Effects of small hydropower plants on mercury

Environ Sci Pollut Res DOI 10.1007/s11356-017-9747-1

RESEARCH ARTICLE

Effects of small hydropower plants on mercury concentrations in fish Elaine C. Cebalho 1 & Sergi Díez 2 & Manoel dos Santos Filho 1 & Claumir Cesar Muniz 1 & Wilkinson Lázaro 1 & Olaf Malm 3 & Aurea R. A. Ignácio 1

Received: 2 March 2017 / Accepted: 10 July 2017 # Springer-Verlag GmbH Germany 2017

Abstract Although the impacts of large dams on freshwater biota are relatively well known, the effects of small hydropower plants (SHP) are not well investigated. In this work, we studied if mercury (Hg) concentrations in fish rise in two tropical SHP reservoirs, and whether similar effects take place during impoundment. Total Hg concentrations in several fish species were determined at two SHP in the Upper Guaporé River basin floodplain, Brazil. In total, 185 specimens were analysed for Hg content in dorsal muscle and none of them reported levels above the safety limit (500 μg kg−1) for fish consumption recommended by the World Health Organisation (WHO). The highest levels of Hg (231 and 447 μg kg−1) were found in carnivorous species in both reservoirs. Mercury increased as a function of standard length in most of the fish populations in the reservoirs, and higher Hg concentrations were found in fish at the reservoir compared with fish downstream. The high dissolved oxygen concentrations and high transparency of the water column (i.e. oligotrophic reservoir) together with the absence of thermal stratification may explain low Hg methylation and low MeHg levels found in fish after flooding. Overall, according to limnological characteristics of Responsible editor: Philippe Garrigues * Sergi Díez [email protected] * Aurea R. A. Ignácio [email protected] 1

Department of Biological Sciences, Mato Grosso State University, Cáceres, Mato Grosso, Brazil

2

Department of Environmental Chemistry, Institute of Environmental Assessment and Water Research (IDAEA-CSIC), Barcelona, Spain

3

Federal University of Rio de Janeiro, Carlos Chagas Filho Biophysics Institute, Rio de Janeiro, Brazil

water, we may hypothesise that reservoir conditions are not favourable to high net Hg methylation. Keywords Hg . Reservoir . Bioaccumulation . Biomagnification . Brazil . Pantanal

Introduction The construction of dams in rivers—whether for water supply or to generate electricity—leads to limnological changes in the aquatic environments at those sites. Dammed reservoirs are also responsible for an increase in mercury (Hg) in fish immediately after impoundment (Hylander et al. 2006), which can extend for decades (Schetagne and Verdon 1999). In aquatic environments, Hg can occur in several physical and chemical forms with a variety of properties; thus, determining its distribution, bioavailability and toxicity patterns is challenging. Among these forms, methylmercury (MeHg) is a cause of concern due to its neurotoxicity (Díez 2009) and because it bioaccumulates and biomagnifies through the aquatic food web (Ikingura and Akagi 2003). Metals deposited into the soil and released from plant material over thousands of years are made available when the soil is flooded (Hylander et al. 2006). Combined with this, the physical and chemical changes in water (e.g. temperature, pH, conductivity, dissolved oxygen) due to the flooding process itself favour bioaccumulation processes and consequently Hg biomagnification in the trophic chain (Pouilly et al. 2013). These processes occur in natural lakes but tend to be more pronounced in the reservoirs of hydroelectric plants, making fish consumption an important source of human MeHg exposure, especially predator species (Kehrig et al. 2008). Moreover, previous studies (Hylander et al. 2006) demonstrate that Hg levels in fish increased exponentially in 7 years.

Environ Sci Pollut Res

This increase was evident in fish within the reservoir and downstream from the impoundment, indicating that the flooding and impoundment effects are a threat to the health of the population who depend on fishing in the dam and downstream river for subsistence. Over the last few decades, 26 small hydropower plants (SHP) were built in the Brazilian state of Mato Grosso, in the Amazon basin (SEMA/MT 2015). According to the Brazilian Electricity Regulatory Agency (ANEEL), SHP are hydropower plants with installed capacity greater than 1 MW and less than or equal to 30 MW with a reservoir area ≤3 km2. In the Pantanal wetland (Da Silva and Girard 2004; Ioris 2013), the link between Hg emissions from gold mining and Hg levels in fish is not fully identified. In fact, recent studies (Ceccatto et al. 2016) in fish sampled in the Bento Gomes River, near the municipality of Poconé (MT, Brazil), which is an area affected by gold mining showed that Hg concentrations are low even in piscivorous species. Although a point source of Hg is not present in the northern part of Pantanal, some studies demonstrated that this environment promotes Hg methylation in periphyton (Guimarães et al. 1998; Lázaro et al. 2013). The subsequent incorporation of Hg in biota is observed in studies of fish (Ceccatto et al. 2016) and crocodiles (Lázaro et al. 2015). The objective of this work was to study the influence on fish Hg levels when constructing SHPs in tropical environments, such as the Pantanal wetland. We surveyed the levels of total Hg (Hg) in different fish species from two reservoirs and downstream sites. Variations in Hg concentration with sampling site, fish species and fish length were investigated in order to evaluate the impoundment effects.

Materials and methods Study area The Cabixi I (C1) and Cabixi II (C2) reservoirs are located on the Cabixi River (Fig. 1), which flows into the Upper Guaporé River basin. This river basin is located in the western Mato Grosso state and south-southeast Rondônia state. The Brazilian stretch of the Upper Guaporé covers up a total area of 43,961 km2. It crosses a region of rich biodiversity, consisting of an area of transition between the Pantanal and the Amazon. The sampling locations are located in the municipality of Comodoro, Mato Grosso. Cabixi I and Cabixi II small hydropower plants At each reservoir, a run-of-river hydroelectric generation plant is located, whereby little or no water storage is provided. The C1 reservoir (12° 57′ 24,00″ S; 60° 07′ 29 W), with a flooded area of 19 ha and a maximum depth of 4 m, began operating in 1995 and is located in the border between the municipalities of

Comodoro and Vilhena, in the states of Mato Grosso and Rondônia, respectively. The C2 reservoir (13° 01′ 10,00″ S; 60° 06′ 46,W), with a flooded area of 6.48 ha and a maximum depth of 3 m, began operating in 2002 and is located in the municipality of Comodoro, Mato Grosso state (Fig. 1). Limnological characteristics of sampled areas Limnological data, such as dissolved oxygen, electrical conductivity, pH, temperature, depth and Secchi transparency, were measured at each sampling site with a Horiba U-55 multi-parameter probe. The water in the reservoirs was of clear water type, acidic (4.56–4.88) and displayed small temperature variations (23.6–26.0 °C) during the sampling period. Conductivity was low during the flood period (9.9 μS cm−1) with a slight reduction during the drought period (6.98 μS cm−1) and dissolved oxygen showed high saturation for both periods (Table 1). A dense bed of macrophytes, represented by only one submerged and fixed species (Cabomba sp.), covered the lake bottom. Sample collection and processing In this study, 185 fish specimens were collected: 67 at the C1 reservoir, 75 at the C2 reservoir and 43 downstream from the C2 dam. Species Bujurquina cf. vittata, Eigenmania trilineata, Hoplerythrinus unitaeniatus, Astyanax sp. and Gymnotus inaequilabiatus were collected at C1. Species Hoplias lacerdae, Astyanax sp. and Geophagus sp. were collected at the C2 reservoir. Species Brycon falcatus, Astyanax sp., Leporius sp. and Pimelodella sp. were collected downstream from the C2 reservoir. The fish were collected during the flood and drought seasons, in early March and late June 2011, respectively. Gillnets, sweep and cast nets were used to collect the fish, which were immediately transferred to a refrigerated container. Once in the laboratory, the fish were measured and identified according to a manual for species identification (Britski et al. 1999). All procedures for collecting specimens conform to the 41671 and 4456-1 SISBIO License. Dorsal muscle samples (about 30 g) were dissected, immediately frozen and stored in a ziploc bag at −20 °C for Hg determination. In smaller fish (about 12 cm or shorter), the entire muscle was removed. Determination of Hg in fish Using the method by Bastos et al. (1998), a fresh weight (fw) sample of homogenised fish muscle (about 0.5 g fw) was treated in duplicate. In each tube, 1 mL of H2O2 (Merck) and 4 mL of a H2SO4/HNO3 (1:1 v/v) solution was added. The tubes then remained in a water bath at 60 °C until samples were fully solubilised. After cooling, 5 mL of KMnO4 5% (m/ v) solution was added. The tubes were again placed in a water

Environ Sci Pollut Res Fig. 1 Location of sampling points at the Cabixi River in the states of Mato Grosso and Rondônia at the Pantanal wetland, Brazil

Table 1 Limnological variables at the Cabixi I (C1) SHP reservoir and at the Cabixi II SHP dam (C2) and downstream (CD2) during the sampled periods

Period SHP C1 Drought SHP C2 Flood Drought

Site

pH

Conductivity (μS cm−1)

DO (mg/L)

C1

4.79

5.12

C2 CD2 C2 CD2

4.67 4.74 4.88 4.56

9.90 6.23 6.98 5.75

DO dissolved oxygen, °C temperature (our data collected in local)

DO (%)

T (°C)

6.37

80.3

23.6

6.86 7.51 7.89 7.89

89.9 104.3 103.5 98.6

25.9 – 26.0 24.5


bath at 60 °C for 30 min. All tubes were then covered in plastic film and left to rest for about 12 h. The next day, 1 mL of hydroxylamine was added to neutralise the oxidant medium. The final volume was adjusted to 13 mL with Milli-Q water, and detection was carried out right after. The Hg in the solution sample was detected and quantified using an atomic absorption spectrometer with flow injection system and cold Hg vapour (FIMS 400; Perkin Elmer). Certified reference materials were used to validate the method and were also analysed using the same fish sample extraction procedures. The THg concentration in the CRMs IAEA-436 and DORM-3 were found to be 4.10 ± 0.45 and 0.35 ± 0.07 μg kg−1 (n = 3), respectively, which are in good agreement to the certified values (4.19 ± 0.36 and 0.382 ± 0.060 μg kg−1). All duplicates showed a coefficient of variation lower than 15%. Statistical analyses Regression analysis was used to evaluate the relationship between Hg and standard length of analysed specimens. To evaluate whether Hg concentrations differed among populations and between trophic categories in the reservoirs, we used oneway ANOVA followed by Tukey HSD and t test analysis. All results were tested for normality and homoscedasticity. The significance level was established at 5% for the null hypothesis (p < 0.05).

Results and discussion Bioaccumulation and biomagnification of Hg in fish species At the C1 reservoir, the highest Hg concentration (446.6 μg kg−1 fw) was found in the carnivorous species H. unitaeniatus, whereas the omnivorous Astyanax sp. showed the lowest value (20.9 μg kg−1 fw) (Table 2). At the C2 reservoir, the highest Hg concentration was also found in a carnivorous species, in this case H. lacerdae with a value of 230.9 μg kg − 1 fw, while the lowest concentration (25.7 μg kg−1 fw) was found in the omnivorous Geophagus sp. (Table 2). However, downstream from this reservoir, the highest and lowest Hg concentrations were found in omnivorous Astyanax sp. and Leporinus sp. which displayed values of 153.18 and 46.13 μg kg−1 fw, respectively. We found evidence of a strong significant positive relationship between Hg concentrations in carnivorous species H. unitaeniatus (R = 0.715; p < 0.001) and H. lacerdae (R = 0.721; p < 0.001) and standard length (Fig. 2a, b) in C1 and C2 reservoirs. In relation to Astyanax sp. and Geophagus sp., we found a weak significant relationship for the same variables (Fig. 2c, d). Moreover, in the C1 reservoir, individuals of B. vittata (R = 0.10, p = 0.30) and the insectivore

E. trilineata (R = 0.26, p = 0.1) did not show a significant relationship between Hg concentrations and standard length. Total mercury concentrations in fish varied significantly in the different trophic categories at the C1 reservoir (ANOVA F(64,2) = 8.059; p < 0.001). According to results of the Tukey HSD test, it was observed that the highest variation in Hg concentrations concerning groups was when carnivores compared to insectivore (p = 0.004) and omnivore (p < 0.001) groups, but not between insectivore and omnivore groups (p = 0.952) (Fig. 3a). At the C2 reservoir, Hg concentrations were significantly higher in the muscle of carnivorous species when compared to omnivorous species (t = 2.387; p = 0.027) (Fig. 3b). The analysed omnivores and carnivores did not differ statistically between the C1 (t = 0.314; p = 0.751) and the C2 (t = 0.401; p = 0.174) reservoirs. Total Hg levels in fish are similar to those reported in previous studies in the Pantanal area during flood and drought periods and do not exceed the maximum threshold of 500 μg kg−1 (ICPS 1990) established by the World Health Organization (WHO). In general, Hg concentrations in carnivorous fish were lower than those found in areas with a history of contamination from gold mining, such as the Amazon basin, where Hg in H. malabaricus ranged from 55 to 1008 μg kg−1 fw, or even in previous studies in the Alto Pantanal (41 to 2048 μg kg−1 fw) (Hylander et al. 2000). Higher Hg concentrations in fish were also reported for other Brazilian areas polluted by Hg from gold mining activities and under the influence of large hydroelectric reservoirs in the Amazon (Malm et al. 2004; Kasper et al. 2012; Dominique et al. 2007; Kasper et al. 2014). Studies performed 20 years ago in the Tucuruí reservoir and River Mojú, in the state of Pará (Porvari 1995), found that the highest Hg concentrations were measured in predatory fish (1300 ± 890 μg kg−1), intermediate values in planktivorous and omnivorous fish (320 ± 200 μg kg−1) and the lowest values in herbivorous fish (110 ± 110 μg kg−1). Moreover, the Hg levels in fish collected both upstream and downstream of the Samuel dam, which is an Amazonian reservoir, were close to 600 and 1400 μg kg−1, respectively (Kasper et al. 2012). In the Pantanal, at the Manso hydroelectric power plant reservoir, Hg levels in all fishes, both in the reservoir and downstream, have increased drastically, five times or more, from background values (Tuomola et al. 2008). In the reservoir, carnivorous fish had an average Hg content of 1100 μg kg−1, whereas omnivorous fish had a concentration of 600 μg kg−1 (Tuomola et al. 2008). In comparison with other areas of the world, very low Hg values were found in fish caught in four Tanzanian reservoirs (Ikingura and Akagi 2003), where Hg content in fish tissue ranged from 5 to 40 μg kg−1, as well as in two newly built reservoirs located in southwestern China (Yao et al. 2011) which averaged 44 μg kg−1. A small catchment area associated with an absence of local Hg sources (gold mining, high soil Hg) may explain the low

Environ Sci Pollut Res Table 2 Concentration of THg (μg kg−1), standard length (SL, in cm) and weight (in g) of fish collected in the reservoir and downstream from Cabixi I and Cabixi II SHP dams. The results are expressed as mean and standard deviation between parenthesis Species

THg (min–max in μg kg−1)

Guild

Sampling site

N

SL

Weight

Eigenmania trilineata Hoplerythrinus unitaeniatus Astyanax sp.

Insectivore Carnivore Omnivore

Reservoir Reservoir Reservoir

12 14 28

19.85(4.06)a 10.51(3.62) 6.56(0.41)

8.18 (2.46)

46.24–124.6

29.32 (24.80) 6.69 (1.12)

40.91–446.6 20.86–207.3

Bujurquina cf. vittata

Omnivore

Reservoir

12

5.03(0.38)

6.00 (0.97)

22.89–73.30

Insectivore

Reservoir

1

18

15.13

68.79

Cabixi I (C1)

Gymnotus inaequilabiatus Cabixi II (C2)

a

Hoplias lacerdae

Carnivore

Reservoir

14

16.14(7.42)

145.47(217.49)

42.49–230.9

Astyanax sp. Geophagus sp.

Omnivore Omnivore

Reservoir Reservoir

23 38

5.87(0.43) 7.72(3.65)

3.60 (1.34) 27.89 (42.76)

32.30–206.7 25.67–105.2

Astyanax sp. Leporinus sp.

Omnivore Herbivore

Downstream Downstream

35 6

8.87(1.25) 10.9(1.04)

16.98 (7.33) 30.09 (9.66)

36.69–153.2 21.69–94.31

Brycon falcatus

Omnivore

Downstream

1

22.5

198.31

46.13

Pimelodella sp.

Omnivore

Downstream

1

10.6

10.57

120.8

Total length. To define the follow trophic guilds (Resende et al. 1996, 1998; Hahn et al. 1998; Pereira and Resende 2006)

values found in our study. Smaller reservoirs also have shorter food chains and thus a lower biomagnification capacity. The construction of big dams in big rivers (usually after large

catchment areas) causes the over-flooding of huge areas, creating new physicochemical and biological conditions associated with the long and complex food chains, common in big

Fig. 2 Hg concentration in the muscle of carnivorous and omnivorous fish in both reservoirs as a function of standard length. H. unitaeniatus (a); H. lacerdae (b); Astyanax sp. (c); Geophagus sp. (d)


Fig. 4 THg concentrations in muscle of Astyanax sp. collected at and downstream of the Small Hydropower Plant Cabixi II

Fig. 3 THg concentrations in the muscle of carnivorous, omnivorous and insectivorous fish at the Cabixi I (A) and Cabixi II (B). Different letters within the graph indicate significant differences

tropical rivers, which usually show higher Hg biomagnification (Hylander et al. 2006; Tuomola et al. 2008). Impoundment effect To evaluate the occurrence of the impoundment effect at the SHPs, Hg concentrations were compared in Astyanax sp., which was the single species collected both at the C2 reservoir and at downstream sites. Statistically significant differences in Hg (t = 3.047; p = 0.003) were observed between specimens from upstream and downstream sites, with higher Hg concentrations found in individuals in the reservoir compared with the individuals caught downstream (Fig. 4). This was unexpected because higher Hg levels in fish are usually reported downstream from dams (Malm et al. 2004; Dominique et al. 2007; Kasper et al. 2012), and this pattern is primarily associated with the stratification of the reservoir lake and the downstream discharge of hypolimnion waters enriched with MeHg (Kasper et al. 2012; Kasper et al. 2014). Hence, the stratification can cause anoxic conditions in the hypolimnion that

favours Hg methylation. In fact, in large and sufficiently deep reservoirs that undergo seasonal stratification, there exists a great potential for increased MeHg. This is one of the main causes for the increase in MeHg in the biota, both upstream and downstream (Canavan et al. 2000; Kasper 2009; Kasper et al. 2014). Consequently, in our study, the absence of thermal stratification in the C1 and C2 dams, due to the shallow depth of both reservoirs, is an important reason for low MeHg values found in fish. Additionally, the high dissolved oxygen concentrations and transparency of the water column observed in both reservoirs do not provide favourable conditions for net methylation. Both Cabixi reservoirs contain very transparent water, resulting in high light penetration allowing more efficient photodecomposition of MeHg in the water column (Hammerschmidt and Fitzgerald 2006). Besides oxic/anoxic conditions and transparency, the acidic condition of the water is frequently attributed to the greater methylation of Hg in sediments and hypolimnetic waters (Bloom et al. 1991). Nevertheless, studies in the Negro River (Belger and Forsberg 2006) suggest that the relation between pH and Hg may be different in tropical ecosystems as Hg in Hoplias malabaricus decreased at lower pH. Studies on Quebec reservoirs found that MeHg transported downstream is mainly in the dissolved phase, associated with suspended particulate matter, and incorporated mostly by plankton (Schetagne and Verdon 1999; Schetagne et al. 2000). On the contrary, studies in northern Manitoba reservoirs, there appeared to be downstream effects, but in Split Lake, there was no apparent effect of upstream flooding on Hg concentrations in fish (Bodaly et al. 2007). In the C1 reservoir, the lack of a significant difference between insectivores and omnivore groups may be due to the diet of the fish species. We hypothesised that this is related to fish exploiting the same food resource: given that Astyanax sp., B. vittata and E. trilineata species are able to exploit a wide range of food resources, from aquatic macrophytes to invertebrates (Giora et al. 2005; Corrêa et al. 2009; Mazzoni et al. 2010).


In the C2 reservoir, Astyanax sp. present significant differences in Hg concentration between upstream and downstream sites. Interestingly, no significant differences were found when all omnivorous species were grouped in a single pool and compared again. Feeding variation is expected between omnivorous species, since different species and even populations of the same species in this category can exploit several environmental resources. This variation enables the coexistence of species in nonoverlapping niches and can directly affect Hg concentrations in different species of the omnivorous group (Mirlean et al. 2005). Therefore, in addition to stratification, differences between Hg concentrations in fish upstream and downstream could be also associated with differences in the feeding habits and trophic levels of fish above and below the dam, as was previously described by Palermo et al. (2004). In large hydroelectric plants, the drift of fish and fingerlings downstream is one of the factors responsible for the increase in Hg at these locations, considering that these fish are crushed when they go through the turbines and mixed with the suspended material. Consequently, fish, primarily from the filtering and omnivorous trophic categories, come to feed on this matter, enriching their diet and, consequently, their concentrations of Hg (Kasper et al. 2012). Considering that our reservoirs are oligotrophic, our results regarding Hg levels in fish are at odds with what was expected based on previous works (Pickhardt et al. 2002; Chen and Folt 2005), which suggested that concentrations of Hg in fish are higher in oligotrophic lakes than in eutrophic lakes as a result of dilution by higher plankton biomass in the more eutrophic lakes. However, recent studies evidenced that biomagnification was higher in the most eutrophic lakes and lower in the oligotrophic lakes (Verburg et al. 2014a). Thus, a recent debate in the literature regarding this issue (Verburg 2014b; Clayden et al. 2014) highlights the need for more robust field studies.

Conclusions Newly constructed reservoirs in tropical environments are usually related to increasing levels of Hg in fish; however, in this study concentrations in several fish species in the Pantanal wetland were much lower than those from other studies in the Amazon basin. Furthermore, our results conflict with studies showing that fish downstream from a dam are more polluted by Hg than the reservoir itself. In fact, Hg concentration increased as a function of standard length in fish populations of several species in both reservoirs but not at downstream sites. Additionally, fish species in the reservoir showed higher Hg concentrations compared with fish downstream. The high dissolved oxygen concentrations and high transparency of the water column result in lower Hg net methylation after flooding. Moreover, the nonexistence of thermal

stratification, due to the shallow depth of both reservoirs, may be another reason for such low fish Hg values. We consider the idea that in oligotrophic lakes less Hg as well as less biomass are being exported downstream. Although mercury levels in fish did not exceed the maximum WHO threshold, according to literature on dietary habits in riverine communities of the Pantanal, there is a need to monitor Hg in fish at reservoirs with SHP plants in other regions in Mato Grosso state (preferably those installed less than 10 years ago), to prevent potential health risks. Acknowledgements Financial support was obtained from the Fundación BBVA (BIOCON06/113; Project EMECO). One of the authors acknowledges the FAPEMAT for a Graduate Fellowship.

References Bastos WR, Malm O, Pfeiffer WC, Cleary D (1998) Establishment and analytical quality control of laboratories for Hg determination in biological and geological samples in the Amazon. Brazil Ciência Cultura 50:255–260 Belger L, Forsberg BR (2006) Factors controlling Hg levels in two predatory fish species in the Negro river basin, Brazilian Amazon. Sci Total Environ 367:451–459 Bloom NS, Watras, CJ, Hurley JP (1991) Impact of acidification on the methylmercury cycle of remote seepage lakes. Water, Air, and Soil Pollution 56:477–491 Bodaly RA, Jansen WA, Majewski AR, Fudge RJP, Strange NE, Derksen AJ, Green DJ (2007) Postimpoundment time course of increased mercury concentrations in fish in hydroelectric reservoirs of Northern Manitoba, Canada. Arch Environ Contam Toxicol 53: 379–389. doi:10.1007/s00244-006-0113-4 Britski HA, Silimon KZ, Lopes BS (1999) Peixes do Pantanal: manual de identificação. Embrapa-SPI, Brasília/Embrapa Pantanal, Corumbá: 184 Canavan CM, Caldwell CA, Bloom NS (2000) Discharge of methylmercury enriched hypolimnetic water from a stratified reservoir. Sci Total Environ 260:159–170 Ceccatto APS, Testoni MC, ARA I, Santos-Filho M, Malm O, Díez S (2016) Mercury distribution in organs of fish species and the associated risk in traditional subsistence villagers of the Pantanal wetland. Environ Geochem Health 38:713–722. doi:10.1007/s10653015-9754-4 Chen CY, Folt C (2005) High plankton densities reduce mercury biomagnification. Environ Sci Technol 39:115–121 Clayden M, Kidd K, Wyn B, Kirk J, Muir D, O'Driscoll N (2014) Response to comment on BMercury biomagnification through food webs is affected by physical and chemical characteristics of lakes^. Environ Sci Technol 48:10526–10527 Corrêa CE, Petry AC, Hahn NS (2009) Influência do ciclo hidrológico na dieta e estrutura trófica da ictiofauna do rio Cuiabá, Pantanal MatoGrossense. Iheringia Sér Zool 99:456–463 Da Silva CJ, Girard P (2004) New challenges in the management of the Brazilian Pantanal and catchment area. Wet Eco Man 12:553–561 Díez S (2009) Human health effects of methylmercury exposure. Rev Environ Contam Toxicol 198:111–132 Dominique Y, Maury-Brachet R, Muresan B, Vigouroux R, Richard S, Cossa D, Mariotti A, Boudou A (2007) Biofilm and mercury availability as key factors for mercury accumulation in fish (Curimata cyprinoids) from a disturbed Amazonian freshwater system. Environ Toxicol Chem 26:45–52

Environ Sci Pollut Res Giora J, Fialho CB, Dufech APS (2005) Feeding habit of Eigenmannia trilineata Lopez Castello, 1966 (Teleostei: Sternopygidae) of Parque Estadual de Itapuã, RS, Brazil. Neotrop Ichthyol 3:291–298 Guimarães JRD, Meili M, Malm O, Brito EMS (1998) Hg methylation in sediments and floating meadows of a tropical lake in the Pantanal floodplain, Brazil. Sci Total Environ 213:165–175 Hahn NS, Agostinho AA, Gomes LC, Bini LM (1998) Estrutura trófica da ictiofauna do reservatório de Itaipu (Paraná – Brasil) nos primeiros anos de sua formação. Interciência 23(5):229–235 Hammerschmidt CR, Fitzgerald WF (2006) Photodecomposition of methylmercury in an arctic Alaskan lake. Environ Sci Technol 40: 1212–1216 Hylander LD, Pinto FN, Guimarães JRD, Meili M, Oliveira LJ, Castro e Silva E (2000) Fish mercury concentration in the Alto Pantanal, Brazil: influence of season and water parameters. Sci Total Environ 261:9–20 Hylander LD, Gröhn J, Tropp M, Vikström A, Wolpher H, Castro e Silva E, Meili M, Oliveira LJ (2006) Fish mercury increase in Lago Manso, a new hydroelectric reservoir in tropical Brazil. J Environ Manag 81:155–166 Ikingura JR, Akagi H (2003) Total mercury and methylmercury levels in fish from hydroelectric reservoirs in Tanzania. Sci Total Environ 304:355–368 Ioris AAR (2013) Rethinking Brazil’s Pantanal wetland: beyond narrow development and conservation debates. J Environ Develop 22:239–260 IPCS (1990). International Programme on Chemical Safety (Environmental Health Criteria 101: Methylmercury, World Health Organization, Geneva) http://www.inchem.org/documents/ehc/ehc/ ehc101.htm Kasper D, Palermo EFA, Dias ACMI, Ferreira GL, Leitão RP, Branco CWC, Malm O (2009) Mercury distribution in different tissues and trophic levels of fish from a tropical reservoir, Brazil. Neotrop Ichthyol 7:751–758 Kasper D, Palermo EFA, Branco CWC, Malm O (2012) Evidence of elevated mercury levels in carnivorous and omnivorous fishes downstream from an Amazon Reservoir. Hydrobiologia 694:87–98 Kasper D, Forsberg BR, Amaral JH, Leitão RP, Py-Daniel SS, Bastos WR, Malm O (2014) Reservoir stratification affects methylmercury levels in river water, plankton, and fish downstream from Balbina hydroelectric dam, Amazonas, Brazil. Environ Sci Technol 48: 1032–1040 Kehrig HA, Howard BM, Malm O (2008) Methylmercury in a predatory fish (Cichla spp.) inhabiting the Brazilian Amazon. Environ Pollut 154:68–76 Lázaro WL, Guimarães JRD, Ignácio ARA, da Silva CJ, Díez S (2013) Cyanobacteria enhance methylmercury production: a hypothesis tested in the periphytonn of two lakes in the Pantanal floodplain, Brazil. Sci Total Environ 456-457:231–238 Lázaro WL, de Oliveira RF, dos Santos-Filho M, da Silva CJ, Malm O, Ignácio ARA, Díez S (2015) Non-lethal sampling for mercury evaluation in crocodilians. Chemosphere 138:25–32 Malm O, Palermo EFA, Santos HSB, Rebelo MF, Kehrig HA, Oliveira RB, Meire RO, Pinto FN, Moreira LPA, Guimarães JRD, Torres JPM, Pfeiffer WC (2004) Transport and cycling of mercury in

Tucuruí reservoir, Amazon, Brazil: 20 years after fulfillment. RMZ Mater Geoenviron 51:1195–1198 Mazzoni R, Nery L, Iglesias RI (2010) Ecologia e ontogenia da alimentação de Astyanax janeiroensis (Osteichthyes, Characidae) de um riacho costeiro do Sudeste do Brasil. Biota Neotrop 10:53–60 Mirlean N, Larned ST, Nikora V, Kütter VT (2005) Mercury in lakes and lake fishes on a conservation-industry gradient in Brazil. Chemosphere 60:226–236 Palermo EFA, Kasper D, Reis TS, Nogueira S, Branco CWC, Malm O (2004) Mercury level increase in fish tissues downstream the Tucuruí Reservoir, Brazil. RMZ Mater Geoenviron 51:1292–1294 Pereira RAC, Resende EK (2006) Alimentação de Gymnotus cf. carapo (Pisces: Gymnotidae) e suas relações com a Fauna Associada às Macrófitas Aquáticas no Pantanal, Brasil. EMBRAPA-CPAP, Corumbá: 21 Pickhardt PC, Folt CL, Chen CY, Klaue B, Blum JD (2002) Algal blooms reduce the uptake of toxic methylmercury in freshwater food webs. Proc Natl Acad Sci U S A 99:4419–4423 Porvari P (1995) Mercury levels of fish in Tucurui hydroelectric reservoir and in River Mojti in Amazonia, in the state of Para brazil. Sci Total Environ 175:109–117 Pouilly M, Rejas D, Pérez T, Duprey JL, Molina CI, Hubas C, Guimarães JRD (2013) Trophic structure and mercury biomagnification in tropical fish assemblages, Iténez River, Bolivia. PLoS One 8(5):e65054. doi:10.1371/journal.pone.0065054 Resende EK, Pereira RAC, Almeida VLL, Silva AG (1996) Alimentação de peixes carnívoros da planície inundável do rio Miranda, Pantanal, Mato Grosso do Sul, Brasil. EMBRAPA-CPAP, Corumbá: 36 Resende EK, Pereira RAC, Almeida VLL, Silva AG (1998) Peixes onívoros da planície inundável do rio Miranda, Mato Grosso do Sul, Brasil. EMBRAPA-CPA,Corumbá: 28 Schetagne R, Verdon R (1999) Post-impoundment evolution of fish mercury levels at the La Grande complex, Québec, Canada from 1978 to 1996. In: Lucotte M, Schetagne R, Thérien N, Langlois C, Tremblay A (eds) Mercury in the biogeochemical cycle: natural environments and hydroelectric reservoirs of northern Québec, Environmental science series. Springer, Berlin, pp 235–258 Schetagne R, Doyo JF, Fournier JJ (2000) Export of mercury downstream from reservoirs. Sci Total Environ 260(1–3):135–145 SEMA/MT (2015) Accessed January 2017. http://sema.mt.gov.br Tuomola L, Niklasson T, Castro e Silva E, Hylander LD (2008) Fish mercury development in relation to abiotic characteristics and carbon sources in a six-year-old, Brazilian reservoir. Sci Total Environ 390:177–187 Verburg P (2014) Lack of evidence for lower mercury biomagnification by biomass dilution in more productive lakes: comment on mercury biomagnification through food webs is affected by physical and chemical characteristics of lakes. Environ Sci Technol 48:10524 Verburg P, Hickey C, Phillips N (2014) Mercury biomganification in three geothermally influenced lakes differing in chemistry and algal biomass. Sci Total Environ 493:342 Yao H, Feng XB, Guo YN, Yan HY, Fu XW, Li ZG, Meng B (2011) Mercury and methylmercury concentrations in 2 newly constructed reservoir in the Wujiang River, Guizhou, China. Environ Toxicol Chem 30:530–537