Harmful algae in the Paranaguá Estuarine Complex, Brazil: a spatio-temporal assessment
DOI:
https://doi.org/10.1590/Keywords:
Algal blooms, Marine phytoplankton, Toxin accumulation, Brazilian coast, Subtropical estuaryAbstract
Harmful algal blooms (HABs) can negatively affect coastal water quality, aquatic fauna, and human health from the consumption of toxin-contaminated seafood. Estuaries are especially prone to the incidence of these noxious events and sensitive to the associated damage. This study represents a comprehensive overview of previous investigations reporting the occurrence of harmful algae and/or phycotoxins in the Paranaguá Estuarine Complex (CEP), in Southern Brazil. Secondary data from 2002 to 2021 were combined with new results obtained from widely spaced sampling campaigns performed from 2018 to 2019 to assess the periods and estuarine sectors at greater risk for the incidence of HABs. In total, about 600 water/sediment samples containing harmful microalgae and 675 tissue samples of phycotoxin-contaminated fauna were analyzed. The most frequent and abundant species of potentially toxic microalgae were dinoflagellates belonging to the species complexes Dinophysis acuminata and Prorocentrum lima, producers of diarrhetic shellfish toxins (DSTs), and diatoms of the genus Pseudo-nitzschia, producers of amnesic shellfish toxins (ASTs). Okadaic acid, a DST, was by far the most common toxin in the fauna, reaching higher levels in primary consumers such as bivalve mollusks (mussels, oysters, and clams), zooplankton, and suspension-feeding crustaceans (ghost shrimps), and moderate to low levels in cephalopods, fishes, gastropods, echinoderms, sea turtles, seabirds, and cetaceans. Less rainy periods (winter-early spring) were associated with the highest incidence of DSTs and blooms of their producing algae P. lima and Dinophysis spp., mainly in the middle region of Paranaguá Bay and on the shallow continental platform adjacent to the estuarine mouth. However, certain HAB-forming species may be more successful in inner estuarine areas (Prorocentrum cordatum) and during different periods, such as late summer—early fall (Pseudo-nitzschia spp.). Continuous monitoring.
References
Alves, T. & Mafra, L. 2018. Diel Variations in Cell Abundance and Trophic Transfer of Diarrheic Toxins during a Massive Dinophysis Bloom in Southern Brazil. Toxins, 10(6), 232. DOI: https://doi.org/10.3390/toxins10060232.
Alves, T. P., Schramm, M. A., Proença, L. A. O., Pinto, T. O. & Mafra, L. L. 2018. Interannual variability in Dinophysis spp. abundance and toxin accumulation in farmed mussels (Perna perna) in a subtropical estuary. Environmental Monitoring and Assessment, 190(6).
DOI: https://doi.org/10.1007/s10661-018-6699-y.
Anderle, P. N. 2004. Fitoplâncton na baía de Paranaguá, Paraná, Brasil (thesis). Setor de Ciências Biológicas, Departamento de Botânica, Universidade Federal do Paraná, Curitiba. Accessed on May 26 2023: https://acervodigital.ufpr.br/handle/1884/32259?show=full.
Angulo, M. A., Soares, C. R., Marone, E., Souza, M. C., Odreski, L. L. R. & Noernberg, M. A. 2004. Atlas de erosão costeira do Estado do Paraná. In: Erosão e progradação no litoral brasileiro (pp. 347–400). MMA. Accessed on May 19 2023: https://www.researchgate. net/publication/303260024_Atlas_de_erosao_costeira_do_Estado_do_Parana.
APPA (Administração dos Portos de Paranaguá e Antonina). 2013. Plano de Emergência Individual – PEI (6th ed.). Paranaguá: APPA. Accessed on May 19 2023: https://www.portosdoparana.pr.gov.br/Meio-Ambiente/Pagina/Plano-de-Emergencia-Individual.
APPA (Administração dos Portos de Paranaguá e Antonina). 2021. Relatório anual do subprograma de monitoramento da comunidade planctônica (ref. 2021). Paranaguá: Portos do Paraná.
Ávila, E. C. 2011. Variação temporal da biodiversidade e abundância do fitoplâncton em Pontal do Sul - PR (thesis). Universidade Federal do Paraná, Pontal do Paraná. Accessed on May 26 2023: https://acervodigital.ufpr.br/handle/1884/75833.
Brandini, F. P. 1985. Ecological studies in the Bay of Paranaguá: I. horizontal distribution and seasonal dynamics of the phytoplankton. Boletim do Instituto Oceanográfico, 33(2), 139–147. DOI: https://doi.org/10.1590/s0373-55241985000200004.
Brandini, F. P. & Fernandes, L. F. 1996. Microalgae of the continental shelf off Paraná State, southeastern Brazil: a review of studies. Revista Brasileira de Oceanografia, 44(1), 69–80. DOI: https://doi.org/10.1590/s1413-77391996000100008.
Brandini, F. P., Thamm, C. A. & Ventura, I. 1988. Ecological studies in the Bay of Paranagua. III. Seasonal and spatial variations of nutrients and chlorophyll a. Nerítica, 3(1), 1–30.
Brustolin, M. C., Thomas, M. C., Mafra, L. L. & Lana, P. C. 2014. Does Encope emarginata (Echinodermata: Echinoidea) affect spatial variation patterns of estuarine subtidal meiofauna and microphytobenthos? Journal of Sea Research, 91, 70–78. DOI: https://doi.org/10.1016/j.seares.2014.03.006.
Carvalho, I. F. P. 2013. Avaliação do impacto de florações de Coscinodiscus wailesii (Gran et Angst) na Baía de Paranaguá, Brasil (thesis). Universidade Federal do Paraná, Pontal do Sul. https://acervodigital.ufpr.br/xmlui/handle/1884/75396. Accessed on May 26 2023.
Dolah, F. M. V. 2000. Marine algal toxins: origins, health effects, and their increased occurrence. Environmental Health Perspectives, 108(suppl 1), 133–141. DOI: https://doi.org/10.1289/ehp.00108s1133.
Edler, L. & Elbrächter, M. 2010. The Utermöhl method for quantitative phytoplankton analysis. In: Karlson, B., Cusack, C. & Bresnan, E. (eds.), Microscopic and molecular methods for quantitative phytoplankton analysis. (pp. 13–20). Unesco. Harmful algae in a Brazilian estuary Ocean and Coastal Research 2024, v72(suppl 1):e24008 19 Mafra et al.
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(4), 283–299. DOI: https://doi.org/10.1016/s1568-9883(03)00047-7.
Fernandes, L. F., Cavalcante, K. P., Proença, L. A. D. O. & Schramm, M. A. 2013. Blooms of Pseudo-nitzschia pseudodelicatissima and P. calliantha, and associated domoic acid accumulation in shellfish from the South Brazilian coast. Diatom Research, 28(4), 381–393.
DOI: https://doi.org/10.1080/0269249x.2013.821424.
Futigami, L. S., Dutra, M. O. & Verruck, S. 2021. Ocorrência de ficotoxinas diarreicas em ostras e mexilhões cultivados entre 2019 e 2020 em Governador Celso Ramos, SC. Revista Brasileira de Agrotecnologia, 11(2), 363–369. DOI: https://doi.org/10.18378/rebagro.
v12i2.8735.
Glibert, P. M. 2020. Harmful algae at the complex nexus of eutrophication and climate change. Harmful Algae, 91, 101583. DOI: https://doi.org/10.1016/j.hal.2019.03.001.
Glibert, P. M. 2019. Phytoplankton in the aqueous ecological theater: Changing conditions, biodiversity, and evolving ecological concepts. Journal of Marine Research, 77(5).
Gobler, C. J. 2020. Climate Change and Harmful Algal Blooms: Insights and perspective. Harmful Algae, 91, 101731. DOI: https://doi.org/10.1016/j.hal.2019.101731.
Hallegraeff, G. M., Anderson, D. M., Belin, C., Bottein, M.-Y. D., Bresnan, E., Chinain, M., Enevoldsen, H., Iwataki, M., Karlson, B., McKenzie, C. H., Sunesen, I., Pitcher, G. C., Provoost, P., Richardson, A., Schweibold, L., Tester, P. A., Trainer, V. L., Yñiguez, A. T. & Zingone, A. 2021. Perceived global increase in algal blooms is attributable to intensified monitoring and emerging bloom impacts. Communications Earth & Environment, 2(1). DOI: https://doi.org/10.1038/s43247-021-00178-8.
Hallegraeff, G. M., Anderson, D. M. & Cembella, A. D. (eds.). 2003. Manual on harmful marine microalgae. Advances in Botanical Research. Paris: Unesco. DOI: https://doi.org/10.1016/b978-0-12-391499-6.00008-6.
Khanaychenko, A. N., Telesh, I. V. & Skarlato, S. O. 2019. Bloom-forming potentially toxic dinoflagellates Prorocentrum cordatum in marine plankton food webs. Protistology, 12(3), 95–125. DOI: https://doi.org/10.21685/1680-0826-2019-13-3-1.
Lana, P. C., Marone, E., Lopes, R. M. & Machado, E. C. 2001. The Subtropical Estuarine Complex of Paranaguá Bay, Brazil. In: Seeliger, U. & Kjerfve, B. (eds.), Coastal Marine Ecosystems of Latin America. Ecological Studies (Vol. 144, pp. 131–145). Berlin: Springer. DOI: https://
doi.org/10.1007/978-3-662-04482-7_11.
Lassus, P., Chomérat, N., Hess, P. & Nézan, E. 2016. Toxic and harmful microalgae of the World Ocean. Paris: Unesco. Leem, C. S. & Dornfeld, D. A. 1996. Design and implementation of sensor-based tool-wear monitoring systems. Mechanical Systems and Signal Processing, 10(4), 439–458. DOI: https://doi.org/10.1006/mssp.1996.0031.
Lopes, R. M., Vale, R. & Brandini, F. P. 1998. Composição, abundância e distribuição espacial do zooplâncton no complexo estuarino de Paranaguá durante o inverno de 1993 e o verão de 1994. Revista Brasileira de Oceanografia, 46(2), 195–211. DOI: https://doi.org/10.1590/s1413-77391998000200008.
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.
Mafra, L. L. Jr., Fernandes, L. F. & Proença, L. A. O. 2006. Harmful algae and toxis in paranaguá bay, Brazil: bases for monitoring. Brazilian Journal of Oceanography, 54(2–3), 107–121. DOI: https://doi.org/10.1590/s1679-87592006000200002.
Mafra, L. L. Jr., Nagai, S., Uchida, H., Tavares, C. P. S., Escobar, B. P. & Suzuki, T. 2016. Harmful effects of Dinophysis to the ciliate Mesodinium rubrum: Implications for prey capture. Harmful Algae, 59, 82–90. DOI: https://doi.org/10.1016/j.hal.2016.09.009.
Mafra, L. L. Jr., Nolli, P. K. W., Mota, L. E., Domit, C., Soeth, M., Luz, L. F. G., Sobrinho, B. F., Leal, J. G. & Domenico, M. D. 2019. Multi-species okadaic acid contamination and human poisoning during a massive bloom of Dinophysis acuminata complex in southern Brazil. Harmful Algae, 89, 101662. DOI: https://doi.org/10.1016/j.hal.2019.101662.
Mafra, L. L. Jr., Ribas, T., Alves, T. P., Proença, L. A. O., Schramm, M. A., Uchida, H. & Suzuki, T. 2015. Differential okadaic acid accumulation and detoxification by oysters and mussels during natural and simulated Dinophysis blooms. Fisheries Science, 81(4), 749–762. DOI: https://doi.org/10.1007/s12562-015-0882-7.
Mafra, L. L. Jr., Tavares, C. & Schramm, M. A. 2014. Diarrheic toxins in field-sampled and cultivated Dinophysis spp. cells from southern Brazil. Journal of Applied Phycology, 26(4), 1727–1739. DOI: https://doi.org/10.1007/s10811-013-0219-9.
Mafra, L. L. Jr., Lopes, D., Bonilauri, V., Uchida, H. & Suzuki, T. 2015. Persistent Contamination of Octopuses and Mussels with Lipophilic Shellfish Toxins during Spring Dinophysis Blooms in a Subtropical Estuary. Marine Drugs, 13(6), 3920–3935. DOI: https://doi.org/10.3390/
md13063920.
Marone, E., Machado, E. C., Lopes, R. M. & Silva, E. T. 2005. Land-Ocean Fluxes in the Paranaguá Bay Estuarine System, Southern Brazil. Brazilian Journal of Oceanography, 53(3–4), 169–181.
Menezes, M., Branco, S., Miotto, M. C. & Alves-de-Souza, C. 2018. The Genus Alexandrium (Dinophyceae, Dinophyta) in Brazilian Coastal Waters. Frontiers in Marine Science, 5. DOI: https://doi.org/10.3389/fmars.2018.00421.
Moreira-González, A. R., Brustolin, M. C. & Mafra, L. L. Jr. 2020. Composition and abundance of benthic microalgae from the Estuarine Complex of Paranaguá Bay (southern Brazil) with special emphasis on toxic species. Ocean and Coastal Research, 68, e20276. DOI: https://doi.org/10.1590/s2675-28242020068276.
Harmful algae in a Brazilian estuary Ocean and Coastal Research 2024, v72(suppl 1):e24008 20 Mafra et al. Moreira-González, Angel R., Comas-González, A., Valle-Pombrol, A., Seisdedo-Losa, M., HernándezLeyva, O., Fernandes, L. F., Chomérat, N., Bilien, G., Hervé, F., Rovillon, G. A., Hess, P., AlonsoHernández, C. M. & Mafra, L. L. 2021. Summer bloom of Vulcanodinium rugosum in Cienfuegos Bay (Cuba)
associated to dermatitis in swimmers. Science of The Total Environment, 757, 143782. DOI: https://doi.org/10.1016/j.scitotenv.2020.143782.
Moreira-González, A. R., Fernandes, L. F., Uchida, H., Uesugi, A., Suzuki, T., Chomérat, N., Bilien, G. & Mafra, L. L. Jr. 2018. Variations in morphology, growth, and toxicity among strains of the Prorocentrum lima species complex isolated from Cuba and Brazil. Journal of
Applied Phycology, 31(1), 519–532. DOI: https://doi.org/10.1007/s10811-018-1587-y.
Moreira-González, A. R., Fernandes, L. F., Uchida, H., Uesugi, A., Suzuki, T., Chomérat, N., Bilien, G., Pereira, T. A. & Mafra, L. L. Jr. 2019. Morphology, growth, toxin production, and toxicity of cultured marine benthic dinoflagellates from Brazil and Cuba. Journal of Applied Phycology, 31(6), 3699–3719. DOI: https://doi.org/10.1007/s10811-019-01855-0.
Moreira-González, A. R., Rosa, K. M. S. & Mafra, L. L. Jr. 2021. Prevalence of okadaic acid in benthic organisms associated Prorocentrum lima complex in a sub-tropical estuary. Food Additives & Contaminants: Part A, 39(2), 382–396. DOI: https://doi.org/10.1080/19440049.2021.1992512.
Moreira-González, A. R., Domit, C., Rosa, K. M. S. & Mafra, L. L. Jr. 2023. Occurrence of potentially toxic microalgae and diarrhetic shellfish toxins in the digestive tracts of green sea turtles (Chelonia mydas) from southern Brazil. Harmful Algae, 128, 102498. DOI: https://doi.org/10.1016/j.hal.2023.102498.
Negrello-Filho, O. A., Ugaz-Codina, J. C., Oliveira, L. H. S., Souza, M. C. & Angulo, R. J. 2018. Subtidal soft sediments of the Paranaguá Bay inlet: mapping habitats and species distribution at a landscape scale. Brazilian Journal of Oceanography, 66(3), 255–266. DOI: https://
doi.org/10.1590/s1679-875920180192406603.
Noernberg, M. A., Lautert, L. F. C., Araújo, A. D., Marone, E., Angelotti, R., Netto, J. P. B. & Krug, L. A. 2006. Remote Sensing and GIS Integration for Modelling the Paranaguá Estuarine Complex -Brazil. Journal of Coastal Research, 39, 1627–1631.
Nolli, P. K. W. 2018. Aspectos sanitários de ostras cultivadas no complexo estuarino de Paranaguá: Vibrio parahaemolyticus, Perkinsus sp. e ficotoxinas (Master's thesis). Universidade Federal do Paraná, Pontal do Paraná. Accessed on May 26 2023: https://docplayer.com.br/214704892-Universidade-federaldo-parana-paula-karine-wormsbecher-nolli.html.
Parizzi, R. A., Machado, E. D. C., Tavares, C. P. D. S., Fernandes, L. F., Camargo, M. G. D. & Mafra, L. L. Jr. 2016. Primary productivity and phytoplankton dynamics in a subtropical estuary: a multiple timescale approach. Scientia Marina, 80(3), 291–303. DOI: https://doi.org/10.3989/scimar.04358.26a.
Passos, A. C., Contente, R. F., Araujo, C. C. V., Daros, F. A. L. M., Spach, H. L., Abilhôa, V. & Fávaro, L. F. 2012. Fishes of Paranaguá Estuarine Complex, South West Atlantic. Biota Neotropica, 12(3), 226–238. DOI: https://doi.org/10.1590/s1676-06032012000300022.
Pellizzari, G. 2008. Estudo analítico e descritivo dos parâmetros geográficos, demográficos e sanitários do Rio Itiberê em Paranaguá, PR (Bachelor's thesis). Universidade Federal do Paraná, Pontal do Sul. Accessed on May 26 2023: https://acervodigital.ufpr.br/handle/1884/76757.
Procopiak, L. K., Fernandes, L. F. & Moreira-Filho, H. 2006. Diatomáceas (Bacillariophyta) marinhas e estuarinas do Paraná, Sul do Brasil: lista de espécies com ênfase em espécies nocivas. Biota Neotropica, 6(3). DOI: https://doi.org/10.1590/s1676-06032006000300013.
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. Proença, L. A. O., Schramm, M. A., Alves, T. P. & Piola, A. R. 2017. The extraordinary 2016 autumn DSP outbreak in Santa Catarina, SouthernBrazil, explained by largescale oceanographic processes. In: Proceedings of the 17th International Conference on Harmful Algae. Florianópolis: ISSHA. Accessed: https://www.divaportal.org/smash/get/diva2:1176988/FULLTEXT01. pdf#page=42.
Proença, L. A. O., Schramm, M. A., Tamanaha, M. S. & Alves, T. P. 2007. Diarrhoetic shellfish poisoning (DSP) outbreak in Subtropical Southwest Atlantic. Harmful Algae News, 33, 19–20. R Studio Team. 2022. RStudio: Integrated Development for R. RStudio, PBC. Accessed on April 14 2023: http://www.rstudio.com/
Schlitzer, R. 2021. Ocean Data View. Accessed on April 13 2023: https://odv.awi.de/Schramm, M. A., Alves, T. P., Honorato, M. C. & Proença, L. A. O. 2010. Primeira detecção de ficotoxinas lipofílicas em mexilhões da Armação do Itapocorói em Santa Catarina através de LC-MS/MS. In: Livro de Resumos do XIII Congresso Brasileiro de Ficologia (p. 381). Paraty: SBFIC. Sobrinho, B. F. 2020. Dinâmica da comunidade planctônica durante uma floração do dinoflagelado toxigênico do complexo Dinophysis acuminata Claparéde & Lachmann, 1859 no sul do Brasil (Master's thesis). Universidade Federal do Paraná, Curitiba.
Tavares, J. F., Proença, L. A. O. & Odebrecht, C. 2009. Assessing the harmful microalgae occurrence and temporal variation in a coastal aquaculture area, southern Brazil. Atlântica, 31(2), 129–144. DOI: https://doi.org/10.5088/atl.2009.31.2.129.
Tibiriçá, C. E. J. A., Fernandes, L. F. & Mafra, L. L. Jr. 2015. Seasonal and spatial patterns of toxigenic species of dinophysis and pseudo-nitzschia in a subtropical brazilian estuary. Brazilian Journal of Oceanography, 63(1), 17–32. DOI: https://doi.org/10.1590/s1679-
Harmful algae in a Brazilian estuary Ocean and Coastal Research 2024, v72(suppl 1):e24008 21 Mafra et al.
Tibiriçá, C. E. J. A., Sibat, M., Fernandes, L. F., Bilien, G., Chomérat, N., Hess, P. & Mafra, L. L. Jr. 2020. Diversity and Toxicity of the Genus Coolia Meunier in Brazil, and Detection of 44-methyl Gambierone in Coolia tropicalis. Toxins, 12(5), 327. DOI: https://doi.org/10.3390/toxins12050327.
Tibiriçá, C., Leite, I., Batista, T., Fernandes, L., Chomérat, N., Herve, F., Hess, P. & Mafra, L. L. Jr. 2019. Ostreopsis cf. ovata Bloom in Currais, Brazil: Phylogeny, Toxin Profile and Contamination of Mussels and Marine Plastic Litter. Toxins, 11(8), 446. DOI: https://doi.org/10.3390/
toxins11080446.
Tranker, V. 2014. Abundância de fitoplâncton e ocorrência de espécies nocivas em uma área destinada à maricultura na Baía de Paranaguá, Paraná. (thesis). Univesidade Federal do Paraná, Pontal do Paraná. Vianna, L. F. N., Souza, R. V., Schramm, M. A. & Alves,
T. P. 2023. Using climate reanalysis and remote sensing-derived data to create the basis for predicting the occurrence of algal blooms, harmful algal blooms and toxic events in Santa Catarina, Brazil. Science of The Total Environment, 880, 163086. DOI: https://doi.org/10.1016/j.scitotenv.2023.163086.
Downloads
Published
Issue
Section
License
Copyright (c) 2024 Ocean and Coastal Research
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
Ocean and Coastal Research is an open-access journal available through SciELO (Scientific Electronic Library Online).
Ocean and Coastal Research journal title abbreviation is Ocean Coast. Res. and should be used in footnotes, references, and bibliographic entries.
All Ocean and Coastal Research scientific articles are freely available without charge to the user or institution. In accordance with the BOAI definition of open access, all contents are available to readers free of charge. Users may read, download, copy, and link to the full texts of the articles. They may be used for any lawful purpose without prior authorization from the publisher or the author, as long as proper credit is given to the original publication.
All Ocean and Coastal Research published scientific articles receive an individual Digital Object Identifier (DOI) persistent digital document identification.
All the content of the journal, except where otherwise noted, is licensed under a Creative Commons License type BY. Authors retain the copyright and full publishing rights without restrictions.
More information on intellectual property can be found here and on Scielo's Open Acess Statement.
Ocean and Coastal Research is listed in Publons and reviewers and editors can add their verified peer review and editing history to their Publons profile.
Ocean and Coastal Research is indexed in the Directory of Open Access Journals (DOAJ) and complies with principles of transparency and best practice for scholarly publications.
Ocean and Coastal Research is committed to the best standards in open-access publishing by adopting ethical and quality standards throughout the publishing process - from initial manuscript submission to the final article publication. This ensures authors that their work will have visibility, accessibility, reputation, usage, and impact in a sustainable model of scholarly publishing.
