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pp 1-46 | Cite as

Bioaccumulation and Toxicological Effects of UV-Filters on Marine Species

  • Clément Lozano
  • Justina Givens
  • Didier Stien
  • Sabine Matallana-Surget
  • Philippe LebaronEmail author
Chapter
  • 15 Downloads
Part of the The Handbook of Environmental Chemistry book series

Abstract

UV-filters are of emerging concern and their toxicity has been demonstrated in many papers. Organic and mineral UV-filters are active ingredients found in sunscreens. Due to the presence of UV-filters in marine waters, studies on these compounds bioaccumulating in organisms have been carried out, and this has been complemented by toxicity studies, with reports of detrimental effects to a variety of organisms. This chapter gives an overview of the bioaccumulation and the toxicity of sunscreen UV-filters on marine species. The toxicity of both inorganic and organic UV-filters is summarized as well as their bioaccumulation in marine biota. Ecotoxicological effects of UV-filters suffer from a lack of standardization across studies. We highlighted the difficulties to make comparisons between studies and emphasize a need for harmonization.

Keywords

Bioaccumulations Ecotoxicology Marine biota UV-filters 

References

  1. 1.
    Rainieri S et al (2017) Occurrence and toxicity of musks and UV filters in the marine environment. Food Chem Toxicol 104:57–68.  https://doi.org/10.1016/j.fct.2016.11.012CrossRefGoogle Scholar
  2. 2.
    Downs CA et al (2016) 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(2):265–288.  https://doi.org/10.1007/s00244-015-0227-7CrossRefGoogle Scholar
  3. 3.
    Paredes E et al (2014) Ecotoxicological evaluation of four UV filters using marine organisms from different trophic levels Isochrysis galbana, Mytilus galloprovincialis, Paracentrotus lividus, and Siriella armata. Chemosphere 104:44–50.  https://doi.org/10.1016/j.chemosphere.2013.10.053CrossRefGoogle Scholar
  4. 4.
    Costello MJ, Chaudhary C (2017) Marine biodiversity, biogeography, deep-sea gradients, and conservation. Curr Biol 27(11):R511–R527.  https://doi.org/10.1016/j.cub.2017.04.060CrossRefGoogle Scholar
  5. 5.
    Danovaro R, Corinaldesi C (2003) Sunscreen products increase virus production through prophage induction in marine bacterioplankton. Microb Ecol 45(2):109–118.  https://doi.org/10.1007/s00248-002-1033-0CrossRefGoogle Scholar
  6. 6.
    Danovaro R et al (2008) Sunscreens cause coral bleaching by promoting viral infections. Environ Health Perspect 116(4):441–447.  https://doi.org/10.1289/ehp.10966CrossRefGoogle Scholar
  7. 7.
    Spisni E, Seo S, Joo SH (2016) Release and toxicity comparison between industrial- and sunscreen-derived nano-ZnO particles. Environ Sci Technol 13(10):2485–2494.  https://doi.org/10.1007/s13762-016-1077-1CrossRefGoogle Scholar
  8. 8.
    Pirotta G (2016) The encyclopedia of allowed sunfilters in the world. Skin Care 11(2):19–21Google Scholar
  9. 9.
    Montaño MD et al (2014) Current status and future direction for examining engineered nanoparticles in natural systems. Environ Chem 11(4):351–366.  https://doi.org/10.1071/EN14037CrossRefGoogle Scholar
  10. 10.
    Barone AN et al (2019) Acute toxicity testing of TiO2 -based vs. oxybenzone-based sunscreens on clownfish (Amphiprion ocellaris). Environ Sci Pollut Res Int 26(14):14513–14520.  https://doi.org/10.1007/s11356-019-04769-zCrossRefGoogle Scholar
  11. 11.
    Ziarrusta H, Mijangos L, Montes R et al (2018) Chemosphere study of bioconcentration of oxybenzone in gilt-head bream and characterization of its by-products. Chemosphere 208:399–407.  https://doi.org/10.1016/j.chemosphere.2018.05.154.CrossRefGoogle Scholar
  12. 12.
    Araújo MJ et al (2018) Effects of UV filter 4-methylbenzylidene camphor during early development of Solea senegalensis Kaup, 1858. Sci Total Environ 628–629:1395–1404.  https://doi.org/10.1016/j.scitotenv.2018.02.112CrossRefGoogle Scholar
  13. 13.
    Cong Y et al (2017) The embryotoxicity of ZnO nanoparticles to marine medaka, Oryzias melastigma. Aquat Toxicol 185:11–18.  https://doi.org/10.1016/j.aquatox.2017.01.006CrossRefGoogle Scholar
  14. 14.
    Bar-On YM, Phillips R, Milo R (2018) The biomass distribution on Earth. Proc Natl Acad Sci U S A 115(25):6506–6511.  https://doi.org/10.1073/pnas.1711842115CrossRefGoogle Scholar
  15. 15.
    Ates M et al (2013) Comparative evaluation of impact of Zn and ZnO nanoparticles on brine shrimp (Artemia salina) larvae: effects of particle size and solubility on toxicity. Environ Sci Process Impacts 15(1):225–233.  https://doi.org/10.1039/c2em30540bCrossRefGoogle Scholar
  16. 16.
    Bhuvaneshwari M et al (2018) Toxicity and trophic transfer of P25 TiO2 NPs from Dunaliella salina to Artemia salina: effect of dietary and waterborne exposure. Environ Res 160:39–46.  https://doi.org/10.1016/j.envres.2017.09.022CrossRefGoogle Scholar
  17. 17.
    Clemente Z et al (2014) Minimal levels of ultraviolet light enhance the toxicity of TiO2 nanoparticles to two representative organisms of aquatic systems. J Nanopart Res 16(8):2559.  https://doi.org/10.1007/s11051-014-2559-zCrossRefGoogle Scholar
  18. 18.
    Li J et al (2017) Comparative toxicity of nano ZnO and bulk ZnO towards marine algae Tetraselmis suecica and Phaeodactylum tricornutum. Environ Sci Pollut Res 24(7):6543–6553.  https://doi.org/10.1007/s11356-016-8343-0.CrossRefGoogle Scholar
  19. 19.
    Lu J et al (2018) TiO2 nanoparticles in the marine environment: impact on the toxicity of phenanthrene and Cd2+ to marine zooplankton Artemia salina. Sci Total Environ 615:375–380.  https://doi.org/10.1016/j.scitotenv.2017.09.292CrossRefGoogle Scholar
  20. 20.
    Miglietta ML et al (2011) Characterization of nanoparticles in seawater for toxicity assessment towards aquatic organisms. Springer, Dordrecht.  https://doi.org/10.1007/978-94-007-1324-6CrossRefGoogle Scholar
  21. 21.
    Buffet PE et al (2012) Fate of isotopically labeled zinc oxide nanoparticles in sediment and effects on two endobenthic species, the clam Scrobicularia plana and the ragworm Hediste diversicolor. Ecotoxicol Environ Saf 84:191–198.  https://doi.org/10.1016/j.ecoenv.2012.07.010CrossRefGoogle Scholar
  22. 22.
    Galloway T et al (2010) Sublethal toxicity of nano-titanium dioxide and carbon nanotubes in a sediment dwelling marine polychaete. Environ Pollut 158(5):1748–1755.  https://doi.org/10.1016/j.envpol.2009.11.013CrossRefGoogle Scholar
  23. 23.
    Provencher JF et al (2017) Quantifying ingested debris in marine megafauna: a review and recommendations for standardization. Anal Methods 9(9):1454–1469.  https://doi.org/10.1039/c6ay02419jCrossRefGoogle Scholar
  24. 24.
    Barmo C et al (2013) In vivo effects of n-TiO2 on digestive gland and immune function of the marine bivalve Mytilus galloprovincialis. Aquat Toxicol 132–133:9–18.  https://doi.org/10.1016/j.aquatox.2013.01.014CrossRefGoogle Scholar
  25. 25.
    Ciacci C et al (2012) Immunomodulation by different types of N-oxides in the hemocytes of the marine bivalve Mytilus galloprovincialis. PLoS One 7(5):1–10.  https://doi.org/10.1371/journal.pone.0036937CrossRefGoogle Scholar
  26. 26.
    D’Agata A, Fasulo S, Dallas LJ et al (2014) Enhanced toxicity of “bulk” titanium dioxide compared to “fresh” and “aged” nano-TiO2 in marine mussels (Mytilus galloprovincialis). Nanotoxicology 8(5):549–558.  https://doi.org/10.3109/17435390.2013.807446CrossRefGoogle Scholar
  27. 27.
    Giraldo A et al (2017) Ecotoxicological evaluation of the UV filters ethylhexyl dimethyl p-aminobenzoic acid and octocrylene using marine organisms Isochrysis galbana, Mytilus galloprovincialis and Paracentrotus lividus. Arch Environ Contam Toxicol 72(4):606–611.  https://doi.org/10.1007/s00244-017-0399-4CrossRefGoogle Scholar
  28. 28.
    Hanna SK et al (2013) Impact of engineered zinc oxide nanoparticles on the individual performance of Mytilus galloprovincialis. PLoS One 8(4):e61800.  https://doi.org/10.1371/journal.pone.0061800CrossRefGoogle Scholar
  29. 29.
    Huang X et al (2016) Hemocyte responses of the thick shell mussel Mytilus coruscus exposed to nano-TiO2 and seawater acidification. Aquat Toxicol 180:1–10.  https://doi.org/10.1016/j.aquatox.2016.09.008CrossRefGoogle Scholar
  30. 30.
    Libralato G et al (2013) Embryotoxicity of TiO2 nanoparticles to Mytilus galloprovincialis (Lmk). Mar Environ Res 92:71–78.  https://doi.org/10.1016/j.marenvres.2013.08.015CrossRefGoogle Scholar
  31. 31.
    Wang Y et al (2014) Immune toxicity of TiO2 under hypoxia in the green-lipped mussel Perna viridis based on flow cytometric analysis of hemocyte parameters. Sci Total Environ 470–471:791–799.  https://doi.org/10.1016/j.scitotenv.2013.09.060CrossRefGoogle Scholar
  32. 32.
    Miller RJ et al (2012) TiO2 nanoparticles are phototoxic to marine phytoplankton. PLoS One 7(1):e30321.  https://doi.org/10.1371/journal.pone.0030321.CrossRefGoogle Scholar
  33. 33.
    Sendra M et al (2017) Effects of TiO2 nanoparticles and sunscreens on coastal marine microalgae: ultraviolet radiation is key variable for toxicity assessment. Environ Int 98:62–68.  https://doi.org/10.1016/j.envint.2016.09.024CrossRefGoogle Scholar
  34. 34.
    Seoane M et al (2017) Flow cytometric assay to assess short-term effects of personal care products on the marine microalga Tetraselmis suecica. Chemosphere 171:339–347.  https://doi.org/10.1016/j.chemosphere.2016.12.097CrossRefGoogle Scholar
  35. 35.
    Thiagarajan V et al (2019) Chemosphere diminishing bioavailability and toxicity of P25 TiO2 NPs during continuous exposure to marine algae Chlorella sp. Chemosphere 233:363–372.  https://doi.org/10.1016/j.chemosphere.2019.05.270CrossRefGoogle Scholar
  36. 36.
    Wong SWY, Leung KMY (2014) Temperature-dependent toxicities of nano zinc oxide to marine diatom, amphipod and fish in relation to its aggregation size and ion dissolution. Nanotoxicology 8(1):24–35.  https://doi.org/10.3109/17435390.2013.848949.CrossRefGoogle Scholar
  37. 37.
    Xia B et al (2015) Interaction of TiO2 nanoparticles with the marine microalga Nitzschia closterium: growth inhibition, oxidative stress and internalization. Sci Total Environ 508:525–533.  https://doi.org/10.1016/j.scitotenv.2014.11.066CrossRefGoogle Scholar
  38. 38.
    Deng XY et al (2017) Biological effects of TiO2 and CeO2 nanoparticles on the growth, photosynthetic activity, and cellular components of a marine diatom Phaeodactylum tricornutum. Sci Total Environ 575:87–96.  https://doi.org/10.1016/j.scitotenv.2016.10.003CrossRefGoogle Scholar
  39. 39.
    Fabrega J et al (2012) Sequestration of zinc from zinc oxide nanoparticles and life cycle effects in the sediment dweller amphipod Corophium volutator. Environ Sci Technol 46(2):1128–1135.  https://doi.org/10.1021/es202570g.CrossRefGoogle Scholar
  40. 40.
    Manzo S et al (2013b) Toxic effects of ZnO nanoparticles towards marine algae Dunaliella tertiolecta. Sci Total Environ 445–446:371–376.  https://doi.org/10.1016/j.scitotenv.2012.12.051CrossRefGoogle Scholar
  41. 41.
    Wang Y et al (2016) TiO2 nanoparticles in the marine environment: physical effects responsible for the toxicity on algae Phaeodactylum tricornutum. Sci Total Environ 565:818–826.  https://doi.org/10.1016/j.scitotenv.2016.03.164CrossRefGoogle Scholar
  42. 42.
    Wong SWY et al (2010) Toxicities of nano zinc oxide to five marine organisms: influences of aggregate size and ion solubility. Anal Bioanal Chem 396:609–618.  https://doi.org/10.1007/s00216-009-3249-zCrossRefGoogle Scholar
  43. 43.
    Downs CA et al (2014) Toxicological effects of the sunscreen UV filter, benzophenone-2, on planulae and in vitro cells of the coral, Stylophora pistillata. Ecotoxicology 23(2):175–191.  https://doi.org/10.1007/s10646-013-1161-yCrossRefGoogle Scholar
  44. 44.
    He T et al (2019) Comparative toxicities of four benzophenone ultraviolet filters to two life stages of two coral species. Sci Total Environ 651:2391–2399.  https://doi.org/10.1016/j.scitotenv.2018.10.148CrossRefGoogle Scholar
  45. 45.
    Stien D et al (2019) Metabolomics reveal that octocrylene accumulates in Pocillopora damicornis tissues as fatty acid conjugates and triggers coral cell mitochondrial dysfunction. Anal Chem 91(1):990–995.  https://doi.org/10.1021/acs.analchem.8b04187CrossRefGoogle Scholar
  46. 46.
    Jovanović B, Guzmán HM (2014) Effects of titanium dioxide (TiO2) nanoparticles on caribbean reef-building coral (Montastraea faveolata). Environ Toxicol Chem 33(6):1346–1353.  https://doi.org/10.1002/etc.2560CrossRefGoogle Scholar
  47. 47.
    Wang Z et al (2017) Trophic transfer of TiO2 nanoparticles from marine microalga (Nitzschia closterium) to scallop (Chlamys farreri) and related toxicity. Environ Sci Nano 4(2):415–424.  https://doi.org/10.1039/c6en00365fCrossRefGoogle Scholar
  48. 48.
    Torres T et al (2016) Screening the toxicity of selected personal care products using embryo bioassays: 4-MBC, propylparaben and triclocarban. Int J Mol Sci 17(10):1762.  https://doi.org/10.3390/ijms17101762CrossRefGoogle Scholar
  49. 49.
    Chen L et al (2018) Multigenerational effects of 4-methylbenzylidene camphor ( 4-MBC ) on the survival, development and reproduction of the marine copepod Tigriopus japonicus. Aquat Toxicol 194:94–102.  https://doi.org/10.1016/j.aquatox.2017.11.008CrossRefGoogle Scholar
  50. 50.
    Kusk KO, Avdolli M, Wollenberger L (2011) Effect of 2,4-dihydroxybenzophenone (BP1) on early life-stage development of the marine copepod Acartia tonsa at different temperatures and salinities. Environ Toxicol Chem 30(4):959–966.  https://doi.org/10.1002/etc.458CrossRefGoogle Scholar
  51. 51.
    Petersen K, Heiaas HH, Tollefsen KE (2014) Combined effects of pharmaceuticals, personal care products, biocides and organic contaminants on the growth of Skeletonema pseudocostatum. Aquat Toxicol 150:45–54.  https://doi.org/10.1016/j.aquatox.2014.02.013CrossRefGoogle Scholar
  52. 52.
    Ziarrusta H, Mijangos L, Picart-Armada S et al (2018b) Non-targeted metabolomics reveals alterations in liver and plasma of gilt-head bream exposed to oxybenzone. Chemosphere 211:624–631.  https://doi.org/10.1016/j.chemosphere.2018.08.013CrossRefGoogle Scholar
  53. 53.
    Fel J-P et al (2018) Photochemical response of the scleractinian coral Stylophora pistillata to some sunscreen ingredients. Coral Reefs 38(1):109–122.  https://doi.org/10.1007/s00338-018-01759-4CrossRefGoogle Scholar
  54. 54.
    He T et al (2019b) Toxicological effects of two organic ultraviolet filters and a related commercial sunscreen product in adult corals. Environ Pollut 245:462–471.  https://doi.org/10.1016/j.envpol.2018.11.029CrossRefGoogle Scholar
  55. 55.
    Román IP, Chisvert Alberto A, Canals A (2011) Dispersive solid-phase extraction based on oleic acid-coated magnetic nanoparticles followed by gas chromatography-mass spectrometry for UV-filter determination in water samples. J Chromatogr A 1218(18):2467–2475.  https://doi.org/10.1016/j.chroma.2011.02.047CrossRefGoogle Scholar
  56. 56.
    Sánchez Rodríguez A, Rodrigo Sanz M, Betancort Rodríguez JR (2015) Occurrence of eight UV filters in beaches of Gran Canaria (Canary Islands). An approach to environmental risk assessment. Chemosphere 131:85–90.  https://doi.org/10.1016/j.chemosphere.2015.02.054CrossRefGoogle Scholar
  57. 57.
    Kim S, Choi K (2014) Occurrences, toxicities, and ecological risks of benzophenone-3, a common component of organic sunscreen products: a mini-review. Environ Int 70:143–157.  https://doi.org/10.1016/j.envint.2014.05.015CrossRefGoogle Scholar
  58. 58.
    Tsui MMP et al (2014) Occurrence, distribution and ecological risk assessment of multiple classes of UV filters in surface waters from different countries. Water Res 67:55–65.  https://doi.org/10.1016/j.watres.2014.09.013CrossRefGoogle Scholar
  59. 59.
    Langford KH et al (2015) Environmental occurrence and risk of organic UV filters and stabilizers in multiple matrices in Norway. Environ Int 80:1–7.  https://doi.org/10.1016/j.envint.2015.03.012CrossRefGoogle Scholar
  60. 60.
    Corinaldesi C et al (2018) Impact of inorganic UV filters contained in sunscreen products on tropical stony corals (Acropora spp.). Sci Total Environ 637–638:1279–1285.  https://doi.org/10.1016/j.scitotenv.2018.05.108CrossRefGoogle Scholar
  61. 61.
    Li M et al (2019) Recovery of Alexandrium tamarense under chronic exposure of TiO2 nanoparticles and possible mechanisms. Aquat Toxicol 208:98–108.  https://doi.org/10.1016/j.aquatox.2019.01.007CrossRefGoogle Scholar
  62. 62.
    Yung MM et al (2015) Salinity dependent toxicities of zinc oxide nanoparticles to the marine diatom Thalassiosira pseudonana. Aquat Toxicol 165:31–40.  https://doi.org/10.1016/j.aquatox.2015.05.015CrossRefGoogle Scholar
  63. 63.
    Doyle JJ, Ward JE, Wikfors GH (2018) Acute exposure to TiO2 nanoparticles produces minimal apparent effects on oyster, Crassostrea virginica (Gmelin), hemocytes. Mar Pollut Bull 127(August 2017):512–523.  https://doi.org/10.1016/j.marpolbul.2017.12.039CrossRefGoogle Scholar
  64. 64.
    Schiavo S et al (2016) Genotoxic and cytotoxic effects of ZnO nanoparticles for Dunaliella tertiolecta and comparison with SiO2 and TiO2 effects at population growth inhibition levels. Sci Total Environ 550:619–627.  https://doi.org/10.1016/j.scitotenv.2016.01.135CrossRefGoogle Scholar
  65. 65.
    Zhu X, Zhou J, Cai Z (2011) The toxicity and oxidative stress of TiO2 nanoparticles in marine abalone (Haliotis diversicolor supertexta). Mar Pollut Bull 63(5–12):334–338.  https://doi.org/10.1016/j.marpolbul.2011.03.006CrossRefGoogle Scholar
  66. 66.
    Li F et al (2015) Toxicity of nano-TiO2 on algae and the site of reactive oxygen species production. Aquat Toxicol 158:1–13.  https://doi.org/10.1016/j.aquatox.2014.10.014CrossRefGoogle Scholar
  67. 67.
    Kong H et al (2019) Nano-TiO2 impairs digestive enzyme activities of marine mussels under ocean acidification. Chemosphere 237:124561.  https://doi.org/10.1016/j.chemosphere.2019.124561CrossRefGoogle Scholar
  68. 68.
    Wang T et al (2019) Differential in vivo hemocyte responses to nano titanium dioxide in mussels: effects of particle size. Aquat Toxicol 212:28–36.  https://doi.org/10.1016/j.aquatox.2019.04.012CrossRefGoogle Scholar
  69. 69.
    Canesi L et al (2010) Biomarkers in Mytilus galloprovincialis exposed to suspensions of selected nanoparticles ( Nano carbon black, C60 fullerene, Nano-TiO2, Nano-SiO2 ). Aquat Toxicol 100(2):168–177.  https://doi.org/10.1016/j.aquatox.2010.04.009CrossRefGoogle Scholar
  70. 70.
    Canesi L et al (2010b) In vitro effects of suspensions of selected nanoparticles ( C60 fullerene, TiO2, SiO2 ) on Mytilus helocytes. Aquat Toxicol 96:151–158.  https://doi.org/10.1016/j.aquatox.2009.10.017CrossRefGoogle Scholar
  71. 71.
    Guan X et al (2018) Neurotoxic impact of acute TiO2 nanoparticle exposure on a benthic marine bivalve mollusk, Tegillarca granosa. Aquat Toxicol 200:241–246.  https://doi.org/10.1016/j.aquatox.2018.05.011CrossRefGoogle Scholar
  72. 72.
    Castro-bugallo A et al (2014) Comparative responses to metal oxide nanoparticles in marine phytoplankton. Arch Environ Contam Toxicol 67(4):483–493.  https://doi.org/10.1007/s00244-014-0044-4CrossRefGoogle Scholar
  73. 73.
    Schiavo S et al (2017) Testing ZnO nanoparticle ecotoxicity: linking time variable exposure to effects on different marine model organisms. Environ Sci Pollut Res 25(5):4871–4880. doi.org/10.1007/s11356-017-0815-3Google Scholar
  74. 74.
    Wang J, Wang W (2014) Significance of physicochemical and uptake kinetics in controlling the toxicity of metallic nanomaterials to aquatic organisms∗. J Zhejiang Univ Sci A 15(8):573–592.  https://doi.org/10.1631/jzus.A1400109CrossRefGoogle Scholar
  75. 75.
    Trevisan R et al (2014) Gills are an initial target of zinc oxide nanoparticles in oysters Crassostrea gigas, leading to mitochondrial disruption and oxidative stress. Aquat Toxicol 153:27–38.  https://doi.org/10.1016/j.aquatox.2014.03.018CrossRefGoogle Scholar
  76. 76.
    Manzo S et al (2013) Embryotoxicity and spermiotoxicity of nanosized ZnO for Mediterranean sea urchin Paracentrotus lividus. J Hazard Mater 254–255:1–9.  https://doi.org/10.1016/j.jhazmat.2013.03.027CrossRefGoogle Scholar
  77. 77.
    Miller RJ et al (2010) Impacts of metal oxide nanoparticles on marine phytoplankton. Environ Sci Technol 44(19):7329–7334Google Scholar
  78. 78.
    Aravantinou AF et al (2015) Effect of cultivation media on the toxicity of ZnO nanoparticles to freshwater and marine microalgae. Ecotoxicol Environ Saf 114:109–116.  https://doi.org/10.1016/j.ecoenv.2015.01.016CrossRefGoogle Scholar
  79. 79.
    Oliviero M et al (2019) DNA damages and offspring quality in sea urchin Paracentrotus lividus. Sci Total Environ 651:756–765.  https://doi.org/10.1016/j.scitotenv.2018.09.243CrossRefGoogle Scholar
  80. 80.
    Peng X et al (2011) Effect of morphology of ZnO nanostructures on their toxicity to marine algae. Aquat Toxicol 102(3–4):186–196.  https://doi.org/10.1016/j.aquatox.2011.01.014.CrossRefGoogle Scholar
  81. 81.
    Hazeem LJ et al (2016) Cumulative effect of zinc oxide and titanium oxide nanoparticles on growth and chlorophyll a content of Picochlorum sp. Environ Sci Pollut Res 23(3):2821–2830.  https://doi.org/10.1007/s11356-015-5493-4CrossRefGoogle Scholar
  82. 82.
    Marisa I et al (2016) In vivo exposure of the marine clam Ruditapes philippinarum to zinc oxide nanoparticles: responses in gills, digestive gland and haemolymph. Environ Sci Pollut Res 23(15):15275–15293.  https://doi.org/10.1007/s11356-016-6690-5CrossRefGoogle Scholar
  83. 83.
    Zhang C et al (2016) Toxic effects of nano-ZnO on marine microalgae Skeletonema costatum: attention to the accumulation of intracellular Zn. Aquat Toxicol 178:158–164.  https://doi.org/10.1016/j.aquatox.2016.07.020CrossRefGoogle Scholar
  84. 84.
    Vicente A et al (2019) Toxicity mechanisms of ZnO UV-filters used in sunscreens toward the model cyanobacteria Synechococcus elongatus PCC 7942. Environ Sci Pollut Res 26(22):22450–22463.  https://doi.org/10.1007/s11682-018-9832-1CrossRefGoogle Scholar
  85. 85.
    Miao AJ et al (2010) Zinc oxide-engineered nanoparticles: dissolution and toxicity to marine phytoplankton. Environ Toxicol Chem 29(12):2814–2822.  https://doi.org/10.1002/etc.340CrossRefGoogle Scholar
  86. 86.
    Yung MMN et al (2017) Physicochemical characteristics and toxicity of surface-modified zinc oxide nanoparticles to freshwater and marine microalgae. Sci Rep 7:1–14.  https://doi.org/10.1038/s41598-017-15988-0.CrossRefGoogle Scholar
  87. 87.
    Bielmyer-Fraser GK et al (2014) Cellular partitioning of nanoparticulate versus dissolved metals in marine phytoplankton. Environ Sci Technol 48(22):13443–13450.  https://doi.org/10.1021/es501187g.CrossRefGoogle Scholar
  88. 88.
    Osterwalder U, Sohn M, Herzog B (2014) Global state of sunscreens. Photodermatol Photoimmunol Photomed 30(2–3):62–80.  https://doi.org/10.1111/phpp.12112CrossRefGoogle Scholar
  89. 89.
    Rodríguez-Romero A et al (2019) Sunscreens as a new source of metals and nutrients to coastal waters. Environ Sci Technol 53(17):10177–10187.  https://doi.org/10.1021/acs.est.9b02739CrossRefGoogle Scholar
  90. 90.
    Tovar-Sánchez A et al (2013) Sunscreen products as emerging pollutants to coastal waters. PLoS One 8(6):e65451.  https://doi.org/10.1371/journal.pone.0065451.CrossRefGoogle Scholar
  91. 91.
    Sánchez-Quiles D, Tovar-Sánchez A (2014) Sunscreens as a source of hydrogen peroxide production in coastal waters. Environ Sci Technol 48(16):9037–9042.  https://doi.org/10.1021/es5020696CrossRefGoogle Scholar
  92. 92.
    Fastelli P, Renzi M (2019) Exposure of key marine species to sunscreens: changing ecotoxicity as a possible indirect effect of global warming. Mar Pollut Bull 149:110517.  https://doi.org/10.1016/j.marpolbul.2019.110517CrossRefGoogle Scholar
  93. 93.
    Mccoshum SM, Schlarb AM, Baum KA (2016) Direct and indirect effects of sunscreen exposure for reef biota. Hydrobiologia 776(1):139–146.  https://doi.org/10.1007/s10750-016-2746-2CrossRefGoogle Scholar
  94. 94.
    Sendra M et al (2017b) Toxicity of TiO2, in nanoparticle or bulk form to freshwater and marine microalgae under visible light and UV-A radiation. Environ Pollut 227:39–48.  https://doi.org/10.1016/j.envpol.2017.04.053CrossRefGoogle Scholar
  95. 95.
    Liu YS et al (2011) Photostability of the UV filter benzophenone-3 and its effect on the photodegradation of benzotriazole in water. Environ Chem 8(6):581–588.  https://doi.org/10.1071/EN11068CrossRefGoogle Scholar
  96. 96.
    Rodil R et al (2009) Photostability and phytotoxicity of selected sunscreen agents and their degradation mixtures in water. Anal Bioanal Chem 395(5):1513–1524.  https://doi.org/10.1007/s00216-009-3113-1CrossRefGoogle Scholar
  97. 97.
    Herzog B, Wehrle M, Quass K (2009) Photostability of UV absorber systems in sunscreens. Photochem Photobiol 85(4):869–878.  https://doi.org/10.1111/j.1751-1097.2009.00544.xCrossRefGoogle Scholar
  98. 98.
    Jentzsch F et al (2016) Photodegradation of the UV filter ethylhexyl methoxycinnamate under ultraviolet light: identification and in silico assessment of photo-transformation products in the context of grey water reuse. Sci Total Environ 572:1092–1100.  https://doi.org/10.1016/j.scitotenv.2016.08.017CrossRefGoogle Scholar
  99. 99.
    MacManus-Spencer LA et al (2011) Aqueous photolysis of the organic ultraviolet filter chemical octyl methoxycinnamate. Environ Sci Technol 45(9):3931–3937.  https://doi.org/10.1021/es103682aCrossRefGoogle Scholar
  100. 100.
    Damiani E et al (2010) Assessment of the photo-degradation of UV-filters and radical-induced peroxidation in cosmetic sunscreen formulations. Free Radic Res 44(3):304–312.  https://doi.org/10.3109/10715760903486065CrossRefGoogle Scholar
  101. 101.
    Li Y et al (2016) Photochemical transformation of sunscreen agent benzophenone-3 and its metabolite in surface freshwater and seawater. Chemosphere 153:494–499.  https://doi.org/10.1016/j.chemosphere.2016.03.080CrossRefGoogle Scholar
  102. 102.
    Beel R, Lütke Eversloh C, Ternes TA (2013) Biotransformation of the UV-filter sulisobenzone: challenges for the identification of transformation products. Environ Sci Technol 47(13):6819–6828.  https://doi.org/10.1021/es400451wCrossRefGoogle Scholar
  103. 103.
    Badia-Fabregat M et al (2012) Degradation of UV filters in sewage sludge and 4-MBC in liquid medium by the ligninolytic fungus Trametes versicolor. J Environ Manag 104:114–120.  https://doi.org/10.1016/j.jenvman.2012.03.039CrossRefGoogle Scholar
  104. 104.
    Volpe A et al (2017) Biodegradation of UV-filters in marine sediments. Sci Total Environ 575:448–457.  https://doi.org/10.1016/j.scitotenv.2016.10.001CrossRefGoogle Scholar
  105. 105.
    Apel C, Joerss H, Ebinghaus R (2018) Environmental occurrence and hazard of organic UV stabilizers and UV filters in the sediment of European North and Baltic Seas. Chemosphere 212:254–261.  https://doi.org/10.1016/j.chemosphere.2018.08.105CrossRefGoogle Scholar
  106. 106.
    Fagervold SK et al (2019) Occurrence and environmental distribution of 5 UV filters during the summer season in different water bodies. Water Air Soil Pollut 230(7):172.  https://doi.org/10.1007/s11270-019-4217-7CrossRefGoogle Scholar
  107. 107.
    Alonso MB et al (2015) Toxic heritage: maternal transfer of pyrethroid insecticides and sunscreen agents in dolphins from Brazil. Environ Pollut 207:391–402.  https://doi.org/10.1016/j.envpol.2015.09.039.CrossRefGoogle Scholar
  108. 108.
    Bachelot M et al (2012) Organic UV filter concentrations in marine mussels from French coastal regions. Sci Total Environ 420:273–279.  https://doi.org/10.1016/j.scitotenv.2011.12.051CrossRefGoogle Scholar
  109. 109.
    Barbosa V et al (2018) Effects of steaming on contaminants of emerging concern levels in seafood. Food Chem Toxicol 118:490–504.  https://doi.org/10.1016/j.fct.2018.05.047.CrossRefGoogle Scholar
  110. 110.
    Castro M et al (2018) Occurrence, profile and spatial distribution of UV-filters and musk fragrances in mussels from Portuguese coastline. Mar Environ Res 138:110–118.  https://doi.org/10.1016/j.marenvres.2018.04.005CrossRefGoogle Scholar
  111. 111.
    Cunha SC et al (2015) Co-occurrence of musk fragrances and UV- filters in seafood and macroalgae collected in European hotspots. Environ Res 143:65–71.  https://doi.org/10.1016/j.envres.2015.05.003CrossRefGoogle Scholar
  112. 112.
    Cunha SC et al (2018) UV-filters and musk fragrances in seafood commercialized in Europe Union: occurrence, risk and exposure assessment. Environ Res 161:399–408.  https://doi.org/10.1016/j.envres.2017.11.015CrossRefGoogle Scholar
  113. 113.
    Gago-Ferrero P et al (2013) First determination of UV filters in marine mammals. Octocrylene levels in Franciscana dolphins. Environ Sci Technol 47(11):5619–5625.  https://doi.org/10.1021/es400675yCrossRefGoogle Scholar
  114. 114.
    Horricks RA et al (2019) Organic ultraviolet filters in nearshore waters and in the invasive lionfish (Pterois volitans) in Grenada, West Indies. PLoS One 14(7):e0220280.  https://doi.org/10.1371/journal.pone.0220280CrossRefGoogle Scholar
  115. 115.
    Kim J et al (2011) Chemosphere Contamination and bioaccumulation of benzotriazole ultraviolet stabilizers in fish from Manila Bay, the Philippines using an ultra-fast liquid chromatography – tandem mass spectrometry. Chemosphere 85(5):751–758.  https://doi.org/10.1016/j.chemosphere.2011.06.054.CrossRefGoogle Scholar
  116. 116.
    Mitchelmore CL et al (2019) Science of the Total Environment Occurrence and distribution of UV-filters and other anthropogenic contaminants in coastal surface water, sediment, and coral tissue from Hawaii. Sci Total Environ 670:398–410.  https://doi.org/10.1016/j.scitotenv.2019.03.034CrossRefGoogle Scholar
  117. 117.
    Molins-Delgado D et al (2018) Occurrence of organic UV filters and metabolites in lebranche mullet (Mugil liza) from Brazil. Sci Total Environ 618:451–459.  https://doi.org/10.1016/j.scitotenv.2017.11.033CrossRefGoogle Scholar
  118. 118.
    Nakata H, Murata S, Filatreau J (2009) Occurrence and concentrations of benzotriazole UV stabilizers in marine organisms and sediments from the Ariake Sea, Japan. Environ Sci Technol 43(18):6920–6926.  https://doi.org/10.1021/es900939jCrossRefGoogle Scholar
  119. 119.
    Nakata H et al (2010) Detection of benzotriazole UV stabilizers in the blubber of marine mammals by gas chromatography-high resolution mass spectrometry (GC-HRMS). J Environ Monit 12(11):2088–2092.  https://doi.org/10.1039/c0em00170hCrossRefGoogle Scholar
  120. 120.
    Nakata H et al (2012) Asia-Pacific mussel watch for emerging pollutants: distribution of synthetic musks and benzotriazole UV stabilizers in Asian and US coastal waters. Mar Pollut Bull 64(10):2211–2218.  https://doi.org/10.1016/j.marpolbul.2012.07.049CrossRefGoogle Scholar
  121. 121.
    Pacheco-Juárez J et al (2019) Analysis and occurrence of benzotriazole ultraviolet stabilisers in different species of seaweed. Chemosphere 236:124344.  https://doi.org/10.1016/j.chemosphere.2019.124344CrossRefGoogle Scholar
  122. 122.
    Peng X et al (2017) Bioaccumulation and biomagnification of ultraviolet absorbents in marine wildlife of the Pearl River Estuarine, South China Sea. Environ Pollut 225:55–65.  https://doi.org/10.1016/j.envpol.2017.03.035CrossRefGoogle Scholar
  123. 123.
    Picot Groz M et al (2014) Detection of emerging contaminants (UV filters, UV stabilizers and musks) in marine mussels from Portuguese coast by QuEChERS extraction and GC-MS/MS. Sci Total Environ 493:162–169.  https://doi.org/10.1016/j.scitotenv.2014.05.062CrossRefGoogle Scholar
  124. 124.
    Rodil R et al (2019) Legacy and emerging pollutants in marine bivalves from the Galician coast (NW Spain). Environ Int 129:364–375.  https://doi.org/10.1016/j.envint.2019.05.018CrossRefGoogle Scholar
  125. 125.
    Tsui MM et al (2017) Occurrence, distribution, and fate of organic UV filters in coral communities. Environ Sci Technol 51(8):4182–4190.  https://doi.org/10.1021/acs.est.6b05211.CrossRefGoogle Scholar
  126. 126.
    Bossart GD (2011) Marine mammals as sentinel species for oceans and human health. Vet Pathol 48(3):676–690.  https://doi.org/10.1177/0300985810388525CrossRefGoogle Scholar
  127. 127.
    Tanabe S, Iwata H, Tatsukawa R (1994) Global contamination by persistent organochlorines and their ecotoxicological impact on marine mammals. Sci Total Environ 154(2–3):163–177.  https://doi.org/10.1016/0048-9697(94)90086-8CrossRefGoogle Scholar
  128. 128.
    Gomez E et al (2012) Bioconcentration of two pharmaceuticals (benzodiazepines) and two personal care products (UV filters) in marine mussels (Mytilus galloprovincialis) under controlled laboratory conditions. Environ Sci Pollut Res 19(7):2561–2569.  https://doi.org/10.1007/s11356-012-0964-3CrossRefGoogle Scholar
  129. 129.
    Vidal-Liñán L et al (2018) Bioaccumulation of UV filters in Mytilus galloprovincialis mussel. Chemosphere 190:267–271.  https://doi.org/10.1016/j.chemosphere.2017.09.144CrossRefGoogle Scholar
  130. 130.
    Jarvis TA et al (2013) Toxicity of ZnO nanoparticles to the copepod Acartia tonsa, exposed through a phytoplankton diet. Environ Toxicol Chem 32(6):1264–1269.  https://doi.org/10.1002/etc.2180CrossRefGoogle Scholar
  131. 131.
    Montes MO et al (2012) Uptake, accumulation and biotransformation of metal oxide nanoparticles by a marine suspension-feeder. J Hazard Mater 225–226:139–145.  https://doi.org/10.1016/j.jhazmat.2012.05.009CrossRefGoogle Scholar
  132. 132.
    Wang Z et al (2016b) Trophic transfer and accumulation of TiO2 nanoparticles from clamworm ( Perinereis aibuhitensis ) to juvenile turbot ( Scophthalmus maximus ) along a marine benthic food chain. Water Res 95:250–259.  https://doi.org/10.1016/j.watres.2016.03.027CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Clément Lozano
    • 1
    • 2
  • Justina Givens
    • 1
  • Didier Stien
    • 1
  • Sabine Matallana-Surget
    • 3
  • Philippe Lebaron
    • 1
    Email author
  1. 1.Sorbonne Université, CNRS, Laboratoire de Biodiversité et Biotechnologies Microbiennes, USR3579, Observatoire Océanologique de BanyulsBanyuls-sur-merFrance
  2. 2.Biological and Environmental SciencesStirling UniversityStirlingUK
  3. 3.Division of Biological and Environmental SciencesFaculty of Natural Sciences, University of StirlingStirlingUK

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