Lymnaea stagnalis and Ophryotrocha diadema as Model Organisms for Studying Genotoxicological and Physiological Effects of Benzophenone-3
Abstract
:1. Introduction
2. Materials and Methods
2.1. Chemicals and Media
2.2. Lymnaea stagnalis
2.3. Experimental Set-up for Lymnaea stagnalis
2.4. Micronuclei Assay on Hemocytes from Lymnaea stagnalis
2.5. Ophryotrocha diadema
2.6. Experimental Set up for Ophryotrocha diadema
2.7. Statistical Analysis
3. Results
3.1. Lymnaea stagnalis
3.2. Ophryotrocha diadema
4. Discussion
5. Conclusions
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Carve, M.; Nugegoda, D.; Allinson, G.; Shimeta, J. A systematic review and ecological risk assessment for organic ultraviolet filters in aquatic environments. Environ. Pollut. 2021, 268, 115894. [Google Scholar] [CrossRef] [PubMed]
- Carve, M.; Allinson, G.; Nugegoda, D.; Shimeta, J. Trends in environmental and toxicity research on organic ultraviolet filters: A scientometric review. Sci. Total Environ. 2021, 773, 145628. [Google Scholar] [CrossRef] [PubMed]
- Matouskova, K.; Vandenberg, L.N. Towards a paradigm shift in environmental health decision-making: A case study of oxybenzone. Environ. Health 2022, 21, 6. [Google Scholar] [CrossRef]
- Careghini, A.; Mastorgio, A.F.; Saponaro, S.; Sezenna, E. Bisphenol A, nonylphenols, benzophenones, and benzotriazoles in soils, groundwater, surface water, sediments, and food: A review. Environ. Sci. Pollut. Res. 2015, 22, 5711–5741. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Q.Y.; Ma, X.Y.; Wang, X.C.; Ngo, H.H. Assessment of multiple hormone activities of a UV-filter (octocrylene) in zebrafish (Danio rerio). Chemosphere 2016, 159, 433–441. [Google Scholar] [CrossRef]
- Montes-Grajales, D.; Fennix-Agudelo, M.; Miranda-Castro, W. Occurrence of personal care products as emerging chemicals of concern in water resources: A review. Sci. Total Environ. 2017, 595, 601–614. [Google Scholar] [CrossRef]
- Vione, D.; Caringella, R.; De Laurentiis, E.; Pazzi, M.; Minero, C. Phototransformation of the sunlight filter benzophenone-3 (2-hydroxy-4-methoxybenzophenone) under conditions relevant to surface waters. Sci. Total Environ. 2013, 463, 243–251. [Google Scholar] [CrossRef]
- Wnuk, W.; Michalska, K.; Krupa, A.; Pawlak, K. Benzophenone-3, a chemical UV-filter in cosmetics: Is it really safe for children and pregnant women? Postepy Dermatol. Alergol. 2022, 39, 26–33. [Google Scholar] [CrossRef]
- Xiao, P.; Dumur, F.; Graff, B.; Gigmes, D.; Fouassier, J.P.; Lalevée, J. Variations on the benzophenone skeleton: Novel high performance blue light sensitive photoinitiating systems. Macromolecules 2013, 46, 7661–7667. [Google Scholar] [CrossRef]
- Kasonga, T.K.; Coetzee, M.A.A.; Kamika, I.; Ngole-Jeme, V.M.; Benteke Momba, M.N. Endocrine-disruptive chemicals as contaminants of emerging concern in wastewater and surface water: A review. J. Environ. Manag. 2021, 277, 111485. [Google Scholar] [CrossRef]
- Kim, S.; Choi, K. Occurrences, toxicities, and ecological risks of benzophenone-3, a common component of organic sunscreen products: A mini-review. Environ. Int. 2014, 70, 143–157. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, K.T.N.; Scapolla, C.; Di Carro, M.; Magi, E. Rapid and selective determination of UV-filters in seawater by liquid chromatography–tandem mass spectrometry combined with stir bar sorptive extraction. Talanta 2011, 85, 2375–2384. [Google Scholar] [CrossRef] [PubMed]
- Sánchez Rodríguez, A.; Rodrigo Sanz, M.; Betancort Rodríguez, J.R. Occurrence of eight UV-filters in beaches of Gran Canaria (Canary Islands). An approach to environmental risk assessment. Chemosphere 2015, 131, 85–90. [Google Scholar] [CrossRef] [PubMed]
- Cadena-Aizaga, M.I.; Montesdeoca-Esponda, S.; Torres-Padrón, M.E.; Sosa-Ferrera, Z.; Santana-Rodríguez, J.J. Organic UV filters in marine environments: An update of analytical methodologies, occurrence, and distribution. Trends Environ. Anal. Chem. 2020, 25, e00079. [Google Scholar] [CrossRef]
- Mao, F.; He, Y.; Kushmaro, A.; Gin, K.Y. Effects of benzophenone-3 on the green alga Chlamydomonas reinhardtii and the cyanobacterium Microcystis aeruginosa. Aquat. Toxicol. 2017, 193, 1–8. [Google Scholar] [CrossRef]
- Zhong, X.; Downs, C.A.; Che, X.; Zhang, Z.; Li, Y.; Liu, B.; Li, Q.; Li, Y.; Gao, H. The toxicological effects of oxybenzone, an active ingredient in suncream personal care products, on prokaryotic alga Arthrospira sp. and eukaryotic alga Chlorella sp. Aquat. Toxicol. 2019, 216, 105295. [Google Scholar] [CrossRef]
- Thorel, E.; Clergeaud, F.; Jaugeon, L.; Rodrigues, A.M.S.; Lucas, J.; Stie, D.; Lebaron, P. Effect of 10 UV Filters on the Brine Shrimp Artemia salina and the Marine Microalga Tetraselmis sp. Toxics 2020, 8, 29. [Google Scholar] [CrossRef]
- Fitt, W.K.; Hofmann, D.K. The Effects of the UV-Blocker Oxybenzone (Benzophenone-3) on Planulae Swimming and Metamorphosis of the Scyphozoans Cassiopea xamachana and Cassiopea frondosa. Oceans 2020, 1, 174–180. [Google Scholar] [CrossRef]
- Picot-Groz, M.; Fenet, H.; Martinez Bueno, M.J.; Rosain, D.; Gomez, E. Diurnal variations in personal care products in seawater and mussels at three Mediterranean coastal sites. Environ. Sci. Poll. Res. 2018, 25, 9051–9059. [Google Scholar] [CrossRef]
- Balmer, M.E.; Buser, H.-R.; Müller, M.D.; Poiger, T. Occurrence of some organic UV filters in wastewater, in surface waters, and in fish from Swiss lakes. Environ. Sci. Technol. 2005, 39, 953–962. [Google Scholar] [CrossRef]
- Nakata, H.; Murata, S.; Filatreau, J. Occurrence and concentrations of benzotriazole UV stabilizers in marine organisms and sediments from the Ariake Sea, Japan. Environ. Sci. Technol. 2009, 43, 6920–6926. [Google Scholar] [CrossRef] [PubMed]
- Cocci, P.; Mosconi, G.; Palermo, F.A. Sunscreen active ingredients in loggerhead turtles (Caretta caretta) and their relation to molecular markers of inflammation, oxidative stress and hormonal activity in wild populations. Mar. Pollut. Bull. 2020, 153, 111012. [Google Scholar] [CrossRef] [PubMed]
- Alonso, M.B.; Feo, M.L.; Corcellas, C.; Gago-Ferrero, P.; Bertozzi, C.P.; Marigo, J.; Flach, L.; Meirelles, A.C.O.; Carvalho, V.L.; Azevedo, A.F.; et al. Toxic heritage: Maternal transfer of pyrethroid insecticides and sunscreen agents in dolphins from Brazil. Environ. Pollut. 2015, 207, 391–402. [Google Scholar] [CrossRef] [PubMed]
- Mitchelmore, C.L.; He, K.; Gonsior, M.; Hain, E.; Heyes, A.; Clark, C.; Blaney, L. Occurrence and distribution of UV-filters and other anthropogenic contaminants in coastal surface water, sediment, and coral tissue from Hawaii. Sci. Total Environ. 2019, 670, 398–410. [Google Scholar] [CrossRef]
- Miller, I.B.; Moeller, M.; Kellermann, M.Y.; Nietzer, S.; Di Mauro, M.; Kambay, E.; Pawlowski, S.; Petersen-Thiery, M.; Schupp, P.J. Towards the Development of Standardized Bioassays for Corals: Acute Toxicity of the UV Filter Benzophenone-3 to Scleractinian Coral Larvae. Toxics 2022, 10, 244. [Google Scholar] [CrossRef]
- Zhong, Q.; Peng, M.; He, J.; Yang, W.; Huang, F. Association of prenatal exposure to phenols and parabens with birth size: A systematic review and meta-analysis. Sci. Total Environ. 2020, 703, 134720. [Google Scholar] [CrossRef]
- Díaz-Cruz, M.S.; Gago-Ferrero, P.; Llorca, M.; Barceló, D. Analysis of UV filters in tap water and other clean waters in Spain. Anal. Bioanal. Chem. 2012, 402, 2325–2333. [Google Scholar] [CrossRef]
- Fent, K.; Kunz, P.Y.; Zenker, A.; Rapp, M. A tentative environmental risk assessment of the UV-filters 3-(4-methylbenzylidene-camphor), 2-ethyl-hexyl-4-trimethoxycinnamate, benzophenone-3, benzophenone-4 and 3-benzylidene camphor. Mar. Environ. Res. 2010, 69, S4–S6. [Google Scholar] [CrossRef]
- Rodil, R.; Moeder, M.; Altenburger, R.; Schmitt-Jansen, M. Photostability and phytotoxicity of selected sunscreen agents and their degradation mixtures in water. Anal. Bioanal. Chem. 2009, 395, 1513–1524. [Google Scholar] [CrossRef]
- Oró-Nolla, B.; Lacorte, S.; Vike-Jonas, K.; Gonzalez, S.V.; Nygård, T.; Alexandros, G.; Asimakopoulos, A.G.; Jaspers, V.L.B. Occurrence of Bisphenols and Benzophenone UV Filters in White-Tailed Eagles (Haliaeetus albicilla) from Smøla, Norway. Toxics 2021, 9, 34. [Google Scholar] [CrossRef]
- Buck Louis, G.M.; Kannan, K.; Sapra, K.J.; Maisog, J.; Sundaram, R. Urinary concentrations of benzophenone-type UV filters and couple fecundity. Am. J. Epidemiol. 2014, 180, 1168–1175. [Google Scholar] [CrossRef]
- Buck Louis, G.M.; Chen, Z.; Schisterman, E.F.; Kim, S.; Sweeney, A.M.; Sundaram, R.; Lynch, C.D.; Gore-Langton, R.E.; Barr, D.B. Perfluorochemicals and human semen quality: The LIFE study. Environ. Health Perspect. 2015, 123, 57–63. [Google Scholar] [CrossRef]
- Wolff, M.S.; Engel, S.M.; Berkowitz, G.S.; Ye, X.; Silva, M.J.; Zhu, C.; Calafat, A.M. Prenatal phenol and phthalate exposures and birth outcomes. Environ. Health Perspect. 2008, 116, 1092–1097. [Google Scholar] [CrossRef] [PubMed]
- Pollack, A.Z.; Louis, G.B.; Chen, Z.; Sun, L.; Trabert, B.; Guo, Y.; Kannan, K. Bisphenol A, benzophenone-type ultraviolet filters, and phthalates in relation to uterine leiomyoma. Environ. Res. 2015, 137, 101–107. [Google Scholar] [CrossRef] [PubMed]
- Scinicariello, F.; Buser, M.C. Serum testosterone concentrations and urinary bisphenol A, benzophenone-3, triclosan, and paraben levels in male and female children and adolescents: NHANES 2011–2012. Environ. Health Perspect. 2016, 124, 1898–1904. [Google Scholar] [CrossRef] [PubMed]
- Mustieles, V.; Balogh, R.K.; Axelstad, M.; Montazeri, P.; Márquez, S.; Vrijheid, M.; Draskau, K.; Taxvig, C.; Peinado, F.C.; Berman, T.; et al. Benzophenone-3: Comprehensive review of the toxicological and human evidence with meta-analysis of human biomonitoring studies. Environ. Int. 2023, 173, 107739. [Google Scholar] [CrossRef]
- Zeiger, E.; Anderson, B.; Haworth, S.; Lawlor, T.; Mortelmans, K.; Speck, W. Salmonella mutagenicity tests: III. Results from the testing of 255 chemicals. Environ. Mutagen. 1987, 9, 61–109. [Google Scholar] [CrossRef]
- French, J.E. NTP technical report on toxicity studies of 2-hydroxy-4-methoxy-benzophenone (CAS No. 131-57-7) Administered topically and in dosed feed to F344/N Rats and B6C3F1 Mice. Toxic Rep. Ser. 1992, 21, 1–52. [Google Scholar]
- Santovito, A.; Ruberto, S.; Galli, G.; Menghi, C.; Girotti, M.; Cervella, P. Induction of chromosomal aberrations and micronuclei by 2-hydroxy-4-methoxybenzophenone (oxybenzone) in human lymphocytes. Drug Chem. Toxicol. 2019, 42, 378–385. [Google Scholar] [CrossRef]
- Commission Regulation (EU) 2017/238 of 10 February 2017 Amending Annex VI to Regulation (EC) No 1223/2009 of the European Parliament and of the Council on Cosmetic Products. L36/37. 2017, p. 36. Available online: https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32017R0238 (accessed on 29 July 2023).
- International Agency for Research on Cancer (IARC). Some Chemicals Present in Industrial and Consumer Products, Food and Drinking Water. IARC Monogr. Eval. Carcinog. Risks Hum. 2013, 101, 285–304. Available online: https://monographs.iarc.fr/ENG/Monographs/vol101/mono101-007.pdf (accessed on 29 July 2023).
- Concil of Europe-Report. Policy Statement Concerning paper and board materials and articles intended to come into contact with foodstuffs. Report about “Partial Agreement in the Social and Public Health Field”. 2009, Volume 4, p. 21. Available online: https://rm.coe.int/CoERMPublicCommonSearchServices/DisplayDCTMContent?documentId=09000016804e4794 (accessed on 29 July 2023).
- Imamović, B.; Trebše, P.; Omeragić, E.; Bečić, E.; Pečet, A.; Dedić, M. Stability and Removal of Benzophenone-Type UV Filters from Water Matrices by Advanced Oxidation Processes. Molecules 2022, 27, 1874. [Google Scholar] [CrossRef] [PubMed]
- SMAT Torino. Caratteristiche di Qualità delle Acque Erogate nei Comuni ATO 3 (Valori Medi Secondo Semestr3 2022). Available online: https://www.smatorino.it/monitoraggio-acque/ (accessed on 12 September 2023).
- Fodor, I.; Hussein, A.A.; Benjamin, P.R.; Koene, J.M.; Pirger, Z. The unlimited potential of the great pond snail, Lymnaea stagnalis. Elife 2020, 9, e56962. [Google Scholar] [CrossRef] [PubMed]
- Koene, J.M.; Ter Maat, A. Energy budget in the simultaneously hermaphroditic pond snail Lymnaea stagnalis: A trade-off between growth and reproduction during development. Belg. J. Zool. 2004, 134, 41–45. [Google Scholar] [CrossRef]
- Sella, G. Reciprocal egg trading and brood care in a hermaphroditic polychaete worm. Anim. Behav. 1985, 33, 938–944. [Google Scholar] [CrossRef]
- Åkesson, B. Morphology and life cycle of Ophryotrocha diadema, a new polychaete species from California. Ophelia 1976, 15, 25–35. [Google Scholar] [CrossRef]
- Berruti, G.; Ferraguti, M.; Lamia Donin, C.L. The aflagellate spermatozoon of Ophryotrocha: A line of evolution of fertilization among polychaetes. Gamete Res. 1978, 1, 278–292. [Google Scholar] [CrossRef]
- Santovito, A.; Ruberto, S.; Gendusa, C.; Cervella, P. In vitro evaluation of genomic damage induced by glyphosate on human lymphocytes. Environ. Sci. Poll. Res. 2018, 25, 34693–34700. [Google Scholar] [CrossRef]
- Seidel, F. Reproductive toxicity of benzophenone-3. Arch. Toxicol. 2020, 10, 3593–3594. [Google Scholar] [CrossRef]
- Kinnber, K.L.; Petersen, G.I.; Albrektsen, M.; Minghlani, M.; Awad, S.M.; Holbech, B.F.; Green, J.W.; Bjerregaard, P.; Holbech, H. Endocrine-disrupting effect of the ultraviolet filter benzophenone-3 in zebrafish, Danio rerio. Environ. Toxicol. Chem. 2015, 34, 2833–2840. [Google Scholar] [CrossRef]
- Chen, S.R.; Batool, A.; Wang, Y.Q.; Hao, X.X.; Chang, C.S.; Cheng, C.Y.; Liu, Y.X. The control of male fertility by spermatid-specific factors: Searching for contraceptive targets from spermatozoon’s head to tail. Cell Death Dis. 2016, 7, e2472. [Google Scholar] [CrossRef] [PubMed]
- He, T.T.; Mei Po Tsui, M.; Tan, C.J.; Ng, K.Y.; Guo, F.W.; Wang, L.H.; Chen, T.H.; Fan, T.Y.; Lam, P.K.S.; Murphy Burkhardt, M. Comparative toxicities of four benzophenone ultraviolet filters to two life stages of two coral species. Sci. Total Environ. 2019, 651, 2391–2399. [Google Scholar] [CrossRef] [PubMed]
- Moreira, A.L.P.; Paiva, W.S.; de Souza, A.M.; Pereira, M.C.G.; Rocha, H.A.O.; de Medeiros, S.R.B.; Luchiari, A.C. Benzophenone-3 causes oxidative stress in the brain and impairs aversive memory in adult zebrafish. Environ. Toxicol. Pharmacol. 2023, 100, 104164. [Google Scholar] [CrossRef] [PubMed]
- Hanson, K.M.; Gratton, E.; Bardeen, C.J. Sunscreen enhancement of UV-induced reactive oxygen species in the skin. Free Radic. Biol. Med. 2006, 41, 1205–1212. [Google Scholar] [CrossRef]
- Bluethgen, N.; Zucchi, S.; Fent, K. Effects of the UV filter benzophenone-3 (oxybenzone) at low concentrations in zebrafish (Danio rerio). Toxicol. Appl. Pharmacol. 2012, 263, 184–194. [Google Scholar] [CrossRef]
- Downs, C.A.; Kramarsky-Winter, E.; Segal, R.; Fauth, J.; Knutson, S.; Bronstein, O.; Ciner, F.R.; Jeger, R.; Lichtenfeld, Y.; Woodley, C.M.; et al. Toxicopathological effects of the sunscreen UV filter, Oxybenzone (Benzophenone-3), on coral Planulae and cultured primary cells and its environmental contamination in Hawaii and the U.S. Virgin Islands. Arch. Environ. Contam. Toxicol. 2016, 70, 265–288. [Google Scholar] [CrossRef]
- Zhang, Q.Y.; Ma, X.Y.; Dzakpasu, M.; Wang, X.C. Evaluation of ecotoxicological effects of benzophenone UV filters: Luminescent bacteria toxicity, genotoxicity and hormonal activity. Ecotoxicol. Environ. Saf. 2017, 142, 338–347. [Google Scholar] [CrossRef]
- Martín-Folgar, R.; Aquilino, M.; Ozáez, I.; Martínez-Guitarte, J.L. Ultraviolet filters and heat shock proteins: Effects in Chironomus riparius by benzophenone-3 and 4-methylbenzylidene camphor. Environ. Sci. Poll. Res. 2018, 25, 333–344. [Google Scholar] [CrossRef]
- Muñiz-González, A.B.; Martínez-Guitarte, J.L. Combined effects of benzophenone-3 and temperature on gene expression and enzymatic activity in the aquatic larvae Chironomus riparius. Sci. Total Environ. 2020, 698, 134292. [Google Scholar] [CrossRef]
- Marazzi, M.; Wibowo, M.; Gattuso, H.; Dumont, E.; Roca-Sanjuán, D.; Monari, A. Hydrogen abstraction by photo-excited benzophenone: Consequences for DNA photosensitization. Phys. Chem. Chem. Phys. 2016, 18, 7829–7836. [Google Scholar] [CrossRef]
- Bonassi, S.; El-Zein, R.; Bolognesi, C. Micronuclei frequency in peripheral blood lymphocytes and cancer risk: Evidence from human studies. Mutagenesis 2011, 26, 93–100. [Google Scholar] [CrossRef] [PubMed]
- Phiboonchaiyanan, P.P.; Busaranon, K.; Ninsontia, C.; Chanvorachote, P. Benzophenone-3 increases metastasis potential in lung cancer cells via epithelial to mesenchymal transition. Cell. Biol. Toxicol. 2017, 33, 251–261. [Google Scholar] [CrossRef] [PubMed]
- Im, H.; Achar, J.C.; Shim, T.; Jung, J. Elevated temperature alleviates benzophenone-3 toxicity in Daphnia magna. Aquat. Toxicol. 2022, 242, 106047. [Google Scholar] [CrossRef]
- Bessa da Silva, M.; Abrantes, N.; Rocha-Santos, T.A.P.; Duarte, A.C.; Freitas, A.C.; Gomes, A.M.; Carvalho, A.P.; Marques, J.C.; Gonçalves, F.; Pereira, R. Effects of dietary exposure to herbicide and of the nutritive quality of contaminated food on the reproductive output of Daphnia magna. Aquat. Toxicol. 2016, 179, 1–7. [Google Scholar] [CrossRef] [PubMed]
- Henry, J.; Brand, J.A.; Bai, Y.; Martin, J.M.; Wong, B.B.M.; Wlodkowic, D. Multi-generational impacts of exposure to antidepressant fluoxetine on behaviour, reproduction, and morphology of freshwater snail Physa acuta. Sci. Total. Environ. 2022, 814, 152731. [Google Scholar] [CrossRef]
- Cole, M.; Lindeque, P.; Fileman, E.; Halsband, C.; Galloway, T.S. The impact of polystyrene microplastics on feeding, function and fecundity in the marine copepod Calanus helgolandicus. Environ. Sci. Technol. 2015, 49, 1130–1137. [Google Scholar] [CrossRef]
Group—20 Individuals Per Container | Treatment [BP-3] |
---|---|
Controls | 0.000 mg/L freshwater |
Group 1 | 0.200 mg/L |
Group 2 | 0.100 mg/L |
Group 3 | 0.050 mg/L |
Group 4 | 0.025 mg/L |
Group—10 Individuals Per Bowl | Treatment [BP-3] |
---|---|
Controls | 0.000 mg/L pure artificial seawater |
Group 1 | 0.200 mg/L |
Group 2 | 0.100 mg/L |
Group 3 | 0.050 mg/L |
Group 4 | 0.025 mg/L |
BP-3 (mg/L) | No. of Observed MNi | ‰ MNi/Total Cells Scored ± SD | No. of Observed NBUDs | ‰ NBUDs/Total Cells Scored ±SD | BNCs | ‰ BNCs/Total Cell Scored ±SD |
---|---|---|---|---|---|---|
NC | 6 | 0.300 ± 0.470 | 20 | 1.000 ± 1.026 | 8 | 0.400 ± 0.60 |
0.025 | 8 | 0.400 ± 0.598 | 21 | 1.050 ± 0.945 | 10 | 0.500 ± 0.83 |
0.050 | 9 | 0.450 ± 0.686 | 23 | 1.150 ± 1.040 | 13 | 0.650 ± 0.99 |
0.100 | 18 | 0.900 ± 0.852 *** | 28 | 1.400 ± 1.536 | 12 | 0.600 ± 1.19 |
0.200 | 25 | 1.250 ± 0.910 * | 44 | 2.200 ± 1.963 ** | 10 | 0.500 ± 0.61 |
NC Mean ± SD | Group 4 0.025 mg/L Mean ± SD | Group 3 0.05 mg/L Mean ± SD | Group 2 0.10 mg/L Mean ± SD | Group 1 0.20 mg/L Mean ± SD | |
---|---|---|---|---|---|
Before treatment | 32.73 ± 1.55 | 32.45 ± 1.92 | 32.40 ± 1.47 | 32.68 ± 1.78 | 32.60 ± 1.78 |
After 4 weeks of treatment | 49.23 ± 2.83 | 48.60 ± 268 | 48.34 ± 2.44 | 46.39 ± 2.57 ** | 44.23 ± 3.16 * |
Differences | 16.51 ± 2.90 | 16.15 ± 1.98 | 15.94 ± 2.19 | 13.71 ± 2.35 °° | 11.61 ± 2.17 ° |
NC | Group 4 (0.025 mg/L) | Group 3 (0.05 mg/L) | Group 2 (0.10 mg/L) | Group 1 (0.20 mg/L) | |
---|---|---|---|---|---|
Week 1 | 2548 | 1010 | 1059 | 2476 | 2042 |
Week 2 | 1529 | 1764 | 1652 | 964 | 908 |
Week 3 | 2756 | 1988 | 1048 | 1422 | 764 |
Week 4 | 3128 | 2756 | 1406 | 2188 | 1854 |
Total | 9961 | 8550 | 6582 | 5633 | 4536 |
Mean ± SD/week | 2490 ± 684 | 2138 ± 430 | 1645 ± 607 | 1408 ± 556 | 1134 ± 490 * |
Between-Group Comparison | Kruskal-Wallis H Test | ||
---|---|---|---|
H | df | p-Value | |
Controls vs. Group 4 (0.025 mg/L) | 5.745 | 1 | =0.017 |
Controls vs. Group 3 (0.050 mg/L) | 13.765 | 1 | <0.001 |
Controls vs. Group 2 (0.100 mg/L) | 15.783 | 1 | <0.001 |
Controls vs. Group 1 (0.200 mg/L) | 15.783 | 1 | <0.001 |
Group 1 (0.200 mg/L vs. Group 4 (0.025 mg/L) | 15.783 | 1 | <0.001 |
Group 1 (0.200 mg/L) vs. Group 3 (0.050 mg/L) | 15.783 | 1 | <0.001 |
Group 1 (0.200 mg/L) vs. Group 2 (0.100 mg/L) | 15.783 | 1 | <0.001 |
Group 2 (0.100 mg/L vs. Group 4 (0.025 mg/L) | 12.574 | 1 | <0.001 |
Group 2 (0.100 mg/L vs. Group 3 (0.050 mg/L) | 11.885 | 1 | <0.001 |
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Santovito, A.; Pappalardo, A.; Nota, A.; Prearo, M.; Schleicherová, D. Lymnaea stagnalis and Ophryotrocha diadema as Model Organisms for Studying Genotoxicological and Physiological Effects of Benzophenone-3. Toxics 2023, 11, 827. https://doi.org/10.3390/toxics11100827
Santovito A, Pappalardo A, Nota A, Prearo M, Schleicherová D. Lymnaea stagnalis and Ophryotrocha diadema as Model Organisms for Studying Genotoxicological and Physiological Effects of Benzophenone-3. Toxics. 2023; 11(10):827. https://doi.org/10.3390/toxics11100827
Chicago/Turabian StyleSantovito, Alfredo, Alessia Pappalardo, Alessandro Nota, Marino Prearo, and Dáša Schleicherová. 2023. "Lymnaea stagnalis and Ophryotrocha diadema as Model Organisms for Studying Genotoxicological and Physiological Effects of Benzophenone-3" Toxics 11, no. 10: 827. https://doi.org/10.3390/toxics11100827
APA StyleSantovito, A., Pappalardo, A., Nota, A., Prearo, M., & Schleicherová, D. (2023). Lymnaea stagnalis and Ophryotrocha diadema as Model Organisms for Studying Genotoxicological and Physiological Effects of Benzophenone-3. Toxics, 11(10), 827. https://doi.org/10.3390/toxics11100827