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http://dx.doi.org/10.11626/KJEB.2014.32.4.271

Toxic Effects of Aluminium on Freshwater Animals: Review  

Park, Chan Jin (Department of Life Science, College of Natural Sciences, Hanyang University)
Kim, Dae Han (Department of Life Science, College of Natural Sciences, Hanyang University)
Han, Sang Ho (Department of Life Science, College of Natural Sciences, Hanyang University)
Gye, Myung Chan (Department of Life Science, College of Natural Sciences, Hanyang University)
Publication Information
Korean Journal of Environmental Biology / v.32, no.4, 2014 , pp. 271-285 More about this Journal
Abstract
Aluminum flows into the river from the abandoned mine leachate, industrial wastewater, and sewage and is responsible for acute toxicity in aquatic organisms. Recently, the number of reports have indicated the increased toxicity in a variety of aquatic organisms' due to the aluminum toxicity. In this study, we reviewed the toxicity of aluminum on aquatic invertebrates, fishes and amphibians and suggested the guideline for management of aluminum residues in aquatic environment and strategies for aluminum toxicity evaluation. In aquatic animals aluminum complexes evoke gill dysfunction primarily, the cytotoxicity, genotoxicity, oxidative stress, disruption of endocrine function, reproductive success, metabolism and homeostasis. Notably, at environmentally relevant concentration, aluminum complex can alter the hormone levels in fish in acidic condition. Further, since the solubility of aluminum is higher in the acidic and basic conditions, thus it is likely that the toxic effects of aluminum may not only occur in acidic water near the abandoned mines but also in lakes and rivers, where pH is raised by algal bloom.
Keywords
aluminium; aquatic animals; toxicity; endocrine disruption; gill disfunction;
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1 Waring CP, JA Brown, JE Collins and P Prunet. 1996. Plasma prolactin, cortisol, and thyroid responses of the brown trout (Salmo trutta) exposed to lethal and sublethal aluminium in acidic soft waters. Gen. Comp. Endocrinol. 102:377-385.   DOI   ScienceOn
2 Vuorinen PJ, M Keinanen, S Peuranen and C Tigerstedt. 2003. Reproduction, blood and plasma parameters and gill histology of vendace (Coregonus albula L.) in long-term exposure to acidity and aluminum. Ecotoxicol. Environ. Saf. 54:255-276.   DOI   ScienceOn
3 Wallstedt T, F Edberg and H Borg. 2009. Long-term water chemical trends in two Swedish lakes after termination of liming. Sci. Total. Environ. 407:3554-3562.   DOI   ScienceOn
4 Wang D, Y He, J Liang, P Liu and P Zhuang. 2013. Distribution and source analysis of aluminum in rivers near Xi'an City, China. Environ. Monit. Assess. 185:1041-1053.   DOI   ScienceOn
5 Weatherley NS, SJ Ormerod, SP Thomas and RW Edwards. 1988. The response of macroinvertebrates to experimental episodes of low pH with different forms of aluminium, during a natural spate. Hydrobiologia 169:225-232.   DOI
6 Wendelaar B. 1997. The stress response in fish. Physiol. Rev. 77:591-625.
7 WHO. 2010. Aluminium in drinking-water (Background document for preparation of WHO Guidelines for drinking water quality). Geneva, Switzerland: World Health Organization Publications.
8 WHO. 2011. Guidelines for drinking water quality. 4th edn. Geneva, Switzerland: World Health Organization Publications. Available at: http://www.who.int/water_sanitation_health/publications/2011/dwq_guidelines/en/
9 Wilson RW, CM Wood and DF Houlihan. 1996. Growth and protein turnover during acclimation to acid and aluminum in juvenile rainbow trout (Oncorhynchus mykiss). Can. J. Fish. Aquat. Sci. 53:802-811.   DOI   ScienceOn
10 Wilson RW, HL Bergman and CM Wood. 1994. Metabolic costs and physiological consequences of acclimation to aluminum in juvenile rainbow trout (Oncorhynchus mykiss). I. Acclimation specificity, resting physiology, feeding and growth. Can. J. Fish. Aquat. Sci. 51:527-535.   DOI   ScienceOn
11 Wilson RW. 1996. Physiological and metabolic costs of acclimation to chronic sublethal acid and aluminium exposure in rainbow trout. pp. 143-167. Toxicology of Aquatic Pollution. Physiological, molecular and cellular approaches (Taylor EW ed.). Cambridge University Publisher, New York.
12 Witters H, JHD Vangenechten, S Van Puymbroeck and OLJ Vanderborght. 1984. Interference of aluminium and pH on the Na-lnflux in an aquatic insect Corixa punctata (lllig.). Environ. Contam. Toxicol. 32:575-579   DOI
13 Witters HE. 1986. Acute acid exposure of rainbow trout Salmo gairdneri Richardson; effects of aluminimun and calcium on ion balance and haematology. Aquat. Toxicol. 8:197-210.   DOI
14 Zhu YZ, DW Liu, ZY Liu and YF Li. 2013. Impact of aluminum exposure on the immune system: a mini review. Environ. Toxicol. Pharmacol. 35:82-87.   DOI   ScienceOn
15 Brady LD and RA Griffiths. 1995. Effects of pH and aluminium on the growth and feeding behaviour of smooth and palmate newt larvae. Ecotoxicology 4:299-306.   DOI   ScienceOn
16 Allin CJ and RW Wilson. 1999. Behavioural and metabolic effects of chronic exposure to sublethal aluminum in acidic soft water in juvenile rainbow trout (Oncorhynchus mykiss). Can. J. Fish. Aquat. Sci. 56:670-678.   DOI
17 Allin CJ and RW Wilson. 2000. Effects of pre-acclimation to aluminium on the physiology and swimming behaviour of juvenile rainbow trout (Oncorhynchus mykiss) during a pulsed exposure. Aquat. Toxicol. 51:213-224.   DOI   ScienceOn
18 Booth CE, DG McDonald, BP Simons and CM Wood. 1988. Effects of Aluminum and Low pH on Net Ion Fluxes and Ion Balance in the Brook Trout (Salvelinus fontinalis). Can. J. Fish. Aquat. Sci. 45:1563-1574.   DOI
19 Brodeur JC, F Okland, B Finstad, DG Dixon and RS Scott McKinley. 2001. Effects of subchronic exposure to aluminium in acidic water on bioenergetics of Atlantic salmon (Salmo salar). Ecotoxicol. Environ. Saf. 49:226-234.   DOI   ScienceOn
20 Camargo MM, MN Fernandes and CB Martinez. 2009. How aluminium exposure promotes osmoregulatory disturbances in the neotropical freshwater fish Prochilus lineatus. Aquat. Toxicol. 94:40-46.   DOI   ScienceOn
21 Camilleri C, SJ Markich, BN Noller, CJ Turley, G Parker and DRA Van. 2003. Silica reduces the toxicity of aluminium to a tropical freshwater fish (Mogurnda mogurnda). Chemosphere 50:355-364.   DOI   ScienceOn
22 Correa M, RA Coler and CM Yin. 1985. Changes in oxygen consumption and nitrogen metabolism in the dragonfly Somatochlora cingulata exposed to aluminum in acid waters. Hydrobiologia 121:151-156.   DOI
23 Campbell PGC, HJ Hansen, B Dubreuil and WO Nelson. 1992. Geochemistry of Quebec North Shore salmon rivers during snowmelt: organic acid pulse and aluminum mobilization. Can. J. Fish. Aquat. Sci. 49:1938-1952.   DOI
24 Campbell PGC and PM Stokes. 1985. Acidification and toxicity of metals to aquatic biota. Can. J. Fish. Aquat. Sci. 42:2034-2049.   DOI
25 Choi SG, SG Park, PK Lee and CS Kim. 2004. An overview of geoenvironmental implications of mineral deposits in Korea. Econ. Environ. Geol. 37:1-19.
26 Correia TG, AM Narcizo, A Bianchini and RG Moreira. 2010. Aluminum as an endocrine disruptor in female Nile tilapia (Oreochromis niloticus). Comp. Biochem. Physiol. C Toxicol. Pharmacol. 151:461-466.   DOI   ScienceOn
27 Cummins CP. 1986. Effects of aluminium and low pH on growth and development in Rana temporaria tadpoles. Oecologia 69:248-252.   DOI
28 Driscoll CT and KM Postek. 1996. The chemistry of aluminum in surface waters. pp. 363-418. In the environmental chemistry of aluminum (Sposito G ed.). CRC Press. London.
29 Driscoll CT and WD Schecher. 1990. The chemistry of aluminum in the environment. J. Environ. Perspect. Health 12:28-49.
30 Erdogan S, G Lououlu, KT Ozgunen and T Ozgunen. 2001. Effects of $Cd^{2+}$, $Zn^{2+}$, $Li^+$ and $Al^{3+}$ on the Fertilization-Induced Membrane Potential Changes in the Egg of the Frog Rana cameranoi. Turk. J. Biol. 25:277-289.
31 Guzman FT, FJ Gonzalez and RR Martinez. 2010. Implementing Lecane quadridentata acute toxicity tests to assess the toxic effects of selected metals (Al, Fe and Zn). Ecotoxicol. Environ. Saf. 73:287-295.   DOI   ScienceOn
32 Farag AM, DF Woodward, EE Little, B Steadman and FA Vertucci. 1993. The effects of low pH and elevated aluminum on Yellowstone cutthroat trout (Oncorhynchus clarki bouvieri). Environ. Toxicol. Chem. 12:719-731.
33 Fernandez-Davila ML, AC Razo-Estrada, S Garcia-Medina, LM Gomez-Olivan, MJ Pinon-Lopez, RG Ibarra and M Galar-Martinez. 2012. Aluminum-induced oxidative stress and neurotoxicity in grass carp (Cyprinidae-Ctenopharingodon idella). Ecotoxicol. Environ. Saf. 76:87-92.   DOI   ScienceOn
34 Garcia-Medina S, AC Razo-Estrada, LM Gomez-Olivan, A Amaya-Chavez, E Madrigal-Bujaidar and M Galar-Martinez. 2010. Aluminum-induced oxidative stress in lymphocytes of common carp (Cyprinus carpio). Fish Physiol. Biochem. 36:875-882.   DOI
35 Garcia-Medina S, C Razo-Estrada, M Galar-Martinez, E Cortez-Barberena, LM Gomez-Olivan, I Alvarez-Gonzalez and E Madrigal-Bujaidar. 2011. Genotoxic and cytotoxic effects induced by aluminum in the lymphocytes of the common carp (Cyprinus carpio). Comp. Biochem. Physiol. C. Toxicol. Pharmacol. 153:113-118.   DOI   ScienceOn
36 Genthe B, WJ Le Roux, K Schachtschneider, PJ Oberholster, NH Aneck-Hahn and J Chamier. 2013. Health risk implications from simultaneous exposure to multiple environmental contaminants. Ecotoxicol. Environ. Saf. 93:171-179.   DOI   ScienceOn
37 Griffitt RJ, J Luo, J Gao, JC Bonzongo and DS Barber. 2008. Effects of particle composition and species on toxicity of metallic nanomaterials in aquatic organisms. Environ. Toxicol. Chem. 27:1972-1778.   DOI   ScienceOn
38 Herrmann J and KG Andersson. 1987. Aluminium Impact on Respiration of Lotic Mayflies at Low pH. Acidic. Precipitation. 703-709.
39 Hutchinson NJ and JB Sprague. 1987. Reduced lethality of Al, Zn and Cu mixtures to American flagfish by complexation with humic substances in acidified soft waters. Environ. Toxicol. Chem. 6:755-765.   DOI
40 Hwang UG, N Kagawa and Y Mugiya. 2000. Aluminium and cadmium inhibit vitellogenin and its mRNA induction by estradiol-17 beta in the primary culture of hepatocytes in the rainbow trout Oncorhynchus mykiss. Gen. Comp. Endocrinol. 119:69-76.   DOI   ScienceOn
41 Jung MC, MY Jung and YW Choi. 2004. Environmental assessment of heavy metals around abandoned metalliferous mine in Korea. Econ. Environ. Geol. 37:21-33.
42 Kendall RJ and RL Dickerson. 1996. Principles and processes for evaluating endocrine disruption in wildlife. Environ. Toxicol. Chem. 25:1253-1254.
43 Kim HJ, JE Yang, YS Ok, JY Lee, BK Park, SH Kong and SH Jun. 2005. Assessment of water pollution by discharge of abandoned mines. J. Soil Groundw. Environ. 10:25-36.
44 Kim JJ and SJ Kim. 2002. Variations in geochemical characteristics of the acid mine drainages due to mineralwater interactions in Donghae mine area in Taebaek, Korea. J. Econ. Env. Geol. 35:55-66.
45 Kim JJ, SJ Kim and YY Kim. 2003. Mineralogy of evapration residues and geochemistry of acid mine drainage in the Donghae mine area. J. Econ. Env. Geol. 36:103-109.
46 Kroglund F, HC Teien, BO Rosseland, B Albu and ECHE Lucassen. 2001. Water Quality Dependent Recovery from Aluminum Stress in Atlantic Salmon Smolt. Water Air Soil Pollut. 130:911-916.   DOI   ScienceOn
47 Kim JK, SH Lee, HH Bang and SO Hwang. 2009. Characteristics of Algae Occurrence in Lake Paldang. J. Kor. Soc. Environ. Eng. 31:325-331.
48 Kim KH, JP Susaya, CG Park, JH Uhm and J Hur. 2013. Comprehensive monitoring of drinking well water quality in Seoul metropolitan city, Korea. Environ. Monit. Assess. 185:6353-6378.   DOI   ScienceOn
49 Kram P, J Hruska, C Driscoll and CE Johnson. 1995. Biogeochemistry of aluminum in a forest catchment in the Czech Republic impacted by atmospheric inputs of strong acids. Water Air Soil Pollut. 85:1831-1836.   DOI
50 Kullberg A, KH Bishop, A Hargeby, M Jansson and RC Peterson. 1993. The ecological significance of dissolved organic carbon in acidified waters. Ambio 22:331-337.
51 McCahon CP and D Pascoe. 1989. Short-term experimental acidification of a Welsh stream: toxicity of different forms of aluminium at low pH to fish and invertebrates. Arch. Environ. Contam. Toxicol. 18:233-242.   DOI
52 Laurent P and SF Perry. 1991. Environmental effects on fish gill morphology. Physiol. Zool. 64:4-25.
53 Lee IG and SH Choi. 2008. Characteristics of stream and soil contamination from the tailing disposal and waste rocks at the abandoned Uljin Mine. Econ. Environ. Geol. 41:63-79.
54 Mazeaud MM, F Mazeaud and EM Donaldson. 1977. Primary and secondary effects of stress in fish: some new data with a general review. T. Am. Fish. Soc. 106:201-212.   DOI
55 McGleenon BM, KB Dynan and AP Passmore. 1999. Acetylcholinesterase inhibitors in Alzheimer's disease. Brit. J. Clin. Pharmaco. 48:471-480.
56 Monette MY and SD McCormick. 2008. Impacts of short-term acid and aluminum exposure on Atlantic salmon (Salmo salar) physiology: a direct comparison of parr and smolts. Aquat. Toxicol. 86:216-226.   DOI   ScienceOn
57 Mount DR, CG Ingersoll, DD Gulley, JD Fernandez, TW LaPoint and HL Bergman. 1988b. Effect of long-term exposure to acid, aluminum and low calcium on adult brook trout (Salvelinus fontinalis). 1. Survival, growth, fecundity and progeny survival. Can. J. Fish. Aquat. Sci. 45:1623-1632.   DOI
58 Nilsen TO, LO Ebbesson, OG Kverneland, F Kroglund, B Finstad and SO Stefansson. 2010. Effects of acidic water and aluminum exposure on gill Na(+), K(+)-ATPase alpha-subunit isoforms, enzyme activity, physiology and return rates in Atlantic salmon (Salmo salar L.). Aquat. Toxicol. 97:250-259.   DOI   ScienceOn
59 Mount DR, JR Hockett and WA Gern. 1988a. Effect of longterm exposure to acid, aluminum and low calcium on adult brook trout (Salvelinus fontinalis). 2. Vitellogenesis and osmoregulation. Can. J. Fish. Aquat. Sci. 45:1633-1642.   DOI
60 Mugiya Y and A Tanahashi. 1998. Inhibitory effects of aluminium on vitellogenin induction by estradiol-17 beta in the primary culture of hepatocytes in the rainbow trout Oncorhynchus mykiss. Gen. Comp. Endocrinol. 109:37-43.   DOI   ScienceOn
61 Pereira S, I Cavalie, V Camilleri, R Gilbin and C Adam-Guillermin. 2013. Comparative genotoxicity of aluminium and cadmium in embryonic zebrafish cells. Mutat. Res. 750:19-26.   DOI   ScienceOn
62 Neville CM. 1985. Physiological response of juvenile rainbow trout, Salmo gairdneri, to acid and aluminium-prediction of field. Can. J. Fish Aquat Sci. 42:2004-2019.   DOI
63 Olaniran AO, K Naicker and B Pillay. 2014. Assessment of physico-chemical qualities and heavy metal concentrations of Umgeni and Umdloti Rivers in Durban, South Africa. Environ. Monit. Assess. 186:2629-2639.   DOI   ScienceOn
64 Parent L, MR Twiss and PGC Campbell. 1996. Influences of natural dissolved organic matter on the interaction of aluminum with the microalga Chlorella: a test of the free-ion model of trace metal toxicity. Environ. Sci. Technol. 30:1713-1720.   DOI   ScienceOn
65 Poleo AB, K OStbye, SA Oxnevad, RA Andersen, E Heibo and LA Vollestad. 1997. Toxicity of acid aluminium-rich water to seven freshwater fish species: a comparative laboratory study. Environ. Pollut. 96:129-139.   DOI   ScienceOn
66 Rengel Z. 2004. Aluminum cycling in the soil-plant-animal-human continuum. Biometals 17:669-689.   DOI   ScienceOn
67 Ryu DC, EY Bae, SG Kim, HJ Son, MJ Song and YJ Kim. 2000. Application of sulfuric acid for improving coagulation efficiency on the down stream of Nakdong River. J. Kor. Soc. Environ. Eng. 22:2059-2065.
68 Sayer MD, JP Reader and R Morris. 1991. Effects of six trace metals on calcium fluxes in brown trout (Salmo trutta L.) in soft water. J. Comp. Physiol. B 161:537-542.
69 Schindler DW. 1988. Effect of acid rain on freshwater ecosystems. Science 239:149-157.   DOI   ScienceOn
70 Shuhaimi-Othman M, N Yakub, NS Umirah and A Abas. 2011b. Toxicity of eight metals to Malaysian freshwater midge larvae Chironomus javanus (Diptera, Chironomidae). Toxicol. Ind. Health. 27:879-886.   DOI   ScienceOn
71 Senger MR, KJ Seibt, GC Ghisleni, RD Dias, MR Bogo and CD Bonan. 2011. Aluminum exposure alters behavioral parameters and increases acetylcholinesterase activity in zebrafish (Danio rerio) brain. Cell. Biol. Toxicol. 27:199-205.   DOI
72 Shuhaimi-Othman M, Y Nadzifah, R Nur-Amalina and NS Umirah. 2012b. Deriving freshwater quality criteria for iron, lead, nickel, and zinc for protection of aquatic life in Malaysia. Scientific World Journal 2012:861576.
73 Shuhaimi-Othman M, N Yakub, NA Ramle and A Abas. 2011a. Toxicity of Metals to a Freshwater Ostracod Stenocypris major. J. Toxicol. 2011:136104.
74 Shuhaimi-Othman M, N Yakub, NA Ramle and A Abas. 2013. Comparative toxicity of eight metals on freshwater fish. Toxicol. Ind. Health. Epub ahead of print.
75 Shuhaimi-Othman M, R Nur-Amalina and Y Nadzifah. 2012a. Toxicity of metals to a freshwater snail, Melanoides tuber-culata. Scientific World Journal 2012:125785.
76 Staurnes M, T Sigholt and OB Reite. 1984. Reduced carbonic anhydrase and Na -K-ATPase activity in gills of salmonids exposed to aluminium-containing acid water. Experientia 40:226-227.   DOI   ScienceOn
77 Taghizadeh V, MR Imanpoor, M Hosseinzadeh and H Azarin. 2013. Effects of acidic water in combination with aluminum on swimming behavior and survival of yolk-sac larval in Goldfish (Carassius auratus gibelio). Springerplus 2:190.   DOI   ScienceOn
78 Tam WH, JN Fryer, I Ali, MR Allaire and B Valentin. 1988. Growth inhibition, gluconeogen esis, and morphometric studies of the pituitary and interrenal cells of acid-stressed brook trout (Salvelinus fontinalis). Can. J. Fish. Aquat. Sci. 45:1197-1211.   DOI
79 Taylor HE, RC Antweiler, DA RothA, CN Alpers and P Dileanis. 2012. Selected trace elements in the Sacramento River, California: occurrence and distribution. Arch. Environ. Contam. Toxicol. 62:557-569.   DOI   ScienceOn
80 Verstraeten SV, L Aimo and PI Oteiza. 2008. Aluminum and lead: molecular mechanisms of brain toxicity. Arch. Toxicol. 82:789-802.   DOI   ScienceOn
81 Vieira VA, TG Correia and RG Moreira. 2013. Effects of aluminum on the energetic substrates in neotropical freshwater Astyanax bimaculatus (Teleostei: Characidae) females. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 157:1-8.   DOI   ScienceOn