Skip to main content

Advertisement

SpringerLink
Log in

Comparative Evaluation on Combined Ecotoxic Effects of Nitrofurazone and NH4CI Using Two Ciliated Protists as Model Organisms: Population Dynamics and Growth Rates

  • Published:
Journal of Ocean University of China Aims and scope Submit manuscript

Abstract

Ecotoxic effects of antibiotics or ammonium have been confirmed independently in aquatic animals, but few studies have investigated their combined effects. In aquaculture ecosystems, these pollutants frequently coexist, and often in high concentrations. In this study, the combined effects of antibiotic nitrofurazone and NH4Cl on the population dynamics and growth rates of two species of ciliated protists, Euplotes vannus and Pseudokeronopsis rubra, were investigated. Profiles of the dose-responses were visualized, and interactions between the two pollutants were quantified by the response surface method (RSM). Results showed that 1) the dynamics of the population growth differed significantly between the testd ciliates and varied with the concentrations of the pollutants; 2) the relative growth rate (RGR) of both ciliates decreased significantly with increased pollutant concentrations, while the difference in RGR between the two ciliates was not significant; 3) RSM analysis demonstrated an additive effect of nitrofurazone and NH4Cl on the RGR in both ciliates. In brief, ecotoxic effects can be caused by nitrofurazone and ammonium independently on the two test ciliates, and such effects can be strengthened when they present at the same time. These findings offer a valuable reference for evaluating combined ecotoxic effects caused by multiple pollutants in aquaculture ecosystems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Belwal, T., Dhyani, P., Bhatt, I. D., Rawal, R. S., and Pande, V., 2016. Optimization extraction conditions for improving phenolic content and antioxidant activity in Berberis asiatica fruits using response surface methodology (RSM). Food Chemistry, 207: 115–124.

    Article  Google Scholar 

  • Bendall, J. G., Crawford, R. A., Evers, J. M., Smythe, B. W., Bessaire, T., Mottier, P., Mujahid, C., Aleksic, G., and Hutchinson, R., 2019. Determination of nitrofurazone in fluid milk and dairy powders. Part 1: An international pilot study. International Dairy Journal, 91: 185–192.

    Article  Google Scholar 

  • Chen, X., Clamp, J. C., and Song, W., 2011. Phylogeny and systematic revision of the family Pseudokeronopsidae (Protista, Ciliophora, Hypotricha), with description of a new estuarine species of Pseudokeronopsis. Zoologica Scripta, 40: 659–671.

    Article  Google Scholar 

  • Colorni, A., and Paperna, I., 1983. Evaluation of nitrofurazone baths in the treatment of bacterial infections of Sparus aurata and Oreochromis mossambicus. Aquaculture, 35: 181–186.

    Article  Google Scholar 

  • Draper, N. R., 1997. Response surface methodology: Process and product optimization using designed experiments. Journal of Statistical Planning and Inference, 59: 185–186.

    Article  Google Scholar 

  • Du, N., Chen, M., Sheng, L., Chen, S., Xu, H., Liu, Z., Song, C., and Qiao, R., 2014. Determination of nitrofuran metabolites in shrimp by high performance liquid chromatography with fluorescence detection and liquid chromatography-tandem mass spectrometry using a new derivatization reagent. Journal of Chromatography A, 1327: 90–96.

    Article  Google Scholar 

  • Ebeling, J. M., Timmons, M. B., and Bisogni, J. J., 2006. Engineering analysis of the stoichiometry of photoautotrophic, autotrophic, and heterotrophic removal of ammonia-nitrogen in aquaculture systems. Aquaculture, 257: 346–358.

    Article  Google Scholar 

  • Esteban, G. F., and Finlay, B. J., 2007. Exceptional species richness of ciliated Protozoa in pristine intertidal rock pools. Marine Ecology Progress Series, 335: 133–141.

    Article  Google Scholar 

  • Farzana, S., and Tam, N. F. Y., 2018. A combined effect of poly-brominated diphenyl ether and aquaculture effluent on growth and antioxidative response of mangrove plants. Chemosphere, 201: 483–491.

    Article  Google Scholar 

  • Ghersi-Egea, J. F., Maupoil, V., Ray, D., and Rochette, L., 1998. Electronic spin resonance detection of superoxide and hydroxyl radicals during the reductive metabolism of drugs by rat brain preparations and isolated cerebral microvessels. Free Radical Biology and Medicine, 24: 1074–1081.

    Article  Google Scholar 

  • Groenveld, T., Kohn, Y. Y., Gross, A., and Lazarovitch, N., 2019. Optimization of nitrogen use efficiency by means of fertigation management in an integrated aquaculture-agriculture system. Journal of Cleaner Production, 212: 401–408.

    Article  Google Scholar 

  • Han, Q., Zhao, S., Zhang, X., Wang, X. L., Song, C., and Wang, S., 2020. Distribution, combined pollution and risk assessment of antibiotics in typical marine aquaculture farms surrounding the Yellow Sea, North China. Environment International, 138: 105551.

    Article  Google Scholar 

  • Hegazi, M. M., Attia, Z. I., and Ashour, O. A., 2010. Oxidative stress and antioxidant enzymes in liver and white muscle of Nile tilapia juveniles in chronic ammonia exposure. Aquatic Toxicology, 99: 118–125.

    Article  Google Scholar 

  • Hiraku, Y., Sekine, A., Nabeshi, H., Midorikawa, K., Murata, M., Kumagai, Y., and Kawanishi, S., 2004. Mechanism of carcinogenesis induced by a veterinary antimicrobial drug, ni-trofurazone, via oxidative DNA damage and cell proliferation. Cancer Letters, 215: 141–150.

    Article  Google Scholar 

  • Hoffmann, W. A., and Poorter, H., 2002. Avoiding bias in calculations of relative growth rate. Annals of Botany, 90: 37–42.

    Article  Google Scholar 

  • Holt, R. D., Grover, J., and Tilman, D., 1994. Simple rules for interspecific dominance in systems with exploitative and apparent competition. American Naturalist, 144: 741–771.

    Article  Google Scholar 

  • Hong, Y., Lin, X., Cui, X., Zhou, L., Al-Rasheid, K. A. S., and Li, J., 2015. Comparative evaluation of genotoxicity induced by nitrofurazone in two ciliated protozoa by detecting DNA strand breaks and DNA-protein crosslinks. Ecological Indicators, 54: 153–160.

    Article  Google Scholar 

  • Hong, Y., Tan, Y., Meng, Y., Yang, H., Zhang, Y., Warren, A., Li, J., and Lin, X., 2017. Evaluation of biomarkers for ecotoxicity assessment by dose-response dynamic models: Effects of nitrofurazone on antioxidant enzymes in the model ciliated protozoan Euplotes vannus. Ecotoxicology and Environmental Safety, 144: 552–559.

    Article  Google Scholar 

  • Hu, S., and Zhang, D., 1993. The effects of initial population-density on the competition for limiting nutrients in 2 freshwater algae. Oecologia, 96: 569–574.

    Article  Google Scholar 

  • Hu, X., and Song, W., 2001. Morphological redescription and morphogenesis of the marine ciliate, Pseudokeronopsis rubra (Ciliophora, Hypotrichida). Acta Protozoologica, 40: 107–115.

    Google Scholar 

  • Ito, K., Kajikawa, S., Aisuke, N., Hanada, T., and Doi, K., 2003. Antioxidants suppress nitrofurazone-induced proliferation of hepatocytes. Experimental and Toxicologic Pathology, 55: 247–250.

    Article  Google Scholar 

  • Kari, F. W., Huff, J. E., Leininger, J., Haseman, J. K., and Eustis, S. L., 1989. Toxicity and carcinogenicity of nitrofurazone in F344/N rats and B6C3F1 mice. Food and Chemical Toxicology, 27: 129–137.

    Article  Google Scholar 

  • Kim, J. H., Kang, Y. J., Kim, K. I., Kim, S. K., and Kim, J. H., 2019. Toxic effects of nitrogenous compounds (ammonia, nitrite, and nitrate) on acute toxicity and antioxidant responses of juvenile olive flounder, Paralichthys olivaceus. Environmental Toxicology and Pharmacology, 67: 73–78.

    Article  Google Scholar 

  • Li, X., Huang, J., Filker, S., Stoeck, T., Bi, Y., Yu, Y., and Song, W., 2019. Spatio-temporal patterns of zooplankton in a main-stem dam affected tributary: A case study in the Xiangxi River of the Three Gorges Reservoir, China. Science China. Life Sciences, 62: 1058–1069.

    Article  Google Scholar 

  • Li, X., Li, W., Zhai, J., Wei, H., and Wang, Q., 2019. Effect of ammonium nitrogen on microalgal growth, biochemical composition and photosynthetic performance in mixotrophic cultivation. Bioresource Technology, 273: 368–376.

    Article  Google Scholar 

  • Liu, X., Steele, J. C., and Meng, X., 2017. Usage, residue, and human health risk of antibiotics in Chinese aquaculture: A review. Environmental Pollution, 223: 161–169.

    Article  Google Scholar 

  • Macri, A., and Sbardella, E., 1984. Toxicological evaluation of ni-trofurazone and furaltadone on Selenastrum capricornutum, Daphnia magna, and Musca domestica. Ecotoxicology and Environmental Safety, 8: 101–105.

    Article  Google Scholar 

  • Madoni, P., and Romeo, G. M., 2006. Acute toxicity of heavy metals towards freshwater ciliated protists. Environmental Pollution, 141: 1–7.

    Article  Google Scholar 

  • Martinez, P. G., Winston, G. W., Metashdickey, C., Ohara, S. C. M., and Livingstone, D. R., 1995. Nitrofurantoin-stimulated reactive oxygen species production and genotoxicity in digestive gland microsomes and cytosol of the common mussel (Mytilus edulis L.). Toxicology and Applied Pharmacology, 131: 332–341.

    Article  Google Scholar 

  • McCracken, R. J., Blanchflower, W. J., Rowan, C., McCoy, M. A., and Kennedy, D. G., 1995. Determination of furazolidone in porcine tissue using thermospray liquid chromatography-mass spectrometry and a study of the pharmacokinetics and stability of its residues. Analyst, 120: 2347–2351.

    Article  Google Scholar 

  • Montagnes, D., Roberts, E., Lukeš, J., and Lowe, C., 2012. The rise of model protozoa. Trends in Microbiology, 20: 184–191.

    Article  Google Scholar 

  • Murphy, A. E., Nizzoli, D., Bartoli, M., Smyth, A. R., Castaldelli, G., and Anderson, I. C., 2018. Variation in benthic metabolism and nitrogen cycling across clam aquaculture sites. Marine Pollution Bulletin, 127: 524–535.

    Article  Google Scholar 

  • Payne, R. J., 2013. Seven reasons why protists make useful bioindicators. Acta Protozoologica, 52: 105–113.

    Google Scholar 

  • Pianka, E. R., 1970. On r and K selection. American Naturalist, 104: 592–597.

    Article  Google Scholar 

  • Pörtner, H. O., Schulte, P. M., Wood, C. M., and Schiemer, F., 2010. Niche dimensions in fishes: An integrative view. Physiological and Biochemical Zoology, 83: 808–826.

    Article  Google Scholar 

  • Rodrigues, R. V., Romano, L. A., Schwarz, M. H., Delbos, B., and Sampaio, L. A., 2014. Acute tolerance and histopathological effects of ammonia on juvenile maroon clownfish Premnas biaculeatus (Block 1790). Aquaculture Research, 45: 1133–1139.

    Article  Google Scholar 

  • Romano, N., and Zeng, C., 2009. Acute toxicity of sodium nitrate, potassium nitrate, and potassium chloride and their effects on the hemolymph composition and gill structure of early juvenile blue swimmer crabs (Portunus pelagicus Linnaeus, 1758) (Decapoda, Brachyuran, Portunidae). Environmental Toxicology and Chemistry, 26: 1955–1962.

    Article  Google Scholar 

  • Ruan, Y., Dou, Y., Chen, J., Warren, A., Li, J., and Lin, X., 2018. Evaluation of phenol-induced ecotoxicity in two model ciliate species: Population growth dynamics and antioxidant enzyme activity. Ecotoxicology and Environmental Safety, 166: 176–185.

    Article  Google Scholar 

  • Sarma, S. S. S., Iyer, N., and Dumont, H. J., 1996. Competitive interactions between herbivorous rotifers: Importance of food concentration and initial population density. Hydrobiologia, 331: 1–7.

    Article  Google Scholar 

  • Smolders, R., Bervoets, L., De Coen, W., and Blust, R., 2004. Cellular energy allocation in zebra mussels exposed along a pollution gradient: Linking cellular effects to higher levels of biological organization. Environmental Pollution, 129: 99–112.

    Article  Google Scholar 

  • Tao, H., Tang, X. Y., Jin, L., Zhao, Y. C., Luo, Y., Zhang, Z., Cai, L., Tao, F. H., and Guo, W. C., 2018. Synergistic effect of docetaxel combined with cisplatin on inhibiting human osteosarcoma in nude mice. Biochemical and Biophysical Research Communications, 505: 372–377.

    Article  Google Scholar 

  • Tilman D., 1982. Resource Competition and Community Structure. Princeton University Press, Princeton, NJ, 1–296.

    Google Scholar 

  • Välitalo, P., Kruglova, A., Mikola, A., and Vahala, R., 2017. Toxicological impacts of antibiotics on aquatic micro-organisms: A mini-review. International Journal of Hygiene and Environmental Health, 220: 558–569.

    Article  Google Scholar 

  • Van Duc, L., Song, B., Ito, H., Hama, T., Otani, M., and Kawagoshi, Y., 2018. High growth potential and nitrogen removal performance of marine anammox bacteria in shrimp-aquaculture sediment. Chemosphere, 196: 69–77.

    Article  Google Scholar 

  • Vlastos, D., Moshou, H., and Epeoglou, K., 2010. Evaluation of genotoxic effects of semicarbazide on cultured human lymphocytes and rat bone marrow. Food and Chemical Toxicology, 48: 209–214.

    Article  Google Scholar 

  • Weinbauer, M. G., and Höfle, M. G., 1998. Distribution and life strategies of two bacterial populations in a eutrophic lake. Applied and Environmental Microbiology, 64(10): 3776–3783.

    Article  Google Scholar 

  • Xiang, F., Yang, W., Chen, Y., and Yang, Z., 2010. Acute toxi-city of nitrite and ammonia to Daphnia similoides of different developmental stages: Using the modified Gaussian model to describe. Bulletin of Environmental Contamination and Toxicology, 84: 708–711.

    Article  Google Scholar 

  • Xu, H., Zhu, M., Jiang, Y., Gao, S., Min, G. S., and Al-Rasheid, K. A. S., 2011. Population dynamics of marine ciliate Euplotes vannus (Protozoa, Ciliophora) in different artificial sea-waters. Chinese Journal of Oceanology and Limnology, 29: 109–117.

    Article  Google Scholar 

  • Yang, J., Hu, W., Tan, Y., Warren, A., Lin, X., and Li, J., 2019. Combined effects of food resources and exposure to ammonium nitrogen on population growth performance in the bac-terivorous ciliate Paramecium caudatum. European Journal of Protistology, 71: 125631.

    Article  Google Scholar 

  • Zeng, C., Gonzalez-Alvarez, A., Orenstein, E., Field, J. A., Shadman, F., and Sierra-Alvarez, R., 2017. Ecotoxicity assessment of ionic As(III), As(V), In(III) and Ga(III) species potentially released from novel III-V semiconductor materials. Ecotoxi-cology and Environmental Safety, 140: 30–36.

    Article  Google Scholar 

  • Zhou, L., Li, J., Lin, X., and Al-Rasheid, K. A. S., 2011. Use of RAPD to detect DNA damage induced by nitrofurazone in marine ciliate, Euplotes vannus (Protozoa, Ciliophora). Aquatic Toxicology, 103: 225–232.

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Nos. 31971519, 31430077, 41476128) and in part by a grant from the Dedicated Fund for Promoting High-Quality Economic Development in Guangdong Province (Marine Economic Development Project: GDOE(2019)A23).

Author information

Authors and Affiliations

  1. Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, South China Normal University, Guangzhou, 510631, China

    Ziyue Yu, Shuxing Liu & Xin Chen

  2. Department of Life Sciences, Natural History Museum, Cromwell Road, London, SW7 5BD, UK

    Alan Warren

  3. The Fujian Provincial Key Laboratory for Coastal Ecology and Environmental Studies, College of the Environment and Ecology, Xiamen University, Xiamen, 361005, China

    Xiaofeng Lin & Jiqiu Li

  4. Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystem, College of the Environment and Ecology, Xiamen University, Xiamen, 361005, China

    Xiaofeng Lin & Jiqiu Li

Authors
  1. Ziyue Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shuxing Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alan Warren
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiaofeng Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jiqiu Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jiqiu Li.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yu, Z., Liu, S., Chen, X. et al. Comparative Evaluation on Combined Ecotoxic Effects of Nitrofurazone and NH4CI Using Two Ciliated Protists as Model Organisms: Population Dynamics and Growth Rates. J. Ocean Univ. China 20, 137–146 (2021). https://doi.org/10.1007/s11802-021-4410-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11802-021-4410-3

Key words

Search

Navigation