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Lethal effects of Northwest Atlantic Ocean isolates of the dinoflagellate, Scrippsiella trochoidea, on Eastern oyster (Crassostrea virginica) and Northern quahog (Mercenaria mercenaria) larvae

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Abstract

The thecate dinoflagellate Scrippsiella trochoidea is a cosmopolitan, bloom-forming alga that has been generally considered non-toxic. Here, we report that environmentally relevant cell densities (104 cells mL−1) of Scrippsiella trochoidea strains isolated from the Northwest Atlantic Ocean caused 100% mortality in Eastern oyster (Crassostrea virginica) larvae during 3-day exposures while parallel control larvae exhibited 100% survival. S. trochoidea also exhibited lethal effects on Northern quahog (Mercenaria mercenaria) larvae (70% mortality during 3-day exposure) but were non-toxic to juvenile fish (Cyprinodon variegates). The cultures of S. trochoidea were more lethal to Northern quahog larvae than ten other species of harmful algae, including the highly toxic species Cochlodinium polykrikoides. Scrippsiella trochoidea cultures within later stages of growth were more toxic than exponential growth stages to bivalve larvae, and the toxicity was dose dependent. Furthermore, toxicity was maintained in the cultures that were sonicated, boiled, and frozen as well as in resuspended residues of the culture but was significantly lower in cell-free culture media. Collectively, these results suggest that S. trochoidea causes mortality in bivalve larvae through a physicochemical rather than strictly chemical mechanism, such as clogging of larval feeding apparatuses by materials produced by S. trochoidea (e.g., lipids, extracellular polysaccharides, and/or cell debris) which accumulate as cells in culture or blooms age. This is the first report of the lethal effects of Scrippsiella trochoidea on shellfish larvae.

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References

  • Alonso-Rodríguez R, Páez-Osuna F (2003) Nutrients, phytoplankton and harmful algal blooms in shrimp ponds: a review with special reference to the situation in the Gulf of California. Aquaculture 219(1–4):317–336

    Article  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  Google Scholar 

  • Anderson DM, Burkholder JM, Cochlan WP, Glibert PM, Gobler CJ, Heil CA, Kudela RM, Parsons ML, Rensel JEJ, Townsend DW, Trainer VL, Vargo GA (2008) Harmful algal blooms and eutrophication: examples of linkages from selected coastal regions of the United States. Harmful Algae 8:39–53

    Article  CAS  Google Scholar 

  • Arnold WS (2008) Application of larval release for restocking and stock enhancement of coastal marine bivalve populations. Rev Fisheries Sci 16:65–71

    Article  Google Scholar 

  • Barber BJ, Blake NJ (1983) Growth and reproduction of the bay scallop, Argopecten irradians (Lamarck) at its southern distributional limit. J Exp Mar Biol Ecol 66:247–256

    Article  Google Scholar 

  • Bardouil M, Bohec M, Cormerais M, Bougrier S, Lassus P (1993) Experimental study of the effects of a toxic microalgal diet on feeding of the oyster Crassostrea gigas Thunberg. J Shellfish Res 12:417–422

    Google Scholar 

  • Bricelj VM, MacQuarrie SP (2007) Effects of brown tide (Aureococcus anophagefferens) on hard clam Mercenaria mercenaria larvae and implications for benthic recruitment. Mar Ecol Prog Ser 331:147–159

    Article  Google Scholar 

  • Bricelj VM, MacQuarrie SP, Schaffner RA (2001) Differential effects of Aureococcus anophagefferens isolates (“brown tide”) in unialgal and mixed suspensions on bivalve feeding. Mar Biol 139:605–615

    Article  Google Scholar 

  • Carriker MR (2001) Functional morphology and behavior of shelled veligers and early juveniles. In: Kraeuter JN, Castagna M (eds) Biology of the hard clam. Elsevier Science, New York, pp 283–302

    Chapter  Google Scholar 

  • Cembella AD, Lewis NI, Quilliam MA (2000) The marine dinoflagellate Alexandrium ostenfeldii (Dinophyceae) as the causative organism of spirolide shellfish toxins. Phycologia 39:67–74

    Article  Google Scholar 

  • Daugbjerg N, Hansen G, Larsen J, Moestrup Ø (2000) Phylogeny of some of the major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of three new genera of unarmoured dinoflagellates. Phycologia 39:302–317

    Article  Google Scholar 

  • Doblin MA, Blackburn SI, Hallegraeff GM (1999) Growth and biomass stimulation of the toxic dinoflagellate Gymnodinium catenatum (Graham) by dissolved organic substances. J Exp Mar Biol Ecol 236:33–47

    Article  CAS  Google Scholar 

  • Dodge JD (1982) Marine dinoflagellates of the British Isles. Her Majesty’s Stationary Office, London, p 303

    Google Scholar 

  • Frehi H, Couté A, Mascarell G, Perrette-Gallet C, Ayada M, Kara MH (2007) Harmful and red-tide dinoflagellates in the Annaba bay (Algeria). Comptes Rendus Biologies 330:615–628

    Article  Google Scholar 

  • Fulco VK (2007) Harmful effects of the toxic dinoflagellate Alexandrium tamarense on the tintinnids Favella taraikaensis and Eutintinnus sp. J Mar Biol Ass UK 87:1085–1088

    CAS  Google Scholar 

  • Gárate-Lizárraga I, Band-Schmidt CJ, López-Cortés DJ, Muñetón-Gómez Mdel S (2009) Bloom of Scrippsiella trochoidea (Gonyaulacaceae) in a shrimp pond in the southwestern Gulf of California, Mexico. Mar Pollut Bull 58(1):145–149

    Article  Google Scholar 

  • Gu H, Sun J, Kooistra WHCF, Zeng R (2008) Phylogenetic position and morphology of thecae and cysts of Scrippsiella (Dinophyceae) species in the East China Sea. J Phycol 44:478–494

    Article  CAS  Google Scholar 

  • Hallegraeff GM (1992) Harmful algal blooms in the Australian region. Mar Pollut Bull 25:186–190

    Article  Google Scholar 

  • Hallegraeff GM (2003) Harmful algal blooms: a global overview. In: Hallegraeff GM, Anderson DM, Cembella AD (eds) Manual on harmful marine microalgae. UNESCO, Paris, pp 25–49

    Google Scholar 

  • Harvey HR, Bradshaw SA, Ohara SCM, Eglinton G, Corne EDS (1988) Lipid-composition of the marine dinoflagellate Scrippsiella-trochoidea. Phytochemistry 27:1723–1729

    Article  CAS  Google Scholar 

  • Heisler J, Glibert P, Burkholder J, Anderson DM, Cochlan W, Dennison W, Dortch Q, Gobler CJ, Heil C, Humphries E, Lewitus A, Magnien R, Marshall H, Sellner K, Stockwell D, Stoecker D, Suddleson M (2008) Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae 8:3–13

    Article  CAS  Google Scholar 

  • Hesselman DM, Barber BJ, Blake NJ (1989) The reproductive cycle of adult hard clams, Mercenaria spp. in the Indian River Lagoon, Florida. J Shellfish Res 8:43–49

    Google Scholar 

  • Hold GL, Smith EA, Rappe MS, Maas EW, Moore ERB, Stroempl C, Stephen JR, Prosser JI, Birkbeck TH, Gallacher S (2001) Characterization of bacterial communities associated with toxic and non-toxic dinoflagellates: Alexandrium spp. and Scrippsiella trochoidea. FEMS Microbiol Ecol 37(2):161–173

    Article  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  CAS  Google Scholar 

  • Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–638

    Article  CAS  Google Scholar 

  • Janofske D (2000) Scrippsiella trochoidea and Scrippsiella regalis, nov. comb. (Peridiniales, Dinophyceae): a comparison. J Phycol 36:178–189

    Article  Google Scholar 

  • Jeong HJ, Yoon JY, Kim JS, Yoo YD, Seong KA (2002) Growth and grazing rates of the prostomatid ciliate Tiarina fusus on red-tide and toxic algae. Aquat Microb Ecol 28:289–297

    Article  Google Scholar 

  • Jeong HJ, Park KH, Kim JS, Kang HJ, Kim CH, Choi HJ, Kim YS, Park JY, Park MG (2003) Reduction in the toxicity of the dinoflagellate Gymnodinium catenatum when fed on by the heterotrophic dinoflagellate Polykrikos kofoidii. Aquat Microb Ecol 31:307–312

    Article  Google Scholar 

  • Jeong HJ, Song JY, Lee CH, Kim ST (2004) Feeding by larvae of the mussel Mytilus galloprovincialis on red-tide dinoflagellates. J Shellfish Res 23:185–195

    Google Scholar 

  • Kemp WM, Boynton WR, Adolf JE, Boesch DF, Boicourt WC, Brush G, Cornwell JC, Fisher TR, Glibert PM, Hagy JD, Harding LW, Houde ED, Kimmel DG, Miller WD, Newell RIE, Roman MR, Smith EM, Stevenson JC (2005) Eutrophication of Chesapeake Bay: historical trends and ecological interactions. Mar Ecol Prog Ser 303:1–29

    Article  Google Scholar 

  • Lassus P, Bardouil M, Beliaeff B, Masselin P, Naviner M, Truquet P (1999) Effect of a continuous supply of the toxic dinoflagellate Alexandrium minutum Halim on the feeding behavior of the Pacific oyster (Crassostrea gigas Thunberg). J Shellfish Res 18:211–216

    Google Scholar 

  • Leverone JR, Blake NJ, Pierce RH, Shumway SE (2006) Effects of the dinoflagellate Karenia brevis on larval development in three species of bivalve mollusc from Florida. Toxicon 48:75–84

    Article  CAS  Google Scholar 

  • Lirdwitayaprasit T, Okaichi T, Montani S, Ochi T, Anderson DM (1990) Changes in cell chemical-composition during the life-cycle of Scrippsiella-trochoidea (Dinophyceae). J Phycol 26:299–306

    Article  CAS  Google Scholar 

  • Lotze HK, Lenihan HS, Bourque BJ, Bradbury RH, Cooke RG, Kay MC, Kidwell SM, Kirby MX, Peterson CH, Jackson JBC (2006) Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312:1806–1809

    Article  CAS  Google Scholar 

  • Marshall HG (2009) Phytoplankton of the York River. J Coast Res (Suppl 57):59–65

  • Montresor M, Sgrosso S, Procaccini G, Kooistra WHCF (2003) Intraspecific diversity in Scrippsiella trochoidea (Dinopbyceae): evidence for cryptic species. Phycologia 42:56–70

    Article  Google Scholar 

  • Myers RA, Baum JK, Shepherd TD, Powers SP, Peterson CH (2007) Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315:1846–1850

    Article  CAS  Google Scholar 

  • Nylander JAA (2004) MrModeltest v2 (program distributed by the author). Evolutionary Biology Centre, Uppsala University, Uppsala

    Google Scholar 

  • Oshima Y, Yamada SH, Matsunaga K, Moriya T, Ohizumi Y (1994) A monogalactosyl diacylglycerol from a cultured marine dinoflagellate, Scrippsiella trochoidea. J Natural Products 57:534–536

    Article  CAS  Google Scholar 

  • Padilla DK, Doall MH, Gobler CJ, Hartson A, O’Boyle K (2006) Brown tide alga, Aureococcus anophagefferens, can affect growth but not survivorship of Mercenaria mercenaria larvae. Harmful Algae 5:736–748

    Article  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  Google Scholar 

  • Qi YZ, Chen JF, Wang ZH, Xu N, Wang Y, Shen PP, Lu SH, Hodgkiss IJ (2004) Some observations on harmful algal bloom (HAB) events along the coast of Guangdong, southern China in 1998. Hydrobiologia 512:209–214

    Article  Google Scholar 

  • Qin XM, Zou JZ (1997) Studies on the effects of N, P, Fe-EDTA, Mn on the growth of a red tide dinoflagellate Scrippsiella trochoidea. Chin Limnol Oceanogr 28:594–598

    CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  Google Scholar 

  • Scholin CA, Villac MC, Buck KR, Krupp JM, Powers DA, Fryxell GA, Chavez EP (1994) Ribosomal DNA sequences discriminate among toxic and non-toxic Pseudonitzschia species. Nat Toxins 2:152–165

    Article  CAS  Google Scholar 

  • Shin K, Jang MC, Jang PK, Ju SJ, Lee TK, Chang M (2003) Influence of food quality on egg production and viability of the marine planktonic copepod Acartia omorii. Prog Oceanog 57:265–277

    Article  Google Scholar 

  • Shumway SE, Burkholder JM, Springer J (2006) Effects of the estuarine dinoflagellate Pfiesteria shumwayae (Dinophyceae) on survival and grazing activity of several shellfish species. Harmful Algae 5:442–458

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1994) Biometry: the principles and practice of statistics in biological research, 3rd edn. Freeman, New York

    Google Scholar 

  • Springer J, Shumway SE, Burkholder JM, Glasgow HB (2002) Interactions between two commercially important species of bivalves and the toxic estuarine dinoflagellate, Pfiesteria piscicida. Mar Ecol Prog Ser 245:1–10

    Article  Google Scholar 

  • Steidinger KA, Tangen K (1997) Dinoflagellates. In: Tomas CR (ed) Identifying marine diatoms and dinoflagellates. Academic Press, Inc., San Diego, pp 387–589

    Google Scholar 

  • Stoecker DK, Adolf JE, Place AR, Glibert PM, Meritt DW (2008) Effects of the dinoflagellates Karlodinium veneficum and Prorocentrum minimum on early life history stages of the Eastern oyster (Crassostrea virginica). Mar Biol 154:81–90

    Article  Google Scholar 

  • Sykes PF, Huntley ME (1987) Acute physiological reactions of Calanus pacificus to selected dinoflagellates: direct observations. Mar Biol 94:19–24

    Article  Google Scholar 

  • Talmage SC, Gobler CJ (2009) The effects of elevated carbon dioxide concentrations on the metamorphosis, size, and survival of larval hard clams (Mercenaria mercenaria), bay scallops (Argopecten irradians), and Eastern oysters (Crassostrea virginica). Limnol Oceanogr 54:2072–2080

    Article  Google Scholar 

  • Tang YZ, Gobler CJ (2009a) Characterization of the toxicity of Cochlodinium polykrikoides isolates from Northeast US estuaries to finfish and shellfish. Harmful Algae 8:454–462

    Article  CAS  Google Scholar 

  • Tang YZ, Gobler CJ (2009b) Cochlodinium polykrikoides blooms and clonal isolates from the northwest Atlantic coast cause rapid mortality in multiple species of bivalve larvae. Mar Biol 156:2601–2611

    Article  CAS  Google Scholar 

  • Tang YZ, Gobler CJ (2010) Allelopathic effect of Cochlodinium polykrikoides isolates and bloom water from North America on co-occurring phytoplankton. Mar Ecol Prog Ser 406:19–31

    Article  Google Scholar 

  • Tang YZ, Kong LS, Holmes MJ (2007) Dinoflagellate Alexandrium leei (Dinophyceae) from Singapore coastal waters produces a water-soluble ichthyotoxin. Mar Biol 150:541–549

    Article  CAS  Google Scholar 

  • Tang XH, Yu RC, Zhang QC, Wang YF, Yan T, Zhou MJ (2010) Molecular phylogenetic analysis of dinoflagellate Scrippsiella trochoidea isolated from the East Asian waters. Chin J Oceanol Limnol 28:323–328

    Article  CAS  Google Scholar 

  • Terenko L, Terenko G (2009) Dynamics of Scrippsiella trochoidea (Stein) Balech 1988 (Dinophyceae) blooms in Odessa Bay of the Black Sea (Ukraine). Oceanol Hydrobiol Stud 38(Supl 2):107–112

    Google Scholar 

  • Thompson RJ, Newell RIE, Kennedy VS, Mann R (1996) Chapter 9. Reproductive processes and early development. In: Kennedy VS, Newell RIE, Eble AF (eds) The Eastern oyster Crassostrea virginica. Maryland Sea Grant College, College Park, pp 335–370

    Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 25:4876–4882

    Article  CAS  Google Scholar 

  • Villarino ML, Figueiras FG, Jones KJ, Alvarezsalgado XA, Richard J, Edwards A (1995) Evidence of in situ diel vertical migration of a red-tide microplankton species in Ria de Vigo (NW Spain). Mar Biol 123:607–617

    Article  Google Scholar 

  • Wang Y, Tang XX (2008) Interactions between Prorocentrum donghaiense Lu and Scrippsiella trochoidea (Stein) Loeblich III under laboratory culture. Harmful Algae 7:65–75

    Article  Google Scholar 

  • Wang ZH, Qi YZ, Yang YF (2007) Cyst formation: an important mechanism for the termination of Scrippsiella trochoidea (Dinophyceae) bloom. J Plankton Res 29:209–218

    Article  Google Scholar 

  • Wikfors GH, Smolowitz RM (1995) Experimental and histological studies of 4 life-history stages of the Eastern oyster, Crassostrea virginica, exposed to a cultured strain of the dinoflagellate Prorocentrum minimum. Biol Bull 188:313–328

    Article  Google Scholar 

  • Yan T, Zhou M, Fu M, Wang Y, Yu R, Li J (2001) Inhibition of egg hatching success and larvae of the scallop, Chlamys farreri, associated with exposure to cells and cell fragments of the dinoflagellate Alexandrium tamarense. Toxicon 39:1239–1244

    Article  CAS  Google Scholar 

  • Yan T, Zhou M, Fu M, Yu R, Wang Y, Li J (2003) Effects of the dinoflagellate Alexandrium tamarense on early development of the scallop Argopecten irradians concentricus. Aquaculture 217:167–178

    Article  Google Scholar 

  • Yu J, Tang DL, Oh IS, Yao LJ (2007) Response of harmful algal blooms to environmental changes in Daya Bay, China. Terr Atmos Ocean Sci 18:1011–1027

    Article  Google Scholar 

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Acknowledgments

We acknowledge the financial support from Suffolk County Department of Health Services, Office of Ecology and the New Tamarind Foundation. We thank Drs. MJ Holmes (National University of Singapore, Singapore) and Gregg Rivara at the Cornell Cooperative Extension shellfish hatchery facility in Southold, New York for providing microalagl cultures and bivalve larvae. We are grateful to Matthew Harke for assisting with the phylogenetic analysis. We also thank Ning Xu, Heidi Mittelsdorf, Ayodeji Ajayi, and Stephanie C. Talmage for technical assistance.

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Correspondence to Ying Zhong Tang or Christopher J. Gobler.

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Communicated by U. Sommer.

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Tang, Y.Z., Gobler, C.J. Lethal effects of Northwest Atlantic Ocean isolates of the dinoflagellate, Scrippsiella trochoidea, on Eastern oyster (Crassostrea virginica) and Northern quahog (Mercenaria mercenaria) larvae. Mar Biol 159, 199–210 (2012). https://doi.org/10.1007/s00227-011-1800-x

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