Skip to main content
SpringerLink
Log in

Effects of fluorene-9-bisphenol exposure on anxiety-like and social behavior in mice and protective potential of exogenous melatonin

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

Abstract

Fluorene-9-bisphenol (BHPF) is widely used in the manufacture of plastic products and potentially disrupts several physiological processes, but its biological effects on social behavior remain unknown. In this study, we investigated the effects of BHPF exposure on anxiety-like and social behavior in female mice and the potential mechanisms, thereby proposing a potential therapy strategy. We exposed female Balb/c mice to BHPF by oral gavage at different doses (0.5, 50 mg/kg bw/2-day) for 28 days, which were found BHPF (50 mg/kg) exposure affected motor activity in the open field test (OFT) and elevated cross maze (EPM), resulting in anxiety-like behaviors, as well as abnormal social behavioral deficits in the Social Interaction Test (SIT). Analysis of histopathological staining results showed that BHPF exposure caused damage to hippocampal neurons in the CA1/CA3/DG region and decreased Nissl pyramidal neurons in the CA1/CA3 regions of the hippocampus, as well as a decrease in parvalbumin neuron expression. In addition, BHPF exposure upregulated the expression of excitatory and inhibitory (E/I) vesicle transporter genes (Vglut1, Vglut2, VGAT, GAD67, Gabra) and axon growth gene (Dcc) in the mouse hippocampus. Interestingly, behavioral disturbances and E/I balance could be alleviated by exogenous melatonin (15 mg/kg bw/2-day) therapy. Our findings suggest that exogenous melatonin may be a potential therapy with protective potential for ameliorating or preventing BHPF-induced hippocampal neuronal damage and behavioral disturbances. This study provided new insight into the neurotoxicological effects on organisms exposed to endocrine-disrupting chemicals and aroused our vigilance in current environmental safety about chemical use.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

The data can be made available upon request.

References

  • Ali T, Rahman SU, Hao Q, Li W, Liu Z, Ali Shah F, Murtaza I, Zhang Z, Yang X, Liu G, Li S (2020) Melatonin prevents neuroinflammation and relieves depression by attenuating autophagy impairment through FOXO3a regulation. J Pineal Res 69:e12667

    Article  CAS  Google Scholar 

  • Bannerman DM, Sprengel R, Sanderson DJ, McHugh SB, Rawlins JN, Monyer H, Seeburg PH (2014) Hippocampal synaptic plasticity, spatial memory and anxiety. Nat Rev Neurosci 15:181–192

    Article  CAS  Google Scholar 

  • Bertoni A, Schaller F, Tyzio R, Gaillard S, Santini F, Xolin M, Diabira D, Vaidyanathan R, Matarazzo V, Medina I, Hammock E, Zhang J, Chini B, Gaiarsa JL, Muscatelli F (2021) Oxytocin administration in neonates shapes hippocampal circuitry and restores social behavior in a mouse model of autism. Mol Psychiatry 26:7582–7595

    Article  CAS  Google Scholar 

  • Boiko DI, Shkodina AD, Hasan MM, Bardhan M, Kazmi SK, Chopra H, Bhutra P, Baig AA, Skrypnikov AM (2022a) Melatonergic receptors (Mt1/Mt2) as a potential additional target of novel drugs for depression. Neurochem Res 47:2909–2924

    Article  CAS  Google Scholar 

  • Boiko DI, Skrypnikov AM, Shkodina AD, Hasan MM, Ashraf GM, Rahman MH (2022b) Circadian rhythm disorder and anxiety as mental health complications in post-COVID-19. Environ Sci Pollut Res Int 29:28062–28069

    Article  CAS  Google Scholar 

  • Boldrini M, Santiago AN, Hen R, Dwork AJ, Rosoklija GB, Tamir H, Arango V, John Mann J (2013) Hippocampal granule neuron number and dentate gyrus volume in antidepressant-treated and untreated major depression. Neuropsychopharmacology 38:1068–1077

    Article  CAS  Google Scholar 

  • Brumback AC, Ellwood IT, Kjaerby C, Iafrati J, Robinson S, Lee AT, Patel T, Nagaraj S, Davatolhagh F, Sohal VS (2018) Identifying specific prefrontal neurons that contribute to autism-associated abnormalities in physiology and social behavior. Mol Psychiatry 23:2078–2089

    Article  CAS  Google Scholar 

  • Cao W, Li JH, Lin S, Xia QQ, Du YL, Yang Q, Ye YZ, Zeng LH, Li XY, Xu J, Luo JH (2022) NMDA receptor hypofunction underlies deficits in parvalbumin interneurons and social behavior in neuroligin 3 R451C knockin mice. Cell Rep 41:111771

    Article  CAS  Google Scholar 

  • Caporale N et al (2022) From cohorts to molecules: adverse impacts of endocrine disrupting mixtures. Science 375:eabe8244

    Article  CAS  Google Scholar 

  • Chen S, Chen F, Amin N, Ren Q, Ye S, Hu Z, Tan X, Jiang M, Fang M (2022) Defects of parvalbumin-positive interneurons in the ventral dentate gyrus region are implicated depression-like behavior in mice. Brain Behav Immun 99:27–42

    Article  CAS  Google Scholar 

  • Chiang MC, Huang AJY, Wintzer ME, Ohshima T, McHugh TJ (2018) A role for CA3 in social recognition memory. Behav Brain Res 354:22–30

    Article  CAS  Google Scholar 

  • Comai S, De Gregorio D, Posa L, Ochoa-Sanchez R, Bedini A, Gobbi G (2020) Dysfunction of serotonergic activity and emotional responses across the light-dark cycle in mice lacking melatonin MT(2) receptors. J Pineal Res 69:e12653

    Article  CAS  Google Scholar 

  • Comai S, Gobbi G (2014) Unveiling the role of melatonin MT2 receptors in sleep, anxiety and other neuropsychiatric diseases: a novel target in psychopharmacology. J Psychiatry Neurosci 39:6–21

    Article  Google Scholar 

  • Deng X, Gu L, Sui N, Guo J, Liang J (2019) Parvalbumin interneuron in the ventral hippocampus functions as a discriminator in social memory. Proc Natl Acad Sci USA 116:16583–16592

    Article  CAS  Google Scholar 

  • Eisch AJ, Petrik D (2012) Depression and hippocampal neurogenesis: a road to remission? Science 338:72–75

    Article  CAS  Google Scholar 

  • Fan X, Guo J, Jia X, Mao X, Zhou Y, Wang Y, Guo X, Shen J, Huai N, Zhang K, Abdusalam A, Hu H, Zhu H, Jia C, Cheng L, Li X, Zhang Z (2023) Reproductive toxicity and teratogenicity of Fluorene-9-bisphenol on Chinese Medaka (Oryzias sinensis): a study from laboratory to field. Environ Sci Technol 57:561–569

    Article  CAS  Google Scholar 

  • Feng Q, Liu Y, Zou L, Lei M, Zhu C, Xia W (2023) Fluorene-9-bisphenol exposure damages the testis in mice through a novel mechanism of ferroptosis. Food Chem Toxicol 184:114385

    Article  Google Scholar 

  • Ferguson BR, Gao WJ (2018) Thalamic control of cognition and social behavior via regulation of gamma-aminobutyric Acidergic signaling and excitation/inhibition balance in the medial prefrontal cortex. Biol Psychiatry 83:657–669

    Article  CAS  Google Scholar 

  • Filice F, Lauber E, Vorckel KJ, Wohr M, Schwaller B (2018) 17-beta estradiol increases parvalbumin levels in Pvalb heterozygous mice and attenuates behavioral phenotypes with relevance to autism core symptoms. Mol Autism 9:15

    Article  Google Scholar 

  • Finlay JM, Dunham GA, Isherwood AM, Newton CJ, Nguyen TV, Reppar PC, Snitkovski I, Paschall SA, Greene RW (2015) Effects of prefrontal cortex and hippocampal NMDA NR1-subunit deletion on complex cognitive and social behaviors. Brain Res 1600:70–83

    Article  CAS  Google Scholar 

  • Gabor CS, Phan A, Clipperton-Allen AE, Kavaliers M, Choleris E (2012) Interplay of oxytocin, vasopressin, and sex hormones in the regulation of social recognition. Behav Neurosci 126:97–109

    Article  CAS  Google Scholar 

  • Gao T, Yin Z, Wang M, Fang Z, Zhong X, Li J, Hu Y, Wu D, Jiang K, Xu X (2020) The effects of pubertal exposure to bisphenol-a on social behavior in male mice. Chemosphere 244:125494

    Article  CAS  Google Scholar 

  • Hashemi E, Ariza J, Rogers H, Noctor SC, Martinez-Cerdeno V (2017) The number of Parvalbumin-expressing interneurons is decreased in the prefrontal cortex in autism. Cereb Cortex 27:1931–1943

    Google Scholar 

  • Hu H, Gan J, Jonas P (2014) Interneurons. Fast-spiking, parvalbumin(+) GABAergic interneurons: from cellular design to microcircuit function. Science 345:1255263

    Article  Google Scholar 

  • Jia Z, Wang H, Feng Z, Zhang S, Wang L, Zhang J, Liu Q, Zhao X, Feng D, Feng X (2019) Fluorene-9-bisphenol exposure induces cytotoxicity in mouse oocytes and causes ovarian damage. Ecotoxicol Environ Saf 180:168–178

    Article  CAS  Google Scholar 

  • Jiao XF, Liang QM, Wu D, Ding ZM, Zhang JY, Chen F, Wang YS, Zhang SX, Miao YL, Huo LJ (2019) Effects of acute Fluorene-9-Bisphenol exposure on mouse oocyte in vitro maturation and its possible mechanisms. Environ Mol Mutagen 60:243–253

    Article  CAS  Google Scholar 

  • Jin ZY, Liu CK, Hong YQ, Liang YX, Liu L, Yang ZM (2022) BHPF exposure impairs mouse and human decidualization. Environ Pollut 304:119222

    Article  CAS  Google Scholar 

  • Kobayashi M, Hayashi Y, Fujimoto Y, Matsuoka I (2018) Decreased parvalbumin and somatostatin neurons in medial prefrontal cortex in BRINP1-KO mice. Neurosci Lett 683:82–88

    Article  CAS  Google Scholar 

  • Kodali M, Attaluri S, Madhu LN, Shuai B, Upadhya R, Gonzalez JJ, Rao X, Shetty AK (2021) Metformin treatment in late middle age improves cognitive function with alleviation of microglial activation and enhancement of autophagy in the hippocampus. Aging Cell 20:e13277

    Article  CAS  Google Scholar 

  • Kogan JH, Franklandand PW, Silva AJ (2000) Long-term memory underlying hippocampus-dependent social recognition in mice. Hippocampus 10:47–56

    Article  CAS  Google Scholar 

  • Lama A, Pirozzi C, Severi I, Morgese MG, Senzacqua M, Annunziata C, Comella F, Del Piano F, Schiavone S, Petrosino S, Mollica MP, Diano S, Trabace L, Calignano A, Giordano A, Mattace Raso G, Meli R (2022) Palmitoylethanolamide dampens neuroinflammation and anxiety-like behavior in obese mice. Brain Behav Immun 102:110–123

    Article  CAS  Google Scholar 

  • Li YD, Luo YJ, Chen ZK, Quintanilla L, Cherasse Y, Zhang L, Lazarus M, Huang ZL, Song J (2022) Hypothalamic modulation of adult hippocampal neurogenesis in mice confers activity-dependent regulation of memory and anxiety-like behavior. Nat Neurosci 25:630–645

    Article  CAS  Google Scholar 

  • Lin J et al (2023) YTHDF2-mediated regulations bifurcate BHPF-induced programmed cell deaths. Natl Sci Rev 10:nwad227

    Article  Google Scholar 

  • Liu Y, Deng SL, Li LX, Zhou ZX, Lv Q, Wang ZY, Wang F, Chen JG (2022) A circuit from dorsal hippocampal CA3 to parvafox nucleus mediates chronic social defeat stress-induced deficits in preference for social novelty. Sci Adv 8:eabe8828

    Article  CAS  Google Scholar 

  • MacQueen G, Frodl T (2011) The hippocampus in major depression: evidence for the convergence of the bench and bedside in psychiatric research? Mol Psychiatry 16:252–264

    Article  CAS  Google Scholar 

  • Mi P, Tang YQ, Feng XZ (2020) Acute fluorene-9-bisphenol exposure damages early development and induces cardiotoxicity in zebrafish (Danio rerio). Ecotoxicol Environ Saf 202:110922

    Article  CAS  Google Scholar 

  • Mi P, Zhang QP, Li SB, Liu XY, Zhang SH, Li M, Chen DY, Zhao X, Feng DF, Feng XZ (2019) Melatonin protects embryonic development and maintains sleep/wake behaviors from the deleterious effects of fluorene-9-bisphenol in zebrafish (Danio rerio). J Pineal Res 66:e12530

    Article  Google Scholar 

  • Moy SS, Nadler JJ, Perez A, Barbaro RP, Johns JM, Magnuson TR, Piven J, Crawley JN (2004) Sociability and preference for social novelty in five inbred strains: an approach to assess autistic-like behavior in mice. Genes Brain Behav 3:287–302

    Article  CAS  Google Scholar 

  • Okuyama T, Kitamura T, Roy DS, Itohara S, Tonegawa S (2016) Ventral CA1 neurons store social memory. Science 353:1536–1541

    Article  CAS  Google Scholar 

  • Pal S, Sahu A, Verma R, Haldar C (2023) BPS-induced ovarian dysfunction: protective actions of melatonin via modulation of SIRT-1/Nrf2/NFĸB and IR/PI3K/pAkt/GLUT-4 expressions in adult golden hamster. J Pineal Res 75:e12869

    Article  CAS  Google Scholar 

  • Pan L et al (2022) A short period of early life oxytocin treatment rescues social behavior dysfunction via suppression of hippocampal hyperactivity in male mice. Mol Psychiatry 27(10):4157–4171

    Article  CAS  Google Scholar 

  • Posa L, De Gregorio D, Gobbi G, Comai S (2018) Targeting melatonin MT2 receptors: a novel pharmacological avenue for inflammatory and neuropathic pain. Curr Med Chem 25:3866–3882

    Article  CAS  Google Scholar 

  • Selimbeyoglu A, Kim CK, Inoue M, Lee SY, Hong ASO, Kauvar I, Ramakrishnan C, Fenno LE, Davidson TJ, Wright M, Deisseroth K (2017) Modulation of prefrontal cortex excitation/inhibition balance rescues social behavior in CNTNAP2-deficient mice. Sci Transl Med 9(401):eaah6733

  • Shi F, Qiu J, Zhang S, Zhao X, Feng D, Feng X (2022a) Exogenous melatonin protects preimplantation embryo development from decabromodiphenyl ethane-induced circadian rhythm disorder and endogenous melatonin reduction. Environ Pollut 292:118445

    Article  CAS  Google Scholar 

  • Shi F, Xu Y, Zhang S, Fu Z, Yu Q, Zhang S, Sun M, Zhao X, Feng X (2022b) Decabromodiphenyl ethane affects embryonic development by interfering with nuclear F-actin in zygotes and leads to cognitive and social disorders in offspring mice. FASEB J 36:e22445

    Article  CAS  Google Scholar 

  • Sohal VS, Rubenstein JLR (2019) Excitation-inhibition balance as a framework for investigating mechanisms in neuropsychiatric disorders. Mol Psychiatry 24:1248–1257

    Article  Google Scholar 

  • Sun Q, Li X, Li A, Zhang J, Ding Z, Gong H, Luo Q (2020) Ventral hippocampal-prefrontal interaction affects social behavior via Parvalbumin positive neurons in the medial prefrontal. Cortex iScience 23:100894

    Google Scholar 

  • Sun Q, Li X, Ren M, Zhao M, Zhong Q, Ren Y, Luo P, Ni H, Zhang X, Zhang C, Yuan J, Li A, Luo M, Gong H, Luo Q (2019) A whole-brain map of long-range inputs to GABAergic interneurons in the mouse medial prefrontal cortex. Nat Neurosci 22:1357–1370

    Article  CAS  Google Scholar 

  • Sun Y, Ma L, Jin M, Zheng Y, Wang D, Ni H (2021) Effects of melatonin on Neurobehavior and cognition in a cerebral palsy model of plppr5−/− mice. Front Endocrinol (Lausanne) 12:598788

    Article  Google Scholar 

  • Tong Q, Cui X, Xu H, Zhang X, Hu S, Huang F, Xiao L (2022) D1 receptor-expressing neurons in ventral tegmental area alleviate mouse anxiety-like behaviors via glutamatergic projection to lateral septum. Mol Psychiatry 28(2):625–638

    Article  Google Scholar 

  • Torres-Berrio A, Lopez JP, Bagot RC, Nouel D, Dal Bo G, Cuesta S, Zhu L, Manitt C, Eng C, Cooper HM, Storch KF, Turecki G, Nestler EJ, Flores C (2017) DCC confers susceptibility to depression-like behaviors in humans and mice and is regulated by miR-218. Biol Psychiatry 81:306–315

    Article  CAS  Google Scholar 

  • Wang HB, Tahara Y, Luk SHC, Kim YS, Hitchcock ON, MacDowell Kaswan ZA, In Kim Y, Block GD, Ghiani CA, Loh DH, Colwell CS (2020) Melatonin treatment of repetitive behavioral deficits in the Cntnap2 mouse model of autism spectrum disorder. Neurobiol Dis 145:105064

    Article  CAS  Google Scholar 

  • Wohr M, Orduz D, Gregory P, Moreno H, Khan U, Vorckel KJ, Wolfer DP, Welzl H, Gall D, Schiffmann SN, Schwaller B (2015) Lack of parvalbumin in mice leads to behavioral deficits relevant to all human autism core symptoms and related neural morphofunctional abnormalities. Transl Psychiatry 5:e525

    Article  CAS  Google Scholar 

  • Xu H, Wang J, Jing H, Ellenbroek B, Shao F, Wang W (2021) mPFC GABAergic transmission mediated the role of BDNF signaling in cognitive impairment but not anxiety induced by adolescent social stress. Neuropharmacology 184:108412

    Article  CAS  Google Scholar 

  • Yang L, Guo X, Mao X, Jia X, Zhou Y, Hu Y, Sun L, Guo J, Xiao H, Zhang Z (2021) Hepatic toxicity of fluorene-9-bisphenol (BHPF) on CD-1 mice. Ecotoxicol Environ Saf 219:112298

    Article  CAS  Google Scholar 

  • Zhang M, Dai X, Lu Y, Miao Y, Zhou C, Cui Z, Liu H, Xiong B (2017a) Melatonin protects oocyte quality from Bisphenol A-induced deterioration in the mouse. J Pineal Res 62(3)

  • Zhang Z, Hu Y, Guo J, Yu T, Sun L, Xiao X, Zhu D, Nakanishi T, Hiromori Y, Li J (2017b) Fluorene-9-bisphenol is anti-oestrogenic and may cause adverse pregnancy outcomes in mice. Nat Commun 8:14585

    Article  Google Scholar 

  • Zhang Z, Hu Y, Guo J, Yu T, Sun L, Xiao X, Zhu D, Nakanishi T, Hiromori Y, Li J, Fan X, Wan Y, Cheng S, Li J, Guo X, Hu J (2017c) Fluorene-9-bisphenol is anti-oestrogenic and may cause adverse pregnancy outcomes in mice. Nat Commun 8:14585

    Article  Google Scholar 

  • Zhang S, Jiao Z, Zhao X, Sun M, Feng X (2021) Environmental exposure to 17beta-trenbolone during adolescence inhibits social interaction in male mice. Environ Pollut 289:117710

    Article  CAS  Google Scholar 

  • Zhang S, Xu Y, Zhang S, Zhao C, Feng D, Feng X (2022) Fluorene-9-bisphenol exposure decreases locomotor activity and induces lipid-metabolism disorders by impairing fatty acid oxidation in zebrafish. Life Sci 294:120379

    Article  CAS  Google Scholar 

  • Zhang S, Zhang S, Zhu D, Jiao Z, Zhao X, Sun M, Che Y, Feng X (2020) Effects of 17beta-trenbolone exposure on sex hormone synthesis and social behaviours in adolescent mice. Chemosphere 245:125679

    Article  CAS  Google Scholar 

  • Zhang S, Zuo X, Luan J, Bai H, Fu Z, Sun M, Zhao X, Feng X (2024) The deleterious effects and potential therapeutic strategy of fluorene-9-bisphenol on circadian activity and liver diseases in zebrafish and mice. J Environ Sci 145:13–27

    Article  Google Scholar 

Download references

Acknowledgments

We thank Professor Xizeng Feng and Xiang Zuo for completing the construction of experimental ideas and the design of experimental methods, Professor Xin Zhao for completing the investigation and financial support, Shuhui Zhang for completing the commentary and editing of the paper, and Huijuan Bai, Qian Yu and Mingzhu Sun for completing the formal analysis of the paper, Qili Zhao providing financial support. This work was jointly supported by the National Natural Science Foundation of China (Grant Nos. 62027812, 62273186).

Funding

This work was jointly supported by the National Natural Science Foundation of China (Grant Nos. 62027812, 62273186).

Author information

Author notes

  1. Xiang Zuo and Shuhui Zhang have the same contribution to this research.

Authors and Affiliations

  1. College of Life Sciences, State Key Laboratory of Medicinal Chemical Biology, Key Laboratory of Bioactive Materials, Ministry of Education, Nankai University, Weijin Road 94, Tianjin, 300071, China

    Zuo Xiang, Zhang Shuhui, Bai Huijuan, Yu Qian & Feng Xizeng

  2. Institute of Robotics & Automatic Information System, College of Artificial Intelligence, Nankai University, Tianjin, 300071, China

    Zhao Qili, Sun Mingzhu & Zhao Xin

Authors
  1. Zuo Xiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhang Shuhui
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bai Huijuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yu Qian
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhao Qili
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sun Mingzhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhao Xin
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Feng Xizeng
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

The first draft of the manuscript was written by Dr. Xiang Zuo and also he read and approved the final submitted manuscript. Xiang Zuo: Conceptualization, Methodology, Investigation, Writing- Original draft; Shuhui Zhang: Conceptualization, Methodology, Visualization, Formal analysis; Huijuan Bai: Methodology, Visualization; Qian Yu: Methodology; Qili Zhao: Conceptualization; Mingzhu Sun: Conceptualization; Xin Zhao: Conceptualization, Validation, Funding acquisition; Xizeng Feng: Conceptualization, Supervision, Methodology, Funding acquisition. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Feng Xizeng.

Ethics declarations

Ethical approval

All experimental processes involving mice were approved by the Committee for Animal Experimentation of the College of Life Sciences at Nankai University (No. 2008) and were performed by the NIH Guide for the Care and Use of Laboratory Animals (No. 8023, revised in 1996).

Consent to participate

All authors have approved the final manuscript and consented to the submission to the journal.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Philippe Garrigues

Publisher’s Note

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

Supplementary information

Supplementary file 1

(DOCX 2888 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

Zuo, X., Zhang, S., Bai, H. et al. Effects of fluorene-9-bisphenol exposure on anxiety-like and social behavior in mice and protective potential of exogenous melatonin. Environ Sci Pollut Res 31, 29385–29399 (2024). https://doi.org/10.1007/s11356-024-33148-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-024-33148-6

Keywords

Search

Navigation