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

  • C. A. Downs
  • Esti Kramarsky-Winter
  • Roee Segal
  • John Fauth
  • Sean Knutson
  • Omri Bronstein
  • Frederic R. Ciner
  • Rina Jeger
  • Yona Lichtenfeld
  • Cheryl M. Woodley
  • Paul Pennington
  • Kelli Cadenas
  • Ariel Kushmaro
  • Yossi Loya
Article

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.

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References

  1. 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 50:576–582CrossRefGoogle Scholar
  2. Agas D, Sabbieti MG, Marchetti L (2013) Endocrine disruptors and bone metabolism. Arch Toxicol 87:735–751CrossRefGoogle Scholar
  3. Agresti A (2002) Categorical data analysis, 2nd edn. Wiley, New YorkCrossRefGoogle Scholar
  4. 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 60:981–994Google Scholar
  5. Anderson SL, Wild GC (1994) Linking genotoxic responses and reproductive success in ecotoxicology. Environ Health Perspect 102:9–12CrossRefGoogle Scholar
  6. 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 20:3496–3515CrossRefGoogle Scholar
  7. Baird AH, Guest JR, Willis BL (2009) Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annu Rev Ecol Evol Syst 40:551–571CrossRefGoogle Scholar
  8. Barnes DJ (1972) The structure and formation of growth-ridges in scleractinian coral skeletons. Proc R Soc Lond B 182:331–350CrossRefGoogle Scholar
  9. 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 92:309–316CrossRefGoogle Scholar
  10. Birnbaum LS (1995) Developmental effects of dioxins. Environ Health Perspect 103:89–94CrossRefGoogle Scholar
  11. Blaauboer BJ (2008) The contribution of in vitro toxicity data in hazard and risk assessment: current limitations and future perspectives. Toxicol Lett 180:81–84CrossRefGoogle Scholar
  12. 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
  13. 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 263:184–194CrossRefGoogle Scholar
  14. Brooks AC, Gaskell PN, Maltby LL (2009) Importance of prey and predator feeding behaviors for trophic transfer and secondary poisoning. Environ Sci Technol 43:7916–7923CrossRefGoogle Scholar
  15. Brown BE (2000) The significance of pollution in eliciting the `bleaching’ response in symbiotic cnidarians. Int J Environ Pollut 13:392–415CrossRefGoogle Scholar
  16. 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 321:560–563CrossRefGoogle Scholar
  17. Carson FL (1997) Histotechnology: a self-instructional text, 2nd edn. American Society of Clinical Pathologists, ChicagoGoogle Scholar
  18. CIR (Cosmetic Ingredient Review) (2005) Annual review of cosmetic ingredient safety assessments: 2003/2003. Int J Toxicol 24:1–102Google Scholar
  19. Colborn T, vom Saal FS, Soto AM (1993) Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ Health Perspect 101:378–384CrossRefGoogle Scholar
  20. Conolly RB, Lutz WK (2004) Nonmonotonic dose-response relationships: mechanistic basis, kinetic modeling, and implications for risk assessment. Toxicol Sci 77:151–157CrossRefGoogle Scholar
  21. 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 90:182–187CrossRefGoogle Scholar
  22. 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 125:439–449CrossRefGoogle Scholar
  23. Crang RFE, Klomparens KL (1988) Artifacts in biological electron microscopy. Plenum Press, New YorkGoogle Scholar
  24. Crawley MJ (1993) GLIM for ecologists. Blackwell, LondonGoogle Scholar
  25. Cuquerella MC, Lhiaubet-Vallet V, Cadet J, Miranda MA (2012) Benzophenone photosensitized DNA damage. Acc Chem Res 45:1558–1570CrossRefGoogle Scholar
  26. Danovaro R, Bongiorni L, Corinaldesi C et al (2008) Sunscreens cause coral bleaching by promoting viral infections. Environ Health Persp 116:441–447Google Scholar
  27. Depledge MH, Billinghurst Z (1999) Ecological significance of endocrine disruption in marine invertebrates. Mar Pollut Bull 39:32–38CrossRefGoogle Scholar
  28. Doherty TM, Fitzpatrick LA, Inoue D et al (2004) Molecular, endocrine, and genetic mechanisms of arterial calcification. Endocr Rev 25:629–672CrossRefGoogle Scholar
  29. Downs CA, Fauth JE, Halas JC, Dustan P, Bemiss J, Woodley CM (2002) Oxidative stress and seasonal coral bleaching. Free Radic Biol Med 32:533–543CrossRefGoogle Scholar
  30. Downs CA, Kramarsky-Winter E, Martinez J et al (2009) Symbiophagy as a mechanism for coral bleaching. Autophagy 5:211–216CrossRefGoogle Scholar
  31. 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 19:171–184CrossRefGoogle Scholar
  32. 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 20:1914–1931CrossRefGoogle Scholar
  33. Downs CA, Ostrander GK, Rougee L et al (2012) The use of cellular diagnostics for identifying sub-lethal stress in reef corals. Ecotoxicology 21:768–782CrossRefGoogle Scholar
  34. 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 CrossRefGoogle Scholar
  35. 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 23:175–191CrossRefGoogle Scholar
  36. Drablos F, Feyzi E, Aas PA et al (2004) Alkylation damage in DNA and RNA: repair mechanisms and medical significance. DNA Repair 3:1389–1407CrossRefGoogle Scholar
  37. Draper NR, Smith H (1966) Applied regression analysis. Wiley, New YorkGoogle Scholar
  38. Dustan P (1977) Vitality of reef coral populations off Key Largo, Florida: recruitment and mortality. Environ Geol 2:51–58CrossRefGoogle Scholar
  39. 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 36:617–630CrossRefGoogle Scholar
  40. Eichenseher T (2006) The cloudy side of sunscreens. Environ Sci Technol 40:1377–1378Google Scholar
  41. Eskelinin EL, Reggiori F, Baba M, Kovacs AL, Seglen PO (2011) Seeing is believing: the impact of electron microscopy on autophagy research. Autophagy 7:935–956CrossRefGoogle Scholar
  42. Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar Pollut Bull 50:125–146CrossRefGoogle Scholar
  43. Fadlallah YH (1983) Sexual reproduction, development and larval biology in scleractinian corals: a review. Coral Reefs 2:129–150CrossRefGoogle Scholar
  44. 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–S6CrossRefGoogle Scholar
  45. Finney DJ (1947) Probit analysis, a statistical treatment of the sigmoid response curve. Cambridge University Press, CambridgeGoogle Scholar
  46. 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 43:1097–1103CrossRefGoogle Scholar
  47. 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 339:61–71CrossRefGoogle Scholar
  48. Fortini P, Raspaglio G, Falchi M, Dogliotti E (1996) Analysis of DNA alkylation damage and repair in mammalian cells by the COMET assay. Mutagen 11:169–175CrossRefGoogle Scholar
  49. 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 21:1–14Google Scholar
  50. 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 12:964–974CrossRefGoogle Scholar
  51. Gago-Ferrero P, Diaz-Cruz MS, Barcelo D (2011) Occurrence of multiclass UV filters in treated sewage sludge from wastewater treatment plants. Chemosphere 84:1158–1165CrossRefGoogle Scholar
  52. 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 93:2507–2513CrossRefGoogle Scholar
  53. Gates RD, Edmunds PJ (1999) The physiological mechanisms of acclimatization in tropical reef corals. Am Zool 39:30–43CrossRefGoogle Scholar
  54. 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 35:208–219CrossRefGoogle Scholar
  55. Gleason DF, Hofmann DK (2011) Coral larvae: from gametes to recruits. J Exp Mar Biol Ecol 408:42–57CrossRefGoogle Scholar
  56. 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 76:14–20CrossRefGoogle Scholar
  57. Golub MS, Hogrefe CE, Germann SL, Jerome CP (2004) Endocrine disruption in adolescence: immunologic, hematologic, and bone effects in monkeys. Toxicol Sci 82:598–607CrossRefGoogle Scholar
  58. Goreau TJ (1990) Coral bleaching in Jamaica. Nature 343:417CrossRefGoogle Scholar
  59. 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):313–314Google Scholar
  60. Gura T (2008) Toxicity testing moves from the legislature to the Petri dish—and back. Cell 134:557–559CrossRefGoogle Scholar
  61. 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 181:13–18CrossRefGoogle Scholar
  62. Hagiwara H, Suizaki T, Tsukamoto Y (2008b) Effects of alkylphenols on bone metabolism in vivo and in vitro. Toxicol Lett 181:13–18CrossRefGoogle Scholar
  63. Hanson KM, Gratton E, Bardeen CJ (2006) Sunscreen enhancement of UV-induced reactive oxygen species in the skin. Free Radic Biol Med 41:1205–1212CrossRefGoogle Scholar
  64. Hany J, Nagel R (1995) Detection of sunscreen agents in human breast milk. Dtsch Lebensm Rundsch 91:341–345Google Scholar
  65. 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 346:89–96CrossRefGoogle Scholar
  66. Hughes TP, Tanner JE (2000) Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 81:2250–2263CrossRefGoogle Scholar
  67. 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 16:1812–1820CrossRefGoogle Scholar
  68. 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 1131:192–202CrossRefGoogle Scholar
  69. Jimenez CE, Cortes J (2003) Coral cover change associated to El Nino, Eastern Pacific, Costa Rica, 1992–2001, PSZNI. Mar Ecol 24:179–192CrossRefGoogle Scholar
  70. Johnston EL, Roberts DA (2009) Contaminants reduce the richness and evenness of marine communities: a review and meta-analysis. Environ Pollut 157:1745–1752CrossRefGoogle Scholar
  71. 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 159:1570–1576CrossRefGoogle Scholar
  72. 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 CrossRefGoogle Scholar
  73. Kerr JFR, Wullie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implication in tissue kinetics. Br J Cancer 26:239–257CrossRefGoogle Scholar
  74. Klionsky DJ, Abdalalla FC, Abeliovich H et al (2012) Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8:445–544CrossRefGoogle Scholar
  75. Knowland J, McKenzie EA, McHugh PJ, Cridland NA (1993) Sunlight-induced mutagenicity of a common sunscreen ingredient. FEBS Lett 324:309–313CrossRefGoogle Scholar
  76. Krysko DV, Berghe TV, D’Herde K, Vandenabeele P (2008) Apoptosis and necrosis: detection, discrimination and phagocytosis. Methods 44:205–221CrossRefGoogle Scholar
  77. 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 46:4624–4632CrossRefGoogle Scholar
  78. Kunz PY, Galicia HF, Fent K (2006) Comparison of in vitro and in vivo estrogenic activity of UV filters in fish. Toxicol Sci 90:349–361CrossRefGoogle Scholar
  79. 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 43:295–302CrossRefGoogle Scholar
  80. Laskowski R (1995) Some good reasons to ban the use of NOEC, LOEC, and related concepts in ecotoxicology. Oikos 73:140–144CrossRefGoogle Scholar
  81. 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 112:359–362CrossRefGoogle Scholar
  82. 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 171:425–433CrossRefGoogle Scholar
  83. 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 13:121–135CrossRefGoogle Scholar
  84. Loya Y (1975) Possible effects of water pollution on the community structure of Red Sea corals. Mar Biol 29:177–185CrossRefGoogle Scholar
  85. Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H et al (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131CrossRefGoogle Scholar
  86. Maloney KO, Munguia P, Mitchell RM (2011) Anthropogenic disturbance and landscape patterns affect diversity patterns of aquatic benthic macroinvertebrates. J N Am Benthol Soc 30:284–295CrossRefGoogle Scholar
  87. 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 19:115–123CrossRefGoogle Scholar
  88. 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 232:384–395CrossRefGoogle Scholar
  89. 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 19:457–469CrossRefGoogle Scholar
  90. Nakajima D, Asada S, Kageyama et al (2006) Activity related to the carcinogenicity of plastic additives in the benzophenone group. J UOEH 28:143–156Google Scholar
  91. 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 79:1189–1199CrossRefGoogle Scholar
  92. Nesa B, Baird AH, Harii S, Yakovleva I, Hidaka M (2012) Algal symbionts increase DNA damage in coral planulae exposed to sunlight. Zool Stud 51:12–17Google Scholar
  93. Newman MC (2013) Quantitative ecotoxicology. CRC Press, Boca RatonGoogle Scholar
  94. Nimrod AC, Benson WH (1998) Reproduction and development of Japanese medaka following an early life stage exposure to xenoestrogens. Aquat Toxicol 44:141–156CrossRefGoogle Scholar
  95. NRC (National Research Council) (2013) Assessing risks to endangered and threatened species from pesticides. National Academy of Sciences. ISBN 978-0-309-28583-4Google Scholar
  96. NTP (National Toxicology Program) (2006) NTP technical report on the toxicology and carcinogenesis of benzophenone in F344/N rats and B6C3F1 mice. NIH Publication # 06-4469Google Scholar
  97. 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, ParisGoogle Scholar
  98. OECD (2013) OECD Guidelines for the testing of chemicals: fish embryo acute toxicity test. Organization for Economic Cooperation and Development, ParisGoogle Scholar
  99. Omori M (2011) Degradation and restoration of coral reefs: experience in Okinawa, Japan. Mar Biol Res 7:3–12CrossRefGoogle Scholar
  100. 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 456–457:120–126CrossRefGoogle Scholar
  101. Peters EC (1984) A survey of cellular reactions to environmental stress and disease in Caribbean scleractinian corals. Helgol Meeresunters 37:113–137CrossRefGoogle Scholar
  102. 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 13:279–284Google Scholar
  103. 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 397:2763–2776CrossRefGoogle Scholar
  104. Platt KL, Aderhold S, Kulpe K, Fickler M (2008) Unexpected DNA damage caused by polycyclic aromatic hydrocarbons under standard laboratory conditions. Mutat Res 650:96–103CrossRefGoogle Scholar
  105. Popkin DJ, Prival MJ (1985) Effects of pH on weak and positive control mutagens in the AMES Salmonella plate assay. Mutat Res 142:109–113CrossRefGoogle Scholar
  106. Posthuma L, Suter GW II, Traas TP (2002) Species sensitivity distributions in ecotoxicology. Lewis Publishers, Boca Raton, p 587 ppGoogle Scholar
  107. 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 28:501–510CrossRefGoogle Scholar
  108. 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 22:627–640CrossRefGoogle Scholar
  109. Richardson SD (2006) Environmental mass spectrometry: emerging contaminants and current issues. Anal Chem 78:4021–4046CrossRefGoogle Scholar
  110. Richardson SD (2007) Water analysis: emerging contaminants and current issues. Anal Chem 79:4295–4324CrossRefGoogle Scholar
  111. Richmond R (1993) Coral reefs: present problems and future concerns resulting from anthropogenic disturbance. Am Zool 33:524–536CrossRefGoogle Scholar
  112. 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 175–197CrossRefGoogle Scholar
  113. Rickard DJ, Subramaniam M, Spelsberg TC (1999) Molecular and cellular mechanism of estrogen action on the skeleton. J Cell Biochem 75:123–132CrossRefGoogle Scholar
  114. 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 86:1040–1049CrossRefGoogle Scholar
  115. 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 306:103–114CrossRefGoogle Scholar
  116. Samara P, Syntichaki P, Tavernarakis N (2008) Autophagy is required for necrotic cell death in Caenorhabditis elegans. Cell Death Differ 15:105–112CrossRefGoogle Scholar
  117. 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 205:123–130CrossRefGoogle Scholar
  118. 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 24:2820–2826CrossRefGoogle Scholar
  119. Schlumpf M, Durrer S, Fass O et al (2008) Developmental toxicity of UV filters and environmental exposure: a review. Int J Androl 31:144–151CrossRefGoogle Scholar
  120. 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 20:448–457CrossRefGoogle Scholar
  121. 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 205:103–112CrossRefGoogle Scholar
  122. 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 929–940Google Scholar
  123. Shlesinger Y, Loya Y (1985) Coral community reproductive patterns: red sea versus the great barrier reef. Science 228:1333–1335CrossRefGoogle Scholar
  124. Simmons DJ (1966) Collagen formation and endochondral ossification in estrogen treated mice. Proc Soc Exp Biol Med 121:1165–1168CrossRefGoogle Scholar
  125. 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 56:1983–1991CrossRefGoogle Scholar
  126. Steel RGD (1959) A multiple comparison rank sum test: treatments versus control. Biometrics 15:560–572CrossRefGoogle Scholar
  127. Suter GW II (2007) Ecological risk assessment. CRC Press, Boca RatonGoogle Scholar
  128. 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 203:9–17CrossRefGoogle Scholar
  129. Taatjes DJ, Sobel BE, Budd RC (2008) Morphological and cytochemical determination of cell death by apoptosis. Histochem Cell Biol 129:33–43CrossRefGoogle Scholar
  130. 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 519:199–204CrossRefGoogle Scholar
  131. Tasdemir E, Galluzzi L, Majuri MN et al (2008) Methods for assessing autophagy and autophagic cell death. Methods Mol Biol 445:29–76CrossRefGoogle Scholar
  132. 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 77:333–340CrossRefGoogle Scholar
  133. Tsujimoto Y, Shimizu S (2005) Another way to die: autophagic programmed cell death. Cell Death Differ 15:1528–1534CrossRefGoogle Scholar
  134. 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 68:739–746CrossRefGoogle Scholar
  135. UNWTO (United Nations World Tourism Organization) website (2007) http://www.unwto.org/index.php. Accessed 30 Jun 2007
  136. US EPA (2012) Sunscreen use. http://www.epa.gov/ged/coralreef/models/SunscreenUse.html. Accessed 28 July 2014
  137. Väänänen HK, Härkönen PL (1996) Estrogen and bone metabolism. Maturitas 23:S65–S69CrossRefGoogle Scholar
  138. 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 279:2448–2456CrossRefGoogle Scholar
  139. 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 463–464:243–251CrossRefGoogle Scholar
  140. 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 77:343–350CrossRefGoogle Scholar
  141. West JM, Salm RV (2003) Resistance and resilience to coral bleaching: implications for coral reef conservation and management. Conserv Biol 17:956–967CrossRefGoogle Scholar
  142. White MK, Cinti C (2004) A morpholic approach to detect apoptosis based on electron microscopy. Methods Mol Biol 285:105–111Google Scholar
  143. Wilkinson C (2008) Status of coral reefs of the world. Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre, TownsvilleGoogle Scholar
  144. Williams DE, Miller MW, Kramer KL (2008) Recruitment failure in Florida Keys Acropora palmata, a threatened Caribbean coral. Coral Reefs 27:697–705CrossRefGoogle Scholar
  145. Xcaret Ecopark (2007) Home page. http://www.xcaret.com/services/faqs.php. Accessed 2 Dec 2013
  146. Xel-há Ecopark (2007) Home page. http://www.xelha.com. Accessed 2 Dec 2013
  147. Yla-Antilla P, Vihinen H, Jokitalo E, Eskelinin EL (2009) Monitoring autophagy by electron microscopy in mammalian cells. Methods Enzymol 452:143–164CrossRefGoogle Scholar
  148. Yu H (2002) Environmental carcinogenic polycyclic aromatic hydrocarbons: photochemistry and phototoxicity. J Environ Sci Health, Part C 20:149–183CrossRefGoogle Scholar
  149. Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice Hall, New JerseyGoogle Scholar
  150. 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 9:1–110CrossRefGoogle Scholar
  151. Zhao H, Wei D, Li M, Du Y (2013) Substituent contribution to the genotoxicity of benzophenone-type UV filters. Ecotoxicol Environ Saf 95:241–246CrossRefGoogle Scholar
  152. 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 164:147–156CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • C. A. Downs
    • 1
  • Esti Kramarsky-Winter
    • 2
    • 3
  • Roee Segal
    • 2
  • John Fauth
    • 4
  • Sean Knutson
    • 5
  • Omri Bronstein
    • 2
  • Frederic R. Ciner
    • 1
  • Rina Jeger
    • 3
  • Yona Lichtenfeld
    • 6
  • Cheryl M. Woodley
    • 7
    • 8
  • Paul Pennington
    • 8
  • Kelli Cadenas
    • 9
  • Ariel Kushmaro
    • 3
  • Yossi Loya
    • 2
  1. 1.Haereticus Environmental LaboratoryCliffordUSA
  2. 2.Department of Zoology, George S. Wise Faculty of Life SciencesTel Aviv UniversityTel AvivIsrael
  3. 3.Avram and Stella Goldstein-Goren Department of Biotechnology Engineering and the National Institute for Biotechnology in the NegevBen-Gurion University of the NegevBeer ShevaIsrael
  4. 4.Department of BiologyUniversity of Central FloridaOrlandoUSA
  5. 5.Pacific Biosciences Research CenterUniversity of HawaiiHonoluluUSA
  6. 6.Department of Life SciencesBen-Gurion University of the NegevBeer ShevaIsrael
  7. 7.Hollings Marine LaboratoryU.S. National Oceanic & Atmospheric AdministrationCharlestonUSA
  8. 8.Center for Coastal Environmental Health and Biomolecular ResearchU.S. National Oceanic & Atmospheric AdministrationCharlestonUSA
  9. 9.National AquariumBaltimoreUSA

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