Abstract
As a cycloaliphatic brominated flame retardant, hexabromocyclododecane (HBCD) has been widely used in building thermal insulation and fireproof materials. However, there is little information on the bioconcentration as well as effects with respect to HBCD exposure in the aquatic environment. To investigate the bioconcentration of HBCD in tissues (muscle and liver) and its biochemical and behavioural effects, juvenile crucian carp (Carassius auratus) were exposed to different concentrations of technical HBCD (nominal concentrations, 2, 20, 200 μg/L) for 7 days, using a flow-through exposure system. HBCD was found to concentrate in the liver and muscle with a terminal concentration of 0.60 ± 0.22 μg/g lw (lipid weight) and 0.18 ± 0.02 μg/g lw, respectively, at an environmentally-relevant concentration (2 μg/L). The total thyroxine and total triiodothyronine in the fish plasma were lowered as a result of exposure to the HBCD. Acetylcholinesterase activity in the brain was increased, while swimming activity was inhibited and shoaling inclination was enhanced after exposure to 200 μg/L HBCD. Feeding rate was suppressed in the 20 and 200 μg/L treatment groups. In summary, HBCD concentrations 10–100× higher than the current environmentally-relevant exposures induced adverse effects in the fish species tested in this study. These results suggest that increasing environmental concentrations and/or species with higher sensitivity than carp might be adversely affected by HBCD.
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Arukwe A, Carteny CC, Möder M, Bonini A, Maubach MA, Eggen T (2016) Differential modulation of neuro- and interrenal steroidogenesis of juvenile salmon by the organophosphates-tris(2-butoxyethyl)- and tris(2-cloroethyl) phosphate. Environ Res 148:63–71. https://doi.org/10.1016/j.envres.2016.03.020
Baldwin DH, Spromberg JA, Collier TK, Scholz NL (2009) A fish of many scales: extrapolating sublethal pesticide exposures to the productivity of wild salmon populations. Ecol Appl A Publ Ecol Soc Am 19(8):2004–2015. https://doi.org/10.1890/08-1891.1
Barry MJ (2013) Effects of fluoxetine on the swimming and behavioural responses of the Arabian killifish. Ecotoxicology 22(2):425–432. https://doi.org/10.1007/s10646-012-1036-7
Brewer SK, Little EE, DeLonay AJ, Beauvais SL, Jones SB, Ellersieck MR (2001) Behavioral dysfunctions correlate to altered physiology in rainbow trout (Oncorynchus mykiss) exposed to cholinesterase-inhibiting chemicals. Arch Environ Contam Toxicol 40(1):70–76. https://doi.org/10.1007/s002440010
Brimijoin S, Koenigsberger C (1999) Cholinesterases in neural development: new findings and toxicologic implications. Environ Health Persp 107(Suppl 1):59–64. https://doi.org/10.2307/3434472
Chen L, Huang C, Hu C, Yu K, Yang L, Zhou B (2012a) Acute exposure to DE-71: effects on locomotor behavior and developmental neurotoxicity in zebrafish larvae. Environ Toxicol Chem 31(10):2338–2344. https://doi.org/10.1002/etc.1958
Chen L, Yu K, Huang C, Yu L, Zhu B, Lam PK, Lam JC, Zhou B (2012b) Prenatal transfer of polybrominated diphenyl ethers (PBDEs) results in developmental neurotoxicity in zebrafish larvae. Environ Sci Technol 46(17):9727–9734. https://doi.org/10.1021/es302119g
Chen Q, Yu L, Yang L, Zhou B (2012c) Bioconcentration and metabolism of decabromodiphenyl ether (BDE-209) result in thyroid endocrine disruption in zebrafish larvae. Aquat Toxicol 110–111:141–148. https://doi.org/10.1016/j.aquatox.2012.01.008
Chiamolera MI, Wondisford FE (2009) Minireview: thyrotropin-releasing hormone and the thyroid hormone feedback mechanism. Endocrinology 150(3):1091–1096. https://doi.org/10.1210/en.2008-1795
Chokwe TB, Okonkwo JO, Sibali LL, Encube EJ (2015) Alkylphenol ethoxylates and brominated flame retardants in water, fish (carp) and sediment samples from the Vaal River, South Africa. Environ Sci Pollut Res 22(15):11922–11929. https://doi.org/10.1007/s11356-015-4430-x
Covaci A, Gerecke AC, Law RJ, Voorspoels S, Kohler M, Heeb NV, Leslie H, Allchin CR, De Boer J (2006) Hexabromocyclododecanes (HBCDs) in the environment and humans: a review. Environ Sci Technol 40(12):3679–3688. https://doi.org/10.1021/es0602492
de Wit CA, Herzke D, Vorkamp K (2010) Brominated flame retardants in the Arctic environment—trends and new candidates. Sci Total Environ 408(15):2885–2918. https://doi.org/10.1016/j.scitotenv.2009.08.037
Denoel M, D’Hooghe B, Ficetola GF, Brasseur C, De Pauw E, Thome JP, Kestemont P (2012) Using sets of behavioral biomarkers to assess short-term effects of pesticide: a study case with endosulfan on frog tadpoles. Ecotoxicology 21(4):1240–1250. https://doi.org/10.1007/s10646-012-0878-3
Dishaw LV, Hunter DL, Padnos B, Padilla S, Stapleton HM (2014) Developmental exposure to organophosphate flame retardants elicits overt toxicity and alters behavior in early life stage zebrafish (Danio rerio). Toxicol Sci 142(2):445–454. https://doi.org/10.1093/toxsci/kfu194
Du M, Lin L, Yan C, Zhang X (2012) Diastereoisomer- and enantiomer-specific accumulation, depuration, and bioisomerization of hexabromocyclododecanes in zebrafish (Danio rerio). Environ Sci Technol 46(20):11040–11046. https://doi.org/10.1021/es302166p
Egea-Serrano A, Tejedo M (2014) Contrasting effects of nitrogenous pollution on fitness and swimming performance of Iberian waterfrog, Pelophylax perezi, (Seoane, 1885), larvae in mesocosms and field enclosures. Aquat Toxicol 146(1):144–153. https://doi.org/10.1016/j.aquatox.2013.11.003
Esslinger S, Becker R, Maul R, Nehls I (2011) Hexabromocyclododecane enantiomers: microsomal degradation and patterns of hydroxylated metabolites. Environ Sci Technol 45(9):3938–3944. https://doi.org/10.1021/es1039584
Fonnum F, Mariussen E (2009) Mechanisms involved in the neurotoxic effects of environmental toxicants such as polychlorinated biphenyls and brominated flame retardants. J Neurochem 111(6):1327–1347. https://doi.org/10.1111/j.1471-4159.2009.06427.x
Fulton MH, Key PB (2001) Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorus insecticide exposure and effects. Environ Toxicol Chem 20(1):37–45. https://doi.org/10.1002/etc.5620200104
Gaworecki KM, Roberts AP, Ellis N, Sowers AD, Klaine SJ (2008) Biochemical and behavioral effects of diazinon exposure in hybrid striped bass. Environ Toxicol Chem 28(1):105–112. https://doi.org/10.1897/08-001.1
Gong W, Zhu L, Hao Y (2016) Lethal and sublethal toxicity comparison of BFRs to three marine planktonic copepods: effects on survival, metabolism and ingestion. PLoS ONE 11(1):e0147790. https://doi.org/10.1371/journal.pone.0147790
Haukås M, Mariussen E, Ruus A, Tollefsen KE (2009) Accumulation and disposition of hexabromocyclododecane (HBCD) in juvenile rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 95(2):144–151. https://doi.org/10.1016/j.aquatox.2009.08.010
Hong H, Shen R, Liu W, Li D, Huang L, Shi D (2015) Developmental toxicity of three hexabromocyclododecane diastereoisomers in embryos of the marine medaka Oryzias melastigma. Mar Pollut Bull 101(1):110–118. https://doi.org/10.1016/j.marpolbul.2015.11.009
Iqbal M, Syed JH, Katsoyiannis A, Malik RN, Farooqi A, Butt A, Li J, Zhang G, Cincinelli A, Jones KC (2017) Legacy and emerging flame retardants (FRs) in the freshwater ecosystem: a review. Environ Res 152:26–42. https://doi.org/10.1016/j.envres.2016.09.024
Janák K, Covaci A, Voorspoels S, Becher G (2005) Hexabromocyclododecane in marine species from the Western Scheldt Estuary: diastereoisomer- and enantiomer-specific accumulation. Environ Sci Technol 39(7):1987–1994. https://doi.org/10.1021/es0484909
Jarque S, Pina B (2014) Deiodinases and thyroid metabolism disruption in teleost fish. Environ Res 135:361–375. https://doi.org/10.1016/j.envres.2014.09.022
Kennedy CJ, Farrell AP (2006) Effects of exposure to the water-soluble fraction of crude oil on the swimming performance and the metabolic and ionic recovery postexercise in Pacific herring (Clupea pallasi). Environ Toxicol Chem 25(10):2715–2724. https://doi.org/10.1897/05-504R.1
Kodavanti PRS, Loganathan BG (2014) Polychlorinated biphenyls, polybrominated biphenyls, and brominated flame retardants. In: Gupta R (ed) Biomarkers in toxicology. Academic Press, Oxford, pp 433–450
Kuiper RV, Canton RF, Leonards PE, Jenssen BM, Dubbeldam M, Wester PW, van den Berg M, Vos JG, Vethaak AD (2007) Long-term exposure of European flounder (Platichthys flesus) to the flame-retardants tetrabromobisphenol A (TBBPA) and hexabromocyclododecane (HBCD). Ecotoxicol Environ Saf 67(3):349–360. https://doi.org/10.1016/j.ecoenv.2006.12.001
Law K, Palace VP, Halldorson T, Danell R, Wautier K, Evans B, Alaee M, Marvin C, Tomy GT (2006) Dietary accumulation of hexabromocyclododecane diastereoisomers in juvenile rainbow trout (Oncorhynchus mykiss) I: bioaccumulation parameters and evidence of bioisomerization. Environ Toxicol Chem 25(7):1757–1761. https://doi.org/10.1897/05-445R.1
Legler J (2008) New insights into the endocrine disrupting effects of brominated flame retardants. Chemosphere 73(2):216–222. https://doi.org/10.1016/j.chemosphere.2008.04.081
Li D, Xie P, Zhang X (2008) Changes in plasma thyroid hormones and cortisol levels in crucian carp (Carassius auratus) exposed to the extracted microcystins. Chemosphere 74(1):13–18. https://doi.org/10.1016/j.chemosphere.2008.09.065
Li L, Weber R, Liu J, Hu J (2016) Long-term emissions of hexabromocyclododecane as a chemical of concern in products in China. Environ Int 91:291–300. https://doi.org/10.1016/j.envint.2016.03.007
Liu J, Lu G, Ding J, Zhang Z, Wang Y (2014) Tissue distribution, bioconcentration, metabolism, and effects of erythromycin in crucian carp (Carassius auratus). Sci Total Environ 490:914–920. https://doi.org/10.1016/j.scitotenv.2014.05.055
Luigi V, Giuseppe M, Claudio R (2015) Emerging and priority contaminants with endocrine active potentials in sediments and fish from the River Po (Italy). Environ Sci Pollut Res 22(18):14050–14066. https://doi.org/10.1007/s11356-015-4388-8
Luo XJ, Ruan W, Zeng YH, Liu HY, Chen SJ, Wu JP, Mai BX (2013) Trophic dynamics of hexabromocyclododecane diastereomers and enantiomers in fish in a laboratory feeding study. Environ Toxicol Chem 32(11):2565–2570. https://doi.org/10.1002/etc.2337
Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101(1):13–30. https://doi.org/10.1016/j.aquatox.2010.10.006
Macaulay LJ, Bailey J, Levin E, Stapleton HM (2015) Persisting effects of a PBDE metabolite, 6-OH-BDE-47, on larval and juvenile zebrafish swimming behavior. Neurotoxicol Teratol 52:119–126. https://doi.org/10.1016/j.ntt.2015.05.002
Macaulay LJ, Chernick M, Chen A, Hinton DE, Bailey JM, Kullman SW, Levin ED, Stapleton HM (2017) Exposure to a PBDE/OH-BDE mixture alters juvenile zebrafish (Danio rerio) development. Environ Toxicol Chem 36(1):36–48. https://doi.org/10.1002/etc.3535
Marvin CH, Tomy GT, Armitage JM, Arnot JA, McCarty L, Covaci A, Palace V (2011) Hexabromocyclododecane: current understanding of chemistry, environmental fate and toxicology and implications for global management. Environ Sci Technol 45(20):8613–8623. https://doi.org/10.1021/es201548c
Noyes PD, Lema SC, Macaulay LJ, Douglas NK, Stapleton HM (2013) Low level exposure to the flame retardant BDE-209 reduces thyroid hormone levels and disrupts thyroid signaling in fathead minnows. Environ Sci Technol 47(17):10012–10021. https://doi.org/10.1021/es402650x
Noyes PD, Stapleton HM (2014) PBDE flame retardants. Endocr Disruptors 2(1):e29430. https://doi.org/10.4161/endo.29430
Oh JK, Kotani K, Managaki S, Masunaga S (2014) Levels and distribution of hexabromocyclododecane and its lower brominated derivative in Japanese riverine environment. Chemosphere 109:157–163. https://doi.org/10.1016/j.chemosphere.2014.01.074
Park BJ, Palace V, Wautier K, Gemmill B, Tomy G (2011) Thyroid axis disruption in juvenile brown trout (Salmo trutta) exposed to the flame retardant beta-tetrabromoethylcyclohexane (beta-TBECH) via the diet. Environ Sci Technol 45(18):7923–7927. https://doi.org/10.1021/es201530m
Pessoa PC, Luchmann KH, Ribeiro AB, Veras MM, Correa JR, Nogueira AJ, Bainy AC, Carvalho PS (2011) Cholinesterase inhibition and behavioral toxicity of carbofuran on Oreochromis niloticus early life stages. Aquat Toxicol 105(3):312–320. https://doi.org/10.1016/j.aquatox.2011.06.020
Rani M, Shim WJ, Han GM, Jang M, Song YK, Hong SH (2014) Hexabromocyclododecane in polystyrene based consumer products: an evidence of unregulated use. Chemosphere 110:111–119. https://doi.org/10.1016/j.chemosphere.2014.02.022
Richendrfer H, Creton R, Colwill RM (2014) The embryonic zebrafish as a model system to study the effects of environmental toxicants on behavior. In: Lessman CA, Carver EA (eds) Zebrafish. Nova Science Publishers, New York, pp 245–264
Rudel H, Muller J, Quack M, Klein R (2012) Monitoring of hexabromocyclododecane diastereomers in fish from European freshwaters and estuaries. Environ Sci Pollut Res 19(3):772–783. https://doi.org/10.1007/s11356-011-0604-3
Shi D, Lv D, Liu W, Shen R, Li D, Hong H (2017) Accumulation and developmental toxicity of hexabromocyclododecanes (HBCDs) on the marine copepod Tigriopus japonicus. Chemosphere 167:155–162. https://doi.org/10.1016/j.chemosphere.2016.09.160
Shuman-Goodier ME, Propper CR (2016) A meta-analysis synthesizing the effects of pesticides on swim speed and activity of aquatic vertebrates. Sci Total Environ 565:758–766. https://doi.org/10.1016/j.scitotenv.2016.04.205
Stadnicka-Michalak J, Schirmer K, Ashauer R (2015) Toxicology across scales: cell population growth in vitro predicts reduced fish growth. Sci Adv 1(7):e1500302. https://doi.org/10.1126/sciadv.1500302
Sun L, Tan H, Peng T, Wang S, Xu W, Qian H, Jin Y, Fu Z (2016) Developmental neurotoxicity of organophosphate flame retardants in early life stages of Japanese medaka (Oryzias latipes). Environ Toxicol Chem 35(12):2931–2940. https://doi.org/10.1002/etc.3477
Tang B, Zeng YH, Luo XJ, Zheng XB, Mai BX (2015a) Bioaccumulative characteristics of tetrabromobisphenol A and hexabromocyclododecanes in multi-tissues of prey and predator fish from an e-waste site, South China. Environ Sci Pollut Res 22(16):12011–12017. https://doi.org/10.1007/s11356-015-4463-1
Tang T, Yang Y, Chen Y, Tang W, Wang F, Diao X (2015b) Thyroid disruption in zebrafish larvae by short-term exposure to bisphenol AF. Int J Environ Res Public Health 12(10):13069–13084. https://doi.org/10.3390/ijerph121013069
Torre CD, Mariottini M, Vannuccini ML, Trisciani A, Marchi D, Corsi I (2014) Induction of CYP1A and ABC transporters in European sea bass (Dicentrarchus labrax) upon 2,3,7,8-TCDD waterborne exposure. Mar Environ Res 99(4):218–222. https://doi.org/10.1016/j.marenvres.2014.06.009
Tufi S, Leonards P, Lamoree M, de Boer J, Legler J, Legradi J (2016) Changes in neurotransmitter profiles during early zebrafish (Danio rerio) development and after pesticide exposure. Environ Sci Technol 50(6):3222–3230. https://doi.org/10.1021/acs.est.5b05665
UNEP (2012) Addendum to the risk management evaluation on hexabromocyclododecane. Report of the Persistent Organic Pollutants Review Committee on the Work of its Eighth Meeting (UNEP/POPS/POPRC.8/16/Add.3), POPRC, Geneva
UNEP (2013) SC-6/13: listing of hexabromocyclododecane. The Conference of the Parties. POPRC, Stockholm
UNEP (2015) Guidance for the inventory, identification and substitution of hexabromocyclododecane (HBCD). Secretariat of the Stockholm Convention, Stockholm
UNEP (2017) Draft guidance on best available techniques and best environmental practices for the production and use of hexabromocyclododecane listed with specific exemptions under the Stockholm Convention. BAT/BEP Group of Experts, Stockholm
Usenko C, Abel E, Hopkins A, Martinez G, Tijerina J, Kudela M, Norris N, Joudeh L, Bruce E (2016) Evaluation of common use brominated flame retardant (BFR) toxicity using a zebrafish embryo model. Toxics 4(3):21. https://doi.org/10.3390/toxics4030021
Wang Q, Lai LS, Wang X, Guo Y, Lam KS, Lam CW, Zhou B (2015) Bioconcentration and transfer of the organophorous flame retardant 1,3-dichloro-2-propyl phosphate causes thyroid endocrine disruption and developmental neurotoxicity in zebrafish larvae. Environ Sci Technol 49(8):5123–5132. https://doi.org/10.1021/acs.est.5b00558
Weis JS, Smith G, Zhou T, Bass CS, Weis P (2001) Effects of contaminants on behavior: biochemical mechanisms and ecological consequences. Bioscience 51(3):209–217. https://doi.org/10.1641/0006-3568(2001)051[0209:EOCOBB]2.0.CO;2
Xia J, Cao Z, Peng J, Fu S, Fu C (2014) The use of spontaneous behavior, swimming performances and metabolic rate to evaluate toxicity of PFOS on topmouth gudgeon Pseudorasbora parva. Acta Ecol Sin 34(5):284–289. https://doi.org/10.1016/j.chnaes.2014.07.006
Xie Z, Lu G, Hou K, Qin D, Yan Z, Chen W (2016) Bioconcentration, metabolism and effects of diphenhydramine on behavioral and biochemical markers in crucian carp (Carassius auratus). Sci Total Environ 544:400–409. https://doi.org/10.1016/j.scitotenv.2015.11.132
Xie Z, Lu G, Li S, Nie Y, Ma B, Liu J (2015) Behavioral and biochemical responses in freshwater fish Carassius auratus exposed to sertraline. Chemosphere 135:146–155. https://doi.org/10.1016/j.chemosphere.2015.04.031
Xie Z, Lu G, Qi P (2014) Effects of BDE-209 and its mixtures with BDE-47 and BDE-99 on multiple biomarkers in Carassius auratus. Environ Toxicol Phar 38(2):554–561. https://doi.org/10.1016/j.etap.2014.08.008
Yu L, Deng J, Shi X, Liu C, Yu K, Zhou B (2010) Exposure to DE-71 alters thyroid hormone levels and gene transcription in the hypothalamic-pituitary-thyroid axis of zebrafish larvae. Aquat Toxicol 97(3):226–233. https://doi.org/10.1016/j.aquatox.2009.10.022
Zhang B, Chen X, Pan R, Xu T, Zhao J, Huang W, Liu Y, Yin D (2017) Effects of three different embryonic exposure modes of 2,2′,4,4′-tetrabromodiphenyl ether on the path angle and social activity of zebrafish larvae. Chemosphere 169:542–549. https://doi.org/10.1016/j.chemosphere.2016.11.098
Zhang X, Yang F, Xiaoling Z, Xu Y, Liao T, Song S, Jianwei W (2008) Induction of hepatic enzymes and oxidative stress in Chinese rare minnow (Gobiocypris rarus) exposed to waterborne hexabromocyclododecane (HBCDD). Aquat Toxicol 86(1):4–11. https://doi.org/10.1016/j.aquatox.2007.07.002
Zhang Y, Sun H, Ruan Y (2014) Enantiomer-specific accumulation, depuration, metabolization and isomerization of hexabromocyclododecane (HBCD) diastereomers in mirror carp from water. J Hazard Mater 264:8–15. https://doi.org/10.1016/j.jhazmat.2013.10.062
Zhu N, Fu J, Gao Y, Ssebugere P, Wang Y, Jiang G (2013) Hexabromocyclododecane in alpine fish from the Tibetan Plateau, China. Environ Pollut 181:7–13. https://doi.org/10.1016/j.envpol.2013.05.050
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This study was supported by the National Natural Science Foundation of China (Grant 51769034, 51509071), the National Science Funds for Creative Research Groups of China (Grant 51421006), and the Priority Academic Program Development of Jiangsu Higher Education Institutions.
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Dong, H., Lu, G., Yan, Z. et al. Bioconcentration and effects of hexabromocyclododecane exposure in crucian carp (Carassius auratus). Ecotoxicology 27, 313–324 (2018). https://doi.org/10.1007/s10646-018-1896-6
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DOI: https://doi.org/10.1007/s10646-018-1896-6