Bioaccumulation of heavy metals in marine fishes (Siganus sutor, Lethrinus harak, and Rastrelliger kanagurta) from Dar es Salaam Tanzania

Regional Studies in Marine Science 7 (2016) 72–80

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Bioaccumulation of heavy metals in marine fishes (Siganus sutor, Lethrinus harak, and Rastrelliger kanagurta) from Dar es Salaam Tanzania Prisca Mziray, Ismael Aaron Kimirei ∗ Tanzania Fisheries Research Institute (TAFIRI), P.O. Box 90, Kigoma, Tanzania

highlights • • • • •

Metal concentrations in muscles, livers and fins of three commercial fish species were studies and health risks of eating contaminated fish assessed. Metal concentrations in the fish muscle varied among fish species reflecting diverse ecological needs and habitat preferences. Metal concentrations in tail fins support the use of this organ for non-invasive biomonitoring of some metals and fish species. Arsenic concentration in Lethrinus harak and Rastrelliger kanagurta was higher than the FAO/WHO maximum recommended levels. The study recommends a reduction of L. harak and R. kanagurta in daily meals.

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Article history: Received 24 March 2016 Received in revised form 22 May 2016 Accepted 31 May 2016 Available online 4 June 2016 Keywords: Fish liver Fish muscle Metal pollution Risk assessment Tail fin Toxic metals

abstract Toxic metals that bioaccumulate and magnify along food chains are a concern to human health worldwide. This study determined heavy metal concentrations in three commercial fish species; viz: whitespotted rabbitfish (Siganus sutor), thumbprint emperor (Lethrinus harak), and the Indian Mackerel (Rastrelliger kanagurta) from Kunduchi fish market in Dar es Salaam, Tanzania, assessed potential risks to human health, and the suitability of their fins as a non-destructive monitoring organ. Metal concentrations in fish muscle differed significantly among fish species as a result of their diverse ecological needs, metabolism, feeding habits, and habitats. The results also indicated that fish fin may not be a very good non-destructive monitoring organ for most metals, but can be used selectively for some metals and fish species. The levels of metal intake (aluminum (Al), cadmium (Cd), copper (Cu), iron (Fe), lead (Pb) and zinc (Zn)) in fish muscles were below the FAO/WHO maximum levels for contaminants and toxins in foods for human consumption except for arsenic (As) which were higher than the recommended levels in Lethrinus harakand Rastrelliger kanagurta. It is recommended to reduce the amount of L. harakand R. kanagurta in daily meals of especially fishers and coastal communities who may eat fish up to three meals daily. Recommendation for further studies is provided. © 2016 Elsevier B.V. All rights reserved.

1. Introduction Marine fishes are important sources of protein. They form a significant part of the human diet to a multitude of people living in and around coastal cities, towns and villages. They are also low in cholesterol, calories, sodium and saturated fats; have high quality protein, essential minerals such as calcium (Ca), potassium (K), iodine (I), iron (Fe), zinc (Zn) and selenium (Se), and are rich in essential omega-3 fatty acids (USEPA, 2004; Denton et al., 2010).

∗

Corresponding author. E-mail addresses: [email protected] (P. Mziray), [email protected] (I.A. Kimirei). http://dx.doi.org/10.1016/j.rsma.2016.05.014 2352-4855/© 2016 Elsevier B.V. All rights reserved.

However, human activities in and near coastal waters, and around rivers draining into the world’s estuaries and oceans have caused severe deterioration of water quality through heavy/trace metal contamination and pollution among many other issues (Govers et al., 2014; Liu et al., 2014). It is within these estuaries and shallow nearshore waters that most artisanal and small scale subsistence fishers go for fishing—to get their daily meals and income. Heavy metals have special ecotoxicological importance because of their persistence and toxicity (Weber et al., 2013). They are known to bio-accumulate in organisms including plants and fish (Kojadinovic et al., 2007; Pereira et al., 2009; Yi et al., 2011; Govers et al., 2014), especially in fish liver (Chi et al., 2007). They can also biomagnify along the food chain—resulting into myriad ecological damages and health risks to ecosystems and humans

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respectively (Chi et al., 2007; Kaneko and Ralston, 2007; Ahmad et al., 2010; Yi et al., 2011; Weber et al., 2013; Govers et al., 2014; Leung et al., 2014; Liu et al., 2014). The risks to humans are most notable when contaminated fishes are consumed beyond the allowed/recommended daily intake levels (Kaneko and Ralston, 2007; Ahmad et al., 2010). Heavy metals enter fish by direct absorption from water through their gills and or skin, and by ingestion of contaminated food or non-food particles (Jargensen and Pedersen, 1994; Weber et al., 2013). The metals then enter the fishes’ blood stream and are carried to and accumulate into their tissues, mainly liver, where they are bio-transformed and excreted or taken up the food chain to consumers – such as human beings – causing either acute or chronic diseases and even fatal cases (Jargensen and Pedersen, 1994; Weber et al., 2013). Metal bioaccumulations in fish, like in most organisms (Mubiana and Blust, 2006), is dependent on bioavailability – which is determined by prevailing environmental factors such as pH, temperature, and alkalinity (Wagner and Boman, 2003), pollutant type, sampling location, and species-specific physiological and ecological characteristics – such as feeding habits, age/life span, size, sex, habitats, and trophic level (Schuhmacher et al., 1992; Kojadinovic et al., 2007; Rejomon et al., 2010; Weber et al., 2013). In the aquatic food chain, fishes are located at the mid-end of the trophic level (Jargensen and Pedersen, 1994). Metal accumulation is less in fishes at low trophic position but high in those positioned high up in the food chain, although contradictory results have been reported for certain metals (Cui et al., 2011). Metals absorbed by fish are distributed differentially in fish organs (e.g. liver, gills, muscle, and gonads) thereby causing variations of metal accumulations in these organs (Chi et al., 2007). Liver, gills and muscle are mostly used as bio-indicators in metal analysis of fish due to their different roles in metal bioaccumulation process and their potential in human diet (Al-Yousuf et al., 2000; Henry et al., 2004; Agusa et al., 2005; Ploetz et al., 2007; Yılmaz et al., 2010). Muscle is the main edible part of fish by human and thus forms the most preferred tool for the assessment of public health risks associated with metal pollution in fish (Reinfelder et al., 1998; Kaneko and Ralston, 2007; Yi et al., 2011). The Indian Ocean and other tropical waters in general are the least monitored in terms of heavy metal contamination in fishes and the associated human health risk assessment in the world (Kojadinovic et al., 2007). However, while very few published studies on metal pollution in fish and their associated human health risk in some Western Indian Ocean coastal states exists (Kojadinovic et al., 2006, 2007), the case is particularly different for Tanzania where such studies are non-existent. This study therefore intended to determine the extent of metal contamination in three commercial marine fish species in Dar es Salaam, Tanzania and assess their associated potential human risk. It also intended to assess the use of a fish fin as a suitable organ for non-destructive/non-invasive monitoring of heavy metal contamination. 2. Material and methods 2.1. Sampling Three fish species namely Siganus sutor (White-spotted rabbitfish), Lethrinus harak (Thumbprint emperor), and Rastrelliger kanagurta (Indian Mackerel) – which belong to the family Siganidae, Lethrinidae and Scombridae respectively – were selected and used in the current study. The species were selected because they are ubiquitously caught and are of economic importance along the Tanzanian, and the entire East African coast of the

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Fig. 1. A map showing the study location.

Indian ocean (Bianchi, 1985). They are also caught by, and form a significant part of the daily meals of, local artisanal fishers in Tanzania. S. sutor is an herbivore—grazing mainly on macro-algae (Kamukuru, 2009), which spends most of its life in seagrass beds in inshore areas (Kimirei et al., 2011). L.harak is a macrobenthivore which sometimes predates on fish. It feeds mainly on zooplankton when juvenile and on mollusks, crabs, echinoderms, worms, and fish during sub-adult and adult stages (Kimirei et al., 2013). L. harak lives in coastal waters, reefs and lagoons, mudflats, and seagrass beds (Richmond, 1997; Kimirei et al., 2011). R. kanagurta is a pelagic species which lives in coastal surface waters; it is mainly a planktivore but sometimes feeds on other pelagic fishes like sardines (Richmond, 1997). For each of the selected species, a total of 50 mature individuals (TL = 25–30 cm for S. sutor, 25–35 cm for L. harak and 30 cm for R. kanagurta) were directly bought from local artisanal fishers who landed at the Kunduchi fish market in Dar es Salaam, Tanzania. Typically, this particular market sells fishes caught by local small scale artisanal fishers who operate along the coast within the limits of Tanzania’s territorial waters. For this study, fishes were bought from local handline fishers, who catch their fish from reefs around the Mbudya and Fungu Yasini Islands (Fig. 1), about 3–5 km from the Kunduchi coastline (Kimirei et al., 2011). Each of the collected fish species was placed on a clean board and a piece of muscle (about 50 g wet weight), liver (8–10 g wet weight), and tail fin (4–6 g) were collected and placed, separately, in clean pre-labeled ziplock polyethylene bags. However, the materials collected were enough for analysis since very small sample sizes are required during sample analysis. The samples were then preserved in cool boxes with ice, transferred to a deep-freezer (temperature = 4 °C) at the University of Dar es Salaam, and

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Table 1 The recovery rates (expressed as percentage of certified values) of all the reference materials used in this study. MV = measured values; CV = certified values; RSD = relative standard deviation. Metal

Reference materials BCR 422

Ag Al As Cd Co Cr Cu Fe Mn Ni Pb Se Zn

Cod muscle

MV (µg/g)

RSD (%)

0.14 6.64 21.5 0.02 0.02 0.01 1.09 5.44 0.52 0.11 0.09 1.79 20.4

0.03 1.53 4.90 0.00 0.00 0.00 0.12 1.01 0.08 0.01 0.00 0.21 4.30

CV (µg/g)

VMK 102 Recovery (%)

21.10 0.02 0.02

101.9 92.00 103.1

1.05 5.46 0.54

103.8 99.60 96.30

0.09 1.63 19.60

103.6 109.7 104.3

transported frozen to the laboratory of ecophysiology, biochemistry and toxicology, at the University of Antwerp, in Belgium for analysis. 2.2. Metal analysis Fish samples (muscle, liver, and tail fin) from the three fish species were placed separately in pre-weighed clean polypropylene tubes, oven dried to constant weight at 60 °C and thereafter cooled for 30 min. The dry weight of each sample was then measured/weighed and recorded. The final sample weights (dry weight) after drying were 2.72 g, 0.48 g and 0.52 g for muscle, liver and fin tissues respectively. From each of the prepared samples, 5 ml of ultra-pure nitric acid (HNO3 , 69%) were added and left at room temperature for forty eight (48) hours after which they were allowed to digest on a hot block (105 ± 2 °C) for 30 min. The digested samples were then left to cool for 5 min followed by an addition of 0.5 ml of 27% Hydrogen peroxide (H2 O2 ) and placed back on the hot block for 25–30 min for the final digestion process. After cooling, the digested samples were diluted to a 50 ml mark using Mill-Q water. The concentrations of metals i.e. Silver (Ag), Aluminum (Al), Arsenic (As), Cadmium (Cd), Cobalt (Co), Chromium (Cr), Copper (Cu), Iron (Fe), Manganese (Mn), Nickel (Ni), Lead (Pb), Selenium (Se), and Zinc (Zn) in the prepared sample solutions were analyzed using a High Resolution-Inductively Coupled Plasma-Mass Spectrometer (HR-ICP-MS). The concentrations of metals in each sample, measured as microgram per liter (µg/L), were converted into microgram per gram (µg/g) of dry tissue by multiplying with the total volume of the sample solution and dividing by the dry weight of the respective tissue sample. Analytical efficiency was checked using VMK 102 (muscle tissue) and cod muscle (422). Blank (only reagents) were also included in each set of run of sample digestion. 2.3. Quality control Blanks were prepared and included in the measurements in order to take into account the background concentrations of metals in the reagents, and any form of unintended contamination during preparation of samples. The concentrations of metals in the blanks were then deducted from the concentration values of the samples. Certified Reference Materials (CRM) were also included in the entire analysis process (i.e. from sample preparation stage to analysis and data analysis). In all cases, the recoveries were within the traditionally accepted 10% of the certified values; which means that the results of this study can be considered to be an accurate reflection of the true concentrations in the samples (see Table 1).

Mussel tissue

MV (µg/g)

RSD (%)

3.08 35.82 14.44 2.80 2.13 1.68 9.44 200.9 4.69 6.71 6.10 5.89 120.0

0.48 4.18 2.05 0.35 0.22 0.25 0.85 27.35 0.55 1.76 0.60 0.72 5.95

CV (µg/g)

Recovery (%)

2.90

96.70

10.10 192.0 4.70

93.40 104.6 99.70

114.0

105.3

2.4. Statistical analysis The data were first tested for normality and homogeneity of variance using Shapiro–Wilk and Levene’s tests respectively. Most of the data were not normally distributed even after log transformation, and thus a non-parametric equivalent was used. Comparisons of metal concentrations among species of fish and organs/tissues (liver, muscle and fin) were tested using Friedman’s statistic (a non-parametric equivalent of a repeated measure ANOVA). Multiple comparisons between groups (species) were performed using a Dunn’s test. Comparisons of metal concentrations on fish muscles were tested by a Kruskal–Wallis test followed by a Dunn’s post-hoc test. Metal concentrations in liver and muscle were correlated with concentrations in the tail fin using a Spearman rank correlation. This was performed to determine a relationship between these tissues with tail fin. This analysis intended to assess the viability of using a fish fin as a nondestructive bio-monitoring organ for metals in fishes instead of using other organs which involve killing the whole fish (e.g. fish liver, muscles). Before the correlation of metal concentrations between fish organs was performed, the data were first corrected for the effect of length using a linear function: y = mx + c, where ‘m’ is the slope of the linear function, ‘x’ is the fish total length and ‘c’ is the y-intercept. The y-intercept was calculated to determine the metal concentrations that are not affected by length. The obtained concentrations were then correlated using a Spearman r statistic. All outliers were removed from the data set before further analysis. All the statistical tests were done using GraphPad Prism 5 (GraphPad Software Inc., USA). Human risk assessment of consuming contaminated fish was calculated based on the fish consumption pattern of Tanzania. This was then compared with the recommended Maximum Levels (ML) for contaminants and toxins in foods by FAO/WHO (2010) (see Table 3). The consumption pattern was calculated based on the Tanzanian average fish intake of 21.92 g/day/person (MLFD, 2010). This intake was multiplied by the metal concentrations in fish. The obtained values were then divided by the average body weight of a person, which in our case we used 75 kg. 3. Results 3.1. Distribution of metal in fish tissues Metal concentrations were generally highest in the liver than in the muscle and tail fin tissues for almost all fish species (Fr ≥ 13.03, p < 0.05; Fig. 2, Table 2); except for S. sutor and R. kanagurta which had high values of Al, Pb, Mn, Cr and Al and Pb in their fins respectively (Fig. 2, Table 2). Moreover, there were highly

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Table 2 Comparisons of mean metal concentrations in liver, muscle, and tail fin of S. sutor, L.harak and R. kanagurta. FR = Friedman’s test. Species

Metal

Liver Mean

Muscle Mean

Tail fin Mean

FR

p-value

S. sutor

Ag (ng/g) Al (µg/g) As (µg/g) Cd (µg/g) Co (µg/g) Cr (µg/g) Cu (µg/g) Fe (µg/g) Mn (µg/g) Ni (µg/g) Pb (ng/g) Se (µg/g) Zn (µg/g) Ag (ng/g) Al (µg/g) As (µg/g) Cd (µg/g) Co (µg/g) Cr (µg/g) Cu (µg/g) Fe (µg/g) Mn (µg/g) Ni (µg/g) Pb (ng/g) Se (µg/g) Zn (µg/g) Ag (ng/g) Al (µg/g) As (µg/g) Cd (µg/g) Co (µg/g) Cr (µg/g) Cu (µg/g) Fe (µg/g) Mn (µg/g) Ni (µg/g) Pb (ng/g) Se (µg/g) Zn (µg/g)

1618.06 24.21 9.92 13.85 5.50 0.51 40.26 1651.05 20.21 1.62 210.26 10.74 952.02 2717.56 129.08 119.86 108.04 5.16 2.61 292.12 20 292.57 78.41 3.09 3806.78 83.26 2319.21 308.77 16.48 29.02 18.36 0.94 0.50 36.12 1156.30 12.95 0.61 367.55 56.88 246.83

4.78 18.44 3.43 0.04 0.26 0.10 1.65 34.02 5.55 0.12 45.92 1.70 67.75 0.64 87.00 18.52 0.14 0.09 0.29 4.71 103.29 10.18 0.15 144.98 4.93 214.59 16.20 15.05 12.13 0.13 0.12 0.11 9.17 125.14 2.79 0.14 67.54 9.51 104.01

3.19 296.02 3.68 0.15 0.75 0.66 1.51 108.32 70.21 0.33 961.98 1.39 338.85 4.11 117.32 1.32 0.04 0.05 0.20 0.76 46.00 18.65 0.09 352.94 1.51 125.91 50.91 30.39 2.65 0.15 0.05 0.18 2.98 40.35 12.32 0.09 456.88 1.89 202.22

45.27 68.40 66.05 74.45 86.05 69.33 58.32 84.05 94.00 80.81 36.10 66.47 77.64 45.60 13.03 78.00 58.26 61.46 56.63 74.00 57.00 78.20 48.25 48.31 86.00 74.21 50.48 38.28 78.00 51.06 68.22 45.50 66.00 88.38 67.78 29.25 49.00 86.00 72.89

<0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001

L. harak

R. kanagurta

significant differences, for all metal concentrations, in different tissues among fish species (p < 0.05). Comparison of metal concentrations among fish tissues were significant for most metals (p < 0.05; Fig. 2) except for Al in S. sutor which did not differ significantly between liver and muscle (p > 0.05; Fig. 2); Al in L. harak, Mn, Pb and Zn in R. kanagurta which did not vary significantly between liver and tail fin (p > 0.05); and Ag, As, Cu, Mn, Se in S. sutor, Ag, Al, Cr, Ni in L. harak and Cd, Ni in R. kanagurta which did not show significant differences between muscle and tail fin (p > 0.05; Fig. 2). 3.2. Metal concentrations in fish muscle The concentrations of metals in muscle tissues of all the three fish species were significantly different (K–W ≥ 7.465, p < 0.02, Fig. 3, Table 3) except for Ni whose concentrations were not significantly different among species (K–W = 5.051, p = 0.08). All metal concentrations were significantly different between muscles of L.harak and S. sutor, with L. harak having generally highest concentrations. Rastrelliger kanagurta had the highest concentration of Ag, Cu, and Se (p < 0.001); while L. harak muscle had significantly highest concentrations of As, Cr, Mn, Al and Zn. S. sutor had significantly highest concentration of Co than in L. harak and R. kanagurta (p < 0.001; Fig. 3, Table 3). 3.3. Non-destructive bio-monitoring organ (using tail fin) The correlations between tail fins of the three fish species with their respective livers and muscles for most metals were generally

0.0015

<0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001

Table 3 Comparison of metal concentrations in the muscle tissues of S. sutor, L. harak, and R. kanagurta. K–W = Kruskal–Wallis test. Metal

K–W

p-value

Ag Al As Cd Co Cr Cu Fe Mn Ni Pb Se Zn

86.19 89.25 108.7 51.71 85.66 58.19 113.4 96.99 86.84 5.051 7.465 121.4 107.2

<0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 <0.0001 0.0800 0.0239 <0.0001 <0.0001

not significant (R ≥ −0.50, p > 0.05; Table 4). However, a few exceptions were observed for some metals, such as Co, Fe, and Ni in S. sutor (R ≥ 0.51, p < 0.05) and Ag and Co in L. harak (R ≥ 0.37, p < 0.05) (Table 3) which showed a significant positive correlation between tail fin and liver; whereas Co, Ni and Pb for S. sutor; Mn for L. harak, and As and Cu for R. kanagurta showed a significant positive correlation between tail fin and fish muscle (R ≥ 0.56, p < 0.05) (Table 5). A few significant negative correlations were also found for R. kanagurta between fin and liver, and fin and muscle for Cr, Ni, and Zn (R ≥ −0.28, p < 0.045) and Ag (R = −0.499, p = 0.002) respectively (Table 4).

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P. Mziray, I.A. Kimirei / Regional Studies in Marine Science 7 (2016) 72–80 Table 4 Correlations of metal concentration between fish tissue (i.e. tail fin vs. liver and tail fin vs. muscle). Shaded values represent significant positive or negative. Specie(s)

Metal

Siganus sutor

Fin vs. Liver p

Spearman r

p

Ag (ng/g) Al (µg/g) As (µg/g) Cd (µg/g)

−0.1748 0.0116 0.0864 0.2292

0.2507 0.9385 0.5508 0.1392

0.1379 −0.0169 0.0715 0.0841

0.3961 0.9124 0.6253 0.5827

Co (µg/g)

0.5162

0.0003

0.5590

0.0001

Cr (µg/g) Cu (µg/g)

0.2382 −0.0826

0.1151 0.6126

0.8048 0.7828 0.1717

Fe (µg/g)

0.5522

0.0001

−0.0393 −0.0438 −0.2123

Mn (µg/g)

0.1503

0.3132

0.1998

0.1781

Ni (µg/g)

0.5118

0.0002

0.4018

0.0051

Pb (ng/g)

0.1275

0.3985

0.4397

0.0358

0.1704 −0.0417

0.2468 0.7736

0.0316 −0.2447

0.8312 0.0974

Se (µg/g) Zn (µg/g) Lethrinus harak

Ag (ng/g)

0.3676

0.0324

0.1726

0.4200

Al (µg/g) As (µg/g) Cd (µg/g)

−0.0803 0.0332 0.1242

0.6132 0.8247 0.4055

0.2513 0.0017 −0.0535

0.1041 0.9913 0.7639

Co (µg/g)

0.3931

0.0047

−0.0535

0.7335

Cr (µg/g) Cu (µg/g) Fe (µg/g)

0.1706 0.2660 0.1093

0.2801 0.0886 0.5136

0.3207 0.1443 −0.1242

0.0603 0.3682 0.4451

Mn (µg/g)

Rastrelliger kanagurta

Fin vs. Muscle

Spearman r

0.1230

0.4153

0.3397

0.0241

Ni (µg/g) Pb (ng/g) Se (µg/g) Zn (µg/g)

−0.0257

−0.2591

0.1432 0.0716 0.0870

0.8815 0.3480 0.6248 0.5611

0.1904 0.0849 0.1991

0.1064 0.3514 0.5884 0.1846

Ag (ng/g)

−0.0605

0.6766

Al (µg/g)

0.1673

0.2719

−0.4993 −0.1075

0.4821

As (µg/g)

0.0980

0.3409

0.0272

0.6253 0.4027 0.0165

−0.1804 −0.0358 −0.1105

0.2853 0.8175

Cr (µg/g)

−0.2653 −0.0739 −0.1379 −0.3818

Cu (µg/g)

0.0112

0.9410

0.3233

0.0235

Fe (µg/g) Mn (µg/g)

0.0952 0.2376

0.5198 0.1078

−0.1310

0.3695 0.6172

Ni (µg/g)

−0.4855

0.0088

0.0916

0.6123

Pb (ng/g) Se (µg/g)

0.2648 −0.2439

0.0754 0.1150

−0.1435 0.1443

0.4181 0.3444

Zn (µg/g)

−0.2849

0.0449

−0.0622

0.6679

Cd (µg/g) Co (µg/g)

0.0748

0.0017

0.4649

Table 5 Comparison of fish consumption pattern in Tanzania and FAO/WHO Maximum Levels for contaminants and toxins in foods. All values are in µg/kg. Min = minimum; Max = maximum; n = sample size. Species

Metal

n

Min

Mean (SD)

FAO

S. sutor

Al As Cd Cu Fe Pb Zn

48 49 47 48 48 23 47

2.121 0.426 0.001 0.124 5.397 2.00E−07 10.088

Max 13.604 1.898 0.076 0.75 25.731 0.047 48.741

5.389 (7.6) 1.003 (1.1) 0.013 (0.03) 0.491 (0.4) 10.148 (8.9) 0.014 (22.1) 20.222 (16.3)

1000 3 7 50–500 800 25 300–1000

L.harak

Al As Cd Cu Fe Pb Zn

44 42 36 43 43 28 43

6.478 2.203 0.002 0.13 13.511 2.70E−07 22.633

84.372 11.211 0.208 5.387 79.229 0.161 102.788

25.427 (51.1) 5.413 (5.6) 0.040 (0.1) 1.408 (1.8) 30.893 (37.7) 0.044 (124.1) 64.182 (63.1)

1000 3 7 50–500 800 25 300–1000

R. kanagurta

Al As Cd Cu Fe Pb Zn

50 49 37 49 49 38 48

1.944 1.897 0.001 0.897 14.268 0.001 17.48

8.74 5.964 0.218 3.953 58.1 0.086 59.062

4.399 (4.9) 3.545 (2.5) 0.037 (0.1) 2.734 (1.1) 37.323 (32.3) 0.0203 (36.3) 31.039 (21.6)

1000 3 7 50–500 800 25 300–1000

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Fig. 2. Metal concentrations (mean + SD) in three fish species and tissues. Different letters (a, b, and c) indicate significant comparisons in metal concentrations between fish tissues among fish species.

3.4. Human risk assessment

4. Discussion

The levels of intake of Al, Cd, Cu, Fe, Pb and Zn in the fish muscles of all the three species were below the FAO/WHO Maximum Levels for contaminants and toxins in foods for human consumption. However, the concentrations of arsenic (As) in L. harak (mean ± SD = 5.413 ± 5.6 µg/kg) and R. kanagurta (3.545 ± 2.5 µg/kg) were found to be higher than the FAO/WHO maximum values (Table 5).

This study reports higher metal concentrations in the fish liver than in the muscles and tail fins for almost all the three fish species. The concentrations of As, Cd, Co, Cr, Cu, Fe, Ni, Se and Zn in the tissues of Lethrinus harak followed the liver > muscle > tail fin order of accumulation. A similar order of metal accumulation was followed for As, Cd, Co, Cu, Fe, Ni and Se in Rastrelliger kanagurta, and Ag, As, Cu and Se in Siganus sutor respectively. However there

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Fig. 3. Comparison of metal concentrations in the muscle tissues of three fish species. Different letters (a, b and c) indicate significant differences in metal concentrations among fish species.

were some intra-specific differences where some metals were highest in the tail fin than in the liver and muscle tissues. For example, the concentration values of Al, Pb, Mn and Cr were high in the tail fin than in the liver and muscle tissues of S. sutor. High metal concentrations in fish liver than in other organs (Al-Yousuf et al., 2000; Bervoets et al., 2001; Henry et al., 2004; Ploetz et al., 2007; Denton et al., 2010), and the existence of inter-specific differences in metal accumulation (e.g. de Mora et al., 2004; Kojadinovic et al., 2006, 2007) have also been reported elsewhere. For example Cd, Cu and Mn concentrations are normally higher in liver than in muscles for pelagic fish, especially tuna and tuna-like species, while Fe, Se and Zn vary among tissues inter-specifically (Kojadinovic et al., 2007; Pereira et al., 2010).

High metal accumulation in liver is probably related to the presence of the mercapto group in the metallothionein protein which is highest in the liver (El-Shahawi, 1996). These proteins bind, for example, Cu, Cd, and Zn allowing the liver to accumulate higher levels of metals than other organs. Therefore livers may accumulate pollutants of various kinds from the environment as a result of this property. Also, fish liver, like in most animals, plays an important role in contaminant storage, redistribution, and detoxification or transformation (Weber et al., 2013), and acts as an active site of pathological effects induced by contaminants (Evans et al., 1993). As a result, metals tend to distribute differentially in liver and muscle (De Smet et al., 2001). Metal turnover rates are also said to be high in liver and kidney than in muscle

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indicating longer time metal intakes in muscle (Kojadinovic et al., 2007). This study therefore finds liver to be the most important organ for heavy metal monitoring in fish and their associated environment; however, for long term exposures, muscle tissue may be appropriate. Metal concentrations in fish muscle, which is the main part of fish that is consumed by human beings, differed significantly among fish species under study (i.e. S. sutor, L. harak and R. kanagurta), except for Ni which showed no difference (see Fig. 3 and Table 3). The observed pattern in levels of heavy metals among fish species may be a consequence of diverse ecological needs, metabolism, feeding habits, and habitats into which they live (Ayse, 2003; Rejomon et al., 2010). L. harak, which accumulated the highest amounts of metals than the rest of the species, is a benthic species which feeds mainly on invertebrates such as echinoderms, worms, mollusks and crabs (Carpenter, 1996; Richmond, 1997; Kimirei et al., 2013); and inhabits coastal waters, reefs, lagoons, sandy bottoms and seagrass beds (Richmond, 1997; Kimirei et al., 2011), where pollution and metal contaminants are highest (Kruitwagen et al., 2008). Although L. harak accumulates substantial amounts of metal from its preys which are in constant contact with the metal-rich sediments, it may also be affected by its benthic lifestyle, thereby accumulating more metal from the environment. Similarly, S. sutor inhabits inshore areas, especially in seagrass beds and coral reefs (as adults), and graze on macro-algae and seagrass (Kamukuru, 2009; Kimirei et al., 2011; Richmond, 1997); however it did not show elevated levels of metals probably as a result of its trophic level (Kamukuru, 2009; Denton et al., 2010). On the other hand, R. kanagurta is a pelagic and highly migratory species which also spends some time in coastal surface waters. It feeds on phytoplankton (diatoms) and zooplankton (Richmond, 1997). It is possible that the availability of fewer metals in the muscle of R. kanagurta is linked to its life style. It has already been shown that some metals accumulate more in benthic fish species than their pelagic counterparts (Romeo et al., 1999; Rejomon et al., 2010). For example, Romeo et al. (1999) found that the concentrations of Cd, Cu and Zn in edible muscles of pelagic fish species were lower than in benthic fish species. Moreover, feeding habits, age, size, and habitats have already been shown to affect the amount of metals found in fishes (Amundsen et al., 1997; Mubiana et al., 2006; Kojadinovic et al., 2007; Weber et al., 2013). It is therefore plausible that the ecology of fishes may play an important role in metal bioaccumulation; however more studies need to be conducted to cement this observation in the Western Indian Ocean. Non-destructive/non-invasive methods in bio-monitoring involve the use of a certain part of the organism without killing or causing harm to it. This method is even more attractive in investigating pollution in endangered or threatened populations as it imposes minimal stress to individuals and populations. It also permits repeated monitoring of contamination levels and population characteristics of the same individuals and populations (D’Have et al., 2006). This study also tried to establish a relationship between metal concentrations in muscle and liver and tail fin in order to allow for non-invasive monitoring of the same in the future. There was no clear relationship for all species; however a few exceptions were found which could be used for this purpose. While Co, Fe, and Ni concentrations in the liver of S. sutor was significantly correlated to those in the tail fin, Co, Ni, and Pb correlated well with those in muscle. A similar relationship was found for Ag and Co for fin and liver, and Mn for fin and muscle in L. harak. While there was a significant negative relationship between fin and liver for Cr, Ni, and Zn, and for Ag between fin and muscle tissue in R. kanagurta, a significant positive relationship was only found for As and Cu between fin and muscle for the same species. Based on these findings, it is

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recommended therefore that tail fin may not be a very good biomonitoring organ for metal contamination in the three fish species since it can only reliably be used in certain species and with certain (very few) heavy metals. A human risk assessment for consuming contaminated fishes was performed for Al, As, Cd, Cu, Fe, Pb and Zn using the FAO/WHO Maximum Levels (MLs) of contaminants and toxins in food (including fish) (see Table 4). The concentrations of these metals were within the safe consumption levels except for As which was above the recommended levels of metal intake from food in two species – L. harak and R. kanagurta – (FAO/WHO, 2010). While the maximum concentration of As was 11.2 µg/kg in L. harak, it was about 6 µg/kg in R. kanagurta (see Table 4). These values are respectively about 4 and 2 times higher than the recommended levels (ATSDR, 2013; FAO/WHO, 2010). Similar results of As accumulation in L. harak and its several congeners have been reported in Saipan Island waters; but no health risks were found (Denton et al., 2010). However, a health risk from Hg, Cd and Zn has been suggested in the Reunion and Madagascar Islands from consuming tunas (Kojadinovic et al., 2006, 2007); and it has been suggested to reduce fish in meals of people in relation to mercury contamination in Madagascar (Kojadinovic et al., 2006). In conclusion, this study is among the first in the western Indian Ocean region to determine metal concentrations in fish landed at local seafood markets, and to assess if metal levels exceed the recommended limits. We acknowledge that this analysis is based on fish from one fish market and that sampling from other markets would have painted a better picture. However, the analysis intended to get a quick preliminary data which would represent local conditions, while assessing the inherent health risks to humans from consuming locally caught fishes. To accomplish this goal a sample for the best representative market of locally caught fishes was necessary; and Kunduchi market served the purpose. Therefore the results of this study should be interpreted in this context. Furthermore, we acknowledge that this study did not determine the different forms of Arsenic and align them to their toxicities. Arsenic is known to occur in two forms – inorganic and organic – with the organic form, which is most abundant in fish, being less toxic than the inorganic forms (Ratnaike, 2003). However, studies in Taiwan (Kar et al., 2011) and Pearl River Delta, China (Cheng et al., 2013) have found appreciable amounts of the toxic forms of Arsenic in fish suggesting that Arsenic contamination should not be taken lightly. Nonetheless, considering that most coastal communities, especially fishers along the Tanzanian coast, eat fish up to three meals daily and that these two species are popular table species, it is recommended to reduce the intake levels of these species until the organic–inorganic ratios of As have been ascertained in these species, and new safe levels established. Considering the findings from this study, it is recommended that future research and or metal pollution monitoring programmes should focus on fish from many other local fish markets in the region, profile the effects of urbanization, and compare pristine versus polluted areas. Also, research should focus on the bioaccumulation of Arsenic (and its forms) in locally caught fish species such as L. harak and R. kanagurta. Moreover, we recommend that further research should also focus on the assessment of the reliability of fish fins as a non-destructive bio-monitoring organ of metal pollution. Acknowledgments The authors extend sincere gratitude to VLIR-OUS who funded the first author’s M.Sc. studies and made this work possible. We are highly grateful to the University of Antwerp, Laboratory of ecophysiology, biochemistry and toxicology for allowing us to use

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