Skip to main content

Toxicological effects of the sunscreen UV filter, benzophenone-2, on planulae and in vitro cells of the coral, Stylophora pistillata

An Erratum to this article was published on 15 March 2014

Abstract

Benzophenone-2 (BP-2) is an additive to personal-care products and commercial solutions that protects against the damaging effects of ultraviolet light. BP-2 is an “emerging contaminant of concern” that is often released as a pollutant through municipal and boat/ship wastewater discharges and landfill leachates, as well as through residential septic fields and unmanaged cesspits. Although BP-2 may be a contaminant on coral reefs, its environmental toxicity to reefs is unknown. This poses a potential management issue, since BP-2 is a known endocrine disruptor as well as a weak genotoxicant. We examined the effects of BP-2 on the larval form (planula) of the coral, Stylophora pistillata, as well as its toxicity to in vitro coral cells. BP-2 is a photo-toxicant; adverse effects are exacerbated in the light versus in darkness. Whether in darkness or light, BP-2 induced coral planulae to transform from a motile planktonic state to a deformed, sessile condition. Planulae exhibited an increasing rate of coral bleaching in response to increasing concentrations of BP-2. BP-2 is a genotoxicant to corals, exhibiting a strong positive relationship between DNA-AP lesions and increasing BP-2 concentrations. BP-2 exposure in the light induced extensive necrosis in both the epidermis and gastrodermis. In contrast, BP-2 exposure in darkness induced autophagy and autophagic cell death. The LC50 of BP-2 in the light for an 8 and 24 h exposure was 120 and 165 parts per billion (ppb), respectively. The LC50s for BP-2 in darkness for the same time points were 144 and 548 ppb. Deformity EC20 levels (24 h) were 246 parts per trillion in the light and 9.6 ppb in darkness.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

References

  • Abelson A, Ronen O, Gaines S (2005) Coral recruitment to the reefs of Eilat, Red Sea: temporal and spatial variation, and possible effects of anthropogenic disturbances. Mar Pollut Bull 50:576–582

    CAS  Google Scholar 

  • Agati G, Mazzinghi P, Fusi F, Ambrosini I (1995) The F685/F730 chlorophyll fluorescence ratio as a tool in plant physiology: response to physiological and environmental factors. J Plant Physiol 14:228–238

    Google Scholar 

  • Agresti A (2002) Categorical data analysis, 2nd edn. Wiley, New York

    Google Scholar 

  • Anderson SL, Wild GC (1994) Linking genotoxic responses and reproductive success in ecotoxicology. Environ Health Perspect 102:9–12

    Google Scholar 

  • Aquera A, Martinez Bueno MJ, Fernandez-Alba AR (2013) New trends in the analytical determination of emerging contaminants and their transformation products in environmental waters. Environ Sci Pollut Res Int 20:3496–3515

    Google Scholar 

  • Bishop CD, Huggett MJ, Heyland A, Hodion J, Brandhorst BP (2006) Interspecific variation in metamorphic competence in marine invertebrates: the significance for comparative investigations into the timing of metamorphosis. Integr Comp Biol 46:662–682

    CAS  Google Scholar 

  • Blaauboe BJ (2008) The contribution of in vitro toxicity data in hazard and risk assessment: current limitations and future perspective. Toxicol Lett 180:81–84

    Google Scholar 

  • Blitz JB, Norton SA (2008) Possible environmental effects of sunscreen run-off. J Am Acad Dermatol 59:898. doi:10.1016/j.jaad.2008.06.013

    Google Scholar 

  • Brooks AC, Gaskell PN, Maltby LL (2009) Importance of prey and predator feeding behaviors for trophic transfer and secondary poisoning. Environ Sci Technol 43:7916–7923

    CAS  Google Scholar 

  • Burke RD (1983) The induction of metamorphosis of marine invertebrate larvae: stimulus and response. Can J Zool 61:1701–1719

    Google Scholar 

  • Carson FL (1997) Histotechnology: a self-instructional text, 2nd edn. American Society of Clinical Pathologists, Chicago

    Google Scholar 

  • CIR (Cosmetic Ingredient Review) (2005) Annual review of cosmetic ingredient safety assessments—2003/2003. Int J Toxicol 24:1–102

    Google Scholar 

  • Cosnefroy A, Brion F, Maillot-Marechal E et al (2012) Selective activation of zebrafish estrogen receptor subtypes by chemicals by using stable reporter gene assay developed in a zebrafish liver cell line. Toxicol Sci 125:439–449

    CAS  Google Scholar 

  • Crawley MJ (1993) GLIM for ecologists. Blackwell, London

    Google Scholar 

  • Cuquerella MC, Lhiaubet-Vallet V, Cadet J, Miranda MA (2012) Benzophenone photosensitized DNA damage. Acc Chem Res 45:1558–1570

    CAS  Google Scholar 

  • Danovaro R, Bongiorni L, Corinaldesi C et al (2008) Sunscreens cause coral bleaching by promoting viral infections. Environ Health Persp 116:441–447

    CAS  Google Scholar 

  • Daughton CG (2002) Environmental stewardship and drugs as pollutants. Lancet 360:1035–1036

    Google Scholar 

  • Depledge MH (1998) The ecotoxicological significance of genotoxicity in marine invertebrates. Mutat Res 399:109–122

    CAS  Google Scholar 

  • Downs CA, Fauth JE, Halas JC, Dustan P, Bemiss J, Woodley CM (2002) Oxidative stress and seasonal coral bleaching. Free Radical Biol Med 32:533–543

    Google Scholar 

  • Downs CA, Karamarsky-Kramer W, Martinez J et al (2009) Symbiophagy as a mechanism for coral bleaching. Autophagy 5:211–216

    CAS  Google Scholar 

  • Downs CA, Fauth JE, Downs VD, Ostrander GK (2010) In vitro cell-toxicity screening as an alternative animal model for coral toxicology: effects of heat stress, sulfide, rotenone, cyanide, and cuprous oxide on cell viability and mitochondrial function. Ecotoxicology 19:171–184

    CAS  Google Scholar 

  • Downs CA, Woodley CM, Fauth JE et al (2011) A survey of environmental pollutants and cellular-stress biomarkers of Porites astreoides at six sites in St. John. US Virgin Islands. Ecotoxicology 20:1914–1931

    CAS  Google Scholar 

  • Downs CA, Ostrander GK, Rougee L et al (2012) The use of cellular diagnostics for identifying sub-lethal stress in reef corals. Ecotoxicology 21:768–782

    CAS  Google Scholar 

  • Downs CA, McDougall KE, Woodley CM et al (2013) Heat stress and light stress induce different cellular pathologies in the symbiotic dinflagellate during coral bleaching. PLoS ONE 8(12):e77173

    CAS  Google Scholar 

  • Drablos F, Feyzi E, Aas PA et al (2004) Alkylation damage in DNA and RNA—repair mechanisms and medical significance. DNA Repair 3:1389–1407

    CAS  Google Scholar 

  • Draper NR, Smith H (1966) Applied regression analysis. Wiley, New York

    Google Scholar 

  • Dustan P (1977) Vitality of reef coral populations off Key Largo, Florida: recruitment and mortality. Environ Geol 2:51–58

    Google Scholar 

  • EC (2003) Technical Guidance Documents on Risk Assessment, Part II. EUR 20418 EN/2 Ispra, Italy: European Commission, Joint Research Centre, http://ihcp.jrc.ec.europa.eu/our_activities/public-health/risk_assessment_of_Biocides/doc/tgd/tgdpart2_2ed.pdf. Accessed 18 Nov 2013

  • Edinger EN, Jompa J, Limmon GV, Widjatmoko W, Risk MJ (1998) Reef degradation and coral biodiversity in Indonesia: effects of land-based pollution, destructive fishing practices and changes over time. Mar Pollut Bull 36:617–630

    CAS  Google Scholar 

  • Eichenseher T (2006) The cloudy side of sunscreens. Environ Sci Technol 40:1377–1378

    CAS  Google Scholar 

  • Eskelinin EL, Reggiori F, Baba M, Kovacs AL, Seglen PO (2011) Seeing is believing: the impact of electron microscopy on autophagy research. Autophagy 7:935–956

    Google Scholar 

  • Fadlallah YH (1983) Sexual reproduction, development and larval biology in scleractinian corals: a review. Coral Reefs 2:129–150

    Google Scholar 

  • Finney DJ (1947) Probit analysis, a statistical treatment of the sigmoid response curve. Cambridge University Press, Cambridge

    Google Scholar 

  • Fortini P, Raspaglio G, Falchi M, Dogliotti E (1996) Analysis of DNA alkylation damage and repair in mammalian cells by the COMET assay. Mutagen 11:169–175

    CAS  Google Scholar 

  • Futch JC, Griffin DW, Lipp EK (2010) Human enteric viruses in groundwater indicate offshore transport of human sewage to coral reefs of the Upper Florida Keys. Environ Microbiol 12:964–974

    CAS  Google Scholar 

  • Gago-Ferrero P, Díaz-Cruz MS, Barceló D (2011) Occurrence of multiclass UV filters in treated sewage sludge from wastewater treatment plants. Chemosphere 84:1158–1165

    CAS  Google Scholar 

  • Gilbert E, Pirot F, Bertholle V, Roussel L, Falson F, Padois K (2013) Commonly used UV filter toxicity on biological functions: review of last decade studies. Int J Cosmetic Sci 35:208–219

    CAS  Google Scholar 

  • Gitelson AA, Buschmann C, Lichtenthaler HK (1999) The chlorophyll fluorescence ration F735/F700 as an accurate measure of the chlorophyll content in plants. Remote Sensing Environ 69:296–302

    Google Scholar 

  • Gleason DF, Hofmann DK (2011) Coral larvae: from gametes to recruits. J Exp Mar Biol Ecol 408:42–57

    Google Scholar 

  • Golbuu Y, Fabricius K, Victor S, Richmond R (2008) Gradients in coral reef communities exposed to muddy river discharges in Pohnpei, Micronesia. Estuar Coast Shelf S 76:14–20

    Google Scholar 

  • Gura T (2008) Toxicity testing moves from the legislature to the Petri dish–and back. Cell 134:557–559. doi:10.1016/j.cell.2008.08.011

    CAS  Google Scholar 

  • Harii S, Nadaoka K, Yamamoto M, Iwao K (2007) Temporal changes in settlement, lipid content, and lipid composition of larvae of the spawning hermatypic coral Acropora tenuis. Mar Ecol-Prog Ser 346:86–89

    Google Scholar 

  • Harper CA, Petrie EM (2003) Plastics materials and processes: a concise encylopedia. Wiley, Hoboken

    Google Scholar 

  • Hsieh MH, Grantham EC, Liu B, Macapagal R, Willingham E, Baskin LS (2007) In utero exposure to benzophenone-2 causes hypospadias through an estrogen receptor dependent mechanism. J Urology 178:1637–1642

    CAS  Google Scholar 

  • Hughes TP, Tanner JE (2000) Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 81:2250–2263

    Google Scholar 

  • Jager T, Heugens EHW, Kooijman SALM (2006) Making sense of ecotoxicological test results: towards application of process-based models. Ecotoxicology 15:305–314

    CAS  Google Scholar 

  • Jarry H, Christoffel J, Rimoldi G, Koch L, Wuttke W (2004) Multi-organic endocrine disrupting activity of the UV screen benzophenone 2 (BP2) in ovariectomized adult rats after 5 days treatment. Toxicology 205:87–93

    CAS  Google Scholar 

  • Kerdivel G, Le Guevel R, Habauzit D, Brion F, Ait-Aissa S, Pakdel F (2013) Estrogenic potency of benzophenone UV filters in breast cancer cells: proliferative and transcriptional activity substantiated by docking analysis. PLoS ONE 8:e60567. doi:10.1371/journal.pone.0060567

    CAS  Google Scholar 

  • Kerr JFR, Wullie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implication in tissue kinetics. Br J Cancer 26:239–257

    CAS  Google Scholar 

  • Kim Y, Ryu JC, Choi H-S, Lee K (2011) Effect of 2,2′,4,4′-tetrahydroxybenzopheonone (BP2) on steroidogenesis in testicular Leydig cells. Toxicology 288:18–26

    CAS  Google Scholar 

  • Klionsky DJ, Abdalalla FC, Abeliovich H et al (2012) Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8:445–544

    CAS  Google Scholar 

  • Knowland J, McKenzie EA, McHugh PJ, Cridland NA (1993) Sunlight-induced mutagenicity of a common sunscreen ingredient. FEBS Lett 324:309–313

    CAS  Google Scholar 

  • Koda T, Umezu T, Kamata R, Morohoshi K, Ohta T, Morita M (2005) Uterotrophic effects of benzophenone derivatives and a p-hydroxybenzoate used in ultraviolet screens. Environ Res 98:40–45

    CAS  Google Scholar 

  • Krysko DV, Vanden Berghe Y, Parthoens E, D’Herde K, Vandenabeele P (2008) Methods for distinguishing apoptotic from necrotic cells and measuring their clearance. Methods Enzymol 442:307–341

    Google Scholar 

  • Kuba K, Ide H, Wallace SS, Kow YK (1992) A novel, sensitive and specific assay for abasic sites, the most commonly produced DNA lesion. Biochemistry–US 31:3703–3708

    Google Scholar 

  • Kunisue T, Chen Z, Buck Louis GM et al (2012) Urinary concentrations of benzopheone-type UV filters in U.S. women and their association with endometriosis. Environ Sci Technol 46:4624–4632

    CAS  Google Scholar 

  • Kunz PY, Fent K (2009) Estrogenic activity of ternary UV filter mixtures in fish (Pimephales promelas) and analysis with nonlinear isobolograms. Toxicol Appl Pharm 234:77–88

    CAS  Google Scholar 

  • Kunz PY, Galicia HF, Fent K (2006) Comparison of in vitro and in vivo estrogenic activity of UV filters in fish. Toxicol Sci 90:349–361

    CAS  Google Scholar 

  • Kvitt H, Rosenfeld H, Zandbank K, Tchernov D (2011) Regulation of apoptotic pathways by Stylophora pistillata to survive thermal stress and bleaching. PLoS ONE 6:e28665

    CAS  Google Scholar 

  • Laskowski R (1995) Some good reasons to ban the use of NOEC, LOEC, and related concepts in Ecotoxicology. Oikos 73:140–144

    Google Scholar 

  • Lichtenthaler HK (1987) Chlorophyll and carotenoids, the pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    CAS  Google Scholar 

  • Miller MW, Weil E, Szmant AM (2000) Coral recruitment and juvenile mortality as structuring factors for reef benthic communities in Biscayne National Park, USA. Coral Reefs 19:115–123

    Google Scholar 

  • Molina-Molina J-M, Escande A, Pillon A et al (2008) Profiling of benzopheone derivatives using fish and human estrogen receptor-specific in vitro bioassays. Toxicol Appl Pharm 232:384–395

    CAS  Google Scholar 

  • Morohoshi K, Yamamoto H, Kamata R, Shiraishi F, Koda T, Morita M (2005) Estrogenic activity of 37 components of commercial sunscreen lotions evaluated by in vitro assays. Toxicol In Vitro 19:457–469

    CAS  Google Scholar 

  • Nashez LG, Schuster D, Laggner C et al (2010) The UV-filter benzophenone-1 inhibits 17 beta-hydrozysteroid dehydrogenase type 3: virtual screening as a strategy to identify potential endocrine disrupting chemicals. Biochem Pharmacol 79:1189–1199

    Google Scholar 

  • Nesa B, Baird AH, Harii S, Yakovleva I, Hidaka M (2012) Algal symbionts increase DNA damage in coral planulae exposed to sunlight. Zool Stud 51:12–17

    CAS  Google Scholar 

  • Newman MC (2013) Quantitative ecotoxicology. CRC Press, Boca Raton

    Google Scholar 

  • NTP (National Toxicology Program) (2006) NTP technical report on the toxicology and carcinogenesis of benzophenone in F344/N rats and B6C3F1 mice. NIH Publication #06-4469

  • Omori M (2011) Degradation and restoration of coral reefs: experience in Okinawa, Japan. Mar Biol Res 7:3–12

    Google Scholar 

  • Paxton CW, Davy SK, Weis VM (2013) Stress and death of cnidarian host cells play a role in cnidarian bleaching. J Exp Biol 216:2813–2820

    Google Scholar 

  • Pitarch E, Portolés T, Marín JM et al (2010) Analytical strategy based on the use of liquid chromatography and gas chromatography with triple-quadrupole and time-of-flight MS analyzers for investigating organic contaminants in wastewater. Anal Bioanal Chem 397:2763–2776

    CAS  Google Scholar 

  • Platt KL, Aderhold S, Kulpe K, Fickler M (2008) Unexpected DNA damage caused by polycyclic aromatic hydrocarbons under standard laboratory conditions. Mut Res 650:96–103

    CAS  Google Scholar 

  • Popkin DJ, Prival MJ (1985) Effects of pH on weak and positive control mutagens in the AMES Salmonella plate assay. Mut Res 142:109–113

    CAS  Google Scholar 

  • Rees JG, Setiapermana D, Sharp VA, Weeks JM, Williams TM (1999) Evaluation of the impacts of land-based contaminants on the benthic faunas of Jakarta Bay, Indonesia. Oceano Acta 22:627–640

    Google Scholar 

  • Richardson SD (2006) Environmental mass spectrometry: emerging contaminants and current issues. Anal Chem 78:4021–4046

    CAS  Google Scholar 

  • Richardson SD (2007) Water analysis: emerging contaminants and current issues. Anal Chem 79:4295–4324

    CAS  Google Scholar 

  • Richmond R (1993) Coral reefs: present problems and future concerns resulting from anthropogenic disturbance. Amer Zool 33:524–536

    Google Scholar 

  • Richmond R (1997) Reproduction and recruitment in corals: critical links in the persistence of reefs. Life and death of coral reefs. Chapman and Hall, New York, pp 175–197

    Google Scholar 

  • Rodil R, Quintana JB, Concha-Grana E, Lopex-Mahia P, Muniatequi-Lorenzo S, Prada-Rodriguez D (2012) Emerging pollutants in sewage, surface and drinking water in Galicia (NW Spain). Chemosphere 86:1040–1049

    CAS  Google Scholar 

  • Samara P, Syntichaki N, Tavernarakis N (2008) Autophagy is required for necrotic cell death in Caenorhabditis elegans. Cell Death Differ 15:105–112

    CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Long Island

    Google Scholar 

  • Schlecht C, Klammer H, Wolfgang W, Jarry H (2006) A dose-response study on the estrogenic activity of benzophenone-2 on various endpoints in the serum, pituitary and uterus of female rats. Arch Toxicol 80:656–661

    CAS  Google Scholar 

  • Schlumpf M, Cotton B, Conscience M, Haller V, Steinmann B, Lichtensteiger W (2001) In vitro and in vivo estrogenicity of UV screens. Environ Health Persp 109:239–244

    CAS  Google Scholar 

  • Schlumpf M, Schmid P, Durrer S et al (2004) Endocrine activity and developmental toxicity of cosmetic UV filters—an update. Toxicology 205:113–122

    CAS  Google Scholar 

  • Schlumpf M, Durrer S, Fass O et al (2008) Developmental toxicity of UV filters and environmental exposure: a review. Int J Androl 31:144–151

    CAS  Google Scholar 

  • Schmutzler C, Bacinski A, Gotthardt I et al (2007) The ultraviolet filter benzophenone 2 interferes with the thyroid hormone axis in rats and is a potent in vitro inhibitor of human recombinant thyroid peroxidase. Endocrinology 148:2835–2844

    CAS  Google Scholar 

  • Scholze M, Boedeker W, Faust M, Backhaus T, Altenburger R, Grimme LH (2001) A general best-fit method for concentration-response curves and the estimation of low-effect concentrations. Environ Toxicol Chem 20:448–457

    CAS  Google Scholar 

  • Seidlova-Wuttke D, Jarry H, Wuttke W (2004) Pure estrogenic effect of benzophenone-2 (BP2) but not of bisphenol A (BPA) and dibutylphtalate (DBP) in uterus, vagina and bone. Toxicology 205:103–112

    CAS  Google Scholar 

  • Seidlova-Wuttke D, Jarry H, Christoffel J, Rimoldi G, Wuttke W (2005) Effects of bisphenol-A, dibutylphtalate, benzophenone-2, procymidone, and linurone on fat tissue, a variety of hormones and metabolic parameters: a 3 months comparison with effect of estradiol in ovariectomized rats. Toxicology 213:13–24

    CAS  Google Scholar 

  • Shaath NA, Shaath M (2005) Recent sunscreen market trends. In: Shaath NA (ed) Sunscreens, regulations and commercial development, 3rd edn. Taylor & Francis, Boca Raton, pp 929–940

    Google Scholar 

  • Smith TB, Nemeth RS, Blondeau J, Calnan JM, Kadison E, Herzlieb S (2008) Assessing coral reef health across onshore to offshore stress gradients in the US Virgin Islands. Mar Pollut Bull 56:1983–1991

    CAS  Google Scholar 

  • Song M, Kim Y-J, Park Y-K, Ryu J-C (2012) Changes in thyroid peroxidase activity in response to various chemicals. J Environ Monitor 14:2121–2127

    CAS  Google Scholar 

  • Spangenberg DB (1971) Thyroxine induced metamorphosis in Aurelia. J Exp Zoo 178:183–194

    CAS  Google Scholar 

  • Sung J-S, Demple B (2006) Roles of base excision repair subpathways in correcting oxidized abasic sites in DNA. FEBS J 273:1620–1629

    CAS  Google Scholar 

  • Suter GW II (1993) Ecological risk assessment. CRC Press, Boca Raton

    Google Scholar 

  • Suter, II GW, Mabrey JB (1994) Toxicological benchmarks for screening potential contaminants of concern for effects on aquatic biota: 1994 Revision. Oak Ridge National Laboratory, Oak Ridge, TN. ES/ER/TM-96/R1

  • Suter GW II, Rosen AE, Linder E, Parkhurst DF (1987) End points for responses of fish to chronic toxic exposures. Environ Toxicol Chem 6:793–809

    CAS  Google Scholar 

  • Suzuki T, Kitamura S, Khota R, Sugihara K, Fujimoto N, Ohta S (2005) Toxicol Appl Pharm 203:9–17

    CAS  Google Scholar 

  • Taatjes DJ, Sobel BE, Budd RC (2008) Morphological and cytochemical determination of cell death by apoptosis. Histochem Cell Biol 129:33–43

    CAS  Google Scholar 

  • Tasdemir Em Galluzzi L, Majuri MN et al (2008) Methods for assessing autophagy and autophagic cell death. Methods Mol Biol 445:29–76

    Google Scholar 

  • Thienpont B, Tingaud-Sequeira A, Prats E, Barata C, Babin P, Raldua D (2011) Zebrafish eleutheroembryos provide a suitable vertebrate model for screening chemicals that impair thyroid hormone synthesis. Environ Sci Technol 45:7525–7532

    CAS  Google Scholar 

  • Tsujimoto Y, Shimizu S (2005) Another way to die: autophagic programmed cell death. Cell Death Differ 15:1528–1534

    Google Scholar 

  • Weisbrod CJ, Kunz PY, Zenker AK, Fent K (2007) Effects of the UV filter benzophenone-2 on reproduction in fish. Toxicol Appl Pharm 225:255–266

    CAS  Google Scholar 

  • Wennig R (2000) Threshold values in toxicology—useful or not? Forensic Sci Int 113:323–330

    CAS  Google Scholar 

  • West JM, Salm RV (2003) Resistance and resilience to coral bleaching: implications for coral reef conservation and management. Conserv Biol 17:956–967

    Google Scholar 

  • White MK, Cinti C (2004) A morphologic approach to detect apoptosis based on electron microscopy. Methods Mol Biol 285:105–111

    Google Scholar 

  • Williams DE, Miller MW, Kramer KL (2008) Recruitment failure in Florida Keys Acropora palmata, a threatened Caribbean coral. Coral Reefs 27:697–705

    Google Scholar 

  • Wilson DM, Barsky D (2001) The major human basic endonuclease: formation, consequences and repair of abasic lesions in DNA. Mut Res 485:283–307

    CAS  Google Scholar 

  • Yamasaki K, Takeyoski M, Yakabe Y, Sawaki M, Takatsuki M (2003) Comparison of the reporter gene assay for ER-alpha antagonists with the immature rat uterotrophic assay of 10 chemicals. Toxicol Lett 142:119–131

    CAS  Google Scholar 

  • Ye L, Su Z-J, Ge R-S (2011) Inhibitors of testosterone biosynthetic and metabolic activation enzymes. Molecules 16:9983–10001

    CAS  Google Scholar 

  • Yla-Antilla P, Vihinen H, Jokitalo E, Eskelinin EL (2009) Monitoring autophagy by electron microscopy in mammalian cells. Methods Enzymol 452:143–164

    Google Scholar 

  • Yu H (2002) Environmental carcinogenic polycyclic aromatic hydrocarbons: photochemistry and phototoxicity. J Environ Sci Heal, Part C 20:149–183

    Google Scholar 

  • Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice Hall, Upper Saddle River

    Google Scholar 

  • Zeiger E, Anderson B, Haworth S, Lawlow T, Mortlemans K, Speck W (1987) Salmonella mutagenicity tests: 3. Results from the testing of 255 chemicals. Environ Mutagen 9:1–110

    CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Fuad Al-horani for his assistance, Ms. Maya Vizel for her assistance with the planula exposure challenges, Dr. Gideon Winters for assistance with Molecular Dynamics microplate fluorimeter, and the anonymous reviewers who greatly improved the quality of this manuscript. We also sincerely thank Dr. Sylvia Galloway and James H. Nicholson for their work on formatting the figures for publication.

Conflict of interest

The authors can identify no potential conflicts of interest, neither financial or ethically, involved in the writing or publication of this manuscript.

Disclaimer

The intent of this article is purely for dissemination of scientific knowledge, and is neither endorsement nor condemnation of the activities of any government, corporation, their employees or subsidiaries, nor to imply liability on their part. This publication does not constitute an endorsement of any commercial product or intend to be an opinion beyond scientific or other results obtained by the U.S. National Oceanic and Atmospheric Administration (NOAA). No reference shall be made to U.S. NOAA, or this publication furnished by U.S. NOAA, to any advertising or sales promotion which, would indicate or imply that U.S. NOAA recommends or endorses any proprietary product mentioned herein, or which has as its purpose an interest to cause the advertised product to be used or purchased because of this publication.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C. A. Downs.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10646_2013_1161_MOESM1_ESM.tif

Proportion of planula alive as a function of benzophenone-2 concentration. Symbol size is proportional to the number of replicates having a given value. Regression line (solid) and 95 % confidence intervals (dashed lines) are shown for each statistically significant fit. a Stylophora pistillata exposed to benzophenone-2 for 8 h in the light. b S. pistillata exposed to benzophenone-2 for 8 h in the dark. c S. pistillata exposed to benzophenone-2 for planulae exposed for 8 h in the light, then 16 h of darkness. d S. pistillata exposed to benzophenone-2 for 24 h in the dark

10646_2013_1161_MOESM2_ESM.tif

Proportion of non-deformed planulae as a function of benzophenone-2 concentration. Symbol size is proportional to the number of replicates having a given value. Regression line (solid) and 95 % confidence intervals (dashed lines) are shown for each statistically significant fit. a Stylophora pistillata exposed to benzophenone-2 for 8 h in the light. b S. pistillata exposed to benzophenone-2 for 8 h in the dark. c S. pistillata exposed to benzophenone-2 for planulae exposed for 8 h in the light, then 16 h of darkness. d S. pistillata exposed to benzophenone-2 for 24 h in the dark

10646_2013_1161_MOESM3_ESM.tif

PROBIT analyses of dose–response curves of cells of Stylophora pistillata exposed to benzophenone-2. PROBITs fit using a Gompertz–Weibull exponential distribution were used to calculate LC50s. a S. pistillata exposed to benzophenone-2 for 8 h in the light. b S. pistillata exposed to benzophenone-2 for 8 h in the dark

10646_2013_1161_MOESM4_ESM.tif

PROBIT analyses of dose–response curves of number of deformed planulae of Stylophora pistillata exposed to benzophenone-2. PROBITs fit using a Gompertz-Weibull exponential distribution were used to calculate EC50s. a S. pistillata exposed to benzophenone-2 for 8 h in the light. b S. pistillata exposed to benzophenone-2 for planulae exposed for 8 h in the light, then 16 h of darkness. c S. pistillata exposed to benzophenone-2 for 8 h in the dark. d S. pistillata exposed to benzophenone-2 for 24 h in the dark

10646_2013_1161_MOESM5_ESM.tif

PROBIT analyses of dose-lethality curves of planulae of Stylophora pistillata exposed to benzophenone-2. PROBITs fit using a Gompertz–Weibull exponential distribution were used to calculate LC50s. a S. pistillata exposed to benzophenone-2 for 8 h in the light. b S. pistillata exposed to benzophenone-2 for 24 h in the light. c S. pistillata exposed to benzophenone-2 for 8 h in the dark

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Downs, C.A., Kramarsky-Winter, E., Fauth, J.E. et al. Toxicological effects of the sunscreen UV filter, benzophenone-2, on planulae and in vitro cells of the coral, Stylophora pistillata . Ecotoxicology 23, 175–191 (2014). https://doi.org/10.1007/s10646-013-1161-y

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-013-1161-y

Keywords

  • Coral
  • Benzophenone-2
  • Cell toxicity
  • Coral planula
  • Sunscreen UV filters