Metal bioaccumulation in representative organisms from different trophic levels of the

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Authors Mirzajani, A.R.; Hamidian, A.H.; Karami, M.

Download date 01/10/2021 01:50:17

Link to Item http://hdl.handle.net/1834/37675 Iranian Journal of Fisheries Sciences 15(3) 1027- 1043 2016

Metal bioaccumulation in representative organisms from different trophic levels of the Caspian Sea

Mirzajani A.R.1,2; Hamidian A.H.1*; Karami M.1

Received: May 2015 Accepted: October 2015

Abstract The bioaccumulations of metals Cu, Cd, Ni, Cr, Co, Mn, Zn and Fe were measured in bivalves, Cerastoderma glucaum, and four species of fishes including chalcoides, Liza aurata, Rutilus frisii and Sander lucioperca from various trophic levels of the Caspian food web. The concentrations of Cd, Cr, Co and Ni in most samples of fish were below the detection limits; while the concentrations were detected in most samples of bivalve C. glucaum. The stable nitrogen isotope ratios varied among the samples from C. glucaum (δ15N=3.5 ‰) to S. lucioperca (δ15N=13.1‰). Among the four fish species, while the highest concentrations of Mn, Ni and Fe were observed in L. aurata, the lowest concentrations of Mn and Fe were observed in S. lucioperca. These species also had the lowest and highest trophic levels with an average of 3.3 and 4.2, respectively. No accumulation of metals with increase in body size was observed in

Downloaded from jifro.ir at 9:20 +0330 on Sunday February 25th 2018 muscles of species from different trophic levels. The comparison of metal concentrations with the health guidelines for human consumption showed that those intakes were lower than the legislated limits. While there was a strong relationship between trophic levels and body size of A. chalcoides and R. frisii, no significant slopes were observed between the total lengths (TLs) and the Ln concentrations of metals. It is necessary to determine metal concentrations in food resources of fish species, particularly in R. frisii that has significantly different δ15N in relation to body size.

Keywords: Metal pollution, Bioaccumulation, Stable isotope, Caspian Sea

1-Department of Environment, Faculty of Natural Resources, University of Tehran, P.O. Box 4314, 31587-77878 Karaj, 2- Present address; Inland waters Aquaculture Research Center, Iranian Fisheries Science Research Institute, Agricultural Research Education and Extension Organization (AREEO), Badar Anzali, P.O. Box 66, Iran *Corresponding author's Email: [email protected] 1028 Mirzajani et al., Metal bioaccumulation in representative organisms from different trophic …

Introduction concentrations in the Caspian fishes. The Caspian Sea, the largest land- While nearly all of these reports were enclosed drainage area in the world, focused on the Acipenseridae species supports substantial fisheries, while it (particularly Acipenser persicus) and has been endangered by massive loads Rutilus frisii, other commercial fishes of contaminants. The various were less concerned. Furthermore, no environmental pollutants produced by research has been done according to natural and anthropogenic sources are trophic levels of Caspian fishes. discharged from coastal catchment Four species, A. chalcoides, Liza (Glantz, 2000; UNEP/UNDP, 2011). aurata, R. frisii and Sander lucioperca, The hazardous effects of heavy metals have a high commercial value and good on human health are reviewed by market demands in the southern international organizations such as the Caspian regions. These species are WHO (Järup, 2003). traditionally known as zooplankton Caspian fishes, an important source feeders, detritivrous, benthivorous and of protein, are consumed by millions of piscivorous, respectively (Ghadirnejad, people living around the Caspian Sea; 1996; Zarinkamar, 1996; Abbasi et al., therefore monitoring their metal 2004; Abdolmaleki and Ghaninezhad, pollution is essential (Fallah et al., 2007; Neamatparast, 2007). 2011). Stable isotope analysis has been Bioaccumulation is defined as an widely used, as a powerful tool, for increase in the concentration of source identification of changes in pollutants by an increase in age, which aquatic and estuarine ecosystems, and sometimes is reflected in size of the also for assessing pollutant flux in organism (Fernandes et al., 2007). marine ecosystems (Broman et al.,

Downloaded from jifro.ir at 9:20 +0330 on Sunday February 25th 2018 Metal bioaccumulation is influenced by 1992; Cabana and Rasmussen, 1996; various environmental and biological Vander Zanden and Rasmussen, 1996; factors particularly the feeding source Lake et al., 2001; Jardine et al., 2006). (Agusa et al., 2004; Wang and However the metal concentrations in Rainbow, 2008). Although referring to muscle tissues are reported to be scientific literature, very few data have usually lower than in other organs been published on metal accumulation (Pourang et al., 2005; Kojadinovic et related to size and age (Anan et al., al., 2007; Mashroofeh et al., 2013), the 2005; Pourang et al., 2005; Foroughi turnover rate of δ15N in muscle protein Fard et al., 2008; Pazooki et al., 2009; is much longer and represents the Hoseini and Tahami, 2012). There have integrated diet and contamination of been some research (Sadeghirad, 2002; fishes for a long time (Cabana and Agusa et al., 2004; Sadeghirad, 2007; Rasmussen, 1996; Vander Zanden and Shahryari et al., 2010; Eslami et al., Rasmussen, 1996). 2011; Fallah et al., 2011; Monsefrad et Typically the 13C/12C and 15N/14N al., 2012) presenting metals ratios of a consumer are slightly higher Iranian Journal of Fisheries Sciences 15(3) 2016 1029

than those in its diet. On average, δ13C sample was measured by Vernier and δ15N values of consumers are calipers; and then they were weighed expected to increase by around 1‰ and using a balance at the nearest 0.01g 3.4‰ compared to those of their food, precision. respectively (Minagawa and Wada, The dorsal muscles of fish samples 1984). The nitrogen isotope were individually dissected using a high compositions are particularly well- quality stainless steel knife; rinsed with suited for examining trophic dynamics distilled water and dried at 60 °C for 48 and provide an estimate of their trophic h. The dried samples were ground and position (Minagawa and Wada, 1984; homogenized with a pestle and mortar, Post, 2002) while carbon isotope stored in distilled water washed in elucidates the origin and pathways of plastic bags and kept at -20°C before organic matter in food webs (Le Loc'h the laboratory experiments. Gut organs et al., 2008). and shells of mollusks were carefully In this study, we determined metal removed under stereomicroscope and concentrations in A. chalcoides, L. their soft tissues were pooled (20-30 aurata, R. frisii and S. lucioperca. individuals as one sample). The Furthermore, we studied the metal samples were oven dried at 60 °C for 24 bioaccumulation based on the trophic h. The preparation of samples followed levels in the Caspian food web. the ROPME instructions (1989).

Material and methods Chemical analyses Sample collection For metal (Cu, Cd, Ni, Cr, Co, Mn, Zn The collections included Pike-perch (S. and Fe) analyses, a mass of around 0.5 lucioperca) (n=16), Kutum (R. frisii) g of each sample was digested in4 ml

Downloaded from jifro.ir at 9:20 +0330 on Sunday February 25th 2018 (n=25), Danube bleak (A. chalcoides) high purity nitric acid (Merck, 65%) (n=20) and Golden grey mullet (L. and 1 mL perchloric acid (Merck, 70%) aurata) (n=16). These species were at room temperature. Digestion freshly collected from Anzali region continued on a sand bath with a (~37 28 N 49 33 E) during winter- maximum temperature of 115 °C, for spring of 2013. Two fishing methods; about 4 h and until the solutions were beach seine and gill net (Gerami and cleared. After cooling, the solutions Dastbaz, 2013) were used for sampling. were filtered through Whatman filter Furthermore about 360 individuals of membranes and were diluted up to 10 the benthic invertebrates bivalvia C. ml in a volumetric flask with deionized glucaum were freshly collected along distilled water. The digestion procedure the beach down to 20 meter depths by followed the ROPME instructions hand and by using a bottom sampler (1989) and Pourang (1995, 1996). (Van-Veen grab: 400 cm²), A HP 4500 ICP-MS, equipped with respectively. The total length of each Asx-520 Autosampler (England) was 1030 Mirzajani et al., Metal bioaccumulation in representative organisms from different trophic …

used for the determination of metal of primary consumers (PC; i.e. bivalve concentrations in the samples. In order C. glucaum ), 3.4 and 2 are the mean to control the quality of the δ15N trophic enrichment occurring per measurement for each 25 samples, 2 trophic level and the trophic position of blanks and 2 spiked samples were used. the baseline organism, respectively. Instrumental detection limits for most Commonly, the primary consumers

metals was 0.02 µg/g, except for Cd (TL2) are preferred to primary

(0.01 µg/g) and Fe (0.1 µg/g). The producers (TL1) for evaluation of recoveries for Cd, Cu, Co, Cr, Ni, Mn, trophic levels (Cabana and Rasmussen, Zn and Fe were 84%, 107%, 79%, 94%, 1996; Vander Zanden et al., 1999; 101%, 86%, 72% and 72%, Vander Zanden and Rasmussen, 2001). respectively. We did not calculate the trophic levels of C. glucaum individuals because the Stable isotope analysis and trophic stable isotopes of particle organic level calculation matter (POM) as its baseline had high The stable isotope signatures were used variations in our sampling. to calculate the trophic levels. Around 1 mg of homogenized powder of each Statistical analyses sample was weighed in tin capsules. No The Kolmogorov-Smirnov and further steps were taken for the Levene’s tests were used to control the elimination of carbonates and lipids normality of distribution and the because this helps us to avoid homogeneity of variances, respectively. dispersion of δ13C and δ15N. Simple linear regressions were All stable isotope measurements performed using ln-transformed metal were performed at the University of concentrations in muscle vs. trophic

Downloaded from jifro.ir at 9:20 +0330 on Sunday February 25th 2018 California, Davis, USA. Isotope values levels. The slopes of regressions were were expressed in standard d-notation used to determine the rate of relative to the international V-PDB bioaccumulation through the body size (Vienna PeeDee Belemnite) for carbon of the Caspian fishes and bivalves. One

and atmospheric N2 for nitrogen, using way ANOVA and Tukey test were used the standard equation; to assess differences among the δ13C, 13 15 15 δ C or δ N = [(R Sample /R Standard)- δ N values and size groups of fishes. 1]×1000 The statistical analyses were not where R is 13C/12C or 15N/14N. conducted when >50% of the The trophic level (TL) was observations were below the detection calculated using the following equation: limit. The statistical tests were 15 15 TLi = [(δ Ni - δ Npc)/3.4]+2 performed at the significance level of where TLi is the trophic level of fish p<0.05 and the software SPSS version 15 15 species i, δ Ni represents the δ N of 13 for Windows was used. 15 15 fish species i, δ Npc represents the δ N Iranian Journal of Fisheries Sciences 15(3) 2016 1031

Results lucioperca (average 9.3 µg g-1), and the According to our results, the content of highest concentrations of most metals C and N in samples was the lowest in were observed in L. aurata (Table bivalves, C. glucaum while those 1).The lowest concentrations of Mn and amounts were the highest in fish A. Fe were observed in S. lucioperca chalcoides (Table 2). The stable (average 0.7, 7.1 and 9.4 µg g-1 dw), nitrogen isotope ratios varied among respectively. the samples from C. glucaum (δ15N=3.5 There was strong correlation between ‰) to S. lucioperca (δ15N=13.1‰). The body length and body weight stable carbon isotope ratios varied from (Spearman’s correlation coefficient = A. chalcoides (δ13C = -25.2‰) to S. 0.99, p<0.05). Therefore, body size was lucioperca (δ13C = -17.9‰) (Fig. 1). used instead of body length and weight The average δ15N was nearly similar for (Table 3). three species R. frisii, L. aurata and A. An increase in trophic levels of A. chalcoides (Table 2). Among fish chalcoides and R. frisii vs. their body species, L. aurata and S. lucioperca had size increase was observed. Generally the lowest and highest TLs; with no accumulation of metals with average TLs of 3.3 and 4.2, increase in body size was observed in respectively. muscles of all species from different The statistical test showed that only trophic levels (Figs 2 and 3). Size- δ13C had significant difference (F=6.4; dependent concentrations of metals p<0.05; ANOVA) with small size (total were only observed for Cr and Fe in C. length<60 mm) and big size groups glucaum (Fig. 2). While no significant (total length>200 mm) of A. chalcoides. correlation were observed between Furthermore, the δ15N and TL values metal concentrations and fish size (also

Downloaded from jifro.ir at 9:20 +0330 on Sunday February 25th 2018 in the small size of R. frisii (total TLs) of L. aurata, negative significant length<140mm) was more than medium relationships were observed between (total length 141-500 mm) and big size Mn and Zn concentrations and fish size (total length>500 mm) (F=7.3 and for A. chalcoides (Fig. 3). These F=5.5, respectively; p<0.05). relationships were also observed for Cu Cd, Cr, Co and Ni concentrations in and Zn in S. lucioperca and for Mn in most of fish samples were below the R. frisii. In our study, no significant detection limits; while the decrease in concentrations of metals concentrations were detected in most was observed with increasing trophic samples of bivalves, C. glucaum (Table levels in fishes (Table 3, Fig 3). 1). Furthermore, the C. glucaum were shown to have the highest metal concentrations. Among the fish samples, however the highest mean concentration of Cu was found in S. 1032 Mirzajani et al., Metal bioaccumulation in representative organisms from different trophic …

Table 1: The biological characteristics and metal concentrations in different fishes and bivalve species collected from Anzali region (C m; number of samples for chemical analysis, F: female, M: male, U: undefined sex, D; percentage of detected sample numbers; the average metals concentrations have been calculated from detected data, minimum values (min) have been recorded from the minimum detected data). Weight Cd Co Cr Cu Mn Ni Zn Fe (g) Species C m Length Mean ± Sd Mean ± Sd Mean ± Sd Mean ± Sd Mean ± Sd Mean± Sd Mean ± Sd Mean ± Sd (mm) (Min-Max) (Min-Max) (Min-Max) (Min-Max) (Min-Max) (Min-Max) (Min-Max) (Min-Max) Age (y) D D D D D D D D Percidae 121- 549 0.77 ± 0.46 9.3 ± 7.76 0.77± 0.67 1.16 23.3 ± 7 7.12 ± 5.04 16 Sander 250-365 (0.36-1.47) (0.22-24.7) (0.01-0.59) (11.2-38.9) (2.1-14.6) (8F, 8M) lucioperca 2-3 38% 100% 88% 6% 100% 60%

2-1248 25 0.54 1.4 ± 0.34 0.22 ± 0.67 2.6 ± 3.8 0.81 26.8 ± 13.6 140.1 ± 198.2 65-500 Rutilus frisii (10F, 10M, (1.1-1.7) (0.12-2.55) (0.26-15.7) (11.2-69.7) (2.9-548.1) 1-6 5U) 3% 9% 30% 82% 3% 100% 90%

2.1-159 Alburnus 20 0.48 1.46 ± 1.97 3.2 ± 4.1 0.42 38.5 ± 30.4 80.9 ± 66.3 70-264 chalcoides (6F, 8M, (0.45-5.75) (0.25-14.3) (8.9-98.9) (21-178) 1-3 6U) 5% 70% 85% 5% 80% 94% 2.1-545 1.34 3.6 ± 11.0 3.2 ± 4.4 1.9 ± 0.6 27.5 ± 12.7 217 ± 171 Mugilidae Liza 16 68-372 (0.1-40.1) (0.4-12.7) (1.4-2.3) (11.7-51.2) (61-510) aurata (3F, M, 8U) 1-5 6% 50% 75% 15% 94% 94%

Cardidae Height= 1.44 ±0.38 1.08±0.42 8.94±5.52 Cerastoderma 14.8-22.4 13 0.54 (0.9-2.1) (0.44-1.62) (0.2-19.8) 14.8±8.5 15.5± 4.7 60.4±14.2 546.3± 430.1 glucaum - 85% 54% 100% (5.4-35.8) (10.4-24.9) (42.6-95.3) (96.2-1558) 2-11 8% 100% 92% 100% 100%

Table 2: The results of isotope analysis (C i: number of samples for isotope analysis, TLPC : trophic level based on primary consumer, TLPom: trophic level based on particulate organic matter, Averages with dissimilar letters (a, b, c) specify significant difference, F: statistic value, P: significant levels. Length classes C amount N amount C δ13C δ15N TL i (mm) (ug) (ug) PC Percidae <300 -19.97 ± 0.1 12.9 ± 0.2 Sander 9 300> -19.96 ± 1.6 12.2 ± 0.8 463.9 ± 183.1 130.5± 48.1 4.2 ± 0.24 lucioperca (F=0.01,P=0.99) (F=2.6,P=0.15) <260 -21.7 ± 0.7 8.9 ± 0.4a Cyprinidae 261-370 -20.4 ± 1.4 10.1± 0.9b 13 326.7 ± 220.7 88.7 ± 55.0 3.4 ± 0.27 Rutilus frisii 370> -21.6 ± 10.5 10.5 ± 0.2b (F=2.6,P=0.12) (F=7.4,P=0.01) <100 -24.2 ± 1.4a 8.6 ±1.9 Alburnus 101-200 -21.9 ± 1.1ab 10.6 ± 0.8 8 559.1 ± 330.6 128.5 ± 68.9 3.7 ± 0.50 chalcoides 201> -21.2 ± 0.2b 11.7 ± 1.0 (F=6.4,P=0.04) (F=4.3,P=0.08) <100 -20.1± 0.2 8.2 ± 0.1 Mugilidae Downloaded from jifro.ir at 9:20 +0330 on Sunday February 25th 2018 5 100> -18.5 ± 0.6 10.1 ± 1.3 404.3 ± 229.6 117.9 ± 71.2 3.3 ± 0.42 Liza aurata (F=6.3,P=0.14) (F=1.4,P=0.42) Height <17 -20.3 ± 0.4 4.5 ± 0.43 Cardidae (mm) 17-20 -21.3 ± 1.1 4.6 ± 1.6 TL Cerastoderma 9 267.8 ± 121 63.9 ± 32.5 Pom 20> -21.7 ± 1.0 5.0 ± 0.1 1.41± 0.21 glucaum (F=2.1,P=0.2) (F=0.4,P=0.69) 1033 Mirzajani et al., Metal bioaccumulationIranian Journal ofin Fisheriesrepresentative Sciences organisms 15(3) 2016 from different t rophic … 1033

Figure 1: Distribution of carbon and nitrogen stable isotope ratios among fishes and bivalves from southwest of the Caspian Sea.

Table 3: The Spearman correlation test for dependence of Ln metal concentrations on body size (length or weight) and trophic level (* significant level <0.05). Body Species Co Cr Cu Mn Ni Zn Fe size Sander lucioperca Body size -0.65* -0.05 -0.84* 0.97 TL -0.18 -0.03 0.12 -0.03 Rutilus frisii Body size 0.86 -0.65* -0.39 0 TL 0.72* -0.57 -0.48 -0.5

Alburnus chalcoides Body size -0.29 -0.54* -0.61* -0.6 TL 0.83* -0.8 -0.25 -0.64 -0.2 Liza aurata Body size 0.14 -0.5 -0.44 0.1 TL 0.67 0.6 -0.86 0.46 0.32 Body Cerastoderma glucaum height 0.11 -0.93* -0.19 -0.55 0.22 0.08 -0.63* TL 0.49 -0.11 0.4 0.5 -0.11 0.05 0.03 -038

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Figure 2: Regression between Ln metal concentration on height and trophic levels of bivalves (significant differences have been showed by lines). 1034 Mirzajani et al., Metal bioaccumulation in representative organisms from different trophic …

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Figure 3: Regression between Ln metal concentration on body length and trophic levels of fishes (significant differences slopes have been showed by lines; vertical lines in horizontal axis indicated the body size classes). Iranian Journal of Fisheries Sciences 15(3) 2016 1035

Table 4: Variations of metals concentrations in Liza aurata and Rutilus frisii in the Southern Caspian Sea as reported in previous investigations (*based on wet weight).

Species Cd Co Cr Cu Mn Ni Zn Fe References Liza aurata ND 0.43 Pazooki et al., 2009 0.04 0.12 Fallah et al., 2011* 0.02 Shahryari et al., 2010 0.02 1.3 3.4 Ardalan et al., 2012 0.03 0.08 Tabari et al., 2010 0.63 ND 10.85 `0.41 217.8 125.6 Varedi, 2011

Rutilus frisii 0.001 0.009 0.33 1.01 0.45 17.2 Anan et al., 2005 2.7 22.3 Foroughi Fard et al., 2008

ND 2.76 15.4 Monsefrad et al., 2012

0.17 0.52 Fallah et al., 2011*

0.11 Hoseini and Tahami, 2012

0.02 Shahryari et al., 2010

0.325 ND 1.68 0.78 2.65 0.63 5.6 Eslami et al., 2011*

0.04 0.06 Tabari et al., 2010

ND ND 0.013 ND 0.4 0.08 Varedi, 2011 ND : not detected

Discussion The study showed that the While only Cu concentration had the concentrations of Mn, Zn and Fe in highest concentrations in piscivorous S. Rutilus frisii and Liza aurata were lucioperca, no significant difference in higher than those reported in previous metals was observed in deposit feeder

Downloaded from jifro.ir at 9:20 +0330 on Sunday February 25th 2018 studies (except Cu level; Tables 1 and L. aurata and benthivorous (R. frisii 4). It might be related to temporal rise and A. chalcoides) (Table 1). According of the Caspian pollutants. According to to Goodyear and McNeill (1999) the Karpinsky (1992) the concentrations of took up Zn in direct proportion metals in sediments of the Caspian Sea to levels found in sediments while Cu have shown high temporal increases. had similar uptake rates from the water There are a few investigations showing and sediment. Therefore the high variations in pollutant concentrations in concentration of Cu in S. lucioperca the southern Caspian Sea. Among them, might be related to its different feeding several authors have reported high habits. variations in metals concentrations of water and substrate (Laloei, 2001; Parizanganeh et al., 2007; Hashemian kafshgari, 2008; Sohrabi et al., 2010).

1036 Mirzajani et al., Metal bioaccumulation in representative organisms from different trophic …

The low concentration of Cr and Cd, of δ13C values were observed in A. similar to what found in previous chalcoides (Fig. 1). Hobson et al. studies (Tables 1 and 4), might be (2002) reported that the high variation related to their concentrations in in δ13C of benthivorous species might sediments. The local sources might be be related to the broad range of δ13C in responsible for metal pollution in the benthic compared to pelagic organisms. Caspian Sea. Similarly, Anan et al. A higher δ13C value observed in L. (2005) found higher concentrations of aurata (Fig. 1) also might be due to Co, Cd in fishes from our study area their diet that mostly contains the than that found in other parts of the substrate invertebrates and the Caspian. Also higher concentrations of meiofauna (Ghadirnejad, 1996). metals such as Cd were observed in the The significant slopes of metals central and southern part of the Caspian concentrations, the fish size and the Sea than those in the northern sector (de TLs showed that the metals do not Mora et al., 2004) because of their rich bioaccumulate, but possibly biodilute natural background resource. by fish size and the TLs (Table 3, Fig. In our investigated species, the 2). Similarly, correlation between δ15N depleted and enriched δ15N values can and metals concentrations in fishes was be due to their diets; i.e. deposit feeders not observed in other investigations and piscivorous, respectively (Table 1, (Campbell et al., 2005; Asante et al., Fig. 1). A. chalcoides has been known 2008; Ikemoto et al., 2008; Zhang and as a zooplankton feeder (Abbasi et al., Wang, 2012). 2004) but its mean TL value is A significant positive correlation relatively higher than benthivorous between TLs and fish size was only species R. frisii (Table 2). observed in Cyprinid species (Table 3).

Downloaded from jifro.ir at 9:20 +0330 on Sunday February 25th 2018 Comparatively, R. frisii seems to have It is probably related to change or longer-distance movements and variety of feeding habits for different probably feeds on depleted δ15N sizes; while the Percidae and Mugilidae sources; while A. chalcoides exists in samples are known as piscivorous and inshore littoral areas where the deposit feeders, respectively. Atherin eutrophication and subsequently the and kilka followed by Mugilidae were trophic base line is higher than offshore found to be the main food items of S. regions. The δ15N values of primary lucioperca (Abbasi et al., 2004). consumers and other organisms in According to Vinagre et al. (2011), coastal areas would be increased after there was no correlation between the eutrophication and upward N loading Carbon and Nitrogen stable isotopes of phenomena (Cabana and Rasmussen, muscles and body size. It seems, there 1996; Martinetto et al., 2006). Asante et is a large range between δ13C and δ15N al. (2008) also found the higher δ15N in values in fish particularly A. chalcoides fishes from shallow water rather than (Fig. 1) due to different food items size. deep water. Furthermore, a broad range The findings showed, the δ13C value in Iranian Journal of Fisheries Sciences 15(3) 2016 1037

the small size of A. chalcoides was et al., 2005; Pourang et al., 2005; significantly lower than in big sizes of Pazooki et al., 2009). The relationships the fish (F=6.4; p<0.05; Table 1). The between metals concentrations in the small size of A. chalcoides might feed muscle and length have been widely on the micro-zooplankton while the big documented by several investigators. size of this fish feed on the crustacean Some contradictory results have been and macro-planktons (Abbasi et al., discussed for fishes in the world by 2004). Pourang et al. (2005). Growth (body The low significant δ15N (F=7.3; weight, length and age) dependent p<0.05; Table 1) in the small size decreases in metals concentrations have groups of R. frisii as compared with the been reported for many fish species big size groups could be related to particularly for Zn, Cu, Cd and Mn in variations in their diets. Additionally, muscle tissues (Anan et al., 2005). Zarinkamar (1996), Abdolmaleki et al. Significant negative correlations were (2009) and Afraei Bandepei et al. found for Co, Zn, Cu in Rutilus (2009) noted that the big size groups of caspicus (Anan et al., 2005). While R. frissi feed on bivalves, while the diet Hoseini and Tahami (2012) found a of small size groups was crustacean in significant relationship between Cd the Caspian Sea. concentrations in muscle and R. frisii Although there were a strong size, no significant relationship was relationship between TLs and body size observed for Cu and Zn concentrations in Cyprinid species (Table 3), there by Foroughi Fard et al. (2008). Pourang were no significant slopes between TLs et al. (2005) did not observe any age and the Ln concentrations of metals related differences in metal (Fig. 2). concentrations in different species; and

Downloaded from jifro.ir at 9:20 +0330 on Sunday February 25th 2018 A significant negative relationship only the concentration of cadmium had was found between the concentrations a negative relationship with weight of of Zn vs. body size for most fish the samples (p=0.038). A significant species (Table 3). However, in the positive relationship was found between biomagnification of Zn documented in bioaccumulation factors and fish age in a few investigations on food web Liza saliens (Fernandes et al., 2007). (Quinn et al., 2003; Campbell et al., Various environmental and 2005), there was also a significant biological factors, nourishment source negative correlation observed between and seasonal changes affect the δ15N and Zn concentration (Yoshinaga differences in metal bioaccumulation et al., 1992). (Agusa et al., 2004; Wang and The negative relationship between Rainbow, 2008). The findings showed, body size and metal concentration in there was no bioaccumulation of metals muscle (Table 3) has been previously in S. lucioperca, A. chalcoides and reported in many Caspian fishes (Anan L. aurata, so no significant differences 1038 Mirzajani et al., Metal bioaccumulation in representative organisms from different trophic …

were observed between δ15N, TLs and M. Farhadinia for their help to do the the fish sizes. laboratory work. The metabolic rate and dilution of metal during growth period can be References responsible for this relationship; as Abbasi, K., Sabkara, J., Rahimi, R. smaller fish have higher metabolic rates and Mahisefat, F., 2004. Feeding and are able to accumulate metals, via studies of Caspain fishes in southern food and water, more rapidly than Caspian Sea. Inland Water larger fish (Anan et al., 2005). The R. Auaculture Research Center, Bandar frisii had a significant difference in Anzali, 4P. δ15N among their different body sizes Abdolmalaki, S., Kor, D. and which could be related to difference in Bandani, G., 2009. Stock metal concentration in their food diet. assessment of the bony fishes in The mean metals concentrations in Iranian coastal waters of the Caspian muscles were lower than the Sea (2005-2007). Iranian Fisheries provisional tolerable Research Organisation, Inland daily/weekly/monthly intake of the Waters Aquaculture Research metals, as established by the United Center, 158P. States Environmental Protection Abdolmaleki, S. and Ghaninezhad, Agency, European Food Safety D., 2007. Stock assessment of the Authority, Ministry of Agriculture Caspian Kutum Rutilus frisii Kutum Fisheries and Food, and the in the Iranian coastal waters of FAO/WHO (the values presented by Caspian Sea. Iranian Journal of Fallah et al.(2011), Zhang and Wang Fisheries Science, 16(1), 103-114. (2012), Mashroofeh et al. (2013)). Afraei Bandepei, M., Mashhor, M., Downloaded from jifro.ir at 9:20 +0330 on Sunday February 25th 2018 The metals concentrations in the Abdolmalaki, S. and El-Sayed, muscles of fishes were lower than those M.A.F., 2009. Food and feeding reported in the previous studies. These habits of the Caspian kutum, Rutilus concentrations could not pose any frisii kutum (Cyprinidae) in Iranian threat to human health. In addition, no waters of the Caspian Sea. Cybium, bioaccumulation was observed for 33, 193-198. metals in different trophic levels of R. Agusa, T., Kunito, T., Tanabe, S., frisii in the Caspian Sea. It is suggested Pourkazemi, M. and Aubrey, that monitoring of metals in aquatic D.G., 2004. Concentrations of trace organisms and the Caspian environment elements in muscle of sturgeons in should be performed to further discover the Caspian Sea. Marine Pollution those trends. Bulletin, 49, 789-800. Acknowledgments Anan, Y., Kunito, T., Tanabe, S., We wish to thank J. Hassan, N. Mitrofanov, I.and Aubrey, D.G., Pourang, H. Babaei, J. Matthews and 2005. Trace element accumulation in Iranian Journal of Fisheries Sciences 15(3) 2016 1039

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