Abstract

Despite its small area, Araçá Bay (AB) holds cultural, historical, and economic value and displays great benthic biodiversity. Thus, it is crucial to monitor its environmental health, including knowing the main groups of phytoplankton and their temporal variability. The shallow waters of Araçá Bay are continuously modified by the complex hydrography of the adjacent São Sebastião channel (SSC), challenging standard experimental designs for phytoplankton collection. Here we report changes in phytoplankton composition at intervals of five to six weeks from September 2013 to August 2014 in both Araçá Bay and SSC. Samples were collected twice daily for three consecutive days to increase taxonomic resolution. Our goal was to provide an inventory of species occurrences to aid future public policies and environmental management of the area. Analyses revealed high species richness and 166 different phytoplankton taxa. Diatoms and dinoflagellates were always numerically dominant, but taxa occurrence changed markedly. Diatoms of the genera Pseudo-nitzschia were abundant during spring and summer concurrently to signatures of South Atlantic Central Water in the SSC, while Thalassiosira occurred when waters displayed relatively lower salinity. The inventory demonstrated several potentially harmful species of microalgae and cyanobacteria, strongly suggesting investments in monitoring programs in this area that currently experience an increase in population.

Keywords
Biodiversity; Pseudo-nitzschia; Thalassiosira; São Paulo coast; coastal marine environments

Resumo

Apesar de sua pequena área, a baía do Araçá (AB) possui grande valor cultural, histórico e econômico, e biodiversidade bentônica. Assim, é fundamental monitorar sua saúde ambiental, que inclui conhecer os principais grupos de fitoplâncton e sua variabilidade temporal. As águas rasas da baía do Araçá são continuamente modificadas pela hidrografia complexa do canal de São Sebastião (SSC), desafiando desenhos experimentais convencionais para coleta de fitoplâncton. Aqui relatamos mudanças sazonais na composição do fitoplâncton, em intervalos de 4 a 6 semanas, de setembro de 2013 a agosto de 2014 na baía do Araçá e no SSC, sendo coletadas duas vezes ao dia por três dias consecutivos em cada campanha de amostragem para aumentar a resolução taxonômica. Nosso objetivo foi fornecer um inventário de ocorrência de espécies para auxiliar futuras políticas públicas e gestão ambiental na área. As análises revelaram alta riqueza de espécies e 166 táxons fitoplanctônicos diferentes. Diatomáceas e dinoflagelados foram numericamente dominantes, mas a ocorrência de táxons mudou acentuadamente entre observações. As diatomáceas do gênero Pseudo-nitzschia foram abundantes durante a primavera e o verão concomitantemente às assinaturas da Água Central do Atlântico Sul no CSS, enquanto Thalassiosira ocorreu durante períodos de salinidade relativamente mais baixa. O inventário demonstrou várias espécies potencialmente nocivas de microalgas e cianobactérias, sugerindo fortemente investimentos para programas de monitoramento nesta área que vem registrando aumento populacional contínuo.

Palavras-chave
Biodiversidade; Pseudo-nitzschia; Thalassiosira; litoral paulista; ambientes marinhos

Introduction

Phytoplankton communities vary according to the physicochemical conditions of the water (Margalef 1967MARGALEF, R. 1967. Ritmos, fluctuaciones y sucesión. In: Ecología Marina. Ginés, H., Margalef, R. (eds.). Fundación La Salle de Ciencias Naturales. Caracas. pp. 454–492.), but knowledge on the specific composition of these communities remain challenging (Basterretxea et al. 2020BASTERRETXEA, G., FONT-MUÑOZ, J.S. & TUVAL, I. 2020. Phytoplankton Orientation in a Turbulent Ocean: A Microscale Perspective. Frontiers in Marine Science, 7(March), 1–8. https://doi.org/10.3389/fmars.2020.00185
https://doi.org/10.3389/fmars.2020.00185... ). The occurrence and the dominance of a given phytoplankton species reflect its adaptation to the environment (e.g., Anderson et al. 2002ANDERSON, D.M., GLIBERT, P.M. & BURKHOLDER, J.M. 2002. Harmful algal blooms and eutrophication: Nutrient sources, composition, and consequences. Estuaries, 25(4), 704–726. https://doi.org/10.1007/BF02804901
https://doi.org/10.1007/BF02804901... , Kremer et al. 2017KREMER, C.T., THOMAS, M.K. & LITCHMAN, E. 2017. Temperature- and size-scaling of phytoplankton population growth rates: Reconciling the Eppley curve and the metabolic theory of ecology. Limnology and Oceanography, 62(4), 1658–1670. https://doi.org/10.1002/lno.10523
https://doi.org/10.1002/lno.10523... , Moser et al. 2017MOSER, G.A.O., PIEDRAS, F.R., OAQUIM, A.B.J., SOUZA, D.S., LELES, S.G., DE LIMA, D.T., RAMOS, A.B.A., FARIAS, C. DE O. & FERNANDES, A.M. 2017. Tidal effects on phytoplankton assemblages in a near-pristine estuary: a trait-based approach for the case of a shallow tropical ecosystem in Brazil. Marine Ecology, 38(4), 1–18. https://doi.org/10.1111/maec.12450
https://doi.org/10.1111/maec.12450... , Ryabov et al. 2021RYABOV, A., KERIMOGLU, O., LITCHMAN, E., OLENINA, I., ROSELLI, L., BASSET, A., STANCA, E. & BLASIUS, B. 2021. Shape matters: the relationship between cell geometry and diversity in phytoplankton. Ecology Letters, 24(4), 847–861. https://doi.org/10.1111/ele.13680
https://doi.org/10.1111/ele.13680... ). Hence some large-scale generalizations about the taxonomic variability and abundance of phytoplankton can be made in the ocean. Nearshore, however, environmental conditions vary over time scales of hours to days, and the same is true for phytoplankton diversity, for which observations require intense sampling effort. The quantification of species in the world ocean (Sournia, 1991SOURNIA, A., CHRETIENNOT-DINET, M.J. & RICARD, M. 1991. Marine phytoplankton: how many species in the world? J. Plankton Res. 13(5):1093–1099.) is a laborious work. Although new instruments and techniques (e.g. Sosik & Olson, 2007SOSIK, H.M., OLSON, R.J. 2007. Automated taxonomic classification of phytoplankton sampled with image-in-flow cytometry. Limnol. & Oceanogr.: Methods, 5, 204–216.) are now available, microscopy analyses remain invaluable for their validation. The availability of phytoplankton species inventories is essential at urbanized coastal sites as they subsidize environmental management actions.

The São Sebastião channel (SSC), located in the north portion of the São Paulo state coast, between the municipalities of São Sebastião and Ilhabela, is partially inserted in the Marine Environmental Protection Area of the North Coast of the State of São Paulo. In the central portion of the channel, a shallow tidal plain (average depth of 1.5 m) limited by rocky flanks (Amaral et al. 2010AMARAL, A.C.Z., MIGOTTO, A.E., TURRA, A. & SCHAEFFER-NOVELLI, Y. 2010. Araçá : biodiversidade, impactos e ameaças Porque Conservar o Araçá para as Futuras Gerações? Histórico de Alterações e Sobrevivência do Araçá. Biota Neotropica, 10(1), 219–230.) is known as Araçá Bay. The bay has an extensive intertidal region, which can be fully exposed to the air and exceeds 300 m in length during low spring tides (Amaral et al. 2018AMARAL, A.C.Z., TURRA, A., CIOTTI, A.M., WONGTSCHOWSKI, C. & SCHAEFFER-NOVELLI, Y. (n.d.) 2018. métodos de estudo em ecossistemas costeiros : biodiversidade e Projeto Biota-Araçá (Amaral (ed.)). ISBN (e-Book): 978-85-85783-81-5), with a large area of the plain being immersed and submerged within the same tidal cycle (Siegle et al. 2018SIEGLE, E., DOTTORI, M. & CAPELARI VILLAMARIN, B. 2018. Hydrodynamics of a subtropical tidal flat: Araçá Bay, Brazil. Ocean & Coastal Management. ). Araçá Bay is of esteemed value to the local population because, in addition to harboring high biological diversity (Amaral et al. 2010AMARAL, A.C.Z., MIGOTTO, A.E., TURRA, A. & SCHAEFFER-NOVELLI, Y. 2010. Araçá : biodiversidade, impactos e ameaças Porque Conservar o Araçá para as Futuras Gerações? Histórico de Alterações e Sobrevivência do Araçá. Biota Neotropica, 10(1), 219–230.), it is a stronghold of artisanal fishers who traditionally use small vessels for fishing or leisure (Amaral et al. 2018AMARAL, A.C.Z., TURRA, A., CIOTTI, A.M., WONGTSCHOWSKI, C. & SCHAEFFER-NOVELLI, Y. (n.d.) 2018. métodos de estudo em ecossistemas costeiros : biodiversidade e Projeto Biota-Araçá (Amaral (ed.)). ISBN (e-Book): 978-85-85783-81-5). In the past years, the north coast of São Paulo experienced increasing population growth and environmental impacts (Xavier et al. 2016XAVIER, L.Y., STORI, F.T. & TURRA, A. 2016. Desvendando os oceanos: Um olhar sobre a Baía do Araçá. http://www.io.usp.br/index.php/arquivos/send/14-61-publicacoes/4212-desvendando-os-oceanos-um-olhar-sobre-a-baia-do-araca
http://www.io.usp.br/index.php/arquivos/... ), including the discharge of untreated sewage. Indeed, there is evidence that the interaction of the São Sebastião channel with the continent plays an important role in the exchange of nutrients (Gubitoso et al. 2008GUBITOSO, S., DULEBA, W., TEODORO, A.C., PRADA, S.M., ROCHA, M.M., LAMPARELLI, C.C., BEVILACQUA, J.E. & MOURA, D.O. 2008. Estudo geoambiental da região circunjacente ao emissário submarino de esgoto do Araçá, São Sebastião (SP). Revista Brasileira de Geociências, v.33, n.3, p.467–475. ) on primary productivity (Regaudie et al. 2017REGAUDIE-DE-GIOUX, A., CASTAGNA, A., FERREIRA, A., ABBRECHT, M., BRAGA, E.S. & CIOTTI, A.M. 2017. Influence of mixed upwelled waters on metabolic balance in a subtropical coastal ecosystem: São Sebastião Channel, southern Brazil. MARINE ECOLOGY PROGRESS SERIES, v. 573.).

Available phytoplankton studies in SSC waters consisted of surveys reporting changes in biomass (i.e., chlorophyll concentration) or relative abundance of major taxonomic groups and their relationships with nutrient concentrations (Muller-Melchers 1955MÜLLER-MELCHERS, F.C. 1955. Las diatomeas del plancton marino de las costas del Brasil. Bol. Inst. Oceanogr. 6(1–2):93–141., Gianesella et al. 1999GIANESELLA, S.M.F., KUTNER, M.B.B., SALDANHA-CORRÊA, F.M.P. & POMPEU, M. 1999. Assessment of plankton community and environmental conditions in São Sebastião Channel prior to the construction of a produced water outfall. Rev. Bras. Oceanogr. 47(1):29–46, Saldanha-Corrêa & Gianesella 2003SALDANHA-CORREA, F.M.P. & GIANESELLA, S.M.F. 2003. Avaliação do fitoplâncton nas águas adjacentes ao difusor do emissário de esgotos do Saco da Capela, Ilha Bela (SP), em janeiro e julho de 2002. In Anais III Congr. Bras. Pesq. Amb. CR-Rom.). A review of phytoplankton studies carried out along the São Paulo coast provided a comprehensive inventory of the species present from 1913 to 2006 (Villac et al. 2008VILLAC, M.C., NORONHA, V.A. DE P.C. & PINTO, T.DE O. 2008. The phytoplankton biodiversity of the coast of the state of São Paulo, Brazil. Biota Neotrop. 8(3): 151–173.). However, no further diversity studies are available. More recent analyses of changes in chlorophyll concentration fractionated by size classes (Giannini & Ciotti 2016GIANNINI, M.F.C. & CIOTTI, A.M. 2016 Parameterization of natural phytoplankton photo-physiology: Effects of cell size and nutrient concentration. Limnology and Oceanography, v. 61, p. 1495–1512.) and main taxonomic groups (Ciotti et al. 2018aCIOTTI, Á.M., FERREIRA, A. & GIANNINI, M.F.C. 2018 a. Seasonal and event-driven changes in the phytoplankton communities in the Araçá Bay and adjacent waters. Ocean and Coastal Management, 164 (August 2017), 14–31. https://doi.org/10.1016/j.ocecoaman.2018.03.024
https://doi.org/10.1016/j.ocecoaman.2018... ) derived from efforts during the Araçá Thematic FAPESP project (https://biota-araca.org/index.html), conducted from September 2013 to August 2014 and showed the importance of diatoms when phytoplankton biomass increased. The present study is also derived from the Araçá Project phytoplankton dataset (Tocci 2016TOCCI, B.R.C. 2016. Ocorrência e coexistência de cianobactérias diazotróficas no Canal de São Sebastião-SP com o aumento da pluviosidade. Dissertação (Oceanografia Biológica) - Instituto Oceanográfico, Universidade de São Paulo, São Paulo.) and focuses on detailed taxonomic descriptions of phytoplankton in Araçá Bay and SSC, using light microscopy. The main objective is to update the phytoplankton taxa for this region, report their relative occurrence frequencies, and describe differences between the species found in Araçá Bay and the adjacent waters in the São Sebastião channel.

Materials and Methods

The phytoplankton checklist is composed of samples derived from three oceanographic stations located in the interior of Araçá Bay (AB) and a single station located in the southern portion of the São Sebastião Channel (SSC) at the 15 m isobath (Figure 1). Nine surveys occurred between September 2013 and August 2014 every five to six weeks, in the morning and afternoon of three consecutive days (Ciotti et al. 2018bCIOTTI, A., MARCOLIN, C.R., SIGNORI, C.N., LOPES, R.M., PELLIZARI, V.H. 2018 b. Sistema Planctônico. In: AMARAL, A.C.Z., TURRA, A., CIOTTI, A.M., WONGTSCHOWSKI, C., SCHAEFFER-NOVELLI, Y. (Org.). Métodos de estudo em ecossistemas costeiros: biodiversidade e funcionamento. Projeto Biota-Araçá.. 1ed. Campinas: Biblioteca UNICAMP, p. 42–60.) to increase the probability of observing the variable hydrodynamics of SSC and rarer phytoplankton taxa. We used a Sontek Castway CTD to vertically profile the temperature and salinity at each station and a 5 L Van Dorn bottle to collect water for analyses of inorganic nutrients, chlorophyll-a, and phytoplankton cell enumeration. Three water samples were combined to represent AB and SSC to increase the representativeness of the occurring taxa analysis. AB samples refer to the combination of three independent stations located at isobaths between 1.5 and 2 m, while SSC refers to three successive deployments of the Van Dorn bottle (Tocci, 2016TOCCI, B.R.C. 2016. Ocorrência e coexistência de cianobactérias diazotróficas no Canal de São Sebastião-SP com o aumento da pluviosidade. Dissertação (Oceanografia Biológica) - Instituto Oceanográfico, Universidade de São Paulo, São Paulo.). The composite samples were further concentrated (2 L to about 100 mL) by reverse filtration with a 5 μm nylon mesh and preserved with formaldehyde neutralized in hexamethylenetetramine (0.4 %). Climatological data on precipitation rates were consulted on the CPTEC-INPE website (http://clima1.cptec.inpe.br/).

Figure 1.
Location of the sampling sites at Araçá Bay (AB) and São Sebastião Channel (SSC) near the oceanographic buoy of SIMCosta Project.

Cell enumeration and taxonomic analysis used Üthermol sedimentation chambers of 5 mL or 10 mL and an inverted optical microscope ZEISS-Axio® Observer D1 equipped with phase contrast and differential interference contrast (DIC). Only cells with maximum linear dimension MLD > 5 μm were counted, and identifications reached the lowest possible taxonomic level (genus and species) only for cells with MLD > 10 μm, with the help of specialized literature (e.g., Tomas 1997TOMAS, C.R. (ed.) 1997. Identifying Marine Phytoplankton. Eds. Academic Press, New York. 858 p., Tenenbaum et al. 2004TENENBAUM, D.R., VILLAC, M.C., VIANA, S.C., MATOS, M.C. de F.G., HATHERLY, M.M.F., LIMA, I.V. & MENEZES, M. 2004. Phytoplankton Identification Atlas- Sepetiba Bay, Brazil. 1. ed. Londres, Grã Bretanha: IOC., Tenenbaum et al. 2006TENENBAUM, D.R. 2006. Dinoflagelados e tintinídeos da região central da Zona Econômica Exclusiva brasileira: guia de identificação. Rio de Janeiro: Museu Nacional., Garcia & Odebrecht 2009GARCIA, M. & ODEBRECHT, C. 2009. Morphology and ecology of Thalassiosira Cleve (Bacillariophyta) species rarely recorded in Brazilian coastal waters. Brazilian Journal of Biology, v. 69., Haraguchi & Odebrecht 2010HARAGUCHI, L. & ODEBRECHT, C. 2010. Dinophysiales (Dinophyceae) no extremo Sul do Brasil (inverno de 2005, verão de 2007). Biota Neotropica (Edição em Português. Online), v. 10, p. 101–114.). Names and synonyms were checked and updated by queries of the Algaebase database (Guiry & Guiry 2021GUIRY, M.D. & GUIRY, G.M. 2021. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. https://www.algaebase.org; searched on 17 June 2021
https://www.algaebase.org... ), and the diatom classification followed the work by Medlin & Kaczmarska (2004)MEDLIN, L.K. & KACZMARSKA, I. 2004. Evolution of the diatoms: V. Morphological and cytological support for the major clades and a taxonomic revision. Phycologia, 43, 245–270.. The records for Pseudo-nitzschia followed the nomenclature of Hasle (1965)HASLE, G.R. 1965. Nitzschia and Fragilariopsis species studied in the light and electron microscope. II. The group Pseudo-nitzschia. Skr. Nor. Vidensk. Akad. Oslo. I. Mat. Naturvidensk. Kl. 18:1–49. that divided the colony-forming species of the genus Nitzschia into two complexes: the “delicatissima” – for cells with widths equal to or smaller than 3 μm, and the «seriata» for cells wider than 3 μm. These two complexes were later combined and updated to the genera Pseudo-nitzshia (Hasle 1994HASLE, G.R. 1994. Pseudo-nitzschia as a genus distinct from Nitzshia (Bacillariophyceae). J. Phycol. 30(6):1036–1039.).

The relative occurrence frequencies of taxa were calculated based on the method described by Matteucci & Colma (1982)MATTEUCCI, S.D. & COLMA, A. 1982. Metodologia para el estudio de la vegetación. Washington: The General Secretarial of The Organization of American States; (Série Biologia – Monografia, n. 22)., which considers the overall number of occurrences of a taxon (65 samples for AB and 65 for SSC samples), following the categories: very frequent (VF) > 70%; frequent (F) ≤ 70% – >40%; infrequent (I) ≤ 40% – > 10%; and sporadic (S) <10%.

Results

Seawater temperature varied from 19.4 to 29.4° C in Araçá Bay (AB) and from 16.4 to 29.7°C in São Sebastião Channel (SSC), while salinity ranged from 30.8 to 36.6 in AB and from 30.9 to 35.7 in SSC (Table 1). A mixture of South Atlantic Central Water (SACW, thermohaline index 20.0 °C; 36.36, according to Miranda, 1985) and Coastal Water (CW, salinity below 35 and temperature higher than 20.0 °C) was observed during December 2013 in both AB and SSC. The CW was a mixture of oceanic water masses and continental outflows and dominated SSC in all samplings with temporally variable thermohaline characteristics (see Ciotti et al. 2018aCIOTTI, Á.M., FERREIRA, A. & GIANNINI, M.F.C. 2018 a. Seasonal and event-driven changes in the phytoplankton communities in the Araçá Bay and adjacent waters. Ocean and Coastal Management, 164 (August 2017), 14–31. https://doi.org/10.1016/j.ocecoaman.2018.03.024
https://doi.org/10.1016/j.ocecoaman.2018... same dataset). Maximum concentrations of ammonia, nitrate + nitrite, phosphate, silicate, and chlorophyll, were generally observed at AB, but their average values were similar at both sampling sites (Table 1). During all surveys, we observed smaller volumes of accumulated precipitation compared to the regional climatology.

Phytoplankton densities were as high as 10⁶ cel L^–1 (Table 2). Despite the significance of picoplankton and nanoplankton for Brazilian coastal waters, it is worth mentioning that this inventory covered organisms greater than 5 μm. Diatoms were the predominant taxonomic group at both AB and SSC, with pennate diatoms representing 67% of phytoplankton species in the latter during the sampling period. Comparatively larger abundances of flagellates and armored dinoflagellates were noticeable at AB and SSC, respectively (Table 2).

The diatom genus Thalassiosira predominated during fall and winter (Figure 2), while Pseudo-nitzschia spp. prevailed during October and December 2013 (spring events) and January 2014 (summer) (Figure 2), after periods of high precipitation rates and when surface waters were warm and showed high phosphate concentrations. The highest densities of Pseudo-nitzschia spp. in October 2013 (10⁵ 10⁵ cel.L^–1) were concurrent with the presence of cold waters (19.4°C, 35.5) near the SSC bottom (data presented in Ciotti et al. 2018aCIOTTI, Á.M., FERREIRA, A. & GIANNINI, M.F.C. 2018 a. Seasonal and event-driven changes in the phytoplankton communities in the Araçá Bay and adjacent waters. Ocean and Coastal Management, 164 (August 2017), 14–31. https://doi.org/10.1016/j.ocecoaman.2018.03.024
https://doi.org/10.1016/j.ocecoaman.2018... ).

Figure 2.
Variation in the density of the predominant phytoplanktonic taxa collected every 5–6 weeks between September 2013 and August 2014. Taxa: Thalassiosira sp.1 (Tha), Pseudo-nitzschia spp. (Pnitz), Paralia sulcata (Psul), Hemiaulus spp. (Hemi), Chaetoceros spp. (Chae), Leptocylindrus spp. (Lepto), Asterionellopsis glacialis (Aglac), Thalassionema nitzschioides (Tnitzsc), Gymnodiniales (Gymn), Scrippsiella spp. (Scrip), Prorocentrum spp. (Proro), Trichodesmium spp. (Tricho) and Richelia intracellularis (Riche). São Sebastião Channel (SSC) and Araçá Bay (AB).

A total of 166 taxa were identified, with 86 genera, 129 species, 33 morphotypes, and 4 complexes, distributed in eight classes: Mediophyceae (42), Coscinodiscophyceae (23), Bacillariophyceae (37), Dinophyceae (48), Dictyochophyceae (02), Coccolithophyceae (10) and Cyanophyceae (04) (Figure 3 – frequent taxa). Of these, 148 taxa were in samples from within AB and 155 from SSC. Trichodesmium was frequently observed at AB, with the occurrence of T. erythraeum and T. thiebautii in the form of free trichomes, tufts, and puffs (Figure 3) The cyanobacterium Richelia intracellularis was observed in association with diatoms of the genus Hemiaulus only, for the species H. hauckii, H. sinensis, and H. membranaceus predominantly and with up to 4 trichomes of R. intracellularis (Figura 3).

Figure 3.
Diazotrophic cyanobacteria of the genus Trichodesmium, aggregates in bundles know as “tuffs” (A), in spherical “puffs” (B) and as a single trichome (C). Diatom Hemiaulus membranaceus (D) and diazotrophic cyanobacteria Richelia intracellularis (E) within it. Diatoms Chaetoceros cf. debilis (F), Thalassiosira sp.1 (G), Leptocylindrus danicus (I) and Paralia sulcata (J). Diatoms Thalassionema nitzschioides (H), Pseudo-nitzschia “seriata complex” sp.1 (see methods for definition) (L, M). Armored Dinoflagellate Prorocentrum micans (K). A, B epifluorescence microscopy image at 10x magnification; E epifluorescence microscopy image at 20x magnification; I, L DIC microscopy image at 200x magnification and C, F, G, H, M at 40x magnification; D, K, J phase-contrast microscopy image at 400x magnification. Scale bar: A, B, D, E, F = 50 μm; C, G, H, I, J, K, L = 10 μm; M = 05 μm.

The richness of the classes differed slightly between the two sites, as did the relative frequency of each taxon (Table 3). Diatoms were the most frequent (AB = 68%; SSC = 60%), with the class Mediophyceae having the highest percentage in AB (28%; 41 taxa) and SSC (25%; 39 taxa), with the genus Thalassiosira being very frequent (AB = 100%; SSC = 98%). Although the frequencies of classes Coscinodiscophyceae (AB = 15%; SSC = 14%), Dictyochophyceae (AB = 1%; SSC = 1%), Coccolithophyceae (AB = 4%; SSC = 6%) and Cyanophyceae (AB = 3%; SSC = 3%) did not vary notably between sites, the taxa from these classes displayed infrequent or sporadic occurrences, with the exceptions for the frequent diatom Paralia sulcata and the coccolithophorid of the genus Umbilicosphaera at both sites, Dictyocha fibula at CSS and cyanobacteria of the genus Trichodesmium at AB. The class Dinophyceae (AB = 24%; SSC = 30%) showed a larger percentage contribution and numerical richness at SSC (46 taxa) than at AB (36 taxa), with the species Scrippsiella acuminata showing the highest frequency. The species Cylindrotheca closterium and Thalassionema nitzschioides, of the class Bacillariophyceae (AB = 25%; SSC = 21%), had higher frequencies in AB and the genus Pseudo-nitzschia in both locations (AB = 82%; SSC = 70%).

Overall, our inventory showed that diatoms and dinoflagellates represented together, over 80% of the total (Figure 4), similar to what was presented by Villac et al. (2008)VILLAC, M.C., NORONHA, V.A. DE P.C. & PINTO, T.DE O. 2008. The phytoplankton biodiversity of the coast of the state of São Paulo, Brazil. Biota Neotrop. 8(3): 151–173. for the coast of São Paulo state (diatoms 62%, dinoflagellate 34%).

Figure 4.
Relative contributions of the main taxonomic groups (diatoms, dinoflagellates and others – coccolithophorids, silicoflagellates, cyanobacteria, among others) at different levels: worldwide distribution (Sournia et al. 1991SOURNIA, A., CHRETIENNOT-DINET, M.J. & RICARD, M. 1991. Marine phytoplankton: how many species in the world? J. Plankton Res. 13(5):1093–1099.), data from 1913–2002 for the state of São Paulo (Villac et al. 2008VILLAC, M.C., NORONHA, V.A. DE P.C. & PINTO, T.DE O. 2008. The phytoplankton biodiversity of the coast of the state of São Paulo, Brazil. Biota Neotrop. 8(3): 151–173.), data from 2004–2006 for the state of São Paulo (Villac et al. 2008VILLAC, M.C., NORONHA, V.A. DE P.C. & PINTO, T.DE O. 2008. The phytoplankton biodiversity of the coast of the state of São Paulo, Brazil. Biota Neotrop. 8(3): 151–173.), data from 2013–2014 for Araçá Bay (AB) and sampling site at São Sebastião Channel (CSS). (Figure adapted from Villac et al. 2008VILLAC, M.C., NORONHA, V.A. DE P.C. & PINTO, T.DE O. 2008. The phytoplankton biodiversity of the coast of the state of São Paulo, Brazil. Biota Neotrop. 8(3): 151–173.).

Discussion

Our results are analogous to those presented by Villac et al., (2008)VILLAC, M.C., NORONHA, V.A. DE P.C. & PINTO, T.DE O. 2008. The phytoplankton biodiversity of the coast of the state of São Paulo, Brazil. Biota Neotrop. 8(3): 151–173., who reported 193 distinct taxa over a longer extension of the São Paulo coast (between Cananéia and Ubatuba) from 2004 to 2006. Their inventory included 120 diatoms, 65 dinoflagellates, and 3 silicoflagellates. In the present study, however, we observed larger contributions of the diatom genera Pseudo-nitzschia, Thalassiosira, Chaetoceros, Hemiaulus, Cyclotella, Coscinodiscus, Guinardia, Rhizosolenia, Thalassionema, Cylindrotheca, and Leptocylindrus, and the dinoflagellate genera Prorocentrum, Scrippsiella, Tripos, Gymnodinium, Dinophysis, and Heterocapsa. One addition to Villac et al. (2008)VILLAC, M.C., NORONHA, V.A. DE P.C. & PINTO, T.DE O. 2008. The phytoplankton biodiversity of the coast of the state of São Paulo, Brazil. Biota Neotrop. 8(3): 151–173. inventory was the diazotrophic cyanobacteria Richelia intracellularis (unfrequent taxa), either free or in symbiosis with diatoms at both AB and SSC. Although this result can be partially related to our sampling design, differences in environmental conditions between the two studies cannot be discarded, reinforcing the importance of frequent assessments of phytoplankton genera or species.

The 5 to 6-week interval observations revealed some temporal distinctions in the taxonomic composition of the phytoplankton. For example, the diatom genera Thalassiosira and Pseudo-nitzschia were consistently frequent (Table 3, Figure 2). However, their abundances tended to alternate. In addition, Thalassiosira (class Mediophyceae) was frequent when taxa richness was high, while when Pseudo-nitzschia (class Bacillariophyceae) was predominant, the richness of taxa was low, and their highest abundances occurred synchronically to intrusions of South Atlantic Central Water in SSC.

In temperate marine ecosystems, the succession between dominant phytoplankton taxa tends to be seasonal, leading to blooms (e.g., Cui et al. 2018CUI, L., LU, X., DONG, Y., CEN, J., CAO, R., PAN, L., LU, S. & OU, L. 2018. Relationship between phytoplankton community succession and environmental parameters in Qinhuangdao coastal areas, China: A region with recurrent brown tide outbreaks. Ecotoxicology and Environmental Safety, 159 (February), 85–93. https://doi.org/10.1016/j.ecoenv.2018.04.043
https://doi.org/10.1016/j.ecoenv.2018.04... , Fragoso et al. 2021FRAGOSO, G.M., JOHNSEN, G., CHAUTON, M.S., COTTIER, F. & ELLINGSEN, I. 2021. Phytoplankton community succession and dynamics using optical approaches. Continental Shelf Research, 213(November 2020), 104322. https://doi.org/10.1016/j.csr.2020.104322
https://doi.org/10.1016/j.csr.2020.10432... ). The genus Pseudo-nitzschia, with about 55 species (Guiry & Guiry 2021GUIRY, M.D. & GUIRY, G.M. 2021. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. https://www.algaebase.org; searched on 17 June 2021
https://www.algaebase.org... ), can form blooms in coastal regions globally (e.g., Trainer et al. 2012TRAINER, V.L., BATES, S.S., LUNDHOLM, N., THESSEN, A.E., COCHLAN, W.P., ADAMS, N.G. & TRICK, C.G. 2012. Pseudo-nitzschia physiological ecology, phylogeny, toxicity, monitoring and impacts on ecosystem health. Harmful Algae, 14, 271–300. https://doi.org/10.1016/j.hal.2011.10.025
https://doi.org/10.1016/j.hal.2011.10.02... ), and some species are known to be potentially harmful by producing the neurotoxin domoic acid (Hasle 2002HASLE, G.R. 2002. Are most of the domoic acid producing species of the diatom genus Pseudo-nitzschia cosmopolites? Harmful Algae 1, 137–146.). The genus Thalassiosira contains more than 100 species (Round et al. 1990ROUND, F.E., CRAWFORD, R.M. & MANN, D.G. 1990. The diatoms. Cambridge University Press, Cambridge.), but as for Pseudo-nitzschia and other genera of the class Bacillariophyceae, such as Navicula, Pleurosigma, and Gyrosigma, species-level identification requires scanning electron microscopy.

Our results suggest not only the establishment of urgent monitoring programs for harmful algal blooms (HABs) given the frequent potential species year-round at both sites but also that these programs need to encompass proper techniques for distinguishing taxa, as species identification by optical microscopy alone is incomplete (e.g., Hoppenrath et al. 2007HOPPENRATH, M. & LEANDER, B.S. 2007. Character evolution in polykrikoid dinoflagellates. Journal of Phycology, 43: 366–377. https://doi.org/10.1111/j.1529-8817.2007.00319.x
https://doi.org/10.1111/j.1529-8817.2007... , Hamsher et al. 2011HAMSHER, S.E., EVANS, K.M., MANN, D.G., POULÍČKOVÁ, A., SAUNDERS, G.W. 2011. Barcoding Diatoms: Exploring Alternatives to COI-5P, Protist, Volume 162, Issue 3, Pages 405–422, ISSN 1434-4610, https://doi.org/10.1016/j.protis.2010.09.005.
https://doi.org/10.1016/j.protis.2010.09... , Fernandes et al. 2014FERNANDES, L. F., HUBBARD, K. A., RICHLEN, M. L., SMITH, J., BATES, S. S., EHRMAN, J., LÉGER, C., MAFRA, L.L., KULIS, D., QUILLIAM, M., LIBERA, K., MCCAULEY, L., ANDERSON, D.M. 2014. Diversity and toxicity of the diatom Pseudo-nitzschia Peragallo in the Gulf of Maine, Northwestern Atlantic Ocean, Deep Sea Research Part II: Topical Studies in Oceanography, Volume 103, Pages 139–162, ISSN 0967-0645, https://doi.org/10.1016/j.dsr2.2013.06.022.
https://doi.org/10.1016/j.dsr2.2013.06.0... , Sterrenburg et al. 2015STERRENBURG, F.A.S., TIFFANY, M.A., HINZ, F., HERWIG, W.E., HARGRAVES, P.E. 2015. Seven new species expand the morphological spectrum of Haslea. A comparison with Gyrosigma and Pleurosigma (Bacillariophyta). Vol. 207 No. 2: 8 May, 143–162. DOI: https://doi.org/10.11646/phytotaxa.207.2
https://doi.org/10.11646/phytotaxa.207.2... ).

In our study area, the typical physical accumulations of phyto­plankton cells nearshore can episodically include organisms that advect from the open ocean guided by winds (Lugomela et al. 2002LUGOMELA, C., LYIMO, T.J., BRYCESON, I., SEMESI, A.K. & BERGMAN, B. 2002. Trichodesmium in coastal waters of Tanzania: diversity, seasonality, nitrogen and carbon fixation. Hydrobiologia 477: 1–13. ), which may be the case for the diazotrophic cyanobacteriaTrichodesmium spp. and Richelia intracellularisat both sampling sites. Slicks of the genusTrichodesmiumare commonly observed in surface waters of the Brazilian Current (Detoni et al. 2016DETONI, A.M.S., CIOTTI, A.M., CALIL, P.H.R., TAVANO, V.M. & YUNES, J.S. 2016. Trichodesmium latitudinal distribution on the shelf break in the southwestern Atlantic Ocean during spring and autumn. Global Biogeochemical Cycles, v. 30, p. 1738–1753.) or in inner shelf waters (< 50 m) during the summer (Brandini et al. 1989BRANDINI, F.P., MORAES, C.L.B., THAMM, C.A. 1989. Shelf break upwelling, subsurface maxima of chlorophyll and nitrite, and vertical distribution of a subtropical nano – and microplankton community off southeastern Brazil. In: Brandini, F.P. (Ed.), Memórias do III Encontro Brasileiro de Plâncton. UFPR, Caiobá, pp. 47–56.). The occurrences could be linked to the relatively low nitrogen input from the continent, as the observations took place during a dry period (Tocci 2016TOCCI, B.R.C. 2016. Ocorrência e coexistência de cianobactérias diazotróficas no Canal de São Sebastião-SP com o aumento da pluviosidade. Dissertação (Oceanografia Biológica) - Instituto Oceanográfico, Universidade de São Paulo, São Paulo.), favoring the growth of diazotrophic cyanobacteria. However, at least forTrichodesmium, the advection of waters from offshore by mesoscale winds (Castro Filho & Mirada 1998CASTRO FILHO, B.M. DE & MIRANDA, L.B. DE. 1998. Physical oceanography of the western atlantic continental shelf located between 4 graus N and 34 graus S: Coastal segment (4,W). In The Sea, vol.11. Oxford: John Wiley & Sons.) could be a source of these organisms for the coast. Moreover, favorable upwelling winds will favor intrusions of the South Atlantic Central Water in the SSC, not only enhancing the local concentration of nutrients and primary production rates (Regaudie et al. 2017REGAUDIE-DE-GIOUX, A., CASTAGNA, A., FERREIRA, A., ABBRECHT, M., BRAGA, E.S. & CIOTTI, A.M. 2017. Influence of mixed upwelled waters on metabolic balance in a subtropical coastal ecosystem: São Sebastião Channel, southern Brazil. MARINE ECOLOGY PROGRESS SERIES, v. 573.) but also transporting diatoms, such asPseudo-nitzschia, that impacted the overall taxa richness. These results indicate the need for future phytoplankton monitoring programs assessing the offshore contribution of water masses to SSC.

The observation of unfrequent taxa of tycopelagic diatoms (Table 1) at AB and SSC included the predominance ofCylindrotheca closterium, Diploneis weissflogii, andThalassionema nitzschioides.The BacillariophyceaeCocconeissp.1,D. didymus, D.cf.smithii,Licmophora tincta, Delphineissp.1, Rhaphoneissp.1, andSurirellasp.1 showed larger densities at AB than SSC, and some species only observed at AB, such asDiploneis didymus, Diploneiscf.smithii, Stenopterobiasp.1,Surirellasp.1, andPlagiogrammasp.1, probably a result from the bay hydrodynamics that due to its shallower depth (Siegle et al. 2018SIEGLE, E., DOTTORI, M. & CAPELARI VILLAMARIN, B. 2018. Hydrodynamics of a subtropical tidal flat: Araçá Bay, Brazil. Ocean & Coastal Management. ) allows organisms to resuspend to the water column during each tidal cycle. This continuous exchange of phytoplankton organisms between the sediments of the bay and SSC water needs further evaluation for a better description of this ecologically important system.

Note that some of the identified taxa are mentioned in the literature as non-toxin-producing bloom formers (Odebrecht et al. 2001ODEBRECHT, C., FERRARIO, M.E., CIOTTI, A.M., KITZMANN, D., MOREIRA, M.O.P., HINZ, F. 2001. The distribution of the diatom Pseudo-nitzschia off southern Brazil, and relationships with oceanographic conditions. In: HALLEGRAEFF, G. et al (Ed) International Conference on Harmful Algal Blooms, 9. Hobart. 42–45., Hallegraeff et al. 2003HALLEGRAEFF, 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. 2th Edition. Paris, UNESCO. 25–50 pp., Moestrup 2004MOESTRUP, O. 2004. IOC Taxonomic reference list of toxic algae. Intergovernmental Oceanographic Commission of UNESCO, Paris. http://www.bi.ku.dk/ioc/default.asp, accessed in June 2008.
http://www.bi.ku.dk/ioc/default.asp... , Villac et al. 2008VILLAC, M.C., NORONHA, V.A. DE P.C. & PINTO, T.DE O. 2008. The phytoplankton biodiversity of the coast of the state of São Paulo, Brazil. Biota Neotrop. 8(3): 151–173.), such as the diatoms Asterionellopsis glacialis, Cerataulina pelagica, Cylindrotheca closterium, Guinardia delicatula, Leptocylindrus minimus, and Chaetoceros spp.; the dinoflagellates Tripos fusus and Tripus hircus; and the silicoflagellate Dictyocha fibula, may alternatively bloom. However, accumulations of these species may result in many other ecologic and economic impacts (Castro et al. 2016CASTRO, N. de O., DOMINGOS, P. & MOSER, G.A.O. 2016. National and international public policies for the management of harmful algal bloom events. A case study on the Brazilian coastal zone. Ocean & Coastal Management, v. 128, p. 40–51.). Additionally, results also reveal the lower diatom diversity when the genus Pseudo-nitzschia was abundant, which occurred during SACW intrusions in the channel.

Our results stress the demand for the urgent implementation of monitoring programs that aid public policies for environmental safety. The occurrences of taxa are known to be potentially harmful, highlighting the dinoflagellates of the genera Alexandrium, cf. Gymnodinium, Dinophysis, Gonoyaulux, and Prorocentrum are unsettling. Although some initiatives are in place, our results demonstrate the need for a comprehensive monitoring program that includes modernized methodologies and hydrodynamical modeling. If conditions for blooming are favored with nutrients input by sewage and warming of seawater temperatures, they may cause fish death, mollusk poisoning, and several public health problems (Hallegraeff et al. 2003HALLEGRAEFF, 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. 2th Edition. Paris, UNESCO. 25–50 pp.).

Acknowledgments

The authors thank colleagues from Laboratório Aquarela and technician staff from CEBIMar/USP for their assistance during field work and data acquisition. This work was funded by Fundação de Apoio à Pesquisa do Estado de São Paulo (FAPESP– 2011/50317-5). A.M.C. received a CNPq fellowship (PQ 312422/2019-9), G.A.O.M. received a FAPERJ/UERJ fellowship (Prociência/2019), B.R.C.T. received a CNPq scholarship (process number 133002/2013-6). This is a contribution of the NP-Biomar/USP. We also thank the detailed revisions provided by two anonymous reviewers.

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