Assessment of mercury contamination in Brycon falcatus (Characiformes: Bryconidae) and human health risk by consumption of this fish from the Teles Pires River, Southern Amazonia

Liliane S. de Matos João Otávio S. Silva Daniele Kasper Lucélia N. Carvalho About the authors

ABSTRACT

Brycon falcatus is one of the most highly consumed species of fish within the region in the Teles Pires basin, and has great commercial importance in sport and professional artisanal fishing. The objective of this study was to analyze the presence and concentration of total mercury (THg) in the muscle, liver and gills of B. falcatus, and calculate the risk to human health of THg contamination from ingestion of the fish. THg concentrations were similar in the liver (0.076 mg kg-1) and muscle (0.052 mg kg-1), and higher than in the gills (0.009 mg kg-1). The levels of HgT present in B. falcatus tissues did not influence weight gain and nutritional status. Based on the condition factor, weight and length ratio and hepatosomatic index, it seems that the concentrations of THg did not influence the health and well-being of B. falcatus collected in the Teles Pires River basin. THg concentrations in the muscle of B. falcatus are below the limit recommended by the World Health Organization for people who consume until 250 g of fish per week. The risk of deleterious effects on human health may exist if there is a greater consumption of B. falcatus such as 340 g/day, that is the mean of fish consumption by indigenous and riverine.

Keywords:
Condition factor; Hepatosomatic index; Matrinxã; Tapajós basin; Weight-length relationship

RESUMO

Brycon falcatus é um dos peixes mais consumidos na região da bacia do rio Teles Pires, tendo grande importância comercial na pesca esportiva e profissional artesanal. O objetivo deste estudo foi analisar a presença e concentrações de mercúrio total (HgT) no músculo, fígado e brânquias do peixe B. falcatus. Foi calculado o risco para a saúde humana de contaminação por Hg pela ingestão deste pescado. As concentrações de HgT foram similares no fígado (0,076 mg.kg-1) e no músculo (0,052 mg.kg-1) e maiores do que nas brânquias (0,009 mg.kg-1). Os níveis de HgT presentes nos tecidos de B. falcatus não influenciaram no incremento de peso e estado nutricional. Com base no fator de condição, relação peso e comprimento e índice hepatossomático, aparentemente as concentrações de THg não influenciaram a saúde e o bem-estar de B. falcatus coletados na bacia do rio Teles Pires. As concentrações de THg no músculo de B. falcatus estão abaixo do limite recomendado pela Organização Mundial de Saúde para pessoas que consomem até 250 g de peixe por semana. O risco de efeitos deletérios para a saúde humana pode existir se houver um maior consumo de B. falcatus, como 340 g/dia, que é a média do consumo de peixe por indígenas e ribeirinhos.

Palavras-chave:
Bacia do Tapajós; Fator de Condição; Índice hepatossomático; Matrinxã; Relação peso-comprimento

Introduction

Cattle farming, agriculture and tannery operations are the current main economic activities within the Teles Pires River basin (Brazil). Trace elements such as Cu, Hg, and Cd are widely used in fungicides, fertilizers, bactericides and disinfectants in agricultural practices (Micaroni et al., 2000Micaroni RCCM, Bueno MIMS, Jardim WF. Compostos de mercúrio. Revisão de métodos de determinação, tratamento e descarte. Quim Nova. 2000; 23(4):487-95. Available from: http://dx.doi.org/10.1590/S0100-40422000000400011
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; Penteado, 2000Penteado SR. Controle alternativo de pragas e doenças com as caldas bordalesa, sulfocálcica e viçosa. Campinas: Bueno Mendes Gráfica e Editora; 2000.; Grant, Sheppard, 2008Grant CA, Sheppard SC. Fertilizer impacts on cadmium availability in agricultural soils and crops. Hum Ecol Risk Assess. 2008; 14(2):210-28. Available from: https://doi.org/10.1080/10807030801934895
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; Sfredo, 2008Sfredo GJ. Soja no Brasil, calagem, adubação e nutrição mineral. Londrina: Embrapa Soja; 2008.). In the 1970s, intense logging activity began with consequent increases in deforestation, burning and erosion (Cordeiro et al., 2002Cordeiro RC, Turcq B, Ribeiro MG, Lacerda LD, Capitâneo J, Oliveira da Silva A, Sifeddine A, Turcq PM. Forest fire indicators and mercury deposition in an intense land use change region in the Brazilian Amazon (Alta Floresta, MT). Sci Total Environ . 2002; 293(1-3):247-56. Available from: https://doi.org/10.1016/S0048-9697(02)00045-1
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). Forest burning, extensive cattle farming and soybean plantations led to the erosion of soils naturally rich in mercury (Lechler et al., 2000Lechler PJ, Miller JR, Lacerda LD, Vinson D, Bonzongo JC, Lyons WB, Warwick JJ. Elevated mercury concentrations in soils, sediments, water, and fish of the Madeira river basin, Brazilian Amazon: a function of natural enrichments? Sci Total Environ . 2000; 260(1-3):87-96. Available from: https://doi.org/10.1016/S0048-9697(00)00543-X
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). Soils of the Amazon region present naturally high Hg concentrations, often higher than those observed globally (Roulet, Lucotte, 1995Roulet M, Lucotte M. Geochemistry of mercury in pristine and flooded ferralitic soils of a tropical rain forest in French Guiana, South America. Water Air Soil Pollut. 1995; 80(1-4):1079-88. Available from: https://doi.org/10.1007/BF01189768
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; Fadini, Jardim, 2001Fadini PS, Jardim WF. Is the Negro River Basin (Amazon) impacted by naturally occurring Hg? Sci Total Environ . 2001; 275(1-3):71-82. Available from: https://doi.org/10.1016/S0048-9697(00)00855-X
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; Wasserman et al., 2003Wasserman JC, Hacon S, Wasserman MA. Biogeochemistry of mercury in the Amazonian Environment. Ambio. 2003; 32(5): 336-42. Available from: <https://www.ncbi.nlm.nih.gov/pubmed/14571962>
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). In the Tapajos River basin an increase in the deposition of Hg in lacustrine sediments was observed in the 1970s (Roulet et al., 2000Roulet M, Lucotte M, Canuel R, Farella N, Courcelles M, Guimarães JRD et al. Increase in mercury contamination recorded in lacustrine sediments following deforestation in the central Amazon. Chem Geol. 2000; 165(3-4): 243-66. Available from: https://doi.org/10.1016/S0009-2541(99)00172-2
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), coinciding with the beginning of intense colonization of the Amazon. These authors have suggested that the colonization of drainage basins and increased land exploration in the Amazon increased the leaching of naturally present mercury from the soil into rivers. In addition, intense gold prospecting activities occurred between the 1970s and 90s in northern Mato Grosso State (where the Teles Pires River basin is located), declining after this period due to the depletion of easily accessible gold deposits (Lobo et al., 2016Lobo FL, Costa M, Novo EMLM, Telmer K. Distribution of artisanal and small-scale gold mining in the Tapajós River Basin (Brazilian Amazon) over the past 40 years and relationship with water siltation. Remote Sens. 2016; 8(7), 579:1-22. Available from: http://www.mdpi.com/2072-4292/8/7/579
http://www.mdpi.com/2072-4292/8/7/579...
). Subsequently, gold prospecting was replaced by agriculture and cattle farming, where fire was used as a way to open new areas for these activities (Cordeiro et al., 2002Cordeiro RC, Turcq B, Ribeiro MG, Lacerda LD, Capitâneo J, Oliveira da Silva A, Sifeddine A, Turcq PM. Forest fire indicators and mercury deposition in an intense land use change region in the Brazilian Amazon (Alta Floresta, MT). Sci Total Environ . 2002; 293(1-3):247-56. Available from: https://doi.org/10.1016/S0048-9697(02)00045-1
https://doi.org/10.1016/S0048-9697(02)00...
).

Among various pollutants, trace elements represent an important group of interest due to their bioaccumulation and toxicity in living organisms (Islam, Tanaka, 2004Islam MS, Tanaka M. Impacts of pollution on coastal and marine ecosystems including coastal and marine fisheries and approach for management: a review and synthesis. Mar Pollut Bul. 2004; 48(7-8):624-49. Available from: https://doi.org/10.1016/j.marpolbul.2003.12.004
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; Abdallah, 2008Abdallah MAM. Trace element levels in some commercially valuable fish species from coastal waters of Mediterranean Sea, Egypt. J Mar Syst. 2008; 73:114-22. Available from: https://doi.org/10.1016/j.jmarsys.2007.09.006
https://doi.org/10.1016/j.jmarsys.2007.0...
). Hg, in particular, is a trace element that biomagnifies along food chains, thus, it is worrying to top levels organisms as piscivorous fish and humans, for example. For teleost fish, the bioavailability of Hg depends not only on its total concentration in the environment but also its chemical species and capacity of absorption through different tissues of the fish (Sweet, Zelikoff, 2001Sweet LI, Zelikoff JT. Toxicology and immunotoxicology of mercury: a comparative review in fish and humans. J Toxicol Environ Heatlth B Crit Rev. 2001; 4(2):161-205. Available from: https://doi.org/10.1080/10937400117236
https://doi.org/10.1080/10937400117236...
). In the organs, Hg first crosses the epithelium to the blood, which transports it through the bloodstream to the tissues. The gills, the digestive system and, to a lesser extent, the skin, are the main sites of mercury capture in fish (Erickson et al., 2008Erickson RJ, Nichols JW, Cook PM, Ankley GT. Bioavailability of chemical contaminants in aquatic systems. In: Di Giulio RT, Hinton DE, editors. The Toxicology of Fishes. Florida, USA: CRC Press - Taylor & Francis Group; 2008. p. 9-45. https://doi.org/10.1201/9780203647295.ch2
https://doi.org/10.1201/9780203647295.ch...
). The primary target tissues of Hg are the central nervous system and the kidney, causing brain damage, abnormal motor coordination, behavioral changes, alterations that impair growth, reproduction and development of the fish (Clarkson et al., 2003Clarkson TW, Magos L, Myers GJ. The toxicology of mercury-current exposures and clinical manifestations. N Engl J Med. 2003; 349(18):1731-37. Available from: https://doi.org/10.1056/NEJMra022471
https://doi.org/10.1056/NEJMra022471...
). Mercury-induced toxicity in the liver can severely affect morphology and structure, impairing its functional role by interfering with key physiological and metabolic processes (Macirella et al., 2016Macirella R, Guardia A, Pellegrino D, Bernabò I, Tronci V, Ebbesson LOE et al. Effects of two sublethal concentrations of mercury chloride on the morphology and metallothionein activity in the liver of zebrafish (Danio rerio). Int J Mol Sci. 2016; 17(3):361-77. Available from: http://www.mdpi.com/1422-0067/17/3/361
http://www.mdpi.com/1422-0067/17/3/361...
). Some fish organs are commonly used to determine the bioaccumulation of total mercury (THg), such as the liver, as it plays vital roles in the accumulation, biotransformation and excretion of contaminants (Figueiredo-Fernandes et al., 2006Figueiredo-Fernandes A, Fontainhas-Fernandes A, Monteiro R, Reis-henriques MA, Rocha E. Effects of the fungicide mancozeb on liver structure of Nile Tilapia, Oreochromis niloticus: Assessment and quantification of induced cytological changes using qualitative histopathology and the stereological point-sampled intercept method. Bull Environ Contam Toxicol . 2006; 76(2):249-55. Available from: https://doi.org/10.1007/s00128-006-0914-1
https://doi.org/10.1007/s00128-006-0914-...
). The gills have a large surface area in contact with contaminants present in the water, therefore, they are an important route of exposure of the organism. High concentrations of Hg in the gills may reflect a transitory state before it is eliminated from that organ (Huang et al., 2012Huang SS-Y, Strathe AB, Fadel JG, Lin P, Liu T-Y, Hung SSO. Absorption, distribution, and elimination of graded oral doses of methylmercury in juvenile white sturgeon. Aquat Toxicol. 2012; 122-123:163-71. Available from: https://doi.org/10.1016/j.aquatox.2012.06.003
https://doi.org/10.1016/j.aquatox.2012.0...
). Finally, evaluating the fish muscle helps determine the direct transfer of Hg to humans, as this is the most consumed part of the fish.

Fish are an important source of protein in the human diet, and represent one of the major sources of Hg ingestion via the food chain. High concentrations of Hg in humans can cause damage to the neurological and immunological systems, congenital malformations and teratogenic effects (Akagi et al., 1995Akagi H, Malm O, Kinjo Y, Harada M, Branches FJP, Pfeiffer WC, Kato H. Methylmercury pollution in the Amazon, Brazil. Sci Total Environ. 1995; 175(2):85-95. Available from: https://doi.org/10.1016/0048-9697(95)04905-3
https://doi.org/10.1016/0048-9697(95)049...
). There are several studies in the Teles Pires River basin investigating Hg contamination in humans through fish consumption (Akagi et al., 1995Akagi H, Malm O, Kinjo Y, Harada M, Branches FJP, Pfeiffer WC, Kato H. Methylmercury pollution in the Amazon, Brazil. Sci Total Environ. 1995; 175(2):85-95. Available from: https://doi.org/10.1016/0048-9697(95)04905-3
https://doi.org/10.1016/0048-9697(95)049...
; Malm et al., 1995Malm O, Branches FJP, Akagi H, Castro MB, Pfeiffer WC, Harada M et al. Mercury and methylmercury in fish and human hair from the Tapajós River basin, Brazil. Sci Total Environ . 1995; 175(2):141-50. Available from: https://doi.org/10.1016/0048-9697(95)04910-X
from: https://doi.org/10.1016/0048-9697(...
; Malm et al., 1997Malm O, Guimarães JRD, Castro MB, Bastos WR, Viana JP, Branches FJP et al. Follow-up of mercury levels in fish, human hair and urine in the Madeira and Tapajós basins, Amazon, Brazil. Water Air Soil Pollut . 1997; 97(1-2):45-51. Available from: https://doi.org/10.1007/BF02409643
https://doi.org/10.1007/BF02409643...
; Hacon et al., 1997Hacon S, Yokoo E, Valente J, Campos RC, Da Silva VA, De Menezes ACC et al. Exposure to mercury in pregnant women from Alta Floresta - Amazon Basin, Brazil. Environ Res . 2000; 84(3): 204-10. Available from: https://doi.org/10.1006/enrs.2000.4115
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; Barbosa et al., 1997Barbosa AC, Garcia AM, Souza JR. Mercury contamination in hair of riverine populations of Apiacás Reserve in the Brazilian Amazon. Water Air Soil Pollut. 1997; 97(1-2):1-8. Available from: https://doi.org/10.1023/A:1018336820227
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; Hacon et al., 2000Hacon S, Yokoo E, Valente J, Campos RC, Da Silva VA, De Menezes ACC et al. Exposure to mercury in pregnant women from Alta Floresta - Amazon Basin, Brazil. Environ Res . 2000; 84(3): 204-10. Available from: https://doi.org/10.1006/enrs.2000.4115
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; Dorea et al., 2005Dórea JG, de Souza JR, Rodrigues P, Ferrari I, Barbosa AC. Hair mercury (signature of fish consumption) and cardiovascular risk in Munduruku and Kayabi Indians of Amazonia. Environ Res . 2005; 97(2):209-19. Available from: https://doi.org/10.1016/j.envres.2004.04.007
https://doi.org/10.1016/j.envres.2004.04...
). However, these studies were performed at contaminated sites. From a food safety point of view, it is important for studies to focus on commonly consumed species of fish and popular fishing sites with professional and amateur fishermen (Kensová et al., 2012Kensová R, Kružíková K, Svobodová Z. Mercury speciation and safety of fish from important fishing locations in the Czech Republic. Czech J Food Sci. 2012; 30(3):276-84. Available from: http://www.agriculturejournals.cz/publicFiles/63476.pdf
http://www.agriculturejournals.cz/public...
). The fish species Brycon falcatus (Müller & Troschel, 1844Miller JC, Miller JN. Statistics for Analytical Chemistry. GreatBritain: Ellis Horwood; 1994.), commonly known as matrinxã, is one of the most highly consumed species in the region due to its excellent quality of meat.

Considering the current scenario of multiple uses of the Teles Pires River basin, and therefore potential mercury contamination, the objectives of this study were to evaluate: (1) the total concentration of THg in the muscle, gills and liver of B. falcatus, (2) whether THg contamination was interfering with the well-being of collected fish, and (3) the risk to human health associated with the consumption of THg in B. falcatus muscle tissue. Our hypotheses are: (1) Since the liver is an important organ of detoxification of contaminants, it will present higher THg levels when compared to the other tissues analyzed (gills and muscle); (2) Fish will present a strict correlation between THg contamination and its condition factor, weight and length ratio and hepatosomatic index, indicating that Hg exposure is interfering with their growth and sanity; (3) The B. falcatus specimens will present low levels of THg in the muscle since are omnivorores, representing a low risk to human health even at high rates of fish consumption in that region.

Material and Methods

Study area. The Teles Pires River basin is located in northern Mato Grosso State (Brazil), and is one of the main tributaries of the Tapajós River basin. Fish were collected from the Celeste River (12°24’56.00”S 55°31’28.00” W) in the municipality of Vera, the Verde River (11°4’1.99”S 55°34’17.00”W) in the municipality of Sorriso, and from the Teles Pires River (11°34’48.00” S and 55°39’5.00” W) in the municipality of Sinop (Fig. 1). There is no history of gold prospecting activities within the studied areas, however the soil is subject to intense use, primarily through cattle farming, agriculture and tannery activities.

Fig. 1a
Brazil, with the state of Mato Grosso marked as stripes. b. The state of Mato Grosso with the Teles Pires River shown in bold. b. Brycon falcatus sample collection sites (black circles), accompanied by pictographs of the main human activities found at each site. The black arrow indicates the flow direction of rivers. The specimens were collected from November 2014 to October 2016.

Fish collection and biometrics. Fish samples were collected from November 2014 to October 2016 using fishing rods and artificial bait. Five specimens were collected on the Celeste river, 33 on the Teles Pires River and 7 on the Verde River. After capture, fish were euthanized with a dose of 287 mg L-1 of Eugenol® for approximately 600 s (American Veterinary Medical Association, 2001American Veterinary Medical Association. Report of the AVMA panel on euthanasia. J Am Vet Med Assoc. 2001; 218(5): 669-96.; Vidal et al., 2008Vidal LVO, Albinati RCB, Albinati ACL, Lira AD, Almeida TR, Santos GB. Eugenol como anestésico para a tilápia do Nilo. Pesq Agropec Bras. 2008; 43(8):1069-74. Available from: http://dx.doi.org/10.1590/S0100-204X2008000800017
http://dx.doi.org/10.1590/S0100-204X2008...
), then submerged in ice and packed in plastic bags. Samples were transported to the laboratory where total length, standard length and weight were measured for each specimen. The liver, gills and dorsolateral muscle (region below the dorsal fin and above the lateral line) were removed. These three tissues were stored at -20°C until analysis for THg concentration. Brycon falcatus specimens were catalogued at the Universidade Estadual de Campinas museum (ZUEC 9190) and the Acervo Biológico da Amazônia Meridional of the Universidade Federal de Mato Grosso (Núm. catalogo?).

THg analysis. Tissue samples were digested as described by Zhou, Wong (2000Zhou HY, Wong MH. Mercury accumulation in freshwater fish with emphasis on dietary influences. Water Res. 2000; 34(17):4234-42. Available from: https://doi.org/10.1016/S0043-1354(00)00176-7
https://doi.org/10.1016/S0043-1354(00)00...
), with 8 ml of HNO3:H2SO4 (2:1 v/v) solution at 25°C for 3 h, and then 60°C for 5 h. Five ml of 30% H2O2 were added and temperature maintained at 65°C until samples were light in color. Samples were added to 25 ml of distilled H2O, and the determination of THg concentration was performed with a Cold Vapor Atomic Absorption Spectrometer (Spectrometer model AA 140, Varian).

Quality Assurance of Analyses. To verify the accuracy of the analytical method, a commercial certified sample (TORT-2 lobster hepatopancreas) provided by the National Research Council of Canada was analyzed. TORT-2 recovery was 81±6% for THg (n=2). Spikes were also made with muscle tissue samples, oven dried at 40ºC to a constant weight, macerated, mixed with 10 mg/L THg solution, oven dried and macerated a second time, weighed and then subjected to the same digestion process as the previous tissue samples. These spikes (n=4) showed a recovery of 91±3% for THg. The THg concentration of samples within this study represent the uncorrected analytical results for the observed recovery in spikes and/or TORT-2. Blank (n=10) were periodically analyzed to test for any memory effect in the analysis and to evaluate any possible contamination of glassware, reagents and the laboratory atmosphere itself. The detection limit corresponds to the mean concentration of blanks samples plus three times the standard deviation (Miller, Miller, 1994). The detection limit was 0.063 μg/L.

Weight-length relationship and condition factor. The condition factor (K) is often used as an indicator of the degree of a species’ well-being. A K with values close to or greater than 1 generally indicates well-nourished and healthy fish, and K values below 0.8 indicate underweight fish (Cizdziel et al., 2002Cizdziel JV, Hinners TA, Pollard JE, Heithmar EM, Cross CL. Mercury concentrations in fish from lake mead, USA, related to fish size, condition, trophic level, location, and consumption risk. Arch Environ Contam Toxicol. 2002; 43(3):309-17. Available from: https://doi.org/10.1007/s00244-002-1191-6
https://doi.org/10.1007/s00244-002-1191-...
). The condition factor and weight-length relationship were analyzed according to Santos (1978Santos EP. Dinâmica de populações aplicada à pesca e piscicultura. São Paulo: Hucitec; 1978.) and Braga (1986Braga FMS. Estudo entre fator de condição e relação peso-comprimento para alguns peixes marinhos. Braz J Biol. 1986; 46(2):339-46.). The allometric condition factor was calculated using the formula K = W/Lb, where W = weight, L = standard length and b = regression coefficient. The weight-length relationship was estimated using the expression W = aLb, where W = weight, a = intercept, L = standard length, and b = angular coefficient (Le Cren, 1951Le Cren ED. The length-weight relationship and seasonal cycle in gonad weight and condition in the perch (Perca fluviatilis). J Anim Ecol. 1951; 20(2):201-19. Available from:<http://www.jstor.org/stable/1540>
http://www.jstor.org/stable/1540...
). The parameters a and b were estimated after logarithmic transformation of the weight and length data and subsequent adjustment of the line of best fit using the least squares method (Vanzolini, 1993Vanzolini PE. Métodos estatísticos elementares em sistemática zoológica. São Paulo: Hucitec ; 1993.). Le Cren (1951Le Cren ED. The length-weight relationship and seasonal cycle in gonad weight and condition in the perch (Perca fluviatilis). J Anim Ecol. 1951; 20(2):201-19. Available from:<http://www.jstor.org/stable/1540>
http://www.jstor.org/stable/1540...
) states that the b values range from 2.0 to 4.0, assuming the value 3.0 for an “ideal fish” which maintains the same shape during ontogenetic growth. Values less or greater than 3.0 indicate individuals that become “longer” or more “round” during growth, respectively. The degree of association between weight and standard length was measured by coefficient of determination (r2).

Hepatosomatic Index (HSI). The HSI reflects a fish’s metabolic energy demand and can be considered as a general indicator of the health of fish which are sensitive to environmental contaminants (Everaarts et al., 1993Everaarts JM, Shugart LP, Gustin MK, Hawkings WE, Walker WW. Biological markers in fish: DNA integrity, hematological parameters and liver somatic index. Mar Environ Res. 1993; 35(1-3):101-07. Available from: https://doi.org/10.1016/0141-1136(93)90021-Q
https://doi.org/10.1016/0141-1136(93)900...
). An increase in liver weight may indicate an increase in the enzymatic detoxification process. In this way, the HSI can be used as a biomarker when fish are exposed to substances toxic to the liver (Haux, Larsson, 1984Haux C, Larsson A. Long-term sublethal physiological effects on rainbow trout, Salmo gairdneri, during exposure to cadmium and after subsequente recovery. In: Di Giulio RT, Hinton DE, editors. The Toxicology of Fishes . New York-NY: CRC Presss, Taylor & Francis Group; 1984. p. 129-142.). The HSI was calculated using the formula described by Vazzoler (1981Vazzoler AEAM. Manual de métodos para estudos biológicos de população de peixes. Reprodução e crescimento. Brasília: CNPq - Programa Nacional de Zoologia. 1981.):

H S I = 100 x ( l i v e r w e i g h t ( g ) / t o t a l b o d y w e i g h t ( g )

Estimated risk to human health. The human health risk assessment was performed in accordance with the United States Environmental Protection Agency (USEPA, 2000United States Environmental Protection Agency (USEPA). Guidance for Assessing Chemical Contamination Data for Use in Fish Advisories. Volume 1: Fish Sampling and Analysis, and Volume 2: Risk Assessment and Fish Consumption Limits. 3rd ed. Cincinnati: U.S. Environmental Protection Agency Report EPA 823-B-97-009; 2000.). We used an approach based on four different consumption rates of B. falcatus: average consumption for consumers in Mato Grosso, Brazil, Instituto Brasileiro de Geografia e Estatística (IBGE, 2011Instituto Brasileiro de Geografia e Estatística (IBGE). Pesquisa de orçamentos familiares 2008-2009: análise do consumo alimentar pessoal no Brasil / IBGE, Coordenação de trabalho e Rendimento. Rio de Janeiro: IBGE; 2011.), average consumption for typical adults (USEPA, 2000United States Environmental Protection Agency (USEPA). Guidance for Assessing Chemical Contamination Data for Use in Fish Advisories. Volume 1: Fish Sampling and Analysis, and Volume 2: Risk Assessment and Fish Consumption Limits. 3rd ed. Cincinnati: U.S. Environmental Protection Agency Report EPA 823-B-97-009; 2000.), consumption for regular adult consumers (USEPA, 2000United States Environmental Protection Agency (USEPA). Guidance for Assessing Chemical Contamination Data for Use in Fish Advisories. Volume 1: Fish Sampling and Analysis, and Volume 2: Risk Assessment and Fish Consumption Limits. 3rd ed. Cincinnati: U.S. Environmental Protection Agency Report EPA 823-B-97-009; 2000.), and consumption for riverine and indigenous populations (Fréry et al., 2001Fréry N, Maury-Brachet R, Maillot E, Deheeger M, Mérona B, Boudou A. Gold-mining activities and mercury contamination of native Amerindian communities in French Guiana: key role of fish in dietary uptake. Environ Health Perspect. 2001; 109(5):449-56. Available from: http://www.jstor.org/stable/3454702
http://www.jstor.org/stable/3454702...
). For each of the four rates, we calculated the mean daily human intake of THg using the specimens with the lowest and highest THg concentration. To calculate the level of THg exposure resulting from the consumption of fish muscle tissue (the most commonly consumed tissue), the mean daily THg intake (MDI) equation was calculated as follows:

M D I ( m g k g d a y ) = ( C * C R ) / ( B W )

Where: C = concentration of THg in fish muscle tissue (mg kg-1), CR = mean consumption rate: 0.030 kg day for typical adults, 0.142 kg day for regular adult consumers, 0.009 kg day for consumers in Mato Grosso (IBGE, 2011Instituto Brasileiro de Geografia e Estatística (IBGE). Pesquisa de orçamentos familiares 2008-2009: análise do consumo alimentar pessoal no Brasil / IBGE, Coordenação de trabalho e Rendimento. Rio de Janeiro: IBGE; 2011.) and 0.340 kg day for indigenous and riverine populations (Fréry et al., 2001Fréry N, Maury-Brachet R, Maillot E, Deheeger M, Mérona B, Boudou A. Gold-mining activities and mercury contamination of native Amerindian communities in French Guiana: key role of fish in dietary uptake. Environ Health Perspect. 2001; 109(5):449-56. Available from: http://www.jstor.org/stable/3454702
http://www.jstor.org/stable/3454702...
), BW = subject’s body weight (70 kg was used).

The risk assessment was quantified by calculating the risk index (RI), which is expressed as the ratio between MDI and the oral reference dose (RfD) of mercury, and gives an idea of how many times above or below the recommended dose the population in question is being exposed to. The RI was calculated according to the following equation:

R I = M D I / R f D

Where RfD is the exposure to mercury to the human that is likely to be without noticeable risk to human health during a lifetime. The present work used RfD of 0.0001 mg kg-1 body weigth/day that is suggested by World Health Organization (WHO, 2008World Health Organization (WHO). United Nations Environment Programme. Guidance for identifying populations at risk from mercury exposure. Geneva: World Health Organization; 2008.) for methylmercury (since almost all THg of muscle of fish is methylmercury) that includes the sensitive groups. Therefore, this RfD used intends to represents the worst scenario of mercury ingestion that should be considered when risk is assessed (the methylmercury ingestion by sensitive groups). Risk index values <1.0 indicate that population exposure is less than the acceptable dose and is likely to be without noticeable risk to human health (WHO, 2008World Health Organization (WHO). United Nations Environment Programme. Guidance for identifying populations at risk from mercury exposure. Geneva: World Health Organization; 2008.). If the IR is ≥1.0, then population exposure is equal to or greater than the recommended acceptable dose, and the potential for adverse health effects increases.

Statistical analysis. Considering that B. falcatus is a migratory species, and that the distance between the three collection sites is no more than approximately 100 km, fish sampled from the three localities were analyzed collectively. Therefore, all data analyses cited above (weight-length relationship, K, HSI, MDI, RI) and subsequent analyses were performed by combining all specimens from the three locations.

Non-normality in the data distribution was verified through the Shapiro-Wilk test. As a result, a non-parametric Kruskal-Wallis test was used to test for differences in THg concentration between B. falcatus tissues. Spearman’s correlation was used to verify any correlation between THg concentration in muscle tissue and condition factor, and between THg in the liver and the HSI. In a previous analysis we found that the variables weight and standard length were dependent, therefore to verify if THg concentration within the tissues was affecting the weight increase of fish, a multiple linear regression was used, using the following model:

l m ( l o g ( w e i g h t ) ~ l o g ( s t a n d a r d l e n g t h ) + T H g c o n c e n t r a t i o n

All analyzes were performed using the Statistical Software R v. 3.3.2 (R Core Team, 2017R Development Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing; 2017.Available from http://www.r-project.org/
http://www.r-project.org/...
).

Results

Forty-five Brycon falcatus individuals were collected and analyzed from the three collection sites within the Teles Pires river basin (Tab. 1). THg concentrations were higher in liver and muscle tissue than in the gills of fish (p=5.96e-10, Kruskal-Wallis, level of 5% probability) (Tab. 2). THg concentration in the muscle tissue (the most commonly consumed part of the fish) was below the World Health Organization (WHO, 2008World Health Organization (WHO). United Nations Environment Programme. Guidance for identifying populations at risk from mercury exposure. Geneva: World Health Organization; 2008.) recommended values for THg in fish intended for human consumption (Tab. 2). The RI values for B. falcatus muscle consumption ranged from 0.01 to 8.74 (Tab. 3).

Tab. 1
Mean and range of total length (TL), standard length (SL) and weight (g) of Brycon falcatus specimens from rivers in the Teles Pires River basin collected from November 2014 to October 2016.

Tab. 2
THg concentration (mean ± standard deviation, in mg kg-1 wet weight) in tissues of Brycon falcatus collected from the Teles Pires River basin and the recommended limit of THg in fish for human consumption (WHO, 2008World Health Organization (WHO). United Nations Environment Programme. Guidance for identifying populations at risk from mercury exposure. Geneva: World Health Organization; 2008.). Same letter indicates no statistical difference, while different letters indicate statistical difference (p=5.96e-10, Kruskal-Wallis, level of 5% probability). The specimens were collected from November 2014 to October 2016.

Tab. 3
Range of average daily intake (MDI) and risk index of adverse health effects (RI) calculated based on four different rates of fish consumption (typical consumers, regular consumers, consumers in the state of Mato Grosso and indigenous and riverine frequent consumers; consumption rates described in Material and Methods). RfD = oral reference dose (0.0001 mg kg day) based on WHO (2008World Health Organization (WHO). United Nations Environment Programme. Guidance for identifying populations at risk from mercury exposure. Geneva: World Health Organization; 2008.). The MDI and RI were calculated based on total mercury concentration observed in Brycon falcatus muscle tissue collected from the Teles Pires River basin (0.009 to 0.180 mg kg-1 wet weight). The specimens were collected from November 2014 to October 2016.

Fish weight increased positively with standard length (r 2 = 0.914; p<0.001; b = 3.387; Fig. 2). The condition factor (K) was 1.025 and the HSI was 0.454 ± 0.286. There was no correlation between THg concentration in the muscle and condition factor (r = -0.073; p = 0.669), or THg in the liver and HSI (r = -0.03; p = 0.832).

THg concentration
in muscle tissue was not related to standard length or weight (r 2 = 0.54; p>0.05).

Discussion

THg concentration in the liver and muscle tissue of B. falcatus was higher than that found in the gill tissue. The gills are in direct contact with the aquatic environment, and as they are responsible for the gas exchange process between the organism and environment, they are extremely irrigated by blood. Thus, the concentration levels in this organ reflect those of the external environment (river water) and the organism’s blood. Other studies with fish have pointed to the liver as the organ with the highest accumulation of Hg (Havelková et al., 2008Havelková M, Dušek L, Némethová D, Poleszczuk G, Svobodová Z. Comparison of mercury distribution between liver and muscle - a biomonitoring of fish from lightly and heavily contaminated localities. Sensors. 2008; 8(7):4095-109. Available from: http://doi.org/10.3390/s8074095
http://doi.org/10.3390/s8074095...
; Azevedo et al., 2012Azevedo JS, Sarkis JES, Oliveira TA, Ulrich JC. Tissue-specific mercury concentrations in two catfish species from the Brazilian coast. Braz J Oceanogr. 2012; 60(2):211-19. Available from: http://dx.doi.org/10.1590/S1679-87592012000200011
http://dx.doi.org/10.1590/S1679-87592012...
, Alvarez et al., 2012Alvarez S, Kolok AS, Jimenez LF, Granados C, Palacio JA. Mercury concentrations in muscle and liver tissue of fish from marshes along the Magdalena River, Colombia. Bull Environ Contam Toxicol. 2012; 89(4):836-40. Available from: https://doi.org/10.1007/s00128-012-0782-9
https://doi.org/10.1007/s00128-012-0782-...
; Watanabe et al., 2012Watanabe N, Tayama M, Inouye M, Yasutake A. Distribution and chemical form of mercury in commercial fish tissues. J Toxicol Sci. 2012; 37(4):853-61. Available from: https://www.ncbi.nlm.nih.gov/pubmed/22863865
https://www.ncbi.nlm.nih.gov/pubmed/2286...
). In fish the Hg can be detoxified by the kidney, liver and, possibly, by the gills (Huang et al., 2012Huang SS-Y, Strathe AB, Fadel JG, Lin P, Liu T-Y, Hung SSO. Absorption, distribution, and elimination of graded oral doses of methylmercury in juvenile white sturgeon. Aquat Toxicol. 2012; 122-123:163-71. Available from: https://doi.org/10.1016/j.aquatox.2012.06.003
https://doi.org/10.1016/j.aquatox.2012.0...
). Maulvault et al. (2016Maulvault AL, Custódio A, Anacleto P, Repolho T, Pousão T, Nunes ML et al. Bioaccumulation and elimination of mercury in juvenile seabass (Dicentrarchus labrax) in a warmer environment. Environ Res . 2016; 149:77-85. Available from: https://doi.org/10.1016/j.envres.2016.04.035
https://doi.org/10.1016/j.envres.2016.04...
) reported that the liver presented the highest percentage of elimination of Hg (64%) in juveniles of Dicentrarchus labrax (perciform fish). In muscle, Hg normally binds to the protein sulfhydryl groups (Azevedo, 2003Azevedo FA. Toxicologia do mercúrio. São Carlos, São Paulo: Rima;. 2003.). The half-life of Hg in this tissue tends to be higher, therefore, it is extremely relevant to know its THg concentration as it integrates environmental concentration in time and space (especially for migratory fish such as B. falcatus). Therefore, liver and muscle tissues can have similar concentrations; however their significance and interpretation must be performed independently. Similar concentrations within these two tissues were also observed in omnivorous, carnivorous and detritivorous fish from the Vigário Reservoir (Rio de Janeiro, Brazil; Kasper et al., 2009Kasper D, Palermo EFA, Dias ACMI, Ferreira GL, Leitão RP, Branco CWC, Malm O. Mercury distribution in different tissues and trophic levels of fish from a tropical reservoir, Brazil. Neotrop Ichthyol. 2009; 7(4):751-58. Available from: http://dx.doi.org/10.1590/S1679-62252009000400025
http://dx.doi.org/10.1590/S1679-62252009...
).

Various anthropogenic impacts are known within the studied region such as tanneries and cattle farming, however agriculture is currently the most widely practiced human activity, and is thus responsible for the greatest impact. It has been shown that the various uses of the soil can be reflected in higher Hg concentrations in fish due to the direct increase of Hg from these activities (e.g., use of mercury fungicides), or through increased leaching of naturally occurring Hg within the soil. Roulet et al. (1999Roulet M, Lucotte M, Farella N, Serique G, Coelho H, Sousa Passos CJ et al. Effects of recent human colonization on the presence of mercury in Amazonian ecosystems. Water Air Soil Pollut. 1999; 112(3-4):297-313. Available from: https://doi.org/10.1023/A:1005073432015
https://doi.org/10.1023/A:1005073432015...
) observed that erosion resulting from deforestation carries mercury absorbed in soil particles to adjacent aquatic systems. Mercury deposition in the sediment of a Southern Amazonian lake increased with intensified deforestation and land use from activities such as road construction (Cordeiro et al., 2002Cordeiro RC, Turcq B, Ribeiro MG, Lacerda LD, Capitâneo J, Oliveira da Silva A, Sifeddine A, Turcq PM. Forest fire indicators and mercury deposition in an intense land use change region in the Brazilian Amazon (Alta Floresta, MT). Sci Total Environ . 2002; 293(1-3):247-56. Available from: https://doi.org/10.1016/S0048-9697(02)00045-1
https://doi.org/10.1016/S0048-9697(02)00...
). Fires caused cationic enrichment of the Tapajós river basin’s soils, causing a change in cationic dynamics and consequent higher soil mercury loss due to leaching (Farella et al., 2006Farella N, Lucotte M, Davidson R, Daigle S. Mercury release from deforested soils triggered by base cation enrichment. Sci Total Environ . 2006; 368(1):19-29. Available from: https://doi.org/10.1016/j.scitotenv.2006.04.025
https://doi.org/10.1016/j.scitotenv.2006...
). Sampaio da Silva et al. (2009Sampaio da Silva D, Lucotte M, Paquet S, Davidson R. Influence of ecological factors and of land use on mercury levels in fish in the Tapajos river basin Amazon. Environ Res . 2009; 109(4):432-46. Available from: https://doi.org/10.1016/j.envres.2009.02.011
https://doi.org/10.1016/j.envres.2009.02...
) studied the Tapajós river basin and suggested that land use in watersheds plays a key role in the Hg concentration of local ichthyofauna. Kütter et al. (2015Kütter VT, Kütter MT, Silva-Filho EV, Marques ED, Gomes OVO, Mirlean N. Mercury bioaccumulation in fishes of a paddy field in Southern of Brazil. Acta Limnol Bras. 2015; 27(2):191-201. Available from: http://dx.doi.org/10.1590/S2179-975X5314
http://dx.doi.org/10.1590/S2179-975X5314...
) observed high mercury concentrations in the omnivorous Astyanax sp. in southern Brazil’s rice plantations. Although within the region of focus of the present study, even with intense agricultural activity and agrochemical use (Pignati et al., 2007Pignati WA, Machado JMH, Cabral JF. Acidente rural ampliado: o caso das “chuvas” de agrotóxicos sobre a cidade de Lucas do Rio Verde - MT. Ciênc Saúde Col. 2007; 12(1): 105-14. Available from: http://dx.doi.org/10.1590/S1413-81232007000100014
http://dx.doi.org/10.1590/S1413-81232007...
; Belo et al., 2012Belo MSSP, Pignati W, Dores EFGC, Moreira JC, Peres F. Uso de agrotóxicos na produção de soja do Estado do Mato Grosso: um estudo preliminar de riscos ocupacionais e ambientais. Rev Bras Saúde Ocup. 2012; 37(125):78-88. Available from: http://dx.doi.org/10.1590/S0303-76572012000100011
http://dx.doi.org/10.1590/S0303-76572012...
), our results showed that B. falcatus presented low concentrations of THg. Mercury is poorly absorbed through gills and skin of fish; the main route of exposure is through its diet (Erickson et al., 2008Erickson RJ, Nichols JW, Cook PM, Ankley GT. Bioavailability of chemical contaminants in aquatic systems. In: Di Giulio RT, Hinton DE, editors. The Toxicology of Fishes. Florida, USA: CRC Press - Taylor & Francis Group; 2008. p. 9-45. https://doi.org/10.1201/9780203647295.ch2
https://doi.org/10.1201/9780203647295.ch...
). Top organisms in the aquatic food chain generally have higher THg concentrations than those at lower trophic levels even though they inhabit the same aquatic system (Voigt, 2004Voigt HR. Concentrations of mercury (Hg) and cadmium (Cd), and the condition of some coastal Baltic fishes. [MSc Thesis]. Helsinki, University of Helsinki; 2004. Environmentalica Fennica. 21:1-22. Available from: http://urn.fi/URN:ISBN:952-10-1738-4
http://urn.fi/URN:ISBN:952-10-1738-4...
; Terra et al., 2008Terra BF, Araújo FG, Calza CF, Lopes RT, Teixeira TP. Heavy metal in tissues of three fish species from different trophic levels in a tropical Brazilian River. Water Air Soil Pollutut. 2008; 187(1-4):275-84. Available from: https://doi.org/10.1007/s11270-007-9515-9
https://doi.org/10.1007/s11270-007-9515-...
). Brycon falcatus has omnivorous food habit with a tendency to frugivory (Correa et al., 2007Correa SB, Winemiller KO, Lopez-Fernandez H, Galetti M. Evolutionary perspectives on seed consumption and dispersal by fishes. Bioscience. 2007; 57(9):748-56. Available from: https://doi.org/10.1641/B570907
https://doi.org/10.1641/B570907...
). In the Teles Pires river basin, due to the great supply of in natura soybeans in attractants, the B. falcatus diet is mainly based on soybeans (Matos et al., 2016aMatos LS, Silva JOS, Andrade PSM, Carvalho LN. Diet of characin, Brycon falcatus (Müller and Troschel, 1844) in the Amazon Basin: a case study on attractant for fish in the Teles Pires river. J Appl Ichthyol. 2016a; 32(6):1080-85. Available from: http://dx.doi.org/10.1111/jai.13108
http://dx.doi.org/10.1111/jai.13108...
). Thus, the low levels of THg in B. falcatus observed in the present study is probably due to its food habit.

The weight-length relationship in the present study revealed a positive allometric growth with a b value greater than 3.0, indicating that the increase in weight was greater than that of length for fish collected from the Teles Pires river basin. This positive allometric standard was also described for wild B. falcatus specimens (Giarrizzo et al., 2015Giarrizzo T, De Sena Oliveira RR, Costa Andrade M, Pedrosa Gonçalves A, Barbosa TAP, Martins AR et al. Length-weight and length-length relationships for 153 fish species from the Xingu River (Amazon Basin, Brazil). J App Ichthyol. 2015; 31(2):415-24. Available from: http://dx.doi.org/10.1111/jai.12677
http://dx.doi.org/10.1111/jai.12677...
), farmed Brycon amazonicus (Arias et al., 2006Arias CJA, Zaniboni-filho E, Aya BE. Indicadores del ciclo reproductivo del yamú Brycon amazonicus, en cautiverio. Orinoquia. 2006; 10(2):24-34. Available from: http://orinoquia.unillanos.edu.co/index.php/orinoquia/article/view/215/636
http://orinoquia.unillanos.edu.co/index....
), wild Brycon siebenthalae (Arias, 1995Arias CJA. Contribución al conocimiento biológico de los peces de los Llanos, yamú (Brycon siebenthalae) y sapuara (Semaprochilodus laticeps cf.), con fines de cultivo. Informe Final.. Villavicencio, Colombia: Unillanos-Colciencias. 1995. Available from: <http://www.scielo.org.co/scielo.php?script=sci_arttext&pid=S0120-06902006000200002&lng=en&nrm=iso>. ISSN 0120-0690.
http://www.scielo.org.co/scielo.php?scri...
) and wild Brycon cephalus (Zaniboni-Filho, 1985Zaniboni-Filho E. Biologia da reprodução do matrinxã, Brycon cephalus (Günther, 1869) (Teleostei: Characidae). [MSc. thesis]. Manaus, AM: Universidade Federal da Amazônia, Instituto Nacional de Pesquisa da Amazônia;1985.). According to Silva et al. (2015Silva TSC, Santos LD, Silva LCR, Michelato M, Furuya VRB, Furuya WM. Length-weight relationship and prediction equations of body composition for growing-finishing cage-farmed Nile tilapia. R Bras Zootec. 2015; 44(4):133-37. Available from: http://dx.doi.org/10.1590/S1806-92902015000400001
http://dx.doi.org/10.1590/S1806-92902015...
), when the value of b exceeds 3.0, the fish are fatter. Therefore, based on the b value, THg levels in collected B. falcatus did not influence weight gain. The condition factor is often used as an indicator of fish nutritional status, where a K value close to 1 generally indicates that fish are well nourished and healthy (Cizdziel et al., 2002Cizdziel JV, Hinners TA, Pollard JE, Heithmar EM, Cross CL. Mercury concentrations in fish from lake mead, USA, related to fish size, condition, trophic level, location, and consumption risk. Arch Environ Contam Toxicol. 2002; 43(3):309-17. Available from: https://doi.org/10.1007/s00244-002-1191-6
https://doi.org/10.1007/s00244-002-1191-...
). The condition factor of collected B. falcatus was 1.025, indicating that collected fish were healthy. In the present study there was no correlation between THg concentration in the muscle and K of collected B. falcatus. This indicates that THg levels in analyzed B. falcatus did not influence nutritional status. In addition, there are other factors besides well-being that were not analyzed in the present study, which can be affected even at low levels of mercury (such as, reproduction, gas exchange through gills and predator avoidance). Studies indicate that Hg affects the capture capacity of fish prey and makes them more susceptible to predation (Weis, Weis 1995aWeis JS, Weis P. Effects of embryonic exposure to methylmercury on larval prey capture ability in the mummichog Fundulus heteroclitus. Environ Toxicol Chem . 1995a; 14(1):153-56. Available from: http://dx.doi.org/10.1002/etc.5620140117
http://dx.doi.org/10.1002/etc.5620140117...
, 1995bWeis JS, Weis P. Swimming performance and predator avoidance by mummichog Fundulus heteroclitus larvae after embryonic or larval exposure to methylmercury. Can J Fish Aquat Sci. 1995b; 52(10):2168-73. Available from: https://doi.org/10.1139/f95-809
https://doi.org/10.1139/f95-809...
; Smith, Weis, 1997Smith GM, Weis JS. Predator/prey interactions of the mummichog (Fundulus heteroclitus(L.)): Effects of living in a polluted environment. J Exp Mar Bio Ecol. 1997; 209(1-2):75-87. Available from: https://doi.org/10.1016/S0022-0981(96)02590-7
https://doi.org/10.1016/S0022-0981(96)02...
). The contamination by Hg also can impair the hormone production in male and female fish, and decrease the quality and quantity of the production of sperm and eggs (Friedmann et al., 2002Friedmann AS, Costain EK, MacLatchy DL, Stansley W, Washuta EJ. Effect of mercury on general and reproductive health of largemouth bass (Micropterus salmoides) from three lakes in New Jersey. Ecotoxicol Environ Saf. 2002; 52(2):117-22. Available from: https://doi.org/10.1006/eesa.2002.2165
https://doi.org/10.1006/eesa.2002.2165...
; Ebrahimi, Taherianfard, 2011Ebrahimi M, Taherianfard M. 2011. The effects of heavy metals exposure on reproductive systems of cyprinid fish from Kor River. Iran J Fish Sci, 10(1):13-24. Available from: <http://jifro.ir/article-1-121-en.html>). The gill epithelium of fish can be ruptured since Hg contamination, affecting the gas exchange and the permeability of cell membranes (Oliveira-Ribeiro et al., 2000Oliveira-Ribeiro CA, Pelletier E, Pfeiffer WC, Rouleau C. Comparative uptake, bioaccumulation, and gill damages of inorganic mercury in tropical and Nordic freshwater fish. Environ Res . 2000; 83(3):286-92. Available from: https://doi.org/10.1006/enrs.2000.4056
https://doi.org/10.1006/enrs.2000.4056...
), which may result in increased energy demands, change in gas exchange efficiency and increase the metabolic rate (Tatara et al., 2001Tatara CP, Newman MC, Mulvey M. Effect of mercury and Gpi-2 genotype on standard metabolic rate of eastern mosquitofish (Gambusia holbrooki). Environ Toxicol Chem. 2001; 20(4):782-6. Available from: http://dx.doi.org/10.1002/etc.5620200413
http://dx.doi.org/10.1002/etc.5620200413...
).

Body indexes, such as the hepatosomatic index, have commonly been used for biomonitoring of environmental stress in fish health. An increase in the HSI may also be associated with increased detoxification activity in response to the presence of contaminants (Pereira, Kuch, 2005Pereira MS, Kuch B. Heavy metals, PCDD/F and PCB in sewage sludge samples from two wastewater treatment facilities in Rio de Janeiro State, Brazil. Chemosphere. 2005; 60(7):844-53. Available from: https://doi.org/10.1016/j.chemosphere.2005.01.079
https://doi.org/10.1016/j.chemosphere.20...
). However, a decreased HSI indicates that fish populations are under chemical stress and are using energy reserves (Kopecka et al., 2006Kopecka J, Lehtonen KK, Barsiene J, Broeg K, Vuorinen PJ, Gercken J, Pempkowiak J. Measurements of biomarker levels in flounder (Platichthys flesus) and blue mussel (Mytilus trossulus) from the Gulf of Gdansk (southern Baltic). Mar Pollut Bul . 2006; 53(8-9):406-21. Available from:10.1016/j.marpolbul.2006.03.009). In farmed Brycon, a HSI of 0.96 was reported for B. cephalus (Monteiro et al., 2006Monteiro DA, Almeida JA, Rantin FT, Kalinin AL. Oxidative stress biomarkers in the freshwater characid fish, Brycon cephalus, exposed to organophosphorus insecticide Folisuper 600 (methyl parathion). Comp Biochem Physiol C Toxicol Pharmacol. 2006; 143(2):141-49. Available from: https://doi.org/10.1016/j.cbpc.2006.01.004
https://doi.org/10.1016/j.cbpc.2006.01.0...
) and 1.31 for B. amazonicus (Tavares-Dias et al., 2008Tavares-Dias M, Affonso EG, Oliveira SR, Marcon JL, Egami MI. Comparative study on hematological parameters of farmed matrinxã, Brycon amazonicus Spix and Agassiz, 1829 (Characidae: Bryconinae) with others Bryconinae species. Acta Amaz. 2008; 38(4):799-806. Available from: http://dx.doi.org/10.1590/S0044-59672008000400026
http://dx.doi.org/10.1590/S0044-59672008...
). In wild B. falcatus, the HSI ranged from 0.166 to 0.390, reflecting stress induced by a low supply of fish food during the dry season, rather than contamination of the specimens (Matos et al., 2016bMatos LS, Silva DR, Silva JOS, Andrade RLT, Carvalho LN. Heavy metal bioaccumulation of the characiform Brycon falcatus Muller & Troschel, 1844 in the Teles Pires basin, Southern Amazon. Acta Sci Biol Sci. 2016b; 38(2):131-38. Available from: http://www.redalyc.org/html/1871/187147823001
http://www.redalyc.org/html/1871/1871478...
). In the present work, the mean HSI of analyzed fish was 0.454 ± 0.286, similar to that described by Matos et al. (2016bMatos LS, Silva DR, Silva JOS, Andrade RLT, Carvalho LN. Heavy metal bioaccumulation of the characiform Brycon falcatus Muller & Troschel, 1844 in the Teles Pires basin, Southern Amazon. Acta Sci Biol Sci. 2016b; 38(2):131-38. Available from: http://www.redalyc.org/html/1871/187147823001
http://www.redalyc.org/html/1871/1871478...
). Considering that this study analyzed wild specimens, where the food supply is likely lower than that in pisciculture, and that there was no correlation between THg concentration in the liver and the HSI, we can conclude that the low HSI does not reflect contamination of the specimens, but rather the specimens’ nutritional status.

The THg levels in muscle tissue of the B. falcatus specimens evaluated in this study ranged from 0.009 to 0.180 mg.kg-1 wet weight, below the value recommended for fish Hg content for human consumption by World Health Organization. This recommendation is based on a person weighing approximately 60 kg and having in his food about 400 g of fish per week (FAO, 1983Food and Agriculture Organization/World Health Organization (FAO/WHO). Food consumption and exposure assessment of chemicals. Geneva, Switzerland: Report of FAO/WHO Consultation; 1983.). However, the RI calculated with different consumption rates of fish of the studied region presents some values greater than 1.0, indicating a potential risk of adverse effects on human health. The RfD used to calculate RI is an estimate of a daily exposure to the human population (including sensitive subgroups) that is unlikely to have a significant risk of deleterious effects during life. It is not a direct risk estimator, but rather a point of reference for assessing the potential effects. In increasing exposures to RfD, the potential for adverse health effects increases (USEPA, 2001United States Environmental Protection Agency (USEPA). Integrated Risk Information System (IRIS) for Methylmercury (CASRN 22967-92-6). Washington, DC: National Center for Environmental Assessment, Office of Research and Development; 2001. Available from: https://www.epa.gov/iris/subst/0073.htm
https://www.epa.gov/iris/subst/0073.htm...
). In the Tapajós basin, Bidone et al. (1997Bidone ED, Castilhos ZC, Souza TMC, Lacerda LD. Fish contamination and human exposure to mercury in the Tapajós river Basin, Pará State, Amazon, Brazil: a screening approach. Bull Environ Contam Toxicol . 1997; 59(2):194-201. Available from: https://doi.org/10.1007/s001289900464
https://doi.org/10.1007/s001289900464...
) and Castilhos et al. (1998Castilhos ZC, Bidone ED, Lacerda LD. Increase of the background human exposure to mercury through fish consumption due to gold mining at the Tapajós river region, Pará State, Amazon. Bull Environ Contam Toxicol . 1998; 61(2):202-09. Available from: https://doi.org/10.1007/s001289900749
https://doi.org/10.1007/s001289900749...
) found similar levels of THg (0.050 mg.kg-1) in matrinxã muscle. Brycon falcatus has excellent meat quality, and as a result is commonly consumed throughout the region, with the muscle flesh the part of the fish most commonly used for human consumption (Kosanovic et al., 2007Kosanovic M, Hasan MY, Subramanian D, Al Ahbabi AA, Al Kathiri OA, Aleassa EM, Adem A. Influence of urbanization of the western coast of the United Arab Emirates on trace metal content in muscle and liver of wild Red-spot emperor (Lethrinus lentjan). Food Chem Toxicol. 2007; 45(11):2261-66. Available from: https://doi.org/10.1016/j.fct.2007.06.010
https://doi.org/10.1016/j.fct.2007.06.01...
). There are three indigenous ethnic groups (mundurukus, kaiabis and apyakas) within the Teles Pires river basin that consume the available fisheries resources (Ricardo, Fany, 2011Ricardo B, Fany R. Povos indígenas no Brasil 2006/2010. São Paulo: Instituto Socioambiental; 2011.; IBGE, 2016Instituto Brasileiro De Geografia e Estatística (IBGE). Atlas nacional digital do Brasil 2016. http://www.ibge.gov.br/apps/atlas_nacional/
http://www.ibge.gov.br/apps/atlas_nacion...
). In addition to the indigenous tribes, there is a fishing colony (named Z-16) with approximately 250 professional fishermen working in the Teles Pires river basin. In the Tapajós basin, researchers found trace element contamination in indigenous and riverine populations; where Barbosa et al. (1997Barbosa AC, Garcia AM, Souza JR. Mercury contamination in hair of riverine populations of Apiacás Reserve in the Brazilian Amazon. Water Air Soil Pollut. 1997; 97(1-2):1-8. Available from: https://doi.org/10.1023/A:1018336820227
https://doi.org/10.1023/A:1018336820227...
) showed that 3% of the riverine population presented levels of mercury above 50 mg.kg-1, Hacon et al. (1997Hacon S, Rochedo ER, Campos R, Rosales G, Lacerda LD. Risk assessment of mercury in Alta Floresta. Amazon Basin - Brazil. Water, Air Soil Pollut. 1997; 97(1-2):91-105. Available from: https://doi.org/10.1023/A:1018367313384
https://doi.org/10.1023/A:1018367313384...
) estimated a Risk Index of 9.3 for families of fishermen, and Brabo et al. (2000Brabo ES, Santos EO, Jesus LM, Mascarenhas AFS, Faial KF. Mercury contamination of fish and exposures of indigenous community in Pará state, Brazil. Environ Res. 2000; 84:197-203. Available from: https://doi.org/10.1006/enrs.2000.4114
https://doi.org/10.1006/enrs.2000.4114...
) concluded that while Hg levels in fish consumed by the Sai Cinza tribe were below the Brazilian limit for consumption, their high consumption rates of large quantities of fish make them highly susceptible to contamination. Considering that the diets of the local indigenous and riverine populations predominately consist of fish (the populations’ main protein source), results in high susceptibility to the contaminants contained in consumed fish. According to Fréry et al. (2001Fréry N, Maury-Brachet R, Maillot E, Deheeger M, Mérona B, Boudou A. Gold-mining activities and mercury contamination of native Amerindian communities in French Guiana: key role of fish in dietary uptake. Environ Health Perspect. 2001; 109(5):449-56. Available from: http://www.jstor.org/stable/3454702
http://www.jstor.org/stable/3454702...
), fish meat constitutes at least seven weekly meals for these populations, consuming approximately 340 g of fish per day. However, studies comparing contamination risks to the benefits provided by the consumption of omega-3 fatty acids have shown that the benefits outweigh the risks (Mozaffarian, Rimm, 2006Mozaffarian D, Rimm EB. Fish intake, contaminants, and human health: evaluating the risks and the benefits. JAMA. 2006; 296(15):1885-99. Available from: https://jamanetwork.com/journals/jama/fullarticle/203640
https://jamanetwork.com/journals/jama/fu...
; Mahaffey et al., 2011Mahaffey KR, Sunderland EM, Chan HM, Choi AL, Grandjean P, Mariën K et al. Balancing the benefits of n-3 polyunsaturated fatty acids and the risks of methylmercury exposure from fish consumption. Nutr Rev. 2011; 69(9):493-508. Available from: https://doi.org/10.1111/j.1753-4887.2011.00415.x
https://doi.org/10.1111/j.1753-4887.2011...
). To balance the risks and benefits of regular fish consumption, species choice, consumption frequency and portion size are essential aspects that need to be looked at (Domingo, 2007Domingo JL. Omega-3 fatty acids and the benefits of fish consumption: is all that glitters gold? Environ Int. 2007; 33(7):993-98. Available from: https://doi.org/10.1016/j.envint.2007.05.001
https://doi.org/10.1016/j.envint.2007.05...
). Based on the data from our study, we conclude that it may be considered unlikely that the consumption of B. falcatus from the Teles Pires river basin for the general population, which consume about 30 g of matrinxã per day or about of 250 g/week, presents a risk for health. However, those who have a high consumption of fish, such as indigenous and riverine people, it is adequate to eat more herbivorous fish (pacu, tambaqui, pirapitinga, jatuarana, piau and others) since they probably have low Hg levels. It is especially important for the fish consumption by children, pregnant and lactating because they are nurturing a nervous system in formation, and, therefore, the most vulnerable life stages.

We summarize that by the condition factor, weight and length ratio and hepatosomatic index analyses the concentrations of THg probably did not influence the health and well-being of B. falcatus collected in the Teles Pires river basin. Liver and muscle tissues presented similar levels of THg, but their significance and interpretation should be performed independently. Regarding the consumption of the B. falcatus, we conclude that the concentrations of THg are within the limit recommended for those that have lower consumption rates of the studied region. The risk of deleterious effects on human health may exist in those that have a greater consumption of B. falcatus because the consumer will be exposed to higher loads of mercury (including the sensitive groups). With the implementation of the Sinop Hydroelectric Power Plant, which it is planned to operates from 2019, future studies on fish assessment should be carried out since the creation of the reservoir may increase the bioaccumulation of Hg in fish, as already seen in many tropical and temperate reservoirs (e.g., Schetagne, Verdon, 1999Schetagne R, Verdon R. Post-impoundment evolution of fish mercury levels at the La Grande complex, Quebec, Canadá (from 1978 to 1996). In: Lucotte M, Schetagne R, Therien N, Langlois C, Tremblay A, editors. Mercury in the biogeochemical cycle: natural environments and hydroelectric reservoirs of northern Québec (Canada). Berlin: Springer Berlin Heidelberg; 1999 (Environ Science and Engineering Series) p.235-258.; Hylander et al., 2006Hylander LD, Gröhn J, Tropp M, Vikström A, Wolpher H, de Castro E Silva E, Meili M, Oliveira LJ. Fish mercury increase in Lago Manso, a new hydroelectric reservoir in tropical Brazil. J Environ Manage. 2006; 81(2):155-66. Available from: https://doi.org/10.1016/j.jenvman.2005.09.025
https://doi.org/10.1016/j.jenvman.2005.0...
; Porvari, 1995Porvari P. Mercury levels of fish in Tucurui hydroelectric reservoir and in River Mojti in Amazonia, in the state of Pará Brazil. Sci Total Environ . 1995; 175: 109-17. Available from: https://doi.org/10.1016/0048-9697(95)04907-X
https://doi.org/10.1016/0048-9697(95)049...
).

Acknowledgments

We especially thank Prof Dr Ricardo L. T. de Andrade for all his efforts in this research, yielding the Integrated Laboratory of Chemical Research-LIPEQ and helping with analyses of fish samples. We thank Denise C. Parisotto for helping with laboratory analyses, Marcos Beckmann for help with the collections, and Lucia Mateus for assistance in the statistical analyses and an anonymous reviewer who provided extensive feedback that significantly improved this manuscript. The research was carried out with the support of the Fundação de Amparo à Pesquisa do Estado de Mato Grosso (FAPEMAT, Universal notice 005/2012) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq Universal, MCTI/CNPq No. 14/2014). Permission to collect specimens was granted by Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). LSM received financial support from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).

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Publication Dates

  • Publication in this collection
    2018

History

  • Received
    05 Sept 2017
  • Accepted
    02 Feb 2018
Sociedade Brasileira de Ictiologia Universidade Estadual de Maringá, Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura/Coleção Ictiologia, Av. Colombo, 5790, 87020-900 Maringá, PR, Brasil, Tel.: (55 44)3011 4632 - Maringá - PR - Brazil
E-mail: neoichth@nupelia.uem.br