Estuarine, Coastal and Shelf Science 216 (2019) 98–109

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Estuarine, Coastal and Shelf Science

journal homepage: www.elsevier.com/locate/ecss

Trophic state of an urban coastal lagoon (northern Brazil), seasonal T

variation of the phytoplankton community and environmental variables
Marco Valério Jansen Cutrima,∗, Francinara Santos Ferreiraa, Ana Karoline Duarte dos Santosa,
Lisana Furtado Cavalcantia, Bethânia de Oliveira Araújoa,
Andrea Christina Gomes de Azevedo-Cutrimb, Jordana Adorno Furtadoa,
Amanda Lorena Lima Oliveiraa
a
Oceanography and Limnology Department, Federal University of Maranhão - UFMA. CEP, 65080-805, São Luís, MA, Brazil
b
Chemistry and Biology Department, State University of Maranhão - UEMA, CEP, 65055-000, São Luís, MA, Brazil

A R T I C LE I N FO A B S T R A C T

Keywords: Jansen Lagoon is an urban coastal area formed by damming the Ana Jansen Creek, which is located in the
Urban lagoon northwest of São Luis Island (northern Brazil) and is influenced by semidiurnal macro-tides. This study aimed to
Trophic index characterize the seasonal variation of the phytoplankton communities and its relationship with environmental
Phytoplankton variables to determine the trophic conditions in the Jansen Lagoon. Samples were collected bimonthly in five
Northern Brazil
fixed sites in 2011 and 2012 to analyze biological and physicochemical data. A total of 55 taxa were identified
including Bacillariophyta (25), Cyanobacteria (17), Chlorophyta (5), Charophyta (2), Euglenophyta (4) and
Miozoa (2). The Closterium setaceum, Pleurosigma elongatum e Oscillatoria sp3 occurrence had a positive corre-
lation with the higher rainfall period, increase in dissolved oxygen concentrations and nutrients (DIP and NO2−)
and elevated trophic levels (TRIX). Cyclotella stelligera and Microcystis aeruginosa were strongly correlated with
chlorophyll a concentration (microphytoplankton) under turbidity and wind speed influence. The trophic state
of Jansen Lagoon ranged from eutrophic to hypereutrophic according to the TRIX index, and this poor water
quality is explained by an intense eutrophication process in the rainy season due to elevated nutrient availability.
Hence, to change the scenario presented in this study the reduction of point and non-point sources is necessary to
slow down the eutrophication and growth of algal blooms in Jansen Lagoon.

1. Introduction
Coastal lagoons are dynamic and naturally stressed systems that
suffer frequent environmental disturbances and fluctuations. Therefore,
a high diversity of environments is included in the term lagoon, with
marked differences in size, morphology, trophic status and salinity,
which condition their biological assemblage structure, species compo-
sition, and fishing yield (Pérez-Ruzafa et al., 2007; Brito et al., 2010;
Pereira et al., 2012).
These environments offer very important ecosystem services (e.g.
recreational areas, tourist activities, and aquaculture) but are being
degraded worldwide (Christia et al., 2014; González et al., 2008;
Loureiro et al., 2005) by human activities associated with rapid urba-
nization (Scheren et al., 2004; Coelho et al., 2007; Cotovicz Junior
et al., 2012, 2013; Silva et al., 2017).
Population growth has led to an increase in waste production, which
has been causing an increase in nutrient inputs, especially nitrogen (N)
and phosphorus (P). Increased concentrations of N and P might result in
accelerated phytoplankton growth (Howarth and Marino, 2006; Brito
et al., 2012). Nutrient enrichment, therefore, is the primary symptom of
a system-based response process named eutrophication, which leads to
the deterioration of ecosystem health (Edwards et al., 2003; Devlin
et al., 2007; Hayn et al., 2014; Monteiro et al., 2016). The consequences
of eutrophication include accelerated growth of opportunistic algae,
shading of benthic primary producers, oxygen depletion and animal
death (Cloern, 2001; Glibert et al., 2010).
These impacts generate a call for the characterization and definition
of the current condition of these environments based on an ecosystem
and trophic approach (Cloern, 2001; Herrera-Silveira et al., 2009;
Smith and Schindler, 2009; Ferreira et al., 2011; Cotovicz Junior et al.,
2012). Over time, many methods and conceptual approaches have been
developed to assess the trophic state and eutrophication of aquatic

∗
Corresponding author.
E-mail address: cutrim@ufma.br (M.V.J. Cutrim).

https://doi.org/10.1016/j.ecss.2018.08.013
Received 5 September 2017; Accepted 15 August 2018
Available online 17 August 2018
0272-7714/ © 2018 Elsevier Ltd. All rights reserved.
M.V.J. Cutrim et al.
water bodies to support management purposes (Carlson, 1977;
Vollenweider et al., 1992; Primpas and Karydis, 2011; Bricker et al.,
1999).
In this type of environment, the cultural eutrophication scenario is
potentiated by seasonal events that increase surface drainage of nu-
trients into these water bodies (García-Pintado et al., 2007), especially
in highly-urbanized areas where there are no rivers (Yanez-Arancibia
et al., 2014.). Rainfall runoff also changes the physical and chemical
characteristics of water because of the freshwater input (Herrera-
Silveira et al., 2002; Coelho et al., 2007).
Eutrophication assessment and classification of coastal lagoons is
complex because of the large variability in spatial and temporal con-
ditions (Coelho et al., 2015). Lately, the trophic index (TRIX), proposed
by Vollenweider et al. (1998), has been used for assessing levels of
eutrophication of marine and transitional water bodies. This index is a
linear combination of the logarithms of four variables related to eu-
trophication: chlorophyll-α, mineral nitrogen, total phosphorus, and
percent deviation from oxygen saturation values. The TRIX assesses the
risks and impacts of eutrophication through useful metrics that clearly
record the destructive and deleterious effects of nutrient enrichment in
these environments (Pettine et al., 2007).
The current study intended to characterize the seasonal variation of
phytoplankton communities (chlorophyll a and phytoplankton abun-
dance) and its relationship with environmental variables (hydrological,
meteorological and physicochemical water) to assess the trophic state
and water quality in a tropical urban lagoon in north Brazil.
2. Material and methods
2.1. Study area
Jansen Lagoon is the result of successive anthropic changes in the
landscape. In the 1970s, the area was an estuarine region intersected by
streams (Jansen and Jaracati), with extensive mangrove cover. The
construction of roads in the late 1970s altered the drainage of the lo-
cality, due to an interception of the main drainage network of the
Jansen stream with the sea. The height of the avenue was above the
height of the terrain, which promoted the damming of the salt water
thus forming the lagoon.
The lagoon is located in the northwest of São Luis Island, between
the coordinates 02º29′08″S and 44º18′02″W, northern Brazil (Fig. 1),
covers 140 ha with an average depth of 1.5 m and is still surrounded in
the east by a mangrove forest. The lagoon maintains a connection to the
sea through a restricted inlet. The water flow between the lagoon and
Sao Marcos Bay is connected by two inlets (or outlets), where seawater
flows into the lagoon from the southwestern side through a canal
(115 m length and 3 m deep).
With regard to the climate, the region is hot and humid because it is
situated in the equatorial belt with equatorial air mass influence ori-
ginating in low-latitude regions where the southern boreal and trade
winds converge, as well as being subject to strong sunlight because of
its location in the low-latitude zone.
The rainfall data and wind speed were obtained from INMET (2013)
(National Institute of Meteorology). Within a 10-year rainfall time
series (2002–2012), the historical average was 1790.42 mm. During the
sampling period, an atypical pattern was observed with annual rainfall
amounts ranging from 995 mm (2012) to 2530 mm (2011), which was
the result of a combination of the effects of the El Niño–Southern Os-
cillation (ENSO; Rodrigues and McPhaden, 2014). In the state of Mar-
anhão, northern of Brazil, where Jansen Lagoon is located, the rainy
season begins in early January and lasts until June, with a wind speed
average corresponding to 2.4 m s−1. The month with the highest
number of rainy days was March with 19 days and 119 mm. The dry
season lasts from July to December, when the highest wind speed
average occurs (s (3.1 m s −1) (Rodrigues and Cutrim, 2010).
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Estuarine, Coastal and Shelf Science 216 (2019) 98–109
2.2. Sampling
Samples were collected bimonthly during the period from
November 2011 to September 2012 at five sites (L1–L5) during the
spring tides. All the sampling locations are near the margin of the la-
goon. L1 (2°30′03″S 44°18′18″W) is located in the southwest area of the
lagoon, which is influenced by a supply of salt water from the São
Marcos Bay. L2 (2°29′56″S 44°18′23″W) and L5 (2°30′12″S
44°18′04″W) are sites located in an area with a predominance of the
aquatic macrophyte Ruppia maritima. The L3 (2°29′40″S 44°18′13″W)
and L2 sites are affected by releases of domestic sewage without
treatment from the local neighborhood. L4 (2°30′07″S 44°17′40″W) is a
semi-closed area and one of the most stagnant ones, its margins are
composed by a mangrove area in an advanced state of degradation,
constituted by Rhizophora mangle and Avicennia germinans (Fig. 1).
The physical and chemical variables, including water temperature,
salinity and pH, were measured in the superficial water layer (50 cm
depth) with a multi parameter probe (HI-9828); depth was measured
with a digital echo sounder (Speedtech), water transparency with a
Secchi disk and turbidity with a turbidimeter 2020 (Turbidimeter). The
dissolved oxygen was determined by the chemical method of Winkler,
modified by Golterman et al. (1978), total phosphorus (TP) and am-
monium (NH4+) according to Koroleff (1983) and nitrate (NO3−) and
nitrite (NO2−) by the methods of Strickland and Parsons (1972); silicate
(SIO2−) and orthophosphate (PO4−) were determined as measured by
the method of Grasshoff et al. (1983). Dissolved inorganic nitrogen
(DIN) was obtained from the sum of NH4+-N, NO2−-N and NO3−-N,
dissolved inorganic silicate (DIS) from the SIO2− and for dissolved in-
organic phosphorus (DIP) only the PO4− was evaluated.
2.3. Phytoplankton composition, abundance and diversity
To analyze the structure of the phytoplankton community and the
phytoplankton abundance, sub-surface water samples (250 mL) were
collected with a Van Dorn bottle and fixed with Lugol solution. The
identification and counting of phytoplankton cells were carried out
with an inverted microscope at 400 × magnification, following
Utermöhl's technique (Utermöhl, 1958). At least 100 fields were
counted using deposited algae contained in 25 ml in each sample. The
phytoplankton community in each site was analyzed in terms of com-
position at the lowest taxonomic level, species richness (Margalef,
1958), diversity (Shannon and Weaver, 1963) and evenness (Pielou,
1966).
Taxonomic identification was conducted according to specialized
literature and for the updated nomenclature the Algaebase database
(Guiry and Guiry, 2016) was used. The frequency of occurrence was
expressed as a percentage, taking into account the number of samples in
which each taxon occurred, and the total number of samples was ana-
lyzed according to Mateucci and Colma (1982): F = N/n × 100, with F
= Frequency of occurrence, N = number of samples in which the taxon
occurred and n = total number of samples analyzed. The species were
grouped in the following categories; very frequent (F > 70%), frequent
(70% ≤ F > 40%), uncommon (40% ≤ F < 10%) and sporadic
(F ≥ 10%).
2.4. Phytoplankton biomass
The phytoplankton biomass was estimated by chlorophyll a con-
centration. Water samples (2 L) for chlorophyll a (mg m−3) determi-
nation were filtered through Whatman GF/F glass fiber filters and
pigment extraction was performed with 90% acetone. In order to se-
parate the microphytoplankton (> 20 μm) from the nanophytoplankton
(< 20 μm) group, chlorophyll sub-samples were passed through a
20 μm mesh, and then filtered. Pigment concentration was measured by
spectrophotometry (Parsons et al., 1984; Greenberg et al., 1992) and
calculations were done according to Strickland and Parsons (1972).
M.V.J. Cutrim et al.
Fig. 1. Location of the study area with sampling points (L1–L5), Jansen Lagoon, São Luís Island - Maranhão, Brazil.
2.5. Abundance–Biomass Comparison (ABC) curves
The relationship between biomass (chlorophyll a concentration) and
phytoplankton abundance was determined through
Abundance–Biomass Comparison (ABC) curves using PRIMER 6.0. ABC
curves were used to determine the level of disturbance in the phyto-
plankton community and whether this was caused by natural processes
or anthropogenic load. The indicator of this method was the W-statistic,
which is a measure of the difference between the abundance and bio-
mass lines on an ABC plot (Clarke, 1990; Clarke and Warwick, 2001). W
can have values ranging from −1 to 1, where values of close to or equal
to −1 indicate dominance in abundance (disturbed community), while
values of close to or equal to 1 indicate dominance in biomass (un-
disturbed community).
2.6. TRIX – trophic index
To characterize the trophic state of Jansen Lagoon, a multivariate
index called the Trophic State Index (TRIX) proposed by Vollenweider
et al. (1998) was used, which uses the values of chlorophyll a, the
dissolved oxygen saturation, the concentration of dissolved inorganic
nitrogen, and the total phosphorous concentration to quantify the es-
tuarine eutrophication. Thus, the extreme or discrepant values are ex-
cluded. The values were converted to the logarithmic base 10. Thus, the
TRIX determination for Jansen Lagoon is proposed by the following
formula:
log [Chla. aD%O. DIN . DIP ] − [k ]
TRIX =
m criminating species and their percentage contribution in relation to
100
Estuarine, Coastal and Shelf Science 216 (2019) 98–109
where Chla is chlorophyll a concentrations (mg.m−3); aD%O is absolute
deviation of dissolved oxygen saturation; DIN is dissolved inorganic
nitrogen and DIP is dissolved inorganic phosphate. The constants
k = 1.5 and m = 1.2 are scalar values introduced to adjust the lower
limit value of the index and to adjust the range of the related trophic
scale. Where k is the lower limits sum of the required variables for TRIX
and m is calculated by the difference between the lower and upper
limits of each variables, divided by 10.
Trophic scales and descriptors for water quality were adopted from
Giovanardi and Vollenweider (2004), Penna et al. (2004),
Nasrollahzadeh et al. (2008) and Cotovicz Junior et al. (2013). Nu-
merically, the index is scaled from 0 to higher than 8, covering a wide
range of trophic conditions from ultra-oligotrophic to hypereutrophic
(Table 1).
2.7. Statistical analysis
Multivariate statistical analysis was applied to environmental and
phytoplankton data to identify seasonal trends or discrete groups and
correlations between environmental and phytoplankton variables.
Significant differences in environmental variables and phytoplankton
data between the seasonal periods were tested individually using
parametric tests (One-Way ANOVA) or nonparametric tests (Kruskal-
Wallis), depending on whether normality and homogeneity of variances
were reached after logarithmic transformation (ln (x+1)) of data.
The similarity percentage analysis (SIMPER), was used to explore
the structure of the phytoplankton community through phytoplankton
abundance, in order to identify the groups of characterizing and dis-
M.V.J. Cutrim et al. Estuarine, Coastal and Shelf Science 216 (2019) 98–109

Table 1 (p > 0.05) and water transparency (p > 0.05) did not present sig-
Classification of trophic status for estuarine waters according to the trophic nificant seasonal differences, and homogeneity of these variables was
index (TRIX) model. observed during the study period. However, dissolved oxygen rates
TRIX Conditions Water Quality Trophic State (p < 0.05) and turbidity (p < 0.05) were higher during the rainy
season with significant differences between seasons.
<2 Water very poorly productive Excellent Ultra-Oligotrophic The DIN concentrations were higher during the dry season, with
and very low trophic status
NO3− as the most relevant nitrogenous compound and its pattern was
2–4 Water poorly productive and High Oligotrophic
low trophic status similar to the DIN variation. However, DIN, NO3− and NH4+ did not
4–5 Water moderately productive Good Mesotrophic show significant seasonal differences (p > 0.05), with stable values
and medium trophic status throughout the year. NO2− (p < 0.05) was significantly higher in the
5–6 Water moderate to very Moderate Mesotrophic to
rainy season. Likewise, TP (p > 0.05) and DIP (p < 0.05) showed
productive and high trophic Eutrophic
status
higher values in the rainy season. SIO2−2 (p > 0.05) was higher spe-
6–8 Water very productive and high Poor Eutrophic cifically in the dry season.
trophic status Regarding the Redfield ratio, seasonally the DIN:DIP ratio was
>8 Water highly productive and Very Poor Hypereutrophic higher in the dry season (51.30 ± 52.91 μmol L−1) than the rainy
highest trophic status
season (27.60 ± 29.01 μmol L−1). The DIS:DIP ratio was higher in the
dry season (87.10 ± 109.36 μmol L −1) as compared with the rainy
seasonal periods (dry and rainy seasons), and then the analysis of si- season (78.70 ± 101.09 μmol L −1). These ratios showed that more
milarity (ANOSIM) was applied to test the significance of the simila- than 70% of the samples had values superior to 16, revealing P lim-
rities in the phytoplankton community. Pearson correlation was used to itation. The DIN:DIS ratio also showed higher values in the dry season
correlate the environmental variables and TRIX index to biological data (1.23 ± 0,89 μmol L −1) than the rainy season (0.96 ± 0.91 μmol L
−1
(phytoplankton abundance and chlorophyll a). ), with 53% of samples presenting values lower than 1, indicating N
The multiple linear regression model analyses (GLM), with stepwise limitation.
backward selection of variables (using p < 0.05 as the inclusion and/
or rejection criterion), were applied to explore the relationships be- 3.2. Composition of phytoplankton community
tween the TRIX index and environmental variables, chlorophyll a and
phytoplankton abundance. The phytoplankton community was represented by 55 taxa dis-
From the predominant groups of species identified by SIMPER tributed in six divisions: Bacillariophyta (25), Cyanobacteria (17),
analysis and environmental variables with significant differences tested Chlorophyta (5), Charophyta (2), Euglenophyta (4) and Miozoa (2).
by ANOVA and Kruskal-Wallis, Canonical Correspondence Analysis Seasonally, the rainy season had a higher occurrence of taxonomic
(CCA) with forward selection using a Monte Carlo permutation test groups. The months of January and March registered six groups, while
(p < 0.001) was applied to investigate the relationship between the November presented only two. The diatoms (45.45%) were the most
biological and environmental variables and TRIX index. The sig- dominant group in the phytoplankton community, with the highest
nificance level used in all statistical tests was 95% (p < 0.05). These proportions in both seasons (rainy season: 38.18%; dry season:
analyses were undertaken using SPSS (version 19), Statistic (version 7) 27.27%), followed by Cyanobacteria (30.91%) with 25.45% in the
and PRIMER (version 6.1). rainy season and 23.63% in the dry season (Fig. 3 and Table 3).

3.3. Phytoplankton abundance and diversity indexes

3. Results
The phytoplankton abundance (p < 0.05) showed heterogeneous
3.1. Environmental variables distribution with significant seasonal variation in Jansen Lagoon. The
values ranged from 1924 ± 1432 × 10³ cells L−1 in the rainy season to
The characteristics of the estuarine waters of Jansen Lagoon are 4504 ± 3919 × 10³ cells L−1 in the dry season. The highest abun-
summarized in Table 2 and Fig. 2, with significant differences in en- dance (15,094 × 10³ cells L−1; L1 - Nov. 11) was obtained in the dry
vironmental variables occurring between the rainy and dry seasons. season (Fig. 4).
The water temperature (p > 0.05), pH (p > 0.05), salinity In the dry season, the most abundant species was Cyclotella stelligera,
which presented an algal bloom (35, 691, 618 cells L−1) in November
Table 2 2011. In the rainy season, Closterium navicula, C. setaceum, M. aerugi-
Seasonal variation of environmental variables in Jansen Lagoon, São Luís - nosa, Oscillatoria sp3 and Pleurosigma elongatum were the most abundant
Maranhão. (KW = Kruskal-Wallis). species (Table 3). All these species were classified as very frequent,
Variables Dry Rainy Anova KW occurring in > 75% of the samples analyzed. Phytoplankton showed
significant seasonal differences in terms of the ecological indexes
Mean ± SD Mean ± SD (Fig. 4). The diversity of species (p < 0.05) was very low with values
varying between 0.37 ± 0.21 bits cell−1 (dry season) and 0.92 ± 0.56
pH 8.89 ± 0.56 8.54 ± 0.40 0.075 –
Salinity (g Kg−1) 28.34 ± 5.82 24.50 ± 8.91 – 0.120 bits cell−1 (rainy season). Evenness (p < 0.05) ranged from
DO (mg L−1) 3.73 ± 1.43 7.05 ± 2.61 0.000* – 0.16 ± 0.09 (dry season) to 0.40 ± 0.20 (rainy season), which clas-
Water Temp. (Cº) 28.60 ± 1.07 28.53 ± 1.64 0.906 – sifies the community as having low homogeneity in its distribution.
Secchi (cm) 58.07 ± 16.45 49.07 ± 17.58 0.159 – Richness (p > 0.05) was very low, ranging from 1.19 ± 0.54 (dry
Turbidity (NTU) 10.79 ± 4.85 17.90 ± 22.39 – 0.000*
NH4+ (μmol L−1) 7.80 ± 3.42 7.65 ± 2.72 0.874
season) to 1.67 ± 0.84 (rainy season).
NO3− (μmol L−1) 23.22 ± 30.51 17.90 ± 22.39 – 1.00
NO2− (μmol L−1) 0.20 ± 0.06 0.87 ± 0.95 – 0.023* 3.4. Phytoplankton biomass – chlorophyll a concentrations
SiO2−2 (μmol L−1) 46.00 ± 32.92 41.16 ± 26.27 – 0.802
TP (μmol L−1) 5.73 ± 3.67 6.05 ± 4.26 – 0.917
Total chlorophyll a concentrations (p > 0.05) did not show sig-
DIN 32.67 ± 31.49 27.57 ± 23.39 – 0.588
DIP 0.73 ± 0.59 1.76 ± 1.43 – 0.043* nificant seasonal variations, with values ranging from
71.61 ± 96.74 mg m−3 in the rainy season to 74.64 ± 55.69 mg m−3
*Variables with significant difference. in the dry season. However, a significant chlorophyll a peak was

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M.V.J. Cutrim et al. Estuarine, Coastal and Shelf Science 216 (2019) 98–109

Fig. 2. Seasonal variation of environmental variables during the study period in Jansen Lagoon, São Luís Island - Maranhão.

Fig. 3. Percentage contribution of phytoplankton groups considering the entire study period in Jansen Lagoon, São Luís Island - Maranhão.

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M.V.J. Cutrim et al. Estuarine, Coastal and Shelf Science 216 (2019) 98–109

Table 3
Phytoplankton abundance and occurrence taxa (OC.) recorded during the dry and rainy seasons in Jansen Lagoon, where: VF - Very Frequent, F - Frequent, UC -
Uncommon, S – Sporadic. Total abundance (Total Abund.). Absent (−).
Taxa Dry Rainy

Nov/11 July/12 Sep/12 Total abund. Jan/12 Mar/12 May/12 Total abund. OC.

Cyanobacteria
Borzia sp. 101,078 – – 101,078 – 4813 – 4813 UC
Botryococcus sp. 67,385 – – 67,385 – – – – S
Chroococcus minor 9626 4813 86,638 101,077 – – – – F
Chroococcus turgidus – 4813 – 4813 – – – – S
Lynbya sp1 – – 4813 4813 14,440 – – 14,440 UC
Lynbya sp2 9626 – – 9626 – – – – S
Merismopedia elegans – – 4813 4813 4813 – – 4813 UC
Merismopedia tenuissima – 9626 – 9626 – 4813 – 4813 UC
Microcystis aeruginosa 320,081 24,066 19,253 363,400 375,433 86,638 19,253 481,324 VF
Microcystis sp. 9626 – – 9626 77,012 38,506 4813 120,331 F
Oscillatoria princeps – – – – 4813 – 4813 S
Oscillatoria sp1 70,754 – 4813 75,567 168,463 4813 – 173,276 F
Oscillatoria sp2 9626 – – 9626 24,066 96,265 – 120,331 F
Oscillatoria sp3 – 577,589 62,572 640,161 81,825 77,012 24,066 182,903 VF
Phormidium sp1 4813 – – 4813 – 9626 – 9626 UC
Phormidium sp2 14,440 – – 14,440 – – – – S
Phormidium sp3 – – – – 4813 – – 4813 S
Bacillariophyta
Amphora laevis – – 4813 4813 – – – – S
Amphora proteus – 4813 4813 9626 – – – – UC
Amphora sp1 9626 24,066 4813 38,505 – – – – F
Amphora sp2 – – – – 24,066 19,253 – 43,319 UC
Entomoneis alata – – 4813 4813 – – – S
Eunotia sp. – 4813 – 4813 – – – S
Chaetoceros sp. 4813 – – 4813 – – – S
Cyclotella stelligera 35,691,618 18,376,303 6,262,025 41,972,019 1,111,858 – 1,054,100 – VF
Gyrosigma balticum – 4813 – 4813 4813 – 4813 9626 F
Navicula sp1 9626 48,132 – 57,758 129,957 52,946 – 182,903 F
Navicula sp2 – 4813 19,253 24,066 4813 19,253 – 24,066 F
Nitzschia fasciculata – – – – 52,946 – – 52,946 S
Nitzschia longissima – 245,475 – 245,475 86,638 14,440 4,226,025 101,078 F
Nitzschia obtusa – – – – – 33,693 – 33,693 S
Nitzschia pacifica – – – – 14,440 – – 14,440 S
Nitzschia sigma – – – – – 4813 – 4813 S
Nitzschia sp. – – 24,066 24,066 14,440 – – 14,440 UC
Odontella longicruris – – 4813 4813 – – – – S
Pleurosigma elongatum – 14,440 4813 19,253 24,066 91,452 4813 120,331 VF
Pleurosigma sp1 – 38,506 28,879 67,385 – 462,071 144,397 606,468 F
Pleurosigma sp2 – – – – – 14,440 – 14,440 S
Synedra ulna – 9626 33,693 43,319 24,066 48,132 – 72,198 F
Thalassionema frauenfeldii – 9626 14,440 24,066 14,440 19,253 – 33,693 F
Thalassiosira nanolineata – – 19,253 19,253 28,879 – – 28,879 UC
Thalassiosira rotula – – – – 962,648 – – 962,648 S
Chlorophyta
Ankistodesmus falcatus – – – – – 24,066 14,440 38,506 UC
Dimorphococcus lunatus. – – 4813 4813 – – – – S
Oedogonium sp. – – – – 14,440 4813 4813 24,066 F
Oocystis sp. – – – – 14,440 – – 14,440 S
Sphaeocystis sp. – – – – – 134,771 9626 144,397 UC
Miozoa
Protoperidinium sp. – – – – – 52,946 – 52,946 S
Peridinium sp. – – – – 428,378 – – 428,378 S
Euglenophyta
Euglena oxyurus – 14,440 4813 19,253 – – – – UC
Euglena acus – 43,319 33,693 77,012 19,253 14,440 – 33,693 F
Euglena sp. – 4813 4813 9626 – – – UC
Phacus curvicauda – 4813 4813 – – – – S
Charophyta
Closterium navicula – 24,066 134,771 158,837 67,385 206,969 – 274,354 F
Closterium setaceum – 1,824,220 – 1,824,220 322,487 12,023,474 5,193,485 322,487 F

observed in March 2012 with 363.2 mg m−3 (Fig. 5). The micro- seasonal differences (Fig. 5).
phytoplankton fraction (p < 0.05) showed significant seasonal differ-
ences, with a greater contribution in the dry season
(39.65 ± 42.75 mg m−3) in relation to the rainy season 3.5. Abundance–Biomass comparison (ABC)
(8.57 ± 9.38 mg m−3). For the nanophytoplankton fraction
(p > 0.05), the values ranged from 34.99 ± 24.43 mg m−3 (dry The level of disturbance in the phytoplankton community, whether
season) to 62.97 ± 91.13 mg m−3 (rainy season), with no significant caused by natural processes or anthropogenic load, was determined by
phytoplankton abundance and biomass-abundance/biomass

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Fig. 4. Seasonal variation in abundance values of phytoplankton (cells L−1), diversity (bits cell−1), and evenness and richness indexes in Jansen Lagoon, São Luís
Island - Maranhão.

Fig. 5. Seasonal variation of the total chlorophyll a and fractional (mg m−3) components in Jansen Lagoon, São Luís Island - Maranhão.

Fig. 6. Abundance–Biomass comparison (ABC) curve by ranked species at Jansen Lagoon, São Luís - Maranhão.

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Fig. 7. Classification of Jansen Lagoon according to the application of the trophic state index (TRIX).

comparison plots (ABC-plots). The W index, visible on the graphs, is a
practical measure of the trophic status of the particular area. W index
negative values, indicating a eutrophic condition and polluted ecosys-
tems, were recorded in both seasons (dry and rainy seasons). Thus,
Jansen Lagoon is characterized as a stressed environment
(W = −0.24), where opportunistic species such as Microcystis aerugi-
nosa and Oscillatoria sp3 are dominant in both seasons. This disturbance
condition is more pronounced during the rainy season (W = −0.26),
with a tendency to moderate stress during the dry season
(W = −0.023) (Fig. 6).
3.6. TRIX – trophic state index
The trophic state index (TRIX) ranged from 6.47 (dry season -
September 2012) to 10.89 (rainy season – March 2012), with mean
values of 8.04 ± 1.41. According to the relationship between the
trophic scale and descriptors for water quality, the Jansen Lagoon
waters changed from poor water quality with very productive water
and a high trophic status (TRIX: 6–8 eutrophic) to very poor water
quality with highly productive water and the highest trophic status
(TRIX: > 8 hypereutrophic) (Fig. 7). Throughout the year, among the
thirty samples analyzed, 50% had poor water quality while 50% had
very poor quality. Significant differences between seasons was not re-
ported (p > 0.05).
3.7. Statistical analysis
The SIMPER analysis of phytoplankton species abundance showed
86.75% as the average similarity of similar species (characterizing)
responsible for formation of groups in both seasonal periods in the
present study (Table 4). The results revealed that the dry season had a
higher similarity (44.45%) of characterizing species in comparison to
the rainy season (42.30%). The main group in the dry season comprised
the diatom Cyclotella stelligera as the predominant species (65.06%),
followed by Oscillatoria sp3 (5.99%), Microcystis aeruginosa (5.33%) and
Closterium navicula (4.29%). In the rainy scenario, Closterium setaceum
(35.87%), Cyclotella stelligera (23.29%), Microcystis aeruginosa (7.71%)
and Pleurosigma elongatum (7.51%) had higher contributions.
In relation to dissimilar species (discriminating), the SIMPER ana-
lysis showed an average dissimilarity of 68.25% and identified
Cyclotella stelligera, Closterium setaceum, Microcystis aeruginosa,
Pleurosigma elongatum as discriminating species that differentiate the
groups of species between the sampling months. The formation of
groups observed was confirmed by ANOSIM analysis with significance

Table 4
Phytoplankton characterizing species that contributed to the average similarity within each seasonal period and discriminating species with mean abundances of
species that contributed to the maximum dissimilarity between the assemblages in Jansen Lagoon.
Characterizing species Av. Abund Av. Sim Contrib% Cum.%

Dry season Average similarity: 44.45% Cyclotella stelligera 41.8 28.92 65.06 65.06
Oscillatoria sp3 8.37 2.66 5.99 71.05
Microcystis aeruginosa 7.02 2.37 5.33 76.37
Closterium navicula 5.83 1.91 4.29 80.67
Chroococcus minor 4.88 1.73 3.89 84.55
Closterium setaceum 7.66 1.18 2.65 87.21
Pleurosigma elongatum 4.03 0.89 2.01 91.39

Rainy season Average similarity: 42.30% Closterium setaceum 27.31 15.17 35.87 35.87
Cyclotella stelligera 17.76 9.85 23.29 59.15
Microcystis aeruginosa 9.17 3.26 7.71 66.86
Pleurosigma elongatum 8.56 3.18 7.51 74.37
Oscillatoria sp3 7.21 2.8 6.61 80.98

Discriminating species: Average dissimilarity: 68.25% Av. Abund Dry season Av. Abund Rainy Season Av. Diss Contrib% Cum.%

Cyclotella stelligera 41.8 17.76 9.5 13.91 13.91

Closterium setaceum 7.66 27.31 9 13.19 27.1
Microcystis aeruginosa 7.02 9.17 3.16 4.63 31.73
Pleurosigma elongatum 4.03 8.56 3.06 4.49 36.22
Nitzschia longissima var. longissima 3.26 6.34 3.06 4.48 40.7
Oscillatoria sp3 8.37 7.21 2.93 4.3 45
Closterium navicula 5.83 3.8 2.51 3.68 48.68

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M.V.J. Cutrim et al. Estuarine, Coastal and Shelf Science 216 (2019) 98–109

Table 5 increase of dissolved oxygen concentrations, nutrients (DIP and NO2−)

Model accounting for the observed variation in the TRIX index in Jansen and elevated trophic levels (TRIX). Cyclotella stelligera and Microcystis
Lagoon according to the results of the multiple linear regression model analyses aeruginosa were strongly correlated with chlorophyll a concentrations
(GLM) with stepwise backward selection of variables (number of cases = 30; (microphytoplankton) under turbidity and wind speed influence. In
Adjusted Squared Multiple R = 0.97).
addition, these species were negatively correlated with lower nutrient
Variable Coefficient Std. Error Tolerance t p-level concentrations and reduced trophic levels in the dry season. In the same
season, the abundance of Closterium navicula was influenced by higher
NO3 0.648 0.043 0.432 15.206 0.000
wind speed. The relationship among the species group, TRIX index and
TP 0.145 0.038 0.538 3.797 0.001
DIP 0.186 0.040 0.487 4.638 0.000 environmental variables was statistically significant (Monte Carlo test;
Wind −0.221 0.040 0.503 −5.599 0.000 p < 0.001).
Chlorophyll a 0.155 0.047 0.356 3.295 0.003
Phytoplankton −0.117 0.034 0.671 −3.433 0.002
abundance
4. Discussion

Jansen Lagoon is influenced by multiple sources of stress, both

of the similarity (Global R = 0.418; p = 0.1%).
natural and anthropogenic. These factors overlap sometimes but show
Regarding the Pearson correlation, chlorophyll a concentration
seasonal patterns that are governed by the very well defined climatic
showed a strong positive correlation to nanophytoplankton (0.92),
structure in Maranhão (Azevedo et al., 2008; Rodrigues and Cutrim,
TRIX index (0.75), DO (0.66) and NO3− (0.64). NO3−showed high
2010). Among the environmental and biological data, dissolved oxygen,
correlation to DIN (0.99). Likewise, phytoplankton abundance was
turbidity, nutrient concentration (NO2− and DIP), phytoplankton
correlated to Cyclotella stelligera (0.77), and Closterium setaceum to rain
abundance and microphytoplankton were correlated with the seasonal
(0.80), NO2− (0.80) and DO (0.61). In addition, the seasonal pattern
variations. This seasonal change has been evidenced in Jansen Lagoon
showed that the rain was correlated positively to NO2− (0.92) and DO
as well as in other coastal ecosystems (Meng et al., 2017; Coelho et al.,
(0.83), and the wind was correlated negatively to rain (−0.70) and DO
2015; Pérez-Ruzafa et al., 2007; Monteiro et al., 2016; Duarte et al.,
(−0.71).
2006). Owing to its semi-closed morphology, the climatologic regime
The multiple linear regression model analyses (GLM) with backward
(rainfall and wind speed) and wastewater discharge are the main fac-
selection of variables show that the values of the TRIX index depend on
tors that drive the condition of the variables. Moreover during the
nutrient concentrations (nitrate, total phosphorous and dissolved in-
spring tides and rainy season, there is a greater water exchange in the
organic phosphorous), wind, chlorophyll a and phytoplankton abun-
Jansen Lagoon.
dance (Adjusted Squared Multiple R = 0.97). The nutrient concentra-
In coastal lagoons, the variability in environmental factors is a
tions and chlorophyll a showed a positive relationship, while wind and
consequence of the interaction of multiple abiotic variables and phy-
phytoplankton abundance had a negative correlation (Table 5).
toplankton (Srichandan et al., 2015). Dissolved oxygen concentrations
The Canonical Correspondence Analysis (CCA) was performed with
in the lagoon showed the lowest values in the dry season mainly due to
seven environmental variables that were significantly influenced by
the highest algae abundance and wind speed presented during this
seasonality and the TRIX index. The data obtained from the CCA
season. In contrast, the rainy season led to well oxygenated water with
showed a separation into two groups, which explained 74.13% of the
the highest values registered in March 2012, as a result of the increase
relationships between species and environmental variables (Fig. 8). The
in chlorophyll a concentration together with a peak of Closterium seta-
first axis explained 47.52% of the correlations while the second axis
ceum.
contributed 26.61%.
Dissolved oxygen in aquatic ecosystems has been conditioned by
The Closterium setaceum, Pleurosigma elongatum e Oscillatoria sp3
many physicochemical variables, which govern its solubility.
occurrence had a positive correlation with the higher rainfall period,
Obviously, oxygen solubility increases as salinity and temperature

Fig. 8. Canonical correspondence analysis with phytoplankton and environmental variables. Phytoplankton: M. aeruginosa (Microcystis aeruginosa), Oscillatoria sp3
(Oscillatoria sp3), C. navicula (Closterium navicula), C. setaceum (Closterium setaceum), C. stelligera (Cyclotella stelligera), P. elongatum (Pleurosigma elongatum).
Environmental variables: Rain. (rainfall), DO (dissolved oxygen concentration), NO2 (nitrite concentration), DIP (Dissolved inorganic phosphorus concentration), NTU
(turbidity), Chla-Micro (microphytoplankton), Wind (wind) and TRIX (Trophic Index).

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M.V.J. Cutrim et al.
decrease, which could be the reason for the low DO concentration in the
dry season. In addition, important biological processes are associated
with oxygen distribution, such as photosynthesis, respiration, and de-
composition (Srichandan et al., 2015). Usually in coastal lagoons the
occurrence of algal blooms is followed by eventual oxygen depletion in
the water column and it allows us to associate the quantitative varia-
bility of the phytoplankton as descriptor of environmental stress
(Domingos et al., 2012).
The chlorophyll a concentrations showed the nanophytoplankton
(< 20 μm) as the most determinant phytoplankton fraction and did not
show seasonal variation. In addition, a correlation between phyto-
plankton abundance and biomass was not observed due to a greater
contribution of this smaller fraction of phytoplankton. Similar results
were also registered by Srichandan et al. (2015), Azevedo et al. (2008)
and Rodrigues and Cutrim (2010). Together with phytoplankton bio-
mass, elevated phytoplankton abundance, with values higher than
1.5 × 106 cells L− 1, may be considered as useful tools for assessing the
ecological quality of aquatic systems (Brito et al., 2012; Coutinho et al.,
2012), emphasizing the use of phytoplankton as an indicator of an-
thropic activities and eutrophication events.
The results showed that the magnitude of the bloom events in-
creased linearly with the rainfall amount. As a consequence of such
events, the chlorophyll a peak was probably stimulated by the enrich-
ment of nutrients in water column (Meng et al., 2017). According to
Pérez-Ruzafa et al. (2007), comprehension of the hydrological and
geomorphological factors is extremely important for the determination
of ecological characteristics of coastal lagoons working as a response to
the fluctuation of environmental disturbances.
The richness index showed the predominance of diatoms in Jansen
Lagoon, as well as in other tropical lagoons (Adesalu and Nwankwo,
2009; Adelasu and Kunrunmi, 2012). In the case of the studied lagoon,
this is favored by the proximity and connectivity with the marine in-
fluence of São Marcos Bay (Azevedo et al., 2008; Rodrigues and Cutrim,
2010). This dominant phytoplankton group is well adapted to eutrophic
conditions under natural and human impacts as reported by Laruste
et al. (2016) and Hemraj et al. (2017). However, the high abundance of
diatoms did not prevent the formation and development of M. aerugi-
nosa blooms during the dry season that were associated with chlor-
ophyll a concentration (Yunes et al., 1996; Rodrigues and McPhaden,
2014) under turbidity and wind speed influence.
The resuspension and recirculation of the aquatic environment
caused by the local hydrodynamics are important in determining the
algal blooms. Factors such as the intensity of mixing of the water
column because of the low depth and its influence on the water
transparency and spatial-temporal variations can interfere directly in
the structure and composition of the phytoplankton community.
The phytoplankton abundance in Jansen Lagoon is similar or su-
perior to the values found in Brazilian coastal lagoons with a eu-
trophication process and phytoplankton blooms (e.g. Conceição Lagoon,
Patos Lagoon, and the Estuarine-Lagoon Complex Mandaú-Manguaba)
(Silva et al., 2017; Abreu et al., 1995; Cotovicz Junior et al., 2012).
According to Castro et al. (2016), HABs are classified into two cate-
gories based on their negative impacts. The first type is related to the
loss of water quality caused by an excessive increase in turbidity and
dissolved oxygen depletion with no toxic substance production. The
second type includes the blooms of harmful algae that produce toxins
and other metabolites.
In Jansen Lagoon, the phytoplankton growth may be limited by
phosphorous concentrations, as the N:P ratio was higher than the ex-
pected Redfield ratio (16:1) and this was also found in the Almargem
coastal lagoon (Coelho et al., 2007). This is a specific situation, as ni-
trogen is usually the limiting nutrient in coastal environments. In
coastal areas, N and P are rarely found in high concentrations yet they
are sufficient to support the simultaneous development of a great
variety of species. Thus, the capacity of seeking limiting nutrients is
fundamental to the preferential proliferation of species (Castro and
107
Estuarine, Coastal and Shelf Science 216 (2019) 98–109
Moser, 2012).
In this current study, the mean annual values of the TRIX Index
characterize Jansen Lagoon as a hypereutrophic environment with le-
vels between 7 and 8, indicating poor water quality and higher trophic
levels particularly in the rainy season. This seasonal variation depends
on the elevated nutrient amount (N03-) and chlorophyll a concentra-
tions, where the dynamics of the environment were insufficient to re-
move excess nutrients in the water column in the rainy period
(Monteiro et al., 2016). However, the decrease in rainfall reduced the
nutrient availability in the dry season with the lowest trophic levels
registered in this season.
The high levels of eutrophication shown in Jansen Lagoon indicate
that the seasonal variation contributes to the intensification of the
scenario effected by human influence (e.g., sewage effluents) and ex-
ternal factors. Higher nutrient amounts may be related to urbanization
processes and industrial activities leading to a high level of eu-
trophication (Béjaoui et al., 2016; Silva et al., 2017; Flores-Montes
et al., 2011; Pérez-Ruzafa et al., 2007). Thus, the very poor water
quality found in Jansen Lagoon is essentially due to the high nutrient
availability (García-Pintado et al., 2007; Yanez-Arancibia et al., 2014;
Hayn et al., 2014; Monteiro et al., 2016).
For Jansen Lagoon, the TRIX index did not cover a wide range of
trophic conditions. This was also observed in eutrophic coastal lagoons
in different countries worldwide (Coelho et al., 2007; Pérez-Ruzafa
et al., 2007; Béjaoui et al., 2016; Brito et al., 2012), and may be ex-
plained by several factors. In contrast to coastal lagoons in Brazil, the
Estuarine-Lagoon Complex Mandaú-Manguaba (Cotovicz Junior et al.,
2012) registered a wide variation in trophic levels, with lower levels in
the dry season because of the higher marine influence, and the Con-
ceição Lagoon (Silva et al., 2017) showed trophic scales varying from
oligotrophic to hypereutrophic conditions in response to local hydro-
dynamics.
In the European Union the Water Framework Directive (WFD) is
used as a tool to assess water quality (EC, 2000), which establishes
several biological elements to determine the ecological state of water
bodies, including the phytoplankton community (Coutinho et al.,
2012). In Brazil, the resolution number 357/2005 (article 24) of the
National Environment Council (CONAMA, 2005) classifies water bodies
and establishes some limits and restrictions for water use depending on
the current water quality, however, there is no systematic monitoring of
the trophic state and water quality by local authorities. Hence, this
study shows that surely a continuous assessment followed by effective
corrective actions for infractions would contribute to a decrease in
pollution in coastal lagoons under intense process urbanization.
In this study, the applicability of the TRIX index, was relevant,
however, might be considered the restrict lagoon-sea water exchange
observed in Jansen Lagoon. In addition, the proposal of a specific cri-
teria of classification in relation to the TRIX index and water quality
should be considered to increase the index efficiency (Coelho et al.,
2007; Salas et al., 2008).
5. Conclusion
The seasonality affected the environmental variables, favoring the
presence of a phytoplankton community usually found in shallow and
semi-closed environments with deteriorating water quality. However,
the increase in nutrients of anthropogenic origin contributed to the
growth of Cyclotella stelligera, Microcystis aeruginosa, Oscillatoria sp3,
Closterium navicula and C. setaceum, as well as increased the local
trophic state, leading to a scenario of ecological instability. Therefore,
tropical environments favor algal blooms, and the reduction of point
and non-point sources is necessary to slow down the eutrophication and
growth of algal blooms in Jansen Lagoon. Without adequate mitigation
measures, future use of the lagoon and its resources by the population
will be compromised.
M.V.J. Cutrim et al.
Acknowledgements
The authors acknowledge the Foundation for Research and
Scientific and Technological Development of Maranhão - Brazil, Grant
Number BM-006776/11 (FAPEMA - Fundação de Amparo à Pesquisa e
ao Desenvolvimento Científico e Tecnológico do Maranhão- Brasil) for
financial support.
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