Atmosphere, earth and water compose the environment. The presence of heavy metals in the environment has grown because of their large employment in some industrial and agricultural activities. Although these metals are terrestrial products, they flow into the sea through effluents and sewage or are directly discharged from industries placed on the seawater front. It should be considered that metals concentrations vary widely according to different seawater latitudes and depths and can be strongly influenced by fresh water discharges from heavily polluted rivers. In this review recent studies on heavy metal pollution in marine ecosystems and their organisms will be presented. Metal speciation, bioaccumulation in biota, as well as abiotic and biotic factors affecting their bioavailability will be reviewed. Moreover, the use of bioindicator organisms for the biomonitoring of heavy metal toxicity and their ecological effects will be defined. Many marine invertebrate species fulfill the following criteria: Sensitivity to a wide range of chemicals (especially to heavy metals), cost-effectiveness for repeatable tests, readily interpretable biological consequences of pollution. Among the most important marine invertebrates used as bioindicators, the sea urchin embryo is one of the most suitable, especially to assess metal/heavy metal pollution.
References
[1]
Singh, V.P. (2005) Metal Toxicity and Tolerance in Plants and Animals. Sarup & Sons, New Delhi, 1-328.
[2]
Fraústo da Silva, J.J.R. and Williams, R.J.P. (1993) The Biological Chemistry of the Elements: The Inorganic Chemistry of Life. Clarendon Press, Oxford, 1-561.
[3]
Tamás, M.J. and Martinoia, E. (2005) Molecular Biology of Metal Homeostasis and Detoxification: From Microbes to Man. Springer Verlag, Heidelberg, 1-506.
[4]
Scheifler, R., Coeurdassier, M., Morilhat, C., Bernard, N., Faivre, B., Flicoteaux, P., et al. (2006) Lead Concentrations in Feathers and Blood of Common Blackbirds (Turdusmerula) and in Earthworms Inhabiting Unpolluted and Moderately Polluted Urban Areas. Science of the Total Environment, 371, 197-205.
http://dx.doi.org/10.1016/j.scitotenv.2006.09.011
[5]
Chapman, P.M., Allen, H.E. and Z’Graggen, M.N. (1996) Evaluation of Bioaccumulation Factors in Regulating Metals. Environmental Science and Technology Journal, 30, 448A-452A. http://dx.doi.org/10.1021/es962436d
[6]
Thirumoorthy, N., Shyam Sunder, A., Manisenthil Kumar, K., Senthil Kumar, M., Ganesh, G. and Chatterjee, M. (2011) A Review of Metallothionein Isoforms and Their Role in Pathophysiology. World Journal of Surgical Oncology, 20, 1-7.
[7]
Reidel, G.F., Abbe, G.R. and Sanders, J.G. (1995) Silver and Copper Accumulation in Two Estuarine Bivalves, the Eastern Oyster (Crassostrea virginica) and the Hooked Mussel (Ischadiumrearrum). Estuaries, 18, 445-455.
http://dx.doi.org/10.2307/1352363
[8]
Bryan, G.W. and Langston, W.J. (1991) Bioavailability, Accumulation and Effects of Heavy Metals in Sediments with Special Reference to United Kingdom Estuaries: A Review. Environmental Pollution, 76, 89-131.
http://dx.doi.org/10.1016/0269-7491(92)90099-V
[9]
Dallinger, E. and Rainbow, P.S. (1992) Ecotoxicology of Metals in Invertebrates. Lewis, Boca Raton, 1-217.
[10]
Rainbow, P.S. (2002) Trace Metal Concentrations in Aquatic Invertebrates: Why and So What? Environmental Pollution, 120, 497-507. http://dx.doi.org/10.1016/S0269-7491(02)00238-5
[11]
Kim, B.M., Rhee, J.S., Jeong, C.B., Seo, J.S., Park, G.S., Lee, Y.M. and Lee, J.S. (2014) Heavy Metals Induce Oxidative Stress and Trigger Oxidative Stress-Mediated Heat Shock Protein (hsp) Modulation in the Intertidal Copepod Tigriopus japonicus. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 66, 65-74.
http://dx.doi.org/10.1016/j.cbpc.2014.07.005
[12]
Tamás, M.J., Sharma, S.K., Ibstedt, S., Jacobson, T. and Christen, P. (2014) Heavy Metals and Metalloids as a Cause for Protein Misfolding and Aggregation. Biomolecules, 4, 252-267. http://dx.doi.org/10.3390/biom4010252
[13]
Graeme, K.A. and Pollack, C.V. (1998) Heavy Metal Toxicity, Part I: Arsenic and Mercury. The Journal of Emergency Medicine, 16, 45-56. http://dx.doi.org/10.1016/S0736-4679(97)00241-2
[14]
Schiff, K.C. (2000) Sediment Chemistry on the Mainland Shelf of the Southern California Bight. Marine Pollution Bulletin, 40, 268-270. http://dx.doi.org/10.1016/S0025-326X(99)00216-7
[15]
Harada, M., Nakanishi, J., Konuma, S., Ohno, K., Kimura, T., Yamaguchi, H., et al. (1998) The Present Mercury Contents of Scalp Hair and Clinical Symptoms in Inhabitants of the Minamata Area. Environmental Research, 77, 160-164.
http://dx.doi.org/10.1006/enrs.1998.3837
[16]
Liu, X., Zhang, L., You, L., Yu, J., Zhao, J., Li, L., et al. (2011) Differential Toxicological Effects Induced by Mercury in Gills from Three Pedigrees of Manila Clam Ruditapes philippinarum by NMR-Based Metabolomics. Ecotoxicology, 20, 177-186. http://dx.doi.org/10.1007/s10646-010-0569-x
[17]
Longo, G., Trovato, M., Mazzei, V., Ferrante, M. and Conti, G.O. (2013) Ligia italica (Isopoda, Oniscidea) as Bioindicator of Mercury Pollution of Marine Rocky Coasts. PLoS ONE, 8, e58548.
http://dx.doi.org/10.1371/journal.pone.0058548
[18]
Singaram, G., Harikrishnan, T., Chen, F.Y., Bo, J. and Giesy, J.P. (2013) Modulation of Immune-Associated Parameters and Antioxidant Responses in the Crab (Scylla serrata) Exposed to Mercury. Chemosphere, 90, 917-928.
http://dx.doi.org/10.1016/j.chemosphere.2012.06.031
[19]
Bosnjak, I., Uhlinger, K.R., Heim, W., Smital, T., Franeki?-Coli?, J., Coale, K., et al. (2009) Multidrug Efflux Transporters Limit Accumulation of Inorganic, but Not Organic, Mercury in Sea Urchin Embryos. Environmental Science & Technology, 43, 8374-8380. http://dx.doi.org/10.1021/es901677r
[20]
Shirneshan, G., Bakhtiari, A.R., Kazemi, A., Mohamadi, M. and Kheirabadi, N. (2012) Oyster Saccostrea cucullata as a Biomonitor for Hg Contamination and the Risk to Humans on the Coast of Qeshm Island, Persian Gulf, Iran. Bulletin of Environmental Contamination and Toxicology, 88, 962-966. http://dx.doi.org/10.1007/s00128-012-0607-x
[21]
Zhang, Q.H., Huang, L., Zhang, Y., Ke, C.H. and Huang, H.Q. (2013) Proteomic Approach for Identifying Gonad Differential Proteins in the Oyster (Crassostrea angulata) Following Food-Chain Contamination with HgCl2. Journal of Proteomics, 94, 37-53. http://dx.doi.org/10.1016/j.jprot.2013.08.018
[22]
Jarup, L., Berglund, M., Elinder, C.G., Nordberg, G. and Vahter, M. (1998) Health Effects of Cadmium Exposure a Review of the Literature and a Risk Estimate. Scandinavian Journal of Work, Environment & Health, 24, 1-51.
[23]
Kingsley, B.S. and Frazier, J.M. (1979) Cadmium Transport in Isolated Perfused Rat Liver: Zinc-Cadmium Competition. American Journal of Physiology, 236, 139-143.
[24]
Foulkes, E.C. (2000) Transport of Toxic Heavy Metals across Cell Membranes. Proceedings of the Society for Experimental Biology and Medicine, 223, 234-240. http://dx.doi.org/10.1046/j.1525-1373.2000.22334.x
[25]
De Lisle, P.F. and Roberts Jr., M.H. (1988) The Effect of Salinity on Cadmium Toxicity to the Estuarine Mysid (Mysidopsis bahia): Role of Chemical Speciation. Aquatic Toxicology, 12, 357-370.
http://dx.doi.org/10.1016/0166-445X(88)90062-8
[26]
Koizumi, T. and Li, Z.G.J. (1992) Role of Oxidative Stress in Single-Dose, Cadmium-Induced Testicular Cancer. Toxicology and Environmental Health, 37, 25-36. http://dx.doi.org/10.1080/15287399209531654
[27]
Waalkes, M.P. and Rehm, S. (1998) Lack of Carcinogenicity of Cadmium Chloride in Female Syrian hamsters. Toxicology, 3,173-178. http://dx.doi.org/10.1016/S0300-483X(98)00012-2
[28]
Rana, S.V. (2008) Metals and Apoptosis: Recent Developments. Journal of Trace Elements in Medicine and Biology, 22, 262-284. http://dx.doi.org/10.1016/j.jtemb.2008.08.002
[29]
Sokolova, I.M., Evans, S. and Hughes, F.M. (2004) Cadmium-Induced Apoptosis in Oyster Hemocytes Involves Disturbance of Cellular Energy Balance but No Mitochondrial Permeability Transition. The Journal of Experimental Biology, 207, 3369-3380. http://dx.doi.org/10.1242/jeb.01152
[30]
Dubois, M. and Hare, L. (2009) Subcellular Distribution of Cadmium in Two Aquatic Invertebrates: Change over Time and Relationship to Cd Assimilation and Loss by a Predatory Insect. Environmental Science & Technology, 15, 356- 361. http://dx.doi.org/10.1021/es801406r
[31]
Müller, W.E.G., Batel, R., Lacorn, M., Steinhart, H., Simat, T., Lauenroth, S., et al. (1998) Accumulation of Cadmium and Zinc in the Marine Sponge Suberites domuncula and Its Potential Consequences on Single-Strand Breaks and on Expression of Heat-Shock Protein: A Natural Field Study. Marine Ecology Progress Series, 167, 127-135.
http://dx.doi.org/10.3354/meps167127
[32]
Cebrian, E. and Uriz, M.J. (2007) Do Heavy Metals Play an Active Role in Sponge Cell Behavior in the Absence of Calcium? Consequences in Larval Settlement. Journal of Experimental Marine Biology and Ecology, 346, 60-65.
http://dx.doi.org/10.1016/j.jembe.2007.02.010
[33]
Viarengo, A., Arena, N., Canesi, L., Alia, F.A. and Orunes, M. (1994) Structural and Biochemical Alteration in the Gills of Copper-Exposed Mussels. In: Renzoni, A., Mattei, N., Lari, L. and Fossi, M.C., Eds., Contaminants in the Environment: A Multidisciplinary Assessment of Risk to Man and Other Organism, CRC Press, Boca Raton, 135-144.
[34]
Nigro, M., Regoli, F., Rocchi, R. and Orlando, E. (1997) Heavy Metals in Antarctic Molluscs. In: Battaglia, B., Valencia, J. and Walton, D.W.H., Eds., Antarctic Communities: Species, Structure and Survival, Cambridge University Press, Cambridge, 409-412.
[35]
Podgurskaya, O.V. and Kavun V.Y. (2006) Cadmium Concentration and Subcellular Distribution in Organs of the Mussel Crenomytilus grayanus from Upwelling Regions of Okhotsk Sea and Sea of Japan. Archives of Environmental Contamination and Toxicology, 51, 567-572. http://dx.doi.org/10.1007/s00244-005-0151-3
[36]
Rodrigues, E., da Silva Santos, M.R., Rodrigues Jr., E., Gannabathula, S.V. and Lavrado, H.P. (2009) Arginine Metabolism of the Antarctic Bivalve Laternula elliptica (King & Broderip, 1831): An Ecophysiological Approach. Polar Biology, 32, 691-702. http://dx.doi.org/10.1007/s00300-008-0574-1
[37]
Roccheri, M.C. and Matranga, V. (2010) Cellular, Biochemical and Molecular Effects of Cadmium on Marine Invertebrates: Focus on Paracentrotus lividus Sea Urchin Development. In: Reini, G.P., Ed., Cadmium in the Environment, Nova Science Publishers Inc., New York, 337-366.
[38]
Chiarelli, R., Agnello, M. and Roccheri, M.C. (2011) Sea Urchin Embryos as a Model System for Studying Autophagy Induced by Cadmium Stress. Autophagy, 7, 1028-1034. http://dx.doi.org/10.4161/auto.7.9.16450
[39]
Kaur, S., Kamli, M.R. and Ali, A. (2011) Role of Arsenic and Its Resistance in Nature. Canadian Journal of Microbiology, 57, 769-774. http://dx.doi.org/10.1139/w11-062
[40]
Mayer, D.R., Kosmus, W., Pogglitsch, H., Mayer, D. and Beyer, W. (1993) Essential Trace Elements in Humans. Serum Arsenic Concentrations in Hemodialysis Patients in Comparison to Healthy Controls. Biological Trace Element Research, 37, 27-38. http://dx.doi.org/10.1007/bf02789399
[41]
Sloth, J.J., Larsen, E.H. and Julshamn, K. (2005) Report on Three Aliphatic Dimethylarsinoyl Compounds as Common Minor Constituents in Marine Samples. An Investigation Using High-Performance Liquid Chromatography/Inductively Coupled Plasma Mass Spectrometry and Electrospray Ionisation Tandem Mass Spectrometry. Rapid Communications in Mass Spectrometry, 19, 227-235. http://dx.doi.org/10.1002/rcm.1770
[42]
Hong, S., Khim, J.S., Park, J., Son, H.S., Choi, S.D., Choi, K., et al. (2014) Species- and Tissue-Specific Bioaccumulation of Arsenicals in Various Aquatic Organisms from a Highly Industrialized Area in the Pohang City, Korea. Environmental Pollution, 192, 27-35. http://dx.doi.org/10.1016/j.envpol.2014.05.004
[43]
Wu, X., Gao, M., Wang, L., Luo, Y., Bi, R., Li, L., et al. (2014) The Arsenic Content in Marketed Seafood and Associated Health Risks for the Residents of Shandong, China. Ecotoxicology and Environmental Safety, 102, 168-173.
http://dx.doi.org/10.1016/j.ecoenv.2014.01.028
[44]
Pagano, G., Esposito, A., Bove, P., de Angelis, M., Rota, A., Vamvakinos, E., et al. (1982) Arsenic-Induced Developmental Defects and Mitotic Abnormalities in Sea-Urchin Development. Mutation Research, 104, 351-354.
http://dx.doi.org/10.1016/0165-7992(82)90168-3
[45]
Gaion, A., Scuderi, A., Pellegrini, D. and Sartori, D. (2013) Arsenic Exposure Affects Embryo Development of Sea Urchin, Paracentrotus lividus (Lamarck, 1816). Bulletin of Environmental Contamination and Toxicology, 91, 565-570.
http://dx.doi.org/10.1007/s00128-013-1098-0
[46]
Natale, G., Basso, N. and Ronco, A. (2000) Effect of Cr (VI) on Early Life Stages of Three Species of Hylid Frogs (Amphibia, Anura) from South America. Environmental Toxicology, 15, 509-512.
http://dx.doi.org/10.1002/1522-7278(2000)15:5<509::AID-TOX21>3.0.CO,2-S
[47]
Urrutia, C., Rudolph, A., Lermanda, M.P. and Ahumada, R. (2008) Assessment of EDTA in Chromium (III-VI) Toxicity on Marine Intertidal Crab (Petrolisthes laevigatus). Bulletin of Environmental Contamination and Toxicology, 80, 526-528. http://dx.doi.org/10.1007/s00128-007-9310-8
[48]
Ciacci, C., Barmo, C., Gallo, G., Maisano, M., Cappello, T., D’Agata, A., et al. (2012) Effects of Sublethal, Environmentally Relevant Concentrations of Hexavalent Chromium in the Gills of Mytilus galloprovincialis. Aquatic Toxicology, 120-121, 109-118. http://dx.doi.org/10.1016/j.aquatox.2012.04.015
[49]
Ciacci, C., Barmo, C., Fabbri, R., Canonico, B., Gallo, G. and Canesi, L. (2011) Immunomodulation in Mytilus galloprovincialis by Non-Toxic Doses of Hexavalent Chromium. Fish & Shellfish Immunology, 31, 1026-1033.
http://dx.doi.org/10.1016/j.fsi.2011.09.002
[50]
Emmanouil, C., Sheehan, T.M. and Chipman, J.K. (2007) Macromolecule Oxidation and DNA Repair in Mussel (Mytilus edulis L.) Gill Following Exposure to Cd and Cr(VI). Aquatic Toxicology, 82, 27-35.
http://dx.doi.org/10.1016/j.aquatox.2007.01.009
[51]
Baumann, Z. and Fisher, N.S. (2011) Modeling Metal Bioaccumulation in a Deposit-Feeding Polychaete from Labile Sediment Fractions and from Pore Water. Science of the Total Environment, 409, 2607-2615.
http://dx.doi.org/10.1016/j.scitotenv.2011.03.009
[52]
Barmo, C., Ciacci, C., Fabbri, R., Olivieri, S., Bianchi, N., Gallo, G. and Canesi, L. (2011) Pleiotropic Effects of Hexavalent Chromium (CrVI) in Mytilus galloprovincialis Digestive Gland. Chemosphere, 83, 1087-1095.
[53]
Tan, Q.G., Ke, C. and Wang, W.X. (2013) Rapid Assessments of Metal Bioavailability in Marine Sediments Using Coelomic Fluid of Sipunculan Worms. Environmental Science and Technology, 47, 7499-7505.
[54]
Bellas, J., Vázquez, E. and Beiras, R. (2001) Toxicity of Hg, Cu, Cd, and Cr on Early Developmental Stages of Ciona intestinalis (Chordata, Ascidiacea) with Potential Application in Marine Water Quality Assessment. Water Research, 35, 2905-2912. http://dx.doi.org/10.1016/S0043-1354(01)00004-5
[55]
Peter, A.L. and Viraraghavan, T. (2005) Thallium: A Review of Public Health and Environmental Concerns. Environment International, 31, 493-501. http://dx.doi.org/10.1016/j.envint.2004.09.003
[56]
Kazantzis, G. (2000) Thallium in the Environment and Health Effects. Environmental Geochemistry and Health, 22, 275-280. http://dx.doi.org/10.1023/A:1006791514080
[57]
Couture, P., Fortin, C., Hare, L., Lapointe, D. and Danaè, P. (2011) Critical Review of Thallium in Aquatic Ecosystems. Research Report No R-1272, 1-36.
[58]
Zitko, V. and Carson, W.V. (1975) Accumulation of Thallium in Clams and Mussels. Bulletin of Environmental Contamination & Toxicology, 14, 530-533.
[59]
Turner, A., Turner, D. and Braungardt, C. (2013) Biomonitoring of Thallium Availability in Two Estuaries of Southwest England. Marine Pollution Bulletin, 69, 172-177. http://dx.doi.org/10.1016/j.marpolbul.2013.01.030
[60]
Nava-Ruiz, C., Méndez-Armenta, M. and Ríos, C. (2012) Lead Neurotoxicity: Effects on Brain Nitric Oxide Synthase. Journal of Molecular Histology, 43, 553-563. http://dx.doi.org/10.1007/s10735-012-9414-2
[61]
Mansoori, A., Nabavi, S.M.B., Parsa, Y., Nabavi, S.N. and Ashrafi, M.G. (2013) The Level of Cd, Hg, Mn and Pb in Sediment and Invertebrate from North of the Persian Gulf. World Applied Sciences Journal, 28, 1048-1050.
[62]
Strizak, Z., Ivankovic, D., Profrock, D., Helmholz, H., Cindric, A.M., Erk, M., et al. (2014) Characterization of the Cytosolic Distribution of Priority Pollutant Metals and Metalloids in the Digestive Gland Cytosol of Marine Mussels: Seasonal and Spatial Variability. Science of the Total Environment, 470-471, 159-170.
http://dx.doi.org/10.1016/j.scitotenv.2013.09.051
[63]
Geraci, F., Pinsino, A., Turturici, G., Savona, R., Giudice, G. and Sconzo, G. (2004) Nickel, Lead, and Cadmium Induce Differential Cellular Responses in Sea Urchin Embryos by Activating the Synthesis of Different HSP70s. Biochemical and Biophysical Research Communications, 322, 873-877. http://dx.doi.org/10.1016/j.bbrc.2004.08.005
[64]
Tellis, M.S., Lauer, M.M., Nadella, S., Bianchini, A. and Wood, C.M. (2014) Sublethal Mechanisms of Pb and Zn Toxicity to the Purple Sea Urchin (Strongylocentrotus purpuratus) during Early Development. Aquatic Toxicology, 146, 220-229. http://dx.doi.org/10.1016/j.aquatox.2013.11.004
[65]
Hariharan, G., Purvaja, R. and Ramesh, R. (2014) Toxic Effects of Lead on Biochemical and Histological Alterations in Green Mussel (Perna viridis) Induced by Environmentally Relevant Concentrations. Journal of Toxicology and Environmental Health, Part A, 77, 246-260. http://dx.doi.org/10.1080/15287394.2013.861777
[66]
Russo, R., Bonaventura, R., Zito, F., Schr?der, H.C., Müller, I., Müller, W.E., et al. (2003) Stress to Cadmium Monitored by Metallothionein Gene Induction in Paracentrotus lividus Embryos. Cell Stress Chaperones, 8, 232-241.
http://dx.doi.org/10.1379/1466-1268(2003)008<0232:STCMBM>2.0.CO,2
[67]
Matranga, V., Zito, F., Costa, C., Bonaventura, R., Giarrusso, S. and Celi, F. (2010) Embryonic Development and Skeletogenic Gene Expression Affected by X-Rays in the Mediterranean Sea Urchin Paracentrotus lividus. Ecotoxicology, 19, 530-537. http://dx.doi.org/10.1007/s10646-009-0444-9
[68]
Vacquier, V.D. (2011) Laboratory on Sea Urchin Fertilization. Molecular Reproduction and Development, 78, 553-564.
http://dx.doi.org/10.1002/mrd.21360
[69]
Roccheri, M.C., Agnello, M., Bonaventura, R. and Matranga, V. (2004) Cadmium Induces the Expression of Specific Stress Proteins in Sea Urchin Embryos. Biochemical and Biophysical Research Communications, 321, 80-87.
http://dx.doi.org/10.1016/j.bbrc.2004.06.108
[70]
Agnello, M., Filosto, S., Scudiero, R., Rinaldi, A.M. and Roccheri, M.C. (2007) Cadmium Induces an Apoptotic Response in Sea Urchin Embryos. Cell Stress Chaperones, 12, 44-50. http://dx.doi.org/10.1379/CSC-229R.1
[71]
Hamdoun, A. and Epel, D. (2007) Embryo Stability and Vulnerability in an Always Changing World. Proceedings of the National Academy of Sciences of the United States of America, 104, 1745-1750.
http://dx.doi.org/10.1073/pnas.0610108104
[72]
Filosto, S., Roccheri, M.C., Bonaventura, R. and Matranga, V. (2008) Environmentally Relevant Cadmium Concentrations Affect Development and Induce Apoptosis of Paracentrotus lividus Larvae Cultured in Vitro. Cell Biology and Toxicology, 24, 603-610. http://dx.doi.org/10.1007/s10565-008-9066-x
[73]
Agnello, M. and Roccheri, M.C. (2010) Apoptosis: Focus on Sea Urchin Development. Apoptosis, 15, 322-330.
http://dx.doi.org/10.1007/s10495-009-0420-0
[74]
Chiarelli, R., Agnello, M., Bosco, L. and Roccheri, M.C. (2014) Sea Urchin Embryos Exposed to Cadmium as an Experimental Model for Studying the Relationship between Autophagy and Apoptosis. Marine Environmental Research, 93, 47-55. http://dx.doi.org/10.1016/j.marenvres.2013.06.001
[75]
Klionsky, D.J., Abdalla, F.C., Abeliovich, H., Abraham, R.T., Acevedo-Arozena, A., Adeli, K., et al. (2012) Guidelines for the Use and Interpretation of Assays for Monitoring Autophagy. Autophagy, 8, 445-544.
http://dx.doi.org/10.4161/auto.19496
[76]
Chiarelli, R. and Roccheri, M.C. (2012) Heavy Metals and Metalloids as Autophagy Inducing Agents: Focus on Cadmium and Arsenic. Cells, 1, 597-616. http://dx.doi.org/10.3390/cells1030597
