Assessment of biosorption and transfer of heavy metals (chromium and copper) by Microalgae (Arthrospira platensis), Amphipoda (Pontogammarus maeoticus), and Beluga fish of Caspian Sea (Huso huso)

doi:10.21203/rs.3.rs-4380678/v1

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Assessment of biosorption and transfer of heavy metals (chromium and copper) by Microalgae (Arthrospira platensis), Amphipoda (Pontogammarus maeoticus), and Beluga fish of Caspian Sea (Huso huso)

https://doi.org/10.21203/rs.3.rs-4380678/v1

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The Caspian Sea is an environment from the entry of river waters with various pollutants including heavy metals. The absorption or accumulation of metals by the organisms of an ecosystem will have a different effect on their food chain. This research aims is to compare the amount of heavy metal absorption of copper and chromium in algae, Gammarus and fish. The working method included preparation and digestion stage of the samples to read them by atomic absorption spectroscopy (AAS).

In this research, Algae had a better efficiency in chromium absorption at the initial time. On the contrary, Gammarus had a better efficiency in copper absorption and the absorption process increased with time. In direct competition, metal absorption by algae was better than Gammarus. The accumulation of heavy metals in liver was more than in muscle. In body tissue, copper accumulated more than chromium. Among the adsorbent samples, the highest metal absorption by algae and metal accumulation by Gammarus observed in fish body tissues.

The result of this research, Algae is a strong absorber of metal from the environment and repels metal from the fish body. On the other hand, Gammarus absorbs metal from the environment and transports metal to the fish body.

biosorption

Heavy metals

Spirulina microalgae (Arthrospira platensis)

Gammarus Amphipoda (Pontogammarus maeoticus)

Beluga fish (Huso huso)

The Caspian Sea has a large amount of metal from sewage due to being closed and supplying most of the incoming water from rivers. With the rapid development of industries, especially in developing countries, heavy metal wastes are discharged directly or indirectly into the environment. Organic and mineral materials are discharged into the environment due to domestic, agricultural, and industrial activities and finally turn into organic and mineral pollutants (Abdel-Raouf et al., 2012). Unlike organic pollutants, heavy metals are not degradable but tend to accumulate in organisms. Therefore, wastewaters combine with inorganic nitrogen and phosphorus due to resistance and the presence of heavy metals, and cause damage to the food chain (Souza et al., 2012).

Copper is an essential element for all organisms because the lack of this mineral can cause enzyme dysfunction. However, the same metal is toxic to fish in high concentrations in water (Pickering and Henderson, 1966). The importance of testing copper metal because it is essential for organisms and extensive agricultural activity due to pesticides, as well as the entry of detergents from urban sewage into the southern part of the Caspian Sea.

Chromium metal exists in several oxidation states in the environment and usually appears as trivalent and hexavalent (Ghosh and Singh, 2005). Hexavalent chromium is toxic to all plants and animals, highly carcinogenic, and has high solubility and accessibility in water and soil (Goyer and Clarkson, 2001). The importance of chromium metal testing is due to the discharge of chrome metal wastewater into this water basin by a factory near the Tajen River.

Bioremediation used by natural mechanisms, including microorganisms and plants, to remove dangerous pollutants (Sibi, 2019). Biosorption has particular importance due to its contribution to the environment and its excellent performance in removing heavy metals (Wang et al., 2006). The essential advantages of this method can attributed to its effectiveness in reducing the concentration of metal ions to shallow levels, beneficial live microorganisms, simple technology, nutrient recycling, adsorbent regeneration capability, no production of sludge, the possibility of metal recycling and the use of cheap absorbent materials such as natural algae (de la Noüe and Proulx, 1988; Herrero et al., 2006).In biosorption efficiency, several factors are influential, such as the initial concentration of metal ions, contact time, pH, temperature, the concentration of the biological absorbent, the rate of turbulence, and the competition of ions (Salam, 2019).

Spirulina microalga species (Arthrospira platensis) used in food industry and bioabsorption of heavy metals in wastewater. In recent years, algae have used to assess ecological risks and effects of heavy metals, herbicides, and other pollutants in aquatic systems for sensitivity to metal pollutants (Levy et al., 2007; Qian et al., 2008). In other words, algae can provide suitable places for connection metals due to having polysaccharides, protein, and fat on the surface of their cell walls, which have functional groups such as amine, hydroxyl, carboxyl, and sulfate (Rajfur et al. ., 2011). Therefore, algae have always been of interest due to their high absorption capacity and availability in almost unlimited amounts (Klimmek et al., 2001). It should mention that the effect type of heavy metals in different concentrations is diverse on the biological and biochemical properties of microscopic algae (Soeder et al., 1978).

The absorption of heavy metals in the body of Creatures is mostly through receive of metals in food and water in the form of suspended or dissolved. Excessive absorption of essential and unnecessary metals accumulates in different tissues (Canli and Atli, 2003). Micro-benthic species (Pontogammarus maeoticus) is crustaceans and one of the most abundant amphipods with wide distribution and high density at the edge of the Caspian Sea. There are more than 100 freshwater, brackish, and marine species in the Northern Hemisphere. They are ecologically significant in the Caspian Sea because they fed by many economically valuable fish, including sturgeons, kutum, mullet, perch, kilka, and carp. Also, these animals transfer pollutants to the food chain through contact with water, seafloor sediments, and the consumption of phytoplanktons and zooplanktons containing heavy metals (Ghareyazie and Mottaghi, 2012). Due to their wide distribution, importance in the food web, and sensitivity to a wide range of pollutants, they are essential bioindicators for water quality assessment (Gerhardt et al., 2011).

In fish, heavy metals in food absorbed by the digestive system, and heavy metals in water absorbed by the gills. At the end of the absorption process, heavy metals usually accumulate in liver and muscle tissue (Rajeshkumar and Li, 2018). High concentrations of metals cause changes in the biological activities of fish (Canli and Atli, 2003). Humans can cause serious health problems by consuming metal-contaminated fish (Kamaruzzaman et al., 2011). The dangerous effect of metals on fish at the top of the food pyramid is more than terrestrial vertebrates (Kousar and Javed, 2014). Beluga fish (Huso huso) are among the predatory and carnivorous creatures of the Caspian Sea. They feed on the creatures around them in different life stages depending on the place and location. They usually feed on benthic invertebrates, insects, and crustaceans at a young age. They feed on small and large fish in their habitat, including big-scale sand smelt (Atherina boyeri), kutum (Rutilus rutilus), and so forth in old age. Beluga fish is on the Red List of the International Union for Conservation of Nature (IUCN) and is currently in the status of critically endangered (CR) species (Gessner et al., 2022).

Bioaccumulation of heavy metals by organisms may be passive or selective. When the excretory, metabolic, Storage, and detoxification mechanisms cannot resist absorption, the toxic effects of these substances become visible. These effects ultimately lead to physiological and histological changes (Jia et al., 2017). Therefore, researchers believe that the transfer of heavy metals from the lower to the upper levels of the food chain causes danger in the ecosystem because these substances tend to accumulate and transferred from one to another food chain (Martin and Griswold, 2009).

The purpose of this research is to compare and influence the amount of Gammarus macrobenthos (P. maeoticus) and spirulina microalgae (A. platensis) in the maximum concentration of biosorption and also the final lethality limit of heavy metals chromium and copper. At the end of this stage was the process and amount of heavy metals absorbed in the diet of beluga fish (H. huso) at the top of the food pyramid of the Caspian Sea.

Preparation

In the spirulina algae experiment, pre-cultivated algae in the number of treatments placed inside the Erlens containing heavy metals chromium and copper (1 ml/L^− 1) with proper aeration and light (Budi et al., 2020). Algal biomass removed using a 5 micron (µm) net during periods of zero (less than one hour), 24 and 48 hours. Algae samples removed to complete the preparation stage of the experiment dried and finally powdered in an oven at 50°C for 24 hours. For accurate and reliable calculation of the experiment, the water sample separated from the algae fixed with nitric acid (1.5 ml per liter) to calculate the amount of remaining or unabsorbed metal (Moopam, 1999).

Gammarus specimens were caught in the Tejn River estuary into the Caspian Sea with 1 mm net and kept in an aquarium under laboratory conditions. To start the Gammarus experiment, the amount of Gammarus calculated according to the number of treatments based on the heavy metals chromium and copper (1 ml/L^− 1) was inside Erlen. Gammarus removed during periods of zero (less than one hour), 24 and 48 hours, and dried and powdered in an oven at 50°C for 48 hours to complete the experiment preparation stage. Similar to the previous experiment, the water sample isolated from Gammarus fixed with nitric acid (1.5 ml per liter) for the accuracy of the experiment (Moopam, 1999).

In the co-cultivation experiment, similar to the previous two methods were performed, with the difference that algae and Gammarus samples placed in direct competition and with a typical tank, separated by the type of metal and periods (Moopam, 1999).

In the beluga fish experiment, heavy metals chromium and copper with a ratio of one milliliter of metal in one liter of water (mg/L^− 1) were separately absorbed and finally dried by adsorbents. Powdered adsorbent samples introduced, including algae (treatment 1), Gammarus (treatment 2), co-culture of algae with Gammarus (treatment 3), and control or food containing two metals, chromium and copper (treatment 4) to this stage. Each of the treatments mixed with fish food at a ratio of 3 grams per kilogram. For treatment 4, One milligram of metal added per kilogram of fish food. After two months of feeding based on fish body weight, 10 pieces of fish with an approximate weight of 100 grams from each pool transferred to the research institute with dry ice and kept at -20°C until the experiment. At the end of this stage, the liver and muscle tissues of the fish separated, and their wet weight measured with a digital scale (AND, Japan); then the samples transferred to a freeze dryer (Christ, Germany) for drying. At the end of this stage, muscle tissue samples crushed using an electric shredder (Moulinex, France), and liver tissue samples powdered using a mortar (Moopam, 1999).

Digestion

In this stage of the experiment, the powdered samples of algae, Gammarus, and the liver and muscle tissue of beluga fish placed separately in the amount of 0.3 grams of each sample into the laboratory tubes. Then, 4 ml of nitric acid 65% added to each of the samples, and the digestion process performed for one hour. In the following, laboratory tubes for 3 hours placed into the digestion device (Header Digest) at 90°C to final digestion. Finally, the cooled samples were put into a 50 ml volumetric flask with Whatman filter paper and made up to volume with distilled water (Moopam, 1999). In algae and Gammarus of the experiment, 100 ml of water samples passed through filter paper, and then initial digestion done with 5 ml of 65% nitric acid. The samples transferred to a water bath with a temperature of 100°C for final digestion. After 7 hours, the water samples brought to the required volume of 15 ml. Each sample filled with distilled water in a 100 ml volumetric flask (Moopam, 1999).

Numerical and statistical calculations

The device for evaluating the amount of absorption of heavy metals in the samples carried out by an atomic absorption spectrometer (Solaar.M5, Thermo Electron Company, America) in both flame and furnace methods (Crump, 1993; Parsons, 2013). After the samples prepared, they transferred to the atomic absorption laboratory to read the amount of metal absorption. The amount of metal absorption observed for algae and Gammarus by flame method (mg/kg) and for body tissue by graphite furnace method (µg/kg).

C_i= number of the device, V = final volume of the sample (50 ml), m = dry weight of the sample (0.3 or 0.1 grams), C_r= final number

C_r = C_i×V/m

SPSS 19 software used to analyze the data results, and the statistical tests used included a t-test, one-way analysis of variance, and Tukey's test (ANOVA). A significant difference determined with a confidence level of 95% and a p number.

Spirulina algae (type of metal and time)

Chromium metal absorption was more than copper by algae. Statistically, a significant difference observed in the absorption of algae between the heavy metals copper and chromium (P < 0.01) (Table 1).

In the comparison between time intervals, the highest absorption of copper metal by algae seen in 24 hours; it showed a downward trend over time. The highest absorption of chromium metal seen in 48 hours; it showed an upward trend over time. Nevertheless statistically, no difference observed in the absorption of two metals, copper and chromium, by algae (P > 0.05) (Table 1).

Gammarus (type of metal and time)

In the comparison between heavy metals, the biosorption of copper (Cu) metal was more than that of chromium (Cr) by Gammarus. Statistically, a significant difference observed in the biosorption of Gammarus between heavy metals copper and chromium (P < 0.01) (Table 1).

In the comparison between the periods, the highest absorption of copper and chromium metal by Gammarus seen in 48 hours; it showed an upward trend over time. Statistically, a difference observed in the comparison between periods for the absorption of copper and chromium by Gammarus (P < 0.05) (Table 1).

Table 1

Comparison of periods by absorbents in algae and Gammarus culture (mg/L^− 1)
Gammarus		Algae		Time
Cr	Cu	Cr	Cu	Time
0.117 ± 0.004^a	0.203 ± 0.003^a	0.601 ± 0.02^a	0.365 ± 0.06^a	0
0.398 ± 0.1^ab	0.541 ± 0.09^b	0.791 ± 0.21^a	0.582 ± 0.13^a	24
0.462 ± 0.09^b	0.613 ± 0.07^b	0.836 ± 0.12^a	0.501 ± 0.06^a	48
0.325 ± 0.17	0.452 ± 0.2	0.742 ± 0.15	0.483 ± 0.12	Total

Lowercase letters on each column indicate significant differences between the data.

Co-cultivation (algae and Gammarus)

Metal type

In general comparison, chromium absorption observed more than copper metal. Statistically, a significant difference observed in the absorption of heavy metals between heavy metals (P < 0.05) (Table 2). In the comparison of algae absorption between heavy metals, the absorption of chromium (Cr) seen more than copper metal (Cu). Statistically, a significant difference observed in the absorption of heavy metals by algae (P < 0.05). In comparing the absorption of Gammarus between heavy metals, the absorption of copper (Cu) was relatively higher than that of chromium metal (Cr). Nevertheless statistically, no difference observed in the absorption of heavy metals by Gammarus (P > 0.05) (Table 2).

The highest initial absorption of copper (Cu) and chromium (Cr) metal was in zero hours (under one hour). In this time statistically, significant difference seen between the two metals (P < 0.01). The maximum copper and chromium metal absorption observed in 24 hours. In this time, there was no statistically significant difference between the two metals (P > 0.05). The downward course of absorption of copper and chromium metal, mainly algae, was in 48 hours. In this time, there was no statistically significant difference between the two metals (P > 0.05) (Table 2).

Absorbents

In the general comparison of the biosorption of heavy metals between the adsorbents, the absorption of algae was more than that of Gammarus. Statistically, a significant difference observed between algae and Gammarus (P < 0.01) (Table 2).

The maximum absorption of heavy metals between the adsorbents was to algae at zero (under one hour) and 24 hours. Statistically, a significant difference observed between Gammarus and algae in both periods (P < 0.01). The relative superiority of metal absorption by algae was in the period of 48 hours. Statistically, no significant difference observed between Gammarus and algae (P > 0.05) (Table 2).

The separate comparison of copper (Cu) and chromium (Cr) metal absorption between adsorbents showed absorption algae more than Gammarus. Statistically, there was a significant difference in metal absorption between algae and Gammarus (P < 0.01) (Table 2).

Periods

In general comparison, the highest absorption of heavy metals was at the initial time. It showed the maximum absorption of metal in 24 hours by algae and its continuation up to 48 hours by Gammarus. Statistically, there was no significant difference in the absorption of heavy metals between periods (P > 0.05) (Table 2).

The maximum absorption of heavy metals by Gammarus was in 48 hours. Statistically, it showed a significant difference in the absorption of heavy metals by Gammarus between periods (P < 0.01). The maximum absorption of heavy metals by algae was in 24 hours. Statistically, there was no significant difference in the absorption of heavy metals by algae between periods (P > 0.05) (Table 2).

In the separate comparison of copper and chromium metal between time intervals, the maximum initial absorption observed in less than one hour, and its final limit in 24 hours. Statistically, there was no significant difference in heavy metals between periods (P > 0.05) (Table 2).

Table 2

Comparison of time periods based on heavy metals and adsorbents in co-cultivation (mg/L^− 1)
Cr		Cu		Time
Gammarus	Algae	Gammarus	Algae	Time
0.1 ± 0.02^a	0.51 ± 0.01^a	0.1 ± 0.018^a	0.3 ± 0.012^a	0
0.25 ± 0.08^ab	0.53 ± 0.07^a	0.2 ± 0.03^b	0.51 ± 0.002^b	24
0.32 ± 0.07^b	0.45 ± 0.01^a	0.3 ± 0.017^c	0.35 ± 0.03^a	48
0.23 ± 0.11	0.5 ± 0.07	0.2 ± 0.09	0.39 ± 0.1	Total

Lowercase letters on each column indicate significant differences between the data.

Beluga fish

Absorbent (treatments)

In general comparison, Gammarus had the highest and algae had the lowest accumulation of heavy metals shown in fish tissue. Statistically, there was no significant difference between absorbent samples in the amount of heavy metals and fish tissues (P > 0.05) (Table 3). Algae had the highest absorption, and Gammarus had the highest accumulation of heavy metals among absorbent samples in liver and muscle tissue. Statistically, there was no significant difference between absorbent samples in fish tissues (P < 0.05) (Table 3).

Algae had the highest absorption, and Gammarus had the highest concentration of heavy metals among the adsorbent samples in copper, and chromium metals. Statistically, no significant difference observed between absorbent samples in both metals (P < 0.05) (Table 3).

Table 3

Comparison of treatments based on heavy metals and fish tissues (mg/L^− 1)
Liver		Muscle		Treatments
Cr	Cu	Cr	Cu	Treatments
0.0039 ± 0.0003^a	0.054 ± 0.01^a	0.0004 ± 0.00007^a	0.004 ± 0.001^a	Algae
0.011 ± 0.0007^a	0.305 ± 0.007^c	0.002 ± 0.001^a	0.024 ± 0.004^b	Gammarus
0.006 ± 0.002^a	0.161 ± 0.03^b	0.0013 ± 0.0001^a	0.011 ± 0.002^ab	Co-culture
0.0073 ± 0.003^a	0.163 ± 0.004^b	0.0013 ± 0.0001^a	0.013 ± 0.004^ab	Control
0.0071 ± 0.003	0.171 ± 0.09	0.0014 ± 0.001	0.013 ± 0.008	Total

Lowercase letters on each column indicate significant differences between the data.

Fish tissues

In general comparison, the amount of accumulation of heavy metals was in the liver more than in muscle tissue. Statistically, there was a significant difference between fish tissues in the accumulation of heavy metals (P < 0.01) (Table 3).

The accumulation of heavy metals for copper and chromium was in the liver more than in muscle tissue. Statistically, there was a significant difference between the two fish tissues in both metals (P < 0.01) (Table 3).

The accumulation in adsorbent samples (algae, Gammarus, co-culture, and control) showed liver more than muscle tissue. Also, algae had the highest absorption, and Gammarus had the highest accumulation of heavy metals among absorbent samples in two fish tissues. Statistically, there was a significant difference between fish tissues in each absorbent sample (P < 0.01) (Table 4).

Type of metal

In general comparison, the amount of accumulation in fish tissues was copper (Cu) higher than chromium metal (Cr). Statistically, there was a significant difference between copper and chromium metal in fish tissues (P < 0.01).

The accumulation in fish tissues showed copper more than chromium metal. Statistically, a significant difference was seen between copper and chromium metals in both fish body tissues (P < 0.01) (Table 3).

The accumulation in adsorbent samples (algae, Gammarus, co-culture, and control) showed copper more than chromium metal. Also, algae, the lowest, and Gammarus, the highest concentration of heavy metals, showed among the absorbent samples of fish tissue. Statistically, there was a significant difference between heavy metals in each absorbent sample (P < 0.01) (Table 4).

Table 4

Comparison of heavy metals and fish body tissue based on treatments (mg/L^− 1)
Control	Co-culture	Gammarus	Algae	Metal	Tissue
0.01 ± 0.005^a	0.01 ± 0.002^a	0.02 ± 0.004^b	0.004 ± 0.001^a	Cu	Muscle
0.001 ± 0.001^a	0.001 ± 0.0001^a	0.002 ± 0.001^a	0.0004 ± 0.007^a	Cr	Muscle
0.16 ± 0.005^b	0.16 ± 0.03^b	0.3 ± 0.007^c	0.05 ± 0.01^b	Cu	Liver
0.007 ± 0.003^a	0.006 ± 0.002^a	0.01 ± 0.0007^ab	0.003 ± 0.0003^a	Cr	Liver

Lowercase letters on each column indicate significant differences between the data.

Comparison of experiments (algae, Gammarus, and liver and muscle fish tissue)

In general comparison, the absorption of heavy metals copper (Cu) and chromium (Cr) observed in the highest amount in algae and the lowest amount in Gammarus, liver, and then muscle tissue. Statistically, there was a significant difference between the samples absorbed in each metal (P < 0.01) (Fig. 1).

The amount of absorption of heavy metals in algae culture observed to be higher for chromium than copper metal. It showed its effect in inhibiting heavy metals for the liver and muscle tissue. Statistically, a significant difference was between absorbed samples (P < 0.01).

The amount of absorption of heavy metals in Gammarus culture observed to be higher for copper than chromium metal. It showed its effect on the transfer of metals in the liver and then in the muscle tissue. Statistically, a significant difference was between absorbed samples (P < 0.05).

In co-cultivation, chromium metal observed with the highest metal absorption by algae and copper metal with the highest metal accumulation by body tissues. Algae are effective in inhibiting the transfer of metals to Gammarus in co-culture. Statistically, a significant difference was between absorbed samples (P < 0.01) (Table 5).

Table 5

Comparison of heavy metal absorbing samples based on metal-containing cultures (mg/L^− 1)
Co-culture	Gammarus culture	Algae culture	Sample
0.44 ± 0.06^c	-	0.61 ± 0.19^b	Algae
0.21 ± 0.09^b	0.38 ± 0.18^b	-	Gammarus
0.07 ± 0.08^ab	0.15 ± 0.16^ab	0.2 ± 0.01^a	Liver
0.006 ± 0.005^a	0.01 ± 0.01^a	0.002 ± 0.001^a	Muscle

Lowercase letters on each column indicate significant differences between the data.

Figure 1 Comparison of copper (Cu) and chromium (Cr) in heavy metal absorbing samples (mg/L^− 1)

Comparison of bioabsorption of heavy metals based on period

In this research, an experiment was to compare the bioabsorption of heavy metals copper and chromium by adsorbents including algae, Gammarus, and co-culture based on period of zero (less than one hour), 24 and 48 hours. In the present research, the absorption of copper and chromium heavy metals by adsorbents observed according to the periods for Algae > Algae in co-culture > Gammarus > Gammarus in co-culture. The initial absorption rate in algae was higher than other adsorbents, but it showed a downward trend over time. Similar to this opinion, Sayadi and Kumar reported in their articles that the absorption rate of algae in the first minutes is high, and the metal removal efficiency is almost constant over time (Kumar, 2014; Sayadi and Shekari, 2018). In Alowitz's research, the reason for the high amount of metal absorption in the first minutes was the presence of empty pores on the surface of the absorbent, which were occupied by chromium and copper metal ions over time, and it decreased the amount of metal absorption (Alowitz and Scherer, 2002).

In another experiment from this research, the initial rate of metal absorption by Gammarus observed to be lower than that of algae, but it showed an upward trend over time. According to the present research, Attaran introduced time as a function of metal absorption by Gammarus. It concluded that as time increases, this increased the accumulation of absorbed metal (Attaran et al., 2015). In Rainbow, Felten, and Vellinger's research, any increase in the amount of metal, whether gratis in the environment or the form of food in the diet, as well as skin absorption, increases the rate of metal absorption in the body of these organisms (Rainbow, 2002; Felten et al., 2008; Vellinger et al., 2012). In Rainbow's research of several crustaceans, especially Amphipoda, they concluded that all the metal absorbed by the creature remained in their body without any excretion (Rainbow and White, 1989).

In the present research, maximum bioabsorption by adsorbents (algae and Gammarus) observed in the first period (early hours). According to the present research, Hu concluded that 90% of chromium removed in the first minutes. In the beginning, the removal rate was very high, and then it decreased, and at the end of the time, it reached equilibrium (Hu et al., 2005). In Utomo's research, the absorption process of a metal was speedy, which done within a few minutes and remained constant during the absorption time (Utomo et al., 2016). In Nourisepehr's research, the speed of metal absorption increases with time, but this increase over time has been almost uniform and has not had a significant effect (Nourisepehr et al., 2015).

Comparison of biosorption of heavy metals based on metal type

In this research, a comparison was made of the biosorption of heavy metals copper and chromium by adsorbents, including algae, Gammarus, and co-culture. According to the present research, absorption of heavy metals in two metals, copper and chromium, by adsorbents was observed respectively for Algae > Algae in co-culture > Gammarus > Gammarus in co-culture. According to the current research, Kanamarlapudi found algae to be better absorbents than other biological absorbents for absorbing metal ions (Kanamarlapudi et al., 2018). According to Almomani, microalgae can remove several types of heavy metals from wastewater at the same time (Almomani and Bhosale, 2021). In the articles of Ahmad, Chen, and Yang, algae could absorb and accumulate significant amounts of heavy metals (Chen et al., 2021; Yang et al., 2021; Ahmad et al., 2022a). In Putri's research, the high absorption of algae considered due to the wide surface and empty spaces in the cell walls (Putri, 2015). According to Mane, algae protect themselves against the toxicity caused by heavy metals by several mechanisms, including removal, absorption to the cell surface, or intracellular accumulation (Mane and Bhosle, 2012).

In this research, chromium absorption observed more than copper metal in algae, and the maximum absorption of both metals was in 24 hours. According to the results of this research, Putri, Hadiyanto, and Sayadi found algae to be an adsorbent with better absorption efficiency for chromium metal, and the reason for that was the larger size of copper compared to chrome metal (Hadiyanto et al., 2014; Putri, 2015; Sayadi and Shekari, 2018). In Duffus' article, algae can absorb chromium metal about 4,000 times more than their water environment (Duffus, 1980). In the Avenant-Oldewage article, the highest concentration of chromium reported in the lowest level of the food pyramid, i.e. algae (Avenant-Oldewage and Marx, 2000). In the research of Salmani and Mane, the microalgae spirulina (A. platensis) found to be an algae with high efficiency in removing chromium (Mane and Bhosle, 2012; Salmani et al., 2018). In the research of Soeprobowati and Mane, the absorption of copper was much higher than that of chromium metal by algae (Mane and Bhosle, 2012; Soeprobowati and Hariyati, 2013). In Putri and Mane's article, algae act selectively in the absorption of some metals, and its cause is related to the detoxification mechanism of metals in the cell wall of algae with metal-binding peptides or proteins such as metallothionein (Mane and Bhosle, 2012; Putri, 2015).

Contrary to the results of the present research, in the research of Gelagutashvili and Kumar, the absorption of Cu(II) metal was more efficient than Cr(VI) and Cr(III) by microalgae Spirulina (A. platensis) (Kumar, 2014; Gelagutashvili et al., 2017). In the current research, unlike algae, it observed that copper absorption was more than chromium metal in Gammarus. Also, the maximum absorption of both metals by Gammarus was in 48 hours (maximum test time). In El Qoraychy's article, the absorption copper observed more than chromium metal by crustacean Louisiana crab (Procambarus clarkii) (El Qoraychy et al., 2015). Flemming and Rehwoldt, in performing LC50 tests, showed that organisms of the order Gastropoda, Crustacea, and Oligochaeta are sensitive to copper (Rehwoldt et al., 1973; Flemming and Trevors, 1989). In Rainbow's research on the Gammarus family and crustaceans in general, they found that these organisms are unable to regulate the concentration of unnecessary metals (such as chromium) in their bodies. So far, no mechanism has been to control these metals in their body (Rainbow and White, 1989). In Khaksar's research, the concentration of copper metal in Gammarus was higher than that of sediments, which indicates the high capacity of Gammarus to accumulate copper metal (Khaksar, 2014). According to the standards expressed by the European Union, American, and Australian organizations for the accumulation of metals in the body of animals, copper metal has a high concentration in the body of Gammarus (ASTM, 2013; ASTM International, 2013; Australian Government, 2015). Hemocyanin is a respiratory protein containing copper salt, which is a phylum in arthropods, and about 0.17% of their body weight made of copper (Redfield, 1934). Therefore, the amount of copper in their body with the amount of metal injected in the experiment is shallow and incalculable.

Comparison of absorbents in the absorption of heavy metals on fish body tissue

In this research, an experiment conducted to compare the biosorption of heavy metals copper and chromium by adsorbents including algae (treatment 1), Gammarus (treatment 2), co-culture (treatment 3), and control (treatment 4) in muscle and liver tissue of beluga fish. In the present research, the absorption of heavy metals in fish tissue by adsorbents seen in the order of Algae > co-culture > control > Gammarus. According to the present research, Abdel-Motleb and Khalila found that the injection of spirulina algae (A. platensis) through feed to fish causes severe changes in the histopathological reduction caused by heavy metals in the tissues of tilapia fish (Oreochromis niloticus). Also, consumption of algae in fish diets reduces the accumulation of heavy metals in their tissues (Khalila et al., 2018; Abdel-Motleb, 2022). In the articles of Ahmad and Rangsayatorn, they achieved specific strategies to prevent the accumulation of heavy metals in the food chain by injecting high concentrations of microalgae containing heavy metals into fish. They found that living algae remove heavy metals by two biochemical methods: biosorption (metal absorption on the cell surface) or bioaccumulation (metal absorption inside the cell) (Rangsayatorn et al., 2002; Ahmad et al., 2022b). In Kaoud's research, they found that microalgae improve the toxic effects of heavy metals on fish. They stated that it is due to the ability to separate heavy metals from water (Kaoud et al., 2012).

In the present research, a comparison was between the two metals chromium and copper absorbed by absorbents in fish body tissues. Based on the obtained results, absorption of chromium metal observed more than copper metal in fish body tissue by adsorbents. According to the results of previous experiments, chromium absorption was more than copper metal. Algae may absorb metal on their cell surface and then excretion the metal from the fish body. According to the present research, James, Ashfaq, and Tran, algal diet reduces metal accumulation in fish tissue. Also, metal removal mainly done by excretion from the digestive system (James, 2009; Tran et al., 2016; Ashfaq et al., 2017). In Mertz's research, fish excrete chromium metal through urine and reported the reason for high bile secretion after eating metal-contaminated food or water (Mertz, 1969).

Comparison of bioaccumulation of heavy metals in fish tissue

In this research, a comparison made of the accumulation of heavy metals copper and chromium in muscle tissue and liver of beluga fish. In the present study, the accumulation of heavy metals observed in liver tissue more than in muscle. According to the current research, Safahieh, Golovanova, Benamar, Rajeshkumar, and Parvin stated that the concentration of heavy metals in the liver is higher than in other parts of the fish body, and this tissue used to investigate the accumulation process. Liver, kidney, gill, and muscle tissues, respectively have the highest concentration of heavy metals (Golovanova, 2008; Safahieh et al., 2011; Benamar and Zitouni, 2013; Rajeshkumar and Li, 2018; Parvin et al., 2019). In the research of Hashemi and his colleagues, there is a significant difference in the amount of metal accumulation between liver and fish tissues, and the amount of metal in muscle tissue is meager (Hashemi et al., 2016). In the research of Tayel and Klaassen, the liver tissue plays a vital role in the detoxification and storage of heavy metals through the blood that comes from the intestine, and this shows that it is the primary tissue in receiving heavy metals through the consumption of metal-contaminated food (Klaassen, 1976; I Tayel et al., 2018). In several other studies, the concentration of heavy metals was in the liver higher than in muscle tissue (Gbem et al., 2001; Moiseenko and Kudryavtseva, 2001; Canli and Atli, 2003; El-Shaer and Alabssawy, 2019). In the articles of Krishnamurti and Yilmaz, the muscle tissue has the lowest accumulation of heavy metals among the fish tissues. Also, this tissue, in exposure to high levels of heavy metals in the external environment, often does not reflect an increase in metal accumulation (Krishnamurti and Nair, 2000; Yilmaz, 2003).

In the present research, algae had the lowest, and Gammarus had the highest concentration of heavy metals in fish tissues. According to the current research, in the Al-Weher article, crustaceans and mollusks store metals and other pollutants, and fish transfer heavy metals to their body while feeding on these organisms (Al-Weher, 2008). In the research of Yabanli and Gharedaashi on the food pyramid, Gammarus are considered primary consumers for juvenile fish such as white fish (kutum), mullet, and sturgeon, and they considered this as a warning sign for the transfer and accumulation of heavy metals in the body of fish (Gharedaashi et al., 2013; Yabanli et al., 2014). In the research of Shuhaimi, Marijic, and Mohanty, the contamination of Gammarus with heavy metals is the result of the transfer of pollution through feeding to fish and then to humans (Marijić and Raspor, 2007; Mohanty et al., 2009; Shuhaimi-Othman et al., 2010). In the present study, the accumulation of copper was higher than chromium metal in fish tissues. The reason is the higher absorption of chromium than copper metal by algae. Gammarus accumulates in fish body tissue due to its high amount of copper metal in fish feeding. Another reason can be due to the necessity and more excellent absorption of copper metal in the body tissue of the fish. According to the present research, Costa, Rajeshkumar, Kumar, Benamar, and Zidan declared the liver as the tissue with the highest accumulation of copper metal compared to other tissues of the fish body. Also, the liver introduced as a vital organ in copper regulation (Costa and Hartz, 2009; Benamar and Zitouni, 2013; Kumar, 2014; Rajeshkumar and Li, 2018; Zidan and El-Zaeem, 2020). In researching the effect of heavy metals on the white muscle of the Caspian Sea fish, Mousavi Moghadam stated that the copper metal accumulates twice as much as the chromium metal in the muscle tissue (Mousavi Moghadam et al., 2017). In Goyer's research, it was that the amount of accumulation of copper metal is higher than that of chromium metal, and the reason that it is essential copper metal for homeostatic regulation in all living organisms (Goyer and Clarkson, 1996). Also, according to Bennani and Duffus in their research, copper metal introduced as a trace element necessary for the natural growth and metabolism of plants, animals, and most microorganisms (Duffus, 1980; Bennani et al., 1996). In Miller's research, they found a direct relationship between copper metal in liver tissue and fish diet (Miller et al., 1993). In another research, Klerks, Carpene, and Forstner mentioned the high affinity of metallothioneins from copper metal and other heavy metals in liver tissue (Forstner and Wittmann, 1981; Carpene and Vašák, 1989; Klerks and Levinton, 1989).

According to Doudoroff, hexavalent chromium metal identified as toxicologically different from most heavy metals. Hexavalent chromium metal can penetrate the gill membranes by passive diffusion and concentrate at higher levels in different organs and tissues (Doudoroff and Katz, 1953). Also, Avenant-Oldewage stated in their article that the absorption of chromium metal not transferred through the food chain. In their research, they experimentally transferred chromium metal directly to the intestine, and the result of this action was the immediate removal of chromium without accumulation in other tissues. They identified gills as the primary source of chromium absorption (Avenant-Oldewage and Marx, 2000). In research by Buhler, they introduced the high concentration of chromium metal accumulation in the gills and liver due to the slow rate of removal of chromium metal from the body tissue of the fish (Buhler et al., 1977). In Oldewage's article, some fishes considered capable of accumulating high levels of chromium, nearly 100 times the concentration in water (Oldewage & Marx, 2000). In another article by Duffus, he introduced chromium as a dangerous metal for accumulation in many living organisms (Duffus, 1980).

In this research, a comparison was in transferring heavy metals from spirulina algae to Gammarus and then to beluga fish. In the present research, a general comparison of the accumulation of heavy metals observed in fish tissue, including algae (muscle) < co-culture (muscle) < Gammarus (muscle) < algae (liver) < co-culture (liver) < Gammarus (liver). Based on the transfer of heavy metals through the food chain, the maximum absorption of metal seen by algae, and in the next stage, it transferred to the Gammarus and then with a smaller amount to the liver and muscle tissue of fish. It can be that the increase of algae at the base of the pyramid does not cause the transfer of heavy metals and its harmful effects on the top of the pyramid.

Gammarus, by absorbing heavy metals, especially copper metal, accumulates and transmits them more strongly to the fish tissue. Therefore, algae in the food composition of fish will increase metal absorption and, as a result, reduce the accumulation and transfer of metals to fish tissue. Also, the accumulation of metal in the body tissue of the fish observed through the consumption of Gammarus (treatment 2) more than the direct injection of metal (treatment 4). Based on the results, Algae has an inhibitory role and Gammarus has a transporter role for heavy metals in fish body tissue.

There are two possibilities for the effect of algae on fish body tissue. In the first possibility, the algae absorb the metals from the environment, and during consumption in the fish diet, it not transferred to the fish body. Finally, it is excreted from the fish body (the possibility of this research). In the second possibility, the algae absorb the metals from the fish's body and finally the algae with metals are removed from the fish's body (need more time). Also, there are two possibilities for the effect of Gammarus on fish body tissue. In the first possibility, Gammarus absorbs the maximum metals from the environment and finally transfers all the absorbed metals as food to the fish (the possibility of this research). In the second possibility, it provides of digestion and absorption of Gammarus in the fish body is more than that of algae and provides enough time for the maximum absorption of metals in the fish tissue (requires metal absorption experiments during the digestive process).

As a result, if algae are not present in an ecosystem, it causes the direct transfer of heavy metals to tiny organisms such as Gammarus. During the consumption of these organisms by fish and, finally humans, it will have harmful effects on health in the long term. Therefore, algae cannot be directly food for fish in nature, but in the water ecosystem chain, they refine heavy metals for fish by directly absorbing metal from the environment and also by consuming algae by tiny organisms such as Gammarus as mediators.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Author Contribution

"A.B. and C.D. wrote the main manuscript text . All authors reviewed the manuscript."

Acknowledgements

This work is a university (student) research and I appreciate Khorramshahr University of Marine Sciences and Techniques for awarding the grant to student number 9634501. We are very grateful to the Caspian Sea Ecology Research Institute for allocating its laboratories, as well as the private fish breeding center of Qarehbron for preparing and testing fish.

Data availability

Data will be made available on request.

Credit author statement

A. Amri-Sahebi: Methodology, Data curation, Formal analysis and Writing– original draft. B. Dostshenas: Resources, Reviewing and Editing. R. Safari: Conceptualization, Methodology, Investigation, Resources, Supervision. A. Larki: Reviewing and Editing

Abdel-Motleb A (2022) Enhancement effects of microalgae against heavy metals-induced toxicity in Oreochromis niloticus fish with emphasis on hematological, immunological and histological aspects. Egyptian Journal of Aquatic Biology and Fisheries 26, 803-823. DOI: 10.21608/EJABF.2022.234761
Abdel-Raouf N, Al-Homaidan A, Ibraheem I (2012) Microalgae and wastewater treatment. Saudi journal of biological sciences 19, 257-275. doi.org/10.1016/j.sjbs.2012.04.005
Ahmad A, Banat F, Alsafar H, Hasan SW (2022a) Algae biotechnology for industrial wastewater treatment, bioenergy production, and high-value bioproducts. Science of The Total Environment 806, 150585. doi.org/10.1016/j.scitotenv.2021.150585
Ahmad A, Hassan S, Banat F (2022b) An overview of microalgae biomass as a sustainable aquaculture feed ingredient: Food security and circular economy. Bioengineered 13,9521-9547. doi.org/10.1080/21655979.2022.2061148
Al-Weher S (2008) Levels of heavy metal Cd, Cu and Zn in three fish species collected from the Northern Jordan Valley, Jordan. Jordan journal of biological sciences 1, 41-46.
Almomani F, Bhosale RR (2021) Bio-sorption of toxic metals from industrial wastewater by algae strains Spirulina platensis and Chlorella vulgaris: Application of isotherm, kinetic models and process optimization. Science of the Total Environment 755, 142654. doi.org/10.1016/j.scitotenv.2020.142654
Alowitz MJ, Scherer MM (2002) Kinetics of nitrate, nitrite, and Cr (VI) reduction by iron metal. Environmental Science & Technology 36, 299-30. doi.org/10.1021/es011000h
Ashfaq A, Bhat A, Azizul B (2017) Immobilized Chlorella vulgaris for efficient palm oil mill effluent treatment and heavy metals removal. Desalination and Water Treatment 81, 105-117. DOI : 10.5004/dwt.2017.20991
ASTM, D- (2013) Standard Practice for Total Digestion of Sediment Samples for Chemical Analysis of Various Metals, ASTM International, West Conshohocken, PA .
ASTM International (2013) ASTM E1022‐94(2013) standard guide for conducting bioconcentration tests with fishes and saltwater bivalve mollusks. West Conshohocken. DOI: 10.1520/E1022-94R13
Attaran A (2016) Comparison between biotic (Gammarus sp.) and abiotic (Coastal sediment) absorption performances in Caspian Sea Coast. Journal of Natural Environment, 69(3), 791-802. DOI: 10.22059/JNE.2016.61880
Australian Government (2015) Australia New Zealand Standard Code - Standard 1.4.1 – Contaminants and Natural Toxicants – F2015c00052, last amendment, 15/1/2015. Available in: www.comlaw.gov.au.
Avenant-Oldewage A, Marx H (2000) Bioaccumulation of chromium, copper and iron in the organs and tissues of Clarias gariepinus in the Olifants River, Kruger National Park. Water SA 26, 569-582. http://www.wrc.org.za
Benamar N, Zitouni B (2013) Levels of chromium and copper in liver and muscle tissues of the round Sardinella Sardinella aurita (Valenciennes) from the Oran Coastline, Algeria. Jordan Journal of Biological Sciences 6. DOI:10.12816/0001622
Bennani N, Schmid-Alliana A, Lafaurie M (1996) Immunotoxic Effects of Copper and Cadmiun the Sea Bass Dicentrarchus Labrax. Immunopharmacology and immunotoxicology 18, 129-144. doi.org/10.3109/08923979609007115
Budi R, Rahardja B, Masithah ED (2020) Potential concentration of heavy metal copper (cu) and microalgae growth Spirulina plantesis in culture media, IOP Conference Series: Earth and Environmental Science, IOP Publishing, p. 012147. DOI: 10.1088/1755-1315/441/1/012147
Buhler DR, Stokes RM, Caldwell RS (1977) Tissue accumulation and enzymatic effects of hexavalent chromium in rainbow trout (Salmo gairdneri). Journal of the Fisheries Board of Canada 34, 9-18. doi.org/10.1139/f77-002
Canli M, Atli G (2003) The relationships between heavy metal (Cd, Cr, Cu, Fe, Pb, Zn) levels and the size of six Mediterranean fish species. Environmental pollution 121, 129-136. doi.org/10.1016/S0269-7491(02)00194-X
Carpene E, Vašák M (1989) Hepatic metallothioneins from goldfish (Carassius auratus L.). Comparative Biochemistry and Physiology Part B: Comparative Biochemistry 92, 463-468. doi.org/10.1016/0305-0491(89)90117-X
Chen Z, Qiu S, Yu Z, Li M, Ge S (2021) Enhanced secretions of algal cell-adhesion molecules and metal ion-binding exoproteins promote self-flocculation of Chlorella sp. cultivated in municipal wastewater. Environmental Science & Technology 55, 11916-11924. doi.org/10.1021/acs.est.1c01324
Costa SdC, Hartz SM (2009) Evaluation of trace metals (cadmium, chromium, copper and zinc) in tissues of a commercially important fish (Leporinus obtusidens) from Guaíba Lake, Southern Brazil. Brazilian archives of biology and technology 52, 241-250. doi.org/10.1590/S1516-89132009000100029
Crump A (1993) Dictionary of environment and development: people, places, ideas, and organizations. MIT press. nla.gov.au/nla.cat-vn1375546
de la Noüe J, Proulx D (1988) Biological tertiary treatment of urban wastewaters with chitosan-immobilized Phormidium. Apply Microbiology Biotechnology 29, 292-297. doi.org/10.1007/BF00939324
Doudoroff P, Katz M (1953) Critical review of literature on the toxicity of industrial wastes and their components to fish: II. The metals, as salts. Sewage and Industrial Wastes, 802-839. www.jstor.org/stable/25032224
Duffus JH (1980) Environmental Toxicology. Edward Arnold (Publishers) Ltd. nla.gov.au/nla.cat-vn1496584
EL-SHAER FM, ALABSSAWY AN (2019) Assessment of heavy metals concentration in water and edible tissues of Nile tilapia (Oreochromis niloticus) and (Clarias gariepinus) from Burullus Lake, Egypt with liver histopathological as pollution indicator. Journal of the Egyptian Society of Parasitology 49, 183-194. DOI: 10.21608/jesp.2019.68301
El Qoraychy I, Fekhaoui M, El Abidi A, Benakame R, Bellaouchou A, Yahyaoui A (2015) Accumulation of copper, lead, chrome, cadmium in some tissues of Procambarus clarkii in Rharb Region in Morocco. Journal of Geoscience and Environment Protection 3, 74. DOI: 10.4236/gep.2015.38008
Felten V, Charmantier G, Mons R, Geffard A, Rousselle P, Coquery M, Garric J, Geffard O (2008) Physiological and behavioural responses of Gammarus pulex (Crustacea: Amphipoda) exposed to cadmium. Aquatic Toxicology 86, 413-425. doi.org/10.1016/j.aquatox.2007.12.002
Flemming C, Trevors J (1989) Copper toxicity and chemistry in the environment: a review. Water, air, and soil pollution 44, 143-158. doi.org/10.1007/BF00228784
Forstner U, Wittmann GT (1981) Metal Pollution in Aquatic Environment. 2nd Edition, Springer, 486. doi.org/10.1007/978-3-642-69385-4
Gbem T, Balogun J, Lawal F, Annune P (2001) Trace metal accumulation in Clarias gariepinus (Teugels) exposed to sublethal levels of tannery effluent. Science of the total environment 271, 1-9. doi.org/10.1016/S0048-9697(00)00773-7
Gelagutashvili E, Bagdavadze N, Rcheulishvili A (2017) Biosorption of Cr (III), Cr (VI), Cu (II) ions by intact cells of Spirulina platensis. arXiv preprint arXiv:1706.05307. doi.org/10.48550/arXiv.1706.05307
Gerhardt A, Bloor M, Mills CL (2011) Gammarus: important taxon in freshwater and marine changing environments, Hindawi. doi.org/10.1155/2011/524276
Gessner J, Chebanov M, Freyhof J (2022) Huso huso. The IUCN Red List of Threatened Species 2022 : E.T10269A135087846. Available online: doi.org/10.2305/IUCN. UK.2022-1.RLTS.T10269A135087846.en
Gharedaashi E, Nekoubin H, Imanpoor MR, Taghizadeh V (2013) Effect of copper sulfate on the survival and growth performance of Caspian Sea kutum, Rutilus frisii kutum. Springerplus 2, 1-5. doi.org/10.1186/2193-1801-2-498
Ghareyazie B, Mottaghi A (2012) Studing pontogammarus maeoticus among southern coast of caspian sea. Middle-East Journal of Scientific Research 12, 1484-1487. DOI: 10.5829/idosi.mejsr.2012.12.11.21
Ghosh M, Singh S (2005) Comparative uptake and phytoextraction study of soil induced chromium by accumulator and high biomass weed species. Applied Ecology and Environmental Research 3, 67-79. DOI:10.15666/aeer/0302_067079
Golovanova I (2008) Effects of heavy metals on the physiological and biochemical status of fishes and aquatic invertebrates. Inland Water Biology 1, 93-101. doi.org/10.1007/s12212-008-1014-1
Goyer RA, Clarkson TW (1996) Toxic effects of metals. Casarett and Doull’s toxicology: the basic science of poisons 5, 691-736.
Goyer RA, Clarkson TW (2001) Castanet and Doull's Toxicology the basic science of poisons. 6th ed: PP. 826-827.
Hadiyanto ABP, Buchori L, Budiyati CS (2014) Research Article Biosorption of Heavy Metal Cu₂ and Cr₂ in Textile Wastewater by Using Immobilized Algae. Research Journal of Applied Sciences, Engineering and Technology 7, 3539-3543. dx.doi.org/10.19026/rjaset.7.706
Hashemi E, Salari Ali Abadi MA, Safahieh A, Ghanemi K (2016) Bioaccumulation of Heavy Metals in Muscle and Liver of Shark (Chiloscyllium punctatum) in Khor Musa. Journal of Environmental Science and Technology 18, 201-208.
Herrero R, Cordero B, Lodeiro P, Rey-Castro C, de Vicente MS (2006) Interactions of cadmium (II) and protons with dead biomass of marine algae Fucus sp. Marine Chemistry 99, 106-116. doi.org/10.1016/j.marchem.2005.05.009
Hu J, Chen G, Lo IM (2005) Removal and recovery of Cr (VI) from wastewater by maghemite nanoparticles. Water research 39, 4528-4536. doi.org/10.1016/j.watres.2005.05.051
I Tayel S, A Mahmoud S, AM Ahmed N (2018) Pathological impacts of environmental toxins on Oreochromis niloticus fish inhabiting the water of Damietta branch of the River Nile, Egypt. Egyptian Journal of Aquatic Biology and Fisheries 22, 309-321. DOI: 10.21608/ejabf.2018.25660
James R, Sampath K, Nagarajan R, Vellaisamy P, Manikandan MM (2009) Effect of dietary Spirulina on reduction of copper toxicity and improvement of growth, blood parameters and phosphatases activities in carp, Cirrhinus mrigala (Hamilton, 1822). pubmed.ncbi.nlm.nih.gov/19957889/
Jia Y, Wang L, Qu Z, Wang C, Yang Z (2017) Effects on heavy metal accumulation in freshwater fishes: species, tissues, and sizes. Environmental Science and Pollution Research 24, 9379-9386. doi.org/10.1007/s11356-017-8606-4
Kamaruzzaman BY, Rina Z, John BA, Jalal KCA (2011) Heavy metal accumulation in commercially important fishes of South West Malaysian coast. Research Journal of Environmental Sciences 5, 595-602. DOI: 10.3923/rjes.2011.595.602
Kanamarlapudi S, Chintalpudi VK, Muddada S (2018) Application of biosorption for removal of heavy metals from wastewater. Biosorption 18, 70-116. DOI: 10.5772/intechopen.77315
Kaoud HA, Mahran KM, Rezk A, Khalf MA (2012) Bioremediation the toxic effect of mercury on liver histopathology, some hematological parameters and enzymatic activity in Nile tilapia, Oreochromis niloticus. Researcher 4, 60-70. doi:10.7537/marsrsj040112.10
Khaksar K, Negaristan H, Mashinchian A (2014) Study the concentration of heavy metals (lead, copper and cadmium) in Pontogammarus maeoticus on the southwestern shores of the Caspian Sea between Ramsar and Anzali. Marine Science and Technology Research Journal, Year 9, Number 1.
Khalila H, Fayed W, Mansour A, Srour T, Omar E, Darwish S, Nour A (2018) Dietary supplementation of Spirulina, Arthrospira platensis, with plant protein sources and their effects on growth, feed utilization and histological changes in Nile Tilapia, Oreochromis niloticus. Journal of Aquaculture Research & Development 9. DOI:10.4172/2155-9546.1000549
Klaassen CD (1976) Biliary excretion of metals. Drug Metabolism Reviews 5, 165-196. doi.org/10.3109/03602537609029977
Klerks PL, Levinton JS (1989) Effects of heavy metals in a polluted aquatic ecosystem, Ecotoxicology: Problems and approaches, Springer, pp. 41-67. doi.org/10.1007/978-1-4612-3520-0_3
Klimmek S, Stan H-J, Wilke A, Bunke G, Buchholz R (2001) Comparative analysis of the biosorption of cadmium, lead, nickel, and zinc by algae. Environmental science & technology 35, 4283-4288. doi.org/10.1021/es010063x
Kousar S, Javed M (2014) Heavy metals toxicity and bioaccumulation patterns in the body organs of four fresh water fish species. Pak. Vet. J 34, 161-164. api.semanticscholar.org/CorpusID:83192348
Krishnamurti AJ, Nair VR (2000) Concentration of metals in fishes from Thane and Basin creeks of Bombay. Indian Journal of Geo-Marine Sciences 28, 39-44. api.semanticscholar.org/CorpusID:73715921
Kumar R (2014) Heavy metal biosorption using algae. oai:generic.eprints.org:6471/core1451
Levy JL, Stauber JL, Jolley DF (2007) Sensitivity of marine microalgae to copper: the effect of biotic factors on copper adsorption and toxicity. Sci. Total Environ. 387, 141-154. doi.org/10.1016/j.scitotenv.2007.07.016
Mane P, Bhosle A (2012) Bioremoval of some metals by living algae Spirogyra sp. and Spirullina sp. from aqueous solution. DOI:10.22059/IJER.2012.527
Marijić VF, Raspor B (2007) Metal exposure assessment in native fish, Mullus barbatus L., from the Eastern Adriatic Sea. Toxicology letters 168, 292-301. doi.org/10.1016/j.toxlet.2006.10.026
Martin S, Griswold W (2009) Human health effects of heavy metals. Environmental Science and Technology briefs for citizens 15.
Mertz W (1969) Chromium occurrence and function in biological systems. Physiological reviews 49, 163-239. doi.org/10.1152/physrev.1969.49.2.163
Miller P, Lanno R, McMaster M, Dixon D (1993) Relative contributions of dietary and waterborne copper to tissue copper burdens and waterborne-copper tolerance in rainbow trout (Oncorhynchus mykiss). Canadian Journal of Fisheries and Aquatic Sciences 50, 1683-1689. doi.org/10.1139/f93-189
Mohanty, M., Adhikari, S., Mohanty, P., Sarangi, N., 2009. Role of waterborne copper on survival, growth and feed intake of Indian major carp, Cirrhinus mrigala Hamilton. Bulletin of environmental contamination and toxicology 82, 559-563. doi.org/10.1007/s00128-009-9652-5
Moiseenko, T., Kudryavtseva, L., 2001. Trace metal accumulation and fish pathologies in areas affected by mining and metallurgical enterprises in the Kola Region, Russia. Environmental Pollution 114, 285-297. doi.org/10.1016/S0269-7491(00)00197-4
Moopam, R., 1999. Manual of oceanographic observations and pollutant analysis methods. ROPME. Kuwait 1, 122-133.
Mousavi Moghadam, S. A., Nowrozi, M., Esmaili, M. 2018. Study heavy metals and its relationship with some biometric indicators in the muscle and gills of white fish (Rutilus frisii kutum) of the Caspian Sea. Scientific-research journal of marine biology, year 10, number 37.
Nourisepehr, M., Hajibagher Tehrani, S., Molaei Tavani, S., & Ghanbari, A. H. (2016). The survey of biological absorption of hexavalent chromium from aqueous solutions by Wastewater stabilization pond algae. Journal of Environmental Health Enginering, 3(3), 249-258. doi.org/10.18869/acadpub.jehe.3.3.249
Parsons, T.R., 2013. A manual of chemical & biological methods for seawater analysis. Elsevier.
Parvin, A., Hossain, M.K., Islam, S., Das, S.S., Munshi, J.L., Suchi, P.D., Moniruzzaman, M., Saha, B., Mustafa, M.G., 2019. Bioaccumulation of heavy metals in different tissues of Nile tilapia (Oreochromis niloticus) in Bangladesh. Malaysian Journal of Nutrition 25, 237-246. doi.org/10.31246/mjn-2018-0153
Pickering, Q.H., Henderson, C., 1966. The acute toxicity of some heavy metals to different species of warmwater fishes. Air and water pollution 10, 453-463.
Putri, L.S.E., 2015. Biosorption ability of microalgae Scenedesmus dimorphus for Cr (VI) and Cd in aqueous solution. Adv. Sci. Lett. 21, 196-198. doi.org/10.1166/asl.2015.5853
Qian, H., Chen, W., Sheng, G.D., Xu, X., Liu, W., Fu, Z., 2008. Effects of glufosinate on antioxidant enzymes, subcellular structure, and gene expression in the unicellular green alga Chlorella vulgaris. Aquat. Toxicol. 88, 301-307. doi.org/10.1016/j.aquatox.2008.05.009
Rainbow P, White S (1989) Comparative strategies of heavy metal accumulation by crustaceans: zinc, copper and cadmium in a decapod, an amphipod and a barnacle. Hydrobiologia 174, 245-262. doi.org/10.1007/BF00008164
Rainbow PS (2002) Trace metal concentrations in aquatic invertebrates: why and so what? Environmental pollution 120, 497-507. doi.org/10.1016/S0269-7491(02)00238-5
Rajeshkumar S, Li X (2018) Bioaccumulation of heavy metals in fish species from the Meiliang Bay, Taihu Lake, China. Toxicology reports 5, 288-295. doi.org/10.1016/j.toxrep.2018.01.007
Rajfur M, Kłos A, Wacławek M (2011) Algae utilization in assessment of the large Turawa Lake (Poland) pollution with heavy metals. J. Environ. Sci. Health, Part A 46, 1401-1408. doi.org/10.1080/10934529.2011.606717
Rangsayatorn N, Upatham E, Kruatrachue M, Pokethitiyook P, Lanza G (2002) Phytoremediation potential of Spirulina(Arthrospira) platensis: biosorption and toxicity studies of cadmium. Environmental Pollution 119, 45-53. doi.org/10.1016/S0269-7491(01)00324-4
Redfield AC (1934) The haemocyanins. Biological Reviews 9, 175-212. doi.org/10.1111/j.1469-185X.1934.tb01002.x
Rehwoldt R, Lasko L, Shaw C, Wirhowski E (1973) The acute toxicity of some heavy metal ions toward benthic organisms. Bulletin of Environmental Contamination and Toxicology 10, 291-294. doi.org/10.1007/BF01684818
Safahieh A, Monikh FA, Savari A, Doraghi A (2011) Heavy metals concentration in Mullet Fish, Liza abu from petrochemical waste receiving creeks, Musa Estuary (Persian Gulf). Journal of Environmental Protection 2, 1218. doi:10.4236/jep.2011.29140
Salam KA (2019) Towards sustainable development of microalgal biosorption for treating effluents containing heavy metals. Biofuel Res. J. 6, 948. DOI:10.18331/BRJ2019.6.2.2
Salmani N, Sayadi M, Rezaei M (2018) Optimization of Adsorption Process of Cr (VI) from Aqueous Solution Using Biosynthesized Palladium Nanoparticles by Spirulina Platensis. Modares Journal of Biotechnology 9, 171-177. biot.modares.ac.ir/article-22-24327-en.html
Sayadi M, Shekari H (2018) Efficiency of Spirogyra at Bioadsorption of Heavy Metals such as Chromium, Copper, and Zinc from Aquatic Environments. Modares Journal of Biotechnology 9, 241-246. biot.modares.ac.ir/article-22-14325-en.html
Shuhaimi-Othman M, Nadzifah Y, Ahmad A (2010) Toxicity of copper and cadmium to freshwater fishes. International Journal of Bioengineering and Life Sciences 4, 319-321. doi.org/10.5281/zenodo.1058189
Sibi G (2019) Factors influencing heavy metal removal by microalgae—A review. J. Crit. Rev 6, 29-32. DOI:10.22159/jcr.2019v6i6.35600
Soeder CJ, Payer H-D, Runkel K-H, Beine J, Briele E (1978) Sorption and concentration of toxic minerals by mass cultures of Chlorococcales: With 2 figures and 6 tables in the text. Internationale Vereinigung für Theoretische und Angewandte Limnologie: Mitteilungen 21, 575-584. doi.org/10.1080/05384680.1978.11903994
Soeprobowati TR, Hariyati R (2013) Bioaccumulation of Pb, Cd, Cu, and Cr by Porphyridium cruentum (SF Gray) Nägeli. International Journal of Marine Science 3. doi: 10.5376/ijms.2013.03.0027
Souza PO, Ferreira LR, Pires NR, S Filho PJ, Duarte FA, Pereira CM, Mesko MF (2012) Algae of economic importance that accumulate cadmium and lead: a review. Rev. bras. farmacogn. 22, 825-837. doi.org/10.1590/S0102-695X2012005000076
Tran HT, Vu ND, Matsukawa M, Okajima M, Kaneko T, Ohki K, Yoshikawa S (2016) Heavy metal biosorption from aqueous solutions by algae inhabiting rice paddies in Vietnam. Journal of environmental chemical engineering 4, 2529-2535. doi.org/10.1016/j.jece.2016.04.038
Utomo HD, Tan KXD, Choong ZYD, Yu JJ, Ong JJ, Lim ZB (2016) Biosorption of heavy metal by algae biomass in surface water. Journal of Environmental Protection 7, 1547-1560. DOI: 10.4236/jep.2016.711128
Vellinger C, Parant M, Rousselle P, Immel F, Wagner P, Usseglio-Polatera P (2012) Comparison of arsenate and cadmium toxicity in a freshwater amphipod (Gammarus pulex). Environmental Pollution 160, 66-73. doi.org/10.1016/j.envpol.2011.09.002
Wang X, Chen L, Xia S, Zhao J, Chovelon JM, Renault NJ (2006) Biosorption of Cu (II) and Pb (II) from aqueous solutions by dried activated sludge. Minerals engineering 19, 968-971. doi.org/10.1016/j.mineng.2005.09.042
Yabanli M, Yozukmaz A, Alparslan Y, Acar Ü (2014) Evaluation of heavy metals and selenium contents in the muscle tissues of rainbow trout (Oncorhynchus mykiss Walbaum, 1792) in Western Anatolia. Journal of Food, Agriculture and Environment 12. doi.org/10.1234/4.2014.4424
Yang L, Li H, Lu Q, Zhou W (2021) Emerging trends of culturing microalgae for fish-rearing environment protection. Journal of Chemical Technology & Biotechnology 96, 31-37. doi.org/10.1002/jctb.6563
Yilmaz AB (2003) Levels of heavy metals (Fe, Cu, Ni, Cr, Pb, and Zn) in tissue of Mugil cephalus and Trachurus mediterraneus from Iskenderun Bay, Turkey. Environmental research 92, 277-281. doi.org/10.1016/S0013-9351(02)00082-8
Zidan EM, El-Zaeem S (2020) Heavy Metals Profile Assessment in the Liver and Muscle Tissues of Nile Tilapia at The End of Production Cycle. Oceanography & Fisheries Open access Journal 12. DOI: 10.19080/OFOAJ.2020.12.555844

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Assessment of biosorption and transfer of heavy metals (chromium and copper) by Microalgae (Arthrospira platensis), Amphipoda (Pontogammarus maeoticus), and Beluga fish of Caspian Sea (Huso huso)

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