EFFECTS OF TEMPERATURE AND METALS (ZINC AND CADMIUM) IN EMBRYONIC STAGE OF Anabas testudineus: AN ALTERNATIVE FRESHWATER FISH EMBRYO TEST IN THE SOUTHEAST ASIA REGION

https://doi.org/10.55230/mabjournal.v51i1.2004

Authors

  • MOHD YUSOFF NURULNADIA Faculty of Science and Marine Environment, Universiti Malaysia Terengganu; Institute of Oceanography and Environment, Universiti Malaysia Terengganu; Ocean Pollution and Ecotoxicology (OPEC) Research Group, Universiti Malaysia Terengganu https://orcid.org/0000-0002-6553-2249
  • BAHAROM MOHAMAD ZAHID Faculty of Science and Marine Environment, Universiti Malaysia Terengganu https://orcid.org/0000-0002-6972-1776
  • MUHAMMAD AZRI SHARIFF Faculty of Science and Marine Environment, Universiti Malaysia Terengganu
  • LOOI YONG CHING Faculty of Science and Marine Environment, Universiti Malaysia Terengganu
  • NAJIHAH MOHAMED Fisheries Research Institute Batu Maung, Penang, Malaysia https://orcid.org/0000-0001-8169-5964

Keywords:

Toxicity, Climbing perch, LC50, abnormality, Bioconcentration factor

Abstract

The fish embryo acute toxicity test (FET) was proposed as a promising alternative to the general practice of fish acute toxicity test (FAT) on living animals. To date, the available information on freshwater fish embryos in Southeast Asia is limited. Hence, this study aims to present preliminary data on the single and combined exposure effects of temperature and metals, including zinc and cadmium, on the embryonic development of Anabas testudineus. Over 80% of the embryos died after 10 hour post-fertilization (hpf) in all cadmium treatments, whereas the same effect was only observed in 49.6 and 146 mg/L of zinc treatment. The optimum temperature for rearing the embryos ranged from 27 to 34°C, with a survival rate greater than 90% was recorded. The combined test of zinc + cadmium showed the additive effect with approximately 80% mortality rate at 12 hpf, while the combination of temperature and cadmium had increased the mortality rate up to 100% at 16 hpf. The temperature was found to elevate the cadmium uptake in the embryos and magnified the concentration higher than the concentration in water.

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

References

Abdul Ghani, M.S.H. 2016. Effect of cadmium on embryonic and larval development of climbing perch, Anabas testudienus (Bloch 1792) (M.Sc). Universiti Malaysia Terengganu.

Agusa, T., Kunito, T., Yasunaga, G. & Iwata, H. 2005. Concentrations of trace elements in marine fish and its risk assessment in Malaysia. Marine Pollution Bulletin, 51(8-12): 896-911. DOI: https://doi.org/10.1016/j.marpolbul.2005.06.007

Alafiatayo, A. A., Lai, K. S., Syahida, A., Mahmood, M. & Shaharuddin, N. A. 2019. Phytochemical evaluation, embryotoxicity, and teratogenic effects of Curcuma longa extract on zebrafish (Danio rerio). Evidence-Based Complementary and Alternative Medicine, (10). DOI: https://doi.org/10.1155/2019/3807207

Al-Rasheed, A., Handool, K.O., Garba, B., Noordin, M.M., Bejo, S.K., Kamal, F.M. & Daud, H.H.M. 2018. Crude extracts of epidermal mucus and epidermis of climbing perch Anabas testudineus and its antibacterial and hemolytic activities. The Egyptian Journal of Aquatic Research, 44(2): 125-129. DOI: https://doi.org/10.1016/j.ejar.2018.06.002

Ansari, S. & Ansari, B.A. 2015. Effects of Heavy Metals on the Embryo and Larvae of Zebrafish, Danio rerio (Cyprinidae). Scholars Academic Journal of Biosciences, 3(1b): 52–56.

Avdesh, A., Chen, M., Martin-Iverson, M.T., Mondal, A., Ong, D., Rainey-Smith, S., Taddei, K., Lardelli, M., Groth, D.M., Verdile, G. & Martins, R.N. 2012. Regular care and maintenance of a zebrafish (Danio rerio) laboratory: an introduction. JoVE (Journal of Visualized Experiments), (69): e4196. DOI: https://doi.org/10.3791/4196

Birge, W.J., Black, J.A. & Westerman, A.G. 1985. Short‐term fish and amphibian embryo‐larval tests for determining the effects of toxicant stress on early life stages and estimating chonic values for single compounds and complex effluents: Complex mixtures. Environmental Toxicology and Chemistry: An International Journal, 4(6): 807-821. DOI: https://doi.org/10.1002/etc.5620040612

Braunbeck, T., Böttcher, M., Hollert, H., Kosmehl, T., Lammer, E., Leist, E., Rudolf, M. & Seitz, N. 2005. Towards an alternative for the acute fish LC50 test in chemical assessment: the fish embryo toxicity test goes multi-species-an update. ALTEX-Alternatives to Animal Experimentation, 22(2); 87-102.

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

Caamal-Monsreal, C., Uriarte, I., Farias, A., Díaz, F., Sánchez, A., Re, D. & Rosas, C. 2016. Effects of temperature on embryo development and metabolism of Octopus maya. Aquaculture, 451: 156-162. DOI: https://doi.org/10.1016/j.aquaculture.2015.09.011

Cao, L., Huang, W., Shan, X., Xiao, Z., Wang, Q. & Dou, S. 2009. Cadmium toxicity to embryonic–larval development and survival in red sea bream Pagrus major. Ecotoxicology and Environmental Safety, 72(7): 1966-1974. DOI: https://doi.org/10.1016/j.ecoenv.2009.06.002

Chahardehi, A.M., Arsad, H. & Lim, V. 2020. Zebrafish as a successful animal model for screening toxicity of medicinal plants. Plants, 9(10): 1–35. DOI: https://doi.org/10.3390/plants9101345

Cheung, C.C.C. & Lam, P.K.S. 1998. Effect of cadmium on the embryos and juveniles of a tropical freshwater snail, Physa acuta (Draparnaud, 1805). Water Science and Technology, 38(7): 263-270. DOI: https://doi.org/10.2166/wst.1998.0300

Damodaran, T., Chear, N.J.Y., Murugaiyah, V., Mordi, M.N. & Ramanathan, S. 2021. Comparative Toxicity Assessment of Kratom Decoction, Mitragynine and Speciociliatine Versus Morphine on Zebrafish (Danio rerio) Embryos. Frontiers in Pharmacology, 2193. DOI: https://doi.org/10.3389/fphar.2021.714918

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 chomium and zinc as toxicants. Environmental Toxicology and Chemistry: An International Journal, 6(1): 61-71. DOI: https://doi.org/10.1002/etc.5620060108

Din, E.N. 2001. German standard methods for the examination of water, waste water and sludge–subanimal testing (group T)–part 6: toxicity to fish. Determination of the non-acute-poisonous effect of waste water to fish eggs by dilution limits (T 6). DIN 38415–6; German Standardization Organization.

Eaton, J.G. 1973. Chonic toxicity of a copper, cadmium and zinc mixture to the fathead minnow (Pimephales promelas rafinesque). Water Research, 7(11): 1723-1736. DOI: https://doi.org/10.1016/0043-1354(73)90140-1

Embry, M.R., Belanger, S.E., Braunbeck, T.A., Galay-Burgos, M., Halder, M., Hinton, D.E., Léonard, M.A., Lillicrap, A., Norberg-King, T. & Whale, G. 2010. The fish embryo toxicity test as an animal alternative method in hazard and risk assessment and scientific research. Aquatic Toxicology, 97(2): 79-87. DOI: https://doi.org/10.1016/j.aquatox.2009.12.008

Fernández, N. & Beiras, R. 2001. Combined toxicity of dissolved mercury with copper, lead and cadmium on embryogenesis and early larval growth of the Paracentrotus lividus sea-urchin. Ecotoxicology, 10(5): 263–271. DOI: https://doi.org/10.1023/A:1016703116830

Gamain, P., Gonzalez, P., Cachot, J., Clérandeau, C., Mazzella, N., Gourves, P. Y. & Morin, B. 2017. Combined effects of temperature and copper and S-metolachlor on embryo-larval development of the Pacific oyster, Crassostrea gigas. Marine Pollution Bulletin, 115(1–2): 201–210. DOI: https://doi.org/10.1016/j.marpolbul.2016.12.018

Hallare, A.V., Factor, P.A., Santos, E.K. & Hollert, H. 2009. Assessing the impact of fish cage culture on Taal Lake (Philippines) water and sediment quality using the zebrafish embryo assay. Philippine Journal of Science, 138(1): 91-104.

Hallare, A.V., Schirling, M., Luckenbach, T., Köhler, H.R. & Triebskorn, R. 2005. Combined effects of temperature and cadmium on developmental parameters and biomarker responses in zebrafish (Danio rerio) embryos. Journal of Thermal Biology, 30(1): 7-17. DOI: https://doi.org/10.1016/j.jtherbio.2004.06.002

Hermsen, S.A., van den Brandhof, E.J., van der Ven, L.T. & Piersma, A.H. 2011. Relative embryotoxicity of two classes of chemicals in a modified zebrafish embryotoxicity test and comparison with their in vivo potencies. Toxicology in Vitro, 25(3): 745-753. DOI: https://doi.org/10.1016/j.tiv.2011.01.005

Huang, W., Cao, L., Shan, X., Xiao, Z., Wang, Q. & Dou, S. 2010. Toxic effects of zinc on the development, growth, and survival of red sea bream Pagrus major embryos and larvae. Archives of Environmental Contamination and Toxicology, 58(1): 140-150. DOI: https://doi.org/10.1007/s00244-009-9348-1

International Organization for Standardization. 2007. Water Quality-Determination of the Acute Toxicity of Waste Water to Zebrafish Eggs (Danio rerio). International Organization for Standardization 15088 [WWW Document]. URL

https://www.iso.org/obp/ui/#iso:std:iso:15088:en (accessed 08.09.21)

Ismail, A. & Yusof, S. 2011. Effect of mercury and cadmium on early life stages of Java medaka (Oryzias javanicus): a potential tropical test fish. Marine Pollution Bulletin, 63(5-12): 347-349. DOI: https://doi.org/10.1016/j.marpolbul.2011.02.014

Kawano, M., Uno, S., Koyama, J., Kokushi, E. & McElroy, A. 2017. Effects of oxygenated polycyclic aromatic hydrocarbons on the early life stages of Japanese medaka. Environmental Science and Pollution Research, 24(36): 27670-27677. DOI: https://doi.org/10.1007/s11356-016-6917-5

Kinth, P., Mahesh, G. & Panwar, Y. 2013. Mapping of zebrafish research: a global outlook. Zebrafish, 10(4): 510-517. DOI: https://doi.org/10.1089/zeb.2012.0854

Kitipaspallop, W., Sillapaprayoon, S., Taepavarapruk, P., Chanchao, C. & Pimtong, W. 2021. Evaluation of developmental and transcriptional effects of α-mangostin on zebrafish embryos. Toxicological & Environmental Chemistry, 1-15. DOI: https://doi.org/10.1080/02772248.2021.1960349

Klüver, N., König, M., Ortmann, J., Massei, R., Paschke, A., Kühne, R. & Scholz, S. 2015. Fish embryo toxicity test: Identification of compounds with weak toxicity and analysis of behavioral effects to improve prediction of acute toxicity for neurotoxic compounds. Environmental Science and Technology, 49(11): 7002–7011. DOI: https://doi.org/10.1021/acs.est.5b01910

Küçükoǧlu, M., Binokay, U.S. & Pekmezekmek, A.B. 2013. The effects of zinc chloride during early embryonic development in zebrafish (Brachydanio rerio). Turkish Journal of Biology, 37(2): 158–164.

Lammer, E., Carr, G.J., Wendler, K., Rawlings, J.M., Belanger, S.E. & Braunbeck, T. 2009. Is the fish embryo toxicity test (FET) with the zebrafish (Danio rerio) a potential alternative for the fish acute toxicity test? Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 149(2): 196-209. DOI: https://doi.org/10.1016/j.cbpc.2008.11.006

Nguyen, L.T. & Janssen, C.R. 2001. Comparative sensitivity of embryo–larval toxicity assays with African catfish (Clarias gariepinus) and zebra fish (Danio rerio). Environmental Toxicology, 16(6): 566-571. DOI: https://doi.org/10.1002/tox.10018

Nurulnadia, M.Y., Koyama, J., Uno, S., Kokushi, E., Bacolod, E.T., Ito, K. & Chuman, Y. 2013. Bioaccumulation of dietary endocrine disrupting chemicals (EDCs) by the polychaete, Perinereis nuntia. Bulletin of Environmental Contamination and Toxicology, 91(4): 372-376. DOI: https://doi.org/10.1007/s00128-013-1073-9

Nurulnadia, M.Y., Nik-Nurasyikin, N.M.A., Ling, K.H., Zahid, B.M., Adiana, G. & Nurlemsha, B.I. (2021). Metal concentrations in fresh and salt-dried anchovy, Encrasicholina devisi, and estimation of target hazard quotient for consumers in Kuala Terengganu. Regional Studies in Marine Science, 41: 101595. DOI: https://doi.org/10.1016/j.rsma.2020.101595

Nurulnadia, M.Y., Noradila, A.B. & Adiana, G. 2020. Turbidity effects of suspended bauxite in embryonic stage of climbing perch (Anabas testudineus) post fertilization. The Egyptian Journal of Aquatic Research, 46(2): 181-186. DOI: https://doi.org/10.1016/j.ejar.2020.02.006

Omar, A.H., Kue, C.S., Dianita, R. & Yu, K.X. 2020. Teratogenic potential of traditional Malaysian vegetables (ulam) in the zebrafish model. British Food Journal, 122(10): 3089-3098. DOI: https://doi.org/10.1108/BFJ-02-2020-0118

Parvin, E., Ahmed, K., Islam, M., Salma, M. & Alamgir, A. 2011. Preliminary Acute Toxicity Bioassays of Lead and Cadmium on Fresh Water Climbing Perch, Anabas testudineus (Bloch). Terrestrial and Aquatic Environmental Toxicology, 5: 55–58.

Pavlaki, M.D., Araújo, M.J., Cardoso, D.N., Silva, A.R.R., Cruz, A., Mendo, S., Soares, A.M., Calado, R. & Loureiro, S. 2016. Ecotoxicity and genotoxicity of cadmium in different marine trophic levels. Environmental Pollution, 215: 203-212. DOI: https://doi.org/10.1016/j.envpol.2016.05.010

Ramli, M.D.B.C., Chong, W.N.C.B.M.R., Hussin, N.H.B., Uzid, M.B.M. & Sanusi, J. 2020. An evaluation of toxicity assessment in zebrafish (Danio rerio) embryo induced by Mitragyna speciosa. International Journal of Medical Toxicology & Legal Medicine, 23(1and2): 31-41. DOI: https://doi.org/10.5958/0974-4614.2020.00007.8

Razak, M.R., Aris, A.Z., Zakaria, N.A.C., Wee, S.Y. & Ismail, N.A.H. 2021. Accumulation and risk assessment of heavy metals employing species sensitivity distributions in Linggi River, Negeri Sembilan, Malaysia. Ecotoxicology and Environmental Safety, 211: 111905. DOI: https://doi.org/10.1016/j.ecoenv.2021.111905

Repolho, T., Baptista, M., Pimentel, M.S., Dionısio, G., Trübenbach, K., Lopes, V.M., Lopes, A.R., Calado, R., Diniz, M. & Rosa, R. 2014. Developmental and physiological challenges of octopus (Octopus vulgaris) early life stages under ocean warming. Journal of Comparative Physiology B. 184: 55–64. DOI: https://doi.org/10.1007/s00360-013-0783-y

Rosli, M.N.R., Samat, S.B., Yasir, M.S. & Yusof, M.F.M. 2018. Analysis of heavy metal accumulation in fish at Terengganu coastal area, Malaysia. Sains Malaysiana, 47(6): 1277–1283. DOI: https://doi.org/10.17576/jsm-2018-4706-24

Schirone, R.C. & Gross, L. 1968. Effect of temperature on early embryological development of the zebra fish, Brachydanio rerio. Journal of Experimental Zoology, 169(1): 43-52. DOI: https://doi.org/10.1002/jez.1401690106

Schulte, C. & Nagel, R. 1994. Testing acute toxicity in the embryo of zebrafish, Brachydanio rerio, as an alternative to the acute fish test: preliminary results. Alternatives to Laboratory Animals, 22(1): 12-19. DOI: https://doi.org/10.1177/026119299402200104

TG236, O.E.C.D. 2013. OECD guidelines for the testing of chemicals section 2: Effects on biotic systems test No 236: fish embryo acute toxicity (FET) test. Organization for Economic Cooperation and Development, Paris, France.

Thitinarongwate, W., Mektrirat, R., Nimlamool, W., Khonsung, P., Pikulkaew, S., Okonogi, S. & Kunanusorn, P. 2021. Phytochemical and Safety Evaluations of Zingiber ottensii Valeton Essential Oil in Zebrafish Embryos and Rats. Toxics, 9(5): 102. DOI: https://doi.org/10.3390/toxics9050102

Thorp, V.J. & Lake, P.S. 1974. Toxicity bioassays of cadmium on selected freshwater invertebrates and the interaction of cadmium and zinc on the freshwater shimp, Paratya tasmaniensis Riek. Marine and Freshwater Research, 25(1): 97-104. DOI: https://doi.org/10.1071/MF9740097

Uriarte, I., Martínez-Montaño, E., Espinoza, V., Rosas, C., Hernández, J. & Farías, A. 2016. Effect of temperature increase on the embryonic development of Patagonian red octopus Enteroctopus megalocyathus in controlled culture. Aquaculture Research, 47(8): 2582–2593. DOI: https://doi.org/10.1111/are.12707

US EPA. 1997. Method 1640: Determination of trace elements in water by preconcentration and inductively coupled plasma-mass spectrometry. Office of Water and Office of Science and Technology. [WWW Document]. URL https://www.epa.gov/sites/production/files/2015-10/documents/method_1640_1997.pdf (accessed 09.08.21)

Van Leeuwen, C.J., Grootelaar, E.M.M. & Niebeek, G. 1990. Fish embryos as teratogenicity screens: a comparison of embryotoxicity between fish and birds. Ecotoxicology and Environmental Safety, 20(1): 42-52. DOI: https://doi.org/10.1016/0147-6513(90)90045-7

Volckaert, F.A., Hellemans, B.A., Galbusera, P., Ollevier, F., Sekkali, B. & Belayew, A. 1994. Replication, expression, and fate of foreign ADN during embryonic and larval development of the African catfish (Clarias gariepinus). Molecular Marine Biology and Biotechnology, 3: 57–69.

Wankanapol, A. & Vera Cruz, E.M. 2020. Investigation of appropriate cryoprotectants to be used in the cryopreservation of Thai walking catfish (Clarias macrocephalus) embryo. International Journal of Agricultural Technology, 16(4):1047-1062.

Williams, N.D. & Holdway, D.A. 2000. The effects of pulse‐exposed cadmium and zinc on embryo hatchability, larval development, and survival of Australian crimson spotted rainbow fish (Melanotaenia fluviatilis). Environmental Toxicology, 15(3): 165-173. DOI: https://doi.org/10.1002/1522-7278(2000)15:3<165::AID-TOX3>3.0.CO;2-Q

Witeska, M., Sarnowski, P., Ługowska, K. & Kowal, E. 2014. The effects of cadmium and copper on embryonic and larval development of ide Leuciscus idus L. Fish Physiology and Biochemistry, 40(1): 151–163. DOI: https://doi.org/10.1007/s10695-013-9832-4

Yulin, W., Hongru, Z. & Lanying, H. 1990. Effects of Heavy Metals on Embryos and Larvae of Flat Fish Paralichthys olivaceus (in Chinese). Oceanologia et Limnologia Sinica, 21(4): 386-392.

Yusoff, N.M., Koyama, J. & Uno, S. 2017. Bioaccumulation of sedimentary endocrine disrupting chemicals (EDCs) by the benthic fish, Pleuronectes yokohamae. Malaysian Journal of Analytical Sciences, 21(3): 535-543. DOI: https://doi.org/10.17576/mjas-2017-2103-03

Yusoff, N.M., Jaafar, S.N., Shazili, N.A.M., Azmi, N.N.N.M. & Hassan, M.S.A. 2018. Assessment of metals concentration in tilapia (Oreochomis sp.) and estimation of daily intake by Malaysian. Malaysian Journal of Analytical Sciences, 22(4): 594-604. DOI: https://doi.org/10.17576/mjas-2018-2204-04

Zhang, H., Cao, H., Meng, Y., Jin, G. & Zhu, M. 2012. The toxicity of cadmium (Cd2+) towards embryos and pro-larva of soldatov's catfish (Silurus soldatovi). Ecotoxicology and Environmental Safety, 80: 258-265. DOI: https://doi.org/10.1016/j.ecoenv.2012.03.013

Published

31-03-2022

How to Cite

NURULNADIA, . M. Y., MOHAMAD ZAHID, B., SHARIFF, M. A., CHING, L. Y., & MOHAMED, N. (2022). EFFECTS OF TEMPERATURE AND METALS (ZINC AND CADMIUM) IN EMBRYONIC STAGE OF Anabas testudineus: AN ALTERNATIVE FRESHWATER FISH EMBRYO TEST IN THE SOUTHEAST ASIA REGION. Malaysian Applied Biology, 51(1), 59–72. https://doi.org/10.55230/mabjournal.v51i1.2004

Issue

Section

Research Articles