Dissolved inorganic nutrients and chlorophyll a in an estuary receiving ...
Environ Monit Assess (2013) 185:5387–5399 DOI 10.1007/s10661-012-2953-x
Dissolved inorganic nutrients and chlorophyll a in an estuary receiving sewage treatment plant effluents: Cachoeira River estuary (NE Brazil) Maria Aparecida Macêdo Silva & Gilmara Fernandes Eça & Danielle Felix Santos & Alonso Góes Guimarães & Michelle Coêlho Lima & Marcelo Friederichs Landim de Souza
Received: 15 March 2012 / Accepted: 8 October 2012 / Published online: 24 November 2012 # Springer Science+Business Media Dordrecht 2012
Abstract Sampling was conducted monthly during a transition period between the dry and rainy seasons in order to evaluate the effectiveness of a municipal sewage treatment plant (STP) in eutrophication control. STP
effluent and fluvial input data were also estimated. In the dry period, high concentrations of nutrients, chlorophyll a (up to 360 μgL−1), and anoxia in bottom waters were observed in the upper portion of the estuary. Nitrate was
M. A. M. Silva : G. F. Eça : D. F. Santos : M. C. Lima : M. F. L. de Souza (*) Programa de Pós-Graduação em Sistemas Aquáticos Tropicais, Laboratório de Oceanografia Química, Universidade Estadual de Santa Cruz—UESC, Rod. Ilhéus-Itabuna km 16, 45650-000 Ilhéus, BA, Brazil e-mail: [email protected]
Present Address: G. F. Eça Programa de Pós-Graduação em Química, Universidade Federal da Bahia, Instituto de Química, Laboratório de Oceanografia Química, Rua Barão de Geremeoabo, s/n, Campus Universitário de Ondina, 40.170-115 Salvador, BA, Brazil
M. A. M. Silva e-mail: [email protected] G. F. Eça e-mail: [email protected] D. F. Santos e-mail: [email protected] A. G. Guimarães Programa Regional de Pós-Graduação em Desenvolvimento e Meio Ambiente, Universidade Estadual de Santa Cruz—UESC, Rod. Ilhéus-Itabuna km 16, 45650-000 Ilhéus, BA, Brazil Present Address: M. A. M. Silva Programa de Pós-Graduação em Oceanografia Biológica, Laboratório de Fitoplâncton e Microorganismos, Universidade Federal do Rio Grande FURG, Av. Itália, Km 08, 96201-900 Rio Grande, RS, Brazil
Present Address: D. F. Santos Instituto Federal de Educação, Ciência e Tecnologia da Bahia—IFBA, Porto Seguro, BA, Brazil
Present Address: A. G. Guimarães Faculdade de Tecnologia e Ciências—FTC, Itabuna, BA, Brazil
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scarce during the dry months, although high concentrations were observed at the river sources and the upper estuary. The N:P and Si:P molar ratios were usually below 16:1, and the Si:N ratio was higher than 1:1. The fluvial inputs were a greater source of nutrients to the estuary than the STP, but nutrient loading by these effluents were also important in contributing to the eutrophication of the upper estuarine zone, especially in the dry season when symptoms were more intense. Keywords Brackish water pollution . Sewage treatment . Denitrification . Nutrient loading . Tropical environment . Northern Brazil
Introduction Estuaries are of biological and socioeconomic importance and are characterized by high rates of primary productivity and biomass. These systems, which occur at the continent/ocean interface, receive, process, and export/import large amounts of organic matter and/or nutrients from natural and anthropogenic sources. Estuaries are dynamic environments that are subject to wide variations in physical, chemical, and biological characteristics. This variability leads to complex reactions and phase changes of the materials present in the water (Davies and Eyre 2005; Divya et al. 2009). However, when the natural and anthropogenic nutrient load to these systems exceeds the assimilation capacity for production, eutrophication and degradation of the water quality can occur (Boyd 2001; Boyer et al. 2002; Rabalais 2002). The primary producers are the first components of ecosystems to respond to increases in nutrient concentrations. The structure and function of phytoplankton can change, causing excessive increases in the population and consequent decreases in the concentration of oxygen during decomposition. These changes can even lead to hypoxia or anoxia in the water column (Millie et al. 2004). Secondary effects of the increase of phytoplankton biomass include blooms of harmful algae, enhanced turbidity, diminished light penetration, and loss of submersed vegetation. These changes lead to a collapse of ecosystem functioning, specifically, a loss of habitat and biodiversity, and a displacement of trophic chains (Rabalais 2002). Marti et al. (2004) note that sewage treatment plants (STP) have improved water quality, but problems associated with
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sewage discharge remain. These problems include difficulties in controlling nonpoint sources, removal inefficiencies of nutrients in STP, and increases in populations and residues. In developing countries, most STPs only conduct a primary treatment and convert organic matter to dissolved inorganic nutrients (Pereira-Filho et al. 2003). These nutrient-rich effluents can cause eutrophication, especially in systems with a high water residence time. Nutrient limitation by nitrogen, phosphorus, and silicon can occur along the salinity gradient and can affect primary productivity and the accumulation of phytoplankton biomass (Rabalais 2002). If the actual concentrations are also considered, the stoichiometric ratio of N, Si, and P postulated by Redfield for marine and coastal environments (16:16:1) can be used to determine which nutrient limits phytoplankton productivity (Smith 1984). Nitrogen is likely the major cause of eutrophication in most coastal systems, especially in pristine systems (Rabalais 2002), but other nutrients, such as phosphorus and silica, can also limit primary production in some systems (Howarth and Marino 2006; Jennerjahn et al. 2004). The excess phosphorus in estuaries can influence cycling and the availability of nitrogen and dissolved silica, thus negatively affecting the community structure of primary producers. Agricultural activity and urbanization in some regions has likely increased N fluxes to the coast (Howarth and Marino 2006). Anthropogenic impacts in the watersheds, such as deforestation, soil erosion, and dam construction, can also alter the DIN:DIP, DSi:DIN, and DSi:DIP ratios and affect phytoplanktonic community structure in coastal waters dominated by diatoms (Jennerjahn et al. 2004). The objective of this work was to determine the concentrations and temporal/spatial distribution of dissolved inorganic nutrients and chlorophyll a in an estuarine system subject to in natura and treated sewage during a transition period between the dry and rainy seasons.
Materials and methods Study area The Cachoeira River estuary is located in the south of Bahia State, Northern Brazil (Fig. 1). The drainage
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basin of the Cachoeira River has an area of approximately 4,600 km2. The total population in the basin is approximately 600,000 inhabitants, who are primarily concentrated in the cities of Itabuna and Ilhéus (approximately 200,000 inhabitants live in each). Cocoa cultivation, livestock, and pasture activities constitute the main land use in this region (BAHIA 2001). The predominant tropical humid climate in the area is demonstrated by an annual average temperature of 24.6 °C and an annual precipitation of between 1,500 and 2,000 mm (Klumpp et al. 2002). The rain and fluvial discharges are characterized by extreme irregularities, with ill-defined dry and rainy seasons. The annual average fluvial discharge is 24.1 m3 s−1, with historical records showing values between 0.2 and 1,460 m3 s−1 (BAHIA 2001). Lima et al. (2010) observed an increase in discharge from 0 to 826 m3 s−1 in the period from 2003 to 2004. During the dry season, the river presents an extensive development of floating aquatic macrophytes, which are carried to the estuary and coastal waters during flooding episodes (Souza 2005). The estuarine area is approximately 16 km2, including an area of mangroves of approximately 13 km2 (Souza 2005). Semidiurnal tides reach heights of approximately 2 m. The inner portion of the estuary receives the effluents of a STP, which conducts a primary level treatment of part of the domestic sewage from the city of Ilhéus. These effluents present high dissolved inorganic nutrient concentrations. The release of untreated domestic effluents is also widespread in outer estuarine areas. The city of Itabuna releases untreated sewage and treated industrial effluents into the Cachoeira River approximately 10 km upstream of the estuary, which are transported into the estuary as fluvial inputs. Sample collection and analytical producers Water sampling was carried out in November and December of 2003 (the dry season), January and February of 2004 (the transition period), and March of 2004 (the peak of the rainy season). Samples were collected at ten points with Van Dorn bottles in surface, mid depth, and bottom waters according to depth (Fig. 1). pH, dissolved oxygen, salinity, and temperature were measured in the field with portable digital meters. The samples were filtered using fiberglass filters of type GF/C. The concentrations of dissolved inorganic
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nutrients (ammonium, nitrite, nitrate (DIN), and phosphate (DIP)) were determined according to Grasshoff et al. (1983), while the silicate (DSi) concentration was established using the method of Carmouze (1994). Total suspended solids (TSS) were determined using a gravimetric method (Strickland and Parsons 1972). Chlorophyll a was analyzed using a spectrophotometric method (Parsons et al. 1984). Inputs of dissolved inorganic nutrients from the STP and the river The fluxes of dissolved inorganic nutrients (FY) from the STP and the Cachoeira River were obtained by multiplying the values of the concentration of each inorganic nutrient by the discharge of STP effluent and the river at a monthly time scale. The following formula was used in this assessment: FY ¼ ½Y plant Qplant where [Y]plant and Qplant represent the concentration of each nutrient and the monthly discharge of the STP, respectively. The nutrient loadings in the Cachoeira River were obtained from Lima et al. (2010).
Results Hydrochemical characteristics The inner reaches of the estuary presented saline stratification during the dry period and the beginning of the rainy period, while the outer section was more mixed vertically. Salinity was high in the dry period, varying from 34 to 36 in the outer estuary and from 13 to 30 in the inner portion (Table 1). The salinity decreased along the entire estuary in February, reaching a maximum value of 13. In March, the high input of freshwater almost entirely flushed the estuary (S00), and salinity values were only recorded at Station 4f (S0 33.0). This anomalous value was likely due to the retention of denser water with a higher salinity (~36) in a depression of approximately 10 m depth near this station. The temperature varied from 25.5 to 33.9 °C, with the higher values measured at the inner reaches of the estuary during the dry period. The pH exhibited values between 7.23 and 8.83, with higher values occurring in surface water samples
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Fig. 1 Map of the study area showing the location of sampling stations in the Cachoeira River estuary
during the dry period. The inner portion of the estuary exhibited lower pH values in most of the months sampled. During the dry period, dissolved oxygen concentrations in surface samples in the inner estuary varied from 12.2 to 17.4 mgL−1, while values from 0.00 to 4.40 mgL−1 were observed in bottom samples. During the rainy season, the dissolved oxygen concentrations varied from 0.00 to 8.31 mgL−1 in the inner estuary and from 5.20 to 6.80 mgL−1 in the outer estuary (Table 1). Ammonium concentrations in the dry and transition periods presented high values, ranging from 35 to 50 μmolL−1 (Fig. 2). However, samples below the detection limit were also observed during the dry period. Ammonium values were higher in the inner estuary and in the bottom samples. In the rainy period, the maximum concentration of ammonium was 21 μmolL−1, while nitrite presented maximum concentrations of 3.5 μmolL−1 in the study period. The higher values were observed in November and March and in surface samples. In January, nitrite was undetectable. In November, high concentrations of nitrate were observed in the inner portion of the estuary, with a maximum value of 87 μmolL−1, while concentrations were lower than the detection limit in the outer estuary. In December, the entire estuary presented concentrations of nitrate that were lower than the detection limit. The concentrations of nitrate in the
estuary increased in the rainy season but did not exceed 16.0 μmolL−1. Phosphate concentrations in the inner portion of the estuary varied from 0.40 to 18.0 μmolL−1 in the dry period, while values in the rainy period varied from 7.54 to 13.0 μmolL−1. In the outer estuary, minimum and maximum values of 0.44 and 2.27 μmolL−1 were observed throughout the study (Fig. 3). Silicate was observed in the inner portion at concentrations of 87.6 μmolL−1 in the dry season, while concentrations observed during the transition and rainy periods varied from 0.56 to 214 and from 57.3 to 229 μmol sL−1, respectively. Concentrations of silicate were lower in the outer estuary and coastal regions, with a minimum value of 1.59 and a maximum value of 96.7 μmolL−1 (Fig. 3). High chlorophyll a concentrations were observed in the inner portion of the estuary (November0133 μg L−1 and December0368 μgL−1). In the rainy season, the concentrations of chlorophyll a were lower in the inner estuary, varying from 0.94 to 79.0 μgL−1. The chlorophyll a concentrations in the outer estuary and at the coastal station were similar, with a minimum value of 0.9 and a maximum value of 2.74 μgL−1 (Fig. 4). The highest concentrations of TSS were observed in the dry season (11.2 to 341 mgL−1) in the inner portion of the estuary, followed by the outer portion of
36.4±0.24 (36.2–36.8)
16.6±2.60 (13.5–20.9)
Outer
Inner
26.2±1.0 (26.2–29.0)
31.4±1.02 (30.2–32.7)
Outer
Inner
8.09±0.56 (7.34–8.83)
Inner
5.98±0.18 (5.76–6.20)
6.14±0.11 (6.00–6.25)
7.25±6.88 (0.00–17.4)
Coastal
Outer
Inner
DO (mgL−1)
8.20±0.02 (8.17–8.22)
8.22±0.02 (8.20–8.25)
Coastal
Outer
pH
28.4±0.18 (28.6–28.1)
Coastal
T (°C)
36.8±0.34 (36.2–37.1)
Coastal
S
November
6.74±6.18 (0.00–15.9)
6.92±0.71 (5.97–7.54)
6.83±0.90 (5.55–7.66)
8.21±0.42 (7.76–8.83)
7.97±0.33 (7.31–8.17)
8.02±0.12 (7.80–8.15)
31.6±1.65 (29.1–33.9)
28.1±0.46 (27.8–29.0)
27.3±0.80 (26.2–28.3)
23.6±4.78 (18.8–30.9)
36.1±0.90 (34.4–36.8)
36.8±0.23 (36.4–37.0)
December
4.15±2.66 (0.00–8.31)
6.01±0.10 (5.88–6.10)
6.10±0.07 (6.06–6.18)
7.81±0.46 (7.23–8.69)
8.18±0.03 (8.15–8.22)
8.17±0.05 (8.13–8.22)
29.6±0.82 (28.2–30.6)
26.6±0.43 (26.2–27.1)
29.6±0.82 (28.2–30.6)
18.5±9.78 (0.90–30.0)
35.9±0.80 (34.8–36.6)
36.5±0.00 (36.5–36.5)
January
Table 1 Mean, standard deviation, and range (in brackets) of the physicochemical variables in Cachoeira River estuary
4.15±2.07 (1.34–6.37)
5.88±0.36 (5.20–6.21)
6.04±0.10 (5.93–6.13)
7.85±0.24 (7.55–8.12)
8.16±0.06 (8.09–8.24)
8.17±0.11 (8.05–8.25)
30.2±0.73 (28.8–30.7)
28.1±0.28 (27.7–28.5)
26.8±0.26 (26.6–27.1)
35.6±0.95 (34.5–36.2)
33.3±4.23 (24.3–36.1)
35.6±0.95 (34.5–36.2)
February
7.13±0.22 (6.75–7.32)
6.90±0.51 (6.60–7.80)
8.06±0.01 (8.05–8.07)
7.53±0.05 (7.49–7.61)
7.56±0.34 (7.35–8.17)
8.24±0.12 (8.16–8.33)
27.5±1.63 (26.4–28.7)
26.0±0.67 (25.5–27.1)
27.5±1.63 (26.4–28.7)
0.00±0.00 (0.00–0.00)
7.30±14.8 (0.00–33.7)
33.6±0.42 (33.3–33.9)
March
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5392 Fig. 2 Mixing diagram of ammonium, nitrite, and nitrate during the dry, transition, and rainy seasons
Fig. 3 Mixing diagram of phosphate and silicate during the dry, transition, and rainy seasons
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Fig. 4 Concentration of chlorophyll a and total suspended solids (TSS) along a salinity gradient during the dry, transition, and rainy seasons
the estuary (6.78 to 109 mgL−1). In the rainy season, TSS values during the month of February ranged from 7.2 to 9.0 mgL−1 (Fig. 4). Stoichiometric ratios The DIN:DIP ratios were usually below 16:1 (0 to 12; Table 2). Ratios higher than 16:1 were observed in the outer estuary in November (27), in the inner portion of the estuary in January (19), and at the coastal station in March (31). The DSi:DIN ratio was usually higher than 1:1, with values varying from below 1 to as high as 150. The DSi:DIP ratio was generally lower than 11. Higher values of this ratio were observed at the inner portion of the estuary in January (values of 8 to 21) at all estuary and coastal stations in February (values of 4 to 43) and at the coastal station in March (values of 13 to 35; Table 2). Inputs of dissolved inorganic nutrients from the STP and the river Fluvial inputs of nutrients to the estuary are shown in Table 3. The largest inputs of nutrient occurred in March 2004, which coincided with the period of the greatest fluvial discharge (Table 3). Despite the low discharge observed in November 2003, fluvial fluxes of nutrients were higher in this month than in December. December
and January of 2003 were marked by an increase in nitrate inputs from the STP, which reached values that were equal to and more than twice the values of the fluvial inputs, respectively. The fluvial inputs of nitrate, nitrite, phosphate, and silicate were higher than the fluxes from the STP during most of the study period. Notable exceptions included the inputs from the STP of phosphate in December (21.0×103 molmonth−1), of ammonium during the dry period (22.0 to 250×103 mol month −1 ), and of nitrate in January (5 × 10 3 mol month−1), which were higher than the fluvial inputs.
Discussion The high water residence time observed in December (Guimarães 2006) and the salinity distribution in the inner portion of the estuary indicate that the tide was the main physical hydrological force acting on the estuary during the dry period. The intrusion of salt water and the small fluvial discharge resulted in saline stratification in the inner portion of the estuary during the dry months but showed a negligible water residual flow or mixing. This stratification was intensified in the beginning of the rainy period due to the increase in fluvial discharge. The stagnation of the water was associated with the sources of nutrients, such as the input of treated
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Table 2 Mean, standard deviation, and range (in brackets) of the stoichiometric ratios in Cachoeira River estuary November
December
January
February
March
N:P Coastal
7.9±5.7 (0.1–16)
1.5±3.5 (0.0–8.8)
5.2±1.7 (3.6–7.0)
7.4±4.6 (2.6–12)
31±0.6 (30–31)
Outer
8.5±9.6 (2.7–28)
0.0±0.0 (0.0–0.1)
2.2±157 (0.5–4.8)
10±4.6 (5.0–18)
4.1±3.5 (2.2–10)
Inner
5.4±3.6 (1.2–12)
0.3±0.4 (0.0–1.q)
7.4±6.2 (1.8–19)
7.3±0.6 (6.4–8.0)
2.6±0.5 (1.7–3.0)
Si:P Coastal
6.3±2.0 (4.4–9.4)
2.2±0.4 (1.9–3.1)
5.5±1.4 (4.2–7.0)
18±12 (11–32)
24±15 (13–35)
Outer
6.5±2.6 (3.1–9.8)
6.1±1.9 (4.2–8.5)
7.4±2.3 (4.6–11)
24±16 (3.7–43)
5.7±1.8 (4.1–8.2)
Inner
7.6±1.7 (5.2–9.4)
2.4±2.6 (0.1–5.9)
14±4.5 (8.3–21)
30±3.7 (26–37)
6.9±1.4 (5.2–8.2)
Si:N Coastal
10±23 (0.5–57)
190±303 (0.26–796)
1.2±0.7 (0.8–1.9)
3.2±2.0 (0.9–4.7)
0.8±0.5 (0.4–1.1)
Outer
1.4±0.9 (0.3–2.9)
120±42 (91–150)
2.2±1.57 (0.5–4.8)
2.2±1.3 (0.7–3.4)
1.7±0.6 (0.8–2.3)
Inner
2.0±1.2 (0.7–4.3)
2.2±0.1 (1.0–1.2)
7.4±6.2 (1.8–19)
4.1±0.5 (3.4–4.9)
2.7±0.4 (2.0–3.1)
ammonium and nitrite in the coastal stations denote a local source of sewage or a resuspension of the sediments. In the rainy period, the input of material from the drainage basin and the washing of the inner estuarine portion resulted in an increase of nutrient concentrations in the outer portion of the estuary. The low nutrient concentrations observed in the inner portion of the estuary during this period suggest the dilution of those nutrients due to the large amount of fresh water in the system. In February, the nearly linear distribution of nutrients along the salinity gradient indicated that the mixture between the salt water and fresh water was fast and did not allow for the expression of nonconservative processes (Uncles et al. 2003). Assimilation by primary producers was likely the process by which ammonium in the Cachoeira River estuary is removed during the dry period, especially in the inner portion of the estuary. The plot of chlorophyll a
sewage from the STP and fluvial sources. High concentrations of nutrients occurred despite the low fluvial discharge, which resulted in an increase of nutrients and chlorophyll a concentrations in the inner portion of the estuary during the dry period. The remineralization of the organic matter from fluvial and STP inputs explain the deficit of oxygen and the value of the pH observed in the bottom waters. The hypoxia in the bottom waters is characteristic of stratified and eutrophic environments. These environments present a high biological demand of oxygen in the bottom waters and sediments, which can be accentuated in the summer because of high temperatures (Lin et al. 2006). In the dry period, the outer portion of the estuary presented little exchange with the inner portion, which was richer in nutrients. This and the intrusion of seawater can explain the low values of nutrient and chlorophyll concentrations observed in the outer portion of the estuary. Higher concentrations of
Table 3 Monthly inputs of dissolved inorganic nutrients by the municipal sewage treatment plant (STP) and fluvial station (103 mol month−1) November
NH3/NH4+
January
February
STP
Rivera
STP
Rivera
STP
Rivera
STP
22.0
17.8
250
0.33
250
30.2
NO2−
0.80
NO3−
3.70
PO43−
35.0
H3SiO−
82.0
a
December
5.42 470 58.5 691
Data from Lima et al. (2010)
March Rivera
0.00
38.2
0.58
0.12
1.60
4.81
0.00
30.4
1.40
1.46
4.70
1.77
0.00
21.0 140
1.86 15.6
7.90 84.0
2,080
STP
Rivera
170
5,100
1.30
562
4.10
5,100
119
0.00
329
16.0
3,440
837
0.00
1,940
32.0
31,700
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Fig. 5 Relationship between nitrate and chlorophyll a (a), ammonium (b), and dissolved oxygen (c) in a November 2004 survey
versus nitrate in the November survey (Fig. 5a) demonstrated a decrease in nitrate concentrations and an increase in chlorophyll a from the fluvial source towards the sea in the surface waters up to Station 7. The low
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concentrations in the outer portion of the estuary were due to internal processes in the estuary and likely to the intrusion of coastal waters with a lower nutrient content, since mixing between the inner and outer estuaries was negligible at this time (Guimarães 2006). The denitrification process could also remove nitrate in the inner portion of the estuary. Low oxygen concentrations observed in November, December, and January at Stations 7, 8, and 9 in bottom samples might have favored that process. An inverse relationship between nitrate and ammonium can be observed along the surface at Stations 7 and 8, and in bottom waters at Stations 7 to 9 in November (Fig. 5b). Stations BV and 9 s showed different trends fits outside, mainly because the former represents the fluvial input and the latter reflects the influence of the STP input under the high tide conditions occurring during the sampling. A linear regression between nitrate and ammoniacal nitrogen was used to verify the possible occurrence of denitrification at these stations. This analysis presented an r value of 0.81, suggesting the occurrence of denitrification in this area. A strong linear correlation (r00.90) between nitrate and dissolved oxygen was also observed in November, when the surface waters of Stations 7 to 8, and bottom waters of Stations 7 to 9 were considered (Fig. 5c). In principle, the oxic conditions at the other stations were not suitable for denitrification. However, some authors describe that denitrification can occur, although infrequently, in the presence of higher concentrations of dissolved oxygen in the water (Paerl and Pinckney 1996; Robertson and Kuenen 1992; Vidal et al. 2002). Particulate material in suspension can develop anoxic microzones where denitrifying action by anaerobic bacteria can occur in aquatic systems (Paerl and Pinckney 1996). Studies have shown that aquatic macrophytes can also stimulate denitrification because they easily trap organic debris from the water column or liberate organic carbon through their roots. Fecal pellets have also been recognized as sites of intense microbial activity, which result in a high demand of oxygen and favor denitrification close to the surface of oxic sediments (Herbert 1999). There is an intense growth of floating macrophytes occurring along the fluvial portion of the Cachoeira River during the dry season, which are transported to the estuary in variable amounts during higher discharge episodes (Klumpp et al. 2002; Souza 2005).
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Sedimentation can also explain the removal of nitrate from the River Cachoeira estuary during the dry period. In spite of removing less nitrogen than the processes discussed above, sedimentation can represent an important mechanism of nitrogen removal, especially during periods of high water residence time (Boyd 2001; Tappin 2002), as observed in the study area during November and December of 2003. The phosphate concentrations in the inner portion of the estuary might have been primarily influenced by external sources, but contributions from sediment fluxes may also have been important. The high water residence time in the dry period probably favored the recycling of phosphate, thus increasing the concentration of phosphate in the water column. The regeneration of phosphorus in the sediment is described as an important process that contributes to the input of phosphorus in the estuary (Davies and Eyre 2005), mainly during the dry period when the internal processes are most expressive. In the rainy period, the smallest assimilation of the phytoplankton and the input of sewage and fluvial discharge may explain the phosphate concentrations in February, particularly in the outer portion of the estuary and in the sea, where the chlorophyll concentrations were low. The apparent removal of phosphate in the outer portion of the estuary in December was related to the adsorption of phosphate in particles of minerals and organic material in suspension or the pseudoremoval of phosphate due to dilution of water with low concentrations of phosphate. In the rainy period, the removal of phosphate in the inner portion of the estuary was likely due to consumption by phytoplankton and adsorption. During the dry period, benthic regeneration can be a significant source of silicate for the estuary. In this period, continental drainage was not an important source of this nutrient in the estuary due to the low fluvial flow. Benthic dissolution of the biogenic silica was observed in an Australian tropical estuary (Eyre and Balls 1999) that originated from fresh water and was the main source of silicate during the rainy period. Moreover, in the present study, the removal of the silicate in the dry period in the inner portion of the estuary indicates assimilation by the diatoms. In higher salinity areas, decreases in silicate can be due to the dilution of this nutrient. Data from a regression of silicate on chlorophyll in December showed that silicate removal was due to assimilation by diatoms, except at Stations 7s and 8s, where the high chlorophyll concentrations did not
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correlate with silicate, suggesting that other groups of phytoplankton were responsible for these chlorophyll concentrations. In many estuarine systems, diatoms are among the main factors influencing chlorophyll concentrations (Millie et al. 2004). The maximum chlorophyll a concentrations observed in this study were higher than those observed previously in this same system (Souza 2005). This author found concentrations that were below or close to the detection limit up to maximum values, which were between 39 μgL−1 and 64 μgL−1 in May 2001 and in August 2001, a period of low discharge (Fig. 6a). The sampling surveys made during this previous study were conducted 5 and 11 months after the STP became operational (in September 2000) and more than 2 years before the present study, but a causal relationship between sewage management and eutrophication can be speculated. The maximum chlorophyll a concentrations found in the low discharge period in 2003 were higher than those found in 2001 during the same hydrological conditions. Chlorophyll a in 2003 reached concentrations up to threefold the maximum recorded in 2001. The higher chlorophyll a concentrations (outliers) were observed at the inner estuary in November and December 2003 and coincided with high concentrations of oxygen, high pH, and phytoplanktonic biomass at the surface, suggesting that the removal of the dissolved inorganic nutrients was predominantly due to primary production. The outer estuary presented lower concentrations than those observed in 2001 (boxes), probably due to the lower availability of dissolved nutrients after removal at the inner estuary. The total solids in suspension during the dry months and at the beginning of the rainy period in the present study primarily originated from autochthonous material. The dispersion graphs for the dry period showed higher TSS concentrations in the outer portion of the estuary and in the bottom samples, which suggests the occurrence of sediment resuspension. The STP and diffuse points of sewage inputs were probably additional sources of particulate matter, mainly in the inner portion of the estuary. The low DIN:DIP molar ratio, especially in the dry season, can be associated with the biogeochemical removal of nitrogen and mainly the high availability of phosphorus in relation to nitrogen. The molar DIN: DIP ratio could imply the nitrogen limitation of primary production in the outer estuary during the dry
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Fig. 6 Chlorophyll a (a) and phosphate (b) concentrations measured in the surveys carried since 2000 in Cachoeira River estuary. Asterisk not analyzed
period, when DIN concentrations were low. In the inner portion of the estuary, high chlorophyll concentrations indicated that low DIN:DIP values did not affect the phytoplankton, since nutrients were largely available. A deviation in the molar ratio does not indicate that phytoplankton are nutrient-limited (Smith 1984). Larger amounts of a nutrient in relation to another nutrient can cause a deviation in the molar ratio without affecting the phytoplankton nutrient supply. The DIN:DIP molar ratio observed (Souza 2005) in the inner portion of the River Cachoeira estuary was low during 2001 (with a value of approximately 13) but very high in February of 2000 (with a value of 344). This same author observed that increased concentrations of phosphate in this system, which have occurred since February 2000 (before the STP became operational; Fig. 6b), caused low values of the DIN:DIP and DSi:DIP molar ratios after September
2001 (the beginning of the STP operation). Similar results were also found in the current study. These low concentrations of phosphate, near or below detection limit were not observed since February 2000. The median value remained almost constant after September 2000, but the general increase of high concentrations and the upper 75th percentile can be attributed to STP operation. Aside from the high availability of phosphate, the removal of dissolved silica by the diatoms during the dry period could also explain the observed values of the DSi:DIP molar ratio. In February and March 2004, the higher Si: DIP values in the inner portion and coastal station might reflect the fluvial input of silicate and a decrease in assimilation by the phytoplankton due to turbidity. The DSi:DIN ratio found in this study indicated that the productivity of the diatoms was not limited by the availability of dissolved silica.
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During the dry season, the low freshwater input is enough to create salt stratification of the water column in the upper estuary, but with low mixing with the outer portion. This allows for accumulation of the nutrient and organic matter loading from the STP in this area, in addition to fluvial inputs. The high nutrient content in the surface photic layer increases phytoplanktonic biomass, consumes dissolved nitrogen and phosphorus, and produces dissolved oxygen supersaturation. The respiration of organic matter in the bottom waters promotes anoxic conditions, favoring the occurrence of denitrification on the oxic/anoxic interface. The consumption of nitrate by phytoplankton assimilation and denitrification generates an excess of phosphate with high chlorophyll a concentrations. As fluvial discharge increases, vertical mixing and export of this material to the outer estuary occurs, dispersing the phosphate along the entire estuary but with chlorophyll a concentrations somewhat lower due to light limitation. In the peak of the rainy season, chlorophyll a concentration remains low but with higher phosphate concentrations from the leaching of the drainage basin soils.
Conclusion During the dry period, the high water residence time, large inputs of nutrients and organic matter by treated sewage and fluvial discharge, and estuarine morphology were responsible for forming two compartments of distinct characteristics inside the system. The inner estuarine presented characteristics of eutrophic waters, which were very different from those observed in the outer estuary. During the rainy period, due to the increase in the fluvial contribution and the low water residence time, mixing and transport processes were dominant. During this period, the drainage basin is the main source of dissolved inorganic nutrients and particulate matter to the estuary. This resulted in the increase of the nutrients in the outer portion of estuary and possibly an export to coastal waters. The DIN:DIP ratio and the low concentration of ammonium and nitrate in the outer part of the estuary indicated phytoplankton limitation by nitrogen, especially in December. The fluvial inputs of nutrients, mostly originated from effluents of Itabuna City, which represented an important contribution to the estuary. However, the
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STP discharge can provide an important source of ammonium, nitrate, and phosphate during the dry period. In addition, these effluents also contribute to dissolved and particulate organic N and P that can be remineralized. The high nitrate concentrations found in November were mainly due to external sources such as STP and fluvial inputs. The large removal of nitrate in the estuary was likely not only due to assimilation by primary producers but also due to denitrification in sediments and anoxic bottom waters. There was an increase of phosphate concentrations and a decrease of DIN:DIP ratio after the STP became operational. Extreme values of chlorophyll a were observed at the inner estuary but lower concentrations at the outer portion, compared with samplings made in 2001, both during the dry season. This is an indication that the STP increased eutrophication at the inner estuary, and this effect is more acute during the dry season. It is important that these results be taken into account by environmental managers, especially in developing countries where there is a growing awareness of the need to treat domestic sewage. The option to release the effluents at the inner estuarine area instead of constructing a submarine outfall is frequently considered due to political, logistical, and economic reasons. It was not possible to evaluate the impacts of the STP with a proper sampling design including a time series before and after the beginning the STP became operational. However, the results of this and a former study shows that changes in the nutrient concentrations and stoichiometric ratios, chlorophyll a concentrations, and the intensity of anoxia in bottom waters were at least partially caused by the release of effluents from this STP, especially during the dry season. The planned construction of a dam in the Cachoeira River to supply water for the city of Itabuna would increase these effects during the dry season. Acknowledgments We thank Dr. D. M. L. Silva (UESC) for the valuable comments and suggestions on the text and also thank Mr. R. R. Cavalcanti for his help during sampling. M. A. M. Silva would like to thank FAPESB for the IC grant and CAPES, CNPq/CTHidro for the grant supporting her master studies. M. Lima and G.F. Eça would like to thank CNPq for the PIBIC grant. In addition, M.F.L. Souza thanks CNPq for the PQ grant, proc. number 350286/2000-0. We also thank CADCT/BA (public notice PRODOC) and PROPP/UESC for providing financial support to the project entitled “Avaliação da Qualidade da Água e Diagnóstico das Fontes de Poluição Orgânica do Estuário do Rio Cachoeira, Ilhéus, Bahia.” The
Environ Monit Assess (2013) 185:5387–5399 work described in this paper is also in the scope of the projects CNPq CT-HIDRO 2005 and INCT-TMCOcean.
References BAHIA. (2001). Programa de recuperação das bacias dos rios Cachoeira e Almada. Diagnóstico regional. Caracterização hidrológica. Unpublished report, BAHIA/SRH/UESC, Ilhéus, Brazil. Report s/n, vol. 1, Tomo IV. Boyd, S. R. (2001). Nitrogen in future biosphere studies. Chemical Geology, 176, 1–30. Boyer, E. W., Gooodale, C. L., Jaworski, N. A., & Howart, R. N. (2002). Anthropogenic nitrogen sources and relationships to riverine nitrogen export in the northeastern USA. Biogeochemistry, 57–58, 137–169. Carmouze, J. P. (1994). O Metabolismo dos Ecossistemas Aquáticos. São Paulo: Ed. Edgar Blücher/SBL/FAPESP. Davies, P. L., & Eyre, B. D. (2005). Estuarine modification of nutrient and sediment exports to the Great Barrier Reef Marine Park from the Daintree and Annan River catchments. Marine Pollution Bulletin, 51, 174–185. Divya, B., Sheryl, O. F., Sheelu, G., Shanta Nair, P. A., Bharathi, L., & Chandramohan, D. (2009). Limno-tolerant bacteria govern nitrate concentration in Mandovi Estuary, India. Estuarine, Coastal and Shelf Science, 82, 29–34. Eyre, B., & Balls, P. (1999). A comparative study of nutrient behavior along the salinity gradient of tropical and temperate estuaries. Estuaries, 22, 313–326. Grasshoff, K., Ehrardt, M., & Kremling, K. (1983). Methods of seawater analysis. Weinhein: Verlag Chemie. Guimarães, A. G. (2006). Tempo de Residência da Água e Estado Trófico da Porção Interna do Estuário do Rio Cachoeira, Ilhéus-BA: M.Sc. Dissertation , Universidade Estadual de Santa Cruz, Brasil. http://www.uesc.br/cursos/ pos_graduacao/mestrado/mdrma/teses/dissertacao_alonso_ goes_guimaraes.pdf. Accessed 9 June 2011. Herbert, R. A. (1999). Nitrogen cycling in coastal marine ecosystems. FEMS Microbiology Reviews, 23, 563–590. Howarth, R. W., & Marino, R. (2006). Nitrogen as the limiting nutrient for eutrophication in coastal marine ecosystems: evolving views over three decades. Limnology and Oceanography, 51, 364–376. Jennerjahn, T. C., Ittekkot, V. S., Klopper, S., Adi, S. P., Nugroho, N., Yusmal, S. A., & Prihartanto, G.-H. B. (2004). Biogeochemistry of a tropical river affected by human activities in its catchment: Brantas River estuary and coastal waters of Madura Strait, Java, Indonesia. Estuarine, Coastal and Shelf Science, 60, 503–514. Klumpp, A., Bauer, K., Franz-Gerstein, C., & Menezes, M. (2002). Variation of nutrient and metal concentracion in aquatic macrophytes along the Rio Cachoeira in Bahia (Brazil). Environmental International, 28, 165–171.
5399 Lima, M. C., Souza, M. F. L., Eça, G. F., & Silva, M. A. M. (2010). Export and retention of dissolved inorganic nutrients in the Cachoeira River, Ilhéus, Bahia, Brazil. Journal of Limnology, 69, 138–145. Lin, J., Xie, L., Pietrafesa, L. J., Shen, J., Mallin, M. A., & Durako, M. J. (2006). Dissolved oxygen stratification in two micro-tidal partially-mixed estuaries. Estuarine, Coastal and Shelf Science, 70, 423–437. Marti, E., Aumatell, J., Godé, L., Poch, M., & Sabater, F. (2004). Nutrient retention efficiency in streams receiving inputs from wastewater treatment plants. Journal of Environmental Quality, 33, 285–293. Millie, D. F., Carrick, H. J., Doering, P. H., & Steidinger, K. A. (2004). Intra-annual variability of water quality and phytoplankton in the North Fork of the St. Lucie River Estuary, Florida (USA): a quantitative assessment. Estuarine, Coastal and Shelf Science, 61, 137– 149. Paerl, H. W., & Pinckney, J. L. (1996). A mini-review of microbial consortia: their roles in aquatic production and biogeochemical cycling. Microbial Ecology, 31, 225–247. Parsons, T. R., Maita, Y., & Lalli, C. M. (1984). A manual of chemical and biological methods for seawater analysis. Ann Arbor: Pergamon. Pereira-Filho, J., Spillere, L. C., & Schettini, C. A. F. (2003). Dinâmica de nutrientes na região portuária do estuário do Rio Itajaí-Açu, SC. Atlantica, 25, 11–20. Rabalais, N. N. (2002). Nitrogen in aquatic ecosystems. Ambio, 31, 102–112. Robertson, L. A., & Kuenen, J. G. (1992). The effect of electron acceptor variations on the behavior of Thiosphaera pantotropha and Paracoccus denitrificans in pure and mixed cultures. Microbial Ecology, 86, 221–228. Smith, S. V. (1984). Phosphorus versus nitrogen limitation in the marine environment. Limnology and Oceanography, 29, 149–1160. Souza, M. F. L. (2005). Nutrient biogeochemistry and mass balance of a tropical estuary: estuary of Cachoeira River, Northern Brazil. International Journal of Ecology and Environmental Sciences, 31, 177–188. Strickland, J. D. H., & Parsons, T. R. (1972). A practical handbook of seawater analysis. Bull. Fisheries Research Board of Canada, n. 167. Tappin, A. D. (2002). An examination of the fluxes of nitrogen and phosphorus in temperate and tropical estuaries: current estimates and uncertainties. Estuarine, Coastal and Shelf Science, 55, 885–901. Uncles, R. J., Frickers, P. E., & Harris, C. (2003). Dissolved nutrients in the Tweed Estuary, UK: inputs, distributions and effects of residence time. Science of the Total Environment, 314–316, 727–736. Vidal, S., Rocha, C., & Galvão, H. (2002). A comparison of organic and inorganic carbon controls over biological denitrification in aquaria. Chemosphere, 48, 445– 451.
Dissolved inorganic nutrients and chlorophyll a in an estuary receiving sewage treatment plant effluents: Cachoeira River estuary (NE Brazil) Maria Aparecida Macêdo Silva & Gilmara Fernandes Eça & Danielle Felix Santos & Alonso Góes Guimarães & Michelle Coêlho Lima & Marcelo Friederichs Landim de Souza
Received: 15 March 2012 / Accepted: 8 October 2012 / Published online: 24 November 2012 # Springer Science+Business Media Dordrecht 2012
Abstract Sampling was conducted monthly during a transition period between the dry and rainy seasons in order to evaluate the effectiveness of a municipal sewage treatment plant (STP) in eutrophication control. STP
effluent and fluvial input data were also estimated. In the dry period, high concentrations of nutrients, chlorophyll a (up to 360 μgL−1), and anoxia in bottom waters were observed in the upper portion of the estuary. Nitrate was
M. A. M. Silva : G. F. Eça : D. F. Santos : M. C. Lima : M. F. L. de Souza (*) Programa de Pós-Graduação em Sistemas Aquáticos Tropicais, Laboratório de Oceanografia Química, Universidade Estadual de Santa Cruz—UESC, Rod. Ilhéus-Itabuna km 16, 45650-000 Ilhéus, BA, Brazil e-mail: [email protected]
Present Address: G. F. Eça Programa de Pós-Graduação em Química, Universidade Federal da Bahia, Instituto de Química, Laboratório de Oceanografia Química, Rua Barão de Geremeoabo, s/n, Campus Universitário de Ondina, 40.170-115 Salvador, BA, Brazil
M. A. M. Silva e-mail: [email protected] G. F. Eça e-mail: [email protected] D. F. Santos e-mail: [email protected] A. G. Guimarães Programa Regional de Pós-Graduação em Desenvolvimento e Meio Ambiente, Universidade Estadual de Santa Cruz—UESC, Rod. Ilhéus-Itabuna km 16, 45650-000 Ilhéus, BA, Brazil Present Address: M. A. M. Silva Programa de Pós-Graduação em Oceanografia Biológica, Laboratório de Fitoplâncton e Microorganismos, Universidade Federal do Rio Grande FURG, Av. Itália, Km 08, 96201-900 Rio Grande, RS, Brazil
Present Address: D. F. Santos Instituto Federal de Educação, Ciência e Tecnologia da Bahia—IFBA, Porto Seguro, BA, Brazil
Present Address: A. G. Guimarães Faculdade de Tecnologia e Ciências—FTC, Itabuna, BA, Brazil
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scarce during the dry months, although high concentrations were observed at the river sources and the upper estuary. The N:P and Si:P molar ratios were usually below 16:1, and the Si:N ratio was higher than 1:1. The fluvial inputs were a greater source of nutrients to the estuary than the STP, but nutrient loading by these effluents were also important in contributing to the eutrophication of the upper estuarine zone, especially in the dry season when symptoms were more intense. Keywords Brackish water pollution . Sewage treatment . Denitrification . Nutrient loading . Tropical environment . Northern Brazil
Introduction Estuaries are of biological and socioeconomic importance and are characterized by high rates of primary productivity and biomass. These systems, which occur at the continent/ocean interface, receive, process, and export/import large amounts of organic matter and/or nutrients from natural and anthropogenic sources. Estuaries are dynamic environments that are subject to wide variations in physical, chemical, and biological characteristics. This variability leads to complex reactions and phase changes of the materials present in the water (Davies and Eyre 2005; Divya et al. 2009). However, when the natural and anthropogenic nutrient load to these systems exceeds the assimilation capacity for production, eutrophication and degradation of the water quality can occur (Boyd 2001; Boyer et al. 2002; Rabalais 2002). The primary producers are the first components of ecosystems to respond to increases in nutrient concentrations. The structure and function of phytoplankton can change, causing excessive increases in the population and consequent decreases in the concentration of oxygen during decomposition. These changes can even lead to hypoxia or anoxia in the water column (Millie et al. 2004). Secondary effects of the increase of phytoplankton biomass include blooms of harmful algae, enhanced turbidity, diminished light penetration, and loss of submersed vegetation. These changes lead to a collapse of ecosystem functioning, specifically, a loss of habitat and biodiversity, and a displacement of trophic chains (Rabalais 2002). Marti et al. (2004) note that sewage treatment plants (STP) have improved water quality, but problems associated with
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sewage discharge remain. These problems include difficulties in controlling nonpoint sources, removal inefficiencies of nutrients in STP, and increases in populations and residues. In developing countries, most STPs only conduct a primary treatment and convert organic matter to dissolved inorganic nutrients (Pereira-Filho et al. 2003). These nutrient-rich effluents can cause eutrophication, especially in systems with a high water residence time. Nutrient limitation by nitrogen, phosphorus, and silicon can occur along the salinity gradient and can affect primary productivity and the accumulation of phytoplankton biomass (Rabalais 2002). If the actual concentrations are also considered, the stoichiometric ratio of N, Si, and P postulated by Redfield for marine and coastal environments (16:16:1) can be used to determine which nutrient limits phytoplankton productivity (Smith 1984). Nitrogen is likely the major cause of eutrophication in most coastal systems, especially in pristine systems (Rabalais 2002), but other nutrients, such as phosphorus and silica, can also limit primary production in some systems (Howarth and Marino 2006; Jennerjahn et al. 2004). The excess phosphorus in estuaries can influence cycling and the availability of nitrogen and dissolved silica, thus negatively affecting the community structure of primary producers. Agricultural activity and urbanization in some regions has likely increased N fluxes to the coast (Howarth and Marino 2006). Anthropogenic impacts in the watersheds, such as deforestation, soil erosion, and dam construction, can also alter the DIN:DIP, DSi:DIN, and DSi:DIP ratios and affect phytoplanktonic community structure in coastal waters dominated by diatoms (Jennerjahn et al. 2004). The objective of this work was to determine the concentrations and temporal/spatial distribution of dissolved inorganic nutrients and chlorophyll a in an estuarine system subject to in natura and treated sewage during a transition period between the dry and rainy seasons.
Materials and methods Study area The Cachoeira River estuary is located in the south of Bahia State, Northern Brazil (Fig. 1). The drainage
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basin of the Cachoeira River has an area of approximately 4,600 km2. The total population in the basin is approximately 600,000 inhabitants, who are primarily concentrated in the cities of Itabuna and Ilhéus (approximately 200,000 inhabitants live in each). Cocoa cultivation, livestock, and pasture activities constitute the main land use in this region (BAHIA 2001). The predominant tropical humid climate in the area is demonstrated by an annual average temperature of 24.6 °C and an annual precipitation of between 1,500 and 2,000 mm (Klumpp et al. 2002). The rain and fluvial discharges are characterized by extreme irregularities, with ill-defined dry and rainy seasons. The annual average fluvial discharge is 24.1 m3 s−1, with historical records showing values between 0.2 and 1,460 m3 s−1 (BAHIA 2001). Lima et al. (2010) observed an increase in discharge from 0 to 826 m3 s−1 in the period from 2003 to 2004. During the dry season, the river presents an extensive development of floating aquatic macrophytes, which are carried to the estuary and coastal waters during flooding episodes (Souza 2005). The estuarine area is approximately 16 km2, including an area of mangroves of approximately 13 km2 (Souza 2005). Semidiurnal tides reach heights of approximately 2 m. The inner portion of the estuary receives the effluents of a STP, which conducts a primary level treatment of part of the domestic sewage from the city of Ilhéus. These effluents present high dissolved inorganic nutrient concentrations. The release of untreated domestic effluents is also widespread in outer estuarine areas. The city of Itabuna releases untreated sewage and treated industrial effluents into the Cachoeira River approximately 10 km upstream of the estuary, which are transported into the estuary as fluvial inputs. Sample collection and analytical producers Water sampling was carried out in November and December of 2003 (the dry season), January and February of 2004 (the transition period), and March of 2004 (the peak of the rainy season). Samples were collected at ten points with Van Dorn bottles in surface, mid depth, and bottom waters according to depth (Fig. 1). pH, dissolved oxygen, salinity, and temperature were measured in the field with portable digital meters. The samples were filtered using fiberglass filters of type GF/C. The concentrations of dissolved inorganic
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nutrients (ammonium, nitrite, nitrate (DIN), and phosphate (DIP)) were determined according to Grasshoff et al. (1983), while the silicate (DSi) concentration was established using the method of Carmouze (1994). Total suspended solids (TSS) were determined using a gravimetric method (Strickland and Parsons 1972). Chlorophyll a was analyzed using a spectrophotometric method (Parsons et al. 1984). Inputs of dissolved inorganic nutrients from the STP and the river The fluxes of dissolved inorganic nutrients (FY) from the STP and the Cachoeira River were obtained by multiplying the values of the concentration of each inorganic nutrient by the discharge of STP effluent and the river at a monthly time scale. The following formula was used in this assessment: FY ¼ ½Y plant Qplant where [Y]plant and Qplant represent the concentration of each nutrient and the monthly discharge of the STP, respectively. The nutrient loadings in the Cachoeira River were obtained from Lima et al. (2010).
Results Hydrochemical characteristics The inner reaches of the estuary presented saline stratification during the dry period and the beginning of the rainy period, while the outer section was more mixed vertically. Salinity was high in the dry period, varying from 34 to 36 in the outer estuary and from 13 to 30 in the inner portion (Table 1). The salinity decreased along the entire estuary in February, reaching a maximum value of 13. In March, the high input of freshwater almost entirely flushed the estuary (S00), and salinity values were only recorded at Station 4f (S0 33.0). This anomalous value was likely due to the retention of denser water with a higher salinity (~36) in a depression of approximately 10 m depth near this station. The temperature varied from 25.5 to 33.9 °C, with the higher values measured at the inner reaches of the estuary during the dry period. The pH exhibited values between 7.23 and 8.83, with higher values occurring in surface water samples
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Fig. 1 Map of the study area showing the location of sampling stations in the Cachoeira River estuary
during the dry period. The inner portion of the estuary exhibited lower pH values in most of the months sampled. During the dry period, dissolved oxygen concentrations in surface samples in the inner estuary varied from 12.2 to 17.4 mgL−1, while values from 0.00 to 4.40 mgL−1 were observed in bottom samples. During the rainy season, the dissolved oxygen concentrations varied from 0.00 to 8.31 mgL−1 in the inner estuary and from 5.20 to 6.80 mgL−1 in the outer estuary (Table 1). Ammonium concentrations in the dry and transition periods presented high values, ranging from 35 to 50 μmolL−1 (Fig. 2). However, samples below the detection limit were also observed during the dry period. Ammonium values were higher in the inner estuary and in the bottom samples. In the rainy period, the maximum concentration of ammonium was 21 μmolL−1, while nitrite presented maximum concentrations of 3.5 μmolL−1 in the study period. The higher values were observed in November and March and in surface samples. In January, nitrite was undetectable. In November, high concentrations of nitrate were observed in the inner portion of the estuary, with a maximum value of 87 μmolL−1, while concentrations were lower than the detection limit in the outer estuary. In December, the entire estuary presented concentrations of nitrate that were lower than the detection limit. The concentrations of nitrate in the
estuary increased in the rainy season but did not exceed 16.0 μmolL−1. Phosphate concentrations in the inner portion of the estuary varied from 0.40 to 18.0 μmolL−1 in the dry period, while values in the rainy period varied from 7.54 to 13.0 μmolL−1. In the outer estuary, minimum and maximum values of 0.44 and 2.27 μmolL−1 were observed throughout the study (Fig. 3). Silicate was observed in the inner portion at concentrations of 87.6 μmolL−1 in the dry season, while concentrations observed during the transition and rainy periods varied from 0.56 to 214 and from 57.3 to 229 μmol sL−1, respectively. Concentrations of silicate were lower in the outer estuary and coastal regions, with a minimum value of 1.59 and a maximum value of 96.7 μmolL−1 (Fig. 3). High chlorophyll a concentrations were observed in the inner portion of the estuary (November0133 μg L−1 and December0368 μgL−1). In the rainy season, the concentrations of chlorophyll a were lower in the inner estuary, varying from 0.94 to 79.0 μgL−1. The chlorophyll a concentrations in the outer estuary and at the coastal station were similar, with a minimum value of 0.9 and a maximum value of 2.74 μgL−1 (Fig. 4). The highest concentrations of TSS were observed in the dry season (11.2 to 341 mgL−1) in the inner portion of the estuary, followed by the outer portion of
36.4±0.24 (36.2–36.8)
16.6±2.60 (13.5–20.9)
Outer
Inner
26.2±1.0 (26.2–29.0)
31.4±1.02 (30.2–32.7)
Outer
Inner
8.09±0.56 (7.34–8.83)
Inner
5.98±0.18 (5.76–6.20)
6.14±0.11 (6.00–6.25)
7.25±6.88 (0.00–17.4)
Coastal
Outer
Inner
DO (mgL−1)
8.20±0.02 (8.17–8.22)
8.22±0.02 (8.20–8.25)
Coastal
Outer
pH
28.4±0.18 (28.6–28.1)
Coastal
T (°C)
36.8±0.34 (36.2–37.1)
Coastal
S
November
6.74±6.18 (0.00–15.9)
6.92±0.71 (5.97–7.54)
6.83±0.90 (5.55–7.66)
8.21±0.42 (7.76–8.83)
7.97±0.33 (7.31–8.17)
8.02±0.12 (7.80–8.15)
31.6±1.65 (29.1–33.9)
28.1±0.46 (27.8–29.0)
27.3±0.80 (26.2–28.3)
23.6±4.78 (18.8–30.9)
36.1±0.90 (34.4–36.8)
36.8±0.23 (36.4–37.0)
December
4.15±2.66 (0.00–8.31)
6.01±0.10 (5.88–6.10)
6.10±0.07 (6.06–6.18)
7.81±0.46 (7.23–8.69)
8.18±0.03 (8.15–8.22)
8.17±0.05 (8.13–8.22)
29.6±0.82 (28.2–30.6)
26.6±0.43 (26.2–27.1)
29.6±0.82 (28.2–30.6)
18.5±9.78 (0.90–30.0)
35.9±0.80 (34.8–36.6)
36.5±0.00 (36.5–36.5)
January
Table 1 Mean, standard deviation, and range (in brackets) of the physicochemical variables in Cachoeira River estuary
4.15±2.07 (1.34–6.37)
5.88±0.36 (5.20–6.21)
6.04±0.10 (5.93–6.13)
7.85±0.24 (7.55–8.12)
8.16±0.06 (8.09–8.24)
8.17±0.11 (8.05–8.25)
30.2±0.73 (28.8–30.7)
28.1±0.28 (27.7–28.5)
26.8±0.26 (26.6–27.1)
35.6±0.95 (34.5–36.2)
33.3±4.23 (24.3–36.1)
35.6±0.95 (34.5–36.2)
February
7.13±0.22 (6.75–7.32)
6.90±0.51 (6.60–7.80)
8.06±0.01 (8.05–8.07)
7.53±0.05 (7.49–7.61)
7.56±0.34 (7.35–8.17)
8.24±0.12 (8.16–8.33)
27.5±1.63 (26.4–28.7)
26.0±0.67 (25.5–27.1)
27.5±1.63 (26.4–28.7)
0.00±0.00 (0.00–0.00)
7.30±14.8 (0.00–33.7)
33.6±0.42 (33.3–33.9)
March
Environ Monit Assess (2013) 185:5387–5399 5391
5392 Fig. 2 Mixing diagram of ammonium, nitrite, and nitrate during the dry, transition, and rainy seasons
Fig. 3 Mixing diagram of phosphate and silicate during the dry, transition, and rainy seasons
Environ Monit Assess (2013) 185:5387–5399
Environ Monit Assess (2013) 185:5387–5399
5393
Fig. 4 Concentration of chlorophyll a and total suspended solids (TSS) along a salinity gradient during the dry, transition, and rainy seasons
the estuary (6.78 to 109 mgL−1). In the rainy season, TSS values during the month of February ranged from 7.2 to 9.0 mgL−1 (Fig. 4). Stoichiometric ratios The DIN:DIP ratios were usually below 16:1 (0 to 12; Table 2). Ratios higher than 16:1 were observed in the outer estuary in November (27), in the inner portion of the estuary in January (19), and at the coastal station in March (31). The DSi:DIN ratio was usually higher than 1:1, with values varying from below 1 to as high as 150. The DSi:DIP ratio was generally lower than 11. Higher values of this ratio were observed at the inner portion of the estuary in January (values of 8 to 21) at all estuary and coastal stations in February (values of 4 to 43) and at the coastal station in March (values of 13 to 35; Table 2). Inputs of dissolved inorganic nutrients from the STP and the river Fluvial inputs of nutrients to the estuary are shown in Table 3. The largest inputs of nutrient occurred in March 2004, which coincided with the period of the greatest fluvial discharge (Table 3). Despite the low discharge observed in November 2003, fluvial fluxes of nutrients were higher in this month than in December. December
and January of 2003 were marked by an increase in nitrate inputs from the STP, which reached values that were equal to and more than twice the values of the fluvial inputs, respectively. The fluvial inputs of nitrate, nitrite, phosphate, and silicate were higher than the fluxes from the STP during most of the study period. Notable exceptions included the inputs from the STP of phosphate in December (21.0×103 molmonth−1), of ammonium during the dry period (22.0 to 250×103 mol month −1 ), and of nitrate in January (5 × 10 3 mol month−1), which were higher than the fluvial inputs.
Discussion The high water residence time observed in December (Guimarães 2006) and the salinity distribution in the inner portion of the estuary indicate that the tide was the main physical hydrological force acting on the estuary during the dry period. The intrusion of salt water and the small fluvial discharge resulted in saline stratification in the inner portion of the estuary during the dry months but showed a negligible water residual flow or mixing. This stratification was intensified in the beginning of the rainy period due to the increase in fluvial discharge. The stagnation of the water was associated with the sources of nutrients, such as the input of treated
5394
Environ Monit Assess (2013) 185:5387–5399
Table 2 Mean, standard deviation, and range (in brackets) of the stoichiometric ratios in Cachoeira River estuary November
December
January
February
March
N:P Coastal
7.9±5.7 (0.1–16)
1.5±3.5 (0.0–8.8)
5.2±1.7 (3.6–7.0)
7.4±4.6 (2.6–12)
31±0.6 (30–31)
Outer
8.5±9.6 (2.7–28)
0.0±0.0 (0.0–0.1)
2.2±157 (0.5–4.8)
10±4.6 (5.0–18)
4.1±3.5 (2.2–10)
Inner
5.4±3.6 (1.2–12)
0.3±0.4 (0.0–1.q)
7.4±6.2 (1.8–19)
7.3±0.6 (6.4–8.0)
2.6±0.5 (1.7–3.0)
Si:P Coastal
6.3±2.0 (4.4–9.4)
2.2±0.4 (1.9–3.1)
5.5±1.4 (4.2–7.0)
18±12 (11–32)
24±15 (13–35)
Outer
6.5±2.6 (3.1–9.8)
6.1±1.9 (4.2–8.5)
7.4±2.3 (4.6–11)
24±16 (3.7–43)
5.7±1.8 (4.1–8.2)
Inner
7.6±1.7 (5.2–9.4)
2.4±2.6 (0.1–5.9)
14±4.5 (8.3–21)
30±3.7 (26–37)
6.9±1.4 (5.2–8.2)
Si:N Coastal
10±23 (0.5–57)
190±303 (0.26–796)
1.2±0.7 (0.8–1.9)
3.2±2.0 (0.9–4.7)
0.8±0.5 (0.4–1.1)
Outer
1.4±0.9 (0.3–2.9)
120±42 (91–150)
2.2±1.57 (0.5–4.8)
2.2±1.3 (0.7–3.4)
1.7±0.6 (0.8–2.3)
Inner
2.0±1.2 (0.7–4.3)
2.2±0.1 (1.0–1.2)
7.4±6.2 (1.8–19)
4.1±0.5 (3.4–4.9)
2.7±0.4 (2.0–3.1)
ammonium and nitrite in the coastal stations denote a local source of sewage or a resuspension of the sediments. In the rainy period, the input of material from the drainage basin and the washing of the inner estuarine portion resulted in an increase of nutrient concentrations in the outer portion of the estuary. The low nutrient concentrations observed in the inner portion of the estuary during this period suggest the dilution of those nutrients due to the large amount of fresh water in the system. In February, the nearly linear distribution of nutrients along the salinity gradient indicated that the mixture between the salt water and fresh water was fast and did not allow for the expression of nonconservative processes (Uncles et al. 2003). Assimilation by primary producers was likely the process by which ammonium in the Cachoeira River estuary is removed during the dry period, especially in the inner portion of the estuary. The plot of chlorophyll a
sewage from the STP and fluvial sources. High concentrations of nutrients occurred despite the low fluvial discharge, which resulted in an increase of nutrients and chlorophyll a concentrations in the inner portion of the estuary during the dry period. The remineralization of the organic matter from fluvial and STP inputs explain the deficit of oxygen and the value of the pH observed in the bottom waters. The hypoxia in the bottom waters is characteristic of stratified and eutrophic environments. These environments present a high biological demand of oxygen in the bottom waters and sediments, which can be accentuated in the summer because of high temperatures (Lin et al. 2006). In the dry period, the outer portion of the estuary presented little exchange with the inner portion, which was richer in nutrients. This and the intrusion of seawater can explain the low values of nutrient and chlorophyll concentrations observed in the outer portion of the estuary. Higher concentrations of
Table 3 Monthly inputs of dissolved inorganic nutrients by the municipal sewage treatment plant (STP) and fluvial station (103 mol month−1) November
NH3/NH4+
January
February
STP
Rivera
STP
Rivera
STP
Rivera
STP
22.0
17.8
250
0.33
250
30.2
NO2−
0.80
NO3−
3.70
PO43−
35.0
H3SiO−
82.0
a
December
5.42 470 58.5 691
Data from Lima et al. (2010)
March Rivera
0.00
38.2
0.58
0.12
1.60
4.81
0.00
30.4
1.40
1.46
4.70
1.77
0.00
21.0 140
1.86 15.6
7.90 84.0
2,080
STP
Rivera
170
5,100
1.30
562
4.10
5,100
119
0.00
329
16.0
3,440
837
0.00
1,940
32.0
31,700
Environ Monit Assess (2013) 185:5387–5399
Fig. 5 Relationship between nitrate and chlorophyll a (a), ammonium (b), and dissolved oxygen (c) in a November 2004 survey
versus nitrate in the November survey (Fig. 5a) demonstrated a decrease in nitrate concentrations and an increase in chlorophyll a from the fluvial source towards the sea in the surface waters up to Station 7. The low
5395
concentrations in the outer portion of the estuary were due to internal processes in the estuary and likely to the intrusion of coastal waters with a lower nutrient content, since mixing between the inner and outer estuaries was negligible at this time (Guimarães 2006). The denitrification process could also remove nitrate in the inner portion of the estuary. Low oxygen concentrations observed in November, December, and January at Stations 7, 8, and 9 in bottom samples might have favored that process. An inverse relationship between nitrate and ammonium can be observed along the surface at Stations 7 and 8, and in bottom waters at Stations 7 to 9 in November (Fig. 5b). Stations BV and 9 s showed different trends fits outside, mainly because the former represents the fluvial input and the latter reflects the influence of the STP input under the high tide conditions occurring during the sampling. A linear regression between nitrate and ammoniacal nitrogen was used to verify the possible occurrence of denitrification at these stations. This analysis presented an r value of 0.81, suggesting the occurrence of denitrification in this area. A strong linear correlation (r00.90) between nitrate and dissolved oxygen was also observed in November, when the surface waters of Stations 7 to 8, and bottom waters of Stations 7 to 9 were considered (Fig. 5c). In principle, the oxic conditions at the other stations were not suitable for denitrification. However, some authors describe that denitrification can occur, although infrequently, in the presence of higher concentrations of dissolved oxygen in the water (Paerl and Pinckney 1996; Robertson and Kuenen 1992; Vidal et al. 2002). Particulate material in suspension can develop anoxic microzones where denitrifying action by anaerobic bacteria can occur in aquatic systems (Paerl and Pinckney 1996). Studies have shown that aquatic macrophytes can also stimulate denitrification because they easily trap organic debris from the water column or liberate organic carbon through their roots. Fecal pellets have also been recognized as sites of intense microbial activity, which result in a high demand of oxygen and favor denitrification close to the surface of oxic sediments (Herbert 1999). There is an intense growth of floating macrophytes occurring along the fluvial portion of the Cachoeira River during the dry season, which are transported to the estuary in variable amounts during higher discharge episodes (Klumpp et al. 2002; Souza 2005).
5396
Sedimentation can also explain the removal of nitrate from the River Cachoeira estuary during the dry period. In spite of removing less nitrogen than the processes discussed above, sedimentation can represent an important mechanism of nitrogen removal, especially during periods of high water residence time (Boyd 2001; Tappin 2002), as observed in the study area during November and December of 2003. The phosphate concentrations in the inner portion of the estuary might have been primarily influenced by external sources, but contributions from sediment fluxes may also have been important. The high water residence time in the dry period probably favored the recycling of phosphate, thus increasing the concentration of phosphate in the water column. The regeneration of phosphorus in the sediment is described as an important process that contributes to the input of phosphorus in the estuary (Davies and Eyre 2005), mainly during the dry period when the internal processes are most expressive. In the rainy period, the smallest assimilation of the phytoplankton and the input of sewage and fluvial discharge may explain the phosphate concentrations in February, particularly in the outer portion of the estuary and in the sea, where the chlorophyll concentrations were low. The apparent removal of phosphate in the outer portion of the estuary in December was related to the adsorption of phosphate in particles of minerals and organic material in suspension or the pseudoremoval of phosphate due to dilution of water with low concentrations of phosphate. In the rainy period, the removal of phosphate in the inner portion of the estuary was likely due to consumption by phytoplankton and adsorption. During the dry period, benthic regeneration can be a significant source of silicate for the estuary. In this period, continental drainage was not an important source of this nutrient in the estuary due to the low fluvial flow. Benthic dissolution of the biogenic silica was observed in an Australian tropical estuary (Eyre and Balls 1999) that originated from fresh water and was the main source of silicate during the rainy period. Moreover, in the present study, the removal of the silicate in the dry period in the inner portion of the estuary indicates assimilation by the diatoms. In higher salinity areas, decreases in silicate can be due to the dilution of this nutrient. Data from a regression of silicate on chlorophyll in December showed that silicate removal was due to assimilation by diatoms, except at Stations 7s and 8s, where the high chlorophyll concentrations did not
Environ Monit Assess (2013) 185:5387–5399
correlate with silicate, suggesting that other groups of phytoplankton were responsible for these chlorophyll concentrations. In many estuarine systems, diatoms are among the main factors influencing chlorophyll concentrations (Millie et al. 2004). The maximum chlorophyll a concentrations observed in this study were higher than those observed previously in this same system (Souza 2005). This author found concentrations that were below or close to the detection limit up to maximum values, which were between 39 μgL−1 and 64 μgL−1 in May 2001 and in August 2001, a period of low discharge (Fig. 6a). The sampling surveys made during this previous study were conducted 5 and 11 months after the STP became operational (in September 2000) and more than 2 years before the present study, but a causal relationship between sewage management and eutrophication can be speculated. The maximum chlorophyll a concentrations found in the low discharge period in 2003 were higher than those found in 2001 during the same hydrological conditions. Chlorophyll a in 2003 reached concentrations up to threefold the maximum recorded in 2001. The higher chlorophyll a concentrations (outliers) were observed at the inner estuary in November and December 2003 and coincided with high concentrations of oxygen, high pH, and phytoplanktonic biomass at the surface, suggesting that the removal of the dissolved inorganic nutrients was predominantly due to primary production. The outer estuary presented lower concentrations than those observed in 2001 (boxes), probably due to the lower availability of dissolved nutrients after removal at the inner estuary. The total solids in suspension during the dry months and at the beginning of the rainy period in the present study primarily originated from autochthonous material. The dispersion graphs for the dry period showed higher TSS concentrations in the outer portion of the estuary and in the bottom samples, which suggests the occurrence of sediment resuspension. The STP and diffuse points of sewage inputs were probably additional sources of particulate matter, mainly in the inner portion of the estuary. The low DIN:DIP molar ratio, especially in the dry season, can be associated with the biogeochemical removal of nitrogen and mainly the high availability of phosphorus in relation to nitrogen. The molar DIN: DIP ratio could imply the nitrogen limitation of primary production in the outer estuary during the dry
Environ Monit Assess (2013) 185:5387–5399
5397
Fig. 6 Chlorophyll a (a) and phosphate (b) concentrations measured in the surveys carried since 2000 in Cachoeira River estuary. Asterisk not analyzed
period, when DIN concentrations were low. In the inner portion of the estuary, high chlorophyll concentrations indicated that low DIN:DIP values did not affect the phytoplankton, since nutrients were largely available. A deviation in the molar ratio does not indicate that phytoplankton are nutrient-limited (Smith 1984). Larger amounts of a nutrient in relation to another nutrient can cause a deviation in the molar ratio without affecting the phytoplankton nutrient supply. The DIN:DIP molar ratio observed (Souza 2005) in the inner portion of the River Cachoeira estuary was low during 2001 (with a value of approximately 13) but very high in February of 2000 (with a value of 344). This same author observed that increased concentrations of phosphate in this system, which have occurred since February 2000 (before the STP became operational; Fig. 6b), caused low values of the DIN:DIP and DSi:DIP molar ratios after September
2001 (the beginning of the STP operation). Similar results were also found in the current study. These low concentrations of phosphate, near or below detection limit were not observed since February 2000. The median value remained almost constant after September 2000, but the general increase of high concentrations and the upper 75th percentile can be attributed to STP operation. Aside from the high availability of phosphate, the removal of dissolved silica by the diatoms during the dry period could also explain the observed values of the DSi:DIP molar ratio. In February and March 2004, the higher Si: DIP values in the inner portion and coastal station might reflect the fluvial input of silicate and a decrease in assimilation by the phytoplankton due to turbidity. The DSi:DIN ratio found in this study indicated that the productivity of the diatoms was not limited by the availability of dissolved silica.
5398
During the dry season, the low freshwater input is enough to create salt stratification of the water column in the upper estuary, but with low mixing with the outer portion. This allows for accumulation of the nutrient and organic matter loading from the STP in this area, in addition to fluvial inputs. The high nutrient content in the surface photic layer increases phytoplanktonic biomass, consumes dissolved nitrogen and phosphorus, and produces dissolved oxygen supersaturation. The respiration of organic matter in the bottom waters promotes anoxic conditions, favoring the occurrence of denitrification on the oxic/anoxic interface. The consumption of nitrate by phytoplankton assimilation and denitrification generates an excess of phosphate with high chlorophyll a concentrations. As fluvial discharge increases, vertical mixing and export of this material to the outer estuary occurs, dispersing the phosphate along the entire estuary but with chlorophyll a concentrations somewhat lower due to light limitation. In the peak of the rainy season, chlorophyll a concentration remains low but with higher phosphate concentrations from the leaching of the drainage basin soils.
Conclusion During the dry period, the high water residence time, large inputs of nutrients and organic matter by treated sewage and fluvial discharge, and estuarine morphology were responsible for forming two compartments of distinct characteristics inside the system. The inner estuarine presented characteristics of eutrophic waters, which were very different from those observed in the outer estuary. During the rainy period, due to the increase in the fluvial contribution and the low water residence time, mixing and transport processes were dominant. During this period, the drainage basin is the main source of dissolved inorganic nutrients and particulate matter to the estuary. This resulted in the increase of the nutrients in the outer portion of estuary and possibly an export to coastal waters. The DIN:DIP ratio and the low concentration of ammonium and nitrate in the outer part of the estuary indicated phytoplankton limitation by nitrogen, especially in December. The fluvial inputs of nutrients, mostly originated from effluents of Itabuna City, which represented an important contribution to the estuary. However, the
Environ Monit Assess (2013) 185:5387–5399
STP discharge can provide an important source of ammonium, nitrate, and phosphate during the dry period. In addition, these effluents also contribute to dissolved and particulate organic N and P that can be remineralized. The high nitrate concentrations found in November were mainly due to external sources such as STP and fluvial inputs. The large removal of nitrate in the estuary was likely not only due to assimilation by primary producers but also due to denitrification in sediments and anoxic bottom waters. There was an increase of phosphate concentrations and a decrease of DIN:DIP ratio after the STP became operational. Extreme values of chlorophyll a were observed at the inner estuary but lower concentrations at the outer portion, compared with samplings made in 2001, both during the dry season. This is an indication that the STP increased eutrophication at the inner estuary, and this effect is more acute during the dry season. It is important that these results be taken into account by environmental managers, especially in developing countries where there is a growing awareness of the need to treat domestic sewage. The option to release the effluents at the inner estuarine area instead of constructing a submarine outfall is frequently considered due to political, logistical, and economic reasons. It was not possible to evaluate the impacts of the STP with a proper sampling design including a time series before and after the beginning the STP became operational. However, the results of this and a former study shows that changes in the nutrient concentrations and stoichiometric ratios, chlorophyll a concentrations, and the intensity of anoxia in bottom waters were at least partially caused by the release of effluents from this STP, especially during the dry season. The planned construction of a dam in the Cachoeira River to supply water for the city of Itabuna would increase these effects during the dry season. Acknowledgments We thank Dr. D. M. L. Silva (UESC) for the valuable comments and suggestions on the text and also thank Mr. R. R. Cavalcanti for his help during sampling. M. A. M. Silva would like to thank FAPESB for the IC grant and CAPES, CNPq/CTHidro for the grant supporting her master studies. M. Lima and G.F. Eça would like to thank CNPq for the PIBIC grant. In addition, M.F.L. Souza thanks CNPq for the PQ grant, proc. number 350286/2000-0. We also thank CADCT/BA (public notice PRODOC) and PROPP/UESC for providing financial support to the project entitled “Avaliação da Qualidade da Água e Diagnóstico das Fontes de Poluição Orgânica do Estuário do Rio Cachoeira, Ilhéus, Bahia.” The
Environ Monit Assess (2013) 185:5387–5399 work described in this paper is also in the scope of the projects CNPq CT-HIDRO 2005 and INCT-TMCOcean.
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