Preliminary Histological Investigation of East Asian Bullfrog (Hoplobatrachus rugulosus) Tadpoles Exposed to Potassium Chlorate

Main Article Content

Wararut Buncharoen
Monruedee Chaiyapo
Supap Saenphet
Athibeth Buajai
Phornphan Phrompanya
Kanokporn Saenphet

Abstract

Potassium chlorate has been used widely in northern Thailand to induce off-season flowering of longan trees. Therefore, it is highly possible that potassium chlorate could contaminate the surrounding waters. Although adverse effects of agrochemicals on the aquatic vertebrates are well documented, the exploration of histopathological changes under potassium chlorate toxic effects on amphibians is limited. The present study aimed to histopathologically investigate the effect of potassium chlorate on the kidney, liver, and gonad of east Asian bullfrog Hoplobatrachus rugulosus larvae. The 3-day-old tadpoles were divided into 0.1, 0.5, 1.0, and 1.5 ppm exposure groups to potassium chlorate for 24 weeks. Larval samplings were conducted for histopathological examination in pro- and complete- metamorphic stages. The histopathological changes of all investigated organs were observed in potassium chlorate treated groups, especially at the high concentrations (1.0 and 1.5 ppm). Kidney tissues showed glomerular shrinkage together with congestion, while vacuolization and degeneration of hepatocytes, expanded sinusoidal spaces, and leukocyte infiltration were found in the liver. Moreover, atretic oocytes and karyorrhexis were recognized in the ovary. Our results suggested that the use of potassium chlorate at high concentrations adversely affected vital organs of H. rugulosus tadpoles and might lead to the decline of the amphibian population.

Article Details

How to Cite
(1)
Buncharoen, W.; Chaiyapo, M.; Saenphet, S. .; Buajai, A.; Phrompanya, P.; Saenphet, K. Preliminary Histological Investigation of East Asian Bullfrog (Hoplobatrachus Rugulosus) Tadpoles Exposed to Potassium Chlorate. Microsc. Microanal. Res. 2022, 35, 38-45.
Section
Original Articles

References

N. Hasachoo, P. Kalaya, Competitiveness of local agriculture: case of longan fruit trade between China and the north of Thailand, Les Notes de l’Irasec n°15 - Irasec’s Discussion Papers, Vol. 15, 1-19 (2013).

R. Janthasri, S. Subhadrabandhu, L. Janthasri, Methods of producing off-season longan in Thailand, J. Sci. Tech. UBU, Vol. 7(2) (2005).

T.K. Matsumoto, M.A. Nagao, B. Mackey, Off-season flower induction of longan with potassium chlorate, sodium chlorite, and sodium hypochlorite, HortTechnology, Vol. 17(3), 296-300 (2007).

L. Chit-aree, P. Suwannawong, P. Somboonchai, F.B. Matta, W. Prathumyot, Effect of potassium chlorate combined with paclobutrazol, monopotassium phosphate and mepiquat chloride on fruit quality of longan (Dimocarpus longan), Int. J. Agric. Technol., Vol. 15(2), 241-248 (2019).

C.M. Couillard, R.W. Macdonald, S.C. Courtenay, V.P. Palace, Chemical-environment interactions affecting the risk of impacts on aquatic organisms: A review with a Canadian perspective-interactions affecting exposure, Environ. Rev., Vol. 16, 1-17 (2008).

S. Schäfer, G. Buchmeier, E. Claus, L. Duester, P. Heininger, A. Körner, P. Mayer, A. Paschke, C. Rauert, G. Reifferscheid, H. Rüdel, C. Schlechtriem, C. Schröter-Kermani, D. Schudoma, F. Smedes, D. Steffen, F. Vietoris, Bioaccumulation in aquatic systems: methodological approaches, monitoring and assessment, Environ. Sci. Eur., Vol. 27, 5 (2015).

I. Bashir, F.A. Lone, R.A. Bhat, S.A. Mir, Z.A. Dar, S.A. Dar, Concerns and threats of contamination on aquatic ecosystems, Bioremediation and Biotechnology, K.R. Hakeem, R.A. Bhat, H. Quadri (eds.), Springer Nature, 1-26 (2020)

J.E. Tiege, G.W. Holcombe, K.M. Flynn, P.A. Kosian, J.J. Korte, L.E. Anderson, D.C. Wolf, S.J. Degitz, Metamorphic inhibition of Xenopus laevis by sodium perchlorate: effects on development and thyroid histology, Environ. Toxicol. Chem., Vol. 24(4), 926-933 (2005).

F. Liu, G.P. Cobb, T.A. Anderson, Q. Cheng, C.W. Theodorakis, Uptake, accumulation and depuration of sodium perchlorate and sodium arsenate in zebrafish (Danio rerio), Chemosphere, Vol. 65, 1679-1689 (2006).

E. Bulaeva, C. Lanctôt, L. Reynolds, V.L. Trudeau, L. Navarro-Martín, Sodium perchlorate disrupts evelopment and affects metamorphosis- and growth-related gene expression in tadpoles of the wood frog (Lithobates sylvaticus), Gen. Comp. Endocrinol., Vol. 222, 33-43 (2015).

C.G. Furin, F.A. von Hippel, J.H. Postlethwait, C.L. Buck, W.A. Cresko, T.M. O’Hara, Developmental timing of sodium perchlorate exposure alters angiogenesis, thyroid follicle proliferation and sexual maturation in stickleback, Gen. Comp. Endocrinol., Vol. 219, 24-35 (2015).

R. Zheng, R. Liu, M. Wu, H. Wang, L. Xie, Effects of sodium perchlorate and exogenous L-thyroxine on growth, development and leptin signaling pathway of Bufo gargarizans tadpoles during metamorphosis, Ecotoxicol. Environ. Saf., Vol. 206, 111410 (2020).

L.A. Miranda, A. Pisanó, V. Casco, Ultrastructural study on thyroid glands of Bufo arenarum larvae kept in potassium perchlorate solution, Biocell., Vol. 20(2), 147-53 (1996).

F. Schmidt, S. Schnurr, R. Wolf, T. Braunbeck, Effects of the anti-thyroidal compound potassium perchlorate on the thyroid system of the zebrafish, Aquat. Toxicol., Vol. 109, 47-58 (2012).

M.A. Nagao, E.B. Ho-a, Stimulating longan flowering in Hawaii with potassium chlorate, J. Hawaiian Pacific Agric., Vol. 11, 23-27 (2000).

W. Singhagun, T. Pankasemsuk, Effect of potassium chlorate in combination with paclobutrazol on flowering of lychee cv., J. Agri., Vol. 23(1), 1–9 (2007).

P. Manochai, T. Jaroenkit, S. Ussahatanonta, S. Ongprasert, B. Kativat, Seasonal effect of potassium chlorate on flowering and yield of longan (Dimocarpus longan) Lour., Acta Hortic., Vol. 863, 363-366 (2010).

N. Somboonkaew, L.A. Terry, Health-promoting properties of fruits and vegetables, L.A. Terry (ed.), CABI, Oxfordshire, 400 pp. (2011).

N. Nahar, M.S.H. Choudhury, M.A. Rahim, Effects of KCLO3, KNO3, and urea on the flowering and fruiting of mango and longan, J. Agrofor. Environ., Vol. 4(1), 31-34 (2010).

S. Jeenkajon, S. Ruamrungsri, Effect of potassium chlorate on growth, flowering and nitrogen concentration in leaf of Phalaenopsis orchid hybrid, Thai J. Bot., Vol. 6, 157-163 (2014).

S. Thitithanakul, S. Choengthong, Effects of potassium chlorate (KCLO3), potassium nitrate (KNO3), and Thiourea on bud break in Rambutan (Nephelium lappaceum L.) cv. RongRien, Khon Khaen Agr. J., Vol. 42 (suppl.3), 25-31 (2014).

S. Huang, D. Han, J. Wang, D. Gua, J. Li, Floral induction of longan (Dimocarpus longan) by potassium chlorate: application, mechanism, and future perspectives, Front. Plant. Sci., Vol. 12, 670587 (2021).

S. Ongprasert, P. Sutikool, S. Aumtong, The impact of application of chlorates in longan plantations on the environment and the remedy, 17th World Congress of Soil Science, Symposium, 14-21 August 2002, Bangkok, Thailand, 1191 (2002).

A. Diesmos, P.P. van Dijk, R. Inger, D. Iskandar, M. Wai, N. Lau, E. Zhao, S. Lu, B. Geng, K. Lue, Z. Yuan, H. Gu, H. Shi, W. Chou, Hoplobatrachus rugulosus, IUCN Red List of Threatened Species 2004, e.T58300A11760194 (2004).

A. Venturino, E. Rosenbaum, A. Caballero de Castro, O.L. Anguiano, L. Gauna, T. Fonovich, de Schroeder, A.M. Pechen de D’Angelo, Biomarkers of effect in toads and frogs, Biomarkers, Vol. 8 (3-4), 167-186 (2003).

S.R. de Solla, K.E. Pettit, C.A. Bishop, K.M. Cheng, J.E. Elliott, Effects of agricultural runoff on native amphibians in the lower Fraser river valley, British Columbia, Canada, Environ. Toxicol. Chem., Vol. 21(2), 353-360, (2002).

A. Egea-Serrano, R.A. Relyea, M. Tejedo, M. Torralva, Understanding of the impact of chemicals on amphibians: a meta-analytic review, Ecol. Evol., Vol. 2(7), 1382-1397 (2012).

C. Pinelli, A. Santillo, G.C. Baccari, S. Flavo, M.M. Di Fiore, Effects of chemical pollutants on reproductive and developmental processes in Italian amphibians, Mol. Reprod. Dev., Vol. 86, 1324-1332 (2019).

P. Sanchanta, Effects of chitosan and cypermethrin on metamorphosis and microanatomy of kidney in East Asian bullfrog (Hoplobatrachus rugulosus) larvae, Thesis of Master Degree (Teaching Biology), Chiang Mai University, 100 pp. (2014).

W. Trachantong, S. Saenphet, K. Saenphet, M. Chaiyapo, Lethal and sublethal effects of a methomyl-based insecticide in Hoplobatrachus rugulosus. J. Toxicol. Pathol., Vol. 30, 15-24 (2017).

Ö. Çakıcı, Histopathologic changes in liver and kidney tissues induced by carbary in Bufotes variabilis (Anura: Bufonidae), Exp. Toxicol. Pathol. Vol. 67, 237-243 (2015).

A. Păunescu, C.M. Ponepal, V.T. Grigorean, M. Popescu, Histopathological changes in the liver and kidney tissues of marsh frog (Pelophylax ridibundus) induced by the action of Talstar 10EC insecticide, Anlale Univer. din Oradea - Fasc. Biol., Vol. 19 (1), 5-10 (2012).

A. Riaz, M. Majeed, M. A. Riaz, A. Iqbal, U.A. Ashfaq, Histopathological alteration in organs of adult male frog after exposure to alpha-cypermethrin, Pure Appl. Biol., Vol. 11 (1), 175-180 (2022).

L. Sena, J.A. Johnson, P. Nkomozepi, E.F. Mbajiorgu, Atrazine-induced hepato-renal toxicity in adult male Xenopus laevis frogs, Appl. Sci., Vol. 11, 11776 (2021).

I. Bernabò, A. Guardia, R. Macirella, S. Tripepi, E. Brunelli, Chronic exposures to fungicide pyrimethanil: multi-organ effects on Italian tree frog (Hyla intermedia), Sci. Rep., Vol. 7, 6869, (2017).

J. Kitana, O. Achayapunwanich, P. Thammachoti, M. S. Othman, W. Khonsue, N. Kitana, Cadmium contamination and health assessment in frog Microhyla fissipes living downstream of zinc mining area in Thailand, EnviromentAsia, Vol. 8(1), 16-23 (2015).

A. Capaldo, F. Gay, R. Scudiero, F. Trinchella, I. Caputo, M. Lepretti, A. Marabotti, C. Esposito, V. Laforgia, Histological changes, apoptosis and metallothionein levels in Triturus carnifex (Amphibia, Urodela) exposed to environmental cadmium concentrations. Aquat. Toxicol., Vol. 173, 63-73 (2016).

M.F. Medina, M.E. González, S.M.R. Klyver, I.M.A. Odstrcil, Histopathological and biochemical changes in the liver, kidney, and blood of amphibians intoxicated with cadmium, Turk. J. Biol., Vol. 40, 229-238 (2016).

C. Fenoglio, F. Albicini, G. Milanesi, S. Barni, Response of renal parenchyma and interstitium of Rana snk. esculenta to environmental pollution, Ecotoxicol. Environ. Saf., Vol. 74, 1381-1390 (2011).

U. A. Jayawardena, P. Angunawela, D. D. Wickramasinghe, W. D. Ratnasooriya, P. V. Udagama, Heavy metal-induced toxicity in the Indian green frog: Biochemical and histopathological alterations, Environ. Toxicol. Chem., Vol. 36 (10), 2855-2867 (2017).

W. Pffaler, G. Gstraunthaler, Nephrotoxicity testing in vitro-What we know and what we need to know, Environ. Health Perspect., Vol. 106, 559-569 (1998)

T.R. Van Vleet and R.G. Schnellmann, Toxic nephropathy: environmental chemicals, Semin. Nephrol., Vol. 23(5), 500-508 (2003)

R.E. Dudley, L.M. Gammal, C.D. Klassen, Cadmium-induced hepatic and renal injury in chronically exposed rats: likely role of hepatic cadmium-metallothionein in nephrotoxicity, Toxicol. Appl. Pharmacol., Vol. 77, 414-426 (1985).

N. Khalid, M. Azimpouran, Necrosis, StatPearls, Treasure Islands (2022).

L.M. Curi, P. M. Peltzer, Alterations in gonads and liver tissue in two neotropical anuran species commonly occuring in rice fields crops, Water Air Soil Pollut., Vol. 232, 203 (2021).

A. Figueiredo-Fernandes, A. Fontainhas-Fernandes, E. Rocha, M. A. Reis-Henriques, The effect of paraquat on hepatic EROD activity, liver, and gonadal histology in males and females of Nile tilapia, Oreochromis niloticus, exposed at different temperatures, Arch. Environ. Contam. Toxicol., Vol, 51, 626-632 (2006).

M.O. Olufayo, O.H. Alade, Acute toxicity and histological changes in gills, liver and kidney of catfish, Heterobranchus bidorsalis exposed to cypermethrin concentration, Afr. J. Agric. Res., Vol. 7(31), 4453-4459 (2012).

L. Chai, A. Chen, P. Luo, H. Zhao, H. Wang, Histopathological changes and lipid metabolism in the liver of Bufo gargarizans tadpoles exposed to Triclosan, Chemosphere, Vol. 182, 255-266 (2017).

H. Ando, Handbook of Hormones, 2nd ed., Academic Press, Vol. 1, 553-554 (2021).

C. Berg, An amphibian model for studies of developmental reproductive toxicity, C. Harris, J.M. Hansen (eds.), Developmental Toxicology: Methods and Protocols, Methods in Molecular Biology, Vol. 889, 73-83 (2012).

P. Y. Liu, T. Meng, Y. Y. Li, M. Cai, X. H. Li, J. Chen, Z. F. Qin, Tetrabromoethyl-cyclohexane affects gonadal differentiation and development in the frog Pelophylax nigromaculatus, Aquat. Toxicol., Vol. 192, 40-47 (2017).

W. Trachantong, J. Promya, S. Saenphet, K. Saenphet, Effects of atrazine herbicide on metamorphosis and gonadal development of Hoplobatrachus rugulosus, Maejo Int. J. Sci. Technol., Vol. 7 (special issue), 60-71 (2013).

M. Säfholm, A. Norder, J. Fick, C. Berg, Disrupted oogenesis in the frog Xenopus tropicalis after exposure to environmental progestrin concentrations, Biol. Reprod., Vol. 86 (4), 1-7 (2012).

X. Jia, C. Cai, J. Wang, N. Gao, H. Zhang, Endocrine-disrupting effects and reproductive toxicity of low dose MCLR on male frogs (Rana nigromaculata) in vivo, Aquat. Toxicol., Vol. 55, 24-31 (2014).

M.F. Medina, A. Cosci, S. Cisint, C.A. Crespo, I. Ramos, A.L.I. Villagra, S.N. Fernández, istopathological and biological studies of the effect of cadmium on Rhinella arenarum gonads, Tissue Cell, Vol. 44, 418-426 (2012).

A. Zahra, M. Tayyab, I.Z. Qureshi, Histopathological effects and element concentration of body tissues of ranid frog inhibiting polluted water sites, Eur. Sci. J., Vol. 12 (8), 388-400 (2016).

W.L. Goleman, J.A. Carr, T.A. Anderson, Environmentally relevant concentrations of ammonium perchlorate inhibit thyroid function and alter sex ratios in developing Xenopus laevis, Environ. Toxicol. Chem., Vol. 21, 590–597 (2002).

J. Van Sande, C. Massart, R. Neauwens, A. Schoutens, S. Costagliola, J.E. Dumont, J. Wolff, Anion selectivity by the sodium iodide symporter, Endocrinology, Vol. 144(1), 247-252 (2003).

E. Darrouzet, S. Lindenthal, D. Marcellin, J. Pellequer, T. Pourcher, The sodium/iodide symporter: state of the art of its molecular characterization, Biochim. Biophys. Acta, Vol. 1838, 244-253 (2014).

J. A. Carr, C. Theodorakis, Perchlorate Toxicology, R. J. Kendall, P. N. Smith, eds., 125-153 (2006).

K. Katawutpoonphan, Effects of artrazine on the early development and gonad development of rice field frog Hoplobatrachus rugulosus. Thesis of Master Degree. Chulalongkorn University, 120 pp. (2008).