Comparison of Arsenic and Antimony Contents in Tissues and Organs ...

Arch Environ Contam Toxicol (2009) 57:581–589 DOI 10.1007/s00244-009-9300-4

Comparison of Arsenic and Antimony Contents in Tissues and Organs of Brown Trout Caught from the River Presa Polluted by Ancient Mining Practices and from the River Bravona in Corsica (France): A Survey Study J. Foata Æ Y. Quilichini Æ J. Torres Æ E. Pereira Æ M. M. Spella Æ J. Mattei Æ B. Marchand

Received: 27 June 2008 / Accepted: 9 February 2009 / Published online: 1 March 2009 Ó Springer Science+Business Media, LLC 2009

Abstract The present study evaluates the concentrations of arsenic (As) and antimony (Sb) in the intestine, liver, muscle, gonads, gills, and kidney of Salmo trutta subsp. from the Presa River in Corsica (France; n = 10), which crosses an abandoned arsenic mine, and from the Bravona River (reference site; n = 10). Both metalloids were analyzed by means of ICP-MS. The relationships between fish size (length and weight) and metalloid concentrations in their tissues were investigated by linear regression analysis. In all fish samples concentrations of As and Sb (expressed as micrograms per gram fresh weight) were highest in the kidney. Lowest Sb concentrations were found in the muscle, whereas lowest As concentrations were found in the gonads of S. trutta. Two organotropisms were revealed: one for As—kidney (21.4656) [ intestine (3.9535) [ gills (3.0404) [ liver (1.1743) [ muscle (0.9976) [ gonads (0.8081); and the other for Sb—kidney (0.70067) [ gills (0.6181) [ intestine (0.2576) [ gonads (0.1673) [ liver J. Foata (&) Y. Quilichini B. Marchand CNRS UMR SPE 6134, Laboratoire Parasites et Ecosyste`mes me´diterraneéns, Faculte´ des Sciences et Techniques, Universite´ de Corse, Campus Grossetti, 20250 Corte, France e-mail: [email protected] J. Torres Laboratori de Parasitologia, Departament de Microbiologia i Parasitologia Sanita`ries, Facultat de Farma`cia, Universitat de Barcelona, Av. Joan XXIII, sn, 08028 Barcelona, Spain E. Pereira M. M. Spella CNRS UMR SPE 6134, Laboratoire Sciences de la Terre, Faculte´ des Sciences et Techniques, Universite´ de Corse, Campus Grossetti, 20250 Corte, France J. Mattei Office National de l’Eau et des Milieux Aquatiques, lieu-dit Guazza, 20290 Prunelli di Casacconi, Corse, France

(0.9625) [ muscle (0.0753). Results of linear regression analysis in most cases showed a significant negative correlation between metalloid concentration and fish size. Highly significant (p \ 0.05) negative correlations were found between fish length and As concentration in the gonads, as well as between fish length and Sb concentrations in the gills. Arsenic concentrations in female fish were significantly higher than those in males in the kidney, gonads, gills, and liver. The same results were found for Sb, except in the liver, where the tendency was reversed.

The contamination of fresh waters with a wide range of pollutants has become a matter of great concern over the last few decades, not only because of the problem of public health but also because of the damage caused to the aquatic life. The concentration of some toxic elements in the aquatic ecosystem has increased due to agricultural, industrial, and mining activities. Consequently, contamination of rivers with heavy metals and other toxic elements may have devastating effects on the ecological balance of the aquatic environment, and the diversity of aquatic organisms becomes limited with the extent of contamination (Migon et al. 1995; Mori et al. 1999). There is an increasing need for current information on toxic metalloid concentrations in fish in view of the consequent environmental disturbances arising from ancient mining activities. Most studies of toxic elements have been restricted to marine fish species and deal with toxic elements such as as Cd, Cu, Fe, Pb, Zn, Hg, and Ni (Canli and Atli 2003; Dıàz et al. 1994; Filazi et al. 2003; Foran et al. 2004; Nickless et al. 1972; Yilmaz 2005). Some works consider freshwater species, too, and metals such as Cu, Zn, Cr, and Mn (Bajc et al. 2005; Barak and Mason 1990; Canli et al. 1998; Jankong et al. 2007; Kargin 1998).

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Very few works have been carried out to analyze arsenic and antimony concentrations in fish (Calendini 2000; Foley et al. 1978; Maeda et al. 1993). Some elements such as zinc, copper, and iron are essential in trace amounts for growth and development. But others, such as mercury, cadmium, and lead, are known for their toxicity in all their forms (metal, vapor, organical compound, etc.). Nonessential elements are also taken up by fish and accumulate in their tissues (Canli and Atli 2003). For example, arsenic is classified as a very toxic substance according to the criteria of Directive 67/548/ CEE. The presence of antimony has been reported in seawater and some fresh waters (Cabon and Madec 2004; Hirata et al. 1997; Quentel and Filella 2002). Effects of antimony are still little known. Like arsenic, antimony is omnipresent in the environment, especially in the ground (Filella et al. 2002). Antimony is considered a major pollutant by the U.S. Environmental Protection Agency (EPA 1999). Data on contaminant quantities in tissues provide a better understanding of the complexity of their distribution and effects of various xenobiotics (Crawford and Luoma 1993). Therefore, we considered it important to determine the concentrations of As and Sb in Salmo trutta. We also wanted to assess the possible risk of fish consumption for human health, namely, for the population living close to the ancient mine. Moreover, fish are particularly good indicators of environmental biological contaminants because they can accumulate in fish tissue at concentrations higher than in the surrounding water (Watanabe et al. 2003). To our knowledge, few investigations have been concerned with the levels of contamination which occur in natural freshwater fish (Calendini 2000) and invertebrates (Mori et al. 1999) living in Corsican rivers. Therefore, the aim of the present study was to determine the arsenic and antimony levels in intestine, muscle, gill, liver, gonads, and kidney of fish inhabiting the area exposed to an old realgar (sulfides of arsenic) mine. This study also evaluates the relationships between concentrations of As and Sb and fish size (length) and gender in organs and tissues of the brown trout.

Materials and Methods Study Area The Bravona River (30 km length) begins at 1700 m of altitude and joins the Tyrrhenian Sea on the Eastern plain of Corsica in the north of Aleria (42°170 N, 9°230 E; Fig. 1). The Presa is a minor river, which crosses an ancient realgar mine nearer to Matra village. At the end of 1880, following a rising of the Presa River, the existence of an arsenic sulfide outcrop in the bed of the river was found.

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Arch Environ Contam Toxicol (2009) 57:581–589

In 1910 about 1840 tons containing 50%–60% realgar was extracted. The last period of exploitation was from 1935 to 1945 (Gauthier 1991). The Presa River is one affluent of the Bravona. The distance from the mine to the Bravona River is approximately 10 km (Migon et al. 1995). Figure 1 shows also the different sampling locations. The station Presa, where samples were collected, is downstream from the abandoned mine. This location was selected in order to provide As and Sb concentration values close to the source of pollution. The station Bravona, upstream from the confluence with the Presa, was the reference site. Sample Collection After electrofishing capture (May 2006), fish were placed in plastic bags and transported to the laboratory in freezer bags with ice. The total body length (cm) and weight (g) were recorded for each specimen. Altogether 120 samples (intestine, liver, muscle, gonads, gills, and kidney) were taken from both locations and prepared using stainlesssteel instruments. All samples were deep-frozen at –20°C until subsequent metal analysis. Analytical Procedure Tissue portions weighing 20–200 mg were submitted to As and Sb analysis. All material used in the digestion process was thoroughly acid-rinsed. Further mineralization was performed in Teflon vessels with 2 ml HNO3 (Suprapur; Merck) and 1 ml H2O2 (Panreak). Samples were left overnight in an oven at 90°C according to the internal standard protocol used at the Serveis Cientı´fico-Te`cnics of the University of Barcelona (Torres et al. 2006). After their complete digestion, they were diluted with milliQ water and then analyzed in an inductively coupled plasma mass spectrometer (Perkin Elmer Elan 6000). The analytical procedure for As was checked using dogfish liver (DOLT-3) as the standard reference material (National Research Council, Canada). Analytical blanks were prepared under the same conditions to determine the detection limits. Element concentrations are expressed as micrograms per gram fresh weight (lg/g), and the level of significance was 0.05 (5%). Inductively Coupled Plasma Mass Spectrometry Analysis The detection limit (mean blank value ± 3 standard deviations of the mean blank) for As (0.02 9 10-3 lg/g) and Sb (0.16 9 10-3 lg/g) was always lower than 1.10-3 lg/mL. Series of two analytical blanks were carried out for all 10 samples in the 120 analyses. The accuracy of As with respect to the standard reference material was higher than 90%.


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Fig. 1 Map of sample areas: 42°170 N, 9°230 E

Statistical Analysis Statistical analysis was carried out using MINITAB statistical package programs. Distribution analysis of experimental data displayed a normal or nearly normal distribution. Therefore, no transformation was done for further statistical procedures. To compare the relationship between fish size and toxic element concentrations in organs and tissues, linear regression analysis was applied. Correlation coefficients were also calculated and

the level of significance was 0.05 (5%) (Artusi et al. 2002).

Results Table 1 shows the number of fish sampled, their length and weight ranges, and the relationship between length and weight expressed as the coefficient of correlation R, as well as the correlation significance (p).

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Table 1 Size ranges and relationships between weight and total length (expressed as coefficient of correlation, R) of Salmo trutta caught in two Corsican rivers (Presa and Bravona) River

n

Length range (cm)

Weight range (g)

Equationa

R

Presa

10

14.1–25.2

30–160

y = 11.798x - 140.6

0.99

Bravona

10

12.9–20.5

26–68

y = 4.2982x - 20.596

0.68

a

x is total fish length (cm) and y is total fish weight (g)

Table 2 Concentrations (lg/g wet weight) of arsenic and antimony in tissue and organs of S. trutta from two Corsican rivers (Presa and Bravona) Presa Min–max As (lg/g tissue) Intestine Liver Muscle

Bravona Average ± SD

Min–max

Average ± SD

2.477–7.993

3.953 ± 1.555

0.026–0.116

0.066 ± 0.033

0.5268–2.465

1.174.32 ± 0.574

0.024–0.074

0.044 ± 0.014

0.619–1.365

0.997 ± 0.283

0.031–0.067

0.053 ± 0.012 0.061 ± 0.048

Gonads

0.127–1.788

0.808 ± 0.634

0.022–0.173

Gills

0.983–6.745

3.040 ± 1.965

0.032–0.794

0.129 ± 0.234

Kidney

9.055–59.241

21.465 ± 14.706

0.043–0.321

0.142 ± 0.097

0.053–0.481

0.257 ± 0.169

ND

ND ND

Sb (lg/g tissue) Intestine Liver

0.037–0.269

0.096 ± 0.082

ND

Muscle

0.023–0.179

0.075 ± 0.061

ND

ND

Gonads

0.046–0.321

0.167 ± 0.118

ND

ND

Gills

0.173–1.299

0.618 ± 0.312

ND

ND

Kidney

0.264–1.419

0.701 ± 0.380

ND

ND

Note: SD standard deviation; ND not detected (below detection values). Arsenic detection limit, 0.02 9 10-3 lg/g; antimony detection limit, 0.16 9 10-3 lg/g

In Table 2 the concentrations of As and Sb in fish tissues and organs from both polluted and reference sites are presented. In the Presa River for both arsenic and antimony, the highest concentrations were found in the kidney (21.4656 and 0.7007 lg/g, respectively). The lowest arsenic concentration (0.8081 lg/g) was measured in gonads, but it was still very elevated compared to those in previously cite organs and also to values obtained at the reference site. Fish caught downstream from the mine had higher arsenic concentrations in intestine, followed by gills, liver, and muscles, compared with adequate fish samples from the reference site. Antimony concentrations in the gills were also high in the polluted river compared with the reference site. The antimony levels are less important in intestine, gonads, liver, and muscle compared to those found in gills and kidney. The lowest antimony levels were reported in muscles. At the Bravona site many values were under the detection limit and could not be quantified. The linear correlation between arsenic and antimony concentrations in the contaminated zone (Presa) and fish

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size is reported in Table 3. No relationships were found between fish length and arsenic levels in the intestine, liver, muscle, gills, and kidney (p [ 0.05). Nevertheless, a negative correlation was recorded between fish length and arsenic levels in the gonads (p \ 0.05). Bigger fish concentrate more arsenic than small ones. There was also no correlation between length and antimony levels measured, except for the negative correlation for gills (p \ 0.05). Relationship between weight and arsenic and antimony concentrations was identical to that with length (not presented). For the polluted area, the effect of fish gender on the level of the tested metalloids was also examined (Fig. 2). Concentrations of arsenic in all tissue and organ samples of female fish (kidney, gonads, gills, and liver) were generally higher than those in males. Antimony levels in kidney, gills, and gonads of female fish from the polluted zone appeared to be significantly higher than in male specimens (Fig. 3). The concentration of antimony in male fish was found to be significantly higher than in females in muscles and liver.


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Table 3 Relationships between As and Sb concentrations and total length of Salmo trutta, expressed as the coefficient of correlation, R Arsenic

Antimony

Equation

y = -0.050x ? 4.795

y = -0.0306x ? 0.771

R2

0.0107

0.338

R

0.103

0.581

p

[0.05

[0.05

Intestine

Sb, µg/g wet-weight

Tissue

2,50 2,00

Sb concentrations in some tissues and organs of Salmo trutta in relation to fish sex MALE FEMALE

1,50 1,00 0,50 0,00 Muscle

Liver Equation R2

y = -0.0392x ? 1.833 0.0481

y = -0.004x ? 0.171 0.0318

Liver

Intestine

Gonads

Gills

Kidney

Fig. 3 Antimony (lg/g wet weight) concentrations in tissues and organs of S. trutta in the Presa River in relation to fish gender

R

0.219

0.178

p

[0.05

[0.05

Discussion

y = -0.014x ? 1.244

y = 0.028x - 0.367

0.0278

0.1451

According to Luoma (1983), the mechanisms of traceelement accumulation and storage in aquatic organisms are complex and diverse, varying with the chemical form of the metal, mode of uptake, and species. As a consequence, concentrations of toxins in tissues of freshwater fish vary considerably among different studies, possibly due to differences in metalloid concentrations and chemical characteristics of the water from which fish were sampled and the ecological needs, metabolism and feeding patterns of fish. Arsenic and antimony are known to be toxic to aquatic life (Eisler 1985, 1987, 1988) but they are rarely measured in freshwater fish (Calendini 2000; Foley et al. 1978; Maeda et al. 1993). In the present study, concentrations of these toxic metalloids in the tissues of trout from contaminated waters of the Presa River as well as the reference site of the Bravona River were measured (Table 3). The results obtained showed great variations. The average content in analyzed fish tissues from the Bravona River were 150 (As) and 700 (Sb) times higher than those at the reference site (Table 2). Similarly, Calendini (2000) has reported mean values for arsenic to be 145 times higher in the polluted zone (Presa) than in the Bravona. The French Agency of Sanitary Safety of Food (AFSSA) has not defined nutritional contributions advised for arsenic, because needs are widely covered by the food. Nevertheless, they would be about 12 to 25 lg. Naturally, arsenic at high doses is toxic (causing skin problems, liver problems, nervous disorders, etc.). But the limit not to be exceeded is indeed over the average contributions from food. The FASSF proposes a safe limit of from 140 to 250 lg a day. European directive 98/83/CE and the World Health Organization fix the maximum acceptable arsenic concentration at from 50 to 10 lg 9 L-1, and the maximum acceptable antimony concentration ranges from 10 to 5 lg/L, in water intended for human consumption. However, Spella et al. (1993) found higher values (As & 2200 lg/L, Sb & 150 lg/L) than those normalized for water by the

Muscle Equation R

2

R

0.167

0.381

p

[0.05

[0.05

y = -0.125.11x ? 2.909

y = -0.112x ? 1.912

0.4005

0.3536

Gonads Equation R

2

R

0.633

0.595

p

\0.05

[0.05

y = -0.326x ? 8.531 0.2847

y = -0.064x ? 1.686 0.4255

Gills Equation R2 R

0.534

0.652

P

[0.05

\0.05

y = -2.023x ? 55.454

y = -0.061x ? 1.728

0.1949

0.266

Kidney Equation R

2

R

0.441

0.515

p

[0.05

[0.05

Arsenic concentrations in some tissues and organs of Salmo trutta in relation to fish sex 70

As, µg/g wet-weight

60

MALE FEMALE

50 40 30 20 10 0 Muscle

Liver

Gonads

Gills

Intestine

Kidney

Fig. 2 Arsenic (lg/g wet weight) concentrations in tissues and organs of S. trutta in the Presa River in relation to fish gender

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World Health Organization. When fish are exposed to elevated element levels in aquatic environment, they can absorb the bioavailable arsenic and antimony directly from the environment via the gills or by ingesting contaminated water and food. In the fish, toxic elements are transported by the bloodstream, which brings them into contact with various organs and tissues. In our study, arsenic concentrations in tissues of S. trutta (0.8081–21.4656 lg/g; Table 2) were higher than those found in Pomoxis nigromaculatus (0.14–2.04 lg/g) or Perca flavescens and Micropterus salmoides (0.02–0.13 lg/g) in Chautauqua Lake, reported by Foley et al. (1978). Our arsenic concentrations were also higher than those reported in Salvelinus fontinalis, Salmo trutta, and Onchorhynchus mykiss (0.2–0.6 lg/g) in northern Rockies intermontane basins measured by Maret and Skinner (2000). It is well known that fish accumulate arsenic from water but they do not magnify it (Foley et al. 1978; Maeda et al. 1993). Our results also show that arsenic and antimony are more concentrated in kidneys and less in muscles (Table 2). Yilmaz (2005) reported that target organs, such as kidney, gills, and liver, have a tendency to accumulate toxic elements at high levels, as shown in many fish species in different Mediterranean areas, for example, in Mugil cephalus from the Mediterranean Sea (Abdel-Moniem et al. 1994) and in Trachurus mediterraneus in eastern Mediterranean waters (Abdel-Moniem et al. 1994; Yı¨lmaz 2003). On the other hand, Legorburu et al (1988) stated that it is generally accepted that muscle is not a tissue in which toxic elements accumulate. Similar findings were recorded in several freshwater fish species, showing that muscle is not active in accumulating heavy metals (Calendini 2000; ¨ nlu¨ 1998, 2000; Kargin and Erdem 1991; Karadede and U ¨ Unlu¨ et al. 1994). Moreover, many trace elements concentrate in the viscera of fish such as the liver and kidneys (Crawford and Luoma 1993). These elements accumulate mainly in metabolically active organs such as the kidney that store metals to detoxicate them by producing metallothioneins. Although arsenic and antimony are not metals, but metalloids, we can assume that a similar process exists for metalloids which could explain our findings in kidney. The concentrations of elements in the liver depends on a number of factors such as the chemical properties and the fish species (Maret and Skinner 2000). The levels of toxic elements in fish also vary depending on the aquatic environment (Canli and Atli 2003). Our results have shown that As and Sb accumulation in S. trutta varies depending on the fish organ and metalloid. The highest accumulation of As is in the kidney, followed by the intestine, gills, liver, muscle, and gonads, while for Sb the highest concentrations are also found in the kidney, followed by the gills, intestine, gonads, liver, and muscle. This phenomenon, called organotropism, has already been described

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(Calendini 2000; Farag et al. 1994; Sindayigaya et al. 1992). It may be related to differences in the ecological needs, swimming behavior, and metabolic activities of various fish species (Canli and Atli 2003). The levels of arsenic and antimony in Salmo trutta are higher in the river that crosses the abandoned mine, although mining stopped several decades ago. More attention should be paid to organotrophism as a warning signal for fish health and human consumption; however, Spella et al. (1993) pointed out that arsenic at the studied site (Presa) was found in two forms: (i) AsIII?, preponderant in more toxic sediments; and (ii) AsV?, in less toxic water. Consumption of the water is prohibited in the village of Matra. However, contamination risks remain because there are kitchen gardens near the Presa. Thus, contamination can take place by ‘‘washing’’ of the grounds or streaming of rainwater. It would be interesting to see if signs of arsenicose develop, with the appearance of skin problems, cancer, and vascular diseases, subsequent to consumption, after a long period, of fruit, vegetables, fish, etc. The brown trout is a carnivorous fish, but the composition of its diet varies according to the season and its size. The behavior and ecology of fish may be significantly influenced by contamination. They feed indifferently on small invertebrates (crustacean, mollusks, aquatic larvae, and air insects) and sometimes congeneric fish or small frogs, which are known to accumulate high levels of toxic elements in their body (Roesijadi and Robinson 1994). Our study also aimed to investigate relationships between arsenic and antimony tissue concentrations and fish length. We found a negative correlation between fish size and arsenic levels in the gonads as well as between fish size and antimony levels in the gills (Table 3). The negative relationship obtained can be explained by more active metabolism in younger, compared to older, individuals. Canli and Atli (2003) also supported the idea that accumulation decreases with an increase in fish length. On the contrary, it has been reported that organs tend to accumulate high concentrations of heavy metals with increased fish size (Zyadah 1999). Barghigiani and De Ranieri (1992) and Nussey et al. (2000) reported that bioaccumulation of elements in tissues varies depending on fish length. There are reports in the literature that trout have also shown reduced growth and survival as a result of ingesting macroinvertebrates in which toxic element concentrations were elevated (Farag et al. 1994; Woodward et al. 1994). Elevated trace-element concentrations in the Clark Fork River in Montana have caused fish kills and suppression of fish production (Phillips and Lipton 1995). According to Canpolat and Calta (2003) and Hellin (1986), higher levels of elements in gills of small fish can be explained by the fact that smaller fish perform more intensive activities than adults and require more oxygen to


provide higher energy. In order to maintain oxygen small fish filter more water through their gills (location of respiratory and osmoregulatory functions). Consequently, the concentration of arsenic and antimony in gill tissue is important. Indeed, the adsorption of elements on the gill surface could also have an important influence on the total contamination level of the gills (Canli and Furness 1993; Roesijadi and Robinson 1994). Moreover, studies carried out on fish exposed to toxic elements have reported an increase in the production of mucus that covers the body and gills (Handy and Eddy 1989; Wilson et al. 1994). This excess mucus may serve as a binding site to capture toxic elements. In the present study, the average arsenic concentrations in tissue and organs (kidney, gonads, and liver) of female brown trout were higher than those in male fish (Fig. 2). This can be explained by physiological differences between males and females. Furthermore, it may be related to differences in the metabolic activities, ecological needs, and swimming behaviors of the two genders. The relationship between metal accumulation in tissues and organs according to fish gender is supported in the literature (AlYousuf et al. 2000). Deb and Santra (1997) carried out research in sewage-polluted areas in India and showed that the levels of toxic elements in fish tissues were highest in the liver, followed by the brain, muscles, and ovaries in females.

Conclusion In summary, the findings of this study indicate that As and Sb concentrations in trout vary according to tissue or organ, fish length, and fish gender. The lowest As and Sb concentrations were found in the gonads and the liver, respectively. For both As and Sb, the highest concentration was recorded in the kidney. There was a negative correlation between fish size and arsenic levels in the gonads as well as between fish size and antimony levels in the gills. Female fish appeared to accumulate higher concentrations than males. Despite the high concentrations found in trout, the risk for human consumption seems to be minimal relative to the maximum recommended concentration per day. Knowledge of the concentrations of arsenic and antimony in salmonid freshwater fish species is important with respect to nature management and human consumption of fish and could serve to support the authorities responsible for monitoring food and environmental pollution in the locale. Acknowledgment We thank the Serveis Cientı´fico-Te`cnics of the University of Barcelona for their valuable contribution to the development of this study.

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