Harmful algae and toxis in paranaguá bay , Brazil: bases for monitoring

Mafra Junior, Luiz Laureno; Fernandes, Luciano Felício; Proença, Luís Antonio O.

Abstracts

The estuarine complex of Paranaguá - ECP (South Brazil, 25º30'S, 48º30'W) is a large subtropical system, where pristine mangrove forests are still present, and fishery and aquaculture are important economic activities. This work investigated the occurrence of harmful algae in Paranaguá Bay, as well as the presence of toxins in the filter feeding mussel Mytella guyanensis, a local fishery resource. Samples along the Paranaguá sub-system were collected almost monthly from August 2002 to October 2003. Besides physical and chemical variables, cell densities of harmful species and presence of toxins in the mussel by mouse bioassay (DSP, PSP) and HPLC (ASP) were performed. HAB species included Pseudo-nitzschia spp., Dinophysis acuminata,Prorocentrum minimum,Gymnodinium catenatum,Phaeocystis spp., Chattonella spp. and Heterosigma akashiwo.Trichodesmium erythraeum and Coscinodiscus wailesii were also included in this study due to their potential for harmful bloom formation. Toxin results showed the occurrence of DSP (December 2002) in shellfish related to the presence of D. acuminata (max. 4,566 cells.l-1). Additionally, cultivated strains produced paralytic and amnesic toxins in laboratory. Spring (October to December, Southern Hemisphere) and late summer (February to April) were the periods of higher abundance of harmful algae, mainly in euhaline and inner polyhaline sectors of the ECP.

Phytoplankton; Harmful Algae; Monitoring; Toxins; Mytella guyanensis; Paranaguá; South Brazil

O complexo estuarino de Paranaguá (CEP; 25º30'S, 48º30'W), localizado no litoral sul do Brasil, abriga extensas áreas preservadas de manguezais e tem a pesca e aqüicultura como importantes atividades econômicas. Este trabalho investigou a ocorrência de microalgas nocivas no CEP e a presença de ficotoxinas no molusco bivalve Mytella guyanensis. Para tanto, foram coletadas amostras com periodicidade aproximadamente mensal, entre agosto de 2002 e outubro de 2003. Foram avaliadas variáveis físico-químicas, densidade de espécies nocivas e a presença de toxinas nos moluscos através de bioensaio com camundongos (DSP e PSP) e por cromatografia líquida (ASP). As espécies nocivas encontradas foram Pseudo-nitzschia spp., Dinophysis acuminata,Prorocentrum minimum,Gymnodinium catenatum,Phaeocystis spp., Chattonella spp. e Heterosigma akashiwo. Além dessas, Trichodesmium erythraeum e Coscinodiscus wailesii foram também incluídas no estudo pelo potencial de produzirem eventos nocivos na região. Toxinas diarréicas (DSP) foram detectadas em moluscos em dezembro de 2002 associadas à presença de D. acuminata (até 4.566 cel.l-1). Toxinas paralisantes e amnésicas foram produzidas por cepas cultivadas em laboratório. Primavera (de outubro a dezembro no hemisfério Sul) e final do verão (fevereiro a abril) foram os períodos de maior abundância de algas nocivas principalmente nos setores euhalino e polihalino interno do CEP.

Fitoplâncton; Algas Nocivas; Monitoramento; Toxinas; Mytella guyanensis; Paranaguá; Sul do Brasil

Anderson, D. M.; Andersen, P.; Bricelj, V. M.; Cullen, J. J.; Rensel, J. E. 2001. Monitoring and management strategies for Harmful Algal Blooms in Coastal Waters, APEC # 201-MR-01.1 (IOC Technical Series No. 59). Paris, IOC-UNESCO. 268p.
AOAC. 1990. Paralytic shellfish poison: Biological method. Final Action. In: Hellrich, K. ed. Official Methods of Analysis. Arlington, Association of Official Analytical Chemists. p. 881-882.
APHA - American Public Health Association/ AWWA - American Water Works Association/ WEF - Water Environmental Federation. 1999. Standard Methods for the Examination of Water and Wastewater. 20^th ed. Washington, D.C., American Public Health Association. 1220p.
Bates, S. S.; Garrison, D. L.; Horner, R. A. 1998. Bloom dynamics and physiology of domoic acid-producing Pseudo-nitzschia species. In: Anderson, D. M.; Cembella, A. D.; Hallegraeff, G. M. eds. Physiological Ecology of Harmful Algal Blooms. Heidelberg, Springer-Verlag. p. 267-292.
Brandini, F. P. 1988. Composição e distribuição do fitoplâncton na região Sueste do Brasil e suas relações com as massas de água (Operação Sueste - julho/agosto 1982). Ciência e Cultura, v. 40(4):334-341.
Brandini, F. P.; Thamm, C. A.; Ventura, I. 1988. Ecological Studies in the Bay of Paranaguá. III. Seasonal and Spatial Variations of Nutrients and Chlorophyll-a. Nerítica, 3(1):1-30.
Burkholder, J. M. & Glasgow Jr., H. B. 1997. Trophic controls on stage transformations of a toxic amnush-predator dinoflagellate. J. Eukariot. Microbiol., 44(3):200-205.
Chang, F. H. 1996. Distribution and abundance of Dinophysis acuminata (Dinophyceae) and Pseudonitzschia australis (Bacillariophyceae) in Kenepuru and Pelorus Sounds, New Zealand. In: Yasumoto, T.; Oshima,Y.; Fukuyo, Y. eds. Harmful and toxic algal blooms. Paris, UNESCO. p. 93-96.
Clementson, L. A.; Parslow, J. S.; Turnbull, A. R.; Bonham, P. I. 2004. Properties of light absorption in a highly coloured estuarine system in south-east Australia which is prone to blooms of the toxic dinoflagellate Gymnodinium catenatum Estuar. Coast. Shelf Sci., 60(1):101-112.
Fan, C.; Glibert, P. M.; Burkholder, J. M. 2003. Characterization of the affinity for nitrogen, uptake kinetics, and environmental relationships for Prorocentrum minimum in natural blooms and laboratory cultures. Harmful Algae, 2:283-299.
Fernandes, L. F.; Zehnder-Alves, L.; Bassfeld, J. 2001. The recently established diatom Coscinodiscus wailesii (Coscinodiscales, Bacillariophyta) in Brazilian waters. I. Remarks on morphology and distribution. Phycol. Res., 49:89-96.
Fernández, M. L.; Richard, D. J. A.; Cembella, A. D. 2003. In vivo assays for phycotoxins. In: Hallegraeff, G. M.; Anderson, D. M.; Cembella, A. D. eds. Manual on Harmful Marine Microalgae - Monographs on oceanographic methodology 11. 2^nd ed. Paris, UNESCO. p. 347-380.
Gárate-Lizárraga, I.; Bustillos-Gusman, J. J.; Alonso-Rodriguez, R.; Luckas, B. 2004. Comparative paralytic shellfish toxin profiles in two marine bivalves during outbreaks of Gymnodinium catenatum (Dinophyceae) in the Gulf of California. Mar. Pollut. Bull., 48:378-402.
Hallegraeff, G. M. 2003. Harmful Algal Blooms: a global overview. In: Hallegraeff, G. M.; Anderson, D. M.; Cembella, A. D. eds. Manual on Harmful Marine Microalgae - Monographs on oceanographic methodology 11. 2^nd ed. Paris, UNESCO. p. 25-50.
Holmes, R. W. 1970. The Secchi disk in turbid coastal zones. Limnol. Oceanogr., 31:688-694.
Imai, I.; Yamaguchi, M.; Watanabe, M. 1998. Ecophysiology, life cycle, and bloom dynamics of Chattonella in the Seto Inland Sea, Japan. In: Anderson, D. M.; Cembella, A. D.; Hallegraeff, G. M. eds. Physiological Ecology of Harmful Algal Blooms. Heidelberg, Springer-Verlag. p. 95-111.
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Knoppers, B. A.; Brandini, F. P.; Thamm, C. A. C. 1987. Ecological studies in the Bay of Paranaguá. II. Some physical and chemical characteristics. Nerítica, 2(1):1-36.
Köppen, W. 1936. Das geographische System der Klimate. In: Köppen, W. & Geiger, R. eds. Handbuch der Klimatologie. Berlin, Gebrüder Bornträger, 1(1):part C.
Lana, P. C.; Marone, E.; Lopes, R. M.; Machado, E. C. 2001. The subtropical estuarine complex of Paranaguá Bay, Brazil. In: Selliger, U.; Kjerfve, P. eds. Ecological Studies, v. 144 - Coastal Marine Ecosystems of Latin America. Berlin, Springer-Verlag Berlin Heidelberg. p. 131-145.
Lancelot, C.; Keller, M. D.; Rousseau, V.; Smith Jr., W. O.; Mathot, S. 1998. Autoecology of the marine haptophyte Phaeocystis sp. In: Anderson, D.; Cembella, A.D.; Hallegraeff, G.H. eds. Physiological Ecology of Harmful Algal Blooms: NATO ASI Series, v. G41. Berlin, Springer-Verlag Berlin Heidelberg. p. 209-224.
Lee, J. H.; Yanagi, T.; Kenma, R.; Yasumoto, T. 1987. Fluorometric determination of diarrhetic shellfish toxins by high-performance liquid chromatography. Agr. Biol. Chem., 51(3)877-881.
Llewellyn, L..; Negri, A.; Quilliam, M. 2004. High affinity for the rat brain sodium channel of newly discovered hydroxybenzoate saxitoxin analogues from the dinoflagellate Gymnodinium catenatum Toxicon, 43:101-104.
Machado, E. C.; Daniel, C. B.; Brandini, N.; Queiroz, R. L. V. 1997. Temporal and spatial dynamics of nutrients and particulate suspended matter in Paranaguá Bay, PR, Brazil. Nerítica, 11:15-34.
MacKenzie, L.; Beuzenberg, V. Holland, P.; McNabb, P.; Suzuki, T.; Selwood, A. 2005. Pectenotoxin and okadaic acid-based toxin profiles in Dinophysis acuta and Dinophysis acuminata from New Zealand. Harmful Algae, 4(1):75-85.
Marone, E. & Camargo, R. 1994. Marés meteorológicas no litoral do estado do Paraná: o evento de agosto de 1993. Nerítica, 8(1-2):73-85.
Míguez, A.; Fernández, M. L.; Fraga, S. 1996. First detection of domoic acid in Galicia (NW of Spain). In: Yasumoto, T.; Oshima,Y.; Fukuyo, Y. eds. Harmful and toxic algal blooms. Paris, UNESCO. p. 143-145.
Negri, A. P.; Bunter, O.; Jones, B.; Llewellyn, L. 2004. Effects of the bloom-forming alga Trichodesmium erythraeum on the pearl oyster Pinctada máxima Aquaculture, 232(1-4)91-102.
Odebrecht, C.; Azevedo, S. M. F. Q.; Garcia, V. M. T.; Huszar, V.; Magalhães, V. F.; Menezes, M.; Proença, L. A. O.; Rörig, L. R.; Tenenbaum, D. R.; Villac, M. C.; Yunes, J. S. 2002. Floraciones de microalgas nocivas en Brasil: estado del arte y proyectos en curso. In: Sar, E. A.; Ferrario, M. E.; Reguera, B. eds. Floraciones Algales Nocivas en el Cono Sur Americano. Vigo, Instituto Español de Oceanografia. p. 219-233.
Pereira, A. D.; Klein, D.; Sohet, K.; Houvenagel, G.; Braekman, J.C. 1995. Improvement to the HPLC-Fluorescence analysis method for the determination of acid DSP toxins. In: Lassus, P.; Arzul, G.; Erard-Le Denn, E.; Gentien, P.; Marcaillou-Le Baut, C. eds. Harmful Marine Algal Blooms. Paris, Lavoisier. p. 33-38.
Proença, L. A. O. 2002. Clorofila a do fitoplâncton em seis enseadas utilizadas para o cultivo de moluscos bivalves no litoral de Santa Catarina. Notas Técnicas da FACIMAR, 6:33-44.
Proença, L. A. O. & Fernandes, L. F. 2004. Introdução de microalgas no ambiente marinho: impactos negativos e fatores controladores. In: Silva, J. S. V. & Souza, R. C. C. L. eds. Água de Lastro e Bioinvasão. Rio de Janeiro, Interciência. p. 77-97.
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Quilliam, M. A.; Xie, M.; Hardstaff, W. R. 1995. A rapid extraction and cleanup procedure for the liquid chromatographic determination of domoic acid in unsalted seafood. In: Hallegraeff, G. M.; Anderson, D. M.; Cembella, A. D. ed. Manual on Harmful Marine Microalgae. Paris, UNESCO. p. 95-112.
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Publication Dates

Publication in this collection
01 Nov 2007
Date of issue
Sept 2006

History

Accepted
25 Apr 2006
Reviewed
05 Oct 2005
Received
15 Aug 2005

This work is licensed under a Creative Commons Attribution 4.0 International License.

[1] Anderson, D. M.; Andersen, P.; Bricelj, V. M.; Cullen, J. J.; Rensel, J. E. 2001. Monitoring and management strategies for Harmful Algal Blooms in Coastal Waters, APEC # 201-MR-01.1 (IOC Technical Series No. 59). Paris, IOC-UNESCO. 268p.

[2] AOAC. 1990. Paralytic shellfish poison: Biological method. Final Action. In: Hellrich, K. ed. Official Methods of Analysis. Arlington, Association of Official Analytical Chemists. p. 881-882.

[3] APHA - American Public Health Association/ AWWA - American Water Works Association/ WEF - Water Environmental Federation. 1999. Standard Methods for the Examination of Water and Wastewater. 20^th ed. Washington, D.C., American Public Health Association. 1220p.

[4] Bates, S. S.; Garrison, D. L.; Horner, R. A. 1998. Bloom dynamics and physiology of domoic acid-producing Pseudo-nitzschia species. In: Anderson, D. M.; Cembella, A. D.; Hallegraeff, G. M. eds. Physiological Ecology of Harmful Algal Blooms. Heidelberg, Springer-Verlag. p. 267-292.

[5] Brandini, F. P. 1988. Composição e distribuição do fitoplâncton na região Sueste do Brasil e suas relações com as massas de água (Operação Sueste - julho/agosto 1982). Ciência e Cultura, v. 40(4):334-341.

[6] Brandini, F. P.; Thamm, C. A.; Ventura, I. 1988. Ecological Studies in the Bay of Paranaguá. III. Seasonal and Spatial Variations of Nutrients and Chlorophyll-a. Nerítica, 3(1):1-30.

[7] Burkholder, J. M. & Glasgow Jr., H. B. 1997. Trophic controls on stage transformations of a toxic amnush-predator dinoflagellate. J. Eukariot. Microbiol., 44(3):200-205.

[8] Chang, F. H. 1996. Distribution and abundance of Dinophysis acuminata (Dinophyceae) and Pseudonitzschia australis (Bacillariophyceae) in Kenepuru and Pelorus Sounds, New Zealand. In: Yasumoto, T.; Oshima,Y.; Fukuyo, Y. eds. Harmful and toxic algal blooms. Paris, UNESCO. p. 93-96.

[9] Clementson, L. A.; Parslow, J. S.; Turnbull, A. R.; Bonham, P. I. 2004. Properties of light absorption in a highly coloured estuarine system in south-east Australia which is prone to blooms of the toxic dinoflagellate Gymnodinium catenatum Estuar. Coast. Shelf Sci., 60(1):101-112.

[10] Fan, C.; Glibert, P. M.; Burkholder, J. M. 2003. Characterization of the affinity for nitrogen, uptake kinetics, and environmental relationships for Prorocentrum minimum in natural blooms and laboratory cultures. Harmful Algae, 2:283-299.

[11] Fernandes, L. F.; Zehnder-Alves, L.; Bassfeld, J. 2001. The recently established diatom Coscinodiscus wailesii (Coscinodiscales, Bacillariophyta) in Brazilian waters. I. Remarks on morphology and distribution. Phycol. Res., 49:89-96.

[12] Fernández, M. L.; Richard, D. J. A.; Cembella, A. D. 2003. In vivo assays for phycotoxins. In: Hallegraeff, G. M.; Anderson, D. M.; Cembella, A. D. eds. Manual on Harmful Marine Microalgae - Monographs on oceanographic methodology 11. 2^nd ed. Paris, UNESCO. p. 347-380.

[13] Gárate-Lizárraga, I.; Bustillos-Gusman, J. J.; Alonso-Rodriguez, R.; Luckas, B. 2004. Comparative paralytic shellfish toxin profiles in two marine bivalves during outbreaks of Gymnodinium catenatum (Dinophyceae) in the Gulf of California. Mar. Pollut. Bull., 48:378-402.

[14] Hallegraeff, G. M. 2003. Harmful Algal Blooms: a global overview. In: Hallegraeff, G. M.; Anderson, D. M.; Cembella, A. D. eds. Manual on Harmful Marine Microalgae - Monographs on oceanographic methodology 11. 2^nd ed. Paris, UNESCO. p. 25-50.

[15] Holmes, R. W. 1970. The Secchi disk in turbid coastal zones. Limnol. Oceanogr., 31:688-694.

[16] Imai, I.; Yamaguchi, M.; Watanabe, M. 1998. Ecophysiology, life cycle, and bloom dynamics of Chattonella in the Seto Inland Sea, Japan. In: Anderson, D. M.; Cembella, A. D.; Hallegraeff, G. M. eds. Physiological Ecology of Harmful Algal Blooms. Heidelberg, Springer-Verlag. p. 95-111.

[17] IOC Taxonomic Reference List of Toxic Plankton Algae. In: Intergovernmental Oceanographic Commission. http:// www.bi.ku.dk/ioc, 2003 (on-line).

[18] Knoppers, B. A.; Brandini, F. P.; Thamm, C. A. C. 1987. Ecological studies in the Bay of Paranaguá. II. Some physical and chemical characteristics. Nerítica, 2(1):1-36.

[19] Köppen, W. 1936. Das geographische System der Klimate. In: Köppen, W. & Geiger, R. eds. Handbuch der Klimatologie. Berlin, Gebrüder Bornträger, 1(1):part C.

[20] Lana, P. C.; Marone, E.; Lopes, R. M.; Machado, E. C. 2001. The subtropical estuarine complex of Paranaguá Bay, Brazil. In: Selliger, U.; Kjerfve, P. eds. Ecological Studies, v. 144 - Coastal Marine Ecosystems of Latin America. Berlin, Springer-Verlag Berlin Heidelberg. p. 131-145.

[21] Lancelot, C.; Keller, M. D.; Rousseau, V.; Smith Jr., W. O.; Mathot, S. 1998. Autoecology of the marine haptophyte Phaeocystis sp. In: Anderson, D.; Cembella, A.D.; Hallegraeff, G.H. eds. Physiological Ecology of Harmful Algal Blooms: NATO ASI Series, v. G41. Berlin, Springer-Verlag Berlin Heidelberg. p. 209-224.

[22] Lee, J. H.; Yanagi, T.; Kenma, R.; Yasumoto, T. 1987. Fluorometric determination of diarrhetic shellfish toxins by high-performance liquid chromatography. Agr. Biol. Chem., 51(3)877-881.

[23] Llewellyn, L..; Negri, A.; Quilliam, M. 2004. High affinity for the rat brain sodium channel of newly discovered hydroxybenzoate saxitoxin analogues from the dinoflagellate Gymnodinium catenatum Toxicon, 43:101-104.

[24] Machado, E. C.; Daniel, C. B.; Brandini, N.; Queiroz, R. L. V. 1997. Temporal and spatial dynamics of nutrients and particulate suspended matter in Paranaguá Bay, PR, Brazil. Nerítica, 11:15-34.

[25] MacKenzie, L.; Beuzenberg, V. Holland, P.; McNabb, P.; Suzuki, T.; Selwood, A. 2005. Pectenotoxin and okadaic acid-based toxin profiles in Dinophysis acuta and Dinophysis acuminata from New Zealand. Harmful Algae, 4(1):75-85.

[26] Marone, E. & Camargo, R. 1994. Marés meteorológicas no litoral do estado do Paraná: o evento de agosto de 1993. Nerítica, 8(1-2):73-85.

[27] Míguez, A.; Fernández, M. L.; Fraga, S. 1996. First detection of domoic acid in Galicia (NW of Spain). In: Yasumoto, T.; Oshima,Y.; Fukuyo, Y. eds. Harmful and toxic algal blooms. Paris, UNESCO. p. 143-145.

[28] Negri, A. P.; Bunter, O.; Jones, B.; Llewellyn, L. 2004. Effects of the bloom-forming alga Trichodesmium erythraeum on the pearl oyster Pinctada máxima Aquaculture, 232(1-4)91-102.

[29] Odebrecht, C.; Azevedo, S. M. F. Q.; Garcia, V. M. T.; Huszar, V.; Magalhães, V. F.; Menezes, M.; Proença, L. A. O.; Rörig, L. R.; Tenenbaum, D. R.; Villac, M. C.; Yunes, J. S. 2002. Floraciones de microalgas nocivas en Brasil: estado del arte y proyectos en curso. In: Sar, E. A.; Ferrario, M. E.; Reguera, B. eds. Floraciones Algales Nocivas en el Cono Sur Americano. Vigo, Instituto Español de Oceanografia. p. 219-233.

[30] Pereira, A. D.; Klein, D.; Sohet, K.; Houvenagel, G.; Braekman, J.C. 1995. Improvement to the HPLC-Fluorescence analysis method for the determination of acid DSP toxins. In: Lassus, P.; Arzul, G.; Erard-Le Denn, E.; Gentien, P.; Marcaillou-Le Baut, C. eds. Harmful Marine Algal Blooms. Paris, Lavoisier. p. 33-38.

[31] Proença, L. A. O. 2002. Clorofila a do fitoplâncton em seis enseadas utilizadas para o cultivo de moluscos bivalves no litoral de Santa Catarina. Notas Técnicas da FACIMAR, 6:33-44.

[32] Proença, L. A. O. & Fernandes, L. F. 2004. Introdução de microalgas no ambiente marinho: impactos negativos e fatores controladores. In: Silva, J. S. V. & Souza, R. C. C. L. eds. Água de Lastro e Bioinvasão. Rio de Janeiro, Interciência. p. 77-97.

[33] Proença, L. A. O. & Mafra Jr., L. L. 2005. Ocorrência de ficotoxinas na costa brasileira. In: Reunião Brasileira de Ficologia, X. 2004. Anais. (Série Livros do Museu Nacional; 10). Rio de Janeiro, Museu Nacional. p. 57-77.

[34] Proença, L. A. O.; Schmit, F.; Tamanaha, M.S.; Guimarães, S.; Rörig, L. 1999. Produção de ácido okadaico, uma toxina diarréica, por Dinophysis acuminata em Santa Catarina. Atlântica, 21:121-127.

[35] Quilliam, M. A.; Xie, M.; Hardstaff, W. R. 1995. A rapid extraction and cleanup procedure for the liquid chromatographic determination of domoic acid in unsalted seafood. In: Hallegraeff, G. M.; Anderson, D. M.; Cembella, A. D. ed. Manual on Harmful Marine Microalgae. Paris, UNESCO. p. 95-112.

[36] Schantz, E. J. 1984. Historical perspective on paralytical shellfish poisoning. In: Ragelis, M. ed. Seafood Toxins, ACS - Symposium Series 262. Washington, D.C., American Chemical Society. p. 99-111.

[37] Setälä, O.; Autio, R.; Kuosa, H.; Rintala, J.; Ylostalo, P. 2005. Survival and photosynthetic activity of different Dinophysis acuminata populations in the northern Baltic Sea. Harmful Algae, 4(2):337-350.

[38] Smayda, T. J. 1997. What is a bloom? A commentary. Limnol. Oceanogr., 42:1132-1136.

[39] Smayda, T. J. 1998. Ecophysiology and Bloom Dynamics of Heterosigma akashiwo (Raphidophyceae). In: Anderson, D. M.; Cembella, A. D.; Hallegraeff, G. M. eds. Physiological Ecology of Harmful Algal Blooms. Heidelberg, Springer-Verlag. p. 113-131.

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