Persian Gulf is chronically exposed to oil pollution associated with exploration, exploitation, refining, and routine handling of oil. War related pollution has recently been added to this list. Frequent mass mortality of corals in this area is attributed to a combination of extreme water temperatures and high sedimentation/turbidity. The brown algae have been reported to have been most harshly affected by pollution. Reduction in algae population due to pollution is suggested to threaten food chain integrity in the area (Buo-Olayan and Subrahmanyam 1996). Worldwide, the use of algae (including Ulva, Sargassum, Padina, and Cystoseira) in biomonitoring, has been well established. Metal content and accumulation in seaweed and sediment are recognized as a suitable bioindicator for assessing the degree of contamination in marine ecosystems. However, since sediment composition varies according to particle size, rate of deposition, rate of particle sedimentation, and presence and amount of organic matter direct measurement of metal in the sediment is often misleading when it comes to assessing the risks that metals pose to the local ecosystems. Bioavailability of metal contaminants to local ecosystems can be better evaluated by calculating the Biosediment accumulation factor (BSAF = Cx/Cs, where Cx and Cs are the mean concentrations of metals in a biological organism and in associated sediment). We selected Acanthophora, Gracilaria, and Sargassum because they are common in the area and although in Iran algae is not used as food, but algae is cultivated and used in production of food ingredients, and manufacturing of drugs and health products.

We selected Ni, Cd, Cu, and Pb because they are petroleum related. Gondal et al. (2006) reported on elemental analysis of Arabian crude oil residue samples which included Cu, and Ni. Lead is also found in petroleum and it originates from tetraethylic lead. Lead and cadmium are found in petroleum and have been reported on by Al-Swaidan (1994). These metals are also listed in the Dangerous Substances Directive (76/464/EEC) and its annex (a list of substances originally published by the European Economic Community in 1976), as substances that pose particular concern in aquatic environments, due to their high production volume, environmental persistence, and bioaccumulation properties. Our objective was to measure Ni, Cd, Cu, and Pb in seven common seaweed species (green: Ulva interstinalis, brown: Padina pavonica, Cystoseira myrica, Sargassum angustifolium, and red: Acanthophora spicifera, Gracilaria corticata, Hypnea cervicornis), and associated sediment from six sites in Bushehr Province (Fig. 1). Seaweed from these areas is used in local food industry, drug manufacturing, and health products in Iran. We wanted to: (1) measure metal levels in seaweed and associated sediment form sites that are important in seaweed harvest (Olee, Taheri, and Haleh); and areas close to sources of pollution (Ganaveh, University of Bushehr, and Nuclear power facilities), (2) find which species of algae is a better bioindicator of metals by evaluating correlations between sediment and algae metal.

Fig. 1
figure 1

Numbers (1–6) indicate sampling sites; circles indicate location of industrial facilities: Ganaveh Port (1), University of Bushehr (2), Nuclear power facilities (3), Village of Olee (4), Taheri port (5), and Village of Haleh (6)

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Materials and Methods

The studied sites are areas of importance in seaweed harvest (Olee, Taheri, and Haleh) and areas close to sources of anthropogenic pollution (Ganaveh, University of Bushehr, and Nuclear power facilities). Samples were collected in October 2008 and January, May, and July 2009. Locations of sampling sites were recorded using a global positioning system (GPS): (#1) Ganaveh Port (29°39′N, 50°24′E), (#2) University of Bushehr (28°54′N, 50°49′E), (#3) Bushehr Nuclear Power Facilities (28°50′N, 50°52′E), (#4) Village of Olee (27°49′N, 51°55′E), (#5) Taheri Port (27°40′N, 52°20′E), and (#6) Haleh village (27°24′N, 52°38′E) (Fig. 1).

Seven species of seaweeds were sampled (0.5–1 kg) at low tide, in the intertidal zone at the depth of ≤1 m. Five–8 cm from the tip of the algae was removed. At the same spots, surface sediment (top 5 cm) was collected (n = 3). Seaweed was rinsed with DDW, oven dried (at 105°C for 48 h) to constant weigh then crushed, homogenized, and stored in sterile bottles. Samples (1–2 g) were digested and refrigerated until analysis. For digestion (12 h on a hot plate at 140°C), samples were placed in sealed flasks with 10 mL HNO3/HCl (1:3 v/v) to prevent sample loss. Digests were filtered through acid-cleaned 0.45 mm filters, diluted to 25 mL with DDW and stored at 4°C for analysis. Sediment samples were made into a fine powder, sieved using a 63 μm nylon mesh, and the <63 μm size fraction was used for digestion. Metal determination was done by a flame atomic absorption spectrophotometer. The instrument was calibrated based on a linear six-point calibration curve for Ni and Pb (0.5, 1, 10, 50 and 100 mg L−1); and for Cu, and Cd (0.1, 0.5, 1, 10 and 50 mg L−1). Standard calibration curves for Ni and Cd (with r 2 = 0.99), and Cu (r 2 = 0.99), and Pb (r 2 = 0.97) were generated. Blanks were run with each batch of samples (ten samples in each batch) and run similarly. The flame composition was acetylene 2.0 and air 13.5 (L/min). The nebulizer aspiration flow rate was kept between 5.5 and 6.0 mL/min. Detection limits in the sample tests were: Ni (0.05 μg g−1), Cd (0.02 μg g−1), Cu (1 μg g−1) for and Pb (2 μg g−1). All statistical analyses were performed by SPSS version 12. Analytical precision gave a mean error of 5 %. Mean values of three replicates were calculated. All data were tested for normality and homogeneity of variance before the parametric statistical analysis. Variability between seasons and sampling sites was analyzed for each metal by one-way ANOVA. To detect differences between individual means, we used Tukey’s Multiple Comparison test. The relationships between heavy metal’s concentrations in the sediments and macroalgal species were evaluated by simple correlation coefficients (p was set at ≤0.05).

Results and Discussion

Table 1 indicates the range of values for trace metal concentrations (μg/g) which previous investigators have deemed “unpolluted” sediment in this area. Cd in our sediment samples is higher than these areas, while sediment Cu is in the lower ranges of values reported for unpolluted areas. Nickel is in the medium range, and Pb appears similar to other unpolluted areas. The high levels of metals in seaweeds reflect the high bioavailability of metals in these waters and the capacity of the seaweed to accumulate heavy metals.

Table 1 Range of values for trace metal concentrations (μg/g) in unpolluted marine sediments of different areas in the Persian Gulf
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Figures 2 and 3 show Ni, Cd, Cu and Pb levels we found in sediment and seaweed. We evaluated the efficiency of metal bioaccumulation in the seven species of seaweed by calculating their respective BSAF (Table 2), which is defined as the ratio between the metal concentration in the organism and that in the associated sediment (Szefer et al. 1999). The highest BSAF was obtained for Cu in A. spicifera. The lowest BSAF value was for Pb and Ni, which may be explained by higher levels of these metals in the sediment. Average BSAFs for Pb and Ni was significantly <1; a comparison between BSAFs of Cd and Cu with that of Pb and Ni indicates that, with the exception of Enteromorpha intestinalis and C. myrica, capacity of seaweed for bioaccumulation of ingestible Pb and Ni is low considering the high levels we have observed in the sediment. A strong correlation between metal levels in the sediment and the seaweed indicates that metal in the sediment may easily become available to the seaweed. Table 3 indicates correlations and suggests that both Ni, Cd, can best be monitored in H. cervicornis, while Cu and Pb bio monitoring is beset done in G. corticata and P. pavonica.

Fig. 2
figure 2

Seaweed concentrations of Ni, Cd, Cu and Pb collected from the coastal area of the Bushehr Province in Iran. Error bars indicate the mean of three replicate samples (n = 3) ± SEM (μg g−1 dry weight). *Significant at p ≤ 0.05; **significant at p ≤ 0.01; and ***significant at p ≤ 0.001

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Fig. 3
figure 3

Sediment concentrations of Ni, Cd, Cu and Pb from the Iranian coast of Bushehr Province. Error bars indicate the mean of three replicate samples (n = 3) ± SEM (μg g−1 dry weight). *Significant at p ≤ 0.05; **significant at p ≤ 0.01; and ***significant at p ≤ 0.001

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Table 2 Mean BSAF from Bushehr Province on the coast of the Persian Gulf, Iran
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Table 3 Significant correlations between metal concentrations in sediment and seven local species of seaweed from Bushehr Province on the coast of the Persian Gulf, Iran
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Ganaveh is closest to the most heavily industrialized areas of the Gulf. Nickel in U. interstinalis is higher than those found in Kuwaiti Coast but lower than Saudi Coast, in the same algae (Table 4). Elevated Ni maybe attributed to oil pollution (Al-Homaidan 2008) and Ni in rock formations. we compared metals between algae species to detect interspecific differences. Maximum concentrations of Ni, Cd, Cu and Pb were found in U. intestinalis, P. pavonica, A. spicifera, and C. myrica respectively. G. corticata had least Ni, S. angustifolium contained lowest Cd, Pb, and Cu. Nickel was significantly lower in S. angustifolium and G. corticata when compared to C. myrica (p < 0.05; Fig. 2). Cadmium in algae >2 μg g−1 have been coined for polluted environments (Lozano et al. 2003). Domestic sewage and Cd in rock formations have been suggested as the source of Cd pollution. Further, galvanized steel use in the Assaloyeh oil and gas facilities contain cadmium coating which can end up in these waters. Copper contamination is associated with algal levels of >20.00 μg g−1. Lozano et al. (2003), coins Pb values >10 μg g−1 to algal species from contaminated areas. High levels of Pb in alga of the area can be attributed to combustion of fossil fuels and oil pollution. Collectively, our data and others suggest that the seaweed of the Persian Gulf has been severely affected by metal contamination. The scope of research in the Gulf is currently limited to biomonitoring of sediment, fish, and economically valued invertebrates but, we plan to expand research to conservation, remediation and clean-up work in order to restore these fragile ecosystems to a stable condition. To reverse the current destructive trends, immediate rehabilitation measures must be undertaken to protect the area for the future generation (Table 5).

Table 4 Ulva (green seaweed), Padina, Sargassum, and Cystoseira (brown seaweed), and Gracilaria, Hypnea and Acanthophora (red seaweed) metal concentrations (μg g−1 dry weight) from various geographical locations
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Table 5 Physical and environmental characteristics of sampling sites (values are in mean ± SEM) with associated pollution sources and highest and lowest metal levels in sediment and algae from the Bushehr Province of Iran in the Persian Gulf
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