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Uptake, transformation, and elimination kinetics of paralytic shellfish toxins in white seabream (Diplodus sargus)

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Abstract

Marine toxins generated by harmful algal blooms can be transferred through the marine food web and ultimately cause massive deaths of piscivorous predators. However, very few studies have explored the processes of accumulation and biotransformation of paralytic shellfish toxins (PSTs) within fishes. White seabream (Diplodus sargus) were orally challenged with contaminated cockles (Cerastoderma edule) containing N-sulfocarbamoyl and decarbamoyl toxins and non-contaminated cockles afterwards. Specific PSTs that occurred in low abundance in cockles (B1 7.6% and dcSTX 1.6% molar fraction) were the only toxins detected in fish viscera possibly resulting from selective elimination and transformation of the various PSTs. Concentration of toxins progressively increased in fish viscera throughout the uptake period. Toxins were then rapidly depurated (B1 0.905 day−1, dcSTX 0.467 day−1) when diet was changed to non-toxic cockles. Results indicate conversion of a precursor toxin into B1 which in turn might be converted into dcSTX at a lower extent. Low accumulation efficiency of 1.7 and 5.0% was calculated to B1 and dcSTX, respectively. This study contributes to a better understanding of dynamics of PSTs in fish and the fate of these compounds in the marine food web.

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References

  • Bakke MJ, Horsberg TE (2010) Kinetic properties of saxitoxin in Atlantic salmon (Salmo salar) and Atlantic cod (Gadus morhua). Comp Biochem Phys C 152:444–450. doi:10.1016/j.cbpc.2010.07.005

    Google Scholar 

  • Barber MC (2008) Dietary uptake models used for modeling the bioaccumulation of organic contaminants in fish. Environ Toxicol Chem 27:755–777. doi:10.1897/07-462.1

    Article  CAS  Google Scholar 

  • Benchalel W, Derbal F, Kara MH (2010) Régime alimentaire du sar commun Diplodus sargus sargus (Sparidae) des côtes de l’est algérien. Cybium 34:231–242

    Google Scholar 

  • Blanco J, Reyero MI, Franco J (2003) Kinetics of accumulation and transformation of paralytic shellfish toxins in the blue mussel Mytilus galloprovincialis. Toxicon 42:777–784. doi:10.1016/j.toxicon.2003.10.007

    Article  CAS  Google Scholar 

  • Castonguay M, Levasseur M, Beaulieu J-L, Grégoire F, Michaud S, Bonneau E, Bates SS (1997) Accumulation of PSP toxins in Atlantic mackerel: seasonal and ontogenic variations. J Fish Biol 50:1203–1213. doi:10.1111/j.1095-8649.1997.tb01648.x

    Article  CAS  Google Scholar 

  • Choi M-C, Hsieh DPH, Lam PKS, Wang W-X (2003) Field depuration and biotransformation of paralytic shellfish toxins in scallop Chlamys nobilis and green-lipped mussel Perna viridis. Mar Biol 143:927–934. doi:10.1007/s00227-003-1148-y

    Article  CAS  Google Scholar 

  • Choi M-C, Yu PKN, Hsieh DPH, Lam PKS (2006) Trophic transfer of paralytic shellfish toxins from clams (Ruditapes philippinarum) to gastropods (Nassarius festivus). Chemosphere 64:1642–1649. doi:10.1016/j.chemosphere.2006.01.036

    Article  CAS  Google Scholar 

  • Costa PR, Botelho MJ, Lefebvre KA (2010) Characterization of paralytic shellfish toxins in seawater and sardines (Sardina pilchardus) during blooms of Gymnodinium catenatum. Hydrobiologia 655:89–97. doi:10.1007/s10750-010-0406-5

    Article  CAS  Google Scholar 

  • Fast MD, Cembella AD, Ross NW (2006) In vitro transformation of paralytic shellfish toxins in the clams Mya arenaria and Protothaca staminea. Harmful Algae 5:79–90. doi:10.1016/j.hal.2005.05.005

    Article  CAS  Google Scholar 

  • Geraci JR, Anderson DM, Timperi RJ, St Aubin DJ, Early GA, Prescott JH, Mayo CA (1989) Humpback whales (Megaptera novaeangliae) fatally poisoned by dinoflagellate toxin. Can J Fisher Aquat Sci 46:1895–1898. doi:10.1139/f89-238

    Article  Google Scholar 

  • Gubbins MJ, Eddy FB, Gallacher S, Stagg RM (2000) Paralytic shellfish poisoning toxins induce xenobiotic metabolising enzymes in Atlantic salmon (Salmo salar). Mar Environ Res 50:479–483. doi:10.1016/S0141-1136(00)00095-7

    Article  CAS  Google Scholar 

  • Haya K, Martin JL, Waiwood BA, Burridge LE, Hungerford JM, Zitko V (1990) Identification of paralytic shellfish toxins in mackerel from southwest Bay of Fundy, Canada. In: Graneli E, Sundstrom B, Edler L, Anderson DM (eds) Toxic marine phytoplankton. Elsevier, New York, pp 350–355

    Google Scholar 

  • Jester RJ, Baugh KA, Lefebvre KA (2009) Presence of Alexandrium catenella and paralytic shellfish toxins in finfish, shellfsh and rock crabs in Monterey Bay, California, USA. Mar Biol 156:493–504. doi:10.1007/s00227-008-1103-z

    Article  CAS  Google Scholar 

  • Kodama M (2010) Paralytic shellfish poisoning toxins: biochemistry and origin. Aqua-Biosci Monogr 3:1–38

    Article  Google Scholar 

  • Kwong RWM, Wang WX, Lam PKS, Yu PKN (2006) The uptake, distribution and elimination of paralytic shellfish toxins in mussels and fish exposed to toxic dinoflagellates. Aquat Toxicol 80:82–91. doi:10.1016/j.aquatox.2006.07.016

    Article  CAS  Google Scholar 

  • Landsberg JH (2002) The effects of harmful algal blooms on aquatic organisms. Rev Fisher Sci 10:113–390. doi:10.1080/20026491051695

    Article  Google Scholar 

  • Lawrence JF, Niedzwiadek B (2001) Quantitative determination of paralytic shellfish poisoning toxins in shellfish by using prechromatographic oxidation and liquid chromatography with fluorescence detection. J AOAC Int 84:1099–1108

    CAS  Google Scholar 

  • Lefebvre KA, Elder NE, Hershberger PK, Trainer VL, Stehr CM, Scholz NL (2005) Dissolved saxitoxin causes transient inhibition of sensorimotor function in larval Pacific herring (Clupea harengus pallasi). Mar Biol 147:1393–1402. doi:10.1007/s00227-005-0048-8

    Article  CAS  Google Scholar 

  • Leitão F, Santos MN, Monteiro CC (2007) Contribution of artificial reefs to the diet of the white sea bream (Diplodus sargus). ICES J Mar Sci 64:473–478. doi:10.1093/icesjms/fsm027

    Article  Google Scholar 

  • Lin H-P, Cho Y, Yashiro H, Yamada T, Oshima Y (2004) Purification and characterization of paralytic shellfish toxin transforming enzyme from Mactra chinensis. Toxicon 44:457–468. doi:10.1016/j.toxicon.2004.07.024

    Article  Google Scholar 

  • Llewellyn LE (2006) Saxitoxin, a toxic marine natural product that targets a multitude of receptors. Nat Prod Rep 23:200–222. doi:10.1039/B501296c

    Article  CAS  Google Scholar 

  • Monteiro A, Costa PR (2011) Distribution and selective elimination of paralytic shellfish toxins in different tissues of Octopus vulgaris. Harmful Algae (in press) doi:10.1016/j.hal.2011.06.004

  • Montoya NG, Akselman R, Franco J, Carreto JI (1996) Paralytic shellfish toxins and mackerel (Scomber japonicus) mortality in the Argentine Sea. In: Yasumoto T, Oshima Y, Fukuyo Y (eds) Harful and toxic algal blooms. Intergovernmental Oceanographic Commission of UNESCO, Paris, pp 417–420

    Google Scholar 

  • Montoya NG, Reyero MI, Akselman R, Franco M, Carreto JI (1998) Paralytic shellfish toxins in the anchovy Engraulis anchiota from the Argentinian coast. In: Reguera B, Blanco J, Fernández ML, Wyatt T (eds) Harmful Algae. Xunta de Galicia and Intergovernmental Oceanographic Commission of UNESCO, Santiago de Compostela, pp 72–73

    Google Scholar 

  • Negri AP, Stirling D, Quilliam M, Blackburn S, Bolch C, Burton I, Eaglesham G, Thomas K, Walter J, Willis R (2003) Three novel hydroxybenzoate saxitoxin analogues isolated from the dinoflagellate Gymnodinium catenatum. Chem Res Toxicol 16:1029–1033. doi:10.1021/tx034037j

    Article  CAS  Google Scholar 

  • Negri AP, Bolch CJS, Geier S, Green DH, Park T-G, Blackburn SI (2007) Widespread presence of hydrophobic paralytic shellfish toxins in Gymnodinium catenatum. Harmful Algae 6:774–780. doi:10.1016/j.hal.2007.04.001

    Article  CAS  Google Scholar 

  • Oshima Y (1995) Chemical and enzymatic transformation of paralytic shellfish toxins in marine organisms. In: Lassus P, Arzul G, Erard E, Gentian P, Marcaillou C (eds) Harmful marine algal blooms. Lavoisier Publishers, Paris, pp 475–480

    Google Scholar 

  • Osman AM, Mahmoud HH (2009) Feeding biology of Diplodus sargus and Diplodus vulgaris (Teleostei, Sparidae) in Egyptian Mediterranean waters. World J Fish Mar Sci 1:290–296

    Google Scholar 

  • Penry DL (1998) Applications of efficiency measurements in bioaccumulation studies: definitions, clarifications, and a critique of methods. Environ Toxicol Chem 17:1633–1639. doi:10.1002/etc.5620170827

    Article  CAS  Google Scholar 

  • Reyero M, Cacho E, Martínez A, Vázquez J, Marina A, Fraga S, Franco JM (1999) Evidence of saxitoxin derivatives as causative agents in the 1997 mass mortality of monk seals in the Cape Blanc Peninsula. Nat Toxins 7:311–315. doi:10.1002/1522-7189(199911/12)7:6<311:AID-NT75>3.0.CO;2-I

    Article  CAS  Google Scholar 

  • Robineau B, Gagné JA, Fortier L, Cembella AD (1991) Potential impact of a toxic dinoflagellate (Alexandrium excavatum) bloom on survival of fish and crustacean larvae. Mar Biol 108:293–301. doi:10.1007/bf01344344

    Article  Google Scholar 

  • Sakamoto S, Sato S, Ogata T, Kodama M (2000) Formation of intermediate conjugates in the reductive transformation of gonyautoxins to saxitoxins by thiol compounds. Fisher Sci 66:136–141. doi:10.1046/j.1444-2906.2000.00020.x

    Article  CAS  Google Scholar 

  • Samson JC, Shumway SE, Weis JS (2008) Effects of the toxic dinoflagellate, Alexandrium fundyense on three species of larval fish: a food-chain approach. J Fish Biol 72:168–188. doi:10.1111/j.1095-8649.2007.01698.x

    Article  CAS  Google Scholar 

  • Sato S, Ogata T, Kodama M (1993) Wide distribution of toxins with sodium channel blocking activity similar to tetrodotoxin and paralytic shellfish toxins in marine animals. In: Smayda TJ, Shimizu Y (eds) Toxic phytoplankton blooms in the sea. Elsevier, Amsterdam, pp 429–434

    Google Scholar 

  • Sato S, Sakai R, Kodama M (2000) Identification of thioether intermediates in the reductive transformation of gonyautoxins into saxitoxins by thiols. Bioorg Med Chem Lett 10:1787–1789. doi:10.1016/S0960-894X(00)00332-2

    Article  CAS  Google Scholar 

  • Sephton DH, Haya K, Martin JL, LeGresley MM, Page FH (2007) Paralytic shellfish toxins in zooplankton, mussels, lobsters and caged Atlantic salmon, Salmo salar, during a bloom of Alexandrium fundyense off Grand Manan Island, in the Bay of Fundy. Harmful Algae 6:745–758. doi:10.1016/j.hal.2007.03.002

    Article  CAS  Google Scholar 

  • Shimizu Y (2000) Paralytic shellfish poisoning. Chemistry and mechanism of action. In: Botana LM (ed) Seafood and freshwater toxins. Marcel Dekker, New York, pp 151–172

    Google Scholar 

  • Silvert WL, Cembella AD (1995) Dynamic modeling of phycotoxin kinetics in the blue mussel, Mytilus edulis, with implications for other marine invertebrates. Can J Fish Aquat Sci 52:521–531. doi:10.1139/f95-053

    Article  CAS  Google Scholar 

  • Sullivan JJ, Iwaoka WT, Liston J (1983) Enzymatic transformation of PSP toxins in the littleneck clam (Protothaca staminea). Biochem Biophys Res Commun 114:465–472. doi:10.1016/0006-291X(83)90803-3

    Article  CAS  Google Scholar 

  • White AW (1977) Dinoflagellate toxins as probable cause of an Atlantic herring (Clupea harengus harengus) kill, and pteropods as apparent vector. J Fish Res Board Can 34:2421–2424. doi:10.1139/f77-328

    Article  CAS  Google Scholar 

  • White AW (1981) Marine zooplankton can accumulate and retain dinoflagellate toxins and cause fish kills. Limnol Oceanogr 26:103–109

    Article  Google Scholar 

  • White AW (1984) Paralytic shellfish toxins and finfish. In: Ragelis EP (ed) Seafood Toxins. ACS Symposium series 262:171–180

  • Wiese M, D’Agostino PM, Mihali TK, Moffitt MC, Neilan BA (2010) Neurotoxic alkaloids: saxitoxin and its analogs. Mar Drugs 8:2185–2211. doi:10.3390/md8072185

    Article  CAS  Google Scholar 

  • Yu KN, Kwong RWM, Wang W-X, Lam PKS (2007) Biokinetics of paralytic shellfish toxins in the green-lipped mussel, Perna viridis. Mar Pollut Bull 54:1068–1071. doi:10.1016/j.marpolbul.2007.02.007

    Article  CAS  Google Scholar 

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Acknowledgments

The Portuguese Foundation for Science and Technology (FCT) supported this study through the research grant PTDC/MAR/78997/2006. C. Vale and M. J. Botelho (IPIMAR) provided valuable comments to earlier drafts of this manuscript. We also appreciate the very valuable suggestions given by M. Peck and two anonymous reviewers.

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Authors and Affiliations

  1. IPIMAR—National Institute for Biological Resources (INRB/IPIMAR), Av. Brasília, 1449-006, Lisbon, Portugal

    Pedro Reis Costa & Sandra Lage

  2. IPIMAR—National Institute for Biological Resources (INRB/IPIMAR), Av. 5 Outubro, 8700-305, Olhão, Portugal

    Marisa Barata & Pedro Pousão-Ferreira

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  1. Pedro Reis Costa
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  2. Sandra Lage
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Correspondence to Pedro Reis Costa.

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Communicated by M. A. Peck.

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Costa, P.R., Lage, S., Barata, M. et al. Uptake, transformation, and elimination kinetics of paralytic shellfish toxins in white seabream (Diplodus sargus). Mar Biol 158, 2805–2811 (2011). https://doi.org/10.1007/s00227-011-1779-3

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