Skip to main content

Advertisement

SpringerLink
Log in

Freshwater crustacean exposed to active pharmaceutical ingredients: ecotoxicological effects and mechanisms

  • Review Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Concerns over the ecotoxicological effects of active pharmaceutical ingredients (APIs) on aquatic invertebrates have been raised in the last decade. While numerous studies have reported the toxicity of APIs in invertebrates, no attempt has been made to synthesize and interpret this dataset in terms of different exposure scenarios (acute, chronic, multigenerational), multiple crustacean species, and the toxic mechanisms. In this study, a thorough literature review was performed to summarize the ecotoxicological data of APIs tested on a range of invertebrates. Therapeutic classes including antidepressants, anti-infectives, antineoplastic agents, hormonal contraceptives, immunosuppressants, and neuro-active drugs exhibited higher toxicity to crustaceans than other API groups. The species sensitivity towards APIs exposure is compared in D. magna and other crustacean species. In the case of acute and chronic bioassays, ecotoxicological studies mainly focus on the apical endpoints including growth and reproduction, whereas sex ratio and molting frequency are commonly used for evaluating the substances with endocrine-disrupting properties. The multigenerational and “Omics” studies, primarily transcriptomics and metabolomics, were confined to a few API groups including beta-blocking agents, blood lipid-lowing agents, neuroactive agents, anticancer drugs, and synthetic hormones. We emphasize that in-depth studies on the multigenerational effects and the toxic mechanisms of APIs on the endocrine systems of freshwater crustacean are warranted.

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

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this published article.

References

  • Agatz A, Cole TA, Preuss TG, Zimmer E, Brown CD (2013) Feeding inhibition explains effects of imidacloprid on the growth, maturation, reproduction, and survival of Daphnia magna. Environ Sci Technol 47(6):2909–2917

    Article  CAS  Google Scholar 

  • Alves N, Neuparth T, Barros S, Santos MM (2021) The anti-lipidemic drug simvastatin modifies epigenetic biomarkers in the amphipod Gammarus locusta. Ecotoxicol Environ Saf 209:111849

    Article  CAS  Google Scholar 

  • Ankley GT, Bennett RS, Erickson RJ, Hoff DJ, Hornung MW, Johnson RD, mount DR, Nichols JW, Russom CL, Schmieder PK, Serrano JA, Tietge JE, Villeneuve DL (2010) Adverse outcome pathways: a conceptual framework to support ecotoxicology research and risk assessment. Environ Toxicol Chem 29(3):730–741

  • Anskjaer GG, Rendal C, Kusk KO (2013) Effect of pH on the toxicity and bioconcentration of sulfadiazine on Daphnia magna. Chemosphere 91(8):1183–1188

    Article  CAS  Google Scholar 

  • Arslan-Alaton I, Caglayan AE (2006) Toxicity and biodegradability assessment of raw and ozonated procaine penicillin G formulation effluent. Ecotoxicol Environ Saf 63(1):131–140

    Article  CAS  Google Scholar 

  • Baker TR, Peterson RE, Heideman W (2014) Using zebrafish as a model system for studying the transgenerational effects of dioxin. Toxicol Sci 2:403

    Article  Google Scholar 

  • Barbosa IR, Nogueira AJ, Soares AM (2008) Acute and chronic effects of testosterone and 4-hydroxyandrostenedione to the crustacean Daphnia magna. Ecotoxicol Environ Saf 71(3):757–764

    Article  CAS  Google Scholar 

  • Bas V, Lina G, Erik K, Tobias Ö, Owen SF, Snape JR, Tyler CR (2017) ECOdrug: a database connecting drugs and conservation of their targets across species. Nucleic Acids Res 46(1):930–936

    Google Scholar 

  • Bayer A, Asner R, Schüssler W, Kopf W, Weiss K, Sengl M, Letzel M (2014) Behavior of sartans (antihypertensive drugs) in wastewater treatment plants, their occurrence and risk for the aquatic environment. Environ Sci Pollut Res Int 21(18):10830–10839

    Article  CAS  Google Scholar 

  • Berninger JP, Du B, Connors KA, Eytcheson SA, Kolkmeier MA, Prosser KN, Valenti TW Jr, Chambliss CK, Brooks BW (2011) Effects of the antihistamine diphenhydramine on selected aquatic organisms. Environ Toxicol Chem 30(9):2065–2072

    Article  CAS  Google Scholar 

  • Borgatta M, Decosterd LA, Waridel P, Buclin T, Chevre N (2015) The anticancer drug metabolites endoxifen and 4-hydroxy-tamoxifen induce toxic effects on Daphnia pulex in a two-generation study. Sci Total Environ 520:232–240

    Article  CAS  Google Scholar 

  • Borgatta M, Waridel P, Decosterd LA, Buclin T, Chevre N (2016) Multigenerational effects of the anticancer drug tamoxifen and its metabolite 4-hydroxy-tamoxifen on Daphnia pulex. Sci Total Environ 545–546:21–29

    Article  Google Scholar 

  • Bownik A (2020) Physiological endpoints in daphnid acute toxicity tests. Sci Total Environ 700:134400

    Article  CAS  Google Scholar 

  • Brennan SJ, Brougham CA, Roche JJ, Fogarty AM (2006) Multi-generational effects of four selected environmental oestrogens on Daphnia magna. Chemosphere 64(1):49–55

    Article  CAS  Google Scholar 

  • Brooks BW, Turner PK, Stanley JK, Weston JJ, Glidewell EA, Foran CM, Slattery M, La Point TW, Huggett DB (2003) Waterborne and sediment toxicity of fluoxetine to select organisms. Chemosphere 52(1):135–142

    Article  CAS  Google Scholar 

  • Campos B, Pina B, Barata CC (2012) Mechanisms of action of selective serotonin reuptake inhibitors in Daphnia magna. Environ Sci Technol 46(5):2943–2950

    Article  CAS  Google Scholar 

  • Campos B, Garcia-Reyero N, Rivetti C, Escalon L, Habib T, Tauler R, Tsakovski S, Pina B, Barata C (2013) Identification of metabolic pathways in Daphnia magna explaining hormetic effects of selective serotonin reuptake inhibitors and 4-nonylphenol using transcriptomic and phenotypic responses. Environ Sci Technol 47(16):9434–9443

    Article  CAS  Google Scholar 

  • Campos B, Rivetti C, Kress T, Barata C, Dircksen H (2016) Depressing antidepressant: Fluoxetine affects serotonin neurons causing adverse reproductive responses in Daphnia magna. Environ Sci Technol 50(11):6000–6007

    Article  CAS  Google Scholar 

  • Campos B, Fletcher D, Piña B, Tauler R, Barata C (2018) Differential gene transcription across the life cycle in Daphnia magna using a new all genome custom-made microarray. BMC Genom 19: 370

  • Castro BB, Freches AR, Rodrigues M, Nunes B, Antunes SC (2018) Transgenerational effects of toxicants: An extension of the Daphnia 21-day chronic assay? Arch Environ Contam Toxicol 74(4):616–626

    Article  CAS  Google Scholar 

  • Chen K-F, Huang S-Y, Chung Y-T, Wang K-S, Wang C-K, Chang S-H (2018) Detoxification of nicotine solution using Fe0-based processes: Toxicity evaluation by Daphnia magna neonate and embryo assays. Chem Eng J 331:636–643

    Article  CAS  Google Scholar 

  • Cleuvers M (2003) Aquatic ecotoxicity of pharmaceuticals including the assessment of combination effects. Toxicol Lett 142(3):185–194

    Article  CAS  Google Scholar 

  • Cleuvers M (2004) Mixture toxicity of the anti-inflammatory drugs diclofenac, ibuprofen, naproxen, and acetylsalicylic acid. Ecotoxicol Environ Saf 59(3):309–315

    Article  CAS  Google Scholar 

  • Cleuvers M (2005) Initial risk assessment for three beta-blockers found in the aquatic environment. Chemosphere 59(2):199–205

    Article  CAS  Google Scholar 

  • Cleuvers M (2008) Chronic mixture toxicity of pharmaceuticals to Daphnia – the example of nonsteroidal anti-inflammatory drugs. In: Kümmerer C (ed) Pharmaceuticals in the environment: sources, fate, effects and risks, 3rd edn. Springer, Verlag Berlin Heidelberg, pp 277–284

  • Colbourne JK, Pfrender ME, Gilbert D, Thomas WK, Tucker A (2011) The ecoresponsive genome of Daphnia pulex. Science 331(6017):555

    Article  CAS  Google Scholar 

  • Constantine LA, Huggett DB (2010) A comparison of the chronic effects of human pharmaceuticals on two cladocerans, Daphnia magna and Ceriodaphnia dubia. Chemosphere 80(9):1069–1074

    Article  CAS  Google Scholar 

  • Czech B, Josko I, Oleszczuk P (2014) Ecotoxicological evaluation of selected pharmaceuticals to Vibrio fischeri and Daphnia magna before and after photooxidation process. Ecotoxicol Environ Saf 104:247–253

    Article  CAS  Google Scholar 

  • Dalla Bona M, Di Leva V, De Liguoro M (2014) The sensitivity of Daphnia magna and Daphnia curvirostris to 10 veterinary antibacterials and to some of their binary mixtures. Chemosphere 115:67–74

    Article  CAS  Google Scholar 

  • Dalla Bona M, Zounkova R, Merlanti R, Blaha L, De Liguoro M (2015) Effects of enrofloxacin, ciprofloxacin, and trimethoprim on two generations of Daphnia magna. Ecotoxicol Environ Saf 113:152–158

    Article  CAS  Google Scholar 

  • Daniel D, Dionisio R, de Alkimin GD, Nunes B (2018) Acute and chronic effects of paracetamol exposure on Daphnia magna: How oxidative effects may modulate responses at distinct levels of organization in a model species. Environ Sci Pollut Res Int 26(4):3320–3329

    Article  Google Scholar 

  • Dave G, Herger G (2012) Determination of detoxification to Daphnia magna of four pharmaceuticals and seven surfactants by activated sludge. Chemosphere 88(4):459–466

    Article  CAS  Google Scholar 

  • De Liguoro M, Fioretto B, Poltronieri C, Gallina G (2009) The toxicity of sulfamethazine to Daphnia magna and its additivity to other veterinary sulfonamides and trimethoprim. Chemosphere 75(11):1519–1524

    Article  Google Scholar 

  • De Liguoro M, Di Leva V, Gallina G, Faccio E, Pinto G, Pollio A (2010) Evaluation of the aquatic toxicity of two veterinary sulfonamides using five test organisms. Chemosphere 81(6):788–793

    Article  Google Scholar 

  • De Liguoro M, Di Leva V, Dalla Bona M, Merlanti R, Caporale G, Radaelli G (2012) Sublethal effects of trimethoprim on four freshwater organisms. Ecotoxicol Environ Saf 82:114–121

    Article  Google Scholar 

  • De Liguoro M, Riga A, Fariselli P (2018) Synergistic toxicity of some sulfonamide mixtures on Daphnia magna. Ecotoxicol Environ Saf 164:84–91

    Article  Google Scholar 

  • De Liguoro M, Maraj S, Merlanti R (2019) Transgenerational toxicity of flumequine over four generations of Daphnia magna. Ecotoxicol Environ Saf 169:814–821

    Article  Google Scholar 

  • DellaGreca M, Fiorentino A, Isidori M, Lavorgna M, Previtera L, Rubino M, Temussi F (2004) Toxicity of prednisolone, dexamethasone and their photochemical derivatives on aquatic organisms. Chemosphere 54(5):629–637

    Article  CAS  Google Scholar 

  • DellaGreca M, Iesce MR, Isidori M, Nardelli A, Previtera L, Rubino M (2007) Phototransformation products of tamoxifen by sunlight in water. Toxicity of the drug and its derivatives on aquatic organisms. Chemosphere 67(10):1933–1939

    Article  CAS  Google Scholar 

  • Di Lorenzo T, Di Cicco M, Di Censo D, Galante A, Boscaro F, Messana G, Galassi DMP (2019) Environmental risk assessment of propranolol in the groundwater bodies of Europe. Environ Pollut 255:113189

    Article  Google Scholar 

  • Di Lorenzo T, Cifoni M, Baratti M, Pieraccini G, Di Marzio WD, Galassi DMP (2021) Four scenarios of environmental risk of diclofenac in European groundwater ecosystems. Environ Pollut 287:117315

    Article  Google Scholar 

  • Dietrich S, Ploessl F, Bracher F, Laforsch C (2010) Single and combined toxicity of pharmaceuticals at environmentally relevant concentrations in Daphnia magna – A multigenerational study. Chemosphere 79(1):60–66

    Article  CAS  Google Scholar 

  • Ding J, Lu G, Liu J, Yang H, Li Y (2016) Uptake, depuration, and bioconcentration of two pharmaceuticals, roxithromycin and propranolol, in Daphnia magna. Ecotoxicol Environ Saf 126:85–93

    Article  CAS  Google Scholar 

  • Dionisio R, Daniel D, Alkimin GD, Nunes B (2020) Multi-parametric analysis of ciprofloxacin toxicity at ecologically relevant levels: Short- and long-term effects on Daphnia magna. Environ Toxicol Pharmacol 74:103295

    Article  CAS  Google Scholar 

  • Dong F, Li J, Chankvetadze B, Cheng Y, Xu J, Liu X, Li Y, Chen X, Bertucci C, Tedesco D, Zanasi R, Zheng Y (2013) Chiral triazole fungicide difenoconazole: absolute stereochemistry, stereoselective bioactivity, aquatic toxicity, and environmental behavior in vegetables and soil. Environ Sci Technol 47(7):3386–3394

    Article  CAS  Google Scholar 

  • Donk EV, Peacor S, Grosser K, Domis L, Lürling M (2016) Pharmaceuticals may disrupt natural chemical information flows and species interactions in aquatic systems: Ideas and perspectives on a hidden global change. Rev Environ Contam Toxicol 238: 91–105

  • Drzymala J, Kalka J (2020) Ecotoxic interactions between pharmaceuticals in mixtures: Diclofenac and sulfamethoxazole. Chemosphere 259:127407

    Article  CAS  Google Scholar 

  • Du J, Mei CF, Ying GG, Xu MY (2016) Toxicity Thresholds for diclofenac, acetaminophen and ibuprofen in the water flea Daphnia magna. Bull Environ Contam Toxicol 97(1):84–90

    Article  CAS  Google Scholar 

  • Dzialowski EM, Turner PK, Brooks BW (2006) Physiological and reproductive effects of beta adrenergic receptor antagonists in Daphnia magna. Arch Environ Contam Toxicol 50(4):503–510

    Article  CAS  Google Scholar 

  • Ebele AJ, Abou-Elwafa Abdallah M, Harrad S (2017) Pharmaceuticals and personal care products (PPCPs) in the freshwater aquatic environment. Emerg Contam 3(1):1–16

    Article  Google Scholar 

  • Emara Y, Lehmann A, Siegert MW, Finkbeiner M (2018) Modeling pharmaceutical emissions and their toxicity-related effects in life cycle assessment (LCA): A review. Integr Environ Assess Manag 15(1):6–18

    Article  Google Scholar 

  • Férard J-F, Blaise C (2013) Encyclopedia of Aquatic Ecotoxicology. Springer, Dordrecht, Netherlands

    Book  Google Scholar 

  • Fuertes I, Barata C (2021) Characterization of neurotransmitters and related metabolites in Daphnia magna juveniles deficient in serotonin and exposed to neuroactive chemicals that affect its behavior: A targeted LC-MS/MS method. Chemosphere 263:127814

    Article  CAS  Google Scholar 

  • Fuertes I, Campos B, Rivetti C, Pina B, Barata C (2019) Effects of single and combined low concentrations of neuroactive drugs on Daphnia magna reproduction and transcriptomic responses. Environ Sci Technol 53(20):11979–11987

    Article  CAS  Google Scholar 

  • Fuertes I, Pina B, Barata C (2020) Changes in lipid profiles in Daphnia magna individuals exposed to low environmental levels of neuroactive pharmaceuticals. Sci Total Environ 733:139029

    Article  CAS  Google Scholar 

  • Galdiero E, Maselli V, Falanga A, Gesuele R, Galdiero S, Fulgione D, Guida M (2015) Integrated analysis of the ecotoxicological and genotoxic effects of the antimicrobial peptide melittin on Daphnia magna and Pseudokirchneriella subcapitata. Environ Pollut 203:145–152

    Article  CAS  Google Scholar 

  • Gallina G, Poltronieri C, Merlanti R, De Liguoro M (2008) Acute toxicity evaluation of four antibacterials with Daphnia magna. Vet Res Commun 32(S1):287–290

    Article  Google Scholar 

  • Godoy AA, Oliveira AC, Silva JGM, Azevedo CCJ, Domingues I, Nogueira AJA, Kummrow F (2019) Single and mixture toxicity of four pharmaceuticals of environmental concern to aquatic organisms, including a behavioral assessment. Chemosphere 235:373–382

    Article  CAS  Google Scholar 

  • Gomez-Canela C, Rovira Garcia X, Martinez-Jeronimo F, Marce RM, Barata C (2019) Analysis of neurotransmitters in Daphnia magna affected by neuroactive pharmaceuticals using liquid chromatography-high resolution mass spectrometry. Environ Pollut 254:113029

    Article  CAS  Google Scholar 

  • Gomez-Olivan LM, Galar-Martinez M, Islas-Flores H, Garcia-Medina S, SanJuan-Reyes N (2014) DNA damage and oxidative stress induced by acetylsalicylic acid in Daphnia magna. Comp Biochem Physiol C Toxicol Pharmacol 164:21–26

    Article  CAS  Google Scholar 

  • Grabarczyk L, Mulkiewicz E, Stolte S, Puckowski A, Pazda M, Stepnowski P, Bialk-Bielinska A (2020) Ecotoxicity screening evaluation of selected pharmaceuticals and their transformation products towards various organisms. Environ Sci Pollut Res Int 27(21):26103–26114

    Article  CAS  Google Scholar 

  • Guo J, Sinclair CJ, Selby K, Boxall AB (2016) Toxicological and ecotoxicological risk-based prioritization of pharmaceuticals in the natural environment. Environ Toxicol Chem 35(6):1550–1559

    Article  CAS  Google Scholar 

  • Haap T, Triebskorn R, Kohler HR (2008) Acute effects of diclofenac and DMSO to Daphnia magna: immobilisation and hsp70-induction. Chemosphere 73(3):353–359

    Article  CAS  Google Scholar 

  • Haeba MH, Hilscherova K, Mazurova E, Blaha L (2008) Selected endocrine disrupting compounds (vinclozolin, flutamide, ketoconazole and dicofol): effects on survival, occurrence of males, growth, molting and reproduction of Daphnia magna. Environ Sci Pollut Res Int 15(3):222–227

    Article  CAS  Google Scholar 

  • Han S, Choi K, Kim J, Ji K, Kim S, Ahn B, Yun J, Choi K, Khim JS, Zhang X, Giesy JP (2010) Endocrine disruption and consequences of chronic exposure to ibuprofen in Japanese medaka (Oryzias latipes) and freshwater cladocerans Daphnia magna and Moina macrocopa. Aquat Toxicol 98(3):256–264

    Article  CAS  Google Scholar 

  • Hansen LK, Frost PC, Larson JH, Metcalfe CD (2008) Poor elemental food quality reduces the toxicity of fluoxetine on Daphnia magna. Aquat Toxicol 86(1):99–103

    Article  CAS  Google Scholar 

  • Heckmann LH, Callaghan A, Hooper HL, Connon R, Hutchinson TH, Maund SJ, Sibly RM (2007) Chronic toxicity of ibuprofen to Daphnia magna: Effects on life history traits and population dynamics. Toxicol Lett 172(3):137–145

    Article  CAS  Google Scholar 

  • Hosamani N, Reddy BS, Reddy PR (2017) Crustacean molting: Regulation and effects of environmental toxicants. J Mar Sci Res Dev 7(5): 1000236

  • Huggett DB, Brooks BW, Peterson B, Foran CM, Schlenk D (2001) Toxicity of select beta adrenergic receptor-blocking pharmaceuticals (B-blockers) on aquatic organisms. Arch Environ Contam Toxicol 43(2):229–235

    Article  Google Scholar 

  • Isidori M, Lavorgna M, Nardelli A, Pascarella L, Parrella A (2005) Toxic and genotoxic evaluation of six antibiotics on non-target organisms. Sci Total Environ 346(1–3):87–98

    Article  CAS  Google Scholar 

  • Jeong TY, Kim TH, Kim SD (2016) Bioaccumulation and biotransformation of the beta-blocker propranolol in multigenerational exposure to Daphnia magna. Environ Pollut 216:811–818

    Article  CAS  Google Scholar 

  • Jeong TY, Asselman J, De Schamphelaere KAC, Van Nieuwerburgh F, Deforce D, Kim SD (2018a) Effect of beta-adrenergic receptor agents on cardiac structure and function and whole-body gene expression in Daphnia magna. Environ Pollut 241:869–878

    Article  CAS  Google Scholar 

  • Jeong TY, Yoon D, Kim S, Kim HY, Kim SD (2018b) Mode of action characterization for adverse effect of propranolol in Daphnia magna based on behavior and physiology monitoring and metabolite profiling. Environ Pollut 233:99–108

    Article  CAS  Google Scholar 

  • Ji K, Kim S, Han S, Seo J, Lee S, Park Y, Choi K, Kho YL, Kim PG, Park J, Choi K (2012) Risk assessment of chlortetracycline, oxytetracycline, sulfamethazine, sulfathiazole, and erythromycin in aquatic environment: are the current environmental concentrations safe? Ecotoxicology 21(7):2031–2050

    Article  CAS  Google Scholar 

  • Jureczko M, Przystas W (2019) Ecotoxicity risk of presence of two cytostatic drugs: Bleomycin and vincristine and their binary mixture in aquatic environment. Ecotoxicol Environ Saf 172:210–215

    Article  CAS  Google Scholar 

  • Kamaya Y, Fukaya Y, Suzuki K (2005) Acute toxicity of benzoic acids to the crustacean Daphnia magna. Chemosphere 59(2):255–261

    Article  CAS  Google Scholar 

  • Kang HM, Kim MS, Hwang UK, Jeong CB, Lee JS (2019) Effects of methylparaben, ethylparaben, and propylparaben on life parameters and sex ratio in the marine copepod Tigriopus japonicus. Chemosphere 226:388–394

    Article  CAS  Google Scholar 

  • Kashian DR (2003) Effects of vertebrate hormones on development and sex determination in Daphnia magna. Environ Toxicol Chem 23(5):1282–1288

    Article  Google Scholar 

  • Kim Y, Choi K, Jung J, Park S, Kim PG, Park J (2007) Aquatic toxicity of acetaminophen, carbamazepine, cimetidine, diltiazem and six major sulfonamides, and their potential ecological risks in Korea. Environ Int 33(3):370–375

    Article  CAS  Google Scholar 

  • Kim HY, Yu SH, Lee MJ, Kim TH, Kim SD (2009a) Radiolysis of selected antibiotics and their toxic effects on various aquatic organisms. Radiat Phys Chem 78(4):267–272

    Article  CAS  Google Scholar 

  • Kim J, Park Y, Choi K (2009b) Phototoxicity and oxidative stress responses in Daphnia magna under exposure to sulfathiazole and environmental level ultraviolet B irradiation. Aquat Toxicol 91(1):87–94

    Article  CAS  Google Scholar 

  • Kim HY, Lee MJ, Yu SH, Kim SD (2012a) The individual and population effects of tetracycline on Daphnia magna in multigenerational exposure. Ecotoxicology 21(4):993–1002

    Article  CAS  Google Scholar 

  • Kim P, Park Y, Ji K, Seo J, Lee S, Choi K, Kho Y, Park J, Choi K (2012b) Effect of chronic exposure to acetaminophen and lincomycin on Japanese medaka (Oryzias latipes) and freshwater cladocerans Daphnia magna and Moina macrocopa, and potential mechanisms of endocrine disruption. Chemosphere 89(1):10–18

    Article  CAS  Google Scholar 

  • Kim HY, Yu S, Jeong TY, Kim SD (2014) Relationship between transgenerational effects of tetracycline on Daphnia magna at the physiological and whole organism level. Environ Pollut 191:111–118

    Article  CAS  Google Scholar 

  • Kim HJ, Koedrith P, Seo YR (2015) Ecotoxicogenomic approaches for understanding molecular mechanisms of environmental chemical toxicity using aquatic invertebrate, Daphnia model organism. Int J Mol Sci 16(6):12261–12287

    Article  CAS  Google Scholar 

  • Kim B, Ji K, Kho Y, Kim PG, Park K, Kim K, Kim Y, Kim KT, Choi K (2017a) Effects of chronic exposure to cefadroxil and cefradine on Daphnia magna and Oryzias latipes. Chemosphere 185:844–851

    Article  CAS  Google Scholar 

  • Kim HY, Asselman J, Jeong TY, Yu S, De Schamphelaere KAC, Kim SD (2017b) Multigenerational effects of the antibiotic tetracycline on transcriptional responses of Daphnia magna and its relationship to higher levels of biological organizations. Environ Sci Technol 51(21):12898–12907

    Article  CAS  Google Scholar 

  • Kimberly DA, Salice CJ (2015) Multigenerational contaminant exposures produce non-monotonic, transgenerational responses in Daphnia magna. Environ Pollut 207:176–182

    Article  CAS  Google Scholar 

  • Kolar B, Arnus L, Jeretin B, Gutmaher A, Drobne D, Durjava MK (2014) The toxic effect of oxytetracycline and trimethoprim in the aquatic environment. Chemosphere 115:75–80

    Article  CAS  Google Scholar 

  • Kovacevic V, Simpson AJ, Simpson MJ (2016) (1)H NMR-based metabolomics of Daphnia magna responses after sub-lethal exposure to triclosan, carbamazepine and ibuprofen. Comp Biochem Physiol Part D Genomics Proteomics 19:199–210

    Article  CAS  Google Scholar 

  • Kovacevic V, Simpson AJ, Simpson MJ (2019) The concentration of dissolved organic matter impacts the metabolic response in Daphnia magna exposed to 17alpha-ethynylestradiol and perfluorooctane sulfonate. Ecotoxicol Environ Saf 170:468–478

    Article  CAS  Google Scholar 

  • Kristofco LA, Du B, Chambliss CK, Berninger JP, Brooks BW (2014) Comparative pharmacology and toxicology of pharmaceuticals in the environment: diphenhydramine protection of diazinon toxicity in Danio rerio but not Daphnia magna. AAPS J 17(1):175–183

    Article  Google Scholar 

  • Kusk H (2000) Acute and chronic toxicity of veterinary antibiotics to Daphnia magna. Chemosphere 40(7):723–730

    Article  Google Scholar 

  • Kwak K, Ji K, Kho Y, Kim P, Lee J, Ryu J, Choi K (2018) Chronic toxicity and endocrine disruption of naproxen in freshwater waterfleas and fish, and steroidogenic alteration using H295R cell assay. Chemosphere 204:156–162

    Article  CAS  Google Scholar 

  • Lamichhane K, Garcia SN, Huggett DB, Deangelis DL, La Point TW (2014) Exposures to a selective serotonin reuptake inhibitor (SSRI), sertraline hydrochloride, over multiple generations: changes in life history traits in Ceriodaphnia dubia. Ecotoxicol Environ Saf 101:124–130

    Article  CAS  Google Scholar 

  • LeBlanc GA (2007) Crustacean endocrine toxicology: a review. Ecotoxicology 16(1):61–81

    Article  CAS  Google Scholar 

  • Lee J, Ji K, Lim Kho Y, Kim P, Choi K (2011) Chronic exposure to diclofenac on two freshwater cladocerans and Japanese medaka. Ecotoxicol Environ Saf 74(5):1216–1225

    Article  CAS  Google Scholar 

  • Lee S, Jung D, Kho Y, Ji K, Kim P, Ahn B, Choi K (2015) Ecotoxicological assessment of cimetidine and determination of its potential for endocrine disruption using three test organisms: Daphnia magna, Moina macrocopa, and Danio rerio. Chemosphere 135:208–216

    Article  CAS  Google Scholar 

  • Lee J, Park N, Kho Y, Lee K, Ji K (2017) Phototoxicity and chronic toxicity of methyl paraben and 1,2-hexanediol in Daphnia magna. Ecotoxicology 26(1):81–89

    Article  CAS  Google Scholar 

  • Lee BY, Choi BS, Kim MS, Park JC, Jeong CB, Han J, Lee JS (2019) The genome of the freshwater water flea Daphnia magna: A potential use for freshwater molecular ecotoxicology. Aquat Toxicol 210:69–84

    Article  CAS  Google Scholar 

  • Lei Y, Guo J, Chen Q, Mo J, Tian Y, Iwata H, Song J (2022) Transcriptomic alterations in water flea (Daphnia magna) following pravastatin treatments: Insect hormone biosynthesis and energy metabolism. Toxics 10(3):110

    Article  CAS  Google Scholar 

  • Leung KMY (2018) Joining the dots between omics and environmental management. Integr Environ Assess Manag 14(2):169–173

    Article  Google Scholar 

  • Li SW, Wang YH, Lin AY (2017) Ecotoxicological effect of ketamine: Evidence of acute, chronic and photolysis toxicity to Daphnia magna. Ecotoxicol Environ Saf 143:173–179

    Article  CAS  Google Scholar 

  • Li J, Carter LJ, Boxall ABA (2020) Evaluation and development of models for estimating the sorption behaviour of pharmaceuticals in soils. J Hazard Mater 392:122469

    Article  CAS  Google Scholar 

  • Liu Y, Ding R, Pan B, Wang L, Liu S, Nie X (2019) Simvastatin affect the expression of detoxification-related genes and enzymes in Daphnia magna and alter its life history parameters. Ecotoxicol Environ Saf 182:109389

    Article  CAS  Google Scholar 

  • Lomba L, Lapeña D, Ros N, Aso E, Cannavò M, Errazquin D, Giner B (2020) Ecotoxicological study of six drugs in Aliivibrio fischeri, Daphnia magna and Raphidocelis subcapitata. Environ Sci Pollut Res Int 27(9):9891–9900

    Article  CAS  Google Scholar 

  • Lonappan L, Brar SK, Das RK, Verma M, Surampalli RY (2016) Diclofenac and its transformation products: Environmental occurrence and toxicity - A review. Environ Int 96:127–138

    Article  CAS  Google Scholar 

  • Luo T, Chen J, Li X, Zhang S, Yao H, Peijnenburg W (2018) Effects of lomefloxacin on survival, growth and reproduction of Daphnia magna under simulated sunlight radiation. Ecotoxicol Environ Saf 166:63–70

    Article  CAS  Google Scholar 

  • Martins A, Guimaraes L, Guilhermino L (2013) Chronic toxicity of the veterinary antibiotic florfenicol to Daphnia magna assessed at two temperatures. Environ Toxicol Pharmacol 36(3):1022–1032

    Article  CAS  Google Scholar 

  • Maselli V, Siciliano A, Giorgio A, Falanga A, Galdiero S, Guida M, Fulgione D, Galdiero E (2017) Multigenerational effects and DNA alterations of QDs-Indolicidin on Daphnia magna. Environ Pollut 224:597–605

    Article  CAS  Google Scholar 

  • Meredith-Williams M, Carter LJ, Fussell R, Raffaelli D, Ashauer R, Boxall A (2011) Uptake and depuration of pharmaceuticals in aquatic invertebrates. Environ Pollut 165:250–258

    Article  Google Scholar 

  • Miller TH, Bury NR, Owen SF, MacRae JI, Barron LP (2018) A review of the pharmaceutical exposome in aquatic fauna. Environ Pollut 239:129–146

    Article  CAS  Google Scholar 

  • Minagh E, Hernan R, O’Rourke K, Lyng FM, Davoren M (2009) Aquatic ecotoxicity of the selective serotonin reuptake inhibitor sertraline hydrochloride in a battery of freshwater test species. Ecotoxicol Environ Saf 72(2):434–440

    Article  CAS  Google Scholar 

  • Minguez L, Ballandonne C, Rakotomalala C, Dubreule C, Kientz-Bouchart V, Halm-Lemeille MP (2014a) Transgenerational effects of two antidepressants (sertraline and venlafaxine) on Daphnia magna life history traits. Environ Sci Technol 49(2):1148–1155

    Article  Google Scholar 

  • Minguez L, Di Poi C, Farcy E, Ballandonne C, Benchouala A, Bojic C, Cossu-Leguille C, Costil K, Serpentini A, Lebel JM, Halm-Lemeille MP (2014b) Comparison of the sensitivity of seven marine and freshwater bioassays as regards antidepressant toxicity assessment. Ecotoxicology 23(9):1744–1754

    Article  CAS  Google Scholar 

  • Miyakawa H, Iguchi T (2017) Comparative luciferase assay for establishing reliable in vitro screening system of juvenile hormone agonists. J Appl Toxicol 37(9):1082–1090

    Article  CAS  Google Scholar 

  • Miyakawa H, Toyota K, Hirakawa I, Ogino Y, Miyagawa S, Oda S, Tatarazako N, Miura T, Colbourne JK, Iguchi T (2013) A mutation in the receptor methoprene-tolerant alters juvenile hormone response in insects and crustaceans. Nat Commun 4:1856

    Article  Google Scholar 

  • Miyakawa H, Sato T, Song Y, Tollefsen KE, Iguchi T (2018) Ecdysteroid and juvenile hormone biosynthesis, receptors and their signaling in the freshwater microcrustacean Daphnia. J Steroid Biochem Mol Biol 184:62–68

    Article  CAS  Google Scholar 

  • Neuparth T, Martins C, Carmen B, Costa MH, Martins I, Costa PM, Santos MM (2014) Hypocholesterolaemic pharmaceutical simvastatin disrupts reproduction and population growth of the amphipod Gammarus locusta at the ng/L range. Aquat Toxicol 155:337–347

    Article  CAS  Google Scholar 

  • Neuparth T, Lopes AI, Alves N, Oliveira JMA, Santos MM (2019) Does the antidepressant sertraline show chronic effects on aquatic invertebrates at environmentally relevant concentrations? A case study with the keystone amphipod. Gammarus Locusta Ecotoxicol Environ Saf 183:109486

    Article  CAS  Google Scholar 

  • Neuparth T, Machado AM, Montes R, Rodil R, Barros S, Alves N, Ruivo R, Castro L Filipe C, Quintana JB Santos MM (2020a) Transcriptomic data on the transgenerational exposure of the keystone amphipod Gammarus locusta to simvastatin. Data Brief 32: 106248

  • Neuparth T, Machado AM, Montes R, Rodil R, Barros S, Alves N, Ruivo R, Castro L Filipe C, Quintana JB, Santos MM (2020b) Transgenerational inheritance of chemical-induced signature: A case study with simvastatin. Environ Int 144:106020

  • Neuparth T, Alves N, Machado AM, Pinheiro M, Montes R, Rodil R, Barros S, Ruivo R, Castro L Filipe C, Quintana JB, Santos MM (2022) Neuroendocrine pathways at risk? Simvastatin induces inter and transgenerational disruption in the keystone amphipod Gammarus locusta. Aquatic Toxicol 244:106095

  • Nielsen ME, Roslev P (2018) Behavioral responses and starvation survival of Daphnia magna exposed to fluoxetine and propranolol. Chemosphere 211:978–985

    Article  CAS  Google Scholar 

  • Nunes B, Antunes SC, Santos J, Martins L, Castro BB (2014) Toxic potential of paracetamol to freshwater organisms: a headache to environmental regulators? Ecotoxicol Environ Saf 107:178–185

    Article  CAS  Google Scholar 

  • OECD (2012) Guidelines for the Testing of Chemicals, Paris: Organization for Economic Co-operation and Development, Daphnia magna reproduction Test 211. https://www.oecd.org/chemicalsafety/test-no-211-daphnia-magna-reproduction-test-9789264185203-en.htm. Accessed 11 Dec 2022

  • Parrella A, Lavorgna M, Criscuolo E, Russo C, Fiumano V, Isidori M (2014) Acute and chronic toxicity of six anticancer drugs on rotifers and crustaceans. Chemosphere 115:59–66

    Article  CAS  Google Scholar 

  • Parrella A, Lavorgna M, Criscuolo E, Russo C, Isidori M (2015) Eco-genotoxicity of six anticancer drugs using comet assay in daphnids. J Hazard Mater 286:573–580

    Article  CAS  Google Scholar 

  • Peng Y, Luo Y, Nie XP, Liao W, Yang YF, Ying GG (2013) Toxic effects of triclosan on the detoxification system and breeding of Daphnia magna. Ecotoxicology 22(9):1384–1394

    Article  CAS  Google Scholar 

  • Qi Q, Li Q, Li J, Mo J, Tian Y, Guo J (2022) Transcriptomic analysis and transgenerational effects of ZnO nanoparticles on Daphnia magna: Endocrine-disrupting potential and energy metabolism. Chemosphere 290:133362

    Article  CAS  Google Scholar 

  • Riessen HP, Young JD (2005) Daphnia defense strategies in fishless lakes and ponds: one size does not fit all. J Plankton Res 27(6):531–544

    Article  Google Scholar 

  • Robledo-Sanchez KCM, Guevara-Pantoja FJ, Ruiz-Suarez JC (2019) Video-tracking and high-speed bright field microscopy allow the determination of swimming and cardiac effects of D. magna exposed to local anaesthetics. Sci Total Environ 691:278–283

    Article  CAS  Google Scholar 

  • Rocha R, Goncalves F, Marques C, Nunes B (2013) Environmental effects of anticholinesterasic therapeutic drugs on a crustacean species, Daphnia magna. Environ Sci Pollut Res Int 21(6):4418–4429

    Article  Google Scholar 

  • Russo C, Isidori M, Deaver JA, Poynton HC (2018) Toxicogenomic responses of low level anticancer drug exposures in Daphnia magna. Aquat Toxicol 203:40–50

    Article  CAS  Google Scholar 

  • Sanderson H (2003) Probabilistic hazard assessment of environmentally occurring pharmaceuticals toxicity to fish, daphnids and algae by ECOSAR screening. Toxicol Lett 144(3):383–395

    Article  CAS  Google Scholar 

  • Schluter-Vorberg L, Coors A (2019) Impact of an immunosuppressive human pharmaceutical on the interaction of a bacterial parasite and its invertebrate host. Aquat Toxicol 206:91–101

    Article  Google Scholar 

  • Schmid S, Song Y, Tollefsen KE (2021) AOP Report: Inhibition of Chitin Synthase 1 Leading to Increased Mortality in Arthropods. Environ Toxicol Chem 40(8):2112–2120

    Article  CAS  Google Scholar 

  • Silva AR, Cardoso DN, Cruz A, Lourenco J, Mendo S, Soares AM, Loureiro S (2015) Ecotoxicity and genotoxicity of a binary combination of triclosan and carbendazim to Daphnia magna. Ecotoxicol Environ Saf 115:279–290

    Article  CAS  Google Scholar 

  • Song Y, Evenseth LM, Iguchi T, Tollefsen KE (2017) Release of chitobiase as an indicator of potential molting disruption in juvenile Daphnia magna exposed to the ecdysone receptor agonist 20-hydroxyecdysone. J Toxicol Environ Health Part A 80(16–18):954–962

    Article  CAS  Google Scholar 

  • Sousa AP, Nunes B (2020) Standard and biochemical toxicological effects of zinc pyrithione in Daphnia magna and Daphnia longispina. Environ Toxicol Pharmacol 80:103402

    Article  CAS  Google Scholar 

  • Stanley JK, Ramirez AJ, Chambliss CK, Brooks BW (2007) Enantiospecific sublethal effects of the antidepressant fluoxetine to a model aquatic vertebrate and invertebrate. Chemosphere 69(1):9–16

    Article  CAS  Google Scholar 

  • Steinkey D, Lari E, Woodman SG, Luong KH, Wong CS, Pyle GG (2018) Effects of gemfibrozil on the growth, reproduction, and energy stores of Daphnia magna in the presence of varying food concentrations. Chemosphere 192:75–80

    Article  CAS  Google Scholar 

  • Tian Y, Xia X, Wang J, Zhu L, Wang J, Zhang F, Ahmad Z (2019) Chronic Toxicological Effects of Carbamazepine on Daphnia magna straus: Effects on reproduction traits, body length, and intrinsic growth. Bull Environ Contam Toxicol 103(5):723–728

    Article  CAS  Google Scholar 

  • Tkaczyk A, Bownik A, Dudka J, Kowal K, Ślaska B (2021) Daphnia magna model in the toxicity assessment of pharmaceuticals: A review. Sci Total Environ 763:143038

    Article  CAS  Google Scholar 

  • Toyota K, Kato Y, Sato M, Sugiura N, Miyagawa S, Miyakawa H, Watanabe H, Oda S, Ogino Y, Hiruta C, Mizutani T, Tatarazako N, Paland S, Jackson C, Colbourne JK, Iguchi T (2013) Molecular cloning of doublesex genes of four cladocera (water flea) species. BMC Genom 14:239

  • Toyota K, Miyakawa H, Yamaguchi K, Shigenobu S, Ogino Y, Tatarazako N, Miyagawa S, Iguchi T (2015) NMDA receptor activation upstream of methyl farnesoate signaling for short day-induced male offspring production in the water flea, Daphnia pulex. BMC Genom 16:186

  • Trombini C, Hampel M, Blasco J (2016) Evaluation of acute effects of four pharmaceuticals and their mixtures on the copepod Tisbe battagliai. Chemosphere 155:319–328

    Article  CAS  Google Scholar 

  • Tsui M, Wang WX (2010) Maternal transfer efficiency and transgenerational toxicity of methylmercury in Daphnia magna. Environ Toxicol Chem 23(6):1504–1511

    Article  Google Scholar 

  • Valimana-Traverso J, Amariei G, Boltes K, Garcia MA, Marina ML (2019) Enantiomer stability and combined toxicity of duloxetine and econazole on Daphnia magna using real concentrations determined by capillary electrophoresis. Sci Total Environ 670:770–778

    Article  CAS  Google Scholar 

  • Vandegehuchte MB, Lemiere F, Vanhaecke L, Vanden Berghe W, Janssen CR (2010) Direct and transgenerational impact on Daphnia magna of chemicals with a known effect on DNA methylation. Comp Biochem Physiol C Toxicol Pharmacol 151(3):278–285

    Article  Google Scholar 

  • Varano V, Fabbri E, Pasteris A (2017) Assessing the environmental hazard of individual and combined pharmaceuticals: acute and chronic toxicity of fluoxetine and propranolol in the crustacean Daphnia magna. Ecotoxicology 26(6):711–728

    Article  CAS  Google Scholar 

  • Vieira M, Soares A, Nunes B (2019) Biomarker-based assessment of the toxicity of the antifungal clotrimazol to the microcrustacean Daphnia magna. Environ Toxicol Pharmacol 71:103210

    Article  CAS  Google Scholar 

  • Watanabe H, Tamura I, Abe R, Takanobu H, Nakamura A, Suzuki T, Hirose A, Nishimura T, Tatarazako N (2015) Chronic toxicity of an environmentally relevant mixture of pharmaceuticals to three aquatic organisms (alga, daphnid, and fish). Environ Toxicol Chem 35(4):996–1006

    Article  Google Scholar 

  • Wilkinson JL, Hooda PS, Barker J, Barton S, Swinden J (2015) Ecotoxic pharmaceuticals, personal care products, and other emerging contaminants: A review of environmental, receptor-mediated, developmental, and epigenetic toxicity with discussion of proposed toxicity to humans. Crit Rev Environ Sci Technol 46(4):336–381

    Article  Google Scholar 

  • Wu W, Kong D, Zhang W, Bu Y, Li J, Shan Z (2020) Acute toxicity of fluazinam to aquatic organisms and its bioaccumulation in Brachydanio rerio. Environ Sci Pollut Res Int 27(28):35000–35007

    Article  CAS  Google Scholar 

  • Zhang X, Xia P, Wang P, Yang J, Baird DJ (2018a) Omics advances in ecotoxicology. Environ Sci Technol 52(7):3842–3851

    Article  CAS  Google Scholar 

  • Zhang Y, Guo P, Wu Y, Zhang X, Wang M, Yang S, Su H (2018b) Evaluation of the subtle effects and oxidative stress response of chloramphenicol, thiamphenicol, and florfenicol in Daphnia magna. Environ Toxicol Chem 38(3):575–584

    Google Scholar 

  • Zhang P, Yan Z, Lu G, Ji Y (2019) Single and combined effects of microplastics and roxithromycin on Daphnia magna. Environ Sci Pollut Res Int 26(17):17010–17020

    Article  CAS  Google Scholar 

  • Zhang K, Zhao Y, Fent K (2020) Cardiovascular drugs and lipid regulating agents in surface waters at global scale: Occurrence, ecotoxicity and risk assessment. Sci Total Environ 729:138770

    Article  CAS  Google Scholar 

  • Zounkova R, Odraska P, Dolezalova L, Hilscherova K, Blaha L (2007) Ecotoxicity and genotoxicity assessment of cytotoxic pharmaceuticals. Environ Toxicol Chem 26(10): 2208-2214

  • Zounkova R, Klimesova Z, Nepejchalova L, Hilscherova K, Blaha L (2011) Complex evaluation of ecotoxicity and genotoxicity of antimicrobials oxytetracycline and flumequine used in aquaculture. Environ Toxicol Chem 30(5):1184–1189

    Article  CAS  Google Scholar 

  • Zurita JL, Repetto G, Jos A, Salguero M, Lopez-Artiguez M, Camean AM (2007) Toxicological effects of the lipid regulator gemfibrozil in four aquatic systems. Aquat Toxicol 81(1):106–115

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the  International Science and Technology Cooperation Project of Shaanxi Province [No. 2023-GHZD-30] and ShaanXi Thousand Talent Program for Young Outstanding Scientists given to Dr. Jiahua Guo [No. 334041900007].

Funding

This work was supported by the Key Research and Development Program of ShaanXi Province [No. 2020SF-387] and ShaanXi Thousand Talent Program for Young Outstanding Scientists given to Dr. Jiahua Guo [No. 334041900007].

Author information

Authors and Affiliations

  1. Shaanxi Key Laboratory of Earth Surface System and Environmental Carrying Capacity, College of Urban and Environmental Sciences, Northwest University, Xi’an, 710127, China

    Jiahua Guo, Jingya Ren, Chao Chang, Qiannan Duan & Fangshe Yang

  2. Department of Environment and Geography, University of York, Heslington, York, YO10 5NG, UK

    Jun Li

  3. Center for Marine Environmental Studies, Ehime University, Matsuyama, 7908577, Japan

    Mirella Kanerva

  4. State Key Laboratory of Marine Pollution and Department of Chemistry, City University of Hong Kong, Kowloon, Hong Kong SAR, China

    Jiezhang Mo

Authors
  1. Jiahua Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jingya Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chao Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qiannan Duan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jun Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mirella Kanerva
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Fangshe Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jiezhang Mo
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization: Jiahua Guo and Jiezhang Mo; Methodology: Jiahua Guo and Jiezhang Mo; Data curation: Jiahua Guo, Jiezhang Mo, and Jingya Ren; Writing – original draft preparation: Jiahua Guo and Jiezhang Mo; Funding acquisition: Jiahua Guo; Formal analysis and investigation: Jingya Ren and Chao Chang; Writing – review & editing: Qiannan Duan, Jun Li, Mirella Kanerva, and Fangshe Yang; Supervision: Fangshe Yang and Jiezhang Mo.

Corresponding author

Correspondence to Fangshe Yang.

Ethics declarations

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Bruno Nunes

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 303 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guo, J., Ren, J., Chang, C. et al. Freshwater crustacean exposed to active pharmaceutical ingredients: ecotoxicological effects and mechanisms. Environ Sci Pollut Res 30, 48868–48902 (2023). https://doi.org/10.1007/s11356-023-26169-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-023-26169-0

Keywords

Search

Navigation