Organophosphate-based flame retardant (tris(1,3-dichloro-2-propyl) phosphate) reduces fecundity and impairs embryonic development in marine invertebrates
Jill Man-Ying Chiu
A * , Yuk-Wa Lee A and Kelly Su A
+ Author Affiliations
- Author Affiliations
A Department of Biology, Hong Kong Baptist University, Kowloon Tong, Hong Kong SAR, PR China.
Marine and Freshwater Research 73(8) 1056-1063 https://doi.org/10.1071/MF22058
Submitted: 3 March 2022 Accepted: 1 June 2022 Published: 4 July 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: It is important to understand how marine invertebrates may be affected by tris(1,3-dichloro-2-propyl) phosphate (TDCIPP), as an organophosphorus flame retardant.
Aim: The present research verified the hypothesis that TDCIPP would adversely affect the growth, development and reproduction of Crepidula onyx (phylum Mollusca) and Tigriopus japonicus (phylum Arthropoda).
Methods: Effects of chronic exposure for the whole life cycle were examined at two concentrations of TDCIPP chosen on the basis of results from preliminary range-finding test.
Key results: Exposure to 1 and 10 μg L−1 of TDCIPP significantly reduced larval and juvenile survival rate and shell length in C. onyx. TDCIPP caused adverse reproductive effects, including abnormal embryonic development, which led to non-viable broods and the malformation of larvae. Exposure to TDCIPP resulted in a 100-fold increase in incidence rate of abnormal larva formation. In T. japonicus, exposure to TDCIPP (10 μg L−1) resulted in non-viable broods and a significant reduction in the number of eggs and number of nauplii.
Conclusions: Larval survival, larval growth, fecundity, and embryonic development were identified as the TDCIPP-affected ecological endpoints in the marine invertebrate C. onyx and T. japonicus.
Implications: From a management perspective, these results can help us assess the ecological risk posed by TDCIPP.
Keywords: copepod, developmental toxicity, gastropod, larva, marine invertebrate, organophosphate-based flame retardant, reproductive toxicity, TDCIPP.
References
Alzualde, A, Behl, M, Sipes, NS, Hsieh, J-H, Alday, A, Tice, RR, Paules, RS, Muriana, A, and Quevedo, C (2018). Toxicity profiling of flame retardants in zebrafish embryos using a battery of assays for developmental toxicity, neurotoxicity, cardiotoxicity and hepatotoxicity toward human relevance. Neurotoxicology and Teratology 70, 40–50.| Toxicity profiling of flame retardants in zebrafish embryos using a battery of assays for developmental toxicity, neurotoxicity, cardiotoxicity and hepatotoxicity toward human relevance.Crossref | GoogleScholarGoogle Scholar | 30312655PubMed |
Avila-Barnard, S, Dasgupta, S, Cheng, V, Reddam, A, Wiegand, JL, and Volz, DC (2022). Tris(1,3-dichloro-2-propyl) phosphate disrupts the trajectory of cytosine methylation within developing zebrafish embryos. Environmental Research 211, 113078.
| Tris(1,3-dichloro-2-propyl) phosphate disrupts the trajectory of cytosine methylation within developing zebrafish embryos.Crossref | GoogleScholarGoogle Scholar | 35248566PubMed |
Banasik M (2015) Tris[2-chloro-1-(chloromethyl) ethyl] phosphate (TDCPP). In ‘Hamilton & Hardy’s industrial toxicology’. (Eds RD Harbison, MM Bourgeois, GT Johnson) pp. 837–844. (Wiley: New York, NY, USA)
Cao, S, Zeng, X, Song, H, Li, H, Yu, Z, Sheng, G, and Fu, J (2012). Levels and distributions of organophosphate flame retardants and plasticizers in sediment from Taihu Lake, China. Environmental Toxicology and Chemistry 31, 1478–1484.
| Levels and distributions of organophosphate flame retardants and plasticizers in sediment from Taihu Lake, China.Crossref | GoogleScholarGoogle Scholar | 22553152PubMed |
Chan, CYS, and Chiu, JMY (2015). Chronic effects of coated silver nanoparticles on marine invertebrate larvae: a proof of concept study. PLoS ONE 10, e0132457.
| Chronic effects of coated silver nanoparticles on marine invertebrate larvae: a proof of concept study.Crossref | GoogleScholarGoogle Scholar |
Cristale, J, Aragão Belé, TG, Lacorte, S, and Rodrigues de Marchi, MR (2018). Occurrence and human exposure to brominated and organophosphorus flame retardants via indoor dust in a Brazilian city. Environmental Pollution 237, 695–703.
| Occurrence and human exposure to brominated and organophosphorus flame retardants via indoor dust in a Brazilian city.Crossref | GoogleScholarGoogle Scholar | 29129432PubMed |
Dishaw, LV, Hunter, DL, Padnos, B, Padilla, S, and Stapleton, HM (2014). Developmental exposure to organophosphate flame retardants elicits overt toxicity and alters behavior in early life stage zebrafish (Danio rerio). Toxicological Sciences 142, 445–454.
| Developmental exposure to organophosphate flame retardants elicits overt toxicity and alters behavior in early life stage zebrafish (Danio rerio).Crossref | GoogleScholarGoogle Scholar | 25239634PubMed |
Evenset A, Leknes H, Christensen GN, Warner N, Remberger M, Gabrielsen GW (2009) ‘Screening of new contaminants in samples from the Norwegian Arctic: silver, platinum, sucralose, bisphenol A, tetrabrombisphenol A, siloxanes, phtalates (DEHP), phosphororganic flame retardants.’ (Norwegian Pollution Control Authority)
Fu, J, Han, J, Zhou, B, Gong, Z, Santos, EM, Huo, X, Zheng, W, Liu, H, Yu, H, and Liu, C (2013). Toxicogenomic responses of zebrafish embryos/larvae to tris(1,3-dichloro-2-propyl) phosphate (TDCPP) reveal possible molecular mechanisms of developmental toxicity. Environmental Science & Technology 47, 10574–10582.
| Toxicogenomic responses of zebrafish embryos/larvae to tris(1,3-dichloro-2-propyl) phosphate (TDCPP) reveal possible molecular mechanisms of developmental toxicity.Crossref | GoogleScholarGoogle Scholar |
Godfrey, A, Hooser, B, Abdelmoneim, A, and Sepúlveda, MS (2019). Sex-specific endocrine-disrupting effects of three halogenated chemicals in Japanese medaka. Journal of Applied Toxicology 39, 1215–1223.
| Sex-specific endocrine-disrupting effects of three halogenated chemicals in Japanese medaka.Crossref | GoogleScholarGoogle Scholar | 31066087PubMed |
Guo, F, Wang, L, and Wang, W-X (2012). Acute and chronic toxicity of polychlorinated biphenyl 126 to Tigriopus japonicus: effects on survival, growth, reproduction, and intrinsic rate of population growth. Environmental Toxicology and Chemistry 31, 639–645.
| Acute and chronic toxicity of polychlorinated biphenyl 126 to Tigriopus japonicus: effects on survival, growth, reproduction, and intrinsic rate of population growth.Crossref | GoogleScholarGoogle Scholar | 22189719PubMed |
Henry, JQ, Perry, KJ, and Martindale, MQ (2006). Cell specification and the role of the polar lobe in the gastropod mollusc Crepidula fornicata. Developmental Biology 297, 295–307.
| Cell specification and the role of the polar lobe in the gastropod mollusc Crepidula fornicata.Crossref | GoogleScholarGoogle Scholar | 16919619PubMed |
Hu, M, Li, J, Zhang, B, Cui, Q, Wei, S, and Yu, H (2014). Regional distribution of halogenated organophosphate flame retardants in seawater samples from three coastal cities in China. Marine Pollution Bulletin 86, 569–574.
| Regional distribution of halogenated organophosphate flame retardants in seawater samples from three coastal cities in China.Crossref | GoogleScholarGoogle Scholar | 24974164PubMed |
International Programme on Chemical Safety (1998) Flame retardants: tris(chloropropyl) phosphate and tris(2-chloroethyl) phosphate. Environmental health criteria 209. (World Health Organization: Geneva, Switzerland) Available at http://whqlibdoc.who.int/ehc/WHO_EHC_209.pdf
Lai, S, Xie, Z, Song, T, Tang, J, Zhang, Y, Mi, W, Peng, J, Zhao, Y, Zou, S, and Ebinghaus, R (2015). Occurrence and dry deposition of organophosphate esters in atmospheric particles over the northern South China Sea. Chemosphere 127, 195–200.
| Occurrence and dry deposition of organophosphate esters in atmospheric particles over the northern South China Sea.Crossref | GoogleScholarGoogle Scholar | 25732631PubMed |
Liu, X, Ji, K, and Choi, K (2012). Endocrine disruption potentials of organophosphate flame retardants and related mechanisms in H295R and MVLN cell lines and in zebrafish. Aquatic Toxicology 114–115, 173–181.
| Endocrine disruption potentials of organophosphate flame retardants and related mechanisms in H295R and MVLN cell lines and in zebrafish.Crossref | GoogleScholarGoogle Scholar | 22446829PubMed |
Liu, X, Ji, K, Jo, A, Moon, H-B, and Choi, K (2013). Effects of TDCPP or TPP on gene transcriptions and hormones of HPG axis, and their consequences on reproduction in adult zebrafish (Danio rerio). Aquatic Toxicology 134–135, 104–111.
| Effects of TDCPP or TPP on gene transcriptions and hormones of HPG axis, and their consequences on reproduction in adult zebrafish (Danio rerio).Crossref | GoogleScholarGoogle Scholar | 23603146PubMed |
Ma, Y, Cui, K, Zeng, F, Wen, J, Liu, H, Zhu, F, Ouyang, G, Luan, T, and Zeng, Z (2013). Microwave-assisted extraction combined with gel permeation chromatography and silica gel cleanup followed by gas chromatography–mass spectrometry for the determination of organophosphorus flame retardants and plasticizers in biological samples. Analytica Chimica Acta 786, 47–53.
| Microwave-assisted extraction combined with gel permeation chromatography and silica gel cleanup followed by gas chromatography–mass spectrometry for the determination of organophosphorus flame retardants and plasticizers in biological samples.Crossref | GoogleScholarGoogle Scholar | 23790291PubMed |
Marklund, A, Andersson, B, and Haglund, P (2005). Organophosphorus flame retardants and plasticizers in Swedish sewage treatment plants. Environmental Science & Technology 39, 7423–7429.
| Organophosphorus flame retardants and plasticizers in Swedish sewage treatment plants.Crossref | GoogleScholarGoogle Scholar |
Maruya, KA, Dodder, NG, Sengupta, A, Smith, DJ, Lyons, JM, Heil, AT, and Drewes, JE (2016). Multimedia screening of contaminants of emerging concern (CECS) in coastal urban watersheds in southern California (USA). Environmental Toxicology and Chemistry 35, 1986–1994.
| Multimedia screening of contaminants of emerging concern (CECS) in coastal urban watersheds in southern California (USA).Crossref | GoogleScholarGoogle Scholar | 26748657PubMed |
McGee, SP, Cooper, EM, Stapleton, HM, and Volz, DC (2012). Early zebrafish embryogenesis is susceptible to developmental TDCPP exposure. Environmental Health Perspectives 120, 1585–1591.
| Early zebrafish embryogenesis is susceptible to developmental TDCPP exposure.Crossref | GoogleScholarGoogle Scholar | 23017583PubMed |
Mercurio, S, Messinetti, S, Manenti, R, Ficetola, GF, and Pennati, R (2021). Embryotoxicity characterization of the flame retardant tris(1-chloro-2-propyl)phosphate (TCPP) in the invertebrate chordate Ciona intestinalis. Journal of Experimental Zoology – A. Ecological and Integrative Physiology 335, 339–347.
| Embryotoxicity characterization of the flame retardant tris(1-chloro-2-propyl)phosphate (TCPP) in the invertebrate chordate Ciona intestinalis.Crossref | GoogleScholarGoogle Scholar | 33503327PubMed |
Or P (2015) ‘TSCA work plan chemical problem formulation and initial assessment chlorinated phosphate ester cluster flame retardants.’ (Office of Chemical Safety and Pollution Control, United States Environmental Protection Agency)
Po, BHK, and Chiu, JMY (2018). Transgenerational impairments of reproduction and development of the marine invertebrate Crepidula onyx resulted from long-term dietary exposure of 2,2′,4,4′-tetrabromodiphenyl ether (BDE-47). Environmental Pollution 235, 730–738.
| Transgenerational impairments of reproduction and development of the marine invertebrate Crepidula onyx resulted from long-term dietary exposure of 2,2′,4,4′-tetrabromodiphenyl ether (BDE-47).Crossref | GoogleScholarGoogle Scholar | 29339342PubMed |
Scientific Committee on Health and Environmental Risks (2007) Risk assessment report on tris[2-chloro-1-(chloromethyl) ethyl]phosphate (TDCP), environmental part. CAS 13674-87-8, EINECS 237-159-2. (European Commission: Brussels, Belgium) Available at https://ec.europa.eu/health/archive/ph_risk/committees/04_scher/docs/scher_o_068.pdf
Stapleton, HM, Klosterhaus, S, Eagle, S, Fuh, J, Meeker, JD, Blum, A, and Webster, TF (2009). Detection of organophosphate flame retardants in furniture foam and US house dust. Environmental Science & Technology 43, 7490–7495.
| Detection of organophosphate flame retardants in furniture foam and US house dust.Crossref | GoogleScholarGoogle Scholar |
Sundkvist, AM, Olofsson, U, and Haglund, P (2010). Organophosphorus flame retardants and plasticizers in marine and fresh water biota and in human milk. Journal of Environmental Monitoring 12, 943–951.
| Organophosphorus flame retardants and plasticizers in marine and fresh water biota and in human milk.Crossref | GoogleScholarGoogle Scholar | 20383376PubMed |
Tan, H, Peng, C, Guo, Y, Wang, X, Wu, Y, and Chen, D (2017). Organophosphate flame retardants in house dust from South China and related human exposure risks. Bulletin of Environmental Contamination and Toxicology 99, 344–349.
| Organophosphate flame retardants in house dust from South China and related human exposure risks.Crossref | GoogleScholarGoogle Scholar | 28573493PubMed |
van de Merwe, JP, Chan, AKY, Lei, ENY, Yau, MS, Lam, MHW, and Wu, RSS (2011). Bioaccumulation and maternal transfer of PBDE 47 in the marine medaka (Oryzias melastigma) following dietary exposure. Aquatic Toxicology 103, 199–204.
| Bioaccumulation and maternal transfer of PBDE 47 in the marine medaka (Oryzias melastigma) following dietary exposure.Crossref | GoogleScholarGoogle Scholar | 21481818PubMed |
Wang, Q, Liang, K, Liu, J, Yang, L, Guo, Y, Liu, C, and Zhou, B (2013). Exposure of zebrafish embryos/larvae to TDCPP alters concentrations of thyroid hormones and transcriptions of genes involved in the hypothalamic–pituitary–thyroid axis. Aquatic Toxicology 126, 207–213.
| Exposure of zebrafish embryos/larvae to TDCPP alters concentrations of thyroid hormones and transcriptions of genes involved in the hypothalamic–pituitary–thyroid axis.Crossref | GoogleScholarGoogle Scholar | 23220413PubMed |
Wang, X, He, Y, Lin, L, Zeng, F, and Luan, T (2014). Application of fully automatic hollow fiber liquid phase microextraction to assess the distribution of organophosphate esters in the Pearl River Estuaries. Science of the Total Environment 470–471, 263–269.
| Application of fully automatic hollow fiber liquid phase microextraction to assess the distribution of organophosphate esters in the Pearl River Estuaries.Crossref | GoogleScholarGoogle Scholar | 24140697PubMed |
Wang, Q, Lam, JCW, Han, J, Wang, X, Guo, Y, Lam, PKS, and Zhou, B (2015a). Developmental exposure to the organophosphorus flame retardant tris(1,3-dichloro-2-propyl) phosphate: estrogenic activity, endocrine disruption and reproductive effects on zebrafish. Aquatic Toxicology 160, 163–171.
| Developmental exposure to the organophosphorus flame retardant tris(1,3-dichloro-2-propyl) phosphate: estrogenic activity, endocrine disruption and reproductive effects on zebrafish.Crossref | GoogleScholarGoogle Scholar | 25637911PubMed |
Wang, Q, Lam, JC-W, Man, Y-C, Lai, NL-S, Kwok, KY, Guo, Y, Lam, PK-S, and Zhou, B (2015b). Bioconcentration, metabolism and neurotoxicity of the organophorous flame retardant 1,3-dichloro 2-propyl phosphate (TDCPP) to zebrafish. Aquatic Toxicology 158, 108–115.
| Bioconcentration, metabolism and neurotoxicity of the organophorous flame retardant 1,3-dichloro 2-propyl phosphate (TDCPP) to zebrafish.Crossref | GoogleScholarGoogle Scholar | 25461749PubMed |
Wang, L, Huang, X, Laserna, AKC, and Li, SFY (2020). Metabolomics reveals that tris(1,3-dichloro-2-propyl) phosphate (TDCPP) causes disruption of membrane lipids in microalga Scenedesmus obliquus. Science of the Total Environment 708, 134498.
| Metabolomics reveals that tris(1,3-dichloro-2-propyl) phosphate (TDCPP) causes disruption of membrane lipids in microalga Scenedesmus obliquus.Crossref | GoogleScholarGoogle Scholar | 31796289PubMed |
Yan, S, Wang, Q, Yang, L, and Zha, J (2020). Comparison of the toxicity effects of tris(1,3-dichloro-2-propyl) phosphate (TDCIPP) with tributyl phosphate (TNBP) reveals the mechanism of the apoptosis pathway in Asian freshwater clams (Corbicula fluminea). Environmental Science & Technology 54, 6850–6858.
| Comparison of the toxicity effects of tris(1,3-dichloro-2-propyl) phosphate (TDCIPP) with tributyl phosphate (TNBP) reveals the mechanism of the apoptosis pathway in Asian freshwater clams (Corbicula fluminea).Crossref | GoogleScholarGoogle Scholar |
Yin, S-Y, Chen, L, Wu, D-Y, Wang, T, Huo, L-J, Zhao, S, Zhou, J, Zhang, X, and Miao, Y-L (2019). Tris(1,3-dichloro-2-propyl) phosphate disturbs mouse embryonic development by inducing apoptosis and abnormal DNA methylation. Environmental and Molecular Mutagenesis 60, 807–815.
| Tris(1,3-dichloro-2-propyl) phosphate disturbs mouse embryonic development by inducing apoptosis and abnormal DNA methylation.Crossref | GoogleScholarGoogle Scholar | 31411769PubMed |
