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Brazilian Journal of Oceanography

Print version ISSN 1679-8759On-line version ISSN 1982-436X

Braz. j. oceanogr. vol.63 no.3 São Paulo July/Sept. 2015

http://dx.doi.org/10.1590/S1679-87592015086506303 

Original Article

Phytoplankton community structure in one sector of Guanabara Bay (RJ, Brazil) during 2011 and 2012

Katia Regina Vieira de Rezende1  * 

Melissa Medeiros Ferreira Hatherly1 

Cristiane Marques Monteiro Pimenta1 

Janaina Eduardo1 

Simone de Castro Vianna1 

Norberto Mangiavacchi1 

1GESAR, Unidade de Desenvolvimento Tecnológico, Universidade do Estado do Rio de Janeiro (Rua Fonseca Teles, 121, São Cristóvão, Rio de Janeiro, Brazil)

Abstract

This study analyzed the temporal variability of phytoplankton assemblages in the surface waters of Guanabara Bay (RJ, Brazil), at six stations in front of Icaraí Inlet from April/2011 to April/2012. Our results highlight the great contribution of diatoms, dinoflagellates and cyanobacteria, represented by 111 taxa typical of estuarine and coastal areas. The coexistence of benthic and planktonic species suggests considerable hydrodinamism in these waters. All variables were homogeneous (p > 0.05) between the stations, but differed between sampling periods. On average, phytoplankton abundance (107 cells.L-1) was higher than that of other estuaries and its temporal behavior was closely correlated (p < 0.01) with diatoms and cyanobacteria. The richness distribution pattern (7 to 27 taxa) was closely correlated (p < 0.01) with dinoflagellates and diatoms. Ninety per cent of all samples presented a low diversity index (< 2.0 bits.cell-1), which indicated the unstable balance of the system, typical of environments subjected to eutrophication. The population structure analysis revealed that 10% of all taxa were resident, 12% visitors and 78% accidental, suggesting the influence of continental and oceanic water influxes. Between the "typical" taxa, the most common were the cyanobacteria of the order Oscillatoriales, the diatoms Ceratoneis closterium (=Cylindrotheca closterium) and Leptocylindrus minimus and the dinoflagellate Prorocentrum triestinum.

Descriptors: Tropical estuary; Temporal variation; Species Diversity; Microphytoplankton

Resumo

Este trabalho analisou a variabilidade sazonal da comunidade microfitoplanctônica em águas superficiais da Baía da Guanabara (RJ, Brasil) em 6 estações em frente à Enseada de Icaraí, de abril de 2011 a abril de 2012. Os resultados destacaram a alta representatividade de diatomáceas, dinoflagelados e cianobactérias, representados por 111 táxons típicos de ambientes estuarinos/costeiros. A coexistência de espécies bentônicas e planctônicas indicou o alto hidrodinamismo local. Houve homogeneidade (p > 0,05) entre as estações de coleta para todas as variáveis, mas diferenças entre campanhas. A densidade média (107 cel.L-1) foi superior à de outros sistemas estuarinos e seu comportamento temporal esteve altamente correlacionado (p < 0,01) com diatomáceas e cianobactérias. Por sua vez o padrão de distribuição da riqueza (7 a 27 táxons) apresentou alta correlação positiva (p < 0,01) com dinoflagelados e diatomáceas. Baixos índices de diversidade (< 2,0 bits.cel-1) em 90% das amostras reafirmaram o equilíbrio instável do sistema, típico de ambientes sujeitos à eutrofização. A análise da estrutura das populações estabeleceu que 10% dos táxons são residentes, 12% visitantes e 78% acidentais, reafirmando a influência do aporte continental e/ou águas oceânicas. Entre os táxons "típicos", destacaram-se cianobactérias da Ordem Oscillatoriales, diatomáceas Ceratoneis closterium (=Cylindrotheca closterium) e Leptocylindrus minimus e o dinoflagelado Prorocentrum triestinum.

Descritores: Estuário tropical; Variação temporal; Diversidade específica; Microfitoplâncton

INTRODUCTION

The evaluation of the condition of an ecosystem requires the assessment of its primary productivity and trophic dynamics in view of the structure and ecological functions of its communities. Phytoplankton represents the basis of the main food webs in aquatic ecosystems, and its taxonomic composition and abundance respond to environmental disturbances (i.e. physical processes such as advective currents and turbulence, and chemical composition - nutrients), and to the interaction between species (i.e. competition for resources: light and nutrients) (MARGALEF, 1963; 1978). Consequently, the assessment of an aquatic ecosystem dynamics is relevant not only for the system’s production, but also for the possibility of using organisms as an efficient proxy for determining natural and anthropogenic disturbances (LOBO; CALLEGARO; BENDER, 2002).

SIEBURTH, SMETACEK and LENZ (1978)s proposed the classification of planktonic cells in three groups according to their size, named pico (0.2-2 µm), nano (2-20 µm) and microplankton (20-200 µm). Because of their small size, these organisms present a short generation time (hours-days), and their rapid response to environmental conditions makes them good indicators of important environmental processes such as eutrophication (HARRIS, 1986; SOMMER, 1989; REYNOLDS; PADISÁK; SOMMER, 1993).

Coastal and estuarine areas present high productivity due to nutrient rich terrestrial inputs and anthropogenic effects on distinct temporal and spatial scales. The great hydrodynamism caused by these impacts increases the ability of these regions to sustain high primary production and metabolic rates of phytoplanktonic cells (CLOERN; FOSTER; KLECKNER, 2014), due to alterations in phytoplankton community structure that are reflected in the marine food web (JI et al., 2007; CLOERN; JASSBY, 2010; LLEBOT et al., 2011).

Guanabara Bay is one of the largest embayments of the Brazilian coast. It is shallow (5-50 m depth) but presents a north-south axis of 30 km, a perimeter of 131 km, an area of 384 km2, and 1.87 x 109 m3 of water volume (KJERFVE et al., 1997; KJERFVE, SEELIGER; LACERDA, 2001). The climate of this region is warm and wet all year around (average humidity of 78% and temperature of 23.7º C), with a rainy season during spring-summer (September to March) and a drier period during autumn-winter (April to August), a seasonality that influences the hydrobiology of the bay. Hydrological characteristics respond to temporal (daily and seasonal) variations of tides and cold fronts (precipitation and winds), which influence the terrestrial freshwater inflow that impacts certain areas of the bay strongly: high precipitation in summer causes an increase of the terrestrial freshwater input, the opposite occurring in winter. The freshwater input is derived from river catchment basins, which receive domestic and industrial effluents (MAYR; TENENBAUM; VILLAC, 1989), and the input of coastal seawater increases during high tide (VALENTIN et al., 1999). Tides present a semi-diurnal regime (AMADOR, 1997) with average amplitude of 0.7 m, ranging from 1.1 m during spring to 0.3 m in neap tide periods (JICA, 1994; VALENTIN et al., 1999; KJERFVE, SEELIGER; LACERDA, 2001). Guanabara Bay is surrounded by large urbanized areas such as the cities of Rio de Janeiro and Niterói (SCHWAMBORN et al., 2004), and by the second largest industrial park in the country, with around 6000 factories 1% of which account for 80% of the industrial pollution poured into the bay (CIDS, 2000). Because of these conditions, Guanabara Bay is considered a polluted eutrophic system (JICA, 1994), despite the processes of autodepuration that occur through interchanges with the ocean, which save the biota from irreversible damage (VALENTIN et al., 1999).

The sampling area is located in front of Icaraí Inlet (22º55'S-43º08'W) in Niterói city, RJ (Figure 1). The waves that enter the inlet, coming from south and southwest, lead to great hydrodynamism in this area, especially during storm surges (SILVA; RESENDE; SANTOS, 1999; SANTOS; SILVA; SALVADOR, 2004).

Figure 1 Map of Guanabara Bay showing location of the sampling area (Niterói, Rio de Janeiro). 

Phytoplankton from Guanabara Bay has been studied since the early XX century, but most of the studies are scattered in academic thesis and dissertations. The first studies that include analyses of population dynamics as a function of environmental variables were published during the 80’s, and generated a broad characterization of the system’s hydrobiology (MAYR; TENENBAUM; VILLAC, 1989). Recently, VILLAC and TENENBAUM (2010) have gathered information contained in 57 publications with data obtained between 1913 and 2004 in a state of art manuscript on the phytoplankton biodiversity of Guanabara Bay. The analysis of this information allowed them to conclude that, despite the fact that some of the studies published contain lists of microphytoplankton species, most of them adopt an ecological approach and highlight only the most abundant species. According to this historical study, the inventory of phytoplankton species from Guanabara Bay totaled 308 taxa, with the dominance of diatoms (62%) and dinoflagellates (32%), and other groups such as cyanobacteria, euglenophyceans, chlorophyceans, prasinophyceans, silicoflagellates and ebriidae were also represented. Other studies revealed that, in Guanabara Bay, phytoplankton assemblages present spatial heterogeneity, and their abundance is comparable to that of intensely polluted estuaries.

Changes in phytoplankton communities due to the effects of natural events or pollutants can be determined by the investigation of the species’ composition, cell numbers and diversity indices. Thus, the goal of this work is to describe the abundance and community structure of microphytoplankton in surface waters of one sector of Guanabara Bay, during the period between April 2011 and April 2012. These results broaden the information available on the temporal change of the phytoplankton of this system under the influence of the variation of coastal water quality and anthropogenic activities and may be valuable for future environmental monitoring and assessment programs.

MATERIAL AND METHODS

Sampling and analysis

Surface water samples were taken using a Van Dorn bottle and then stored in 500 to 1000 ml glass vials and fixed with a Lugol solution (THRONDSEN, 1978). Sampling was carried out fortnightly (36 samples) from April to June 2011, and monthly during the remaining period (60 samples) at six stations in front of Icaraí inlet (Figure 1). Microphytoplankton abundance and species composition were evaluated in accordance with HASLE (1978). Aliquotes of 2 to 10 ml were analyzed by the UTERMOHL (1958) method, using inverted microscopes (Coleman NIB-100 and Nikon TS100F) with phase contrast and 200x magnification. The phytoplankton counts were based on a minimum of 150 settled units (single cells, chain-forming and filamentous organisms). In addition, the number of cells in each settled unit (SHAW, 1964; TENENBAUM et al., 2001; GUENTHER et al., 2012) was also registered and the results were expressed as cells per liter (cells.L-1).

In order to avoid missing the richness per sample, organisms that could not be identified to the species level were classified into broader taxonomic groups (class, order and family) and identified by their morphotypes according to cells shape and dimension. We would point out that the identification of most taxa requires complex training and the utilization of more advanced microscopy techniques with a higher resolution (SOURNIA, 1978; TOMAS, 1997). The classification systems used for taxonomic denomination were those of ROUND, CRAWFORD and MANN (1990) for Diatoms, FENSOME et al. (1993) for dinoflagellates, KOMÁREK and ANAGNOSTIDIS (1989; 2005) for cyanobacteria and THRONDSEN (1997) for Chlorophythes.

Data analysis

The Kruskal-Wallis non-parametric test was used to test the temporal and spatial variability (p < 0.05) in phytoplankton abundance, richness and the Shannon-Wiener Diversity index. The Mann-Whitney non-parametric test was applied to compare co-temporal independent samples during the biweekly sampling period. To establish correlation between variables the Simple Linear Correlation (Pearson’s r) test, that determines the extent to which values of the two variables are “proportional” to each other, was used. The analysis of microphytoplankton community structure was performed using three ecological indexes: a) the Constancy index: the taxon was considered “resident” when it was recorded in more than 50% of the samples, “visitor” when it was recorded in 25-50% of the samples and “accidental” when recorded in less than 25% of the samples (DAJOZ, 1983); b) the Shannon-Wiener Species Diversity index and c) Pielou's Evenness index (LEGENDRE; LEGENDRE, 1998). The analysis of Similarity Percentages (SIMPER) identified the taxa responsible for the similarity of samples in each sampling period (CLARKE; WARWICK, 1994). Some analyses (Kruskal-Wallis, Mann-Whitney and Simple Linear Correlation) were carried out using STATISTICA (Version 7), other routines (Shannon-Wiener Diversity, Pielou´s Evenness and Simper analysis) were performed using PRIMER (Version 5).

RESULTS

Specific composition, richness and abundance

A total of 110 taxa were identified, belonging to 4 Divisions (Figure 2; Table 1): Diatoms (55 taxa; 25 species), Dinoflagellates (51 taxa; 25 species), Cyanobacteria (2 taxa) and Chlorophythes (2 taxa).

Figure 2 Percentage Contribution of Diatoms, Dinoflagellates, Cyanobacteria and Chlorophytes considering the entire study period (A) and separated by sampling cruise (B). 

Table 1 List of taxa found in Guanabara Bay from April 2011 to April 2012 indicating percentage of occurrence (%) in all samples (n = 96), classification by Constancy Index (R = resident; V = visitor and A = accidental) and occurrence by month (n = 13). The following classification systems were adopted: Round, Crawford and Mann (1990)for Diatoms (Bacillariophyta); Fensome et al. (1993) for dinoflagellates (Dinoflagellata); Komárek and Anagnostidis (1989; 2005) for cyanobacteria (Cyanophyta) and Throndsen (1997) for Chlorophythes (Chlorophyta). The morphotypes are not included in this table. 

TAXONOMY CATEGORY Total Occurrence (%) n = 96 Constancy Index Occurrence by month (n = 13)
2011 2012
Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr
Division Bacillariophyta                              
Class Coscinodiscophyceae                              
Order Thalassiosirales                              
Family Thalassiosiraceae                              
Thalassiosira sp. 18 A *     * *   * * *     * *
Family Skeletonemataceae                              
Skeletonema cf. costatum (Greville) Cleve 25 A *   * *     * *       * *
Skeletonema sp. 6 A           * *            
Order Paraliales                              
Family Paraliaceae                              
Paralia sulcata (Ehrenberg) Cleve 1 A               *          
Order Coscinodiscales                              
Family Coscinodiscaceae                              
Coscinodiscus sp. 1 A                         *
Order Triceratiales                              
Family Triceratiaceae                              
Odontella aurita (Lyngbye) C. Agardh 1 A               *          
Order Hemiaulales                              
Family Hemiaulaceae                              
Cerataulina pelagica (Cleve) Hendey 3 A               *          
Eucampia cornuta (Cleve) Grunow 1 A               *          
Eucampia sp. 1 A               *          
Hemiaulus membranaceus Cleve 1 A               *          
Order Rhizosoleniales                              
Family Rhizosoleniaceae                              
Dactyliosolen fragilissimus (Bergon) Hasle 1 A                         *
Dactyliosolen phuketensis (B. G. Sundstrom) G. R. Hasle 2 A                 *        
Guinardia flaccida (Castracane) H. Peragallo 1 A   *                      
Guinardia striata (Stolterfoth) Hasle 2 A       *               *  
Guinardia sp. 15 A     * *   *              
Proboscia alata (Brightwell) Sundstrom 2 A     *                   *
Rhizosolenia setigera Brightwell 42 V *     * * * * * *     * *
Rhizosolenia setigera f. pungens(Cleve-Euler) Brunel 2 A                 *        
Order Chaetocerotales                              
Family Chaetocerotaceae                              
Chaetoceros compressus Lauder 3 A               * *        
Chaetoceros curvisetum Cleve 2 A               *          
Chaetoceros danicus Cleve 6 A           *   *         *
Chaetoceros radians F. Schutt 2 A           * *            
Chaetoceros socialis H. S. Lauder 1 A                         *
Chaetoceros cf. socialisH. S. Lauder 4 A               *          
Chaetoceros spp. 15 A   * *     *   * *     *  
Order Leptocylindrales                              
Family Leptocylindraceae                              
Leptocylindrus danicus Cleve 31 V *   * * *   * * * * * * *
Leptocylindrus minimus Gran 76 R * * * * * * * * * * * * *
Class Flagilariophyceae                              
Order Fragilariales                              
Family Fragilariaceae                              
Asterionellopsis glacialis (Castracane) Round 5 A         *   * *       *  
Order Licmophorales                              
Familia Licmophoraceae                              
Licmophora sp. 1 A       *                  
Order Thalassionematales                              
Familia Thalassionemataceae                              
Thalassionema nitzschioides (Grunow) Mereschkowsky 5 A       *               * *
Class Bacillariophyceae                              
Order Naviculales                              
Family Phaeodactylaceae                              
Phaeodactylum tricornutum Bohlin 11 A               *     * * *
Family Diploneidaceae                              
Diploneis sp. 6 A       * * * *            
Family Naviculaceae                              
Complex Tropidoneis 3 A               *          
Family Pleurosigmataceae                              
Complex Pleurosigma/Gyrosigma 4 A   *                   * *
Order Thalassiophysales                              
Family Catenulaceae                              
Amphora sp. 1 A         *                
Order Bacillariales                              
Family Bacillariaceae                              
Complex C. closterium/Nitzschia longissima 7 A       * *                
Ceratoneis closterium Ehrenberg (=Cylindrotheca closterium) 97 R * * * * * * * * * * * * *
Pseudo-nitzschia "complex delicatissima" 14 A *   *   * *       *   *  
Pseudo-nitzschia "complex seriata 4 A               *   *   *  
Division DINOFLAGELLATA                              
Class Dinophyceae                              
Order Gymnodiniales                              
Family Gymnodiniaceae                              
Akashiwo sanguinea (K. Hirasaka) G. Hansen & Ø. Moestrup 6 A *                        
Amphidinium spp. 27 V * * * * * * *   *        
Gymnodinium spp. 6 A   *                      
Gyrodinium cf. spirale(Bergh) Kofoid & Swezy 2 A     *                    
Gyrodinium spp. 2 A     *                    
Order Gonyaulacales                              
Family Goniodomaceae                              
Alexandrium spp. 1 A *                        
Order Peridiniales                              
Family Peridiniaceae                              
Scrippsiella cf. spinifera G. Honsell & M. Cabrini 2 A *                        
Scrippsiella cf. trochoidea (Stein) Balech ex Loeblich III 31 V * * * *                  
Scrippsiella sp. 28 V *   * * * * * * *     *  
Family Congruentidiaceae                              
Protoperidinium cf. bipes(Paulsen) Balech 5 A     * * * *              
Protoperidinium cf. steinii (Jorgensen) Balech 1 A       *                  
Protoperidinium spp. 43 V * * * * * * *         * *
Order uncertain                              
Family Oxytoxaceae                              
Oxytoxum crassum Schiller 5 A *   *       *            
Oxytoxum cf. gladiolusStein 2 A         *   *            
Oxytoxum gracile Schiller 7 A   *   * * *     *        
Oxytoxum laticeps Schiller 3 A       *     *       *    
Oxytoxum scolopax Stein 2 A * *                      
Oxytoxum cf. turboKofoid 1 A         *                
Oxytoxum sp. 1 A   *                      
Order Dinophysiales                              
Family Dinophysiaceae                              
Dinophysis acuminata Claparede & Lachmann 9 A * * * * * *   *          
Dinophysis fortii Pavillard 3 A *                        
Dinophysis sp. 2 A *             *          
Family Oxyphysaceae                              
Oxyphysis oxytoxoides Kofoid 38 V * * * * * * *   *   *    
Order Prorocentrales                              
Family Prorocentraceae                              
Prorocentrum balticum (Lohmann) Loeblich 4 A *   *                 *  
Prorocentrum compressum (J. W. Bailey) Abe ex Dodge 2 A   * *                    
Prorocentrum dentatum Stein 1 A               *          
Prorocentrum gracile Schutt 5 A *                        
Prorocentrum micans Ehrenberg 47 V * * * * * * * *   * * * *
Prorocentrum minimum (Pavillard) J. Schiller 40 V * * * * * * * *   * * *  
Prorocentrum scutellum Schroder 2 A *                        
Prorocentrum triestinum J. Schiller 79 R * * * * * * * * * * * * *
Prorocentrum sp. 7 A         *   *   *     *  
Class Noctiluciphyceae                              
Order Noctilucales                              
Family Noctilucaceae                              
Pronoctiluca pelagica Fabre-Domergue 3 A *                   *    
Pronoctiluca spinifera (Lohmann) Schiller 2 A         *   *            
Division Chlorophyta 5 A   *     *                
Class Euglenophyceae 73 R * * * * * * *     * * * *
Eutreptiella sp. 1 A *                        
Division Cyanophyta                              
Class Cyanophyceae                              
Order Nostocales 67 R * * * *   * * * * * * * *
Order Oscillatoriales 91 R * * * * * * * * * * * * *

Richness, Abundance, Diversity Index and Evenness results are presented as the mean values of each sampling period, as the non-parametric tests revealed no differences (p < 0.05) between sampling stations. Table 2 presents information on these variables in each sampling period.

Table 2 Microphytoplankton (Total and by groups) Richness, Abundance and Ecological Indexes (Species Diversity and Evenness) from April 2011 to April 2012 

Date Richness Abundance Index
  Total Diatoms Dinoflagellates Cyanobacteria Chlorophythes Total Diatoms Dinoflagellates Cyanobacteria Chlorophythes Species Diversity Evenness
Apr1 18 4 12 1 1 35580718 10284643 24712437 410283 173355 0.44 0.15
Apr2 17 2 12 1 1 69754673 45297123 19789149 4639174 29226 0.44 0.15
May1 18 3 13 2 1 4107270 2244201 1392402 430008 40659 0.33 0.14
May2 12 2 6 2 2 6631668 4894936 360093 905809 470830 0.10 0.07
Jun1 19 6 10 2 1 18664938 17702565 189872 486232 286269 1.14 0.42
Jun2 20 5 13 1 1 10407854 9241535 93210 1051068 53111 0.94 0.34
Jul 23 10 11 2 1 56865758 56645156 118060 66902 35640 0.99 0.33
Aug 19 5 12 1 1 28571795 27728657 125740 439361 278036 0.11 0.04
Sep 18 5 9 2 1 13277285 12723868 286800 203216 63401 0.10 0.04
Oct 16 5 8 2 1 10212120 2486926 7372138 246037 107019 1.08 0.37
Nov 18 10 6 1   768861 718381 5652 46713   1.57 0.48
Dec 13 7 4 2   12459305 10876155 1569261 13889   0.16 0.07
Jan 9 3 4 2 1 2728105 1885932 531635 306591 3946 1.03 0.51
Feb 16 5 9 2 1 53614363 10990133 42197291 405632 21308 0.81 0.33
Mar 17 9 6 2 1 2168300 851195 1197935 109175 9996 1.07 0.40
Apr 15 7 5 2 1 1454119 345550 1008292 84125 16152 1.49 0.60

The richness distribution pattern (9 to 23 taxa) was highly correlated (p < 0.01) with dinoflagellates (r = 0.77) and diatoms (r = 0.50) which, together, represented 56 to 100% of the total number of taxa, while other groups’ contributions were low (< 3 taxa per sample). Richness values lower than the total average (17 ± 3 taxa) were registered in May, October and December 2011, and from January to April 2012. During the biweekly sampling period, only May presented a distinct (p < 0.05) phytoplankton assemblage, with a low richness of dinoflagellates in the second sampling of the month (Figure 3).

Figure 3 Total Microphytoplankton, Diatoms and Dinoflagellates Richness from April 2011 to April 2012. Dotted line indicates general mean of Total Richness. 

Variations in abundance (7.7 x 105 to 7.0 x 107cells.L-1) were correlated (p < 0.01) with high cell density of diatoms (R = 0.76) and cyanobacteria (R = 0.67). Values lower than the total mean (2.0 x 107 ± 2.2 x 107cells.L-1) were registered in most of the sampling periods (Figure 4). During the biweekly sampling period, differences (p < 0.05) were observed due to Diatom (April), Dinoflagellate (April and June), Cyanobacteria (May and June) and Euglenophycean (June) variability. Diatom abundances varied from 1.6 x 105 to 1.0 x 108 cells.L-1 (1.3 x 107 ± 1.9 x 107 cells.L-1), and this group was dominant in all sampling periods (mean contribution of 66%), except in April2 and October 2011 and February 2012. Cyanobacteria were represented by the Orders Oscillatoriales and Nostocales, showing abundances between 5.7 x 103 and 4.2 x 107cells.L-1 (6.3 x 106 ± 1.2 x 107cell.L-1). Amongst the cyanobacteria, the Order Oscillatoriales was the most numerous throughout the sampling periods, with an average contribution of 79%. The mean abundances of Dinoflagellates and Chlorophythes were of the order of 105 cells.L-1 and 104 cell.L-1, respectively, with an average contribution lower than 7%.

Figure 4 Total Microphytoplankton, Diatoms and Dinoflagellates Abundance (cell.L-1) from April 2011 to April 2012. Dotted line indicates general mean of Total Density. 

Community Structure

According to the Constancy analysis in the study area (Table 1), 78% of the taxa were categorized as ACCIDENTAL (49 diatoms; 36 dinoflagellates; 2 chlorophythes), 10% as RESIDENT (3 diatoms; 5 dinoflagellates, 2 cyanobacteria, 1 chlorophythe), and 12% as VISITORS (3 diatoms; 10 dinoflagellates).

The Shannon-Wiener diversity index varied between 0.10 and 1.57 bits.cell-1 (Table 2), with most values (56%) higher than the mean (0.74 ± 0.50 bits.cell-1; Figure 5). The lowest values were registered in April, May, August, September and December 2011, related to high abundances of certain taxa of Diatoms and Dinoflagellates. Pielou’s evenness varied from 0.04 to 0.60 (0.28 ± 0.18), following the same pattern as the diversity index (Figure 5).

Figure 5 Shannon-Wiener Species Diversity index (bits.cell-1) and Pielou's Evenness index from April 2011 to April 2012. Dotted line indicates general mean of Diversity index. 

A total of 42 taxa (19 diatoms, 19 dinoflagellates, 2 cyanobacteria and 2 chlorophythes) was defined by SIMPER analysis as the most representative (“typical”) in the study area (Table 3), for their contribution of up to 90% of the similarity between the samples of each sampling period. The taxonomic classes with the greatest contributions to the similarity between samples were the dinoflagellates (13-60%) and diatoms (13-55%) (Figure 6). Individual contribution to sample similarity by a singular taxon varied between 2 and 19% in each sampling period. We highlight unidentified cyanobacteria of the Order Oscillatoriales and Order Nostocales, diatoms Ceratoneis closterium (=Cylindrotheca closterium) and Leptocylindrus minimum and dinoflagellate Prorocentrum triestinum for their broad occurrence (> 80%) with high mean abundance (104-107cells.L-1) in many periods. Table 3 shows the high abundance of certain morphotypes with several shapes and dimensions between 20 and 150 µm (1 centric diatom, 4 pennate diatoms and 8 dinoflagellates) and brings out the need for taxonomic studies so that species that make a major contribution to community structure may be correctly identified.

Table 3 Simper analysis results showing average abundance (cell.L-1) of each taxon from April 2011 to April 2012. Values underlined represent taxa with contribution ≥ 10%. Taxa were ordered by the sum (Σ) of average abundance considering the entire sampling period. The Morphotypes are included. 

    2011 2012                            
  Σ Apr1 Apr2 May1 May2 Jun1 Jun2 Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr
DIATOMS                                  
Ceratoneis closterium 1.5 x 108 268795 45288034 2204603 4875816 4900030 6361924 34217077 27582734 12664516 375628   10722583 1450707 107327 15027 34250
Skeletonema cf. costatum 3.7 x 107         12054996 2771530 22341109                  
Leptocylindrus minimus 2.5 x 107 9827038   24869   488356 13543   97592   1992860 53319 124846 423125 10596338 690848 238276
Rhizosolenia setigera 4.2 x 105                   10755 377664 8050     12286 9575
Phaeodactylum tricornutum 2.7 x 105                           269895    
Guinardia sp. 1.7 x 105         135964 31867                    
Chaetoceros cf. social is 8.2 x 104                     82115          
Leptocylindrus danicus 4.3 x 104             13255       14908       14872  
Chaetoceros spp. 3.0 x 104                     29791          
Complex C. closterium/ Nitzschia longissima 2.2 x 104             22222                  
Pseudo-nitzsch ia " delicatissima complex" 2.2 x 104                 22107              
Thalassiosira sp. 1.7 x 104                     13311 3630        
Skeletonema sp. 1.1 x 104                 11087              
Complex Tropidoneis 1.2 x 103                     1222          
MORPHOTYPES                                  
Centric diatom (20-50 μm) 1.1 x 105     7062       20207 24962     61032 947       13048
Pennate diatom (linear; 50-100 μm) 5.9 x 104                             58953  
Pennate diatom (lanceolate; 20-50 μm) 2.3 x 104                 6174           16701  
Pennate diatom (linear; 100-150 μm) 1.6 x 104                             16464  
Pennate diatom (retangular; 20-50 μm) 4.7 x 104             4658                  
DINOFLAGELLATES                                  
Akashiwo sanguinea 4.2 x 106   4200474                            
Prorocentrum triestinum 8.2 x 105 51624 36760   30273 116844 254136 7780 119102 45344 93210 23541   23938 8681   10838
Prorocentrum micans 1.8 x 105 126192 6904       27087       18854            
Amphidinium spp. 1.4 x 105         99583 25759   12879                
Scrippsiella cf. trochoidea 1.2 x 105 11472 69601 5659   21244 15137                    
Protoperidinium spp. 1.2 x 105     9040   48597 18323 1398 29344 11884              
Prorocentrum minimum 8.5 x 104 15774         15402 13283 19120 21776              
Gymnodinium sp. 7.5 x 104       74887                        
Scrippsiella sp. 7.1 x 104               62937 4448   3495          
Oxyphysis oxytoxoides 5.2 x 104 15137   7252     5046 2158             22097    
Prorocentrum gracile 1.9 x 104 19279                              
MORPHOTYPES                                  
Order Gymnodiniales (oblong; 50-100 μm) 9.5 x 105   17898 220521 697083 15668                      
Order Gymnodiniales (oblong; 20-50 μm) 9.2 x 105 33460 52111 59541   47800 452506 9613 26024 23767 12348 7003     125478 44700 23412
Order Gymnodiniales (rounded; 20-50μm) 5.4 x 105 44135 130952 2002       2927 12083     1955 3946 266081 35513 30636  
Armoured cell (rounded; 20-50 μm) 5.3 x 105 25971 65873 14080 41427 64530 113923 8003 45941 47269 45012   1578 4998   29679 18309
Order Gymnodiniales (biconic; 20-50 μm) 1.5 x 105     3260     23369 1732             102592   18256
Armoured cell (oblong; 20-50 μm) 1.2 x 105 21510 29852 11468       4520 51119     3657          
Order Gymnodiniales (ovoid; 20-50 μm) 9.0 x 104                           72603 9079 8733
Order Gymnodiniales (biconic; 50-100 μm) 1.3 x 104     12957                          
CIANOBACTERIA                                  
Order Oscillatoriales 1.0 x 108 24710047 19786421 1383809 150570 165441 35850 107037 125740 141010 7271626 903 1536905 500332 42182297 1479714 921115
Order Nostocales 7.1 x 105     8593 209523 24431   11023   145790 100513   32356 31304 14994 43369  
CHLOROPHYTHES                                  
Unidentified Euglenoficeans 1.5 x 106 171761 29226 40659 402316 286269 53111 35640 242983 63401 107019       21308    
Unidentified Cloroficeans 6.9 x 104       68513                        

Figure 6 Percentual Contribution of phytoplankton groups determined by similarity percentage analysis (SIMPER). 

When compared with the Constancy index, SIMPER analysis was more effective in determining which taxa made a greater contribution to sample similarity in each period. The Constancy index just takes into account the occurrence of each taxon, while SIMPER considers abundance as well as occurrence. This could be observed for the diatom Skeletonema costatum classified as ACCIDENTAL by the Constancy index with occurrence in only 25% of the samples. However, this taxon was highlighted by SIMPER for its high mean densities (2.8 x 106 - 2.2 x 107 cells.L-1) that favored a contribution of up to 12% for the similarity of the samples for the periods of June1, June2 and July.

DISCUSSION

The microphytoplankton community of Guanabara Bay was characterized by typical estuarine and coastal species, influenced by a large number of multifactorial abiotic and biotic processes (LLEBOT et al., 2011; CLOERN; FOSTER; KLECKNER, 2014). Among all the factors that may affect the taxonomic composition and temporal variation of phytoplankton in Guanabara Bay are found: tidal cycle, seasonality of water masses of adjacent continental shelf, cold fronts and continental drainage (rainfall, inflow of domestic sewage, etc.)

The elevated number of taxa classified as ACCIDENTAL confirmed the high local hydrodynamism as being a consequence of the environmental factors mentioned above. The processes which caused such turbulence were probably responsible for the presence of benthic species (diatoms Paralia sulcata,Licmophora sp., Diploneis sp., Amphora sp.) along with planktonic ones (diatoms Leptocylindrus danicus, L. minimus, Thalassionema nitzschioides, Coscinodiscus spp., Pseudo-nitzschia spp., Skeletonema cf. costatum; Dinoflagellates Alexandrium sp.; Protoperidinium spp.) (RICARD, 1987; HASLE; SYVERTSEN, 1997). It is important to state that benthic microalgae are important primary producers in shallow aquatic ecosystems and that their production exceeds that of planktonic microalgae in certain periods (BERGESCH; ODEBRECHT; ABREU, 1995; BRANDINI; FERNANDES, 1996). The relevance of a taxon in the study area was determined by its high contribution to sample similarity in each season. Thus SIMPER analysis confirmed the representativity of “RESIDENT” taxa as well as the occasional contribution of others during the study period.

The organisms identified in the present study had already been observed in Guanabara Bay due to their wide distribution in the system (VILLAC; TENENBAUM, 2010). The low frequency and abundance of Skeletonema costatum called the authors’ attention since this diatom has been consistently reported as opportunist in eutrophic environments. This pattern change may be associated with the location of the sampling stations close to the bay’s entrance, a less polluted site due to the contribution of more saline, cleaner and clearer coastal water (SANTOS et al., 2007). Similar results were found by GUENTHER et al. (2012) in a short temporal scale investigation also in the entrance of Guanabara Bay during summer 2004, in which S. costatum was not considered an abundant taxon. Likewise, SANTOS et al. (2007) registered higher densities of this species in the inner portion when compared with the entrance of the bay. These outcomes suggest that the hydrodynamic conditions found in different areas of Guanabara Bay may exercise great influence on the representation of S. costatum. Another important aspect to be considered is that this diatom was the subject of a taxonomic review revealing that the genus biodiversity at any given place is most likely underestimated and may include more than one species (SARNO et al., 2007; KOISTRA et al., 2008). For instance, the morphology of Skeletonema species was examined in coastal waters of southern Brazil and the authors came to the conclusion that this genus is highly diverse in that geographical area, with the occurrence of four confirmed species: S. costatum, S. pseudocostatum, S. potamos and S. tropicum (BERGESCH; GARCIA; ODEBRECHT, 2009).

The recurrent observation of potentially harmful species in the bay requires some attention, specially concerning diatoms of the genus Pseudo-nitzschiadue to its ability to produce a powerful neurotoxin known as domoic acid (VILLAC; TENENBAUM, 2001; VILLAC; DOUCETTE; KACZMARSKA, 2010). Some studies have shown that Pseudo-nitzschia abundance is related to a major entry of nutrients into the water column (PARSON; DORTCH, 2002). Some other potentially harmful species were also found in Guanabara Bay, such as the diatoms Cerataulina pelagica, Leptocylindrus danicus, L. minimus and Dinoflagellates Akashiwo sanguinea, Oxyphysis oxytoxoides, Prorocentrum micans, P. balticum, Dinophysis acuminata, Scrippsiella cf. trochoidea (FRYXELL; VILLAC, 1999; HALLEGRAEFF; ANDERSON; CEMBELLA, 2003).

The average cell density (107 cel.L-1), described in this study, were higher than those found in other Brazilian coastal estuaries: Sepetiba Bay-RJ (104-106 cel.L-1; TENENBAUM et al. 2004), Estuary of Paraíba do Norte River-PB (103-106 cel.L-1; SASSI, 1991), Paranaguá Bay-PR (104-106cel.L-1; BRANDINI, 1985; BRANDINI; THAMM, 1994), São Sebastião Channel-SP (105-106 cel.L-1; GIANESELLA et al., 1999). However, studies in Guanabara Bay carried out between 1913 and 2004 showed similar values (105-109cel.L-1) (VILLAC; TENENBAUM, 2010). These differences may be related to different environmental conditions related to changes in time and space as well as to human intervention (artificial eutrophication, dredging, navigation, etc.).

Diatoms and dinoflagellates were the predominant groups and together were responsible for more than 96% of the specific composition, in accordance with the literature that indicates their predominance in Brazilian coastal regions (BRANDINI et al., 1997). The dominance of diatoms in shallow coastal regions reflects the instability of this environment, where turbulence homogenizes the water column, increases nutrient concentration in the euphotic zone and reduces cell sinking (MARGALEF, 1978; SMETACEK, 1988; LLEBOT et al., 2011). The high representativeness (40%) of chain-forming diatoms (species of Chaetoceros, Leptocylindrus, Hemiaulus, Skeletonema, Pseudo-nitzschia, Eucampia) has been related to estuarine and coastal environments (FERNANDES; BRANDINI, 2004; BÖTTJER; MORALES, 2005). According to REYNOLDS; PADISÁK and SOMMER (1993) this morphology provides a larger surface for light capture and represents an advantage over environments with high suspended solid concentrations. Laboratory assays also suggest that these organisms thrive in the environment as a result of a lower grazing pressure by microzooplankton (BODE et al., 2005).

The combination of different nutrition strategies (autotrophic and mixotrophic) may give dinoflagellates a competitive advantage over other organisms, even in the conditions of limited light that are very common in estuaries and river deltas (LALLI; PARSONS, 1993). Some taxa such as species of the genus Protoperidium and of the Order Gymnodiniales, considered heterotrophics (STEIDINGER; TANGEN, 1997), have also been frequently observed in samples. The high contribution of organisms of the Order Gymnodiniales to richness and abundance confirms VILLAC and TENENBAUM (2010) statement that Guanabara Bay dinoflagellates, although frequent and highly representative, are underestimated by virtue of the sampling and analysis procedures used in most of the studies. These dinoflagellates have extremely fragile cells that are deformed or destroyed by the commonly used fixative substances. So that a more precise identification of most taxa demands a different methodology from fixation to sample handling combined with the utilization of more advanced microscopy techniques with higher resolution.

The cyanobacteria, of the Orders Oscillatoriales and Nostocales, were also very important in phytoplankton’s attaining up to 99% of abundance in some samples. These results were expected and suggest that the increase in filamentous cyanobacteria density is a response to rainy periods and high levels of eutrophication (SANTOS et al., 2007; VILLAC; TENENBAUM, 2010).

The high concentration of euglenophyceans in the study area can be associated with inland polluted waters (LIMA; TENENBAUM; VALENTIN, 2010; GUENTHER et al. 2012), whereas these organisms require organically enriched water for growth (LEE, 2008).

The presence of the diatoms Proboscia alata, Rhizosolenia setigera, Hemiaulus membranaceus, Guinardia striata, Eucampia cornuta, Dactyliosolen phuketensisand the dinoflagellates Prorocentrum balticum, Pronoctiluca pelagica, Oxytoxum gracile indicates the influence of the Tropical Water that flows along the Brazilian continental shelf mixed with Coastal Water (HASLE; SYVERSTSEN, 1997; STEIDINGER; TANGEN, 1997).

The low diversity index (< 2.0 bits.cell-1), in 90% of samples, is a typical characteristic of systems in unstable equilibrium such as estuaries or polluted environments subject to local eutrophication (LLEBOT et al., 2011). Water mass enrichment processes first induce the proliferation of a reduced number of species and consequently a profound reduction in the species diversity index (MARGALEF, 1958; MARGALEF, 1980).

CONCLUSION

The composition and abundance of the phytoplankton of a certain region is certainly associated with the local hydrography. The interaction between water movements and phytoplankton organisms results from a combination of environmental factors. Thus the hydrodynamic properties of each region play an important role in the temporal variability and structure of phytoplankton populations (MARGALEF, 1978; ESTRADA; BERDALET, 1997). The information produced by this study will, therefore, add to knowledge of the Guanabara Bay system and will be useful for management purposes and also for the regulation of land use in the area surrounding the bay.

ACKNOWLEDGEMENTS

The authors would like to thank the Centro de Biologia Experimental Oceanus for field support and the provision of data. The authors are also grateful to their colleagues Priscila Kienteca Lange and Marcio Lincoln da Silva for their attention and kindness in translating this manuscript.

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