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Climate Influence on Toxin-Producing Alexandrium in Scottish Waters

This study examines the diversity of toxin-producing Alexandrium species in Scottish waters and investigates the potential influence of climate on toxin production. The aim is to understand the complexity of toxic events and provide valuable information for shellfish monitoring and management.

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Climate Influence on Toxin-Producing Alexandrium in Scottish Waters

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  1. Diversity of toxin producing Alexandrium in Scottish waters – is climate influencing toxin producing populations? Liz Turrell *turrelle@marlab.ac.uk www.frs-scotland.gov.uk

  2. 1990s - shellfish harvesting site closures 5000 • Late 90’s to 2005 - Decrease in mussel PSP toxin concentrations • 2004 - No PSP closures • Overall reduction in the number of closures of shellfish monitoring sites due to PSP toxins 4000 3000 PSP toxins (µg STX equiv 100 g-1 shellfish) 2000 1000 Regulatory limit (>80 µg STX equiv 100 g-1 shellfish) 0 0 1 2 3 4 5 6 7 0 1 2 3 4 5 6 7 8 9 0 0 0 0 0 0 0 0 9 9 9 9 9 9 9 9 9 9 0 0 0 0 0 0 0 0 9 9 9 9 9 9 9 9 9 9 2 2 2 2 2 2 2 2 1 1 1 1 1 1 1 1 1 1 Y e a r PSP toxins in Scottish waters decreasing

  3. Stonehaven 4000 Scalloway 8000 3000 6000 2000 4000 1000 2000 0 0 1997 1999 2001 2003 2005 2007 1997 1999 2001 2003 2005 2007 Alexandrium in Scottish waters are variable 8000 Scapa 24,000 cells L-1 6000 Alexandrium cells L-1 4000 2000 0 1997 1999 2001 2003 2005 2007 • Large inter-annual variability in numbers of Alexandrium cells • PSP toxin concentrations decreasing but a concurrent decrease in Alexandrium not observed • Historically, northern (Scotland, Faroe) populations of Alexandrium considered toxic – why are we observing decreasing toxicity…? Year

  4. To understand the complexity of toxic events … • Require knowledge on distribution of Alexandrium species • Information on toxicity of Alexandrium populations • PSP toxins • Spirolides (SPXs) • Project to … • Sample Scottish coastal waters/sediments to isolate single cells and establish cultures • Identify cultures to species level using taxonomic techniques • Identify regional/strain differences using molecular techniques • Determine ability of Scottish isolates of Alexandrium to produce PSP toxins and SPXs

  5. Scapa Isolation and culturing of Alexandrium • Sediment and water samples collected • Cysts and cells isolated • Cysts incubated at 10 & 15 °C to mimic seawater temperatures • Approx 30 viable cultures Stonehaven

  6. Staining - four species

  7. Apical pore 1st apical plate Large Pore Staining - four species A. tamarense A. tamutum Sulcal plate A. ostenfeldii 1st apical plate A. minutum Pore

  8. Sequencing – four species, two strains

  9. Confirmation of species: Sequences A. tamarense Maximum-likelihood tree based on LSU rDNA Japan OFO41; OF151, A. tamarense Korea SJW97046 D1-D2 type G, A. tamarense Japan AT-9; HAT4; OF8442303A. tamarense KoreaSJW97043D1-D2 type D A. tamarense KoreaULW9903 D1-D2 type B; UL7 D1-D2 type BA. tamarense KoreaULW9903 D1-D2 type A; UL7 D1-D2 type A, A. tamarense KoreaSJW97046 D1-D2 type A,A. tamarense KoreaSJW97043 D1-D2 type A A. tamarense KoreaKJC97111 D1-D2 type E; BSW97A. tamarense KoreaKJC97111 D1-D2 type A; YOC98a, A. tamarense KoreaULW9903; SSW0006-7A. tamarense KoreaSJW0003-11; JDW0004-13A. tamarense FaroesK-0055 A. tamarense 100 North American Note: cysts hatched at 10 °C KoreaJHW0003-2 A. tamarense Scotland 04-197-30; 04-197-A1 A. tamarense Scotland Shetland A, A. tamarense UK Orkney9; Orkney12 A. tamarense Japan AX-03 A. tamarense Korea SJC95b; SJW9704-6; HYP970328MA. tamarense Newfoundland AFNFA3.1 A. fundyense 97 UK Orkney1 A. tamarense UK UW4-1; Alex61-2A. tamarense 87 Newfoundland AFNFA3.2 A. fundyense Scotland Shetland B, A. tamarense UK Orkney11;Alex61-1; UW4-2,A. tamarense Korea SJW9704-15; HAT4 D1-D2 type H A. tamarense UK Orkney7 A. tamarense USA PW06 A.tamarense Italy SZN21 A. tamarense 100 Mediterranean Italy SZN08 A. tamarense Italy SZN19 A. tamarense Italy SZN01A. tamarense ScotlandA. tamarense (7) UK ATFE7 A. tamarense UK ATFE6 A. tamarense 100 Ireland Alex 35.3; 35.9 A. tamarense UK Pgt183 A. tamarense UK 173 A. tamarense Western European Note: cysts hatched at 15 °C, but not at 10 °C 100 Ireland Alex31.6 A. tamarense UK AlexW1; W2 A. tamarense UK AlexW10; W11 A. tamarense Ireland Alex31.5 A. tamarense China HK ALEXSPHK A. tamarense China HK ATHK A. tamarense UK AlexW12 A. tamarense UK AlexW7 A. tamarense China HK ATCI01-1A. tamarense Ireland Alex35.2; 35.3; 35.4A. tamarense Australia ACPP01; ACWL01; ACNC50A. catenella Ireland Alex31.4 A. tamarense New Zealand CAWD121 A. tamarense Ireland Alex31.1 A. tamarense Tasmania ACGB01A. catenella Ireland UW53 A. tamarense KoreaSJW0007-7A. catenella Temperate Asian Ireland UW42 A. tamarense KoreaKMC98aA. catenella UK Pgt183 A. tamarense Ireland CCAP 1119/9 A. tamarense KoreaDPC95a; DPC95b; DPC95cA. catenella Spain BAHME215; BAHME217 A. catenella 100 Spain BAHME222 A. catenella Korea CMC98b; SJW0007-8, A. catenella 99 Korea ATTKO01 A. tamarense Tasmania ATBB01 A. tamarense 100 Tasmanian Japan At304A A. tamarense Tasmania ATNWB01 A. tamarense Tasmania ATEB01 A. tamarense Thailand CU-13; CU-15, A. tropicale

  10. A. andersonii AY962833 GTTC02 USA A. minutum AY962855 TML-42 Taiwan A. minutum AY962850 AMTK-1 Taiwan A. minutum AY566187 AmKB06 AY566186 AmKB03 AY566185 AmKB01 Malaysia 60 A. minutum DQ287855 AMTK4 DQ287854 AMKS5 DQ287853 AMKS1 Hong Kong; DQ287851 AMTK7 Taiwan; DQ176657 AM China 100 A. minutum AY962854 CAWD13 AY962853 CAWD12 AY962852 CAWD11 New Zealand A. minutum AY962847 AMBOP014 New Zealand A. minutum AY962846 AMBOP006 New Zealand A. minutum AY268598 AMNZ03 AY268596 AMNZ01 New Zealand 63 A. minutum AY338751 CAWD13 New Zealand 73 A. minutum AF033532 Anakoha Bay New Zealand A. minutum AY962849 AMIR-3 AY962848 AMIR-1 Ireland A. minutum AY962845 AM3 AY962844 AM2 AY962843 AM1 France; AY962842 LAC27 AY962841 AT4 AY962840 AL9T AY962839 AL8T AY962838 AL5T Italy; AY962837 AL2V Spain A. minutum AY962835 AL1T Italy A. minutum DQ453524 AMCTW8 DQ453523 AMCTW6 DQ453522 AMCTW1 South Africa A. minutum A. minutum AY705869 3.9h England 100 A. minutum AF318231 X13 France A. minutum AF318221 AM89BM X10 France A. minutum AY294613 GHmin04 Denmark A. minutum S06/020/01 W07/001/01 Scotland; U44936 AMAD06 Australia; AJ535360 AL9T Italy A. minutum AF318264 95/4 France 64 A. minutum AF318263 95/1 AF318262 91/2 France A. minutum AF318232 X20 France 71 A. minutum AF318222 AM99PZ X9 France A. tamutum AJ535372 SZN29 AJ535373 SNZ28 Italy A. minutum/A. tamutum AY962836 AL2T Italy 86 80 A. tamutum AJ535354 A8/1 AJ535366 AT5 AJ535367 AT3 Italy A. tamutum AY268617 A5t AY268618 C7-2 97 A. tamutum AY962863 AT5 AY962864 AB/2 Italy A. tamutum A. tamutum AY962865 C7/2 Italy A. tamutum S07/036/01 Scotland A. tamutum AY268616 At3 Italy 86 A. tamutum AY962862 AT3 Italy 100 A. minutum/A. tamutum* AY962851 AMTK-5 Taiwan A. minutum/A. tamutum* AY268606 AMTK-5 Taiwan A. ostenfeldii AF033533 Kaitaia New Zealand 95 A. ostenfeldii AJ535357 BAHME136 New Zealand A. ostenfeldii AY268601 AONZ01 AY268603 AONZ04 New Zealand A. ostenfeldii AY962856 CAWD16 New Zealand A. ostenfeldii AJ535356 K0287 Denmark 98 A. ostenfeldii A. ostenfeldii AY962858 K-0287 Denmark 97 A. ostenfeldii AY268611 K-0287 Denmark A. ostenfeldii AY268615 K-0324 Denmark A. ostenfeldii AJ535363 K0324 Denmark A. ostenfeldii S06/S013/01 S06/S015/01 Scotland 88 A. ostenfeldii AY268614 HT140-E4 USA A. ostenfeldii AY962857 HT140-E4 USA 88 Alexandrium Maximum-likelihood tree based on LSU rDNA A. ostenfeldii AJ535358 AOSH1 Canada

  11. A. tamarense North American Western European A. ostenfeldii A. tamutum A. minutum Four species, two strains

  12. Toxin analysis – toxic and non-toxic

  13. A. tamarense (NA) produced a complex array of toxins • Major toxins were NEO, STX, GTX-4, GTX-3 and C2 • Lower concn of epimeric C and GTX toxins • A. ostenfeldii produced lower concn of PSP toxins – STX and NEO • A. ostenfeldii also produced the spirolide toxin 20-methyl spirolide G Culture fg 20-Me-SPX G cell -1 S06/013/01 A. ostenfeldii 19 S06/015/01 A. ostenfeldii 20 Toxin analysis – toxic and non-toxic • A. tamarense (WE), A. tamutum and A. minutum did not produce toxins

  14. A. tamarense North American Toxic (PSP) Western European Non -Toxic A. ostenfeldii Toxic (PSP and spirolides) A. tamutum A. minutum Non -Toxic Non -Toxic Four species, two strains, toxic and non-toxic

  15. Alexandrium tamarense - Conclusions • Historically considered that all Alexandrium from Scottish waters • were highly potent PSP toxin producers • were A. tamarense North American (NA) strain • We propose • non-toxic A. tamarense Western European (WE) strain is extending northwards • in our study, A. tamarense Western European hatched from cysts at warmer temperatures • Warming seas may allow further shift of boundaries northwards • changing distributions of Alexandrium populations

  16. Alexandrium tamerense distribution • Classical picture of distribution based on evolution of Atlantic ocean • Explains basic biogeography of Alexandrium tamarense strains • E.g. Scholin et al., 1995, Medlin et al., 1998 • My simplified interpretation is as follows…

  17. 220 Million Years Ago 1 Land Mass – Pangaea 1 Ocean - Panthalassa Globally distributed Ancestral population 200 Million Years Ago Pangaea split into 2 land masses by Tethys Sea Image by David Dorkin – See http://mediatheek.thinkquest.nl/

  18. 130 - 25 Million Years Ago South Atlantic opens Gondwanaland splits Africa and America forms North American Strain forms in eastern Pacific Western European Strain forms and enters Tethys Sea / Mediterranean Temperate Asian Strain also forms in western Pacific Image by David Dorkin – See http://mediatheek.thinkquest.nl/

  19. North American strain arrives – Scotland and Faroe from the eastern Pacific when North Atlantic opens Western European strain in southern waters 20-10 Million Years Ago North Atlantic opened Image by David Dorkin – See http://mediatheek.thinkquest.nl/

  20. Changes in Alexandriumtamarense distribution • Can we explain the observed changes in the distribution of Alexandrium strains? • If they are real changes – do they make sense in terms of oceanography? • Need to look at present day ocean circulation • First – is there offshore / large scale transport north? • Second – are there inshore linkages on the shelf?

  21. Slope Current transports plankton Links Mediterranean / southern waters to Scottish / northern European waters Present day North Atlantic circulation

  22. Summertime Inshore coastal circulation Transports plankton Links coastal waters around UK Hill et al., 2008 Inshore coastal circulation

  23. What is link to climate change? Hypothesis… • Northerly transport of plankton, including Western European (WE) strain of Alexandrium, has always happened • In the past northern waters too cold for WE strain to survive • Now waters warming – providing suitable environment for WE strain

  24. Southern shelf edge zooplankton species 1960-1975 1996-1999 Other plankton species moving north Beaugrand et al.(2002). Mar. Ecol. Prog. Ser., 232, 179-195

  25. Alexandrium ostenfeldii - Conclusions • This study confirms the presence of A. ostenfeldii • Confirms production of both PSP toxins and a single SPX analogue - 20-methyl SPX G • May be necessary to expand shellfish toxin monitoring to include analysis of SPXs

  26. Alexandrium tamutum - Conclusions • Occurrence of non-toxic A. tamutum remarkable • Previously only reported from the Mediterranean (and very recently from Southwest Ireland) • Northerly spread could be through same mechanism as A. tamarense

  27. Alexandrium minutum - Conclusions • Alexandrium minutum not previously observed in Scottish waters • So far, only non-toxic strains isolated from Scottish waters • Toxic A. minutum from Fleet Lagoon - may have migrated from Brittany coast • Both toxic and non-toxic strains geographically separated in Irish coastal waters • Other non-toxic strains from Gulf of Trieste • The possibility of toxic and non-toxic A. minutum in Scottish waters should be explored to assess the risks of PSP toxin contamination of shellfish caused by the species

  28. Climate Change = Climate Change = A Final Thought…?

  29. Acknowledgements • FRS Colleagues: Jennifer Graham, Jean-Pierre Lacaze, Guillaume Hermann, Eileen Bresnan, Anastasia Amorin, Lyndsay Brown, Catherine Collins, Bill Turrell • This project is supported and funded by the… • Sixth Framework Programme of the EC • SPIES-DETOX Collective Research Project 0302790-2 • Scottish Government (www.frs-scotland.gov.uk) • ROAME AE1193

  30. Thank you for listening!

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