Advertisement

Biological Toxins from Marine and Freshwater Microalgae

  • Antonino Santi Delia
  • Gabriella Caruso
  • Lucia Melcarne
  • Giorgia Caruso
  • Salvatore Parisi
  • Pasqualina Laganà
Chapter
Part of the SpringerBriefs in Molecular Science book series (BRIEFSMOLECULAR)

Abstract

In the last decades the increased occurrence of intoxications caused by biological toxins produced from marine and freshwater microalgae has underlined their relevance as emerging risks for food safety. Biological toxins from algae (i.e. saxitoxin, brevetoxin, okadaic acid, domoic acid) are recognised as a major threat for human and animal health, especially where Harmful Algal Blooms phenomena develop. Many of these toxins are responsible for severe illness or death, mostly related to consumption of seafood contaminated by toxic algae. The present book summarises current knowledge and perspectives for future research on marine and freshwater algal toxins. Specific topics are: overview of the different species producing toxins, their survival strategies in the environment; typologies of toxins, their chemical structure and mechanisms of actions; methods currently in use for their monitoring; emerging issues and future outlooks for their control. The importance of biotoxin monitoring in the framework of the European Marine Strategy Framework Directive is also discussed.

Keywords

Brevetoxin Ciguatoxin Cylindrospermopsin Domoic acid Harmful algal bloom Microcystin Okadaic acid Poisoning Saxitoxin Yessotoxin 

Abbreviations

ASP

Amnesic Shellfish Poisoning

AOAC

Association of Official Analytical Chemists

AZA

Azaspiracid

AZP

Azaspiracid Shellfish Poisoning

BMAA

β-Methylamino-L-Alanine

PbTx

Brevetoxin

CYN

Cylindrospermopsin

BIOTOX

Development of Cost-Effective Tools for Risk Management and Traceability Systems for Marine Biotoxins in Seafood

DSP

Diarrhetic Shellfish Poisoning

DST

Diarrhetic Shellfish Toxin

DiCANN

Dinoflagellate Categorisation by Artificial Neural Network

DTX

Dinophysistoxin

DA

Domoic Acid

ELISA

Enzyme-Linked ImmunoSorbent Assay

EFSA

European Food Safety Authority

EU

European Union

GEOHAB

Global Ecology and Oceanography of Harmful Algal Blooms

GES

Good Environmental Status

HAB

Harmful Algal Bloom

HPLC

High-Performance Liquid Chromatography

LD50

Median Lethal Dose (50 % of the population)

LOQ

Limit of Quantification

LC

Liquid Chromatography

LC-MS

Liquid Chromatography-Mass Spectrometry

LC-MS/MS

Liquid Chromatography Tandem Mass Spectrometry

MSFD

Marine Strategy Framework Directive

MALDI-TOF

Matrix-assisted Laser Desorption/Ionisation Time-of-Flight

MCY

Microcystin

MCY-RR

Microcystin-RR

MW

Molecular Weight

NSP

Neurotoxic Shellfish Poisoning

N

Nitrogen

OA

Okadaic Acid

PLTX

Palitoxin

PSP

Paralytic Shellfish Poisoning

PTX

Pectenotoxin

P

Phosphorus

PCR

Polymerase Chain Reaction

PSU

Practical Salinity Unit

Q-TOF

Quadrupole-Time-of-Flight

STX

Saxitoxin

SPX

Spirolides

USA

United States of America

YTX

Yessotoxin

References

  1. Accoroni S, Romagnoli T, Colombo F, Pennesi C, Di Camillo CG, Marini M, Battocchi C, Ciminiello P, Dell’Aversano C, Dello Iacovo E, Fattorusso E, Tartaglione L, Penna A, Totti C (2011) Ostreopsis cf. ovata bloom in the northern Adriatic Sea during summer 2009: ecology, molecular characterization and toxin profile. Mar Poll Bull 62(11):2512–2519. doi: 10.1016/j.marpolbul.2011.08.003 Google Scholar
  2. Accoroni S, Colombo F, Pichierri S, Romagnoli T, Marini M, Battocchi C, Penna A, Totti C (2012) Ecology of Ostreopsis cf. ovata blooms in the northwestern Adriatic Sea. Cryptogam Algolog 33(2):191–198. doi: 10.7872/crya.v33.iss2.2011.191 Google Scholar
  3. Anderson DM (1989) Toxic algal blooms and red tides: a global perspective. In: Okaichi T, Anderson DM, Nemoto T (eds) Red tides: biology, environmental science and toxicology. Elsevier, New York, pp 11–16Google Scholar
  4. Anderson DM, Glibert PM, Burkholder JM (2002) Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 25(4):704–726. doi: 10.1007/BF02804901 Google Scholar
  5. Anderson DM, Alpermann TJ, Cembella AD, Collos Y, Masseret E, Montresor M (2012a) The globally distributed genus Alexandrium: multifaceted roles in marine ecosystems and impacts on human health. Harmful Algae 14:10–35. doi: 10.1016/j.hal.2011.10.012 Google Scholar
  6. Anderson DM, Cembella AD, Hallegraeff GM (2012b) Progress in understanding harmful algal blooms: paradigm shifts and new technologies for research, monitoring, and management. Ann Rev Mar Sci 4:143–176. doi: 10.1146/annurev-marine-120308-081121 Google Scholar
  7. AOAC (1990) Paralytic Shellfish poison. Biological method. Final action. In: Hellrich K (ed) Official method of analysis, 15th edn, pp 881–882, Sect 959.08. Association of Official Analytical Chemists (AOAC), Arlington, VAGoogle Scholar
  8. Asakawa M, Beppu R, Ito K, Tsubota M, Takayama H, Miyazawa K (2006) Accumulation of paralytic Shellfish poison (PSP) and biotransformation of its components in Oysters Crassostrea gigas fed with the toxic dinoflagellate Alexandrium tamarense. J Food Hyg Soc Japan 47(1):28–32Google Scholar
  9. Aubert M, Aubert J (1986) Eutrophie et distrophie en milieu marin—phenomenes plantoniques et bacteriens. Centre d’etudes et recherches de biologie et d’oceanographie medicale Cerbom (Nice). Rev Int Oceanogr Med 83–84:3–302Google Scholar
  10. Azmil Z, Fresnel J, Le Gal D, Billard C (2001) Domoic acid accumulation in French shellfish in relation to toxic species of Pseudo-nitzschia multiseries and P. pseudodelicatissima. Toxicon 39(8):1245–1251. doi: 10.1016/S0041-0101(01)00096-4 Google Scholar
  11. Backer LC, Fleming LE, Rowan AD, Baden DG (2003) Epidemiology, public health and human illnesses associated with harmful marine algae. In: Hallegraeff GM, Anderson DM, Cembella AD (eds) Manual on harmful marine microalgae. Intergovernmental Oceanographic Commission of UNESCO, Paris, pp 723–750Google Scholar
  12. Baden DG (1983) Marine food-borne dinoflagellate toxins. Int Rev Cytol 82:99–150. doi: 10.1016/S0074-7696(08)60824-4 Google Scholar
  13. Baden DG (1989) Brevetoxins: unique polyether dinoflagellate toxins. Fed Am Soc Exp Biol J 3:1807–1817Google Scholar
  14. Baden DG, Mende TJ, Bikhazi G, Leung I (1982) Bronchoconstriction caused by Florida red tide toxins. Toxicon 20(5):929–932. doi: 10.1016/0041-0101(82)90081-2 Google Scholar
  15. Bagnis R (1968) Clinical aspects of ciguatera (fish poisoning) in French Polynesia. Hawaii Med J 28(1):25–28Google Scholar
  16. Blanco J, Reyero M, José F (2003) Kinetics of accumulation and transformation of paralytic shellfish toxins in the blue mussel Mytilus galloprovincialis. Toxicon 42(7):777–784. doi: 10.1016/j.toxicon.2003.10.007 Google Scholar
  17. Bogialli S, Bruno M, Curini R, Di Corcia A, Laganá A, Mari B (2005) Simple assay for analyzing five microcystins and nodularin in fish muscle tissue: Hot water extraction followed by liquid chromatography-tandem mass spectrometry. J Agric Food Chem 53(17):6586–6592. doi: 10.1021/jf050257m Google Scholar
  18. Bogialli S, Bruno M, Curini R, Di Corcia A, Fanali C, Laganà A (2006a) Monitoring algal toxins in lake water by liquid chromatography tandem mass spectrometry. Environ Sci Technol 40(9):2917–2923. doi: 10.1021/es052546x Google Scholar
  19. Bogialli S, Bruno M, Curini R, Di Corcia A, Laganà A (2006b) Simple and rapid determination of anatoxin-a in lake water and fish muscle tissue by liquid-chromatography-tandem mass spectrometry. J Chromatogr A 1122(1–2):180–185. doi: 10.1016/j.chroma.2006.04.064 Google Scholar
  20. Bold HC, Wynne MG (1985) Introduction to the algae, 2nd edn. Prentice Hall, Englewood CliffsGoogle Scholar
  21. Botana LM (ed) (2008) Seafood and freshwater toxins—pharmacology, physiology, and detection, 2nd edn. CRC Press, Boca Raton, pp 1–941Google Scholar
  22. Botana LM (ed) (2014) Seafood and freshwater toxins: pharmacology, physiology and detection, 3rd edn. CRC Press, Boca Raton, pp 1–1215Google Scholar
  23. Botana LM, Fernández-Araujo A, Alfonso A, Antelo JM, Davila T, Alfonso C, Katikou P (2013) Warm seawater microalgae: growth and toxic profile of Ostreopsis Spp from European costs. Oceanography 1:1–6Google Scholar
  24. Brand LE (2009) Human exposure to cyanobacteria and BMAA. Amyotroph Lateral Scler Suppl 2:124–126. doi: 10.3109/17482960903273585 Google Scholar
  25. Bruno M (2000) Toxic algae in sea and freshwater: health impact and control strategies. ISTISAN Reports 00/31, pp 1–94. Istituto Superiore di Sanità, RomeGoogle Scholar
  26. Bruno M (2013) Cyanotoxin health hazard and risk assessment freshwater lakes. Cyanobacteria: ecology, toxicology and management. Nova Science Publishers, Hauppauge, pp 153–177Google Scholar
  27. Bruno M, Congestri R, Buzzelli E (1997) Indicazioni per il controllo delle specie algali tossiche delle acque marine e lacustri italiane. ISTISAN Reports 97/21, pp 1–128. Istituto Superiore di Sanità, RomeGoogle Scholar
  28. Bruno M, Melchiorre S, Messineo V, Volpi F, Di Corcia A, Aragona I, Guglielmone G, Di Paolo C, Cenni M, Ferranti P, Gallo P (2009) Microcystin detection in contaminated fish from Italian lakes using ELISA immunoassays and LC-MS/MS analysis. Handbook on Cyanobacteria: biochemistry, biotechnology and applications. Nova Science Publishers, Hauppauge, pp 191–210Google Scholar
  29. Cabado AG, Vieites JM (eds) (2012) New trends in marine and freshwater toxins: food and safety concerns. Nova Science Publishers, Hauppauge, pp 1–403Google Scholar
  30. Cabrini M, Falconi C, Culverhouse PF (2010) Metodi automatici per il rilevamento di microalghe planctoniche. In: Socal G, Buttino I, Cabrini M, Mangoni O, Penna A, Totti C (eds) Metodologie di studio del plancton marino. Manuali e Linee Guida ISPRA, 56/2010, Chapter 25. Istituto Superiore per la protezione e la ricerca ambientale, Rome. http://www.isprambiente.gov.it/contentfiles/00009100/9171-mlg56-2010.pdf/at_download/file. Accessed 07 March 2015
  31. Carmichael WW (2001) Health effects of toxin-producing cyanobacteria: “The CyanoHAB”. Hum Ecol Risk Assess 7(5):1393–1407. doi: 10.1080/20018091095087 Google Scholar
  32. Carmichael WW (2008) A world overview—one-hundred-twenty-seven years of research on toxic cyanobacteria—where do we go from here? In: Hudnell KH (ed) Cyanobacterial harmful algal blooms: state of the science and research needs. Adv Exp Med Biol 619:105–125 (Springer, New York). doi: 10.1007/978-0-387-75865-7_4
  33. Caroppo C, Congestri R, Bruno M (2001) Dynamics of Dinophysis sensu lato species (Dinophyceae) in a coastal mediterranean environment (Adriatic Sea). Cont Shelf Res 21(16–17):1839–1854. doi: 10.1016/S0278-4343(01)00028-0 Google Scholar
  34. Caroppo C, Congestri R, Bracchini L, Albertano P (2005) On the presence of Pseudo-nitzschia calliantha Lundholm, Moestrup et Hasle and Pseudo-nitzschia delicatissima (Cleve) Heiden in the Southern Adriatic Sea (Mediterranean Sea, Italy). J Plankton Res 27(8):763–774. doi: 10.1093/plankt/fbi050 Google Scholar
  35. Carrada GC, Casotti R, Modigh M, Saggiomo V (1991) Presence of Gymnodinium catenatum (Dinophyceae) in a coastal mediterranean lagoon. J Plankton Res 13(1):229–238. doi: 10.1093/plankt/13.1.229 Google Scholar
  36. Cembella AD (2003) Chemical ecology of eukaryotic microalgae in marine ecosystems. Phycologia 42:420–447Google Scholar
  37. Cerino F, Orsini L, Sarno D, Dell’Aversano C, Tartaglione L, Zingone A (2005) The alternation of different morphotypes in the seasonal cycle of the toxic diatom Pseudo-nitzschia galaxiae. Harmful Algae 4(1):33–48. doi: 10.1016/j.hal.2003.10.005 Google Scholar
  38. Chen C, Chou H (2002) Fate of paralytic shellfish poisoning toxins in purple clam, in outdoor culture and laboratory culture. Mar Poll Bull 44(8):733–738. doi: 10.1016/S0025-326X(01)00307-1 Google Scholar
  39. 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(5):927–934. doi: 10.1007/s00227-003-1148-y Google Scholar
  40. Chorus I, Bartram J (1999) Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. E&FN Spon, London, pp 41–90Google Scholar
  41. Ciminiello P, Dell’Aversano C, Fattorusso E, Forino M (2009) Recent developments in mediterranean harmful algal events. In: Fishbein JC (ed) Advances in molecular toxicology, vol 3. Elsevier B.V, AmsterdamGoogle Scholar
  42. Codd GA (2000) Cyanobacterial toxins, the perception of water quality and the prioritisation of eutrophication control. Ecol Eng 16(1):51–60. doi: 10.1016/S0925-8574(00)00089-6 Google Scholar
  43. Codd GA, Bell SG, Kaya K, Ward CJ, Beattie KA, Metcalf JS (1999) Cyanobacterial toxins, exposures routes and human health. Eur J Phycol 34(4):405–415Google Scholar
  44. Commission European (2008) European Commission Directive 2008/56/EC of the European Parliament and of the Council of 17 June 2008 establishing a framework for community actions in the field of marine environmental policy (Marine Strategy Framework Directive). Off J Eur Comm L164:19–40Google Scholar
  45. Commission European (2010) European Commission Decision of 1 September 2010 on criteria and methodological standards on good environmental status of marine waters (notified under document C (2010) 5956)(2010/477/EU). Off J Eur Union L232:14–24Google Scholar
  46. Costa PR, Rosa R, Sampayo MAM (2004) Tissue distribution of the amnesic shellfish toxin, domoic acid, in Octopus vulgaris from the Portuguese coast. Mar Biol 144(5):971–976. doi: 10.1007/s00227-003-1258-6 Google Scholar
  47. Costa PR, Rosa R, Duarte-Silva A, Brotas V, Sampayo MAM (2005) Accumulation, transformation and tissue distribution of domoic acid, the amnesic shellfish poisoning toxin, in the common cuttlefish, Sepia officinalis. Aquat Toxicol 74(1):82–91. doi: 10.1016/j.aquatox.2005.01.011 Google Scholar
  48. Costa PR, Botelho MJ, Rodrigues SM (2009) Accumulation of paralytic shellfish toxins in digestive gland of Octopus vulgaris during bloom events including the dinoflagellate Gymnodinium catenatum. Mar Poll Bull 58(11):1747–1750. doi: 10.1016/j.marpolbul.2009.08.005 Google Scholar
  49. Cox PA, Banack SA, Murch SJ (2003) Biomagnification of cyanobacterial neurotoxins and neurodegenerative disease among the Chamorro people of Guam. Proc Natl Acad Sci USA 100:13380–13383. doi: 10.1073/pnas.2235808100
  50. Cox PA, Banack SA, Susan J, Murch SJ, Rasmussen U, Tien G, Bidigare RR, Metcalf JS, Morrison LF, Codd GA, Bergman B (2005) Diverse taxa of cyanobacteria produce-N-methylamino-L-alanine, a neurotoxic amino acid. Proc Natl Acad Sci USA 102:5074–5078Google Scholar
  51. Cox PA, Richer R, Metcalf JS, Banack SA, Codd GA, Bradley WG (2009) Cyanobacteria and BMAA exposure from desert dust: a possible link to sporadic ALS among Gulf War veterans. Amyotroph Lateral Scler 10 Suppl 2:109–117. doi: 10.3109/17482960903286066 Google Scholar
  52. Culverhouse PF, Herry V, Reguera B, Gonzalez-Gil S, Williams R, Fonda S, Cabrini M, Parisini T, Ellis R (2001) Dinoflagellate categorisation by artificial neural network (DiCaNN). In: Hallegraeff GM, Blackburn SI, Bolck CJ, Lewis RJ (eds) Harmful algal blooms 2000. Intergovernmental Oceanographic Commission of UNESCO, Vigo, pp 195–198Google Scholar
  53. Dodge JD (1982) Marine dinoflagellates of the British Isles. Her Majesty’s Stationery Office, LondonGoogle Scholar
  54. Donner G, Platt-Rohloff L, Brummer F, Elbrächter M (2000) (Abstract) A calcium-dependent allelopathic effect of the dinoflagellate Coolia monotis on the chlorophyceae Dunaliella salina. In: Proceedings of the 9th international conference on harmful algal blooms Tasmania 2000, 7–11 Feb 2000, Wrest Point Convention Centre, Hobart, Tasmania, Australia, p 224. http://frdc.com.au/research/Final_Reports/1998-343-DLD.pdf. Accessed 27 Feb 2015
  55. Doucette GJ, Kodama M, Franca S, Gallacher S (1998) Bacterial interactions with harmful algal bloom species: bloom ecology, toxigenesis, and cytology. In: Anderson DM, Cembella AD, Hallegraeff GM (eds) Physiological ecology of harmful algal blooms. Springer, Heidelberg, pp 619–647Google Scholar
  56. Doucette G, Maneiro I, Riveiro I, Svensen C (2006) Phycotoxin pathways in aquatic food webs: transfer, accumulation and degradation. In: Granéli E, Turner JT (eds) Ecology of harmful algae. Ecological studies, vol 189, Springer, Berlin, pp 283–296. doi: 10.1007/978-3-540-32210-8_22
  57. Durando P, Ansaldi F, Oreste P, Moscatelli P, Marensi L, Grillo C, Gasparini R, Icardi G, Collaborative Group for the Ligurian Syndromic Algal Surveillance (2007) Ostreopsis ovata and human health: epidemiological and clinical features of respiratory syndrome outbreaks from a two-year syndromic surveillance, 2005–06, in north-west Italy. Euro Surveillance 12, 23:pii = 3212. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=3212. Accessed 06 March 2015
  58. EFSA (2008a) Marine biotoxins in shellfish—okadaic acid and analogues. Scientific opinion of the panel on contaminants in the food chain. EFSA J 589:1–62. doi: 10.2903/j.efsa.2008.589 Google Scholar
  59. EFSA (2008b) Marine biotoxins in shellfish—Azaspiracid group [1]. Scientific opinion of the panel on contaminants in the food chain. EFSA J 723:1–52. doi: 10.2903/j.efsa.2008.723 Google Scholar
  60. EFSA (2008c) Marine biotoxins in shellfish—Yessotoxin group. Scientific opinion of the panel on contaminants in the food chain. EFSA J 907:1–62. doi: 10.2903/j.efsa.2009.907 Google Scholar
  61. EFSA (2009a) Marine biotoxins in shellfish—Saxitoxin group. Scientific opinion of the panel on contaminants in the food chain. EFSA J 1019:1–76. doi: 10.2903/j.efsa.2009.1019 Google Scholar
  62. EFSA (2009b) Marine biotoxins in shellfish—Pectenotoxin group. Scientific opinion of the panel on contaminants in the food chain. EFSA J 1109:1–47. doi: 10.2903/j.efsa.2009.1109 Google Scholar
  63. EFSA (2009c) Marine biotoxins in shellfish—Domoic acid. Scientific opinion of the panel on contaminants in the food chain. EFSA J 1181:1–61. http://www.efsa.europa.eu/fr/scdocs/doc/1181.pdf. Accessed 06 March 2015
  64. EFSA (2009d) Marine biotoxins in shellfish—Palytoxin group 1. Panel on contaminants in the food chain (CONTAM). EFSA J 7, 12:1393–1433. doi: 10.2903/j.efsa.2009.1393
  65. EFSA (2010a) Marine biotoxins in shellfish—Emerging toxins: Ciguatoxin group. Panel on contaminants in the food chain (CONTAM). EFSA J 8, 6:1627–1665. doi: 10.2903/j.efsa.2010.1627
  66. EFSA (2010b) Scientific Opinion on marine biotoxins in shellfish—Cyclic imines (spirolides, gymnodimines, pinnatoxins and pteriatoxins). EFSA J 8(6):1628–1667. doi: 10.2903/j.efsa.2010.1628 Google Scholar
  67. EFSA (2010c) Marine biotoxins in shellfish—Emerging toxins: Brevetoxin group. Panel on contaminants in the food chain (CONTAM). EFSA J 8, 7:1677–1706. doi: 10.2903/j.efsa.2010.1677
  68. Eilertsen HC, Wyatt T (2000) Phytoplankton models and life history strategies. South Afr J Mar Sci 22(1):323–338. doi: 10.2989/025776100784125717 Google Scholar
  69. Evangelista V, Barsanti L, Frassanito AM, Passarelli V, Gualtieri P (eds) (2008) Algal toxins: nature, occurrence, effect and detection. NATO science for peace and security series A: chemistry and biology. Springer Science+Business Media B.V., Dordrecht, pp 1–399Google Scholar
  70. FAO/IOC/WHO (2005) Report of the Joint FAO/IOC/WHO ad hoc Expert Consultation on Biotoxins in Bivalve Molluscs. Oslo, Norway, 26–30 Sept 2004. ftp://fao.org/es/esn/food/biotoxin_report_en.pdf. Accessed 06 March 2015
  71. Faust MA (1999) Three Ostreopsis specie (Dinophyceae): O. marinus sp.nov., O. beliseanus sp. nov., and O. carribeanus sp. nov. Phycologia 38(2):92–99. doi: 10.2216/i0031-8884-38-2-92.1 Google Scholar
  72. Faust MA, Morton SL, Quod JP (1996) Further SEM study of marine dinoflagellate: the genus Ostreopsis (Dinophyceae). J Phycol 32(6):1053–1065. doi: 10.1111/j.0022-3646.1996.01053.x Google Scholar
  73. Ferranti P, Fabbrocino S, Nasi A, Caira S, Bruno M, Serpe L, Gallo P (2009) Liquid chromatography coupled to quadruple time-of-flight tandem mass spectrometry for microcystin analysis in freshwaters: Method performances and characterisation of a novel variant of microcystin-RR. Rapid Commun Mass Spectrom 23(9):1328–1336. doi: 10.1002/rcm.4006 Google Scholar
  74. Ferranti P, Fabbrocino S, Chiaravalle E, Bruno M, Basile A, Serpe L, Gallo P (2013) Profiling microcystin contamination in a water reservoir by MALDI-TOF and liquid chromatography coupled to Q/TOF tandem mass spectrometry. Food Res Int 54(1):1321–1330. doi: 10.1016/j.foodres.2012.12.028 Google Scholar
  75. Fiedler CP (1982) Zooplankton avoidance and reduced grazing responses to Gymnodinium splendens (Dinophyceae). Limnol Oceanogr 27(5):961–965. doi: 10.4319/lo.1982.27.5.0961 Google Scholar
  76. Fristachi A, Sinclair JL, Hall S, Hambrook Berkman JA, Boyer G, Burkholder J, Burns J, Carmichael W, DuFour A, Frazier W, Morton SL, O’Brien E, Walker S (2008) Occurrence of cyanobacterial harmful algal blooms workgroup report. In: Hudnell KH (ed) Cyanobacterial harmful algal blooms: state of the science and research needs. Springer, New York, pp 45–103Google Scholar
  77. Gallo P, Fabbrocino S, Cerulo MG, Ferranti P, Bruno M, Serpe L (2009) Determination of cylindrospermopsin in freshwaters and fish tissue by liquid chromatography coupled to electrospray ion trap mass spectrometry. Rapid Commun Mass Spectrom 23(20):3279–3284. doi: 10.1002/rcm.4243 Google Scholar
  78. Garcés E, Zingone A, Montresor M, Reguera B, Dale B (eds) (2001). LIFEHAB Life histories of microalgal species causing harmful blooms. European Commission Directorate General, Science, Research and Development. http://www.icm.csic.es/bio/projects/lifehab/LIFEHAB.pdf. Accessed 03 March 2015
  79. Garcés E, Masò M, Camp J (2002) Role of temporary cysts in the population dynamics of Alexandrium taylori (Dinophyceae). J Plankton Res 24:681–686. doi: 10.1093/plankt/24.7.681 Google Scholar
  80. Garrison DL (1981) Monterey Bay phytoplankton. II Resting spore cycles in coastal diatom populations. J Plankton Res 3:137–156. doi: 10.1093/plankt/3.1.137 Google Scholar
  81. Gerssen A, Pol-Hofstad IE, Poelman M, Mulder PPJ, van den Top HJ, de Boer J (2010) Marine toxins: chemistry, toxicity, occurrence and detection, with special reference to the Dutch situation. Toxins 2:878–904. doi: 10.3390/toxins2040878#sthash.jl53gaKm.dpuf Google Scholar
  82. Giacobbe MG (2008) Microalghe tossiche sulle coste italiane (Pericoli dell’estate). Darwin 26:90–95Google Scholar
  83. Giacobbe MG, Maimone G (1994) First report of Alexandrium minutum Halim in a mediterranean lagoon. Cryptogam Algolog 15:47–52Google Scholar
  84. Giacobbe MG, Oliva F, La Ferla R, Puglisi A, Crisafi E, Maimone G (1995) Potentially toxic dinoflagellates in mediterranean waters (Sicily) and related hydrobiological conditions. Aquat Microb Ecol 9:63–68Google Scholar
  85. Giacobbe MG, Vila M, Masò M, Garcés E, Luglié A, Sechi N, Gangemi E, Galletta M, Grasso V, Gotsis-Skretas O, Igniatiades L (2006) Is the spreading of the genus Alexandrium (Dinophyceae) in mediterranean coastal waters related to human activities? Biol Mar Medit 13(1):989–993Google Scholar
  86. Giacobbe MG, Penna A, Gangemi E, Masò M, Garcés E, Fraga S, Bravo I, Azzaro F, Penna N (2007) Recurrent high-biomass bloooms of Alexandrium taylorii (Dinophyceae), a HAB species expanding in the mediterranean. Hydrobiol 580:125–133. doi: 10.1007/978-1-4020-6156-1_11 Google Scholar
  87. Glibert PM, Pitcher G (eds) (2001) GEOHAB Global ecology and oceanography of harmful algal blooms, science plan. SCOR andIOC, Baltimore and Paris. http://www.geohab.info/images/stories/documents/final.pdf. Accessed 06 March 2015
  88. Gorbi S, Avio GC, Benedetti M, Totti C, Accoroni S, Pichierri S, Bacchiocchi S, Orletti R, Graziosi T, Regoli F (2013) Effects of harmful dinoflagellate Ostreopsis cf. ovata exposure on immunological, histological and oxidative responses of mussels Mytilus galloprovincialis. Fish Shellfish Immunol 35(3):941–950. doi: 10.1016/j.fsi.2013.07.003 Google Scholar
  89. Granéli E, Weberg M, Salomon PS (2008) Harmful algal blooms of allelopathic microalgal species: the role of eutrophication. Harmful Algae 8(1):94–102. doi: 10.1016/j.hal.2008.08.011 Google Scholar
  90. Granéli E, Edvardsen B, Roelke DL, Hagström JA (2012) The ecophysiology and bloom dynamics of Prymnesium spp. Harmful Algae 14:260–270. doi: 10.1016/j.hal.2011.10.024 Google Scholar
  91. Hajdu S, Edler L, Olenina I, Witek B (2000) Spreading and establishment of the potentially toxic dinoflagellate Prorocentrum minimum in the Baltic Sea. Int Rev Hydrobiol 85(5–6):561–575Google Scholar
  92. Hajdu S, Pertola S, Kuosa H (2005) Prorocentrum minimum (Dinophyceae) in the Baltic Sea: morphology, occurrence—a review. Harmful Algae 4(3):471–480. doi: 10.1016/j.hal.2004.08.004 Google Scholar
  93. Hallegraeff GM (1993) A review of harmful algal blooms and their apparent global increase. Phycologia 32(2):79–99. doi: 10.2216/i0031-8884-32-2-79.1 Google Scholar
  94. Hallegraeff GM (2010) Ocean climate change, Phytoplankton community responses, and harmful algal blooms: a formidable predictive challenge. J Phycol 46(2):220–235. doi: 10.1111/j.1529-8817.2010.00815.x Google Scholar
  95. Halstead BW (2002) The microbial biogenesis of aquatic biotoxins. Toxicol Mech Meth 12(2):135–153. doi: 10.1080/10517230290075369 Google Scholar
  96. Holmes MJ, Lewis RJ, Poli MA, Gillespie NC (1991) Strain-dependent production of ciguatoxin precursors (Gambiertoxins) by Gambierdiscus toxicus (Dinophyceae) in culture. Toxicon 29(6):761–775. doi: 10.1016/0041-0101(91)90068-3 Google Scholar
  97. Holmes MJ, Lewis RJ, Jones A, Wong Hoy AW (1995) Cooliatoxin, the first toxin from Coolia monotis (Dinophyceae). Nat Toxins 3(5):355–362. doi: 10.1002/nt.2620030506 Google Scholar
  98. Honsell G, Boni L, Cabrini M, Pompei M (1992) Toxic or potentially toxic dinoflagellates from the Northern Adriatic Sea. Sci Tot Environ, Suppl, pp 107–114Google Scholar
  99. Ichimi K, Suzuki T, Yamasaki M (2001) Non-selective retention of PSP toxins by the mussel Mytilus galloprovincialis fed with the toxic dinoflagellate Alexandrium tamarense. Toxicon 39(12):1917–1921. doi: 10.1016/S0041-0101(01)00177-5 Google Scholar
  100. International Council for the Exploration of the Sea (1984) Report of the ICES special meeting on the causes, dynamics and effects of exceptional marine blooms and related events. International Council Meeting Paper 1984/ E:42, pp 1–16. http://www.iode.org/index.php?option=com_oe&task=viewDocumentRecord&docID=6966. Accessed 03 March 2015
  101. Iverson F, Truelove J, Nera E, Tryphonsas L, Campbell J, Lok E (1989) Domoic acid poisoning and mussel associated intoxication: preliminary investigation into the response of mice and rats to toxic mussel extract. Food Chem Toxicol 27(6):377–384. doi: 10.1016/0278-6915(89)90143-9 Google Scholar
  102. Jonasson S, Eriksson J, Berntzon L, Spáčil Z, Ilag LL, Ronnevi LO, Rasmussen U, Bergman B (2010) Transfer of a cyanobacterial neurotoxin within a temperate aquatic ecosystem suggests pathways for human exposure. Proc Natl Acad Sci USA 107:9252–9257. doi: 10.1073/pnas.0914417107 Google Scholar
  103. Kalogerakis N, Arff J, Banat IM, Broch OJ, Daffonchio D, Edvardsen T, Eguiraun H, Giuliano L, Handa A, López-de-Ipiña K, Marigomez I, Martinez I, Øie G, Rojo F, Skjermo J, Zanaroli G, Fava F (2014) The role of environmental biotechnology in exploring, exploiting, monitoring, preserving, protecting and decontaminating the marine environment. New Biotechnol 32(1):157–167. doi: 10.1016/j.nbt.2014.03.007 Google Scholar
  104. Kaniou-Grigoriadou I, Mouratidou T, Katikou P (2005) Investigation on the presence of domoic acid in Greek shellfish. Harmful Algae 4:717–723. doi: 10.1016/j.hal.2004.10.002 Google Scholar
  105. Katircioǧlu H, Akin BS, Atici T (2004) Microalgal toxin(s): characteristics and importance. Afr J Biotechnol 3(12):667–674Google Scholar
  106. Kerbrat AS, Zouher A, Pawlowiez R, Golubic S, Sibat M, Darius HT, Chinain M, Laurent D (2011) First evidence of palytoxin and 42-hydroxy-palytoxin in the marine cyanobacterium Trichodesmium. Mar Drugs 9:543–560. doi: 10.3390/md9040543 Google Scholar
  107. Landsberg JH (2002) The effects of harmful algal blooms on aquatic organisms. Rev Fish Sci 10(2):113–390. doi: 10.1080/20026491051695 Google Scholar
  108. Landsberg J, Van Dolah F, Doucette G (2005) Marine and estuarine harmful algal blooms: impacts on human and animal health. In: Belkin S, Colwell RR (eds) Oceans and health: pathogens in the marine environment. Springer Science+Business Media, Inc, New York, pp 165–210. doi: 10.1007/0-387-23709-7_8
  109. Lee JS, Igarashi T, Fraga S, Dahl E, Hovgaard P, Yasumoto T (1989) Determination of diarrheic shellfish toxins in various dinoflagellate species. J Appl Phycol 1:147–152. doi: 10.1007/BF00003877 Google Scholar
  110. Li A, Ma J, Cao J, Wang Q, Yu R, Thomas K, Quilliam MA (2012) Analysis of paralytic shellfish toxins and their metabolites in shellfish from the North Yellow Sea of China. Food Addit Contam Part A 29(9):1455–1464. doi: 10.1080/19440049.2012.699005 Google Scholar
  111. Litaker RW, Vandersea MW, Faust MA, Kibler SR, Nau AW, Holland WC, Chinain M, Holmes MJ, Tester PA (2010) Global distribution of ciguatera causing dinoflagellates in the genus Gambierdiscus. Toxicon 56:711–730. doi: 10.1016/j.toxicon.2010.05.017 Google Scholar
  112. Liu X, Lu X, Chen Y (2011) The effects of temperature and nutrient rations on Microcystis bloms in Lake Taihu, China: an 11-year investigation. Harmful Algae 10:337–343. doi: 10.1016/j.hal.2010.12.002 Google Scholar
  113. Lugliè A, Giacobbe MG, Fiocca F, Sannio A, Sechi N (2004) The geographical distribution of Alexandrium catenella is extending to Italy! First evidences from the Tyrrhenian Sea. In: Steidinger A, Landsbergh JH, Tomas CR, Vargo GA (eds) Harmful algae 2002. Proceedings of the Xth International Conference on Harmful Algae, St. Pete Beach, Florida, USA, 21–25 Oct 2002, pp 329–331. Florida Fish and Wildlife Conservation Commission and Intergovernmental Oceanographic Commission of UNESCOGoogle Scholar
  114. Margalef R (1978) Life-forms of phytoplankton as survival alternatives in an unstable environment. Oceanol Acta 1(4):493–509Google Scholar
  115. Marine Board—European Science Foundation (2010) Marine biotechnology: a new vision and strategy for Europe. Marine Board-ESF Position Paper 15. http://www.marinebiotech.eu/sites/marinebiotech.eu/files/public/library/MBT%20publications/2010%20ESF%20Position%20Paper.pdf. Accessed 27 Feb 2015
  116. Messineo V, Mattei D, Melchiorre S, Salvatore G, Bogialli S, Salzano R, Mazza R, Capelli G, Bruno M (2006) Microcystin diversity in a Planktothrix rubescens population from Lake Albano (Central Italy). Toxicon 48(2):160–174. doi: 10.1016/j.toxicon.2006.04.006 Google Scholar
  117. Messineo V, Bogialli S, Melchiorre S, Sechi N, Luglié A, Casiddu P, Mariani MA, Padedda BM, Di Corcia A, Mazza R, Carloni E, Bruno M (2009) Cyanobacterial toxins in Italian freshwaters. Limnologica 39(2):95–106. doi: 10.1016/j.limno.2008.09.001 Google Scholar
  118. Messineo V, Melchiorre S, Di Corcia A, Gallo P, Bruno M (2010) Seasonal succession of Cylindrospermopsis raciborskii and Aphanizomenon ovalisporum blooms with cylindrospermopsin occurrence in the volcanic Lake Albano. Central Italy. Environ Toxicol 25(1):18–27. doi: 10.1002/tox.20469 Google Scholar
  119. Metting B, Pyne JW (1986) Biologically active compounds from microalgae. Enz Microb Technol 8(7):386–394. doi: 10.1016/0141-0229(86)90144-4 Google Scholar
  120. Mitrovic SM, Pflugmacher S, James KJ, Furey A (2004) Anatoxin-a elicits an increase in peroxidase and glutathione S-transferase activity in aquatic plants. Aquacult Toxicol 68(2):185–192. doi: 10.1016/j.aquatox.2004.03.017 Google Scholar
  121. Mozetič P, Solidoro C, Cossarini G, Socal G, Precali R, Francé J, Bianchi F, De Vittor C, Smodlaka N, Fonda Umani S (2010) Recent trends towards oligotrophication of the Northern Adriatic: evidence from Chlorophyll-a time series. Estuaries Coasts 33:362–375. doi: 10.1007/s12237-009-9191-7 Google Scholar
  122. Munday R, Quilliam MA, LeBlanc P, Lewis N, Gallant P, Sperker SA, Stephen Ewart H, MacKinnon SL (2012) Investigations into the toxicology of spirolides, a group of marine phycotoxins. Toxins 4(1):1–14. doi: 10.3390/toxins4010001#sthash.fNyxX5pe.dpuf Google Scholar
  123. O’Neil JM, Davis TW, Burford MA, Gobler CJ (2012) The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14:313–334. doi: 10.1016/j.hal.2011.10.027 Google Scholar
  124. Okaichi T, Imatomi Y (1979) Toxicity of Prorocentrum minimum var. mariae-lebouriae assumed to be a causative agent of short-necked clam poisoning. In: Taylor DL, Seliger HH (eds) Toxic dinoflagellates blooms. Elsevier, Amsterdam, pp 385–388Google Scholar
  125. Orsini L, Sarno D, Procaccini G, Poletti R, Dahlmann J, Montresor M (2002) Toxic Pseudo-nitzschia multistriata (Bacillariophyceae) from the Gulf of Naples: morphology, toxin analysis and phylogenetic relationships with other Pseudo-nitzschia species. Eur J Phycol 37:247–257. doi: 10.1017/S0967026202003608 Google Scholar
  126. Paerl HW (2008) Nutrient and other environmental controls of harmful cyanobacterial blooms along the freshwater-marine continuum. In: Hudnell KH (ed) Cyanobacterial harmful algal blooms: state of the science and research needs. Adv Exp Med Biol 619:217–237. doi: 10.1007/978-0-387-75865-7_10
  127. Paerl HW, Huisman J (2008) Blooms like it hot. Science 320:57–58Google Scholar
  128. Paerl HW, Otten TG (2013) Harmful Cyanobacterial blooms: causes, consequences, and controls. Microb Ecol 65(4):995–1010. doi: 10.1007/s00248-012-0159-y Google Scholar
  129. Parsons ML, Aligizaki K, Dechraoui Bottein MY, Fraga S, Morton SL, Penna A, Rhodes L (2012) Gambierdiscus and Ostreopsis: reassessment of the state of knowledge of their taxonomy, geography, ecophysiology, and toxicology. Harmful Algae 14:107–129. doi: 10.1016/j.hal.2011.10.017 Google Scholar
  130. Paul VJ (2008) Global warming and cyanobacterial harmful algal booms. In: Cyanobacterial harmful algal blooms: state of the science and research needs. In: Hudnell KH (ed) Adv Exp Med Biol 619:239–257. Springer Science+Business Media, LLC, New York. doi: 10.1007/978-0-387-75865-7_11
  131. Pearce I, Marshall J, Hallegraeff GM (2000) Toxic temperate epiphytic dinoflagellates in coastal lagoons off the east coast of Tasmania. In: Proceedings of the 9th international conference on harmful algal blooms Tasmania 2000, 7–11 Feb 2000, Wrest Point Convention Centre, Hobart, Tasmania, Australia, p 224. http://frdc.com.au/research/Final_Reports/1998-343-DLD.pdf. Accessed 27 Feb 2015
  132. Penna A, Garcés E, Vila M, Giacobbe MG, Fraga S, Luglié A, Bravo I, Bertozzini E, Vernesi C (2005) Alexandrium catenella (Dinophyceae), a toxic ribotype expanding in the NW Mediterranean Sea. Mar Biol 148:13–23. doi: 10.1007/s00227-005-0067-5 Google Scholar
  133. Penna A, Bertozzini E, Battocchi C, Galluzzi L, Giacobbe MG, Vila M, Garcés E, Luglié A, Magnani M (2007) Monitoring of HAB species in the Mediterranean Sea through molecular methods. J Plankton Res 29(1):19–38. doi: 10.1093/plankt/fbl053 Google Scholar
  134. Perini F, Casabianca A, Battocchi C, Accoroni S, Totti C, Penna A (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):e17699Google Scholar
  135. Perl TM, Bedard L, Kosatsky T, Hockin JC, Todd ECD, Remis RS (1990) An outbreak of toxic encephalopathy caused by eating mussels contaminated with domoic acid. New Engl J Med 322:1775–1780Google Scholar
  136. Pitcher GC (2012) The requirement for species-specific information. Preface. Harmful Algae 14:1–4. doi: 10.1016/j.hal.2011.10.011 Google Scholar
  137. Poletti R, Cettul K, Bovo F, Frate R (1995) Evoluzione delle dinoflagellate tossiche nell’alto Adriatico dal 1989 al 1994 e ricaduta sulla commercializzazione dei molluschi eduli. In: Evoluzione dello stato trofico in Adriatico: analisi degli interventi attuali e future linee di intervento. Marina di Ravenna, 28-29 settembre, 1995, pp 253–258. Regione Emilia Romagna, Provincia di Ravenna, Autorità del fiume PoGoogle Scholar
  138. Potts GW, Edwards JM (1987) The impact of a Gyrodinium aureolum bloom on inshore young fish populations. J Mar Biol Ass UK 67:293–297. doi: 10.1017/S0025315400026618 Google Scholar
  139. Quijano-Scheggia S, Garcés E, Van Lenning K, Sampedro N, Camp J (2005) First time detection of the diatom species Pseudo-nitzschia brasiliana (non toxic) and its relative P. multistriata (presumably toxic) algon the NW mediterranean Sea. Harmful Algal News 29:5Google Scholar
  140. Rabbani MM, Rehman AU, Harms EC (1990) Mass mortality of fishes caused by dinoflagellate blooms in Gwadar Bay, Southwestern Pakistan. In: Graneli E, SunDSTrom B, Edler L, Anderson DM (eds) Toxic Marine Phytoplankton. Elsevier, Amsterdam, pp 209–214Google Scholar
  141. Reguera B, Velo-Suárez L, Raine R, Park RG (2012) Harmful Dinophysis species: a review. Harmful Algae 14:87–106Google Scholar
  142. Reynolds CS (1988) The concept of ecological succession applied to seasonal periodicity of freshwater phytoplankton. Verh Int Ver Limnol 23:683–691Google Scholar
  143. Reynolds CS, Smayda TJ (1998) Principles of species selection and community assembly in the phytoplankton: further explorations of the Mandala. 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 8–10Google Scholar
  144. Rossini GP (ed) (2014) Toxins and Biologically active compounds from microalgae. CRC Press, Boca RatonGoogle Scholar
  145. Sansoni G, Borghini B, Camici G, Casotti M, Righini P, Rustighi C (2003) Fioriture algali di Ostreopsis ovata (Gonyaulacales: Dinophyceae): un problema emergente. Biologia Ambientale 17(1):17–23Google Scholar
  146. Sechet V, Quilliam AM, Rocher G (1998) Diarrhetic Shellfish Poisoning (DSP) toxins in Prorocentrum lima in axenic and non-axenic batch culture: detection of new compound and kinetics of production. In: Reguera B, Blanco J, Fernández ML, Wyatt T (eds) Hamful algae. Xunta de Galicia and intergovernmental oceanographic commission of UNESCO, Santiago de Compostela, pp 485–488Google Scholar
  147. Sivonen K, Jones G (1999) Cyanobacterial toxins. In: Chorus I, Bartram J (eds) Toxic cyanobacteria in water. A guide to their public health consequences. monitoring and management. E and FN Spoon, London, pp 41–111Google Scholar
  148. Skulberg OM (1999) The biological nature of cyanotoxins-types and effects. In: ICRO-UNESCO workshop and training course notes. Pannon Agric. University, HungaryGoogle Scholar
  149. Skulberg OM, Skulberg R (1985) Planktic species of Oscillatoria (Cyanophyceae) from Norway—characterization and classification. Arch Hydrobiol Suppl 71 Algol Stud 38/39:157–174Google Scholar
  150. Steidinger KA, Burklew MA, Ingle RM (1973) The effects of Gymnodinium breve toxin on estuarine animals. In: Martin DF, Padilla GM (eds) Marine pharmacology, action of marine biotoxins at the cellular level, Chapter VI. Academic Press, New York, pp 179–202Google Scholar
  151. Sykes PF, Huntley ME (1987) Acute physiological reactions of Calanus pacificus to selected dinoflagellates: direct observations. Mar Biol 94:19–24. doi: 10.1007/BF00392895 Google Scholar
  152. Tosteson RT, Ballantine LD, Winter A (1998). Sea surface temperature, benthic dinoflagellate toxicity and toxin transmission in the ciguatera food web. 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 48–49Google Scholar
  153. Totti C, Civitarese G, Acri F, Barletta D, Candelari G, Paschini E, Solazzi A (2000) Seasonal variability of phytoplankton populations in the middle Adriatic sub-basin. J Plankton Res 22(9):1735–1756. doi: 10.1093/plankt/22.9.1735 Google Scholar
  154. Totti C, Accoroni S, Cerino F, Cucchiari E, Romagnoli T (2010) Ostreopsis ovata bloom along the Conero Riviera (northern Adriatic Sea): Relationships with environmental conditions and substrata. Harmful Algae 9(2):233–239. doi: 10.1016/j.hal.2009.10.006 Google Scholar
  155. Tubaro A, Sosa S, Bruna M, Gucci PMB, Volterra L, Loggia RD (1992) Diarrhoeic shellfish toxins in Adriatic sea mussels evaluated by an Elisa method. Toxicon 30(5/6):673–676. doi: 10.1016/0041-0101(92)90861-X Google Scholar
  156. van den Hoek C, Mann DG, Jahns HM (eds) (1995) Algae. An introduction to phycology. Cambridge University Press, CambridgeGoogle Scholar
  157. van Dolah FM (2000) Marine algal toxins: origins, health effects, and their increased occurrence. Environ Health Perspect 108(Suppl 1):133–141Google Scholar
  158. Vila M, Camp J, Garcés E, Masó M, Delgado M (2001) High resolution spatio-temporal detection of potentially harmful dinoflagellates in confined waters of the NW Mediterranean. J Plankton Res 23(5):497–514. doi: 10.1093/plankt/23.5.497 Google Scholar
  159. Vila M, Giacobbe MG, Masó M, Gangemi E, Penna A, Sampedro N, Azzaro F, Camp J, Galluzzi L (2005) A comparative study on recurrent blooms of Alexandrium minutum in two mediterranean coastal areas. Harmful Algae 4:673–695. doi: 10.1016/j.hal.2004.07.006 Google Scholar
  160. Viviani R (1992) Biotossine e prodotti della pesca e dell’acquacoltura. Laguna 5:73–83Google Scholar
  161. White AW (1984) Paralytic shellfish toxins and finfish. In: Ragelis EP (ed) Seafood toxins, ACS symposium series 262. American Chemical Society, Washington, pp 171–180Google Scholar
  162. Yasumoto T, Oshima Y, Yamaguchi M (1978) Occurrence of a new type of shellfish poisoning in the Tohoku district. Nippon Suisan Gakkaishi 44(II):1249–1255Google Scholar
  163. Zingone A, Wyatt T (2005) Harmful algal blooms: keys to the understanding of phytoplankton ecology. In: Robinson AR, Brink KH (eds) The Sea. the global coastal ocean: multiscale interdisciplinary processes. Harvard University Press, HarvardGoogle Scholar
  164. Zingone A, Garcés E, Wyatt T, Silvert B, Bolch C (2001) The importance of life cycles in the ecology of harmful algal blooms. In: Garcés E, Zingone A, Montresor M, Reguera B, Dale B (eds) LIFEHAB life histories of microalgal species causing harmful blooms. European Commission Directorate General, Science, Research and DevelopmentGoogle Scholar

Copyright information

© The Author(s) 2015

Authors and Affiliations

  • Antonino Santi Delia
    • 1
  • Gabriella Caruso
    • 2
  • Lucia Melcarne
    • 1
  • Giorgia Caruso
    • 3
  • Salvatore Parisi
    • 4
  • Pasqualina Laganà
    • 1
  1. 1.Department of Biomedical Sciences and Morphological and Functional ImagesUniversity of MessinaMessinaItaly
  2. 2.Italian National Research Council, Institute for Coastal Marine EnvironmentMessinaItaly
  3. 3.Industrial ConsultantPalermoItaly
  4. 4.Industrial ConsultantPalermoItaly

Personalised recommendations