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Seasonal responses of periphytic protozoan fauna to the antibiotic nitrofurazone at sensitive concentration in marine environments

Published online by Cambridge University Press:  04 March 2025

Ning Wang
Affiliation:
Laboratory of Microbial Ecology, Ocean University of China, Qingdao 266003, China
Henglong Xu*
Affiliation:
Laboratory of Microbial Ecology, Ocean University of China, Qingdao 266003, China
Guangjian Xu
Affiliation:
College of Environment and Safety Engineering, Qingdao University of Science & Technology, Qingdao 266042, China
*
Corresponding author: Henglong Xu; Email: henglongxu@126.com

Abstract

In order to evaluate the seasonal responses of periphytic protozoan fauna to the antibiotic nitrofurazone at sensitive concentration, a 1-year baseline survey was carried out in Chinese coastal waters of the Yellow Sea. To assess the nitrofurazone (NFZ)-induced toxicokinetics in different season, the test protozoan samples were collected using microscope slides and exposed to the sensitive NFZ concentration of 8 mg ml−1. Differences in species composition and typical species were observed in the test organism fauna in the control and treatment among four seasons. However, the community patterns were significantly shifted under the sensitive concentration, with a part of stressed test samples significantly departed from a respected taxonomic pattern. Therefore, it is suggested that periphytic protozoan fauna may be significantly changed at the same sensitive concentration in both the species composition and community pattern, although there were significant differences in tolerant species among four seasons in marine environments.

Type
Research Article
Copyright
Copyright © The Author(s), 2025. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

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References

Anderson, MJ, Gorley, RN, Clarke, KS, Anderson, MS, Gorley, RN, Clarke, KR and Andersom, M (2008) PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. Plymouth: PRIMER-E Ltd.Google Scholar
Anh, HQ, Le, TPQ, Da Le, N, Lu, XX, Duong, TT, Garnier, J, Rochelle-Newall, E, Zhang, S, Oh, N, Oeurng, C, Ekkawatpanit, C, Nguyen, TD, Nguyen, QT, Nguyen, TD, Nguyen, T, Tran, TL, Kunisue, T, Tanoue, R, Takahashi, S, Minh, TB, Le, HT, Pham, TMH and Nguyen, TAH (2021) Antibiotics in surface water of east and southeast Asian countries: a focused review on contamination status, pollution sources, potential risks, and future perspectives. Science of the Total Environment 764, 142865.CrossRefGoogle Scholar
Bawa-Allah, KA and Ehimiyein, AO (2022) Ecotoxicological effects of human and veterinary antibiotics on water flea (daphnia magna). Environmental Toxicology and Pharmacology 94, 103932.CrossRefGoogle ScholarPubMed
Bhagat, C, Kumar, M, Tyagi, VK and Mohapatra, PK (2020) Proclivities for prevalence and treatment of antibiotics in the ambient water: a review. NPJ Clean Water 3, 42.CrossRefGoogle Scholar
Chang, G, Chen, H and Lin, F (2016) Analysis of banned veterinary drugs and herbicide residues in shellfish by liquid chromatography-tandem mass spectrometry (lc/ms/ms) and gas chromatography-tandem mass spectrometry (gc/ms/ms). Marine Pollution Bulletin 113, 579584.CrossRefGoogle ScholarPubMed
Clarke, K and Gorley, R (2015) Primer version 7: user manual/tutorial. PRIMER-E 192.Google Scholar
Clarke, KR and Warwick, RM (1998) A taxonomic distinctness index and its statistical properties. Journal of Applied Ecology 35, 523531.CrossRefGoogle Scholar
Dahms, HU, Hagiwara, A and Lee, JS (2011) Ecotoxicology, ecophysiology, and mechanistic studies with rotifers. Aquatic Toxicology 101, 112.CrossRefGoogle ScholarPubMed
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, 9096.CrossRefGoogle ScholarPubMed
Ghosh, S, Majumder, S and Roychowdhury, T (2021) Impact of microbial multi-metal and broad spectrum antibiotic tolerance in urban sw (adi ganga, kolkata) on adjacent groundwater: a future threat. Groundwater for Sustainable Development 14, 100608.CrossRefGoogle Scholar
Girling, AE, Pascoe, D, Janssen, CR, Peither, A, Wenzel, A, Schäfer, H, Neumeier, B, Mitchell, GC, Taylor, EJ, Maund, SJ, Lay, JP, Jüttner, I, Crossland, NO, Stephenson, RR and Persoone, G (2000) Development of methods for evaluating toxicity to freshwater ecosystems. Ecotoxicology and Environmental Safety 45, 148176.CrossRefGoogle ScholarPubMed
Guo, C, Gui, Y, Bai, X, Sikder, MNA and Xu, H (2020) Seasonal variation in biological trait distribution of periphytic protozoa in coastal ecosystem: a baseline study for marine bioassessment. Marine Pollution Bulletin 160, 111593.CrossRefGoogle Scholar
Han, QF, Zhao, S, Zhang, XR, Wang, XL, Song, C and Wang, SG (2020) Distribution, combined pollution and risk assessment of antibiotics in typical marine aquaculture farms surrounding the yellow sea, north China. Environment International 138, 105551.CrossRefGoogle ScholarPubMed
Hassan Kazmi, SSU, Xuexi, T, Xu, G and Xu, H (2021) An approach to optimizing sampling effort for bioassessment surveys based on periphytic ciliates according to water depths in marine ecosystems. Ecological Indicators 122, 107222.CrossRefGoogle Scholar
Hong, Y, Lin, X, Cui, X, Zhou, L, Al-Rasheid, KAS 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, 153160.CrossRefGoogle Scholar
Isidori, M, Lavorgna, M, Nardelli, A, Pascarella, L and Parrella, A (2005) Toxic and genotoxic evaluation of six antibiotics on non-target organisms. Science of the Total Environment 346, 8798.CrossRefGoogle ScholarPubMed
Jiang, Y, Xu, H, Zhu, M and Al-Rasheid, KAS (2013) Temporal distributions of microplankton populations and relationships to environmental conditions in Jiaozhou bay, northern China. Journal of the Marine Biological Association of the United Kingdom 93, 1326.CrossRefGoogle Scholar
Kathol, M, Norf, H, Arndt, H and Weitere, M (2009) Effects of temperature increase on the grazing of planktonic bacteria by biofilm-dwelling consumers. Aquatic Microbial Ecology 55, 6579.CrossRefGoogle Scholar
Kazmi, SSUH, Uroosa, , Warren, A, Zhong, X and Xu, H (2022a) Insights into the ecotoxicity of nitrofurazone in marine ecosystems based on body-size spectra of periphytic ciliates. Marine Pollution Bulletin 174, 113217.CrossRefGoogle ScholarPubMed
Kazmi, SSUH, Uroosa, , Xu, H and Xuexi, T (2022b) An approach to determining the nitrofurazone-induced toxic dynamics for ecotoxicity assessment using protozoan periphytons in marine ecosystems. Marine Pollution Bulletin 175, 113329.CrossRefGoogle ScholarPubMed
Kazmi, SSUH, Xuexi, T, Xu, G, Sikder, MNA and Xu, H (2020) Vertical variability in taxonomic breadth of biofilm-dwelling ciliates in marine bioassessment surveys. Regional Studies in Marine Science 38, 101366.CrossRefGoogle Scholar
Kovalakova, P, Cizmas, L, Mcdonald, TJ, Marsalek, B, Feng, M and Sharma, VK (2020) Occurrence and toxicity of antibiotics in the aquatic environment: a review. Chemosphere 251, 126351.CrossRefGoogle ScholarPubMed
Leonard, DRP, Robert Clarke, K, Somerfield, PJ and Warwick, RM (2006) The application of an indicator based on taxonomic distinctness for UK marine biodiversity assessments. Journal of Environmental Management 78, 5262.CrossRefGoogle ScholarPubMed
Li, J, Zhou, L, Lin, X, Yi, Z and Al-Rasheid, KAS (2014) Characterizing dose–responses of catalase to nitrofurazone exposure in model ciliated protozoan Euplotes vannus for ecotoxicity assessment: enzyme activity and mRNA expression. Ecotoxicology and Environmental Safety 100, 294302.CrossRefGoogle ScholarPubMed
Niemeyer, JC, Moreira-Santos, M, Nogueira, MA, Carvalho, GM, Ribeiro, R, Da Silva, EM and Sousa, JP (2010) Environmental risk assessment of a metal-contaminated area in the tropics. Tier i: screening phase. Journal of Soils and Sediments 10, 15571571.CrossRefGoogle Scholar
Prato, S, Morgana, JG, La Valle, P, Finoia, MG, Lattanzi, L, Nicoletti, L, Ardizzone, GD and Izzo, G (2009) Application of biotic and taxonomic distinctness indices in assessing the ecological quality status of two coastal lakes: Caprolace and Fogliano lakes (central Italy). Ecological Indicators 9, 568583.CrossRefGoogle Scholar
Puckowski, A, Mioduszewska, K, Bukaszewicz, P, Borecka, M, Caban, M, Maszkowska, J and Stepnowski, P (2016) Bioaccumulation and analytics of pharmaceutical residues in the environment: a review. Journal of Pharmaceutical and Biomedical Analysis 127, 232255.CrossRefGoogle ScholarPubMed
Si, R, Yao, Y, Liu, X, Lu, Q and Liu, M (2022) Role of risk perception and government regulation in reducing over-utilization of veterinary antibiotics: evidence from hog farmers of China. One Health 15, 100448.CrossRefGoogle ScholarPubMed
Sikder, MNA, Xu, G and Xu, H (2020a) Seasonal variability in taxonomic breadth of biofilm-dwelling ciliates in colonization surveys for marine bioassessment. Marine Pollution Bulletin 151, 110828.CrossRefGoogle ScholarPubMed
Sikder, MNA, Xu, H, Xu, G and Warren, A (2020b) Seasonal variability in trophic-functional patterns of marine biofilm-dwelling ciliates during the process of colonization. Regional Studies in Marine Science 35, 101236.CrossRefGoogle Scholar
Somerfield, PJ, Clarke, KR, Warwick, RM and Dulvy, NK (2008) Average functional distinctness as a measure of the composition of assemblages. ICES Journal of Marine Science 65, 14621468.CrossRefGoogle Scholar
Song, W, Warren, A and Hu, X (2009) Free-living Ciliates in the Bohai and Yellow Seas. Beijing: Science Press. In both Chinese and English.Google Scholar
Tan, X, Shi, X, Liu, G, Xu, H and Nie, P (2010) An approach to analyzing taxonomic patterns of protozoan communities for monitoring water quality in Songhua river, northeast China. Hydrobiologia 638, 193201.CrossRefGoogle Scholar
Trielli, F, Amaroli, A, Sifredi, F, Marchi, B, Falugi, C and Corrado, MUD (2007) Effects of xenobiotic compounds on the cell activities of Euplotes crassus, a single-cell eukaryotic test organism for the study of the pollution of marine sediments. Aquatic Toxicology 83, 272283.CrossRefGoogle Scholar
Vutukuru, SS, Prabhath, NA, Raghavender, M and Yerramilli, A (2007) Effect of arsenic and chromium on the serum amino-transferases activity in Indian major carp, Labeo rohita. International Journal of Environmental Research and Public Health 4, 224227.CrossRefGoogle ScholarPubMed
Wang, K, Guo, C, Li, J, Wang, K, Liang, S, Wang, W and Wang, J (2024) A critical review of the adsorption-desorption characteristics of antibiotics on microplastics and their combined toxic effects. Environmental Technology & Innovation 35, 103729.CrossRefGoogle Scholar
Wang, Y, Guo, Y, Pan, K, Lin, X and Ni, Y (2020) Electrochemical reaction mechanism of nitrofurazone at poly-ACBK/GCE and its analytic application. Chemistry Africa 3, 727734.CrossRefGoogle Scholar
Warwick, R and Clarke, K (1995) New ‘biodiversity’ measures reveal a decrease in taxonomic distinctness with increasing stress. Marine Ecology Progress Series 129, 301305.CrossRefGoogle Scholar
Wey, JK, Norf, H, Arndt, H and Weitere, M (2009) Role of dispersal in shaping communities of ciliates and heterotrophic flagellates within riverine biofilms. Limnology and Oceanography 54, 16151626.CrossRefGoogle Scholar
Xu, H, Jiang, Y, Al-Rasheid, KAS, Al-Farraj, SA and Song, W (2011a) Application of an indicator based on taxonomic relatedness of ciliated protozoan assemblages for marine environmental assessment. Environmental Science and Pollution Research 18, 12131221.CrossRefGoogle ScholarPubMed
Xu, H, Zhang, W, Jiang, Y and Yang, EJ (2014) Use of biofilm-dwelling ciliate communities to determine environmental quality status of coastal waters. Science of the Total Environment 470–471, 511518.CrossRefGoogle ScholarPubMed
Xu, H, Zhang, W, Jiang, Y, Zhu, M and Al-Rasheid, KAS (2012) Sampling sufficiency for analyzing taxonomic relatedness of periphytic ciliate communities using an artificial substratum in coastal waters. Journal of Sea Research 72, 2227.CrossRefGoogle Scholar
Xu, H, Zhang, W, Jiang, Y, Zhu, M, Al-Rasheid, KA, Warren, A and Song, W (2011b) An approach to determining the sampling effort for analyzing biofilm-dwelling ciliate colonization using an artificial substratum in coastal waters. Biofouling 27, 357366.CrossRefGoogle ScholarPubMed
Zhou, X, Shi, Y, Lu, Y, Song, S, Wang, C, Wu, Y, Liang, R, Qian, L, Xu, Q, Shao, X and Li, X (2024) Ecological risk assessment of commonly used antibiotics in aquatic ecosystems along the coast of China. Science of the Total Environment 935, 173263.CrossRefGoogle ScholarPubMed
Zhou, W, Tang, Y, Du, X, Han, Y, Shi, W, Sun, S, Zhang, W, Zheng, H and Liu, G (2021) Fine polystyrene microplastics render immune responses more vulnerable to two veterinary antibiotics in a bivalve species. Marine Pollution Bulletin 164, 111995.CrossRefGoogle Scholar