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Marine Pollution Bulletin 62 (2011) 19151919

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Marine Pollution Bulletin

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Eutrophication and hypoxia in four streams discharging in Guanabara Bay, RJ, Brazil, a case study
Valquiria Maria de Carvalho Aguiar , Jos Antnio Baptista Neto, Carlos Marclei Rangel
Laboratrio de Geologia Marinha, Instituto de Geocincias, Universidade Federal Fluminense, Av. General MiltonTavares de Souza, 24210-346 Niteri, RJ, Brazil

a r t i c l e
Keywords: Nutrients Guanabara Bay So Gonalo Hypoxia Eutrophication

i n f o

a b s t r a c t
Four streams in the city of So Gonalo, were sampled to evaluate their potential as sources of nutrients to Guanabara Bay aiming to contribute with the government program to decrease the levels of pollution in this area. Imbuau, Guaxindiba, Marimbondo and Brandoas streams were sampled in 2007, 2008 and 2009. The streams revealed to be hipereutrophic with severe limitation of primary production by nitrogen, as shown by the N/P molar ratio. Phosphate levels were abnormally high varying between 4.35 and 130.82 lM, whereas nitrate and nitrite ranged from 0.06 to 54.05 lM and from 0.28 to 19.23 lM, respectively. The streams also presented severe hypoxia and anoxia, with oxygen values varying from nondetected to 3.72 ml l1. Heavy loads of particulate suspended material were recorded in the studied streams, ranging between 6.00 and 400.00 mg l1. The streams were considered inexorable sources of nutrients, enhancing the severe eutrophication process in Guanabara Bay. 2011 Published by Elsevier Ltd.

Water quality of rivers is of crucial importance to the maintenance of biotic and ecological integrity. Rivers transport nutrients to downstream habitats, and some of the impacts of nutrients in large rivers or small streams reach adjacent coastal water. The enrichment of coastal urbanized areas by nutrients is an increasing and widely known problem all around coastal areas. Worldwide is documented that nutrient concentration in rivers are increasing in at least 50% (Dodds, 2006). The main consequences of this process are hypoxia/anoxia, increase of primary production followed by increase of turbidity, decrease of phytoplankton diversity, among others which are direct consequences of eutrophication. The concept of eutrophication can be dened as an increase in the rate of supply of organic matter to an ecosystem, which most commonly is related to nutrient enrichment enhancing the primary production in the system (Newton et al., 2003). In Brazil, the southeast coast experiences great pressure from urbanization, intensive agriculture and aquaculture, besides the implementation of the main industrial poles in the country. Guanabara Bay, situated in the State of Rio de Janeiro, has been under anthropic inuence for a long time, being considered one of the greatest examples of coastal degradation in Brazil (Kjerfve et al., 1997; Knoppers et al., 1999; Crapez et al., 2000; Azevedo et al., 2004; Borges et al., 2007, 2009). The anthropic substances that are discharged into Guanabara Bay are of several types, such as, heavy metals, pesticides, polycyclic aromatic hydrocarbons,
Corresponding author. Tel.: +55 21 2629 5977.
E-mail addresses: valquiria@io.usp.br, valquiria@igeo.uff.br, vallaguiar@yahoo. com (V.M. de C. Aguiar). 0025-326X/$ - see front matter 2011 Published by Elsevier Ltd. doi:10.1016/j.marpolbul.2011.04.035

organochlorides, and, mostly, sewage without treatment. The later reaches the bay through submarine outfalls and through riverine input, such as Alcntara, Bombas, Brandoas, Imbuau, Marimbondo, Guaxindiba, Estrela, Paraba do Sul, among others. Sewage reaching Guanabara Bay through riverine input is quite signicant, due to the great lack of sanitation in the state, arriving in natura at this water body. The sewage charge contains great amounts of organic matter and nutrients, especially phosphorus (Khan and Ansari, 2005). The organic matter discharged into the bay can be deposited in the sediments or suffer bacterial decomposition releasing extra nutrient to the water column, and increasing even more the primary production. Nutrient-enhanced eutrophication is a driver of hypoxia/anoxia (Pearl, 1997), a common situation in Guanabara bay which presents hypoxia in the bottom layers and supersaturation of dissolved oxygen in the surface (Kjerfve et al., 1997; Borges et al., 2009). The rivers and streams that discharge in this coastal bay cross greatly urbanized areas, receiving all kinds of efuents. So Gonalo is the second biggest city in the State of Rio de Janeiro, well known for its lack of wastewater treatment plant and degradation of its rivers. Most of the rivers in this city are channeled, silted and systematically receive solid and untreated liquid wastes, which make them open sewers, and, therefore, they represent a health hazard for the marine life and human population. Besides the environmental impact on its rivers, this region is about to receive a huge petrochemical complex, already under construction, which makes baseline data extremely important, concerning future studies in this area. Considering that there are several rivers and streams crossing this region, the construction of a petrochemical complex will increase the urbanization of this area, which, in the future,


V.M. de C. Aguiar et al. / Marine Pollution Bulletin 62 (2011) 19151919

may impact the water quality and increase pollution issues in Guanabara Bay. Four streams were sampled in the city of So Gonalo; Marimbondo, Imbuau, Brandoas and Guaxindiba. The three campaigns occurred in the winter of 2007 and summer of 2008 and 2009, with the exception of Guaxindiba that was sampled only in 2008 and 2009. In Brazil, usually the summer is rainy and the winter is dry, therefore, two campaigns occurred in the wet season (2008 and 2009) and one campaign in the dry season (2007). Six stations were sampled in Brandoas and Imbuau, and four stations in Guaxindiba and Marimbondo (Fig. 1). Almost all the sampling points were allocated in channeled parts of the rivers that cross the urbanized area of So Gonalo, exceptions were the points near the mouth, in Imbuau, Brandoas and Marimbondo. Since there are no wastewater treatment plants, all the four rivers receive solid and untreated liquid wastes systematically. Water samples for the analysis of dissolved oxygen (DO), chlorophyll-a and phaeophytin-a, particulate suspended matter (SPM), phosphate, nitrate and nitrite were collected with a Van Dorn bottle in the surface water of the four streams. Temperature and pH were measured in situ with a Metrohm 827 pH meter. Samples for the analysis of nutrients and pigments were immediately stored in ice and kept refrigerated until the arrival at the laboratory, where each sample was ltered, through Millipore lters AP 40. Aliquots of the ltered samples for determination of nutrients were stored in polyethylene bottles (pre washed with HCl 10% and rinsed three times with Milli-Q water) and frozen at 20 C until the moment of analysis. The lters were dried in a mufe at 60 C and the determination of suspended particulate matter proceeded according to Strickland and Parsons (1968). The lters for the determination of chlorophyll-a and phaeopigments were

Fig. 1. Sampling stations for Imbuau (I1I6), Marimbondo (M1M4), Guaxindiba (G1G4) and Brandoas (B1B6).

extracted with ketone 90% in the dark and the analysis was carried on according to Strickland and Parsons (1968). The determination of dissolved oxygen was performed through Winkler method described in Grasshoff et al. (1999) with a Metrohm burette. Dissolved inorganic phosphorus, and dissolved nitrate and nitrite were analyzed with a Perkin Elmer spectrophotometer according to Grasshoff et al. (1999). Data analysis was complemented by principal component analysis (PCA), Spearman correlation and KruskallWallis analysis. All the four streams were channeled and silted in the sampling branches. Dark water and clandestine sewage pipes were observed along the four streams, pointing to a systematically input of domestic wastes. In 2007, temperature values varied between 22.60 and 29.50 C. In 2008 and 2009, the maximum temperatures were higher, with values from 25.80 to 32.80 C and between 23.50 and 30.50 C, respectively, reecting the difference between winter and summer campaigns (Table 1). The pH varied greatly along the streams and among the sampling periods (Table 1). The pH values varied between 6.68 and 8.64 in 2007, from 6.70 to 7.76 in 2008 and from 6.57 to 8.09 in 2009. The higher pH values were observed in the stations closer to Guanabara Bay, at the mouth of the streams, showing the inuence of marine water. Brandoas and Marimbondo presented the lower pH values in the campaigns occurred in 2008 and 2009, which is probably a consequence of higher input of organic matter in these streams, decreasing the pH during remineralization process. The streams were also heavily loaded with suspended particulate matter (Table 1), varying between 60.00 and 400.00 mg l1 in 2007, with the highest values in Brandoas and Imbuau, especially in the stations closer to Guanabara Bay (B6 and I6). In 2008, PSM decreased varying from 6.00 to 80.00 mg l1, with the maximum values encountered in Brandoas and Imbuau. In the subsequent year, values of PSM varied from 8.00 to 362.00 mg l1, and the highest concentrations were registered in Marimbondo. Analysis of dissolved oxygen was not performed in the campaign of 2007 due to technical problems. Severe hypoxia was observed in all the sampled streams (Table 1), and anoxia was registered in Marimbondo, Imbuau and Brandoas. The causes of hypoxia/anoxia are related to increasing nutrient loads, although physical factors may inuence the timing and extent of this condition (Conley et al., 2007). Brandoas stations presented values of oxygen between 0 and 3.72 ml l1 in the year of 2008, with the higher values in the most internal stations, whereas in the rest of them, hypoxia and anoxia were characterized. In the following year the Brandoas water were completely anoxic, with non-detectable dissolved oxygen at all stations. The same pattern was observed in Marimbondo, with oxygen values between 0 and 2.32 ml l1 in 2008 and total anoxia in the subsequent year. In Guaxindiba, the water were considered hypoxic in both years, with concentrations between 0.50 and 2.92 ml l1 in 2008 and between 0.59 and 1.85 ml l1 in 2009. In Imbuau the values of dissolved oxygen varied from 0.71 to 1.90 ml l1 in 2008 and from 0 to 1.21 ml l1 in 2009, characterizing hypoxia in both periods. Anoxia in Imbuau was observed only in the year of 2009, in the two stations closer to Guanabara Bay (I5 and I6). Hypoxia is a complex phenomenon that arises from the convergence of several factors, some of which are altered by human activities. Anoxia is rare in the water column of natural rivers and streams, for they are relatively shallow and have signicant greater rates of atmospheric exchange compared to lentic systems. Therefore, the biota of these systems will hardly deplete the dissolved oxygen in the water column, unless a substantial input of organic matter and nutrients occur, to support very rapid rates of heterotrophic activity (Dodds, 2006). In Imbuau, hypoxia was probably a consequence not only from the input of domestic efuents, but also from the mangrove intense produc-

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Table 1 Mean, standard error and range for temperature, pH, dissolved oxygen, suspended particulate material, chlorophyll-a, phaeophytin-a, nitrate, phosphate and nitrite in the four sampled streams between 2007 and 2009. Streams Statistics T (C) pH DO (ml l1) SPM (mg l1) 107.28 22.33 21.88400.00 88.53 25.11 8.0040.00 97.38 28.38 20.00362.00 27.70 4.68 6.0044.64 Chlo-a (lg l1) 15.00 5.35 035.60 47.30 20.79 5.34190.71 11.05 2.12 5.3416.02 7.92 0.29 7.638.21 Phae-a (lg l1) 33.01 7.44 2.1480.99 41.03 10.37 0.89102.80 44.73 15.16 9.35120.68 416.73 387.74 28.99804.47 NO 3 (lM) 5.82 2.13 0.0623.02 15.04 5.18 2.8054.05 3.94 1.27 0.7111.82 10.40 3.64 2.7920.20 NO 2 (lM) 1.59 0.33 0.285.18 4.01 1.10 0.3815.36 1.69 0.52 0.406.37 4.65 2.21 0.4419.23 PO3 4 (lM) 66.83 7.30 38.88130.82 46.29 6.21 4.3586.39 58.81 9.32 4.80128.32 37.66 4.67 17.2959.21





Mean SE Minmax Mean SE Minmax Mean SE Minmax Mean SE Minmax

26.91 0.26 25.0029.10 27.18 0.60 23.2031.00 28.35 0.80 22.6032.40 28.60 1.06 25.4032.80

7.30 0.10 6.688.18 7.52 0.09 7.058.20 7.48 0.16 6.748.64 6.87 0.07 6.577.20

0.82 1.33 03.72 0.86 0.18 01.90 0.50 0.28 02.32 1.45 0.31 0.502.95

tion, with a higher demand of dissolved oxygen for the decomposition of organic matter especially at the stations situated closer to the mouth. Hypoxia also typically occurs during periods of very low discharge, or in rivers with limited ushing rates. Hypoxia was observed during the rainy season in both years (2008 and 2009), when the uvial discharge is higher, which lead us to suppose that anoxia in the studied streams was caused mostly by the degradation of anthropic organic matter. The concentrations of nutrients found in the studied streams were so high that are hardly found in polluted aquatic ecosystems. Natural concentrations of phosphate and nitrate in streams usually vary between 0.02 and 2.60 lM and between 0.81 and 3.22 lM, respectively (Meybeck and Helmer, 1989). Phosphate concentrations were abnormally high (Table 1). In the year of 2007 the concentrations of phosphate varied from 22.49 to 130.82 lM, with the highest value recorded in the inner station of Brandoas (B1). In the same period nitrate and nitrite varied from 0.06 to 27.63 lM and from 0.32 to 10.80 lM, respectively. The highest values of nitrogen forms were exhibited by station 2 in Imbuau stream. In 2008, although the concentrations of phosphate decreased, they were still considered very high, ranging between 1.37 to 78.23 lM, with the highest value registered in station 2 in Brandoas. Nitrate concentrations varied from not detected, at Brandoas (B3), to 54.05 lM, in station I2, located in Imbuau. Concentrations of nitrite for the same period varied between 0.28 (B3) and 15.36 lM (I1). In 2009 concentrations of phosphate varied between 16.80 and 58.83 lM, with the highest concentration in a inner station in Brandoas (B2), whereas nitrite varied between 0.9 and 19.23 lM, with highest contents in inner stations of Imbuau (I1) and Brandoas (B1). Such high concentrations of nutrients undoubtedly reect anthropic input in the studied streams. The concentrations of phosphorus found in this study are hardly comparable to contents found in other polluted aquatic systems, such as Wonokromo river, where Jennerjahn et al. (2004) found concentrations of phosphorus up to 3.0 lM. Kucuksezgin et al. (2006) registered concentrations of phosphate between 0.01 and 10 lM in Izmir Bay (Turkey), which receives the discharge of several streams and domestic sewage outlets. Pereira-Filho et al. (2001) registered phosphate between 0.13 and 3.23 lM in river Cambori estuary (Brazil). Aguiar and Braga (2007) found phosphate concentrations between 0.40 and 19.17 lM in Santos estuary, a well known polluted coastal area in Brazil. The contents of phosphate found in this study are only similar to the ones found by Tas et al. (2006) in the heavily polluted Golden Horn estuary (Turkey), between 0.3 to 135 lM.

The elevated concentrations of phosphorus may have an internal source as well, since anoxia in the water column allow the release of phosphorus from sediments making the bottom water rich with this nutrient. Nitrate and nitrite were also considered very elevated along the studied streams (Table 1). Nitrate varied from 0.06 to 27.63 lM in 2007 and from 0.71 to 54.05 lM in 2008. Nitrite ranged between 0.32 and 10.80 lM in 2007, from 0.28 to 15.36 lM in 2008, and from 0.99 to 19.23 lM in 2009. In both sampling periods the higher concentrations of nitrate occurred in Imbuau in station I1 (2007), and in station I6 (2008). Among the studied streams, Imbuau was nitrate richest, and the higher contents of nitrite were registered in Guaxindiba followed by Imbuau. Smaller streams tend to present more temporal and spatial variability than rivers. Generally, responses of primary production in rivers should be less than in small streams because of increased turbidity and light limitation. Despite the high concentrations of phosphate, phytoplanktonic biomass, measured through chlorophyll a, was very low (Table 1), with the exception of some blooms observed in Imbuau, with concentrations of 190.71 lM in station 5 in 2007 and 106.80 lM in station 6 in 2008, and in Brandoas, with a concentration of 35.60 lM. In Imbuau, the phytoplanktonic blooms were observed closer to the mouth in the mangrove area, suggesting that besides the anthropic discharge, the litter fall contribution must also be considered, whereas in Brandoas, the bloom was registered in the urban area, which lead us to conclude that the primary production was solely due to anthropic inuence. On the other hand, the phaeophytin-a concentrations were quite elevated in most stations throughout the sampling periods (Table 1), varying from 0.89 to 120.68 lM in 2007, from 9.35 to 71.71 lM in 2008 and between 2.14 and 804.47 lM in 2009. The high concentrations of phaeophytin-a accompanied by the low levels of oxygen, point to the severe degradation scenario in the studied streams. The dark water present in the streams may act as a limitation for primary production, but the strongest factor is the nitrogen limitation as shown by N/P ratio, calculated as the sum of nitrate and nitrite/phosphate (Table 2), in accordance with the belief that phosphorus is more likely to be decient, and limit the primary production of any region of the earths surface proposed by Hutchinson (1967) and therefore, the most common cause of eutrophication in freshwater lakes, reservoirs and streams and headwater of estuarine systems (Correll, 1999). According to the classication proposed by Carlson (1977) and adapted by Toledo et al. (1983) for tropical ecosystems, the trophic state of streams can be dened through the concentrations of phosphorus.Based on the following equation the trophic index (TI) was calculated for each stream in the present study:


V.M. de C. Aguiar et al. / Marine Pollution Bulletin 62 (2011) 19151919 Table 3 KruskallWallis test for signicant differences among the campaigns 20072009 and among the four streams. Variables Campaigns p value Temperature pH Suspended particulate material Dissolved oxygen Clorophyll a Phaeophytin a Phosphate Nitrite Nitrate 0.0011 0.0085 0.0000 0.0281 0.2304 0.0001 0.0000 0.0161 0.6662 Streams p value 0.0702 0.2640 0.4997 0.2553 0.1924 0.9941 0.1274 0.1002 0.4643

   In80; 32=P TIP 10 6 In2

The concentrations of phosphorus were transformed in lg.l1 as requested by the formula. According to Toledo et al. (1983), 24 < TI 6 44 describe oligotrophic water; 44 < TI 6 54, mesotrophic; 54 < TI 6 74, eutrophic and TI P 74, hipereutrophic. Results showed that, along the sampling period, all stations were considered hipereutrophic (Table 2), with no expressive differences among the years, pointing to systematic anthropic input, mostly through domestic sewage, which contains approximately 50% of human waste and 2030% of detergents (Khan and Ansari, 2005). The results were tested for signicant differences, considering the particularities between them. The KruskallWallis analysis revealed signicant differences between the three sampling periods (20072009) for temperature, suspended particulate material, dissolved oxygen, phaeophytin-a, phosphate and nitrite (Table 3). The same test did not reveal signicant differences for the same variables among the streams (Table 3), suggesting that the anthropic input is equivalent in the studied streams. Principal component analysis considered the three sampling periods altogether and revealed 49.61% of total variance. The rst two components explained only 29.51% of the total variance (Fig. 2), with minimum differences between them. The rst axis accounted for 20.10% of the total variance, and correlated positively with temperature, pH, SPM, chlorophyll-a, nitrite and nitrate, being this last one the most signicant component. The second axis accounted for 20.10% of the total variance, and correlated positively with pH, chlorophyll-a, SPM and phosphate, being this nutrient the most signicant component for the secondary variance. Both axis showed the main inuence of nitrate and phosphate in the sample variance, reecting a direct effect of anthropic input in the streams, and the decrease of dissolved oxygen related to it. Spearman correlation (Table 4), exhibited signicant positive correlation between pH and chlorophyll-a, suggesting a slight rise in pH during photosynthesis, what indeed was observed in the sampling points where phytoplanktonic blooms were observed. Suspended particulate matter correlated signicant and positively with phosphate and with phaeophytin a, and negatively with dissolved oxygen, suggesting that the increase in primary production

due to the excess of phosphorus, is followed by degradation corroborating the high contents of phaeophytin a and SPM causing low levels of DO in the streams. This hypothesis is corroborated by the signicant and positive correlation between phosphate and phaeophytin a. The positive and signicant correlation of nitrate with chlorophyll a and dissolved oxygen, conrms the limitation of primary production by nitrogen. Denitrication is a form of anaerobic microbial respiration in which nitrate is reduced to nitrous oxide or dinitrogen, and is a major sink for bioavailable nitrogen (Childs et al., 2002). Denitrication can also alter stoichiometric nutrient ratios and drive systems to nitrogen limitations (McCarthy et al., 2008). Water hypoxia or anoxia favors denitrication if nitrate is available for facultative bacteria, since they can get their oxygen directly by taking nitrogen out of water or by taking it off from nitrate molecules and therefore, in depleted oxygen water, nitrate becomes the primary oxygen source for microorganisms. Denitrication also requires carbon to occur, and the organic matter present in raw wastewater is usually enough for this transformation, which make the studied streams proper sites for this process, since they receive a great amount of domestic input. Despite the favoring conditions for denitrication, made by anoxia and high concentrations of nitrate, this process does not seem to proceed all the way to N2, since NO appears in elevated 2

Table 2 Nitrogen and phosphorus molar ratio and trophic index in Brandoas, Marimbondo, Guaxindiba and Imbuau streams. Stream Station 2007 N/P Brandoas Brandoas Brandoas Brandoas Brandoas Brandoas Marimbondo Marimbondo Marimbondo Marimbondo a Guaxindiba a Guaxindiba a Guaxindiba a Guaxindiba Imbuau Imbuau Imbuau Imbuau Imbuau Imbuau

2008 TI 133 131 122 132 130 122 133 121 107 129 127 126 124 121 125 125 N/P 0.70 0.29 0.04 0.10 0.04 0.04 0.03 0.03 0.12 0.11 0.30 0.87 0.06 0.18 4.13 0.14 0.10 0.78 TI 116 126 122 117 118 119 117 123 119 116 114 112 121 120 103 112 112 110

2009 N/P 0.04 0.04 0.05 0.06 0.05 0.05 0.03 0.03 1.33 0.02 0.07 0.60 0.27 0.06 0.07 0.07 0.06 0.08 0.10 2.25 TI 117 121 117 117 120 115 119 118 85 117 113 113 104 116 118 116 114 114 109 84 Fig. 2. Principal factor analysis (2-factors) performed with the data from the streams for 2007, 2008 and 2009.

1 2 3 4 5 6 1 2 3 4 1 2 3 4 1 2 3 4 5 6

0.03 0.01 0.09 0.02 0.07 0.07 0.10 0.05 0.39 0.04 0.18 0.07 0.04 0.18 0.26 0.52

Not sampled in 2007.

V.M. de C. Aguiar et al. / Marine Pollution Bulletin 62 (2011) 19151919 Table 4 Results of Spearman correlation analysis (p < 0.050). T T pH DO SPM Clor a Phae a NO 3 PO3 4 NO 2 1.00 pH 0.26 1.00 DO 0.04 0.05 1.00 SPM 0.18 0.44 0.32 1.00 Clor a 0.00 0.29 0.17 0.14 1.00 Phae a 0.12 0.33 0.09 0.45 0.23 1.00 NO 3 0.08 0.29 0.72 0.03 0.35 0.12 1.00 PO3 4 0.28 0.21 0.10 0.49 0.05 0.43 0.14 1.00


NO 2 0.12 0.07 0.10 0.19 0.25 0.06 0.49 0.47 1.00

concentrations along all the streams. The explanation for the high contents of nitrite in the water may be the presence of suldes which are highly favored by anoxia, inhibiting denitrication and releasing intermediates such as NO and N2O into the water 2 (Childs et al., 2002). The studied streams revealed themselves as major sources of nutrients, through raw sewage, to Guanabara Bay, showing a strong suppression of primary production contrasting with phytoplanktonic blooms along the sampling area, coupled with heavy loads of phosphate, nitrate and nitrite. Besides the economic importance of Guanabara Bay, this area is about to become the stage of important world events in a near future, what might be a chance to adopt measures to decrease the levels of pollution in this ecosystem. The studied area urges for environmental monitoring and recovery and further investigation of pollutants sources to Guanabara Bay, since it is has already collapsed from the ecological point of view. Acknowledgments The authors would like to thank the nancial support of Fundao de Amparo Pesquisa do Rio de Janeiro (FAPERJ) Process n. 151.155/07, and to Universidade Federal Fluminense (UFF), and also to Paula Falheiros, for the map. References
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