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

Craig A. Downs1, Esti Kramarsky‐Winter2,3, Roee Segal3, John E. Fauth4, Sean Knutson5, Omri Bronstein3, Frederic R. Ciner1, Rina Jeger2, Yona Lichtenfeld6, Cheryl M. Woodley7, Paul L. Pennington8, Kelli Cadenas9, Ariel Kushmaro2, Yossi Loya3
1Haereticus Environmental Laboratory, Clifford, USA
2Avram and Stella Goldstein-Goren Department of Biotechnology Engineering and the National Institute for Biotechnology in the Negev, Ben-Gurion University of the Negev, Beer Sheva, Israel
3Department of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel
4Department of Biology, University of Central Florida, Orlando, USA
5Pacific Biosciences Research Center, University of Hawaii, Honolulu, USA
6Department of Life Sciences, Ben Gurion University of the Negev, Beer Sheva, Israel.
7Hollings Marine Laboratory, U.S. National Oceanic & Atmospheric Administration, Charleston, USA
8Center for Coastal Environmental Health and Biomolecular Research, U.S. National Oceanic & Atmospheric Administration, Charleston, USA
9National Aquarium, Baltimore, USA

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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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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