Heavy metal bioaccumulation (Ni, V and Hg) in soft tissues of crustaceans, bivalves and gastropods: A case study on the Northern Persian Gulf

Document Type : Research Paper

Authors

Faculty of Life Sciences and Biotechnology, Shahid Beheshti University, G.C., Evin, Tehran, Iran

10.22124/cjes.2023.7212

Abstract

The efficacy of Planaxis sulcatus (Gastropoda), Clibanarius signatus (Crustacea) and Circenita callipyga (Bivalvia) with different feeding guilds were compared as bioindicator of heavy metal pollution (Ni, V, Hg) in an area subjected to petrochemical development in the Northern Persian Gulf, Iran. Sampling was conducted in two locations with different degrees of exposure to petrochemical development: (i) on the intertidal zone adjacent to the petrochemical effluent (Impacted location); and (ii) on the intertidal zone unimpacted by the petrochemical effluent (Control location). No significance differences were found in heavy metal concentrations in whole-soft tissues of the selected organisms, seawater and sediment samples between two locations. The accumulation patterns for the heavy metals in the tissues of organisms and sediment samples followed the order of Ni > V > Hg, except in seawater. The concentration of nickel varied among the studied taxa and followed the order of C. callipyga > P. sulcatus > C. signatus. The bivalve, C. callipyga showed the high concentration of nickel in its soft tissue and the highest values for bioaccumulation factors (BAFs) as well as the biota-sediment accumulation factors (BSAFs) for nickel among the studied taxa. The results of the present study suggest that C. callipyga and P. sulcatus are efficient accumulators of nickel, while P. sulcatus and C. signatus are efficient accumulator of vanadium.

Keywords


Abdullah, MH, Sidi, J & Aris, AZ 2007, Heavy Metals (Cd, Cu, Cr, Pb and Zn) in Meretrix meretrix Roding, water and sediments from estuaries in Sabah, North Borneo. International Journal of Environmental & Science Education, 2: 69-74.
Alimohammadi, S 2009, Bioaccumulation of Heavy Metals Ni, Cd and Cu in Soft Tissue of Bivalves, Pinctada radiate and Barbatia decussata of intertidal zone of Nayband Bay. MSc. Dissertation, Shahid Beheshti University, [In Persian].
Amiard, JC, Bacheley, H, Barillé, AL, Barillé, L, Geffard, A & Himery, N 2004, Temporal changes in nickel and vanadium concentrations and in condition index and metallothionein levels in three species of molluscs following the “Erika” oil spill. Aquatic Living Resources, 17: 281-288, https://doi.org/10.1051/ alr:2004037.
Astani, M, Vosoughi, AR, Salimi, L & Ebrahimi, M 2012, 'Comparative study of heavy metal (Cd, Fe, Mn, and Ni) concentrations in soft tissue of gastropod Thais mutabilis and sediments from intertidal zone of Bandar Abbas. Advances in Environmental Biology, 6: 319-327.
Balkis, N, Aksu, A, Okus, E & Apak, R 2010, Heavy Metal Concentrations in Water, Suspended Matter, and Sediment from Gokova Bay, Turkey. Environmental Monitoring and Assessment, 167: 359-70, https://doi.org/10.1007/s10661-009-1055-x.
Bat, L, Yesim Özkan, E & Can Öztekin, H 2015, The contamination status of trace metals in Sinop coast of the Black Sea, Turkey', Caspian Journal of Environmental Sciences, 13: 1-10.
Beauvais, SL, Wiener, JG & Atchison, GJ 1995, Cadmium and mercury in sediment and burrowing mayfly nymphs (Hexagenia) in the upper Mississippi River, USA. Archives of Environmental Contamination and Toxicology, 28: 178-83, https://doi.org/10.1007/BF00217614.
Beldi, H, Gimbert, F, Maas, S, Scheifler, R & Soltani, N 2006, Seasonal variations of Cd, Cu, Pb and Zn in the edible mollusc Donax trunculus (Mollusca, Bivalvia) from the gulf of Annaba, Algeria. African Journal of Agricultural Research, 1: 85-90.
Berandah, FE, Kong, YC & Ismail, A 2010, 'Bioaccumulation and distribution of heavy metals (Cd, Cu, Fe, Ni, Pb and Zn) in the different tissues of Chicoreus capucinus Lamarck (Mollusca: Muricidae) collected from Sungai Janggut, Kuala Langat, Malaysia. Environment Asia, 3: 65-71. https://doi.org/10.14456/ea.2010.10.
Biagi, R, Meireles, AL & Mantelatto, FL 2006, Bio-ecological aspects of the hermit crab Paguristes calliopsis (Crustacea, Diogenidae) from Anchieta Island, Brazil', Anais da Academia Brasileira de Ciencias, 78: 451-62, https://doi.org/10.1590/S0001-37652006000300006.
Bosch, D, Dance, SP, Moolenbeek, RG & Oliver, PG 1995, Seashells of Eastern Arabia, UAE, Motivate Publishing.
Cebrian, E, Uriz, MJ & Turon, X 2007, 'Sponges as biomonitors of heavy metals in spatial and temporal surveys in northwestern Mediterranean: Multispecies comparison', Environmental Toxicology and Chemistry, 26: 2430-2439, https://doi.org/10.1897/07-292,1.
Chiffoleau, JF, Chauvaud, L, Amouroux, D, Barats, A, Dufour, A, Pécheyran, C & Roux, N 2004, Nickel and vanadium contamination of benthic invertebrates following the "Erika" wreck. Aquatic Living Resources, 17: 273-80.
Cossa, D 1989, 'A review of the use of Mytilus spp. as quantitative indicators of cadmium and mercury contamination in coastal waters', Oceanologica Acta, 12: 417-432.
Eisler, R 2009. Compendium of trace metals and marine biota, Oxford, UK, Elsevier.
Feng, W, Wang, Z, Xu, H, Zhang, D, Zhang, H & Zhu, W 2020, 'Species-specific bioaccumulation of trace metals among fish species from Xincun Lagoon, South China Sea', Scientific Reports, 10:  1.
Feulner, GR & Hornby, RJ 2006, Intertidal Molluscs in UAE Lagoons. Journal of the Emirates Natural History Group, 16: 17-23.
Foster, P & Cravo, A 2003, Minor elements and trace metals in the shell of marine gastropods from a shore in tropical East Africa. Water, Air, & Soil Pollution, 145: 53-65. https://doi.org/10.1023/A:1023631022989.
Golovanova, IL 2008, 'Effects of Heavy Metals on the Physiological and Biochemical Status of Fishes and Aquatic Invertebrates', Inland Water Biology, 1: 93-101. https://doi.org/10.1007/s12212-008-1014-1.
Gonzalez-Dkila, M 1995, The role of phytoplankton cells on the control of heavy metal concentration in seawater', Marine Chemistry. 48: 215-236. https://doi.org/10.1016/0304-4203(94)00045-F.
Griscom, SB & Fisher, NS 2004, 'Bioavailability of sediment-bound metals to marine bivalve molluscs: an overview', Estuaries and Coasts, 27: 826-38, https://doi.org/10.1007/BF02912044.
Helm, MM, Bourne, N & Lovatelli, A 2004, Hatchery culture of bivalves: A practical manual, Rome, Italy, FAO.
Hogarth, PJ 1988, Anomuran Crustacea (Paguridea, Porcellanidae, and Hippidea) from Oman, principally from Dhofar province, southern Oman', Journal of Natural History 22:  1095-1110. https://doi.org/10.1080/00222938800770681.
Hosseini, SH 2009, The intertidal Decapods of Bushehr, northern part of the Persian Gulf. Iranian Journal of Fisheries Sciences, 8: 37-46.
Houbrick, RS 1987, Anatomy, Reproductive Biology, and Phylogeny of the Planaxidae (Cerithiacea-Prosobranchia). Washington DC, Smithsonian Institution Press.
Kamyab, E 2010, Assessing the Bioaccumulation of Nickel, Vanadium (as oil Pollution Indicators) and Mercury in Some Tissues of an Intertidal Brachyuran Crab (Leptodius exaratus) of Persian Gulf ( a Case Study in Nayband Bay) MSc. Dissertation, Shahid Beheshti University, Tehran, Iran [In Persian].
Khoshnood, Z, Mokhlesi, A & Khoshnood, R 2010, Bioaccumulation of some heavy metals and histopathological alterations in liver of Euryglossa orientalis and Psettodes erumei along North Coast of the Persian Gulf', African Journal of Biotechnology, 9,  41, 6966-72. https://doi.org/10.5897/AJB10.944.
Khummongkol, D, Canterford, GS & Fryer, C 1982, Accumulation of heavy metals in unicellular algae. Biotechnology and Bioengineering, 24: 2643-60, https://doi.org/10.1002/bit.260241204.
Mages, M, Ovari, M, von Tumpling, W & Kröpfl, K 2004, Biofilms as bio-indicator for polluted waters? Analytical and Bioanalytical Chemistry, 378, 1095-1101, https://doi.org/10.1007/s00216-003-2291-5.
Mallahi, M, Ramachandrappa, GT & Dastranj, M 2012, 'A review of the effect of the environmental pollution of The Persian Gulf on the citizen’s dissatisfaction. Journal of Basic and Applied Scientific Research, 2: 5239-5247.
Markert, B 2007, Definitions and Principles for Bioindication and Biomonitoring of Trace Metals in the Environment', Journal of Trace Elements in Medicine and Biology, 21: 77-82, https://doi.org/10.1016/j.jtemb.2007.09.015.
Miramand, P, Guary, JC & Fowler, SW 1980, 'Vanadium transfer in the mussel Mytilus galloprovincialis', Marine Biology, 56,  4, 281-93. https://doi.org/10.1007/BF00386866.
Moradmand, M & Sari, A 2007, Littoral hermit crabs (Decapoda; Anomura; Paguroidea) of the Gulf of Oman, Iran. Iranian Journal of Animal Biosystematics, 3: 25-36.
Mortazavi, S, Esmaeili Sari, A & Riahi Bakhtiari, A 2005, A Determination of nikel to vanadium ratio in P. radiata and S. cucullata resulted from oil pollution in coastal fringes in Hormozgan Province, Iran. Iranian Journal of Natural Resources, 58: 159-172.
Nabavi, SMB, Ghotbeddin, N, Kochanian, P & Dehghan Madise, S 2007, Population growth of the venerid bivalve Circenita callipyga in the Hendijan coast, Persian Gulf, Pakistan Journal of Biological Sciences, 10: 3185-3189. https://doi.org/10.3923/pjbs.2007.3185.3189.
Odzak, N, Zvonaric, T, Kljakovic-Gaspic, Z, Horvat, M & Baric, A 2000, 'Biomonitoring of mercury in the Kastela Bay using transplanted mussels', Science of the Total Environment, 261: 61-68. https://doi.org/10.1016/s0048-9697(00)00595-7.
Pan, K & Wang, WX 2011, 'Mercury accumulation in marine bivalves: Influences of biodynamics and feeding niche. Environmental Pollution, 159,  10, 2500-6. https://doi.org/10.1016/j.envpol.2011.06.029.
Pourang, N, Nikouyan, A & Dennis, JH 2005, 'Trace element concentrations in fish, surficial sediments and water from northern part of the Persian Gulf', Environmental Monitoring and Assessment, 109: 293-316. https://doi.org/10.1007/s10661-005-6287-9.
Rainbow, P, Wolowicz, M, Fialkowski, W, Smith, BD & Sokolowski, A 2000, 'Biomonitoring of trace metals in the Gulf of Gdansk, using mussels (Mytilus trossulus) and barnacles (Balanus improvisus). Water Research, 34: 1823-1829. https://doi.org/10.1016/s0043-1354(99)00345-0.
Rainbow, PS 2006, Biomonitoring of trace metals in estuarine and marine environments. Australasian Journal of Ecotoxicology, 12: 107-122.
Ravera, O 2002, Monitoring of the aquatic environment by species accumulator of pollutants: A review. Journal of Limnology, 60: 63-78, https://doi.org/10.4081/jlimnol.2001.s1.63.
Rhea, DT, Harper, DD, Farag, AM & Brumbaugh, WG 2006, 'Biomonitoring in the boulder river watershed, montana, usa: metal concentrations in biofilm and macroinvertebrates, and relations with macroinvertebrate assemblage', Environmental Monitoring and Assessment, 115: 381-393. https://doi.org/10.1007/s10661-006-7086-7.
ROPME 1999, Manual of oceanographic observations and pollutant analyses methods (MOOPAM). Kuwait Regional Organization for the Protection of the Marine Environment.
Saeedi, H, Ashja Ardalan, A, Hassanzadeh Kiabi, B & Zibaseresht, R 2012, Metal concentrations in razor clam Solen dactylus (Von Cosel, 1989) (Bivalvia: Solenidae), sediments and water in Golshahr coast of Bandar Abbas, Persian Gulf. Iranian Journal of Fisheries Sciences, 11: 165-183.
Sant'Anna, BS, Zangrande, CM, Reigada, ALD & Pinheiro, MAA 2006, Shell utilization pattern of the hermit crab Clibanarius vittatus (Crustacea, Anomura) in an estuary at Sao Vicente, State of Sao Paulo, Brazil. Iheringia Série Zoologia, 96: 261-266.
Soto, DX, Roig, R, Gacia, E & Catalan, J 2011, Differential accumulation of mercury and other trace metals in the food web components of a reservoir impacted by a chlor-alkali plant (Flix, Ebro River, Spain): Implications for biomonitoring. Environmental pollution, 159: 1481-1489. https://doi.org/10.1016/ j.envpol. 2011.03.017.
Uluturhan, E 2010, Heavy metal concentrations in surface sediments from two regions (Saros and Gökova Gulfs) of the Eastern Aegean Sea. Environmental Monitoring and Assessment, 165: 675-684. https://doi.org/10.1007/s10661-009-0978-6.
Unsal, M 1983, Transfer pathways and accumulation of vanadium in the crab Carcinus maenas', Marine Biology, 72: 279-282. https://doi.org/10.1007/BF00396833.
van Hullebusch, ED, Zandvoort, MH & Lens, PNL 2003, Metal immobilisation by biofilms: Mechanisms and analytical tools. Reviews in Environmental Science and Biotechnology, 2: 9-33, https://doi.org/10.1023/B:RESB.0000022995.48330.55.
Williams, JD & McDermott, JJ 2004, Hermit crab biocoenoses: A worldwide review of the diversity and natural history of hermit crab associates. Journal of Experimental Marine Biology and Ecology, 305: 1-128. https://doi.org/10.1016/j.jembe.2004.02.020.
Yap, CK & Cheng, WH 2009, Heavy metal concentrations in Nerita lineata: the potential as a biomonitor for heavy metal bioavailability and contamination in the tropical intertidal area. Marine Biodiversity Records, 2, e46. https://doi.org/10.1017/S1755267209000505.
Zauke, GP, Ritterhoff, J & Rinderhagen, M 1998, Concepts and applications in aquatic biomonitoring-internal review paper (updated version: November 2005), Oldenburg, Germany, Aquatic Ecology Group, ICBM, CvO Univ.