Abstract
Plastic wastes deposited in canals running through Thiruvananthapuram city have created stagnant waters providing breeding sites for mosquitoes. In the present study, plastic waste–derived bisphenol A (BPA) was quantified from four mosquito breeding sites. During summer rain, the concentration of BPA in the stagnant water samples was found to be between 0.86 and 1.14 mg/L, and hence 1 mg/L BPA was considered as the environmentally relevant concentration. In the present study, the effect of BPA on the life cycle and metamorphosis of filarial vector, Culex quinquefasciatus Say was elucidated by rearing larvae in water added with BPA at and above the environmentally relevant concentration viz., 1, 2, and 4 mg/L. The duration required for adult emergence was reduced from 10 to 8.5 days, when the concentration of BPA was increased from 1 to 4 mg/L respectively. Our study revealed that embryonic and larval developments were shortened by BPA treatment. BPA also caused a dose-dependent advancement of 20-hydroxyecdysone (20-E) peaks; phospholipase A2 induction; and upregulation of ecdysone receptor gene, EcRA, and ecdysone inducible gene E75A, which culminated in early pupation. No significant difference in sanguivory and fecundity was observed in adult mosquitoes treated with 1 mg/L of BPA. Our study reveals that BPA is a developmental agonist of C. quinquefasciatus.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are available in this submitted article and its supplementary files.
References
Albi OA, Ologbonjae K, Awasolu O, Alaladi OE (2019) Public health and environmental health effects of plastic waste disposal: a review. J Toxic Risk Assess 5:1–13. https://doi.org/10.23937/2572-4061.1510021
Alti E, Ulnu H (2012) Developmental and reproductive effects of bisphenol a in Drosophila melanogaster, Hacettepe. J Biol Chem 40:61–68
Anuji TK, Shabithraj K, Sunny F, Evans DA (2018) Transgenerational effect of bisphenol A ton phenotypic characters of antennae in Drosophila ananassae (Doleschall). J Entomol Res 42:517–523. https://doi.org/10.5958/0974-4576.2018.00087.7
Banerjee S, Aditya G, Saha G (2015) Household waste as larval habitats of dengue vectors: comparison between Urban and rural areas of Kolkata. Plos One 10(10):e0138082. https://doi.org/10.1371/journal.pone
Barbalas MP, Garland WA (1991) A computer programme for the deconvolution of mass spectral peak abundance data from experiments using stable isotopes. J Pharm Sci 80:911–916. https://doi.org/10.5958/0974-4576.2018.0087.7
Barraud PJ (1934) Diptera-Family Culicidae, Tribes: Megharhini and Culicini. In: Sewel RBS (ed) Fauna of British India including Ceylon and Burma, vol 5. Taylor and Francis, London, pp 420–425
Bialecki M, Shilton A, Fichtenberg C, SegravesWA TCS (2002) Loss of ecdysteroid-inducible E75A orphan nuclear receptor uncouples molting from metamorphosis in Drosophila. Dev Cell 3:209–220. https://doi.org/10.1016/s1534-5807(02)00204-6
Biggers WJ, Laufer H (2004) Identification of Juvenile hormone active alkyl phenols in the lobster Hormarusamericanas and in marine sediments. Biol Bull 206:13–24. https://doi.org/10.2307/1543194.journals.uchicago.edu
Ciota AT, Matacchiero AM, Kilpatric AM, Kramer LD (2014) The effect of temperature on the life history traits of Culex mosquitoes. J Med Entomol 51:55–62. https://doi.org/10.1603/me13003
Corrales J, Kristofco L A, Steele WB, Yates BS, BreedCS, Williams ES, Brooks BW (2015) Global assessment of bisphenol A in the environment: review and analysis of its occurrence and bioaccumulation, Dose- Response,13https://doi.org/10.1177/155932815598308
Crain DA, Eriksen M, Iguchi T, Jobling S (2007) An ecological assessment of bisphenol A: evidence from comparative biology. Reprod Toxicol 24(2):225–239
Dedos SG, Fugo H (2001) Acceleration of pupal – adult development by fenoxycarb in the silk worm Bombyx mori. Zool Sci 18:771–777. https://doi.org/10.2108/zsj.18.771
Denlinger DL (2002) Regulation of diapause. Annu Rev Entomol 47:93–122. https://doi.org/10.1146/annurev.ento.47.091201.145137
Dong J, Li XL, Luan TG, Zou SC, Lin L (2009) Phenol pollution in the sediments of Pearl river estuary area and its potential risk assessment to the eco-security. J Saf Environ 9:113–116
Fabbri R, Montagna M, Balbi T, RaffoE PF, Canesi L (2014) Adaptation of the bivalve embryotoxicity assay for high through put screening of emerging contaminants in Mytilus galloprovincialis. Mar Environ Res 99:1–8. https://doi.org/10.1016/j.marenvres.2014.05.007
Farag AI, Varjas L (1983) Precocious metamorphosis and moulting deficiencies induced by an anti-JH compound, FMEV in the Fall Web Worm Hyphantria Cunea. Entomol Exp Appl 34:55–70. https://doi.org/10.1111/j.1570-7458.1983.tb.0329.1.x
Flint S, Markle T, Thompson S, Wallace E (2012) Bisphenol A exposure, effects, and policy: a wildlife perspective. J Environ Man 104:19–34
Gayathri RVA, Evans DA (2018) Culex quinqnefasciatusSay larva adapts to temperature shock through changes in protein turn over and aminoacid catabolism. JThermBiol 74:149–159. https://doi.org/10.1016/j.therbio.2018.03.016
Huang YQ, Wong CKC, Zheng JS, BouwmanAK BR, WahlstromB NL, Wong MH (2011) Bisphenol A (BPA) in China: a review on sources, environmental levels and potential human health impacts. EnvironInt 42:91–99. https://doi.org/10.1016/jenvnt.2011.04.010
Izumi N, Yanagibori R, Shigeno S, Sajiki J (2008) Effects of bisphenol a on the development, growth and sex ratio of house fly Muscadomestica. Environ Toxicol Chem 27:1343–1353. https://doi.org/10.1897/07-218
Johnston DM, Sedkov Y, Petruk S, Riley KM, Fujioka M, Jaynes JB, Mazo A (2011) Ecdysone and NO mediated gene regulation by competing EcR/USP and E75A nuclear receptor during Drosophila development. Mol Cell 44:51–61. https://doi.org/10.1016/j.molcel.2011.07.033
Kolpin DW, Furlong ET, Meyer MT, Thurman EM, Zaugg SD, BarberLB BuxtonHT (2002) Pharmaceuticals, hormones and other organic wastewater contaminants in US streams, 1999–2000: a national reconnaissance. EnvironSciTechnol 36:1202–1211. https://doi.org/10.1021/es011055j
Kontogiannatos D, Swevers L, Zakasis G, Kourti A (2014) The molecular and physiological impact of bisphenol A in Sesamia nonagrioides (Lepidoptera: Noctuidae). Ecotoxicology 24(2):356–367. https://doi.org/10.1007/s10646-014-1384-6
Kumar MB, Fugimoto T, Potter DW, Deng Q, Palli SR (2002) A single potent modulation is EcR leads to increased ligand specificity: implication is gene switch applications. ProcNatlAcadSci USA 99:14710–14715
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685. https://doi.org/10.1038/227680ao
Maria A, Malbert-Colas A, Boulogne I, Braman V, Boitard C, Dacher M, Chertemps T, Maibeche M, Blais C, Siaussat D (2019) Effects of bisphenol A on post-embryonic development of the cotton pest Spodoptera littoralis. Chemosphere 235:616–625. https://doi.org/10.1016/j.chemosphere.2019.06.073 (Epub 2019 Jun 20 PMID: 31276874)
Margam MV, Gelman DB, Palli SR (2006) Ecdysteroid titers and developmental expression of ecdysteroid regulated genes during metamorphosis of yellow fever mosquito Aedesaegypti, (Diptera-Culicidae). J Insect Physiol 52:558–568. https://doi.org/10.1016/j.insphys.2006.02.03
Mu X, Rider CV, Hwang GS, Hoy H, LeBlanc GA (2005) Covert signal disruption : anti-ecdysteroid activity of bisphenol A involves cross talk between signaling pathways. Environ ToxicolChem 24:146–152. https://doi.org/10.1897/04-063R.1
Porcheron P, Moriniere M, Grassi J, Pradelles P (1989) Development of enzyme immunoassay for ecdysteroids using acetyl choline esterase as label. Insect Biochem 19:117–122. https://doi.org/10.1016/0020-1790(89)90081-4
Planello R, Martinez-Guitarte JL, Morcillo G (2008) Endocrine disruptor bisphenol A increases expression of HSP70 and ecdysone receptor genes in aquatic larvae of Chironomusriparius. Chemosphere 71:1870–1876. https://doi.org/10.1016/j.chemosphere.200801.033
Prud'homme SM, Chaumot A, Cassar E, David J, Reynaud S (2017) Impact of micropollutants on the life-history traits of the mosquito Aedes aegypti: on the relevance of transgenerational studies. Environ Pollut, 220: 242-254, ISSN 0269-7491https://doi.org/10.1016/j.envpol.2016.09.056
Roberts D, Kokkim M (2010) Larval crowding effects on mosquito Culex quinquefasciatus, physical or chemical? Entomol Exp Appl 135:271–275. https://doi.org/10.1111/j.1570-7458.2010.00993.x
Rouch P, Grebe M, ElkeC Spindler KD, Spindler BM (1998) Ecdysteroid receptor and ultraspiracle from Chironomustentans (Insecta) are phospholipoproteins and are regulated differently by moulting hormone. Insect Biochemand Mol Biol 27:945–962. https://doi.org/10.1016/s0965-1748(98)00026-5
Selvaraj KK, Shanmugam G, Sampath S, Larsson DG, Ramaswamy BR (2014) GC-MS determination of bisphenol A and alkylphenol ethoxylates in river water from India and their ecotoxicological risk assessment. Ecotoxicol Environ Saf 99:13–20. https://doi.org/10.1016/j.ecoenv.2013.09.006 (Epub 2013 Nov 1 PMID: 24183982)
Sunilkumar S, Evans DA, Muthulakshmi K, DilipkumarT Pillai RH, Radhakrishnan Nair R, Francis S (2018) Distrbution of Aedesaegypti and Aedesalbopictus in different ecozones of Thiruvananthapuram city with special reference to Dengue viremia in humans. Entomon 43:223–230. https://doi.org/10.33307/entamon.v4314.402
Tripathy K, Dash AP (1988) Larvae of Culex sp. and Aedes sp. Morphology and identifying features In: Proceedings of the symposium on vectors and vector borne diseases, Department of Zoology, University of Kerala, India .152–158.
Tsai WT (2006) Human health risk on environmental exposure to bisphenol-A: a review. J Environ Sci Health, Part C Environ Carcinog Ecotoxicol Rev 24(2):225–255
Virk P, Al-Sarkan AAM, Elobeid MA (2014) Effect of bisphenol A on the levels of vitellogenin and metallothionein in adult male carp CyprinuscarpioL. Trop J Pharm Res 13:1107–1112. https://doi.org/10.4314/tjpr.v13i7.14
Warren JT, Bachmann JS, Dai JD, Gilbert LI (2001) Differential incorporation of cholesterol and cholesterol derivatives into ecdysteroids by the ring gland and adult ovaries of Drosophila melanogaster, a putative explanation for l (3) ecd1 mutation. Insect Biochem Mol Biol 26:931–943. https://doi.org/10.1016/s0965-1748(96)00059-8
Watts MM, Pascoe D, Carroll K (2003) Exposure to 17-α- ethinylestradiol and bisphenola affects larval moulting and mouth parts structure of Chironomusriparius. Ecotoxicol Environ Saf 54:207–215. https://doi.org/10.1016/s0147-6513(02)00029-5
Yamamoto T, Yasuhara A (1999) Quantities of bisphenol A leached from plastic waste samples. Chemosphere 38:2569–2576. https://doi.org/10.1016/s0045-6535(98)00464-0
Yamazaki E, Yamashita N, Taniyasu S, Lam J, Lam PKS, Moon H, Jeong Y, Kannan P, Achyuthan H, Munuswamy N, Kannan K (2015) Bisphenol A and other bisphenol analogues including BPS and BPF in surface water samples from Japan, China, Korea and India. Ecotoxicol Environ Saf 122:565–572. https://doi.org/10.1016/j.ecoenv.2015.09.029
Yang F-X, Xu Y, Wen S (2005) Endocrine disrupting effect of monophenolbisphenol A and p ´ p´ – DDE on Rananigromaculatatadpoles. Bull EnvironContamToxicol 75:1168–1175. https://doi.org/10.1007/s00128-005-0872-2
Yokota H, Tsuruda Y, Maeda M, Oshima Y, Tadokoro H, Nakazano A, Honjo T, Kobayashi K (2000) Effect of bisphenol A on the early life stage in Japanese medaka (Oryziaslatipes). EnvironToxicolChem 19:1925–1930. https://doi.org/10.1002/etc.5620190730
Youngjin P, Kumar S, Kanumuri R, Stanley D, Kim Y (2015) A novel calcium dependent cellular PLA2 acts in insect immunity and larval growth. Insect Biochemistry MolBiol 66:13–23. https://doi.org/10.1016/j.ibmb.2015.09.012
Zhu J,Norigea FG(2016) The role of juvenile hormone in mosquito development. In:Advances in Insect Physiology (Progress in Mosquito Research, A. S. Raikhel, Ed. Vol. 51 (Academic Press, Elsevier, 2016.) pp 110–176. https://doi.org/10.1016/bs-aiip.2016.04.005
Acknowledgements
Authors thank University Grants Commission, India for sanctioning research grant through Faculty Development Programme and Kerala State Council for Science, Technology and Environment for infrastructure development of Research Laboratory of Zoology Department, University College, Kerala, India. Authors also acknowledge the contributions of Dr. S. Sreekumar, former Professor and Head, Department of Zoology, Dr. Shubha N., former Associate Professor and Head, Department of English and Dr. M.N. Parasuraman, Assistant Professor, Department of English, University College, Thiruvananthapuram for their thorough language revision of the article.
Funding
First author (Ms. Ayana Gayathri R.V., Assistant Professor of Zoology) was working under Faculty Improvement Programme of University Grants Commission (India) as Teacher Fellow for her Doctoral work, funded by UGC, India. Infrastructure development of the Corresponding author’s laboratory was supported by Kerala State Council for Science, Technology and Environment, Govt. of Kerala, India. Both organizations (UGC and KSCSTE) are properly acknowledged in this paper.
Author information
Authors and Affiliations
Contributions
Results incorporated in the paper are a portion of the Ph. D thesis of Dr. Ayana Gayathri, R.V., who has done her doctoral work under the guidance and supervision of Dr. Evans, D. A., Associate Professor of Zoology. Contribution of the first author in this paper is 50% and corresponding author is 50%. All the information given above are true to the best of our knowledge.
a. The results incorporated in this paper did not include any information made on humans or on higher animals.
b. Individual person’s data is not incorporated in this paper.
c. All data incorporated in the paper is based on observations made on Culex quinquefasciatus.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interest.
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.
Rights and permissions
About this article
Cite this article
Valsala, A.G.R., Asirvadam, E.D. Bisphenol A acts as developmental agonist in Culex quinquefasciatus Say. Environ Sci Pollut Res 29, 74428–74441 (2022). https://doi.org/10.1007/s11356-022-21001-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-022-21001-7