all the Dinophysis counts made between 2006 and 2013 was created. The median was calculated for each day of the year between 2006 and 2013 and was drawn onto this plot (see Fig. 2 solid line) along with the 5th and 95th percentiles. These are represented in the figure by the dashed lines and form an envelope encompassing 90% of the observations made. The individual datum points have been omitted for clarity. Counts of Dinophysis recorded during 2013 were then plotted against this median and a Chi square test was performed, making the assumption that values recorded during 2013 would be equally distributed around the median. Using the same envelope for counts made between 2006 and 2013 this method was used to investigate Dinophysis counts made during 2006 (see Fig. 3). Active phytoplankton growth in Scottish waters occurs mostly between spring and autumn when light, water temperature and nutrients are sufficient (Davidson et al., 2011). As the monitoring
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Fig. 1. Map of location showing sampling sites mentioned in the text.
summer counts, making them appear more significant than they are. To counter this, counts were transformed using Log10(X + 0.5z), where X = the number of Dinophysis cells counted and z = the detection limit, in this case 20 cells/l. To ascertain wind direction, data were downloaded from the British Atmospheric Data Centre (BADC) (BADC, 2012) for Lerwick, Shetland (BADC station identifier src-id 9). The BADC provided hourly wind direction and wind speed for each day of the year. These data were then averaged to obtain a mean daily scalar wind speed and direction for each year between 2006 and 2013. A ‘‘climatology’’ was then created by calculating the mean values for each day of the year between 2006 and 2013. To generate the monthly wind roses these mean daily values were binned into sixteen 22.5 degree bins and plotted in Microsoft Excel. 2.1. Growth rates
Fig. 2. (A) Dinophysis counts recorded in Shetland during 2013 (circles) plotted against median values of Dinophysis recorded in Shetland between 2006 and 2013 (solid black line). Dashed lines represent the 5th and 95th percentiles of the data collected between 2006 and 2013. (B) Dinophysis counts recorded in Shetland during 2006 (circles) plotted against median values of Dinophysis recorded in Shetland between 2006 and 2013 (solid black line). Dashed lines represent the 5th and 95th percentiles of the data collected between 2006 and 2013.
programme takes place throughout the year, albeit at a reduced frequency during the winter months, many of the observations made in the early and late parts of the year consist of zero counts. This has the tendency to drag the median down and can bias
Any significant changes in the number of Dinophysis recorded could potentially be due to natural, inter-annual differences in growth rates. In situ and cultured growth rates for Dinophysis species grown at different temperatures vary widely in the literature. In an attempt to choose a realistic value, only those growth rates found from in situ studies involving those species of Dinophysis growing in Scottish waters and at the temperatures found in the waters around Shetland were used. To estimate the exponential growth rates of Dinophysis around Shetland, a mean value of 0.32 d 1 calculated from the values shown in Table 1 was used. In situ growth rates cover a wide range of values and the value chosen can have a marked effect on the outcome. To address this, growth rates were also calculated for one standard deviation from the mean. As with growth rates, loss rates can also vary widely in the literature. Zhai et al. (2010) working in the North-west Atlantic calculated loss rates between 10% and 60%, while Kozlowsky-Suzuki et al., 2006 estimated 25% losses from copepod grazing in the Baltic Sea. Again taking a conservative approach, the lowest of these loss rates, i.e. 10% was chosen. Dinophysis is a mixotroph, requiring light, nutrients and live prey to thrive. Unfortunately, suitable data on nutrient levels, irradiance and the availability of prey that would allow a detailed growth model to be constructed for the sites in question were not available. Nevertheless taking a conservative approach, and assuming idyllic growth conditions existed at the sites, a simple
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Fig. 3. Dinophysis numbers recorded at (A) Braewick Voe, (B) Ronas Voe, (C) East of Linga and (D) Busta Voe, Shetland during July and August 2013 (solid line) plotted alongside the numbers of Dinophysis that would be expected from a simple exponential growth model with 10% losses (dashed line). The exponential growth rates for one standard deviation are represented by the lighter shaded lines. Diagrams (E) Basta Voe Cove and (F) Scarvar Ayre, both located on the East coast of Shetland, are shown as a comparison.
model of exponential growth with 10% losses was used to predict the numbers of Dinophysis (N) that could be expected to be present during the bloom, i.e. dN/dt = rmN (0.9), where rm = 0.32 d 1. Table 1 Dinophysis growth rates used in calculations (see text). Growth rate (1/d)
Species
Authors
0.11 0.22 0.63
Dinophysis acuta Dinophysis acuminata Dinophysis norvegica
Stolte and Garce´s (2006)
0.40 0.45
Dinophysis acuminata Dinophysis caudata
Velo-Sua´rez et al., 2009
0.11 0.23
Dinophysis acuminata Dinophysis acuminata
Tong et al. (2010)
0.47 0.57
Dinophysis acuta Dinophysis acuta
Farrell et al. (2013)
0.10 0.17 0.40
Dinophysis norvegica Dinophysis norvegica Dinophysis norvegica
Gisselson et al. (2002)
3. Results 3.1. Increase in Dinophysis spp. Fig. 2A shows the distribution of Dinophysis counts made between 2006 and 2013. Counts of Dinophysis made in 2013 have been plotted over this envelope providing a graphic illustration of the year’s distribution. It is obvious from Fig. 2A that 2013 had exceptionally high levels of Dinophysis. Indeed a Chi squared test carried out, making the assumption that the 2013 observations should be equally distributed along the median, showed a significant change, x2 = 42.13, p < 0.001 in Dinophysis numbers. Fig. 2B was constructed in a similar way to Fig. 2A. In this case the situation is not quite as visually clear as that in 2013. Nevertheless carrying out a Chi square test, again making the assumption that the 2006 observations should be equally
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Table 2 Chi square values for Dinophysis numbers recorded between 2006 and 2013. When calculating the Chi square value for the whole year 2006, 2007, 2008 and 2010 and 2013 all showed a significant difference in Dinophysis numbers. However when the growth period between May and August was considered only 2006 and 2013 showed a significant change (see text for further explanation). Year
Significant
Higher
2006 2007 2008 2009 2010 2011 2012 2013
x
x
x
Lower
x
x
x
x
x
Chi square 29.57 2.22 33.94 0.12 5.23 2.49 1.66 42.13
distributed along the median, still shows that there was a significant change in the numbers of Dinophysis observed in 2006 relative to the 2006–2013 median, x2 = 29.57, p < 0.001. The results of calculating Chi square tests for each of the years between 2006 and 2013 can be found in Table 2. Although not as large as that found during 2006 and 2013, a significant increase in annual Dinophysis numbers was also observed in 2010. In Shetland the highest numbers of Dinophysis occur in the summer between May and August. A Chi square test carried out on each year for this period reveals that only 2006 and 2013 show a significant increase in Dinophysis numbers relative to the 2006–2013 median.
p < 0.001 p < 0.001 p < 0.05
p < 0.001
Month
Significant
Chi square
May–August May–August May–August May–August May–August May–August May–August May–August
x
8.17 1.31 1.33 2.27 0.55 1.36 0.17 36.5
x
p < 0.01
p < 0.001
while the prevalent wind directions observed in August 2006 were similar to those in 2013, the southerly wind speeds were lower than those in 2013 and represented a smaller percentage of the days during August when the wind blew from the south. This may account for the difference in the Dinophysis densities in the two years (Fig. 2). While the Dinophysis bloom observed during 2013 ended rather abruptly at the end of July, corresponding to the change in wind direction, the bloom observed during 2006 peaked again in August of that year before gradually declining during September and October. 4. Discussion
3.2. Net growth rates Fig. 3 shows the result of plotting the actual numbers of Dinophysis cells counted per litre (solid line) in (A) Braewick Voe, (B) Ronas Voe, (C) Vaila Sound and (D) Busta Voe, Shetland, during July 2013, against the numbers that would be expected, assuming exponential growth of Dinophysis, at these sites (represented by dashed line, exponential growth 1 standard deviation represented by lighter shaded lines). It can be seen that in each case the numbers of Dinophysis observed exceeded the numbers that would be expected. As a comparison the actual numbers of Dinophysis cells counted per litre (solid line) from two additional sites (E) Basta Voe and (F) Dales Voe, both located on the east coast of the Shetland Islands, are also shown. In these two locations the accumulation of Dinophysis is less than that expected from exponential growth. 3.3. Wind Patterns Fig. 5 was produced after constructing a climatology for the period between 2006 and 2013 then extracting the mean prevalent wind directions for June, July and August, shown in diagrams (A), (C) and (E). It can be seen that the mean wind direction for the period is mostly from the South (S) or South, South East (SSE). Any surface water movement induced by wind from this direction would tend to move water northwards towards Shetland from the North Sea. In contrast during 2013 the prevalent wind direction changed dramatically to the West (Fig. 4B, D, F) particularly during June and July (Fig. 4B, D) when the unusually high numbers of Dinophysis were observed. Interestingly, as the wind patterns began to move back towards a more Southerly direction in August (Fig. 4F) the numbers of Dinophysis began to return to more usual densities. Fig. 5 shows the same mean prevalent wind direction observed between 2006 and 2013 at Lerwick, Shetland but in this case it is compared with the mean wind direction observed during June, July and August, 2006 (Fig. 5B, D, F). While the bloom during 2006 did not reach the same densities as that observed during 2013 the increase in numbers of Dinophysis observed was still significant. Again it can be seen that there was a major change in wind direction during June, July and August. It is interesting to note that
It is apparent from Fig. 2 that significantly more Dinophysis was observed in Shetland during 2006 and 2013. Although there appeared to be significant increases in annual Dinophysis numbers during 2007, 2008 and 2010 (see Table 2), these are not reflected in the changes observed during the summer months when numbers of Dinophysis are expected to be at their highest. This appears to be an artefact of the large amount of zero values in the dataset. These tend to accrue towards the beginning and end of the year when Dinophysis is scarce. Occasional observations of Dinophysis cells, albeit in low densities at these times of the year, strongly affect the results of a Chi square test when median values are inevitably zero. Analysis of the data for the period between May and August of each year reveals that only 2006 and 2013 show a significant increase in Dinophysis numbers. The information presented in Fig. 3 suggests that, rather than ideal growing conditions accounting for the rapid increase in Dinophysis numbers, the increase was due in part to some mechanical means. Diaz et al. (2013) found that changes to local wind patterns affected upwelling events offshore and speculate that this increased the availability of suitable prey, sustaining large Dinophysis populations which were then advected into the Galician Rı´as Baixas. The experience from the bays of the west coast of Ireland (Raine et al., 2010) is that rapid increases in Dinophysis numbers are again associated with wind driven water advection. Our analyses suggest a similar process may occur in the voes of Shetland. During 2013 unusual wind patterns were observed during June, July and August that, in contrast to the normally prevalent Southerly winds, blew from the West. Edwards et al. (2006) note that over the last four decades the centre for distribution of Dinophysis in the North Sea has moved eastwards towards the coast of Norway. They also observe that there appears to have been a Northwards shift in the distribution of Dinophysis. In this case it could be expected that the usual southerly winds would advect water from the Eastern side of the North Sea which as Edwards et al. (2006) have observed, now contains relatively fewer cells of Dinophysis. Instead, Westerly winds would advect water originating on the edges of the Faroe-Shetland channel. Smayda and Reynolds (2001), classify Dinophysis as a type VII dinoflagellate life-form, adapted to survive in coastal currents and to grow in
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Fig. 4. A series of wind roses illustrating the mean prevalent wind direction observed during (A) June, (C) July and (E) August between 2006 and 2013 compared with the prevalent wind direction observed during (B) June, (D) July and (F) August 2013 at Lerwick, Shetland. Higher wind speeds are shown by darker shades. The percentage of days during the month when the wind blew from a given direction is represented by the length of the diamond.
weak frontal systems. The conditions to the west of Shetland along the edges of this channel which, experience regular upwelling events, followed by periods of relaxation, could be expected to provide ideal conditions for the growth of Dinophysis.
It is interesting to note that the two sites shown that were located on the East coast of Shetland did not show any great increase in Dinophysis numbers during the same period nor did the rates of accumulation of Dinophysis exceed that predicted by
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Fig. 5. [A series of wind roses illustrating the mean prevalent wind direction observed during 2006]. A series of wind roses illustrating the mean prevalent wind direction observed during (A) June, (C) July and (E) August between 2006 and 2013 compared with the prevalent wind direction observed during (B) June, (D) July and (F) August 2006 at Lerwick, Shetland. Higher wind speeds are shown by darker shades. The percentage of days during the month when the wind blew from a given direction is represented by the length of the diamond.
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exponential growth. This conclusion is given strength by the observations made during the summer of 2006, when unusually high numbers of Dinophysis were again accompanied by a change in the prevailing winds from South to West. The changes in Dinophysis distribution reported by Edwards et al. (2006) appear to be related to higher temperatures during winter. A similar change has been found by Wasmund et al. (1998). Working in the Baltic Sea, they observed a change from diatom to dinoflagellate dominance and also connected this to milder winters. Given that dinoflagellates make up the biggest proportion of toxic algae, rising sea temperatures could have serious consequences for outbreaks of harmful algal blooms around our coasts. These impacts will only be acerbated by changes in the prevalent wind patterns. Evidence that winds in the North Sea are becoming stronger and that they increasingly have a west or southwesterly component is growing (Siegismund and Schrum, 2001; Brown, 2009; Christensen et al., 2007). Large scale bipolar patterns such as the NAO are known to influence both the speed and the direction of winds in the North East Atlantic and the North Sea (Phillips et al., 2013) and as these are positively linked with climate change (Gillett et al., 2003) the incidence of changing wind patterns in Shetland may be set to increase and with them the possibility of more prevalent bio-toxic events connected to those species such as Karenia mikimotoi (Davidson et al., 2009), and Dinophysis spp. that are influenced by Westerly, wind advected currents. Predicting harmful algal blooms is fraught with difficulties. Rigorous monitoring is still the safest way to ensure that consumers can eat shellfish with confidence and without worrying about food poisoning. However, as the recent event in London illustrates, the possibility for contaminated shellfish to enter the food supply still exists. Models, such as those developed in the EU project ASIMUTH (ASIMUTH, 2014), that predict harmful algal blooms are gaining in accuracy and sophistication, although there is no room for complacency. As the frequency of harmful algal blooms around the globe is perceived to be on the increase, and as the levels of investment in aquaculture rise, an understanding of their underlying causes, accompanied by tools to help mitigate their impact is more important than ever. Competing interests None. Authors contributions CW has contributed in generation of data, analysis and paper writing. SS has contributed in generation of data and paper writing. KD has contributed in analysis and paper writing. Author’s information For the past nine years SS has been the manager of the monitoring programme for the presence of toxin producing plankton in shellfish production areas in Scotland. Her interests lie in the distribution and development of harmful algal blooms and the taxonomy of potentially toxic phytoplankton. KD is the head of the Microbial and Molecular Biology Department at the Scottish Association for Marine Science. His current interests lie in the processes governing the initiation of harmful algal blooms and the influences that bathymetry and physical drivers play in phytoplankton distribution and productivity. CW is a member of the Department of Microbial and Molecular Biology and deputy manager of the monitoring programme for the
presence of toxin producing plankton in Scottish shellfish production areas. His research interests lie in phytoplankton ecology; specifically those few species that produce bio-toxins. He is trying to understand the drivers that lead to blooms of harmful algae, with the eventual goal of developing tools and methods that help to identify and predict their occurrence. Acknowledgements The authors would like to acknowledge the NERC PURE research programme and the EU FP7 project ASIMUTH who supplied the funding for this study. They would like to thank the following for their assistance in identifying and enumerating the phytoplankton samples: Deborah Brennan, Christine Campbell, Eilidh Cole, Joanne Fielding, Sharon McNeill, Elaine Mitchell and Rachel Saxon. They would also like to thank the British Atmospheric Data Centre and the Food Standards Agency for the generous use of their data.[TS]
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