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Toxicological Assessment of Ammonia Exposure on Carassius auratus red var. Living in Landscape Waters

  • Minghui Hao
  • Qiting Zuo
  • Wei Zhang
  • Yakun Feng
  • Li WangEmail author
  • Luji Yu
  • Xu Zhang
  • Jing Li
  • Zehan Huang
Article

Abstract

To understand the toxic mechanism of ammonia and identify effective biomarkers on the oxidative stress for the fish Carassius auratus red var., acute and chronic toxicity tests were conducted. The 96-h LC50 of total ammonia nitrogen (TAN) for C. auratus was 135.4 mg L−1, the corresponding unionized ammonia (NH3) concentration was 1.5 mg L−1. The activities of superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), glutathione-peroxidase (GSH-Px) and glutathione (GSH) showed an increase with a subsequent falling, while the malondialdehyde (MDA) increased during the chronic test. The SOD, MDA, and GSH could be effective biomarkers to evaluate the TAN oxidative stress, the maximum acceptable toxicant concentration (MATC) was 11.3 mg L−1 for TAN. To our knowledge, this is the first study to propose biomarkers to evaluate potential environmental risk and establish a risk threshold for TAN in C. auratus.

Keywords

Toxicological assessment Ammonia exposure Carassius auratus red var. Landscape waters 

Notes

Acknowledgements

This study was highly supported by the Major Science and Technology Program for Water Pollution Control and Treatment, China (Grant No. 2015ZX07204-002-05). We would also like to give our gratitude to the support of the Key Project of Natural Science Foundation of China—Xinjiang Joint Fund (Grant No. U1803241). What’s more, the Natural Sciences Foundation of China (Grant No. 51779230), Key research and development and promotion special (Grant No. 182102311033), Education department of Henan province science research Program (Grant Nos. 18B610008, 19A610010, and 19B610004), and the China postdoctoral science foundation (Grant No. 2018M632799) should also be thanked.

Compliance with Ethical Standards

Conflict of interest

All the authors declare that they do not have any conflicts of commercial or associative interest to this work.

Supplementary material

128_2019_2728_MOESM1_ESM.doc (1008 kb)
Supplementary material 1 (DOC 1007 kb)

References

  1. Blair SD, Wilkie MP, Edwards SL (2016) Rh glycoprotein immunoreactivity in the skin and its role in extrabranchial ammonia excretion by the sea lamprey (Petromyzon marinus) in fresh water Canadian. J Zool 95:95–105.  https://doi.org/10.1139/cjz-2016-0120 CrossRefGoogle Scholar
  2. Chen W, Fan X, Wang L (2011) Acute toxicity of ammonia-N on young Rhodeus Ocellatus. Guangdong Agric Sci 38:102–103Google Scholar
  3. Cheng C, Yang F, Ling R, Liao S, Miao Y, Ye C, Wang A (2015) Effects of ammonia exposure on apoptosis, oxidative stress and immune response in pufferfish (Takifugu obscurus). Aquat Toxicol 164:61–71.  https://doi.org/10.1016/j.aquatox.2015.04.004 CrossRefGoogle Scholar
  4. Cheng TY, You RC, Ong JLY, Wong WP, Chew SF, Ip YK (2017) Molecular characterization of two Rhesus glycoproteins from the euryhaline freshwater white-rimmed stingray, Himantura signifer, and changes in their transcript levels and protein abundance in the gills, kidney, and liver during brackish water acclimation. J Comp Physiol B 187:911–929.  https://doi.org/10.1007/s00360-017-1067-8 CrossRefGoogle Scholar
  5. Dasarathy S, Mookerjee RP, Rackayova V, Thrane VR, Vairappan B, Ott P, Rose CF (2017) Ammonia toxicity: from head to toe? Metab Brain Dis 32:529–538.  https://doi.org/10.1007/s11011-016-9938-3 CrossRefGoogle Scholar
  6. Dos Santos Silva MJ, Batista da Costa FF, Leme FP, Takata R (2018) Biological responses of Neotropical freshwater fish Lophiosilurus alexandri exposed to ammonia and nitrite. Sci Total Environ 616–617:1566–1575.  https://doi.org/10.1016/j.scitotenv.2017.10.157 CrossRefGoogle Scholar
  7. EL-Shebly AA, Gad HAM (2017) Effect of chronic ammonia exposure on growth performance, serum growth hormone (GH) levels and gill histology of nile tilapia (Oreochromis niloticus). J Microbiol Biotechnol Res 1:183–197Google Scholar
  8. Emerson K, Russo R, Lund RE, Thurston RV (1975) Aqueous ammonia equilibrium calculation: effect of pH and temperature. J Fish Res Board Can 32:2379–2383.  https://doi.org/10.1139/f75-274 CrossRefGoogle Scholar
  9. Gao J, Huang W, Huang Y (2010) NH4 +-N stress on peroxidation damage and antioxidative capability of Ceratophyllum demersum. J Wuhan Univ Nat Sci Ed 56:590–596.  https://doi.org/10.14188/j.1671-8836.2010.05.005 CrossRefGoogle Scholar
  10. Govindasamy R, Rahuman AA (2012) Histopathological studies and oxidative stress of synthesized silver nanoparticles in Mozambique tilapia (Oreochromis mossambicus). J Environ Sci 24:1091–1098.  https://doi.org/10.1016/S1001-0742(11)60845-0 CrossRefGoogle Scholar
  11. Huang Y, Cai Y, Shi J, Wang Y, Cheng X, Wang X (2018) The overview of how artificial water lands help mitigate eutrophication of landscape water system. In: “Environmental engineering” 2018 national academic annual conference, Beijing, China. Environ Eng vol Z:302-306Google Scholar
  12. Ighodaro OM, Akinloye OA (2018) First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): their fundamental role in the entire antioxidant defence grid Alexandria. J Med 54:287–293.  https://doi.org/10.1016/j.ajme.2017.09.001 CrossRefGoogle Scholar
  13. Jayaseelan C et al (2014) Effect of sub-acute exposure to nickel nanoparticles on oxidative stress and histopathological changes in Mozambique tilapia, Oreochromis mossambicus. Ecotoxicol Environ Saf 107:220–228.  https://doi.org/10.1016/j.ecoenv.2014.06.012 CrossRefGoogle Scholar
  14. Jiang HM (2012) Effect of ammonia on antioxidant in the liver, pancreas, and kidney of Yellow River Cyprinus carpio. J Shandong Univ 47:17–22.  https://doi.org/10.6040/j.issn.1671-9352.2012.01.004 CrossRefGoogle Scholar
  15. Lawrence MJ, Wright PA, Wood CM (2015) Physiological and molecular responses of the goldfish kidney (Carassius auratus) to metabolic acidosis, and potential mechanisms of renal ammonia transport. J Exp Biol 218:2124–2135.  https://doi.org/10.1242/jeb.117689 CrossRefGoogle Scholar
  16. Li B (2010) Effect of ammonia and nitrite toxicity on yellow catfish pelteobagrus fulvidraco. Huazhong agricultural university, WuhanGoogle Scholar
  17. Li F, Zhang HP, Chen L (2013) Temporal and spatial distribution of environmental factors and chlorophyll-a and their correlation analysis in a small enclosed lake. Environ Sci 34:3854–3861.  https://doi.org/10.13227/j.hjkx.2013.10.029 CrossRefGoogle Scholar
  18. Li M, Gong S, Li Q, Yuan L, Meng F, Wang R (2016) Ammonia toxicity induces glutamine accumulation, oxidative stress and immunosuppression in juvenile yellow catfish Pelteobagrus fulvidraco. Comp Biochem Physiol C 183–184:1–6.  https://doi.org/10.1016/j.cbpc.2016.01.005 CrossRefGoogle Scholar
  19. Li C, Zhang M, Li M, Zhang Q, Qian Y, Wang R (2018) Effect of dietary alanyl-glutamine dipeptide against chronic ammonia stress induced hyperammonemia in the juvenile yellow catfish (Pelteobagrus fulvidraco). Comp Biochem Physiol C 213:55–61.  https://doi.org/10.1016/j.cbpc.2018.08.001 CrossRefGoogle Scholar
  20. Liang J, Jin B, Wang H, Wu Q, Tang D, Zhao Y (2013) Ammonia toxicity to Hypophthalmichthys molitrix. J Hunan Foddr 2013(6):33–34Google Scholar
  21. Lisser DFJ, Lister ZM, Pham-Ho PQH, Scott GR, Wilkie MP (2017) Relationship between oxidative stress and brain swelling in goldfish (Carassius auratus) exposed to high environmental ammonia. Am J Physiol Regul Integr Comp Physiol 312:R114–R124.  https://doi.org/10.1152/ajpregu.00208.2016 CrossRefGoogle Scholar
  22. Liu Y (2011) Ammonia-N stress on Misgurnus anguillicaudatus and second generation population of mass selection. Master, Soochow UniversityGoogle Scholar
  23. Mooney TJ, Pease C, Trenfield M, van Dam R, Harford AJ (2018) Modeling the pH–ammonia toxicity relationship for Hydra viridissima in soft waters with low ionic concentrations. Environ Toxicol Chem 37:1189–1196.  https://doi.org/10.1002/etc.4071 CrossRefGoogle Scholar
  24. Munné-Bosch S, Pintó-Marijuana M (2017) Free radicals, oxidative stress and antioxidants. Encycl Appl Plant Sci.  https://doi.org/10.1016/B978-0-12-394807-6.00077-0 CrossRefGoogle Scholar
  25. Nagalakshmi N, Prasad MNV (2001) Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Sci 160:291–299.  https://doi.org/10.1016/S0168-9452(00)00392-7 CrossRefGoogle Scholar
  26. Nonnotte G, Salin D, Williot P (2018) Effects of exposure to ammonia in water: determination of the sublethal and lethal levels in Siberian sturgeon, Acipenser baerii. In: Williot P, Nonnotte G, Vizziano-Cantonnet D, Chebanov M (eds) The Siberian Sturgeon (Acipenser baerii, Brandt, 1869), vol 1. Springer, Cham, pp 391–404CrossRefGoogle Scholar
  27. OECD Test guideline 203 (1992) OECD guideline for testing of chemicals. Fish, Acute Toxicity TestGoogle Scholar
  28. Qi X, Xue M, Yang S, Zha J, Wang G, Ling F (2017) Ammonia exposure alters the expression of immune-related and antioxidant enzymes-related genes and the gut microbial community of crucian carp (Carassius auratus). Fish Shellfish Immunol 70:485–492.  https://doi.org/10.1016/j.fsi.2017.09.043 CrossRefGoogle Scholar
  29. Schultz BB (1985) Levene’s test for relative variation. Syst Biol 34:449–456.  https://doi.org/10.1093/sysbio/34.4.449 CrossRefGoogle Scholar
  30. Senthomilselvan D, Chezhian A (2014) Ammonia induced biochemical changes on the muscle tissues of the fish Cyprinus carpio. Res J Environ Toxicol 8(3):117–123.  https://doi.org/10.3923/rjet.2014.117.123 CrossRefGoogle Scholar
  31. Sinha AK, Zinta G, Abdelgawad H, Han A, Blust R, Boeck GD (2015) High environmental ammonia elicits differential oxidative stress and antioxidant responses in five different organs of a model estuarine teleost (Dicentrarchus labrax). Comp Biochem Physiol C 174–175:21–31.  https://doi.org/10.1016/j.cbpc.2015.06.002 CrossRefGoogle Scholar
  32. Souza-Bastos LR, Val AL, Wood CM (2015) Are Amazonian fish more sensitive to ammonia? Toxicity of ammonia to eleven native species. Hydrobiologia 789:1–13.  https://doi.org/10.1007/s10750-015-2623-4 CrossRefGoogle Scholar
  33. Sun H, Wang W, Li J, Yang Z (2014) Growth, oxidative stress responses, and gene transcription of juvenile bighead carp (Hypophthalmichthys nobilis) under chronic-term exposure of ammonia. Environ Toxicol Chem 33:1726–1731.  https://doi.org/10.1002/etc.2613 CrossRefGoogle Scholar
  34. Trenzado C, Morales AE, Palma J, de la Higuera M (2008) Blood antioxidant defenses and hematological adjustments in crowded/uncrowded rainbow trout (Oncorhynchus mykiss) fed on diets with different levels of antioxidant. Comp Biochem Physiol C 149(3):440–447.  https://doi.org/10.1016/j.cbpc.2008.10.105 CrossRefGoogle Scholar
  35. Vieira MC, Torronteras R, Córdoba F, Canalejo A (2012) Acute toxicity of manganese in goldfish Carassius auratus is associated with oxidative stress and organ specific antioxidant responses. Ecotoxicol Environ Saf 78:212–217.  https://doi.org/10.1016/j.ecoenv.2011.11.015 CrossRefGoogle Scholar
  36. Wang HJ, Xiao XC, Wang HZ, Li Y (2017) Effects of high ammonia concentrations on three cyprinid fish: acute and whole-ecosystem chronic tests. Sci Total Environ 598:900–909.  https://doi.org/10.1016/j.scitotenv.2017.04.070 CrossRefGoogle Scholar
  37. Wilkie MP, Stecyk J, Couturier C, Sidhu S, Sandvik G, Nilsson GE (2015) Reversible brain swelling in crucian carp (Carassius carassius) and goldfish (Carassius auratus) in response to high external ammonia and anoxia. Comp Biochem Physiol A 184:65–75.  https://doi.org/10.1016/j.cbpa.2014.12.038 CrossRefGoogle Scholar
  38. Yang W, Xiang F, Liang L, Yang Z (2010) Toxicity of ammonia and its effects on oxidative stress mechanisms of juvenile crucian carp (Carassius auratus). J Freshw Ecol 25:297–302.  https://doi.org/10.1080/02705060.2010.9665080 CrossRefGoogle Scholar
  39. Zhang HM, Jiang H (2011) Effect of ammonia on antioxidant responses in serum of yellow river carps. J Southwest Univ Nat Sci Ed 33:88–93.  https://doi.org/10.3724/SP.J.1011.2011.00187 CrossRefGoogle Scholar
  40. Zhang Q, Yuan J (2001) Technical measures for the comprehensive management of water bodies in parks. Shanghai Constr Sci Technol.  https://doi.org/10.3969/j.issn.1005-6637.2001.03.016 CrossRefGoogle Scholar
  41. Zhao CC, Xu JT, Xu XL, Wang Q, Kong Q, Xu F, Du YD (2019) Organ-specific responses to total ammonia nitrogen stress on juvenile grass carp (Ctenopharyngodon idellus). Environ Sci Pollut Res 26:10826–10834.  https://doi.org/10.1007/s11356-019-04524-4 CrossRefGoogle Scholar
  42. Zirong X, Shijun B (2007) Effects of waterborne Cd exposure on glutathione metabolism in Nile tilapia (Oreochromis niloticus) liver. Ecotoxicol Environ Saf 67:89–94.  https://doi.org/10.1016/j.ecoenv.2006.04.006 CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of Water Conservancy EngineeringZhengzhou UniversityZhengzhouChina
  2. 2.Zhengzhou Key Laboratory of Water Resource and EnvironmentZhengzhouChina
  3. 3.Henan Key Laboratory of Groundwater Pollution Prevention and RehabilitationZhengzhouChina
  4. 4.Henan Province Key Laboratory of Water Pollution Control and Rehabilitation TechnologyPingdingshanChina

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