Oceanography The Official Magazine of
The Oceanography Society
Volume 30 Issue 01

View Issue TOC
Volume 30, No. 1
Pages 36 - 45

OpenAccess

Harmful Algal Blooms in Benthic Systems: Recent Progress and Future Research

By Elisa Berdalet , Patricia A. Tester, Mireille Chinain, Santiago Fraga, Rodolphe Lemée, Wayne Litaker, Antonella Penna, Gires Usup, Magda Vila, and Adriana Zingone 
Jump to
Article Abstract Citation References Copyright & Usage
Article Abstract

Shallow, well-illuminated coastal waters from tropical to temperate latitudes are attractive environments for humans. Beaches and coral reefs have provided lodging and food to coastal communities for centuries. Unfortunately, tropical regions traditionally have been threatened by outbreaks of the toxic benthic dinoflagellate Gambierdiscus, which is associated with ciguatera fish poisoning. The ciguatoxins produced by Gambierdiscus bioaccumulate in reef fishes and are responsible for the most common algal toxin-related illnesses, globally affecting the greatest number of victims and often with significant long-term health effects. Recently, Gambierdiscus has been documented in subtropical and temperate latitudes. Blooms of another benthic and toxic dinoflagellate, Ostreopsis, have become more frequent and intense, especially in temperate waters. Ostreopsis produces palytoxins and analogues, and some outbreaks have been associated with massive benthic faunal damage and respiratory irritations in humans exposed to aerosols. The increased frequency of harmful events and the biogeographic extension of benthic microalgae incentivized the launch of the Global Ecology and Oceanography of Harmful Algal Blooms (GEOHAB) Core Research Project on “Benthic Harmful Algal Blooms” in 2010. This article summarizes the main scientific advances and gaps in related knowledge as well as advances the project has made toward managing and mitigating the impacts of benthic HABs on human illnesses and marine resource losses.

Citation

Berdalet, E., P.A. Tester, M. Chinain, S. Fraga, R. Lemée, W. Litaker, A. Penna, G. Usup, M. Vila, and A. Zingone. 2017. Harmful algal blooms in benthic systems: Recent progress and future research. Oceanography 30(1):36–45, https://doi.org/10.5670/oceanog.2017.108.

References
    Accoroni, S, T. Romagnoli, A. Penna, S. Capelacci, P. Ciminiello, C. Dell’Aversano, L. Tartaglione, M. Abboud-Abi Saab, V. Giussani, V. Asnaghi, and M. Chiantore. 2016. Ostreopsis fatturussoi sp. nov. (Dinophyceae), a new benthic toxic Ostreopsis species from the eastern Mediterranean Sea. Journal of Phycology 52:1,064–1,084, https://doi.org/10.1111/jpy.12464.
  1. Accoroni, S., and C. Toti. 2016. The toxic benthic dinoflagellates of the genus Ostreopsis in temperate areas: A review. Advances in Oceanography and Limnology 7:1–15, https://doi.org/10.4081/aiol.2016.5591.
  2. Aligizaki, K., P. Katikou, G. Nikolaidis, and A. Panou. 2008. First episode of shellfish contamination by palytoxin-like compounds from Ostreopsis species (Aegean Sea, Greece). Toxicon 51:418–427, https://doi.org/10.1016/j.toxicon.2007.10.016.
  3. Bienfang, P., B. Oben, S. DeFelice, P. Moeller, K. Huncik, P. Oben, R. Tooen, T. Daly-Engel, and B. Bowen. 2008. Ciguatera: The detection of neurotoxins in carnivorous reef fish from the coast of Cameroon, West Africa. African Journal of Marine Science 30:533–540, https://doi.org/10.2989/AJMS.2008.30.3.8.642.
  4. Biré, R., S. Trotereau, R. Lemée, D. Oregioni, C. Delpont, S. Krys, and T. Guérin. 2015. Hunt for palytoxins in a wide variety of marine organisms harvested in 2010 on the French Mediterranean coast. Marine Drugs 13:5,425–5,446, https://doi.org/10.3390/md13085425.
  5. Blanfuné, A., C.F. Boudouresque, H. Grossel, and T. Thierry. 2015. Distribution and abundance of Ostreopsis spp. and associated species (Dinophyceae) in the northwestern Mediterranean: The region and the macroalgal substrate matter. Environmental Science and Pollution Research 22:12,332–12,346, https://doi.org/10.1007/s11356-015-4525-4
  6. Boada, L.D., M. Zumbado, O.P. Luzardo, M. Almeida-González, S.M. Plakas, H.R. Granade, A. Abraham, E.L.E. Jester, and R.W. Dickey. 2010. Ciguatera fish poisoning on the West Africa Coast: An emerging risk in the Canary Islands (Spain). Toxicon 56:1,516–1,519, https://doi.org/10.1016/​j.toxicon.2010.07.021.
  7. Bravo, I., and R. Figueroa. 2014. Towards an ecological understanding of dinoflagellate cyst functions. Microorganisms 2:11–32, https://doi.org/10.3390/microorganisms2010011.
  8. Bravo, I., R.I. Figueroa, and S. Fraga. 2014. Cellular and nuclear morphological variability within a single species of the toxigenic dinoflagellate genus Gambierdiscus: Relationship to life-cycle processes. Harmful Algae 40:1–8, https://doi.org/10.1016/j.hal.2014.09.009.
  9. Brissard, C., C. Herrenknecht, V. Séchet, F. Hervé, F. Pisapia, J. Harcouet, R. Lémée, N. Chomérat, P. Hess, and Z. Amzil. 2014. Complex toxin profile of French Mediterranean Ostreopsis cf. ovata strains, seafood accumulation and ovatoxins prepurification. Marine Drugs 12:2,851–2,876, https://doi.org/10.3390/md12052851.
  10. Caillaud, A., P. De la Iglesia, H.T. Darius, S. Pauillac, K. Aligizaki, S. Fraga, M. Chinain, and J. Diogène. 2010. Update on methodologies available for ciguatoxin determination: Perspectives to confront the onset of ciguatera fish poisoning in Europe. Marine Drugs 8:1,838–1,907, https://doi.org/10.3390/md8061838.
  11. Carella, F., A. Sardo, O. Mangoni, D. Di Cioccio, G. Urciuolo, G. De Vico, and A. Zingone. 2015. Quantitative histopathology of the Mediterranean mussel (Mytilus galloprovincialis L.) exposed to the harmful dinoflagellate Ostreopsis cf. ovata. Journal of Invertebrate Pathology 127:130–140, https://doi.org/10.1016/j.jip.2015.03.001.
  12. Casabianca, S., A. Casabianca, P. Riobó, J.M. Franco, M. Vila, and A. Penna. 2013. Quantification of the toxic dinoflagellate Ostreopsis spp. by qPCR assay in marine aerosol. Environmental Science and Technology 47:3,788–3,795, https://doi.org/10.1021/es305018s.
  13. Centers for Disease Control and Prevention. 2013. Ciguatera fish poisoning: New York City, 2010–2011. Morbidity and Mortality Weekly Report 62:61–65, https://www.cdc.gov/mmwr/preview/mmwrhtml/mm6204a1.htm.
  14. Chateau-Degat, M.-L., E. Dewailly, N. Cerf, N.L. Nguyen, M.-O. Huin-Blondey, B. Hubert, F. Laudon, and R. Chansin. 2007. Temporal trends and epidemiological aspects of ciguatera in French Polynesia: A 10-year analysis. Tropical Medicine and International Health 12:485–492, https://doi.org/10.1111/j.1365-3156.2006.01798.x.
  15. Chinain, M., H.T. Darius, A. Ung, P. Cruchet, Z. Wang, D. Ponton, D. Laurent, and S. Pauillac. 2010a. Growth and toxin production in the ciguatera-​causing dinoflagellate Gambierdiscus polynesiensis (Dinophyceae) in culture. Toxicon 56:739–750, https://doi.org/10.1016/​j.toxicon.2009.06.013.
  16. Chinain, M., H.T. Darius, A. Ung, M. Tchou Fouc, T. Revel, P. Cruchet, S. Pauillac, and D. Laurent. 2010b. Ciguatera risk management in French Polynesia: The case study of Raivavae Island (Australes Archipelago). Toxicon 56: 674–690, https://doi.org/10.1016/j.toxicon.2009.05.032.
  17. Ciminiello, P., C. Dell’Aversano, E. Dello Iacovo, E. Fattorusso, M. Forino, L. Grauso, L. Tartaglione, F. Guerrini, and R. Pistocchi. 2010. Complex palytoxin-like profile of Ostreopsis ovata: Identification of four new ovatoxins by high-​resolution liquid chromatography/mass spectrometry. Rapid Communications in Mass Spectrometry 24:2,735–2,744, https://doi.org/​10.1002/rcm.4696
  18. Ciminiello, P., C. Dell’Aversano, E. Dello Iacovo, E. Fattorusso, M. Forino, L. Tartaglione, G. Benedettini, M. Onorari, F. Serena, C. Battocchi, and others. 2014. First finding of Ostreopsis cf. ovata toxins in marine aerosols. Environmental Science and Technology 48:3,532–3,540, https://doi.org/10.1021/es405617d.
  19. Cohu, S., L. Mangialajo, T. Thibaut, A. Blanfuné, S. Marro, and R. Lemé. 2013. Proliferation of the toxic dinoflagellate Ostreopsis cf. ovata in relation to depth, biotic substrate and environmental factors in the North West Mediterranean Sea. Harmful Algae 24:32–44, https://doi.org/10.1016/​j.hal.2013.01.002.
  20. Cohu, S., T. Thibaut, L. Mangialajo, J.-P. Labat, O. Passafiume, A. Blanfuné, N. Simon, J.-L. Cottalorda, and R. Lemée. 2011. Occurrence of the toxic dinoflagellate Ostreopsis cf. ovata in relation with environmental factors in Monaco (NW Mediterranean). Marine Pollution Bulletin 62:2,681–2,691, https://doi.org/10.1016/​j.marpolbul.2011.09.022.
  21. David, H., U. Ganzedo, A. Laza-Martínez, and E. Orive. 2012. Relationships between the presence of (Dinophyceae) in the Atlantic coast of the Iberian Peninsula and sea-surface temperature. Cryptogamie, Algologie 33:199–207, https://doi.org/10.7872/crya.v33.iss2.2011.199.
  22. Delgado, G., C.H. Lechuga-Deveze, G. Popowski, L. Troccoli, and C.A. Salinas. 2006. Epiphytic dinoflagellates associated with ciguatera in the northwestern coast of Cuba. Revista de Biología Tropical 54:299–310, https://doi.org/10.15517/rbt.v54i2.13870.
  23. Di Cioccio, D., M.C. Buia, and A. Zingone. 2014. Ocean acidification will not deliver us from Ostreopsis. Pp. 85–88 in Harmful Algae 2012. Proceedings of the 15th International Conference on Harmful Algae. International Society for the Study of Harmful Algae, Changwon, Korea. H.G. Kim, B. Reguera, G. Hallegraeff, C.K. Lee, M.S. Han, and J.K. Choi, eds.
  24. Durand-Clément, M., and A. Couté. 1991. Tabulation and ultrastructure of theca and trichocysts of Gambierdiscus toxicus (Dinophyceae, Peridinales) in culture. Cryptogamie, Algologie 12:137–156.
  25. EFSA (European Food Safety Authority). 2009. Scientific opinion on marine biotoxins in shellfish—palytoxin group: Panel on contaminants in the food chain. European Food Safety Authority Journal 7:1,393–1,430, https://www.efsa.europa.eu/it/efsajournal/pub/1393.
  26. Escalera, L., G. Benvenuto, E. Scalco, A. Zingone, and M. Montresor. 2014. Ultrastructural features of the benthic dinoflagellate Ostreopsis cf. ovata (Dinophyceae). Protist 165:260–274, https://doi.org/10.1016/j.protis.2014.03.001.
  27. Fraga, S., and F. Rodríguez. 2014. Genus Gambierdiscus in the Canary Islands (NE Atlantic Ocean) with description of Gambierdiscus silvae sp. nov., a new potentially toxic epiphytic benthic dinoflagellate. Protist 165:839–853, https://doi.org/10.1016/j.protis.2014.09.003.
  28. Fraga, S., F. Rodríguez, A. Caillaud, J. Diogène, N. Raho, and M. Zapata. 2011. Gambierdiscus excentricus sp. nov. (Dinophyceae), a benthic toxic dinoflagellate from the Canary Islands (NE Atlantic Ocean). Harmful Algae 11:10–22, https://doi.org/10.1016/j.hal.2011.06.013.
  29. Fraga, S., F. Rodríguez, P. Riobó, and I. Bravo. 2016. Gambierdiscus balechii sp. nov. (Dinophyceae), a new benthic toxic dinoflagellate from the Celebes Sea (SW Pacific Ocean). Harmful Algae 58:93–105, https://doi.org/10.1016/j.hal.2016.06.004.
  30. Friedman, M.A., M. Fernandez, L. Backer, R. Dickey, J. Bernstein, K. Schrank, S. Kibler, W. Stephan, M.O. Gribble, P. Bienfang, and others. In press. An updated review of ciguatera fish poisoning: Clinical, epidemiological, environmental, and public health management. Marine Drugs.
  31. García-Altares, M., L. Tartaglione, C. Dell’Aversano, O. Carnicer, P. de la Iglesia, M. Forino, J. Diogène, and P. Ciminiello. 2015. The novel ovatoxin-g and isobaric palytoxin (so far referred to as putative palytoxin) from Ostreopsis cf. ovata (NW Mediterranean Sea): Structural insights by LC-high resolution MSn. Analytical and Bioanalytical Chemistry 407:1,191–1,204, https://doi.org/10.1007/s00216-014-8338-y.
  32. Gatti, C.M., H.T. Darius, M. Chinain, and D. Lonati. 2015. First report of a mass-poisoning outbreak following the consumption of Tectus niloticus (Gastropod) in French Polynesia: A novel pathway of Ciguatera shellfish poisoning? Harmful Algae News 50:19–20, http://www.e-pages.dk/ku/1086.
  33. GEOHAB. 2012. Global Ecology and Oceanography of Harmful Algal Blooms: Core Research Project—Harmful Algal Blooms in Benthic Systems. E. Berdalet, P. Tester, and A. Zingone, eds, IOC of UNESCO and SCOR, Paris, France, and Newark, Delaware, 64 pp. 
  34. Gingold, D.B., M.J. Strickland, and J.J. Hess. 2014. Ciguatera fish poisoning and climate change: Analysis of the national poison center data in the United States, 2001–2011. Environmental Health Perspectives 122:580–586, https://doi.org/10.1289/ehp.1307196.
  35. Giussani, V., F. Sbrana, V. Asnaghi, M. Vassalli, M. Faimali, S. Casabianca, A. Penna, P. Ciminiello, C. Dell’Aversano, L. Tartaglione, and others. 2015. Active role of the mucilage in the toxicity mechanism of the harmful benthic dinoflagellate Ostreopsis cf. ovata. Harmful Algae 44:46–53, https://doi.org/10.1016/j.hal.2015.02.006.
  36. Gomez, F., D. Qui, R.M. Lopes, and S. Lin. 2015 Fukuyoa paulensis gen. et sp. nov., a new genus for the globular species of the dinoflagellate Gambierdiscus (Dinophyceae). PLoS ONE, https://doi.org/10.1371/journal.pone.0119676.
  37. Hardison, D.R., W.C. Holland, J.R. McCall, A.J. Bourdelais, D.G. Baden, H.T. Darius, M. Chinain, P.A. Tester, D. Shea, H.A. Flores Quintana, and others. 2016. Fluorescent receptor binding assay for detecting ciguatoxin in fish. PLoS ONE, https://doi.org/10.1371/journal.pone.0153348.
  38. Holmes, M.J., R.J. Lewis, A. Jones, and A.W. Hoy. 1995. Cooliatoxin, the first toxin from Coolia monotis (Dinophyceae). Natural Toxins 3:355–362, https://doi.org/10.1002/nt.2620030506.
  39. Honsell, G., A. Bonifacio, M. DeBortoli, A. Penna, C. Battocchi, P. Ciminiello, C. Dell’Aversano, E. Fattorusso, S. Sosa, T. Yasumoto, and A. Tubaro. 2013. New insights on cytological and metabolic features of Ostreopsis cf. ovata Fukuyo (Dinophyceae): A multidisciplinary approach. PLoS ONE, https://doi.org/10.1371/journal.pone.0057291.
  40. Hoppenrath, M., S.A. Murray, N. Chomérat, and T. Horiguchi. 2014. Marine benthic dinoflagellates: Unveiling their worldwide biodiversity. Kleine Senckenberg-Reihe 54, Schweizerbart’sche Verlagsbuchhandlung, Germany, 276 pp.
  41. Illoul, H., F. Rodríguez, M. Vila, N. Adjas, A. Aït Younes, M. Bournissa, A. Koroghli, N. Marouf, S. Rabia, and F.L.K. Ameur. 2012. The genus Ostreopsis along the Algerian coastal waters (SW Mediterranean Sea) associated with a human respiratory intoxication episode. Cryptogamie, Algologie 33:209–216, https://doi.org/10.7872/crya.v33.iss2.2011.209.
  42. Jauzein, C., A. Fricke, L. Mangialajo, and R. Lemee. 2016. Sampling of Ostreopsis cf. ovata using artificial substrates: Optimization of methods for the monitoring of benthic harmful algal blooms. Marine Pollution Bulletin, https://doi.org/10.1016/​j.marpolbul.2016.03.047
  43. Jeong, H.J., A.S. Lim, S.H. Jang, W.H. Yih, N.S. Kang, S.Y. Lee, Y.D. Yoo, and H.S. Kim. 2012. First report of the epiphytic dinoflagellate Gambierdiscus caribaeus in the temperate waters off Jeju Island, Korea: Morphology and molecular characterization. Eukaryotic Microbiology 59(6):637–650, https://doi.org/10.1111/j.1550-7408.2012.00645.x.
  44. Kerbrat, A.S., Z. Amzil, R. Pawlowiez, S. Golubic, M. Sibat, H.T. Darius, M. Chinain, and D. Laurent. 2011. First evidence of palytoxin and 42-hydroxy-palytoxin in the marine cyanobacterium Trichodesmium. Marine Drugs 9:543–560, https://doi.org/10.3390/md9040543.
  45. Kibler, S.R., R.W. Litaker, W.C. Holland, M.W. Vandersea, and P.A. Tester. 2012. Growth of eight Gambierdiscus (Dionphyceae) species: Effects of temperature, salinity and irradiance. Harmful Algae 19:1–14, https://doi.org/10.1016/​j.hal.2012.04.007.
  46. Kibler, S.R., P.A. Tester, K.E. Kunkel, S.K. Moore, and R.W. Litaker 2015. Effects of ocean warming on growth and distribution of dinoflagellates associated with ciguatera fish poisoning in the Caribbean. Ecological Modeling 316:194–210, https://doi.org/​10.1016/j.ecolmodel.2015.08.020.
  47. Kretzschmar, A.L.V., A. Verma, T. Harwood, M. Hoppenrath, and S. Murray. 2017. Characterization of Gambierdiscus lapillus sp. nov. (Gonyaulacales, Dinophyceae): A new toxic dinoflagellate from the Great Barrier Reef (Australia). Journal of Phycology, https://doi.org/10.1111/jpy.12496.
  48. Lapointe, B.E., R. Langton, B.J. Bedford, A.C. Potts, O. Day, and C. Hu. 2010. Land-based nutrient enrichment of the Buccoo Reef Complex and fringing coral reefs of Tobago, West Indies. Marine Pollution Bulletin 60:334–343, https://doi.org/10.1016/j.marpolbul.2009.10.020.
  49. Laurent, D., A.S. Kerbrat, H.T. Darius. F. Rossi, B. Yeeting, M. Haddad, S. Golubic, S. Pauillac, and M. Chinain. 2012. Ciguatera shellfish poisoning (CSP), a new ecotoxicological phenomenon: From cyanobacteria to humans via giant clams. Pp. 1–44 in Food Chain: New Research. M.A. Jensen and D.W. Muller, eds, Nova Publishers New York, NY.
  50. Lemée R., L. Mangialajo, S. Cohu, Z. Amzil, A. Blanfuné, N. Chomérat, N. Ganzin, S. Gasparin, H. Grossel, L. Guidi-Guivar, and others. 2012. Interactions between scientists, managers and policy makers in the framework of the French MediOs Project on Ostreopsis (2008–2010). Cryptogamie, Algologie 33:137–142, https://doi.org/10.7872/crya.v33.iss2.2011.137.
  51. Lewis, R.J., M. Inserra, I. Vetter, W.C. Holland, D.R. Hardison, P.A. Tester, and R.W. Litaker. 2016. Rapid extraction and identification of maitotoxin and ciguatoxin-like toxins from Caribbean and Pacific Gambierdiscus using a new functional bioassay. PLoS ONE, https://doi.org/10.1371/journal.pone.0160006.
  52. Litaker, R.W., M.W. Vandersea, M.A. Faust, S.R. Kibler, M. Chinain, M.J. Holmes, W.C. Holland, and P.A. Tester. 2009. Taxonomy of Gambierdiscus including four new species, Gambierdiscus caribaeus, Gambierdiscus carolinianus, Gambierdiscus carpenteri and Gambierdiscus ruetzleri (Gonyaulacales, Dinophyceae). Phycologia 48:344–390, https://doi.org/10.2216/07-15.1.
  53. Litaker, R.W., M.W. Vandersea, M.A. Faust, S.R. Kibler, A.W. Nau, W.C. Holland, M. Chinain, M.J. Holmes, and P.A. Tester. 2010. Global distribution of ciguatera causing dinoflagellates in the genus Gambierdiscus. Toxicon 56:711–730, https://doi.org/10.1016/j.toxicon.2010.05.017.
  54. Mak, Y.L., T.-C. Wai, M.B. Murphy, W.H. Chan, J.J. Wu, J.C. Lam, L.L. Chan, and P.K. Lam. 2013. Pacific ciguatoxins in food web components of coral reef systems in the Republic of Kiribati. Environmental Science & Technology 47:14,070–14,079, https://doi.org/10.1021/es403175d.
  55. Mangialajo, L., N. Ganzin, S. Accoroni, V. Asnaghi, A. Blanfuné, M. Cabrini, R. Cattaneo-Vietti, F. Chavanon, M. Chiantore, S. Cohu, and others. 2011. Trends in Ostreopsis proliferation along the Northern Mediterranean coasts. Toxicon 57:408–420, https://doi.org/10.1016/​j.toxicon.2010.11.019.
  56. Mattei, C., I. Vetter, A. Eisenblätter, B. Krock, M. Ebbecke, H. Desel, and K. Zimmermann. 2014. Ciguatera fish poisoning: A first epidemic in Germany highlights an increasing risk for European countries. Toxicon 91:76–83, https://doi.org/10.1016/j.toxicon.2014.10.016.
  57. Méjean, A., C. Peyraud-Thomas, A.S. Kerbrat, S. Golubic, S. Pauillac, M. Chinain, and D. Laurent. 2010. First identification of the neurotoxin homoanatoxin-a from mats of Hydrocoleum lyngbyaceum (marine cyanobacterium) possibly linked to giant clam poisoning in New Caledonia. Toxicon 56:829–835, https://doi.org/10.1016/​j.toxicon.2009.10.029.
  58. Migliaccio, O., I. Castellano, D. Di Cioccio, G. Tedeschi, A. Negri, P. Cirino, G. Romano, A. Zingone and A. Palumbo. 2016. Subtle reproductive impairment through nitric oxide-mediated mechanisms in sea urchins from an area affected by harmful algal blooms. Scientific Reports 6:26086, https://doi.org/10.1038/srep26086.
  59. Nakahara, H., T. Sakami T.M. Chinain, and Y. Ishida. 1996. The role of macroalgae in epiphytism of the toxic dinoflagellate Gambierdiscus toxicus (Dinophyceae). Phycological Research 44:113–117, https://doi.org/10.1111/j.1440-1835.1996.tb00385.x.
  60. Nishimura, T., H. Hariganeya, W. Tawong, H. Sakanari, J. Yamaguchi, and M. Adachi. 2016. Quantitative PCR assay for detection and enumeration of ciguatera-causing dinoflagellate Gambierdiscus spp. (Gonyaulacales) in coastal areas of Japan. Harmful Algae 52:11–22, https://doi.org/10.1016/​j.hal.2015.11.018.
  61. Nishimura, T., S. Sato, W. Tawong, H. Sakanari, H. Yamaguchi, and M. Adachi. 2014. Morphology of Gambierdiscus scabrosus sp. nov. (Gonyaulacales): A new epiphytic toxic dinoflagellate from coastal areas of Japan. Journal of Phycology 50:506–514, https://doi.org/10.1111/jpy.12175.
  62. Penna, A., S. Fraga, C. Battocchi, S. Casabianca, F. Perini, S. Capellacci, A. Casabianca, P. Riobo, M.G. Giacobbe, C. Totti, and others. 2012. Genetic diversity of the genus Ostreopsis Schmidt: Phylogeographical considerations and molecular methodology applications for field detection in the Mediterranean Sea. Cryptogamie, Algologie 33:153–163, https://doi.org/10.7872/crya.v33.iss2.2011.153.
  63. Penna, A., M. Vila, S. Fraga, M.G. Giacobbe, F. Andreoni, P. Riobó, and C. Vernesi. 2005. Characterization of Ostreopsis and Coolia (Dinophyceae) isolates in the Western Mediterranean Sea based on morphology, toxicity and internal transcribed spacer 5.8S rDNA sequences. Journal of Phycology 41:212–225, https://doi.org/10.1111/j.1529-8817.2005.04011.x.
  64. Perini, F., A. Casabianca, C. Battocchi, S. Accoroni, C. Totti, and A. Penna. 2011. New approach using the real-time PCR method for estimation of the toxic marine dinoflagellate Ostreopsis cf. ovata in marine environment. PLoS ONE, 6(3):e17699, https://doi.org/10.1371/journal.pone.0017699.
  65. Randall, J.E. 2005. Review of clupeotoxism, an often fatal illness from the consumption of clupeoid fishes. Pacific Science 59:73–77.
  66. Rhodes, L., T. Harwood, K. Smith, P. Argyle, and R. Munday. 2014. Production of ciguatoxin and maitotoxin by strains of Gambierdiscus australes, G. pacificus and G. polynesiensis (Dinophyceae) isolated from Rarotonga, Cook Islands. Harmful Algae 39:185–190, https://doi.org/10.1016/​j.hal.2014.07.018.
  67. Richlen, M.L., and P.S. Lobel. 2011. Effects of depth, habitat, and water motion on the abundance and distribution of ciguatera dinoflagellates at Johnston Atoll, Pacific Ocean. Marine Ecology Progress Series 421:51–66, https://doi.org/10.3354/meps08854.
  68. Rongo, T., and R. van Woesik. 2012. Socioeconomic consequences of ciguatera poisoning in Rarotonga, southern Cook Islands. Harmful Algae 20:92–100, https://doi.org/10.1016/j.hal.2012.08.003.
  69. Sato, S., T. Nishimura, K. Uehara, H. Sakanari, W. Tawong, N. Hariganeya, K. Smith, L. Rhodes, T. Yasumoto, Y. Taira, and others. 2011. Phylogeography of Ostreopsis along west Pacific coast, with special reference to a novel clade from Japan. PLoS ONE 6(12):e27983, https://doi.org/10.1371/journal.pone.0027983.
  70. Séchet, V., M. Sibat, N. Chomérat, E. Nézan, H. Grossel, J.-B. Lehebel-Peron, T. Jauffrais, N. Ganzin, F. Marco-Miralles, R. Lemée, and others. 2012. Ostreopsis cf. ovata in the French Mediterranean coast: Molecular characterisation and toxin profile. Cryptogamie, Algologie 33:89–98, https://doi.org/10.7872/crya.v33.iss2.2011.089.
  71. Shears, N.T., and P.M. Ross. 2009. Blooms of benthic dinoflagellates of the genus Ostreopsis: An increasing and ecologically important phenomenon on temperate reefs in New Zealand and worldwide. Harmful Algae 8:916–925, https://doi.org/10.1016/​j.hal.2009.05.003.
  72. Skinner, M.P., T.D. Brewer, R. Johnstone, L.E. Fleming, and R.J. Lewis. 2011. Ciguatera fish poisoning in the Pacific Islands (1998 to 2008). PLoS Neglected Tropical Diseases 5(12):e1416, https://doi.org/10.1371/journal.pntd.0001416.
  73. Smith, K.F., L. Rhodes, A. Verma, B.G. Curley, D.T. Harwood, G.S. Kohli, D. Solomona, T. Rongo, R. Munday, and S.A. Murray. 2016. A new Gambierdiscus species (Dinophyceae) from Rarotonga, Cook Islands: Gambierdiscus cheloniae sp. nov. Harmful Algae 60:45–56, https://doi.org/10.1016/j.hal.2016.10.006.
  74. Taniyama, S., O. Arakawa, M. Terada, S. Nishio, T. Takatani, Y. Mahmud, and T. Noguci. 2003. Ostreopsis sp., a possible origin of palytoxin (PTX) in parrotfish Scaris ovifrons. Toxicon 42:37–33.
  75. Tartaglione, L., A. Mazzeo, C. Dell’Aversano, M. Forino, V. Giussani, S. Capellacci, A. Penna, V. Asnaghi, M. Faimali, M.-C. Chiantore, and others. 2016. Chemical, molecular, and eco-toxicological investigation of Ostreopsis sp. from Cyprus Island: Structural insights into four new ovatoxins by LC-HRMS/MS. Analytical and Bioanalytical Chemistry 408:915–932, https://doi.org/10.1007/s00216-015-9183-3.
  76. Tester, P.A., S.R. Kibler, W.C. Holland, G. Usup, M.W. Vandersea, C.P. Leaw, P.T. Lim, J. Larsen, N. Mohammad-Noor, M.A. Faust, and R.W. Litaker. 2014. Sampling harmful benthic dinoflagellates: Comparison of artificial and natural substrate methods. Harmful Algae 39:8–25, https://doi.org/10.1016/j.hal.2014.06.009.
  77. Tester, P.A., A.W. Nau, R.L. Feldman, S.R. Kibler, and R.W. Litaker. 2010. Ciguatera fish poisoning and sea surface temperatures in the Caribbean Sea. Toxicon 56:698–710, https://doi.org/10.1016/​j.toxicon.2010.02.026.
  78. Vandersea, M.W., S.R. Kibler, W.C. Holland, P.A. Tester, T.F. Schultz, M.A. Faust, M.J. Holmes, M. Chinain, and R.W. Litaker. 2012. Development of semi-quantitative PCR assays for the detection and enumeration of Gambierdiscus species (Gonyaulacales, Dinophyceae). Journal of Phycology 48:902–915, https://doi.org/10.1111/j.1529-8817.2012.01146.x.
  79. Vanucci, S., F. Guidi, R. Pistocchi, and R.A. Long. 2016. Phylogenetic structure of bacterial assemblages co-occurring with Ostreopsis cf. ovata bloom. Harmful Algae 55:259–271, https://doi.org/10.1016/​j.hal.2016.04.003.
  80. Vila, M., R. Abós-Herràndiz, J. Isern-Fontanet, J. Àlvarez, and E. Berdalet. 2016. Establishing the link between Ostreopsis cf. ovata blooms and human health impacts using ecology and epidemiology. Scientia Marina 80S1:107–115, https://doi.org/10.3989/scimar.04395.08A.
  81. Xu, Y., M.L. Richlen, J.D. Liefer, A. Robertson, D. Kulis, T.B. Smith, M.L. Parsons, and D.M. Anderson. 2016. Influence of environmental variables on Gambierdiscus spp. (Dinophyceae) growth and distribution. PLoS ONE 11(4):e0153197, https://doi.org/10.1371/journal.pone.0153197.
  82. Yasumoto, T., A. Inoue, T. Ochi, K. Fujimoto, Y. Oshima, Y. Fukuyo, R. Adachi, and R. Bagnis. 1980. Environmental studies on a toxic dinoflagellate responsible for ciguatera. Bulletin of the Japanese Society of Scientific Fisheries 46:1,397–1,404, https://doi.org/10.2331/suisan.46.1397.
  83. Zingone, A., E. Berdalet, P. Bienfang, H. Enevoldsen, J. Evans, R. Kudela, and P. Tester. 2012. Harmful algae in benthic systems: A GEOHAB core research program. Cryptogamie, Algologie 33:225–230, https://doi.org/10.7872/crya.v33.iss2.2011.225.
Copyright & Usage

This is an open access article made available under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/), which permits use, sharing, adaptation, distribution, and reproduction in any medium or format as long as users cite the materials appropriately, provide a link to the Creative Commons license, and indicate the changes that were made to the original content. Images, animations, videos, or other third-party material used in articles are included in the Creative Commons license unless indicated otherwise in a credit line to the material. If the material is not included in the article’s Creative Commons license, users will need to obtain permission directly from the license holder to reproduce the material.