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Zinc contamination is an underestimated risk to amphibians: toxicity evaluation in tadpoles of Fejervarya limnocharis

    Arabinda Patar Affiliation
    ; Indranil Das Affiliation
    ; Sarbani Giri Affiliation
    ; Anirudha Giri Affiliation

Abstract

Aquatic environments are often contaminated with zinc. Amphibian tadpoles are likely to be exposed to high concentrations of zinc present in these environments. We determined the acute and sub-chronic toxicity of ZnCl2 on Fejervarya limnocharis tadpoles under laboratory conditions. The LC50 values of ZnCl2 were found to be 5.81, 4.32, 3.79 and 3.61 mg/L at 24, 48, 72 and 96 h of exposure respectively. Long-term exposure to sub-lethal concentrations of ZnCl2 induced significant mortality in concentration and time dependent manner. Sub-lethal ZnCl2 exposure significantly altered survival, body length and body weight at metamorphosis. Micronucleus test and comet assay indicated the genotoxic potential of ZnCl2. Significant increase in DNA strand break was observed following ZnCl2 exposure equivalent to 1% of the of 24 h LC50 value. The findings indicate possible adverse to tadpoles inhabiting aquatic environments contaminated with zinc. In addition, the findings may be extrapolated to aquatic organisms of similar torphic status.

Keyword : zinc, Fejervarya limnocharis, genotoxicity, micronucleus, comet assay

How to Cite
Patar, A., Das, I., Giri, S., & Giri, A. (2021). Zinc contamination is an underestimated risk to amphibians: toxicity evaluation in tadpoles of Fejervarya limnocharis. Journal of Environmental Engineering and Landscape Management, 29(4), 489–498. https://doi.org/10.3846/jeelm.2021.15814
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References

Adamu, C., Nganje, T., & Edet, A. (2015). Heavy metal contamination and health risk assessment associated with abandoned barite mines in Cross River State, southeastern Nigeria. Environmental Nanotechnology, Monitoring & Management, 3, 10–21. https://doi.org/10.1016/j.enmm.2014.11.001

Agency for Toxic Substances and Disease Registry. (1990). Toxicological profile for zinc. ATSDR, Atlanta, Georgia, USA.
https://www.atsdr.cdc.gov/toxprofiles/tp60.pdf

Bagdonas, E., & Vosyliene, M. Z. (2006). A study of toxicity and genotoxicity of copper, zinc and their mixture to rainbow trout (Oncorhynchus mykiss). Biologija, 1, 8–13. http://www.elibrary.lt/resursai/LMA/Biologija/Bio_008_013.pdf

Bakar, S., Ashriya, A., Shuib, A., & Razak, S. (2014). Genotoxic effect of zinc and cadmium following single and binary mixture exposures in tilapia (Oreochromis niloticus) using micronucleus test. Sains Malaysiana, 43(7), 1053–1059.

Baldantoni, D., Alfani, A., Di Tommasi, P., Bartoli, G., & De Santo, A. V. (2004). Assessment of macro and microelement accumulation capability of two aquatic plants. Environmental Pollution, 130(2), 149–156. https://doi.org/10.1016/j.envpol.2003.12.015

Bantle, J. A., Fort, D. J., & James, B. L. (1989). Identification of developmental toxicants using the Frog Embryo Teratogenesis Assay-Xenopus (FETAX). In M. Munawar, G. Dixon, C. I. Mayfield, T. Reynoldson, & M. H. Sadar (Eds.), Developments in hydrobiology: Vol. 54. Environmental bioassay techniques and their application (pp. 577–585). Springer. https://doi.org/10.1007/978-94-009-1896-2_59

Banu, B. S., Devi, K. D., Mahboob, M., & Jamil, K. (2001). In vivo genotoxic effect of zinc sulfate in mouse peripheral blood leukocytes using comet assay. Drug and Chemical Toxicology, 24(1), 63–73. https://doi.org/10.1081/DCT-100103086

Beebee, T. J., & Griffiths, R. A. (2005). The amphibian decline crisis: A watershed for conservation biology? Biological Conservation, 125(3), 271–285. https://doi.org/10.1016/j.biocon.2005.04.009

Benoit, D. A., & Holcombe, G. (1978). Toxic effects of zinc on fathead minnows Pimephales promelas in soft water. Journal of Fish Biology, 13(6), 701–708. https://doi.org/10.1111/j.1095-8649.1978.tb03484.x

Bringolf, R. B., Morris, B. A., Boese, C. J., Santore, R. C., Allen, H. E., & Meyer, J. S. (2006). Influence of dissolved organic matter on acute toxicity of zinc to larval fathead minnows (Pimephales promelas). Archives of Environmental Contamination and Toxicology, 51, 438–444. https://doi.org/10.1007/s00244-005-0088-6

Brinkman, S., & Woodling, J. (2005). Zinc toxicity to the mottled sculpin (Cottus bairdt) in high hardness water. Environmental Toxicology and Chemistry, 24(6), 1515–1517. https://doi.org/10.1897/04-235R.1

Brungs, W. A. (1969). Chronic toxicity of zinc to the fathead minnow, Pimephales promelas Rafinesque. Transactions of the American Fisheries Society, 98(2), 272–279. https://doi.org/10.1577/1548-8659(1969)98[272:CTOZTT]2.0.CO;2

Campana, M. A., Panzeri, A. M., Moreno, V. J., & Dulout, F. N. (2003). Micronuclei induction in Rana catesbeiana tadpoles by the pyrethroid insecticide lambda-cyhalothrin. Genetics and Molecular Biology, 26(1), 99–103. https://doi.org/10.1590/S1415-47572003000100016

Clements, C., Ralph, S., & Petras, M. (1997). Genotoxicity of select herbicides in Rana catesbeiana tadpoles using the alkaline single cell gel DNA electrophoresis (comet) assay. Environmental and Molecular Mutagenesis, 29(3), 277-288. https://doi.org/10.1002/(SICI)1098-2280(1997)29:3<277::AID-EM8>3.0.CO;2-9

Dave, G., Damgaard, B., Grande, M., Martelin, J. E., Rosander, B., & Viktor, T. (1987). Ring test of an embryo‐larval toxicity test with zebrafish (brachydanio rerio) using chromium and zinc as toxicants. Environmental Toxicology and Chemistry, 6(1), 61–71. https://doi.org/10.1002/etc.5620060108

Dilling, W. J., & Healey, C. (1926). Influence of lead and the metallic ions of copper, zinc, thorium, beryllium and thallium on the germination of frogs’ spawn and on the growth of tadpoles. Annals of Applied Biology, 13(2), 177–188. https://doi.org/10.1111/j.1744-7348.1926.tb04262.x

Duellman, W., & Trueb, L. (1986). Biology of amphibians. McGraw Hill.

Fenech, M., Chang, W. P., Kirsch-Volders, M., Holland, N., Bonassi, S., & Zeiger, E. (2003). HUMN project: Detailed description of the scoring criteria for the cytokinesis-block micronucleus assay using isolated human lymphocyte cultures. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 534(1–2), 65–75. https://doi.org/10.1016/S1383-5718(02)00249-8

Frenzilli, G., Nigro, M., & Lyons, B. (2009). The Comet assay for the evaluation of genotoxic impact in aquatic environments. Mutation Research/Reviews in Mutation Research, 681(1), 80–92. https://doi.org/10.1016/j.mrrev.2008.03.001

Frieden, E. (1972). The chemical elements of life. Scientific American, 227, 52–64.

Giri, A., Yadav, S. S., Giri, S., & Sharma, G. D. (2012). Effect of predator stress and malathion on tadpoles of Indian skittering frog. Aquatic Toxicology, 106–107, 157–163. https://doi.org/10.1016/j.aquatox.2011.11.008

Gosner, K. L. (1960). A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16(3), 183–190.

Gupta, T., Talukder, G., & Sharma, A. (1991). Cytotoxicity of zinc chloride in mice in vivo. Biological Trace Element Research, 30, 95–101. https://doi.org/10.1007/BF02990346

Haywood, L. K., Alexander, G. J., Byrne, M. J., & Cukrowska, E. (2004). Xenopus laevis embryos and tadpoles as models for testing for pollution by zinc, copper, lead and cadmium. African Zoology, 39(2), 163–174. https://doi.org/10.1080/15627020.2004.11657213

Ho, E., & Ames, B. N. (2002). Low intracellular zinc induces oxidative DNA damage, disrupts p53, NFκB, and AP1 DNA binding, and affects DNA repair in a rat glioma cell line. Proceedings of the National Academy of Sciences, 99(26), 16770–16775. https://doi.org/10.1073/pnas.222679399

Ho, E., Courtemanche, C., & Ames, B. N. (2003). Zinc deficiency induces oxidative DNA damage and increases p53 expression in human lung fibroblasts. The Journal of Nutrition, 133(8), 2543–2548. https://doi.org/10.1093/jn/133.8.2543

Holcombe, G. W., Benoit, D. A., & Leonard, E. N. (1979). Long term effects of zinc exposures on brook trout (Salvelinus fontinalis). Transactions of the American Fisheries Society, 108(1), 76-87. https://doi.org/10.1577/1548-8659(1979)108<76:LEOZEO>2.0.CO;2

Hopkins, W. A., Congdon, J., & Ray, J. K. (2000). Incidence and impact of axial malformations in larval bullfrogs (Rana catesbeiana) developing in sites polluted by a coal‐burning power plant. Environmental Toxicology and Chemistry, 19(4), 862–868. https://doi.org/10.1002/etc.5620190412

Khangarot, B., & Ray, P. (1987). Sensitivity of toad tadpoles, Bufo melanostictus (Schneider), to heavy metals. Bulletin of Environmental Contamination and Toxicology, 38, 523–527. https://doi.org/10.1007/BF01606623

Khangarot, B., Sehgal, A., & Bhasin, M. (1985). “Man and Biosphere” – Studies on the Sikkim Himalayas. Part 5: Acute toxicity of selected heavy metals on the tadpoles of Rana hexadactyla. Acta hydrochimica et hydrobiologica, 13(2), 259–263. https://doi.org/10.1002/aheh.19850130223

Kowalska-Wochna, E., Moniuszko-Jakoniuk, J., Kulikowska, E., & Miniuk, K. (1988). The effect of orally applied aqueous solutions of lead and zinc on chromosome aberrations and induction of sister chromatid exchanges in the rat (Rattus sp.). Genetica Polonica, 29(2), 181–189.

Lajmanovich, R. C., Cabagna, M., Peltzer, P. M., Stringhini, G. A., & Attademo, A. M. (2005). Micronucleus induction in erythrocytes of the Hyla pulchella tadpoles (Amphibia: Hylidae) exposed to insecticide endosulfan. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 587(1–2), 67–72. https://doi.org/10.1016/j.mrgentox.2005.08.001

Lefcort, H., Meguire, R., Wilson, L., & Ettinger, W. (1998). Heavy metals alter the survival, growth, metamorphosis, and antipredatory behavior of Columbia spotted frog (Rana luteiventris) tadpoles. Archives of Environmental Contamination and Toxicology, 35, 447–456.
https://doi.org/10.1007/s002449900401

Leland, H. V. (1983). Ultrastructural changes in the hepatocytes of juvenile rainbow trout and mature brown trout exposed to copper or zinc. Environmental Toxicology and Chemistry, 2(3), 353–368. https://doi.org/10.1002/etc.5620020312

Linder, G., & Grillitsch, B. (2000). Ecotoxicology of metals. In D. W. Sparling, G. Linder, & C. A. Bishop (Eds.), Ecotoxicology of amphibians and reptiles (pp. 325–459). SETAC Press.

Mohiuddin, K., Ogawa, Y., Zakir, H., Otomo, K., & Shikazono, N. (2011). Heavy metals contamination in water and sediments of an urban river in a developing country. International Journal of Environmental Science & Technology, 8, 723–736. https://doi.org/10.1007/BF03326257

Mondal, P., Reichelt-Brushett, A. J., Jonathan, M. P., Sujitha, S. B., & Sarkar, S. K. (2017). Pollution evaluation of total and acid-leachable trace elements in surface sediments of Hooghly River Estuary and Sundarban Mangrove Wetland (India). Environmental Science and Pollution Research, 25(6), 5681–5699. https://doi.org/10.1007/s11356-017-0915-0

Montalvão, M. F., & Malafaia, G. (2017). Effects of abamectin on bullfrog tadpoles: insights on cytotoxicity. Environmental Science and Pollution Research, 24, 23411–23416. https://doi.org/10.1007/s11356-017-0124-x

Mouchet, F. (2002). Validation du test comete sur larves d’amphibiens (xenopus laevis et Pleurodeles Waltl) et application al’évaluation du potentiel génotoxique de sols, sédiments et déchets contaminés. Comparaison avec filetest micronoyau amphibien [These de doctorat de l’Université Paul Sabatier de Toulouse]. Centre de Biologie du Développement.

Mouchet, F., Baudrimont, M., Gonzalez, P., Cuenot, Y., Bourdineaud, J.-P., Boudou, A., & Gauthier, L. (2006). Genotoxic and stress inductive potential of cadmium in Xenopus laevis larvae. Aquatic Toxicology, 78(2), 157–166. https://doi.org/10.1016/j.aquatox.2006.02.029

Mouchet, F., Gauthier, L., Baudrimont, M., Gonzalez, P., Mailhes, C., Ferrier, V., & Devaux, A. (2007). Comparative evaluation of the toxicity and genotoxicity of cadmium in amphibian larvae (Xenopus laevis and Pleurodeles waltl) using the comet assay and the micronucleus test. Environmental Toxicology, 22(4), 422–435. https://doi.org/10.1002/tox.20267

Mouchet, F., Gauthier, L., Mailhes, C., Ferrier, V., & Devaux, A. (2005). Comparative study of the comet assay and the micronucleus test in amphibian larvae (Xenopus laevis) using benzo (a) pyrene, ethyl methanesulfonate, and methyl methanesulfonate: Establishment of a positive control in the amphibian comet assay. Environmental Toxicology, 20(1), 74–84. https://doi.org/10.1002/tox.20080

Muranli, F. D. G., & Güner, U. (2011). Induction of micronuclei and nuclear abnormalities in erythrocytes of mosquito fish (Gambusia affinis) following exposure to the pyrethroid insecticide lambda-cyhalothrin. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 726(2), 104–108. https://doi.org/10.1016/j.mrgentox.2011.05.004

Nzengue, Y., Candéias, S. M., Sauvaigo, S., Douki, T., Favier, A., Rachidi, W., & Guiraud, P. (2011). The toxicity redox mechanisms of cadmium alone or together with copper and zinc homeostasis alteration: its redox biomarkers. Journal of Trace Elements in Medicine and Biology, 25(3), 171–180. https://doi.org/10.1016/j.jtemb.2011.06.002

Obiakor, M., Okonkwo, J., Ezeonyejiaku, C., & Ezenwelu, C. (2010). Genotoxicology: Single and joint action of copper and zinc to Synodontis clarias and Tilapia nilotica. Journal of Applied Sciences and Environmental Management, 14(3), 59–64. https://doi.org/10.4314/jasem.v14i3.61468

Patar, A., Giri, A., Boro, F., Bhuyan, K., Singha, U., & Giri, S. (2016). Cadmium pollution and amphibians–Studies in tadpoles of Rana limnocharis. Chemosphere, 144, 1043–1049. https://doi.org/10.1016/j.chemosphere.2015.09.088

Purushothaman, P., & Chakrapani, G. (2007). Heavy metals fractionation in Ganga River sediments, India. Environmental Monitoring and Assessment, 132, 475–489. https://doi.org/10.1007/s10661-006-9550-9

Rowe, C. L., Kinney, O. M., Nagle, R. D., & Congdon, J. D. (1998). Elevated maintenance costs in an anuran (Rana catesbeiana) exposed to a mixture of trace elements during the embryonic and early larval periods. Physiological and Biochemical Zoology, 71(1), 27–35. https://doi.org/10.1086/515885

Sarkar, S. K., Mondal, P., Biswas, J. K., Kwon, E. E., Ok, Y. S., & Rinklebe, J. (2017). Trace elements in surface sediments of the Hooghly (Ganges) estuary: Distribution and contamination risk assessment. Environmental Geochemistry and Health, 39(6), 1245–1258. https://doi.org/10.1007/s10653-017-9952-3

Shuhaimi-Othman, M., Nadzifah, Y., Umirah, N., & Ahmad, A. (2012). Toxicity of metals to tadpoles of the common Sunda toad, Duttaphrynus melanostictus. Toxicological & Environmental Chemistry, 94(2), 364–376. https://doi.org/10.1080/02772248.2011.640636

Singh, N. P., McCoy, M. T., Tice, R. R., & Schneider, E. L. (1988). A simple technique for quantitation of low levels of DNA damage in individual cells. Experimental Cell Research, 175(1), 184–191. https://doi.org/10.1016/0014-4827(88)90265-0

Singha, U., Pandey, N., Boro, F., Giri, S., Giri, A., & Biswas, S. (2014). Sodium arsenite induced changes in survival, growth, metamorphosis and genotoxicity in the Indian cricket frog (Rana limnocharis). Chemosphere, 112, 333–339. https://doi.org/10.1016/j.chemosphere.2014.04.076

Sinley, J. R., Goettl, J. P., & Davies, P. H. (1974). The effects of zinc on rainbow trout (Salmo gairdneri) in hard and soft water. Bulletin of Environmental Contamination and Toxicology, 12, 193–201. https://doi.org/10.1007/BF01684960

Skidmore, J. (1964). Toxicity of zinc compounds to aquatic animals, with special reference to fish. The Quarterly Review of Biology, 39(3), 227–248. https://doi.org/10.1086/404229

Skordas, K., Kelepertzis, E., Kosmidis, D., Panagiotaki, P., & Vafidis, D. (2015). Assessment of nutrients and heavy metals in the surface sediments of the artificially lake water reservoir Karla, Thessaly, Greece. Environmental Earth Sciences, 73, 4483–4493. https://doi.org/10.1007/s12665-014-3736-1

Sliwinski, T., Czechowska, A., Kolodziejczak, M., Jajte, J., Wisniewska‐Jarosinska, M., & Blasiak, J. (2009). Zinc salts differentially modulate DNA damage in normal and cancer cells. Cell Biology International, 33(4), 542–547. https://doi.org/10.1016/j.cellbi.2009.02.004

Stebler, E. F., Burks, S. L., Bantle, J. A., & Dawson, D. A. (1988). Evaluation of the developmental toxicity of metal‐contaminated sediments using short term fathead minnow and frog embryo larval assays. Environmental Toxicology and Chemistry, 7(1), 27–34. https://doi.org/10.1002/etc.5620070105

Stuart, S. N., Chanson, J. S., Cox, N. A., Young, B. E., Rodrigues, A. S., Fischman, D. L., & Waller, R. W. (2004). Status and trends of amphibian declines and extinctions worldwide. Science, 306(5702), 1783–1786. https://doi.org/10.1126/science.1103538

Svecevičius, G. (1999). Fish avoidance response to heavy metals and their mixtures. Acta Zoologica Lituanica, 9(2), 103–113. https://doi.org/10.1080/13921657.1999.10512293

Tice, R. R., Agurell, E., Anderson, D., Burlinson, B., Hartmann, A., Kobayashi, H., Miyamae, Y., Rojas, E., Ryu, J. C., & Sasaki, Y. (2000). Single cell gel/comet assay: Guidelines for in vitro and in vivo genetic toxicology testing. Environmental and Molecular Mutagenesis, 35(3), 206-221. https://doi.org/10.1002/(SICI)1098-2280(2000)35:3<206::AID-EM8>3.0.CO;2-J

Vilkina, G., Pomerantseva, M., & Ramaĭia, L. (1978). Absence of a mutagenic effect of cadmium and zinc salts in mouse somatic and sex cells. Genetika, 14, 2212–2214.

Vladimirov, V. (1969). Dependence of the embryonic development and viability of the carp on the trace element zinc. Voprosy Ikhtiologii, 9, 687–696.

Voroshilin, S., Plotko, E., Fink, T., & Nikiforova, V. (1978). Cytogenetic effect of inorganic compounds of tungsten, zinc, cadmium and cobalt on animal and human somatic cells. TSitologiia i genetika, 241–243.

Wei, B., & Yang, L. (2010). A review of heavy metal contaminations in urban soils, urban road dusts and agricultural soils from China. Microchemical Journal, 94(2), 99–107. https://doi.org/10.1016/j.microc.2009.09.014

Wei, L., Ding, G., Guo, S., Tong, M., Chen, W., Flanders, J., Shao, W., & Lin, Z. (2015). Toxic effects of three heavy metallic ions on Rana zhenhaiensis tadpoles. Asian Herpetological Research, 6(2), 132–142.

World Health Organization. (2001). International programme on chemical safety (Environmental Health Criteria 221). Geneva.

Xie, H., Holmes, A. L., Young, J. L., Qin, Q., Joyce, K., Pelsue, S. C., Peng, C., Wise, S. S., Jeevarajan, A. S., Wallace, W. T., Hammond, D., & Sr, J. P. W. (2009). Zinc chromate induces chromosome instability and DNA double strand breaks in human lung cells. Toxicology and Applied Pharmacology, 234(3), 293–299. https://doi.org/10.1016/j.taap.2008.10.010

Yadav, S. S., Giri, S., Singha, U., Boro, F., & Giri, A. (2013). Toxic and genotoxic effects of Roundup on tadpoles of the Indian skittering frog (Euflictis cyanophlyctis) in the presence and absence of predator stress. Aquatic Toxicology, 132, 1–8. https://doi.org/10.1016/j.aquatox.2013.01.016

Yulin, W., Hongru, Z., & Lanying, H. (1990). Effects of heavy metals on embryos and larvae of flat fish paralichthys olivaceus [j]. Oceanologia et Limnologia Sinica, 21, 386–392.

Zhang, Y., Wang, Y., Yu, R., Zhang, S., & Wu, Z. (2008). Effects of heavy metals Cd2+, Pb2+ and Zn2+ on DNA damage of loach Misgurnus anguillicaudatus. Frontiers of Biology in China, 3, 50–54. https://doi.org/10.1007/s11515-008-0012-3