Factors Influencing the Toxicity, Detoxification and Biotransformation of Paralytic Shellfish Toxins

  • Kar Soon Tan
  • Julian RansanganEmail author
Part of the Reviews of Environmental Contamination and Toxicology book series (RECT, volume 235)


The incidence of red tide events globally has escalated in marine coastal environments over the last several decades (Cordier et al. 2000). The term red tide is used to describe a phenomenon in which a water body exhibits red coloration from the presence of high algal cell density. Red tide events are often harmful to both human and aquatic organisms. However, the term may be confusing, because red tide refers not only to the high density of microscopic algal cells that colorize water, but also includes blooms of highly toxic cells that can cause problems even at low cell densities, i.e., a few hundred cells L−1. Therefore, the term Harmful Algal Blooms (HABs) has been introduced to describe blooms of both toxic and non-toxic algae that potentially have negative effects on humans and the environment (Anderson 2009). The reported global incidence of paralytic shellfish poisoning (PSP) that has been associated with HABs has been increasing annually (Anderson 1989). However, it is still unclear whether the increase results from elevated public awareness and reporting of HABs, or from an increase in anthropogenic factors, like increasing marine pollution incidents.


Paralytic shellfish toxins Bivalves Detoxification Biotransformation 



This work was financially supported by the Niche Research Grant Scheme (NRGS0003) from the Ministry of Education Malaysia.


  1. Acres J, Gray J (1978) Paralytic shellfish poisoning. Can Med Assoc J 119:1195–1197Google Scholar
  2. Al-Azad S, Tan KS, Ransangan J (2013) Effects of light intensities and photoperiods on growth and proteolytic activity in purple non-sulfur marine bacterium, Afifella marina strain ME (KC205142). Adv Biosci Biotechnol 4:919–924Google Scholar
  3. Anderson DM (2009) Approaches to monitoring, control and management of harmful algal blooms (HABs). Ocean Coast Manag 52:342Google Scholar
  4. Anderson DM (1989) Toxic algal blooms and red tides: a global perspective. In: Okaido AT, Anderson DM, Nemoto T (eds) Red tides: biology environmental science and toxicology. Elsevier, New York, NY, pp 11–16Google Scholar
  5. Anderson DM, Kulis DM, Sullivan JJ, Hall S (1990) Toxin composition variations in one isolate of the dinoflagellate Alexandrium fundyense. Toxicon 28:885–893Google Scholar
  6. Anderson DM, Glibert PM, Burkholder JM (2002) Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 25:704–726Google Scholar
  7. Anton A, Alexander J, Estim A (2000) Harmful algal blooms in Malaysia: revisiting Kimanis Bay. In: 9th International Conference on Toxic Phytoplankton, Tasmania (Abstract)Google Scholar
  8. AOAC International (1995) Paralytic shellfish poison. Biological method. Chapter 35. In: Williams S (ed) Official methods of analysis, 14th edn. Association of Official Analytical Chemists International, Arlington, VA, pp 21–22Google Scholar
  9. Aune T, Ramstad H, Heidenreich B, Landsverk T, Waaler T, Egaas E, Julshamn K (1998) Zinc accumulation in oysters giving mouse deaths in paralytic shellfish poisoning bioassay. J Shellfish Res 17:1243–1246Google Scholar
  10. Aune T, Aasen JAB, Miles CO, Larsen S (2008) Effect of mouse strain and gender on LD50 of yessotoxin. Toxicon 52:535–540Google Scholar
  11. Baden DG, Trainer VL (1993) Mode of action of saxitoxins of seafood poisoning. In: Falconer I (ed) Algal toxin in seafood and drinking water. Academic, London, pp 49–74Google Scholar
  12. Beitler MK, Liston J (1990) Uptake and tissue distribution od PSP toxin in butter clams. In: Graneli E, Sindstrom B, Edler L, Anderson DM (eds) Toxic marine phytoplankton. Elsevier Science Publications, Amsterdam, pp 257–263Google Scholar
  13. Benavides H, Prado L, Díaz S, Carreto JI (1995) An exceptional bloom of Alexandrium catenella in the Beagle Channel, Argentina. In: Lassus P, Arzul G, Erard-Le Denn E, Gentien P, Marcaillou-Le Baut C (eds) Harmful marine algal blooms. Lavoisier Publishers, Paris, pp 113–119Google Scholar
  14. Bricelj VM, Lee JH, Cembella AD, Anderson DM (1990) Uptake kinetics of paralytic shellfish toxins from the dinoflagellate Alexandrium fundyense in the mussel Mytilus edulis. Mar Ecol Prog Ser 63:177–188Google Scholar
  15. Bricelj VM, Lee JH, Cembella AD (1991) Influence of dinoflagellate cell toxicity on uptake and loss of paralytic shellfish toxins in the northern quahog, Mercenaria mercenaria. Mar Ecol Prog Ser 74:33–46Google Scholar
  16. Bricelj VM, Cembella AD (1995) Fate of gonyautoxins accumulated in surfclams, Spisula solidissima, grazing upon PSP toxin-producing Alexandrium. In: Lassus P, Arzul G, Erard E, Gentien P, Marcaillou C (eds) Harmful marine algal blooms. Lavoisier Science Publishers, ParisGoogle Scholar
  17. Bricelj VM, Cembella AD, Laby D, Shumway SE, Cucci TL (1996) Comparative physiological and behavioral responses to PSP toxins in two bivalve molluscs, the softshell clam, Mya arenaria, and surfclam, Spisula solidissima. In: Yasumoto T, Oshima Y, Fukuyo Y (eds) Harmful and toxic algal blooms. Intergovernmental Oceanographic Commission of UNESCO, Paris, pp 405–408Google Scholar
  18. Bricelj VM, Shumway SE (1998) Paralytic shellfish toxins in bivalve molluscs: occurrence, transfer kinetics and biotransformation. Rev Fisher Sci 6(4):315–383Google Scholar
  19. Brivelj VM, Connell L, Konoki K, Macquarrie SP, Scheuer T, Catteral WA, Trainer VL (2005) Sodium channel mutation leading to saxitoxin resistance in clams increases risk of PSP. Nature 434:764–767Google Scholar
  20. Buckley LJ, Oshima T, Shimizu Y (1978) Construction of a paralytic shellfish toxin analyzer and its application. Anal Biochem 85:157–164Google Scholar
  21. Carreto JI, Benavides HR, Negri RM, Glorioso PD (1986) Toxic red-tide in the Argentine Sea. Phytoplankton distribution and survival of the toxic dinoflagellate Gonyaulax excavata in a frontal area. J Plankton Res 8:15–28Google Scholar
  22. CEN (2002) EN 14194. Foodstuffs - determination of saxitoxin and desaxitoxin in mussels - HPLC method using post-column derivatization with peroxide or periodate oxidation. European Committee for Standardization (CEN).Google Scholar
  23. Cestele S, Catterall WA (2000) Molecular mechanisms of neurotoxin action on voltage-gated sodium channels. Biochemistry 82:883–892Google Scholar
  24. Chen CY, Chou HN (2001) Accumulation and depuration of paralytic shellfish toxins by purple clam Hiatula rostrata. Light Tools Toxicon 39:1029–1034Google Scholar
  25. Choi MC, Hsieh DPH, Lam PKS, Wang WX (2003) Field depuration and biotransformation of paralytic shellfish toxins in scallop Chlamys nobilis and green- lipped mussel Perna viridis. Mar Biol 143:927–934Google Scholar
  26. Chou HN, Huang CP, Chen CY (2005) Accumulation and depuration of paralytic shellfish poisoning toxins by laboratory cultured purple clam Hiatula diphos Linnaeus. Toxicon 46:587–590Google Scholar
  27. Ciminiello P, Fattorusso E, Forino M, Montresor M (2000) Saxitoxin and neosaxitoxin as toxic principles of Alexandrium Anderson (Dinophyceae) from the Gulf of Naples, Italy. Toxicon 38:1871–1877Google Scholar
  28. Cordier S, Monfort C, Miossec L, Richardson S, Belin C (2000) Ecological analysis of digestive cancer mortality related to contamination by diarrhetic shellfish poisoning toxins along the coast of France. Environ Res 84:145–150Google Scholar
  29. Dahl E, Tangen K (1993) 25 years experience with Gyrodinium aureolum in Norwegian waters. In: Smayda TJ, Shimizu Y (eds) Toxic phytoplankton blooms in the sea. Elsevier, New York, NY, pp 15–21Google Scholar
  30. Daigo K, Noguchi P, Miwa A, Kawai N, Hasimoto K (1988) Resistance of nerves from certain toxic crabs to paralytic shellfish poison and tetrodotoxin. Toxicon 26:485–490Google Scholar
  31. Davio SR, Fontelo PAA (1984) Competitive displacement assay to detect saxitoxin and tetrodotoxin. Anal Biochem 141:199–204Google Scholar
  32. Deeds J, Landsberg J, Etheridge S, Pitcher G, Longan S (2008) Non-traditional vectors for paralytic shellfish poisoning. Mar Drugs 6:308–348Google Scholar
  33. Dell’Aversano C, Walter JA, Burton IW, Stirling DJ, Fattorusso E, Quilliam MA (2008) Isolation and structure elucidation of new and unusual saxitoxin analogues from mussels. J Nat Prod 71:1518–1523Google Scholar
  34. Deyoe HR, Sutrle CA (1994) The inability of the Texas “brown tide” alga to use nitrate and the role of nitrogen in the initiation of a persistent Moom of tiffs organism. J Physiol 7(30):800–806Google Scholar
  35. Donovan CJ, Ku JC, Quiliam MA, Gill TA (2008) Bacterial degradation of paralytic shellfish toxins. Toxicon 52:91–100Google Scholar
  36. Donovan CJ, Garduno RA, Kalmokoff M, Ku JC, Quilliam MA, Gill TA (2009) Pseudoalteromonas bacteria are capable of degrading paralytic shellfish toxins. Appl Environ Microbiol 75:6919–6923Google Scholar
  37. Doucette GJ, Logan MM, Ramsdell JS, van Dolah FM (1997) Development and preliminary validation of a microtiter plate-based receptor binding assay for paralytic shellfish poisoning toxins. Toxicon 35:625–636Google Scholar
  38. Fast MD, Cembella AD, Ross NW (2006) In vitro transformation of paralytic shellfish toxins in the clams Mya arenaria and Protothaca staminea. Harmful Algae 5:79–90Google Scholar
  39. Franco J, Fernandez P, Reguera B (1994) Toxin profiles of natural populations and cultures of Alexandrium minitum Halim from Galician (Spain) coastal waters. J Appl Phycol 6:275–279Google Scholar
  40. Gacutan RQ, Tabbu MY, de Castro T, Gallego AB, Arafiles MB, Icatlo F (1989) Detoxification of Pyrodinium generated paralytic shellfish poisoning toxin in Perna viridis from western Samar, Philippines. In: Hallegraeff GM, Maclean JL (eds), Biology, epidemiology and management of Pyrodinium red tides. JCLARM conference proceeding 21. Manila, Philippines, pp 80–85.Google Scholar
  41. Gainey LF Jr, Shumway SE (1988) A compendium of the responses of bivalve molluscs to toxic dinoflagellates. J Shellfish Res 7(4):623–628Google Scholar
  42. Garate-Lizarraga I, Bustillos-Guzman JJ, Morquecho L, Band-Schmidt CJ, Alonso-Rodriguez R, Erler K, Luckas B, Reyes-Salinas A, Gongora-Gonzalez DT (2005) Comparative paralytic shellfish poisoning profiles in the strains of Gymnodinium catenatum Graham from the Gulf of California, Mexico. Mar Pollut Bull 50:211–217Google Scholar
  43. Glasgow HB, Burkholder JM, Mallin MA, Dreamer-Melia NJ, Reed RE (2001) Field ecology of toxic Pfiesteria complex species, and a conservative analysis of their role in estuarine fish kills. Environ Health Perspect 109:715–730Google Scholar
  44. Glibert PM, Magnien R, Lomas MW, Alexander J, Fan C, Haramoro E, Trice M, Kana TM (2001) Harmful algal blooms in the Chesapeake and coastal bays of Maryland, USA: comparison of 1997, 1998, and 1999 events. Estuaries 24:875–883Google Scholar
  45. Graneli E, Carlsson P (1998) The ecological significance of phagoix-ophy in photosynthetic flagellates. In: Anderson DM, Cerebella AD, HallegTaeff GM (eds) Physiological ecology of harmful algal blooms. Springer, Berlin, Germany, pp 540–557Google Scholar
  46. Grzebyk D, Bechemin C, Ward CJ, Verite C, Codd GA, Maestrini SY (2003) Effects of salinity and two coastal waters on the growth and toxin content of the dinoflagellate Alexandrium minitum. J Plankton Res 25:1185–1199Google Scholar
  47. Hamasaki K, Horie M, Tokimitsu S, Toda T, Taguchi S (2001) Variability in toxicity of the dinoflagellate Alexandrium tamarense isolated from Hiroshima Bay, western Japan, as a reflection of changing environmental conditions. J Plankton Res 23:271–278Google Scholar
  48. Hallegraeff GM (1993) A review of harmful algal blooms in the Australian region. Mar Pollut Bull 25:186–190Google Scholar
  49. Hansen PJ, Cembella AD, Moestrup O (1992) The marine dinoflagellate Alexandrium ostenfeldii: paralytic shellfish toxin concentration, composition and toxicity to a tintinid ciliate. J Phycol 28:597–603Google Scholar
  50. Hodgkiss IJ, Ho KC (1997) Are changes in N:P ratios in coastal waters the key to increased red tide blooms. Hydrobiologia 352:141–147Google Scholar
  51. Holmes MJ, Bolch CJS, Green DH, Cembella AD, Teo SLM (2002) Singapore isolates of dinoflagellate Gymnodinium catenatum (Dinophyceae) produce a unique profile of paralytic shellfish poisoning toxins. J Phycol 38:96–106Google Scholar
  52. Humpage AR, Magalhaes VF, Froscio SM (2010) Comparison of analytical tools and biological assays for detection of paralytic shellfish poisoning toxins. Anal Bioanal Chem 397:1655–1671Google Scholar
  53. Hurst JW, Gilfillan ES (1997) Paralytic shellfish poisoning in Maine. In: Wilt ES (ed) Tenth Natl shellfish sanitation workshop. U.S. Dept. Health, Education and Welfare, Food and Drug Administration, Washington, DC, pp 152–161Google Scholar
  54. Hwang DF, Lu YH, Noguchi T (2003) Effects of exogenous polyamines on growth, toxicity, and toxin profile of dinoflagellate Alexandrium minutum. J Food Hygien Soc Jpn 44:49–53Google Scholar
  55. Hwang DR, Lu YH (2000) Influence of environmental and nutritional factors on growth, toxicity, and toxin profile of dinoflagellate Alexandrium minitum. Toxicon 38:1491–1503Google Scholar
  56. Ichimi K, Suzuki T, Ito A (2002) Variety of PSP toxin profile in various culture strains of Alexandrium tamarense and change of toxin profile in natural A. tamarense population. J Exp Mar Biol Ecol 273:51–60Google Scholar
  57. Inami GB, Crandall C, Csuti D, Oshiro M, Brenden RA (2004) Feasibility of reduction in use of mouse bioassay: presence/absence screening for saxitoxin in frozen acidified mussel and oyster extracts from the coast of California with in vitro methods. J AOAC Int 87(5):1133–1142Google Scholar
  58. Jacobson DM, Anderson DM (1996) Widespread phagocytosis of dilates and other protists by marine mixotrophic and heterotrophic thecate dinoflagellates. J Phycol 82:279–285Google Scholar
  59. Jaime E, Gerdts G, Luckas B (2007) In vitro transformation of PSP toxins by different shellfish tissues. Harmful Algae 6:308–316Google Scholar
  60. Jellett JF, Marks LJ, Stewart JE, Dorey MI, Watson-Wright W, Lawrence JF (1992) Paralytic shellfish poisoning (saxitoxin family) bioassays: automated endpoint determination and standardization of the in vitro tissue culture bioassay, and comparison with the standard mouse bioassay. Toxicon 30:1143–1156Google Scholar
  61. Jellett JF, Doucette LI, Belland ER (1998) The MIST ™ shippable cell bioassay kids for PSP: an alternative to the mouse bioassay. J Shellfish Res 17:1653–1655Google Scholar
  62. Johansson N, Graneli E (1999) Cell density, chemical composition and toxicity of Chrysochromulina polylepis (Haptophyta) in relation to different N:P supply ratios. Mar Biol 135:209–217Google Scholar
  63. Johansson N, Graneli E, Yasumoto T, Carlsson P, Legrand C (1996) Toxin production by Dinophysis acuminata and D. acuta cells grown under nutrient sufficient and deficient conditions. In: Yasumoto T, Oshima Y, Fukuyo Y (eds) Harmful and toxic algal blooms. Scientific and Cultural Organization, Intergovernmental Oceanographic Commission of United Nations Educational, Paris, France, pp 227–280Google Scholar
  64. Jones GJ, Bourne DG, Blakeley RL, Doelle H (1994) Degradation of the cyanobacterial hepatotoxin microcystin by aquatic bacteria. Nat Toxins 2:228–235Google Scholar
  65. Kao CY (1993) Paralytic shellfish poisoning. Algal toxins in seafood and drinking water. Academic, London, pp 75–86Google Scholar
  66. Kodama M (1990) Possible link between bacteria and toxin production in algal blooms. In: Granelii EP, Sundstrom B, Edler L, Anderson DN (eds) Toxic marine phytoplankton. Elsevier, New York, NY, pp 52–61Google Scholar
  67. Kodama M (2000) Ecobiology, classification, and origin. In: Botana LM (ed) Seafood and freshwater toxins - pharmacology, physiology, and detection. Marcel Dekker, New York, NY, pp 125–149Google Scholar
  68. Kotaki Y, Oshima Y, Yasumoto T (1985) Bacterial transformation of paralytic shellfish toxins in coral reef crabs and marine snail. Nippon Suisan Gakkashi 51:1009–1013Google Scholar
  69. Kotaki Y (1989) Screening of bacteria which convert gonyautoxin 2, 3 to saxitoxin. Nippon Suisan Gakkashi 55:1293Google Scholar
  70. Krock B, Seguel CG, Gembella AD (2007) Toxin profile of Alexandrium catenella from the Chilean coast as determined by liquid chromatography with fluorescence detection and liquid chromatography coupled with tandem mass spectrometry. Harmful Algal 6:734–744Google Scholar
  71. Kwong RW, Wang WX, Lam PK, Yu PK (2006) The uptake, distribution and elimination of paralytic shellfish toxins in mussels and fish exposed to toxic dinoflagellates. Aquat Toxicol 80:82–91Google Scholar
  72. Larocque R, Cembella AD (1991) Résultats du premier programme de suivi des populations de phytoplancton toxique dans l’estuaire et le Golfe du Saint-Laurent (Région du Québec). Rapp Tech Can Sci Hal Aquat 1796: 42 pGoogle Scholar
  73. Lassus P, Ledoax M, Bardouill M, Bohee M (2000) Comparative efficiencies of different non-toxic microalgal diet in detoxification of PSP-contaminated oyster. J Nat Toxin 9:1–12Google Scholar
  74. Lawrence JF, Menard C, Charbonneau CF, Hall S (1991) A study of ten toxins associated with paralytic shellfish poison using prechromatographic oxidation and liquid chromatography with fluorescence detection. J AOAC 74:404–409Google Scholar
  75. Lee NS, Kim BT, Kim DH, Kobashi K (1995) Purification and reaction mechanism of arylsulfate sulfotransferase from Haemophilus K-12, a mouse intestinal bacterium. J Biochem 118:796–801Google Scholar
  76. Lefebvre KA, Bill BD, Erickson A, Baugh KA, O’Rourke L, Costa PR, Nance S, Trainer VL (2008) Characterization of intracellular and extracellular saxitoxin levels in both field and cultured Alexandrium spp. Samples from Sequim Bay, Washington. Mar Drugs 6:103–116Google Scholar
  77. Lewitus AJ, Haves KC, Gransden SG, Glascow HB, Burkholder JM Jr, Glibert PM, Morton SL (2001) Ecological characterization of a widespread Scrippsiella red tide in South Carolina estuaries: a newly observed phenomenon. In: Hallegraeff GM, Blackbuna S, Bolch C, Lewis R (eds) Proceedings of the ninth international conference on harmful algal blooms. Intergovernmental Oceanographic Commission, United Nations Educational Scientific, and Oalmral Organization, Paris, FranceGoogle Scholar
  78. Li A, Stoeker DK, Coats DW (2000) Spatial and temporal aspects of Gyrodinium galatheanum in Chesapeake Bay: distribution and mixotrophy. J Plankton Res 22:2105–2124Google Scholar
  79. Li A, Stoeker DK, Coats DW (2001) Mixotrophy in Gyrodinium galatheanum (Dinophyceae): grazing responses to light intensity and inorganic nutrients. J Phycol 36:33–45Google Scholar
  80. Lim PT, Leaw CP, Usup G (2001) First incidence of paralytic shellfish poisoning on the east coast of Peninsular Malaysia. In: Sasekumar A, Usup G, Noraieni M, Ung EH, Lee SC (eds), Book of abstracts Asia-Pacific Conference on marine science & technology. Marine science into the new millennium: new perspectives & challenges, 12–16 May 2001, Kuala Lumpur, MalaysiaGoogle Scholar
  81. Lim PT, Usup G, Leaw CP, Ogata T (2005) First report of Alexandrium taylori and Alexandrium peruvianum (Dinophyceae) in Malaysia waters. Harmful Algae 4:391–400Google Scholar
  82. Lim PT, Ogata T (2005) Salinity effect on growth and toxin production of four tropical Alexandrium species (Dinophyceae). Toxicon 45:699–710Google Scholar
  83. Lim PT, Leaw CP, Usup G, Kobiyama A, Koike K, Ogata T (2006) Effects of light and temperature on growth, nitrate uptake, and toxin production of two tropical dinoflagellates: Alexandrium tamiyavanichi and Alexandrium minutum (Dinophyceae). J Phycol 42:786–799Google Scholar
  84. Lim PT, Leaw CP, Kobiyama A, Ogata T (2010) Growth and toxin production of tropical Alexandrium minutum Halim (Dinophyceae) under various nitrogen to phosphorus ratios. J Appl Phycol 22:203–210Google Scholar
  85. Lippemeier S, Frampton DMF, Blackburn SI, Geier SC, Negri AP (2003) Influence of phosphorus limitation on toxicity and photosynthesis of Alexandrium minutum (Dinophyceae) monitored by in-line detection of variable chlorophyll fluorescence. J Phycol 39(2):320–331Google Scholar
  86. Llewellyn LE (2006) Saxitoxin, a toxic marine natural product that targets a multitude of receptors. Nat Prod Rep 23:200–222Google Scholar
  87. Lomas MW, Glibert EM (2000) Comparisons of nitrate uptake, storage, and reduction in marine diatoms and flagellates. J Phycol 36:903–913Google Scholar
  88. Lu YH, Hwang DF (2002) Effects of toxic dinoflagellates and toxin biotransformation in bivalves. J Nat Toxins 11:315–322Google Scholar
  89. Mahar J, Lukàcs GL, Li Y, Hall S, Moczydlowski E (1991) Pharmacological and biochemical properties of saxiphilin, a soluble saxitoxin-binding protein from the bullfrog (Rana catesbiana). Toxicon 29:53–71Google Scholar
  90. Martin JL, White AW, Sullivan JJ (1990) Anatomical distribution of paralytic shellfish toxins in softshell clams. In: Granéli E, Sundström B, Edler L, Anderson DM (eds) Toxic marine phytoplankton. Elsevier, New York, NY, pp 379–384Google Scholar
  91. Negri AP, Bolch CJS, Geier S, Green DH, Park TG, Blackburn SI (2007) Widespread present of hydrophobic paralytic shellfish toxins in Gymnodinium catenatum. Harmful Algae 6:774–780Google Scholar
  92. Negri AP, Jones GJ (1995) Bioaccumulation of paralytic shellfish poisoning (PSP) toxins from the cyanobacterium Anabaena circinalis by the freshwater mussel Alathyria condola. Toxicon 33:667–678Google Scholar
  93. Noguchi T, Chen S, Arakawa O, Hashimoto K (1989) A unique composition of PSP in “hoigi” scallop Chlamys nobilis. In: Natori S, Hashimoto K, Ueno Y (eds) Mycotoxins and phycotoxins’88. Elsevier, Amsterdam, pp 351–358Google Scholar
  94. Nygaard K, Tobiesen A (1998) Bacterivory in algae: a survival strategy during nutrient limitation. Limnol Oceanogr 38:273–279Google Scholar
  95. Ogata T, Kodama M, Ishimaru T (1989) Effect of water temperature and light intensity on growth rate and toxin production in toxic dinoflagellates. In: Okaichi T, Anderson DM, Nemoto T (eds) Red tides: biology, Environmental science and toxicology. Elsevier, New York, NY, pp 423–426Google Scholar
  96. Ogata T, Pholpunthin P, Fukuyo Y, Kodama M (1990) Occurrence of Alexandrium cohorticula in Japanese coastal water. J Appl Phycol 2:351–356Google Scholar
  97. Oshima Y, Sugino K, Yasumoto T (1989) Latest advance in HPLC analysis of paralytic shellfish toxins. In: Natori S, Hashimoto K, Ueno Y (eds) Mycotoxins and phycotoxins’88. Elsevier Science Publishers, Amsterdam, pp 319–326Google Scholar
  98. Oshima Y, Blackburn SI, Hallegraeff GM (1993) Comparative study on paralytic shellfish toxin profiles of the dinoflagellates Gymnodinium catenatum from three different countries. Mar Biol 116:471–476Google Scholar
  99. Oshima Y (1995) Post-column derivatization HPLC method for the analysis of PSP. J AOAC Int 78:795–799Google Scholar
  100. Parkhill J, Cembella A (1999) Effects of salinity, light and organic nitrogen on growth and toxigenicity of marine dinoflagellate Alexandrium tamarense from northeastern Canada. J Plankton Res 21:939–955Google Scholar
  101. Pitcher GC, Cembella AD, Joyce LB, Larsen J, Probyn TA, Ruiz Sebastian C (2007) The dinoflagellate Alexandrium minutum in Cape Town harbour (South Africa): bloom characteristics, phylogenetic analysis and toxin composition. Harmful Algae 6:823–836Google Scholar
  102. Poulton NJ, Keafer BA, Anderson DM (2005) Toxin variability in natural population of Alexandrium fundyense in Casco Bay, Maine-evidence of nitrogen limitation. Deep-Sea Res 52(PT2):2501–2521Google Scholar
  103. Proctor NH, Chan SL, Truvor AJ (1975) Production of saxitoxin by culture of Gonyaulax catenella. Toxicon 13:1–19Google Scholar
  104. Quilliam MA, Janecek M (1993) Characterization of oxidation products of paralytic shellfish poisoning toxins by liquid chromatography/mass spectrometry. Rapid Comm Mass Spectrom 7:482–487Google Scholar
  105. Quilliam MA (1998) Phycotoxins. J AOAC Int 81:142–151Google Scholar
  106. Rodrigue DC, Etzel RA, Hall S, de Porras E, Velasquez OH, Tauxe RV, Kilbourne EM, Blake PA (1990) Lethal paralytic shellfish poisoning in Guatemala. Am J Trop Med Hyg 42:267–271Google Scholar
  107. Rodríguez P, Alfonso A, Botana AM, Vieytes MR, Botana LM (2010) Comparative analysis of pre- and post-column oxidation methods for detection of paralytic shellfish toxins. Toxicon 56:448–457Google Scholar
  108. Romdhane MS, Eilertsen HC, Yahia OKD, Yahia MND (1998) Toxic dinoflagellate blooms in Tunisian lagoons: causes and consequences for aquaculture. In: Reguera B, Blance J, Fernandez ML, Wyatt T (eds) Harmful algae. Xunta de Galicia and Intergovernmental Oceanographic Commission of United Nations Educational, Scientific and Cultural Organization, Paris, France, pp 80–83Google Scholar
  109. Schantz EJ, McFarren EF, Schafer ML, Lewis KH (1958) Purified shellfish poison for bioassay standardization. J Assoc Off Anal Chem 41:160–168Google Scholar
  110. Schantz EJ, Ghazarossian VE, Schnoes HK, Strong FM, Springer JP, Pezzanite JO, Clardy J (1975) Structure of saxitoxin. J Am Chem Soc 97:1238–1239Google Scholar
  111. Sebastian CR, Etheridge SM, Cook PA, O’Ryan C, Pitcher GC (2005) Phylogenetic analysis of toxic Alexandrium (Dinophyceae) isolates from South Africa: implications for the global phylogeography of Alexandrium tamarense species complex. Phycologia 44:49–60Google Scholar
  112. Sharma R, Venkateshvaran K, Purushothaman CS (2011) Bioaccumulation and depuration of paralytic shellfish toxin in Perna viridis and Meretrix meretrix from Mumbai, India. Ind J Marine Sci 40:542–549Google Scholar
  113. Shimizu Y, Yoshioka M (1981) Transformation of paralytic shellfish toxins as demonstrated in scallop homogenates. Science 212:547–549Google Scholar
  114. Shimizu Y, Watanabiz N, Wrensfori G (1993) Biosynthesis of brevetoxins and heterotrophic metabolism in Gymnodinium breve. In: Lassus R, Arzul C, Erard-Le-Denn E, Gentian R, Mm-caillou C (eds) Harmful marine algal blooms. Lavoisier Publishing, Paris, France, pp 351–357Google Scholar
  115. Silvert W, Bricelj M, Cembella A (1998) Dynamic modelling of PSP toxicity in the surfcalm (Spisula solidissima): multicompartmental kinetics and biotransformation. In: Rguera B, Blanco J, Fernandez ML, Wyatt T (eds) Harmful algae. VIII international Conference. Intergovernmental Oceanographic Commission of UNESCO, Paris, pp 437–440Google Scholar
  116. Siu G, Young M, Chan D (1997) Environmental and nutritional factors which regulate population dynamics and toxin production in the dinoflagellate Alexandrium catenella. Hydrobiology 352:117–140Google Scholar
  117. Smil V (2001) Enriching the earth: Fritz Haber, Carl Bosch, and the transformation of world food. Tile MIT Press, Cambridge, UKGoogle Scholar
  118. Smith EA, Grant F, Ferguson CMJ, Gallacher S (2001) Biotransformations of paralytic shellfish toxins by bacteria isolated from bivalve molluscs. Appl Environ Microbiol 67(5):2345–2353Google Scholar
  119. Sommer H, Meyer KF (1937) Paralytic shellfish poisoning. Achiev Pathol Labor Med 24:560–598Google Scholar
  120. Soon TK, Ransangan J (2014) A review of feeding behavior, growth, reproduction and aquaculture site selection for green-lipped mussel, Perna viridis. Adv Biosci Biotechnol 5:462–469Google Scholar
  121. Su Z, Sheets M, Ishida H, Li FH, Barry WH (2004) Saxitoxin blocks L-type I ca. J Pharmacol Exp Ther 308:324–329Google Scholar
  122. Sugawara A, Imamura T, Aso S, Ebitani K (1997) Change of paralytic shellfish poison by the marine bacteria living in the intestine of Japanese surf clam, Pseudocardium sybillae and the brown sole, Pleuronectes herensteini. Sci Rep Hokkaido Fisher Exp Stat 50:35–42Google Scholar
  123. Sullivan JJ (1982) Paralytic shellfish poisoning: analytical and biochemical investigation. PhD thesis, University of Washington, Seattle.Google Scholar
  124. Taylor FJR (1984) Toxic dinoflagellates: taxonomic and biogeographic aspects with emphasis on Protogonyaulax. In: Ragelis EP (ed) Seafood toxins, vol 262, Amer. Chem. Soc. Symposium Ser. ACS, Washington, DC, pp 77–97Google Scholar
  125. Teste V, Briand JF, Nicholson BC, Puiseux-Dao S (2002) Comparison of changes in toxicity during growth of Anabaena circinalis (cyanobacteria) determined by mouse neuroblastoma bioassay and HPLC. J Appl Phycol 14:399–407Google Scholar
  126. Usleber E, Dietrich R, Burk C, Schneider E, Martlbauer E (2001) Immunoassay methods for paralytic shellfish poisoning toxins. J Assoc Off Anal Chem 84(5):1649–1656Google Scholar
  127. Usup G, Kulis DM, Anderson DM (1994) Growth and toxin production of the toxic dinoflagellate Pyrodinium bahamense var. compressum in laboratory cultures. Nat Toxins 2:254–262Google Scholar
  128. Usup G, Kulis DV, Anderson DM (1995) Toxin production in a Malaysian isolate of the toxic dinoflagellate Pyrodinium bahamense var. compressum. In: Lassus P, Arzul G, Erard E, Gentien P, Marcailiou C (eds) Harmful marine algal blooms. Lavoisier, Paris, pp 519–524Google Scholar
  129. Usup G, Pin LC, Ahmad A, Teen LP (2002) Alexandrium (Dinophyceae) species in Malaysian waters. Harmful Algae 1:265–275Google Scholar
  130. Vaulot D, Lebot N, Marie D, Fukai E (1996) Effect of phosphorus on Synechococcus cell cycle in surface Mediterranean waters during summer. Appl Environ Microbiol 62:2527–2533Google Scholar
  131. Velzeboer RMA, Baker PD, Rositano J, Heresztyn T, Codd GA and Raggett SL (2000) Geographical patterns of occurrence and composition of saxitoxins in the cyanobacterial genus Anabaena (Nostocales, Cyanophyta) in Australia. Phycologia 39:395–407Google Scholar
  132. Vieytes MR, Cabado AG, Alfonso A, Louzao MC, Botana AM, Botana LM (1993) Solid phase radioreceptor assay for paralytic shellfish toxins. Anal Biochem 211:87–93Google Scholar
  133. Wang JX, Salata JJ, Bennetn PB (2003) Saxitoxin is a gating modifier of hERG K + channels. J Gen Physiol 121:583–598Google Scholar
  134. Wang S, Tang D, He F, Fukuyo Y, Azanza RV (2008) Occurrences of harmful algal blooms (HABs) associated with ocean environments in the South China Sea. Hydrobiology 596:79–93Google Scholar
  135. Wiese M, D’Agostino PM, Mihali TK, Moffitt MC, Neilan BA (2010) Neurotoxic alkaloids: saxitoxin and its analogs. Mar Drugs 8:2185–2211Google Scholar
  136. World Health Organization (WHO) (1984) Environmental Health Criteria 37: Aquatic (Marine and Freshwater) Biotoxins.Google Scholar
  137. Xie W, Liu X, Yang X, Zhang C, Bian Z (2013) Accumulation and depuration of paralytic shellfish poisoning toxins in the oyster Ostrea rivularis Gould - chitosan facilitates the toxin depuration. Food Control 30:446–452Google Scholar
  138. Yoshida T, Sako Y, Kakutani T, Fujii A, Uchida A, Ishida Y, Arakawa O, Noguchi T (1998) Comparative study of two sulfotransferases for sulfation to N-21 of Gymnodinium catenatum and Alexandrium catenella toxins. In: Reguera B, Blanco J, Fernández ML, Wyatt T (eds) Harmful algae. Xunta de Galicia and IOC, United Nations Educational, Scientific, and Cultural Organization, Grafisant, Spain, pp 366–369Google Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Microbiology and Fish Disease Laboratory, Borneo Marine Research InstituteUniversity Malaysia SabahKota KinabaluMalaysia

Personalised recommendations