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Morphometric characterization of Dinophysis acuminata/D. sacculus complex in Guanabara Bay, Brazil

Caracterização morfométrica de dinoflagelados do Complexo Dinophysis acuminata/D. saculus na Baía de Guanabara, Brasil

Abstract:

Most studies of Dinophysis acuminata in Brazil are for the southern region, where blooms are recurrent. In 2016, the presence of D. acuminata caused the first-ever production and consumption of species of mollusks commercial embargo from the state of Sao Paulo, Southeast Brazil. Potentially toxic species of Dinophysis have been reported in Guanabara Bay (GB) but only occasionally and in low densities. The present note is the first report of a high-density event (~105 cells L-1) of D. acuminata/D. sacculus complex in GB. D. acuminata/D. sacculus complex species were identified using scanning-electron and inverted-light microscopy. Most of the studied cells possessed a dorsally convex hyposomal plate and had dimensions typical of D. acuminata. However, the observed association with warmer and less saline estuarine waters would indicate that the species could be D. sacculus. Whatever the case, based on the high cell densities observed here, we recommend a continued monitoring for Dinophysis presence in GB.

Keywords:
dinoflagellates; Dinophysis acuminata; Dinophysis sacculus; eutrophic marine ecosystem; South Atlantic Central Water

Resumo:

A maioria dos estudos sobre Dinophysis acuminata no Brasil ocorreram na região sul, onde as florações são recorrentes. Em 2016, a presença de D. acuminata causou o primeiro embargo comercial da produção e consumo de espécies de moluscos do estado de São Paulo, sudeste do Brasil. Várias espécies de microalgas potencialmente nocivas foram relatadas na Baía de Guanabara (BG), incluindo espécies tóxicas de Dinophysis, mas estas foram reportadas apenas como ocasionais e em baixas densidades. A presente nota é o primeiro relato de um evento de alta densidade (~ 105 células L-1) do complexo D. acuminata/D. saculus na BG. As espécies foram identificadas através de microscopia eletrônica de varredura e de campo claro. A maioria das células estudadas possuía uma placa hipossômica dorsalmente convexa, e tinha dimensões típicas de D. acuminata. No entanto, a associação observada com águas estuarinas mais quentes e menos salinas indicaria que a espécie seria D. saculus. Qualquer que seja o caso, com base nas altas densidades observadas aqui, recomendamos o monitoramento contínuo da presença de Dinophysis na BG.

Palavras-chave:
dinoflagelados; Dinophysis acuminata; Dinophysis saculus; ecossistema marinho eutrófico; Água Central do Atlântico Sul

Introduction

The genus Dinophysis Ehrenberg includes species with a diverse morphology and different trophic strategies (autotrophic, heterotrophic and mixotrophic) (Zingone et al. 1998ZINGONE, A., MONTRESOR, M. & MARINO, D. 1998. Morphological variability of the potentially toxic dinoflagellate Dinophysis sacculus (Dinophyceae) and its taxonomic relationships with D. pavillardii and D. acuminata. Eur. J. Phycol. 33: 259-273.). Some of these species are potential producers of phytotoxin and can be responsible for human intoxication events, even in densities as low as <102 cells·L-1, which are rarely detected by quantitative methods (Reguera et al. 2012REGUERA, B., VELO-SUÁREZ, L., RAINE, R. & PARK, M.G. 2012. Harmful Dinophysis species: A review. Harmful Algae, 14, 87-106.). Dinophysis acuminata Claparède & Lachmann (Hattenrath-Lehmann et al. 2015HATTENRATH-LEHMANN, T.K., MARCOVAL, M.A., MITTLESDORF, H., GOLESKI, J.A, WANG, Z., HAYNES, B., MORTON, S.L. & GOBLER, C.J. 2015. Nitrogenous Nutrients Promote the Growth and Toxicity of Dinophysis acuminata during Estuarine Bloom Events. PLoS ONE 10(4):e0124148.) has received significant attention because inputs of nutrients and organic matter can promote both its toxicity and growth. Nevertheless, this species belongs to the "D. acuminata complex", which contains taxa that are difficult to discriminate with conventional microscopy due to morphological variability (Reguera et al. 2012REGUERA, B., VELO-SUÁREZ, L., RAINE, R. & PARK, M.G. 2012. Harmful Dinophysis species: A review. Harmful Algae, 14, 87-106.). One such case is the pair D. acuminata Claparède & Lachmann/D. sacculus F. Stein (Zingone et al. 1998), which can co-occur (Reguera et al. 2012REGUERA, B., VELO-SUÁREZ, L., RAINE, R. & PARK, M.G. 2012. Harmful Dinophysis species: A review. Harmful Algae, 14, 87-106.). Both species have been associated with diarrhetic shellfish poisoning (DSP) events (Reguera et al. 2012REGUERA, B., VELO-SUÁREZ, L., RAINE, R. & PARK, M.G. 2012. Harmful Dinophysis species: A review. Harmful Algae, 14, 87-106., and references, García-Altares et al. 2016GARCÍA-ALTARES, M., CASANOVA, A., FERNÁNDEZ-TEJEDOR, M., DIOGÈNE, J. & DE LA IGLESIA, P. 2016. Bloom of Dinophysis spp. dominated by D. SACCULUS and its related diarrhetic shellfish poisoning (DSP) outbreak in Alfacs Bay (Catalonia, NW Mediterranean Sea): Identification of DSP toxins in phytoplankton, shellfish and passive samplers. Reg. Stud. Mar. Sci. 6: 19-28.).

In Brazil, most of the studies on D. acuminata have occurred in the South region, due to its great importance for oyster and mussel cultivation. (Mafra-Junior et al. 2006MAFRA-JUNIOR, L.L., FERNANDES, L.F. & PROENÇA, L.A.O. 2006. Harmful algae and toxins in Paranaguá Bay, Brazil: bases for monitoring. Braz. J. Oceanogr. 54(2-3): 107-121., Mello et al. 2010MELLO, D.F., PROENÇA, L.A.O. & BARRACCO, A.M. 2010. Comparative Study of Various Immune Parameters in Three Bivalve Species during a Natural Bloom of Dinophysis acuminata in Santa Catarina Island, Brazil. Toxins 2: 1166-1178., Simões et al. 2014SIMÕES, E., VIEIRA, R.C., SCHRAMM M.A., MELLO, D.F., PONTINHA, V.A., SILVA, P.M. & BARRACCO, M.A. 2015. Impact of harmful algal blooms (Dinophysis acuminata) on the immune system of oysters and mussels from Santa Catarina, Brazil. J. Mar. Biol. Assoc. UK. 95(4): 773-781., Tibiriçá et al. 2015TIBIRIÇÁ, C.E.J.A., FERNANDES, L.F. & MAFRA-JUNIOR, L.L. 2015. Seasonal and spatial patterns of toxigenic species of Dinophysis and Pseudo-Nitzschia in a subtropical Brazilian Estuary. Braz. J. Oceanogr. 63(1): 17-32.). Natural blooms of this species along the southern Brazilian coast lead to recurrent commercial embargos of cultivated species, resulting in important economic losses (Simões et al. 2014SAHRAOUI, I., BOUCHOUICHA, D., MABROUK, H.H. & HLAILI, A.S. 2013. Driving factors of the potentially toxic and harmful species of Prorocentrum Ehrenberg in a semi-enclosed Mediterranean lagoon (Tunisia, SW Mediterranean). Mediterr. Mar. Sci. 14(2): 353-362.). From May to July 2016, D. acuminata was reported along the coast from Santa Catarina to São Paulo in densities that led to the first-ever commercial embargo of the production and consumption of oysters and mussels by the health authorities of the state of São Paulo (A Tribuna 2016A Tribuna 2016. Consumo e venda de moluscos estão proibidos no Estado de São Paulo. http://www.atribuna.com.br/noticias/noticias-detalhe/santos/consumo-de-moluscos-bivalves-estaproibido/?cHash=c936e644836340a5b4c19ae8655eeacf. (last access 17/02/2017)
http://www.atribuna.com.br/noticias/noti...
).

Although D. acuminata has been detected along Rio de Janeiro's coast, blooms have not been reported yet. At Sepetiba Bay on the southern coast of Rio de Janeiro, D. acuminata was found to be dominant among the five species of the genus detected, but both cell densities and toxin concentrations on mussels were lower than the limit allowed by law (Ferreira et al. 2010FERREIRA V.M., OLIVEIRA G.M., PEREIRA M.M.D., SILVA, P.P.O., BORBA, H.R., LOURENÇO,A.J. & SILVA, P.F.N. 2010. Produção da ficotoxina diarreica ácido ocadaico associada à microalga Dinophysis acuminata (Ehremberg 1839) na baía de Sepetiba, RJ e sua implicação para a saúde pública. R. Bras. Ci. Vet. 17(2): 87-90., Brasil 2012). Guanabara Bay (GB) encompasses many more municipalities than the city of Rio de Janeiro, being the second largest bay of the Brazilian coast, and is historically under intense eutrophication, thus a program of continuous monitoring of planktonic species should be implemented (Fistarol et al. 2015FISTAROL G.O.,COUTINHO F.H., MOREIRA A.P.B., VENAS, T., CANOVAS. A., PAULA, S.E.M., COUTINHO, R., MOURA, R.L.,VALENTIN, J.L., TENENBAUM, D.R., PARANHOS, R.,VALLE, R.A.B., VICENTE, A.C.P., AMADO, G., PEREIRA, R.C., KRUGER, R., REZENDE, C.E, THOMPSON, C.C., SALOMON, P. & THOMPSON, F.L. 2015. Environmental and sanitary conditions of Guanabara Bay, Rio de Janeiro. Front. Microbiol. 6: 1-17.). Several potentially harmful microalgal species have been reported at high densities in GB: Scrippsiella trochoidea (Stein) Loeblich (Villac & Tenenbaum 2010VILLAC, M.C. and TENENBAUM, D.R. 2010. The phytoplankton of Guanabara Bay, Brazil. I. Historical account of its biodiversity. Biota Neotrop. 10(2): 271-293. http://www.biotaneotropica.org.br/v10n2/pt/abstract?article+bn02410022010 ISSN 1676-0603 (último acesso em 05/05/2019)
http://www.biotaneotropica.org.br/v10n2/...
), Pseudo-nitzschia H. Peragallo spp. (Rezende et al. 2015REZENDE, K.R.V., HATHERLY, M.M.F., PIMENTA, C.M.M., EDUARDO, J., VIANNA, S.C. & MANGIAVACCHI, N. 2015. Phytoplankton community structure in one sector of Guanabara Bay (RJ, Brazil) during 2011 and 2012. Braz. J. Oceanogr. 63(3): 239-254.), filamentous cyanobacteria, Prorocentrum Ehrenberg spp. (Villac & Tenenbaum, 2010VILLAC, M.C. and TENENBAUM, D.R. 2010. The phytoplankton of Guanabara Bay, Brazil. I. Historical account of its biodiversity. Biota Neotrop. 10(2): 271-293. http://www.biotaneotropica.org.br/v10n2/pt/abstract?article+bn02410022010 ISSN 1676-0603 (último acesso em 05/05/2019)
http://www.biotaneotropica.org.br/v10n2/...
, Rezende et al. 2015REZENDE, K.R.V., HATHERLY, M.M.F., PIMENTA, C.M.M., EDUARDO, J., VIANNA, S.C. & MANGIAVACCHI, N. 2015. Phytoplankton community structure in one sector of Guanabara Bay (RJ, Brazil) during 2011 and 2012. Braz. J. Oceanogr. 63(3): 239-254.), and Chattonella B.Biecheler spp. (Fistarol et al. 2015FISTAROL G.O.,COUTINHO F.H., MOREIRA A.P.B., VENAS, T., CANOVAS. A., PAULA, S.E.M., COUTINHO, R., MOURA, R.L.,VALENTIN, J.L., TENENBAUM, D.R., PARANHOS, R.,VALLE, R.A.B., VICENTE, A.C.P., AMADO, G., PEREIRA, R.C., KRUGER, R., REZENDE, C.E, THOMPSON, C.C., SALOMON, P. & THOMPSON, F.L. 2015. Environmental and sanitary conditions of Guanabara Bay, Rio de Janeiro. Front. Microbiol. 6: 1-17.). The potentially toxic species of the genus Dinophysis (i.e. D. acuminata/ D. sacculus), however, have been described as only occasional and in low densities (Rezende et al. 2015REZENDE, K.R.V., HATHERLY, M.M.F., PIMENTA, C.M.M., EDUARDO, J., VIANNA, S.C. & MANGIAVACCHI, N. 2015. Phytoplankton community structure in one sector of Guanabara Bay (RJ, Brazil) during 2011 and 2012. Braz. J. Oceanogr. 63(3): 239-254.). Nonetheless, several studies have recommended the implementation of protocols able to detect Dinophysis sp. at low-densities (<102 cells L−1) in the water column serving as an early warning system (Reguera et al. 2014REGUERA, B., RIOBÓ, P., RODRÍGUEZ F., DÍAZ, P.A., PIZARRO, G., PAZ, B., FRANCO, J.M. & BLANCO, J. 2014. Dinophysis toxins: Causative organisms, distribution and fate in shellfish. Mar. Drugs 12(1): 394-461.).

The present work is the first report of a bloom of Dinophysis in Guanabara Bay, Rio de Janeiro (Brazil), and a morphological and morphometric study of the analyzed cells is provided.

Material and Methods

Surveys were performed on September 1st, 2015, along a transect of eight sampling points from Paquetá Island (inner region) to Rasa Island (outer region) along the dredged channel of Guanabara Bay (22°80'S; 43°14'W) (Figure 1). Phytoplankton samples were collected, both during ebb and during flood tides, with Niskin bottles at sub-surface and near the bottom. Sub-samples of 250 mL were fixed with Lugol´s solution and preserved in the dark, at room temperature, until laboratory analysis. At laboratory, aliquots of 5 - 10 mL were prepared according to the Utermölh (1958)UTERMÖHL H., 1958. Zur vervollkommnung der quantitativen phytoplanktonmethodik. Mitt. Int. Ver. Theor. Angew. Limnol. 9: 1-38. method and examined and photographed under 200 x and 400 x magnification using a ZEISS® Axiovert A1 inverted microscope and an ZEISS® AxioCAM 105 camera. Bright field (BF) and phase contrast (PH) were used for identification. Images of the different organisms identified were captured with the AxioCAM 105 camera and processed with the software Zen (Blue Edition; Carl ZEISS®). The images of 55 organisms were used to measure the morphological parameters (length, width and the hidden dimension) of the cells of D. acuminata/D. sacculus complex. Cell surface and cell volume were calculated according with the equations described in Sun & Liu (2003)SUN, J. & LIU, D. 2003. Geometric Models for Calculating Cell Biovolume and Surface Area for Phytoplankton. J. Plankton Res.. 25(11): 1331-1346.. Samples were prepared for scanning electron microscopy (SEM) by gentle filtration of 20 ml through 0.2 µm pore-size Nuclepore membranes. Salt was removed by washing the filters with small amounts of deionized water. The filters were dried, mounted on stubs with double-sided sticky tape and vacuum coated with graphite. The samples were examined with a JEOL JSM 6510LV scanning electron microscope.

Figure 1
Study area - Guanabara Bay (Rio de Janeiro, Brazil). Sampling points (red dots) in a transect from the inner part of the bay (denoted by a number and letter D) to the inner continental shelf (denoted by a number and letter F).

The relationships among phytoplanktonic cell densities and abiotic variables were determined using Pearson's correlation (Software Statistica® by Statsoft) (Cassie, 1962CASSIE, R.M. 1962. Frequency distribution models in the ecology of plankton and other organisms. J. Anim. Ecol. 31: 65-92.).

Results

Water temperature was higher in the inner region (19.9 - 25.1 °C) than in the outer region (16.1 - 19.8 °C) of the bay. Salinity ranged from 24.2 to 35.2 in the inner region, and from 35.3 to 36.0 in the outer. Total chlorophyll ranged from 2.04 to 45.03 mg m-3 in the inner region, and from 0.45 to 7.48 mg m-3 in the outer.

Phytoplankton densities were higher in the inner region (2.8x105 - 2.8x107 cells L-1) than in the outer region (5.1x103 - 4.1x106 cells L-1). Although they were not dominant, dinoflagellate densities ranged from 1.3x104 - 2.2x106 cells L-1 to 4.0x101 - 3.9x105 cells L-1, in the inner and outer regions, respectively. Among the dinoflagellates, the genus Prorocentum was dominant (average > 50 %), both in the inner and outer regions. The contribution of the genus Dinophysis was lower than 10% on average (maximum 25%), with the D. acuminata/D. sacculus complex being dominant for this genus (maximum 1.2x105 cells L-1 at inner portion) (Table 1). The cell density of the D. acuminata/D. sacculus complex was positively correlated with that of P. dentatum (r=0.91; p<0.001) and P. micans (r=0.79; p<0.01). The abundance of D. acuminata/D. sacculus complex was also positively correlated (r= 0.72; p<0.001) with temperature and negatively correlated (r= -0.61; p<0.001) with salinity.

Table 1
Average (av.), standard deviation (sd), minimum (min) and maximum (max) of cell densities (x103 cells L-1) of Dinophysis genera, Dinophysis acuminata/sacculus complex, and Prorocentrum genera at inner and outer regions.

Cells of the Dinophysis acumitata/D. sacculus complex were 33.2 - 44.2 µm long, 20.3 - 32.3 µm wide, and 13.5 - 20.1 µm of hidden dimension (Table 2). The length/width (l/w) ratio varied from 1.2 to 1.9 and the Surface/Volume ratio ranged from 0.24 to 0.28. The shape of the cells was slightly convex, with a convex and sculptured sulcal platelet with three ribs, which was almost half of the hypothecal length (Figure 2a-g); this morphotype is intermediate between the two species of this complex.

Table 2
Average (av.), standard deviation (sd, minimum (min) and maximum (max) length, width, hidden dimension, length/width (l/w) ratio, surface (S), volume (V) and S/V ratio for the Dinophysis acuminata/D. sacculus complex at September 2015 (n=55).

Figure 2
Lateral view (a-g) and hidden dimension (h) view of complete cells at Light Microscopy (LM) of Dinophysis acuminata/D. sacculus complex from Guanabara Bay samples. Scale bars: 10 µm.

Under SEM, small smooth pores were seen irregularly scattered on the surface of the hypotheca (Figure 2a). The number of pores distributed along 10 µm varies from six in the middle region of the hypotheca, to 12 near the cingular platelet (Figure 3a-b). Two rows of pores were observed on the sulcal platelet (Figure 3c).

Figure 3
Details of the theca, scanning electron microscopy (SEM), of the cells of Dinophysis acuminata/D. sacculus complex from Guanabara Bay samples. Scale bars: a 10 µm; b-c 2 µm. Arrows indicate pores distribution.

Discussion

During the winter of 2015, a high-abundance (~105-106 cells L-1) event of dinoflagellates was observed at Guanabara Bay (Rio de Janeiro, Brazil). It was dominated by the genus Prorocentrum Ehrenberg, mainly the species P. dentatum F.Stein and P. micans Ehrenberg. Associated with these, the high cell densities of the Dinophysis acuminata/D. sacculus complex were also observed. The co-occurrence of Dinophysis and Prorocentrum blooms were previously reported by several studies (i.e. Reguera et al. 2012REGUERA, B., VELO-SUÁREZ, L., RAINE, R. & PARK, M.G. 2012. Harmful Dinophysis species: A review. Harmful Algae, 14, 87-106., Hattenrath-Lehmann et al. 2015HATTENRATH-LEHMANN, T.K., MARCOVAL, M.A., MITTLESDORF, H., GOLESKI, J.A, WANG, Z., HAYNES, B., MORTON, S.L. & GOBLER, C.J. 2015. Nitrogenous Nutrients Promote the Growth and Toxicity of Dinophysis acuminata during Estuarine Bloom Events. PLoS ONE 10(4):e0124148.), as well as the occurrence of a bloom of Prorocentrum after Dinophysis events (Campbell et al. 2010CAMPBELL, L., OLSO, R.J., SOSIK, H.M., ABRAHAM, A., HENRICHS, D.W., HYATT, C.J., & BUSKEY, E.J. 2010. First harmful Dinophysis (Dinophyceae, Dinophysiales) bloom in the U.S. is revealed by automated imaging flow cytometry. J. Phycol. 46(1): 66-75.). Prorocentrum micans, which reached densities as high as 106 cells L-1 in the present work, was reported as highly abundant in warm and nutrient-rich waters, such as that of GB (Sahraoui et al. 2013SAHRAOUI, I., BOUCHOUICHA, D., MABROUK, H.H. & HLAILI, A.S. 2013. Driving factors of the potentially toxic and harmful species of Prorocentrum Ehrenberg in a semi-enclosed Mediterranean lagoon (Tunisia, SW Mediterranean). Mediterr. Mar. Sci. 14(2): 353-362.). Prorocentrum micans was also reported as a producer of putative palytoxin and ovatoxin-a (Ignatiades & Gotsis-Skretas 2010IGNATIADES, L. & GOTSIS-SKRETAS, O. 2010. A Review on Toxic and Harmful Algae in Greek Coastal Waters (E. Mediterranean Sea). Toxins 2: 1019-1037.), nevertheless, the frequent association of this species with DSP could be due to the presence of D. acuminata in densities too low to be detected (Reguera et al. 2014REGUERA, B., RIOBÓ, P., RODRÍGUEZ F., DÍAZ, P.A., PIZARRO, G., PAZ, B., FRANCO, J.M. & BLANCO, J. 2014. Dinophysis toxins: Causative organisms, distribution and fate in shellfish. Mar. Drugs 12(1): 394-461. and references therein).

Although D. acuminata is usually associated with colder waters and D. sacculus with warmer waters, the two species were reported coexisting in several coastal environments, probably due to the difficulty in distinguishing their cells (Zingone et al. 1998ZINGONE, A., MONTRESOR, M. & MARINO, D. 1998. Morphological variability of the potentially toxic dinoflagellate Dinophysis sacculus (Dinophyceae) and its taxonomic relationships with D. pavillardii and D. acuminata. Eur. J. Phycol. 33: 259-273.). Thus, in GB, the Dinophysis complex was clearly associated with the warmer and less saline waters of the inner estuary. In a study in southern Brazil, Haraguchi and Odebrecht (2010)HARAGUCHI, L., and ODEBRECHT, C. 2010. Dinophysiales (Dinophyceae) no extremo Sul do Brasil (inverno de 2005, verão de 2007). Biota Neotrop. 10(3): 101-114. http://www.biotaneotropica.org.br/v10n3/en/abstract?article+bn01910032010 (último acesso em 05/05/2019)
http://www.biotaneotropica.org.br/v10n3/...
reported high abundances of D. acuminata (~104 cells L-1) associated with intrusions of a cold and salty water mass, the South Atlantic Central Water (SACW), while other species of Dinophysis, such as D. fortii Pavillard, were associated with warmer waters. In the present work, the influence of the SACW was especially observed in the outer region of GB (data not published), where lower densities of the D. acuminata/D. sacculus complex were observed, suggesting that most of the cells identified were probably D. sacculus.

Based on morphometric characteristics, most of the cells identified here possess a more dorsally-convex hypothecal plate with dimensions (especially the ratio l/w) typical of D. acuminata, and even the length of the cells found here is considerably shorter than those described in the literature (Zingone et al. 1998ZINGONE, A., MONTRESOR, M. & MARINO, D. 1998. Morphological variability of the potentially toxic dinoflagellate Dinophysis sacculus (Dinophyceae) and its taxonomic relationships with D. pavillardii and D. acuminata. Eur. J. Phycol. 33: 259-273.). On the other hand, the association with warmer and less saline estuarine waters was reported more often for D. sacculus than for D. acuminata, the latter being typical of colder waters. Nevertheless, both species of this complex were reported as potentially toxic even in low densities, as is the case for D acuminata (Zingone et al. 1998ZINGONE, A., MONTRESOR, M. & MARINO, D. 1998. Morphological variability of the potentially toxic dinoflagellate Dinophysis sacculus (Dinophyceae) and its taxonomic relationships with D. pavillardii and D. acuminata. Eur. J. Phycol. 33: 259-273., Reguera et al. 2012REGUERA, B., VELO-SUÁREZ, L., RAINE, R. & PARK, M.G. 2012. Harmful Dinophysis species: A review. Harmful Algae, 14, 87-106., Reguera et al. 2014REGUERA, B., RIOBÓ, P., RODRÍGUEZ F., DÍAZ, P.A., PIZARRO, G., PAZ, B., FRANCO, J.M. & BLANCO, J. 2014. Dinophysis toxins: Causative organisms, distribution and fate in shellfish. Mar. Drugs 12(1): 394-461.). In addition, nutrient loading can enhance both growth and toxicity of Dinophysis species (Hattenrath-Lehmann et al. 2015HATTENRATH-LEHMANN, T.K., MARCOVAL, M.A., MITTLESDORF, H., GOLESKI, J.A, WANG, Z., HAYNES, B., MORTON, S.L. & GOBLER, C.J. 2015. Nitrogenous Nutrients Promote the Growth and Toxicity of Dinophysis acuminata during Estuarine Bloom Events. PLoS ONE 10(4):e0124148.).

Thus, even without the ability to distinguish between the two species of the D. acuminata/D. sacculus complex, high densities of this complex would be monitored in highly eutrophic coastal areas, such as Guanabara Bay.

Acknowledgements

We thank CAPES CIÊNCIAS DO MAR (Nº 43/2013) for their financial support and for providing scholarship; and the collaboration of Drs. Alexandre Macedo Fernandes and Ana Furtado.

References

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Publication Dates

  • Publication in this collection
    01 July 2019
  • Date of issue
    2019

History

  • Received
    07 Jan 2019
  • Reviewed
    21 May 2019
  • Accepted
    23 May 2019
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