Skip to main content

Advertisement

Log in

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

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

Benzophenone-3 (BP-3; oxybenzone) is an ingredient in sunscreen lotions and personal-care products that protects against the damaging effects of ultraviolet light. Oxybenzone is an emerging contaminant of concern in marine environments—produced by swimmers and municipal, residential, and boat/ship wastewater discharges. We examined the effects of oxybenzone on the larval form (planula) of the coral Stylophora pistillata, as well as its toxicity in vitro to coral cells from this and six other coral species. Oxybenzone is a photo-toxicant; adverse effects are exacerbated in the light. Whether in darkness or light, oxybenzone transformed planulae from a motile state to a deformed, sessile condition. Planulae exhibited an increasing rate of coral bleaching in response to increasing concentrations of oxybenzone. Oxybenzone is a genotoxicant to corals, exhibiting a positive relationship between DNA-AP lesions and increasing oxybenzone concentrations. Oxybenzone is a skeletal endocrine disruptor; it induced ossification of the planula, encasing the entire planula in its own skeleton. The LC50 of planulae exposed to oxybenzone in the light for an 8- and 24-h exposure was 3.1 mg/L and 139 µg/L, respectively. The LC50s for oxybenzone in darkness for the same time points were 16.8 mg/L and 779 µg/L. Deformity EC20 levels (24 h) of planulae exposed to oxybenzone were 6.5 µg/L in the light and 10 µg/L in darkness. Coral cell LC50s (4 h, in the light) for 7 different coral species ranges from 8 to 340 µg/L, whereas LC20s (4 h, in the light) for the same species ranges from 0.062 to 8 µg/L. Coral reef contamination of oxybenzone in the U.S. Virgin Islands ranged from 75 µg/L to 1.4 mg/L, whereas Hawaiian sites were contaminated between 0.8 and 19.2 µg/L. Oxybenzone poses a hazard to coral reef conservation and threatens the resiliency of coral reefs to climate change.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

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

    Article  CAS  Google Scholar 

  • Agas D, Sabbieti MG, Marchetti L (2013) Endocrine disruptors and bone metabolism. Arch Toxicol 87:735–751

    Article  CAS  Google Scholar 

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

    Book  Google Scholar 

  • Alcolado-Prieto P, Aragon HC, Alcolado PM, Castillo AL (2012) Stony coral recruitment in coral reefs at different distances from pollution sources in Habana, Cuba. Rev Biol Trop 60:981–994

    Google Scholar 

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

    Article  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

    Article  CAS  Google Scholar 

  • Baird AH, Guest JR, Willis BL (2009) Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annu Rev Ecol Evol Syst 40:551–571

    Article  Google Scholar 

  • Barnes DJ (1972) The structure and formation of growth-ridges in scleractinian coral skeletons. Proc R Soc Lond B 182:331–350

    Article  Google Scholar 

  • Baron E, Gago-Ferrero P, Gorga M et al (2013) Occurrence of hydrophobic organic pollutants (BFRs and UV-filters) in sediments from South America. Chemosphere 92:309–316

    Article  CAS  Google Scholar 

  • Birnbaum LS (1995) Developmental effects of dioxins. Environ Health Perspect 103:89–94

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Bluthgen N, Zucchi S, Fent K (2012) Effects of the UV filter benzophenone-3 (oxybenzone) at low concentrations in zebrafish (Danio rerio). Toxicol Appl Pharmacol 263:184–194

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Brown BE (2000) The significance of pollution in eliciting the `bleaching’ response in symbiotic cnidarians. Int J Environ Pollut 13:392–415

    Article  CAS  Google Scholar 

  • Carpenter KE, Abrar M, Aeby G et al (2008) One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321:560–563

    Article  CAS  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 

  • Colborn T, vom Saal FS, Soto AM (1993) Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ Health Perspect 101:378–384

    Article  CAS  Google Scholar 

  • Conolly RB, Lutz WK (2004) Nonmonotonic dose-response relationships: mechanistic basis, kinetic modeling, and implications for risk assessment. Toxicol Sci 77:151–157

    Article  CAS  Google Scholar 

  • Coronado M, De Haro H, Deng X et al (2008) Estrogenic activity and reproductive effects of the UV-filter oxybenzone (2-hydroxy-4-methoxyphenyl-methanone) in fish. Aquat Toxicol 90:182–187

    Article  CAS  Google Scholar 

  • Cosnefroy A, Brion F, Maillot-Marechal E et al (2011) 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

    Article  CAS  Google Scholar 

  • Crang RFE, Klomparens KL (1988) Artifacts in biological electron microscopy. Plenum Press, New York

    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

    Article  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 

  • Depledge MH, Billinghurst Z (1999) Ecological significance of endocrine disruption in marine invertebrates. Mar Pollut Bull 39:32–38

    Article  CAS  Google Scholar 

  • Doherty TM, Fitzpatrick LA, Inoue D et al (2004) Molecular, endocrine, and genetic mechanisms of arterial calcification. Endocr Rev 25:629–672

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Downs CA, Fauth JF, 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

    Article  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, U.S. Virgin Islands. Ecotoxicology 20:1914–1931

    Article  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

    Article  CAS  Google Scholar 

  • Downs CA, McDougall KE, Woodley CM et al (2013) Heat stress and light stress induce different cellular pathologies in the symbiotic dinoflagellate during coral bleaching. PLoS One 8(12):e77173. doi:10.137/journal.pone.0077173

    Article  CAS  Google Scholar 

  • Downs CA, Kramarsky-Winter E, Fauth JE et al (2014) Toxicological effects of the sunscreen UV filter, benzophenone-2, on planula and in vitro cells of the coral, Stylophora pistillata. Ecotoxicology 23:175–191

    Article  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

    Article  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

    Article  Google Scholar 

  • 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

    Article  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

    Article  CAS  Google Scholar 

  • Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar Pollut Bull 50:125–146

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Fent K, Kunz PY, Zenker A, Rapp M (2010) 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 69:S4–S6

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Finnila MA, Zioupos P, Herlin M, Miettinen HM, Simanainen U, Hakansson H, Tuukkanen J, Viluksela M, Jamsa T (2010) Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure on bone material properties. J Biomech 43:1097–1103

    Article  Google Scholar 

  • Fisher EM, Fauth JE, Hallock-Muller P, Woodley CM (2007) Lesion regeneration rates in reef-building corals Monstrastrea Spp. as indicators of colony condition. Mar Ecol Prog Ser 339:61–71

    Article  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

    Article  CAS  Google Scholar 

  • French JE (1992) NTP technical report on the toxicity studies of 2-hydroxy-4-methoxybenzophenone (CAS No. 131-57-7) administered topically and in dosed feed to F344/N Rats and B6C3F1 mice. Toxic Rep Ser 21:1–14

    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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Gao L, Yuan T, Zhou C, Cheng P, Bai Q et al (2013) Effects of four commonly used UV filters on the growth, cell viability and oxidative stress responses of the Tetrahymena thermophila. Chemosphere 93:2507–2513

    Article  CAS  Google Scholar 

  • Gates RD, Edmunds PJ (1999) The physiological mechanisms of acclimatization in tropical reef corals. Am Zool 39:30–43

    Article  Google Scholar 

  • Gilbert E, Pirot F, Bertholle V, Roussel L, Falson F, Padois K (2012) Commonly used UV filter toxicity on biological functions: review of last decade studies. Int J Cosmet Sci 35:208–219

    Article  CAS  Google Scholar 

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

    Article  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

    Article  Google Scholar 

  • Golub MS, Hogrefe CE, Germann SL, Jerome CP (2004) Endocrine disruption in adolescence: immunologic, hematologic, and bone effects in monkeys. Toxicol Sci 82:598–607

    Article  CAS  Google Scholar 

  • Goreau TJ (1990) Coral bleaching in Jamaica. Nature 343:417

    Article  Google Scholar 

  • Gulati D, Mounce R (1997) NTP reproductive assessment by continuous breeding study for 2-hydroxy-4-methoxybenzophenone in Swiss CD-1 mice. NTIS# PB91158477. Environ Health Perspect 105(Suppl 1):313–314

    Google Scholar 

  • Gura T (2008) Toxicity testing moves from the legislature to the Petri dish—and back. Cell 134:557–559

    Article  CAS  Google Scholar 

  • Hagiwara H, Sugizaki T, Tsukamoto Y, Senoh E, Goto T, Ishihara Y (2008a) Effects of alkylphenols on bone metabolism in vivo and in vitro. Toxicol Lett 181:13–18

    Article  CAS  Google Scholar 

  • Hagiwara H, Suizaki T, Tsukamoto Y (2008b) Effects of alkylphenols on bone metabolism in vivo and in vitro. Toxicol Lett 181:13–18

    Article  CAS  Google Scholar 

  • Hanson KM, Gratton E, Bardeen CJ (2006) Sunscreen enhancement of UV-induced reactive oxygen species in the skin. Free Radic Biol Med 41:1205–1212

    Article  CAS  Google Scholar 

  • Hany J, Nagel R (1995) Detection of sunscreen agents in human breast milk. Dtsch Lebensm Rundsch 91:341–345

    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 346:89–96

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Jamsa T, Viluksela M, Tuomisto JT, Tuomisto J, Tuukkanen J (2001) Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on bone in two rat strains with different aryl hydrocarbon receptor structures. J Bone Miner Res 16:1812–1820

    Article  CAS  Google Scholar 

  • Jeon HK, Chung Y, Ryu JC (2006) Simultaneous determination of benzophenone-type UV filters in water and soil by gas chromatography-mass spectrometry. J Chromatogr A 1131:192–202

    Article  CAS  Google Scholar 

  • Jimenez CE, Cortes J (2003) Coral cover change associated to El Nino, Eastern Pacific, Costa Rica, 1992–2001, PSZNI. Mar Ecol 24:179–192

    Article  Google Scholar 

  • Johnston EL, Roberts DA (2009) Contaminants reduce the richness and evenness of marine communities: a review and meta-analysis. Environ Pollut 157:1745–1752

    Article  CAS  Google Scholar 

  • Kameda Y, Kimura K, Miyazaki M (2011) Occurrence and profiles of organic sun-blocking agents in surface waters and sediments in Japanese rivers and lakes. Environ Pollut 159:1570–1576

    Article  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

    Article  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

    Article  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

    Article  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

    Article  CAS  Google Scholar 

  • Krysko DV, Berghe TV, D’Herde K, Vandenabeele P (2008) Apoptosis and necrosis: detection, discrimination and phagocytosis. Methods 44:205–221

    Article  CAS  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

    Article  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

    Article  CAS  Google Scholar 

  • Kushmaro A, Henning G, Hofmann DK, Benayahu Y (1997) Metamorphosis of Heteroxenia fuscescens planulae (Cnidaria: Octocorallia) is inhibited by crude oil: a novel short-term toxicity bioassay. Mar Environ Res 43:295–302

    Article  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

    Article  Google Scholar 

  • Lind PM, Milnes MR, Lundberg R et al (2004) Abnormal bone composition in female juvenile American alligators from a pesticide-polluted lake. Environ Health Perspect 112:359–362

    Article  CAS  Google Scholar 

  • Lindberg MK, Erlandsson M, Alatalo SL et al (2001) Estrogen receptor alpha, but not estrogen receptor beta, is involved in the regulation of the OPG/RANKL (osteoprotegerin/receptor activator of NF-kappa B ligand) ratio and serum interleukin-6 in male mice. J Endocrinol 171:425–433

    Article  CAS  Google Scholar 

  • Lirman D, Orlando B, Macia S, Manzello D, Kaufman L et al (2003) Coral communities of Biscayne Bay, Florida and adjacent offshore areas: diversity abundance, distribution, and environmental correlates. Aquat Conserv 13:121–135

    Article  Google Scholar 

  • Loya Y (1975) Possible effects of water pollution on the community structure of Red Sea corals. Mar Biol 29:177–185

    Article  Google Scholar 

  • Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H et al (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131

    Article  Google Scholar 

  • Maloney KO, Munguia P, Mitchell RM (2011) Anthropogenic disturbance and landscape patterns affect diversity patterns of aquatic benthic macroinvertebrates. J N Am Benthol Soc 30:284–295

    Article  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

    Article  Google Scholar 

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

    Article  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

    Article  CAS  Google Scholar 

  • Nakajima D, Asada S, Kageyama et al (2006) Activity related to the carcinogenicity of plastic additives in the benzophenone group. J UOEH 28:143–156

    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

    Article  CAS  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 

  • Nimrod AC, Benson WH (1998) Reproduction and development of Japanese medaka following an early life stage exposure to xenoestrogens. Aquat Toxicol 44:141–156

    Article  CAS  Google Scholar 

  • NRC (National Research Council) (2013) Assessing risks to endangered and threatened species from pesticides. National Academy of Sciences. ISBN 978-0-309-28583-4

  • 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

  • OECD (2006) Current approaches in the statistical analysis of ecotoxicity data: a guidance to application. OECD Environment Health & Safety Publications Series on Testing and Assessment. No. 54. Organization for Economic Cooperation and Development, Paris

  • OECD (2013) OECD Guidelines for the testing of chemicals: fish embryo acute toxicity test. Organization for Economic Cooperation and Development, Paris

    Google Scholar 

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

    Article  Google Scholar 

  • Ozáez I, Martinez-Guitarte JL, Morcillo G (2013) Effects of in vivo exposure to UV filters (4-MBC, OMC, BP-3, 4-HB, OC, OD-PABA) on endocrine signaling genes in the insect Chironomus riparius. Sci Total Environ 456–457:120–126

    Article  CAS  Google Scholar 

  • Peters EC (1984) A survey of cellular reactions to environmental stress and disease in Caribbean scleractinian corals. Helgol Meeresunters 37:113–137

    Article  Google Scholar 

  • Pfeiffer CA, Kirschbaum A, Gardner WU (1940) Relation of estrogen to ossification and the levels of serum calcium and lipoid in the English Sparrow, Passer domesticus. Yale J Biol Med 13:279–284

    CAS  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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Posthuma L, Suter GW II, Traas TP (2002) Species sensitivity distributions in ecotoxicology. Lewis Publishers, Boca Raton, p 587 pp

    Google Scholar 

  • Rachon D, Rimoldi G, Wuttke G (2006) In vitro effects of benzophenone-3 and octyl-methoxycinnamate on the production of interferon-γ and interleukin-10 by murine splenocytes. Immunopharmacol Immunotoxicol 28:501–510

    Article  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. Oceanol Acta 22:627–640

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  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

    Chapter  Google Scholar 

  • Rickard DJ, Subramaniam M, Spelsberg TC (1999) Molecular and cellular mechanism of estrogen action on the skeleton. J Cell Biochem 75:123–132

    Article  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

    Article  CAS  Google Scholar 

  • Rogers CS, Miller J (2006) Permanent ‘phase shifts’ or reversible declines in coral cover? Lack of recovery of two coral reefs in St. John, US Virgin Islands. Mar Ecol Prog Ser 306:103–114

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Schlecht C, Klammer H, Wuttke W (2004) Effects of estradiol, benzophenone-2 and benzophenone-3 on the expression pattern of the estrogen receptors (ER) alpha and beta, the estrogen receptor-related receptor 1 (ERR1) and the aryl hydrocarbon receptor (Ahr) in adult ovariectomized rats. Toxicology 205:123–130

    Article  CAS  Google Scholar 

  • Schlenk D, Sapozhnikova Y, Irwin MA et al (2005) In vivo bioassay-guided fractionation of marine sediment extracts from the southern California bight, USA, for estrogenic activity. Environ Toxicol Chem 24:2820–2826

    Article  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

    Article  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

    Article  CAS  Google Scholar 

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

    Article  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 

  • Shlesinger Y, Loya Y (1985) Coral community reproductive patterns: red sea versus the great barrier reef. Science 228:1333–1335

    Article  CAS  Google Scholar 

  • Simmons DJ (1966) Collagen formation and endochondral ossification in estrogen treated mice. Proc Soc Exp Biol Med 121:1165–1168

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Steel RGD (1959) A multiple comparison rank sum test: treatments versus control. Biometrics 15:560–572

    Article  Google Scholar 

  • Suter GW II (2007) Ecological risk assessment. CRC Press, Boca Raton

    Google Scholar 

  • Suzuki T, Kitamura S, Khota R, Sugihara K, Fujimoto N, Ohta S (2005) Estrogenic and anti-androgenic activities of 17 benzophenone derivatives used as UV stabilizers and sunscreens. Toxicol Appl Pharmacol 203:9–17

    Article  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

    Article  CAS  Google Scholar 

  • Takemoto K, Yamazaki H, Nakajima M, Yokoi T (2002) Genotoxic activation of benzophenone and its two metabolites by human cytochrome P450s in SOS/umu assay. Mutat Res 519:199–204

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Tashiro Y, Kameda Y (2013) Concentration of organic sun-blocking agents in seawater of beaches and coral reefs of Okinawa Island, Japan. Mar Pollut Bull 77:333–340

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Tsukamoto Y, Ishihara Y, Miyagawa-Tomita S, Hagiwara H (2004) Inhibition of ossification in vivo and differentiation of osteoblasts in vitro by tributyltin. Biochem Pharmacol 68:739–746

    Article  CAS  Google Scholar 

  • UNWTO (United Nations World Tourism Organization) website (2007) http://www.unwto.org/index.php. Accessed 30 Jun 2007

  • US EPA (2012) Sunscreen use. http://www.epa.gov/ged/coralreef/models/SunscreenUse.html. Accessed 28 July 2014

  • U.S. National Park Service (2012) http://www.nps.gov/ever/planyourvisit/upload/NPS-Site-Bulletin_Sunscreen_FY12.pdf

  • Väänänen HK, Härkönen PL (1996) Estrogen and bone metabolism. Maturitas 23:S65–S69

    Article  Google Scholar 

  • van Woesik R, Franklin EC, O’Leary J, McClanahan TR, Klaus JS et al (2012) Hosts of the Plio-Pleistocene past reflect modern-day coral vulnerability. Proc R Soc Lond B Biol Sci 279:2448–2456

    Article  Google Scholar 

  • Vione D, Caringella R, De Laurentiis E, Pazzi M, Minero C (2013) Phtotransformation of the sunlight filter benzophenone-3 (2-hydroxy-4-methoxybenzophenone) under conditions relevant to surface waters. Sci Total Environ 463–464:243–251

    Article  CAS  Google Scholar 

  • Vom Saal F, Nagel S, Palanza P et al (1995) Estrogenic pesticides: binding relative to estradiol in MCF-7 cells and effects of exposure during fetal life on subsequent territorial behavior in male mice. Toxicol Lett 77:343–350

    Article  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

    Article  Google Scholar 

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

    Google Scholar 

  • Wilkinson C (2008) Status of coral reefs of the world. Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre, Townsville

    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

    Article  Google Scholar 

  • Xcaret Ecopark (2007) Home page. http://www.xcaret.com/services/faqs.php. Accessed 2 Dec 2013

  • Xel-há Ecopark (2007) Home page. http://www.xelha.com. Accessed 2 Dec 2013

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice Hall, New Jersey

    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

    Article  CAS  Google Scholar 

  • Zhao H, Wei D, Li M, Du Y (2013) Substituent contribution to the genotoxicity of benzophenone-type UV filters. Ecotoxicol Environ Saf 95:241–246

    Article  CAS  Google Scholar 

  • Ziolkowaska A, Rucinski M, Pucker A et al (2006) Expression of osteoblast marker genes in rat calvarial osteoblast-like cells, and effects of the endocrine disruptors diphenylolpropane, benzophenone-3, resveratrol and silymarin. Chem-Biol Interact 164:147–156

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The study in Israel was partially funded by the Israel Science Foundation (ISF) No. 1169/07 to Yossi Loya. No other organization or government provided Grant-in-aid funding for this project. The authors thank Dr. Jon Martinez and Dr. Katherine Schaefer for assistance with water sampling in Oahu, Hawai’i, Ms. Maya Vizel for her assistance with the planula exposure challenges, Dr. Gideon Winters for assistance with Molecular Dynamics microplate fluorimeter, and Dr. Fuad Al-Horani for his assistance with toxicological exposures. We sincerely thank Dr. Sylvia Galloway and Mr. James H. Nicholson for their work on formatting the figures for publication. We also wish to thank the U.S. National Park Service of the U.S. Virgin Islands National Park for their assistance. We wish to thank the two anonymous reviewers for their comments in improving the manuscript. C.A. Downs thanks the unidentified Virgin Islander in Cruz Bay who gave him insight into the hypothetical cause of the ecological collapse occurring at Trunk Bay; hypothesizing that the visible “sheen” on the surface of the water produced from swimmers’ sunscreen lotions was somehow impacting coral reef health.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C. A. Downs.

Ethics declarations

Conflict of Interest

The authors can identify no potential conflicts of interest, neither financial nor 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 an 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.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Downs, C.A., Kramarsky-Winter, E., Segal, R. 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 70, 265–288 (2016). https://doi.org/10.1007/s00244-015-0227-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-015-0227-7

Keywords

Navigation