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Toxicity effects of ciprofloxacin on biochemical parameters, histological characteristics, and behaviors of Corbicula fluminea in different substrates

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Abstract

Antibiotic toxicity and antibiotic resistance have become significant challenges to human health. However, the potential ecotoxicity of sediment-associated antibiotics remains unknown. In this study, biochemical responses, histological changes, and behavioral responses of Corbicula fluminea exposed to sediment-associated ciprofloxacin (CIP) were systemically investigated. Special attention was paid to the influence of different substrate types. Biochemical analyses revealed that the balance of the antioxidant system was disrupted, eventually leading to oxidative damage to the gills and digestive gland with increasing CIP concentration. Severe histopathological changes appeared along with the oxidative damage. An enlargement of the tubule lumen and thinning of the epithelium in the digestive gland were observed under exposure to high CIP concentrations (0.5 and 2.5 μg/g CIP). In a behavioral assay, the filtration rate of C. fluminea in high concentration exposure groups was clearly inhibited. Moreover, from the integrated biomarker response (IBR) index, the toxicity response gradients of the digestive gland (no substrate--NOS > Sand > Sand and kaolinite clay-- SKC > Sand, kaolinite clay, and organic matter--SCO) and gills (NOS > SCO > SKC > Sand) were different among substrate exposure groups. The most serious histopathological damage and highest siphoning inhibition were observed in the NOS group. The changes in the morphological structure of digestive gland cells in C. fluminea were similar in the other three substrate groups. The inhibition of the filtration rate in the higher concentration groups decreased in the order Sand > SKC > SCO.

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Data availability

The datasets in this study are available from the corresponding author upon reasonable request.

References

  • Arini A, Daffe G, Gonzalez P, Feurtet-Mazel A, Baudrimont M (2014) Detoxification and recovery capacities of Corbicula fluminea after an industrial metal contamination (Cd and Zn): a one-year depuration experiment. Environ Pollut 192:74–82

    Article  CAS  Google Scholar 

  • Aguirre-Martínez GV, DelValls AT, Laura Martín-Díaz M (2015) Yes, caffeine, ibuprofen, carbamazepine, novobiocin and tamoxifen have an effect on Corbicula fluminea (Müller, 1774). Ecotoxicol Environ Saf 120:142–154

    Article  Google Scholar 

  • Beliaeff B, Burgeot T (2002) Integrated biomarker response: a useful tool for ecological risk assessment. Environ Toxicol Chem 21:1316–1322

    Article  CAS  Google Scholar 

  • Boening D (1999) An evaluation of bivalves as biomonitors of heavy metals pollution in marine waters. Environ Monit Assess 55:459–470

    Article  CAS  Google Scholar 

  • Wilson C, Clarke R, D’Arcy BC et al (2005) Persistent pollutants urban rivers sediment survey: implications for pollution control. Water Sci Technol 51(3-4):217–224

    Article  CAS  Google Scholar 

  • Carvalho IT, Santos L (2016) Antibiotics in the aquatic environments: a review of the European scenario. Environ Int 94:736–757

    Article  Google Scholar 

  • Coughlan J (1969) The estimation of filtering rate from the clearance of suspensions. Mar Biol 2:356–358

    Article  Google Scholar 

  • Chen H, Zha J, Liang X, Li J, Wang Z (2014) Effects of the human antiepileptic drug carbamazepine on the behavior, biomarkers, and heat shock proteins in the Asian clam Corbicula fluminea. Aquat Toxicol 155:1–8

    Article  Google Scholar 

  • Chen H, Zha J, Yuan L, Wang Z (2015) Effects of fluoxetine on behavior, antioxidant enzyme systems, and multixenobiotic resistance in the Asian clam Corbicula fluminea. Chemosphere 119:856–862

    Article  CAS  Google Scholar 

  • Chen K, Zhou JL (2014) Occurrence and behavior of antibiotics in water and sediments from the Huangpu River, Shanghai, China. Chemosphere 95:604–612

    Article  CAS  Google Scholar 

  • Cid A, Picado A, Correia JB, Chaves R, Silva H, Caldeira J, de Matos APA, Diniz MS (2015) Oxidative stress and histological changes following exposure to diamond nanoparticles in the freshwater Asian clam Corbicula fluminea (Müller, 1774). J Hazard Mater 284:27–34

    Article  CAS  Google Scholar 

  • Crawford SE, Liber K (2015) Effects of clay minerals and organic matter in formulated sediments on the bioavailability of sediment-associated uranium to the freshwater midge, Chironomus dilutus. Sci Total Environ 532:821–830

    Article  CAS  Google Scholar 

  • Csiszár J, Horváth E, Bela K, Gallé Á (2016) Glutathione-Related enzyme system: glutathione reductase (GR), glutathione transferases (GSTs) and Glutathione peroxidases (GPXs). In: Gupta DK, Palma JM, Corpas FJ (eds) Redox State as a Central Regulator of Plant-Cell Stress Responses. Springer International Publishing, Cham, pp 137–158

    Chapter  Google Scholar 

  • Doherty FG (1990) The Asiatic clam, Corbicula spp., as a biological monitor in freshwater environments. Environ Monit Assess 15:143

    Article  CAS  Google Scholar 

  • Esperanza M, Seoane M, Servia MJ, Cid Á (2020) Effects of Bisphenol A on the microalga Chlamydomonas reinhardtii and the clam Corbicula fluminea. Ecotoxicol Environ Saf 197:110609

    Article  CAS  Google Scholar 

  • Feng C, Guo X, Yin S, Tian C, Li Y, Shen Z (2017) Heavy metal partitioning of suspended particulate matter–water and sediment–water in the Yangtze Estuary. Chemosphere 185:717–725

    Article  CAS  Google Scholar 

  • Feng C, Zhao S, Wang D, Niu J, Shen Z (2014) Sedimentary records of metal speciation in the Yangtze Estuary: role of hydrological events. Chemosphere 107:415–422

    Article  CAS  Google Scholar 

  • Fournier E, Adam C, Massabuau JC, Garnierlaplace J (2005) Bioaccumulation of waterborne selenium in the Asiatic clam Corbicula fluminea: influence of feeding-induced ventilatory activity and selenium species. Aquat Toxicol 72:251–260

    Article  CAS  Google Scholar 

  • Fu L, Huang T, Wang S, Wang X, Su L, Li C, Zhao Y (2017) Toxicity of 13 different antibiotics towards freshwater green algae Pseudokirchneriella subcapitata and their modes of action. Chemosphere 168:217–222

    Article  CAS  Google Scholar 

  • Graney RL, Cherry DS, Cairns J (1984) The influence of substrate, pH, diet and temperature upon cadmium accumulation in the asiatic clam (Corbicula fluminea) in laboratory artificial streams. Water Res 18:833–842

    Article  CAS  Google Scholar 

  • Guilhermino L, Vieira LR, Ribeiro D, Tavares AS, Cardoso V, Alves A, Almeida JM (2018) Uptake and effects of the antimicrobial florfenicol, microplastics and their mixtures on freshwater exotic invasive bivalve Corbicula fluminea. Sci Total Environ 622-623:1131–1142

    Article  CAS  Google Scholar 

  • Guo X, Feng C (2018) Biological toxicity response of Asian Clam (Corbicula fluminea) to pollutants in surface water and sediment. Sci Total Environ 631-632:56–70

    Article  CAS  Google Scholar 

  • Guo X, Feng C, Gu E, Tian C, Shen Z (2019) Spatial distribution, source apportionment and risk assessment of antibiotics in the surface water and sediments of the Yangtze Estuary. Sci Total Environ 671:548–557

    Article  CAS  Google Scholar 

  • Herrero A, Vila J, Eljarrat E, Ginebreda A, Sabater S, Batalla RJ, Barceló D (2018) Transport of sediment borne contaminants in a Mediterranean river during a high flow event. Sci Total Environ 633:1392–1402

    Article  CAS  Google Scholar 

  • Ho KT, Burgess RM, Pelletier MC, Serbst JR, Ryba SA, Cantwell MG, Kuhn A, Raczelowski P (2002) An overview of toxicant identification in sediments and dredged materials. Mar Pollut Bull 44:286–293

    Article  CAS  Google Scholar 

  • Huang Y, Wang Y, Huang Y, Zhang L, Ye F, Wang J, Shang J, Liao Q (2020) Impact of sediment characteristics on adsorption behavior of typical antibiotics in Lake Taihu Chinau. Sci Total Environ 718:137329

    Article  CAS  Google Scholar 

  • Jiang Y, Li M, Guo C, An D, Xu J, Zhang Y, Xi B (2014) Distribution and ecological risk of antibiotics in a typical effluent–receiving river (Wangyang River) in north China. Chemosphere 112:267–274

    Article  CAS  Google Scholar 

  • Jr. G. Allen Burton (2002) Sediment quality criteria in use around the world. Jpn J Limnol 3, 65-76

  • Kaeseberg T, Zhang J, Schubert S, Oertel R, Siedel H, Krebs P (2018) Sewer sediment-bound antibiotics as a potential environmental risk: adsorption and desorption affinity of 14 antibiotics and one metabolite. Environ Pollut 239:638–647

    Article  CAS  Google Scholar 

  • Legeay A, Achard-Joris M, Baudrimont M, Massabuau J, Bourdineaud J (2005) Impact of cadmium contamination and oxygenation levels on biochemical responses in the Asiatic clam Corbicula fluminea. Aquat Toxicol 74:242–253

    Article  CAS  Google Scholar 

  • Li D, Wang P, Wang C, Fan X, Hu B (2018) Combined toxicity of organophosphate flame retardants and cadmium to Corbicula fluminea in aquatic sediments. Environ Pollut 243:S597672460

    Article  Google Scholar 

  • Liu Y, Junaid M, Xu P, Zhong W, Pan B, Xu N (1987) (2020) Suspended sediment exacerbates perfluorooctane sulfonate mediated toxicity through reactive oxygen species generation in freshwater clam Corbicula fluminea. Environ Pollut 267:115671

    Article  Google Scholar 

  • Lubecki L, Kowalewska G (2019) Plastic-derived contaminants in sediments from the coastal zone of the southern Baltic Sea. Mar Pollut Bull 146:255–262

    Article  CAS  Google Scholar 

  • Luo Y, Xu L, Rysz M, Wang Y, Zhang H, Alvarez PJJ (2011) Occurrence and Transport of tetracycline, sulfonamide, quinolone, and macrolide antibiotics in the Haihe River Basin, China. Environ Sci Technol 45:1827–1833

    Article  CAS  Google Scholar 

  • Matić Bujagić I, Grujić S, Laušević M, Hofmann T, Micić V (2019) Emerging contaminants in sediment core from the Iron gate i reservoir on the Danube River. Sci Total Environ 662:77–87

    Article  Google Scholar 

  • Naylor C, Rodrigues C (1995) Development of a test method for Chironomus riparius using a formulated sediment. Chemosphere 31:3291–3303

    Article  CAS  Google Scholar 

  • Ortmann C (2003) (2003) Energy metabolism and valve closure behaviour in the Asian clam Corbicula fluminea. J Exp Biol 206(22):4167–4178

    Article  CAS  Google Scholar 

  • Qi W, Müller B, Pernet-Coudrier B, Singer H, Liu H, Qu J, Berg M (2014) Organic micropollutants in the Yangtze River: seasonal occurrence and annual loads. Sci Total Environ 472:789–799

    Article  CAS  Google Scholar 

  • Ren J, Luo J, Ma H, Wang X, Ma LQ (2013) Bioavailability and oxidative stress of cadmium to Corbicula fluminea. Environ Sci Process Impacts 15:86–869

    Article  Google Scholar 

  • Riaz L, Mahmood T, Khalid A, Rashid A, Ahmed Siddique MB, Kamal A, Coyne MS (2018) Fluoroquinolones (FQs) in the environment: a review on their abundance, sorption and toxicity in soil. Chemosphere 191:704–720

    Article  CAS  Google Scholar 

  • Roman YE, De Schamphelaere KAC, Nguyen LTH, Janssen CR (2007) Chronic toxicity of copper to five benthic invertebrates in laboratory-formulated sediment: sensitivity comparison and preliminary risk assessment. Sci Total Environ 387:128–140

    Article  CAS  Google Scholar 

  • Rusina TP, Smedes F, Brborić M, Vrana B (2019) Investigating levels of organic contaminants in Danube River sediments in Serbia by multi–ratio equilibrium passive sampling. Sci Total Environ 696:133935

    Article  CAS  Google Scholar 

  • Saidani W, Sellami B, Khazri A, Mezni A, Dellali M, Joubert O, Sheehan D, Beyrem H (2019) Metal accumulation, biochemical and behavioral responses on the Mediterranean clams Ruditapes decussatus exposed to two photocatalyst nanocomposites (TiO2 NPs and AuTiO2NPs). Aquat Toxicol 208:71–79

    Article  CAS  Google Scholar 

  • Sajjad. Zare, H.P. (2012) Changes activities of antioxidant enzymes in oilseed rape in response to salinity stress. Int JAgricult Crop Sci 7:398–403

    Google Scholar 

  • Sanchez W, Burgeot T, Porcher JM (2012) A novel “integrated biomarker response” calculation based on reference deviation concept. Environ Sci Pollut Res 20:2721–2725

    Article  Google Scholar 

  • Santos KCD, Martinez CBR (2014) Genotoxic and biochemical effects of atrazine and Roundup ®; alone and in combination, on the Asian clam Corbicula fluminea. Ecotoxicol Environ Saf 100:7–14

    Article  Google Scholar 

  • Shan Y, Yan S, Hong X, Zha J, Qin J (2020) Effect of imidacloprid on the behavior, antioxidant system, multixenobiotic resistance, and histopathology of Asian freshwater clams (Corbicula fluminea). Aquat Toxicol 218:105333

    Article  CAS  Google Scholar 

  • Suzuki J, Nakano D, Imamura M, Yamamoto R, Fujita M (2019) Assessing a polluted river environment by oxidative stress biomarker responses in caddisfly larvae. Sci Total Environ 696:134005

    Article  CAS  Google Scholar 

  • Sheehan D, Meade G, Foley VM, Dowd CA (2001) Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem J 360:1–16

    Article  CAS  Google Scholar 

  • Silva SN, Azevedo AP, Teixeira V, Pina JE, Rueff J, Gaspar JF (2009) The role of GSTA2 polymorphisms and haplotypes in breast cancer susceptibility: a case-control study in the Portuguese population. Oncol Rep 22:593–598

    CAS  Google Scholar 

  • Su T, Shao Q, Wang P, Ma C (2016) Oxidative Stress and its role in peroxisome homeostasis in plants. In: Gupta DK, Palma JM, Corpas FJ (eds) Redox state as a central regulator of plant-cell stress responses. Springer International Publishing, Cham, pp 117–136

    Chapter  Google Scholar 

  • Tolls J (2001) Sorption of veterinary pharmaceuticals in soils: a review. Environ Sci Technol 35:3397–3406

    Article  CAS  Google Scholar 

  • Trchounian A, Petrosyan M, Sahakyan N (2016) Plant Cell redox homeostasis and reactive oxygen species. In: Gupta DK, Palma JM, Corpas FJ (eds) Redox State as a Central Regulator of Plant-Cell Stress Responses. Springer International Publishing, Cham, pp 25–50

    Chapter  Google Scholar 

  • US Environmental Protection Agency (2007) Sediment toxicity identification evaluation (TIE) phases I, II, and III guidance document. EPA 600/R-07/080. Final Report, Washington DC

  • Vale G, Franco C, Diniz MS, Santos MMCD, Domingos RF (2014) Bioavailability of cadmium and biochemical responses on the freshwater bivalve Corbicula fluminea–the role of TiO2 nanoparticles. Ecotoxicol Environ Saf 109:161–168

    Article  CAS  Google Scholar 

  • Wang D, Ning Q, Dong J, Brooks BW, You J (2020) Predicting mixture toxicity and antibiotic resistance of fluoroquinolones and their photodegradation products in Escherichia coli. Environ Pollut 262:114275

    Article  CAS  Google Scholar 

  • Wang Q, Hong X, Chen H, Yuan L, Zha J (2018) The neuropeptides of Asian freshwater clam (Corbicula fluminea) as new molecular biomarker basing on the responses of organophosphate chemicals exposure. Ecotoxicol Environ Saf 160:52–59

    Article  CAS  Google Scholar 

  • Wu Y, Gu E, Li H, Tian C, Feng C (2019) Oxidative stress and histological changes in Corbicula fluminea exposed to nano-Al13 and monomeric Al coagulants. Environ Sci Nano 6:2736–2748

    Article  CAS  Google Scholar 

  • Xu J, Zhang Y, Zhou C, Guo C, Wang D, Du P, Luo Y, Wan J, Meng W (2014) Distribution, sources and composition of antibiotics in sediment, overlying water and pore water from Taihu Lake, China. Sci Total Environ 497-498:267–273

    Article  CAS  Google Scholar 

  • Yan S, Wu H, Qin J, Zha J, Wang Z (2017) Halogen-free organophosphorus flame retardants caused oxidative stress and multixenobiotic resistance in Asian freshwater clams (Corbicula fluminea). Environ Pollut 225:559–568

    Article  CAS  Google Scholar 

  • Yang JF, Ying GG, Zhao JL, Tao R, Su HC, Chen F (2010) Simultaneous determination of four classes of antibiotics in sediments of the Pearl Rivers using RRLC-MS/MS. Sci Total Environ 408:3424–3432

    Article  CAS  Google Scholar 

  • Zhang H, Hong X, Yan S, Zha J, Qin J (2020) Environmentally relevant concentrations of bifenthrin induce changes in behaviour, biomarkers, histological characteristics, and the transcriptome in Corbicula fluminea. Sci Total Environ 728:138821

    Article  CAS  Google Scholar 

  • Zhou Q, Zhang J, Fu J, Shi J, Jiang G (2008) Biomonitoring: an appealing tool for assessment of metal pollution in the aquatic ecosystem. Anal Chim Acta 606:135–150

    Article  CAS  Google Scholar 

  • Zhou J, Broodbank N (2014) Sediment-water interactions of pharmaceutical residues in the river environment. Water Res 48:61–70

    Article  CAS  Google Scholar 

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Funding

This work was supported by the National Natural Science Foundation of China (42007368), the Natural Science Foundation of Guangdong Province (2021A1515011863), and the National Key Research and Development Program of China (2016YFF0204502, 2016YFF0204500).

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Authors and Affiliations

  1. Guangdong Provincal Academic of Environmental Science, Guangzhou, 510045, China

    Xiaoyu Guo

  2. State Key Laboratory of Water Environment Simulation, School of Environment, Beijing Normal University, Beijing, 100875, China

    Chenghong Feng & Akhtar Islam

  3. National Institute of Metrology, Beijing, 100029, China

    Zhe Bi

  4. Guangdong Provincial Key Laboratory of Water Quality Improvement and Ecological Restoration for Watersheds, Institute of Environmental and Ecological Engineering, Guangdong University of Technology, Guangzhou, 510006, China

    Yanpeng Cai

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  1. Xiaoyu Guo
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  2. Chenghong Feng
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  3. Zhe Bi
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  4. Akhtar Islam
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  5. Yanpeng Cai
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Contributions

Xiaoyu Guo: conceptualization, methodology, validation, formal analysis, investigation, data curation, writing - original draft. Chenghong Feng: conceptualization, methodology, validation, formal analysis, investigation, data curation, writing - review & editing, supervision, project administration, funding acquisition. Zhe Bi: review & editing. Akhtar Islam: review & editing. Yanpeng Cai: review & editing.

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Correspondence to Chenghong Feng.

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Approval was obtained from the ethics committee of Beijing Normal University. The benthic bivalve- Corbicula fluminea used in this study was not listed as a protected species in China.

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The authors declare no competing interests.

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Guo, X., Feng, C., Bi, Z. et al. Toxicity effects of ciprofloxacin on biochemical parameters, histological characteristics, and behaviors of Corbicula fluminea in different substrates. Environ Sci Pollut Res 29, 23700–23711 (2022). https://doi.org/10.1007/s11356-021-17509-z

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