Exposure to four chemical UV filters through contaminated sediment: impact on survival, hatching success, cardiac frequency, and aerobic metabolic scope in embryo-larval stage of zebrafish.


Journal

Environmental science and pollution research international
ISSN: 1614-7499
Titre abrégé: Environ Sci Pollut Res Int
Pays: Germany
ID NLM: 9441769

Informations de publication

Date de publication:
Jun 2021
Historique:
received: 01 07 2020
accepted: 18 01 2021
pubmed: 9 2 2021
medline: 29 6 2021
entrez: 8 2 2021
Statut: ppublish

Résumé

UV filters are widely used in many pharmaceutical and personal care products such as sunscreen and cosmetics to protect from UV irradiation. Due to their hydrophobic properties and relative stability, they have a high capacity to accumulate in sediment. Little information is available on their ecotoxicity on fish. In aquatic ecosystems, fish eggs could be directly affected by UV filters through contact with contaminated sediment. The aim of this study was to investigate the individual toxicity of four UV filters: benzophenone-3 (BP3), butyl methoxydibenzoylmethane (BM), bis-ethylhexyloxyphenol methoxyphenyl triazine (BEMT), and methylene bis-benzotriazolyl tetramethylbutylphenol (MBBT), in embryo-larval stages of zebrafish Danio rerio. Fish eggs were exposed to single UV filters by contact with spiked sediment during 96 h at a concentration of 10 μg g

Identifiants

pubmed: 33555472
doi: 10.1007/s11356-021-12582-w
pii: 10.1007/s11356-021-12582-w
doi:

Substances chimiques

Sunscreening Agents 0
Water Pollutants, Chemical 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

29412-29420

Références

Araújo MJ, Rocha RJM, Soares AMVM, Benedé JL, Chisvert A, Monteiro MS (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.2018.02.112
doi: 10.1016/j.scitotenv.2018.02.112
Barjhoux J, Baudrimont M, Morin B, Landi L, Gonzalez P, Cachot J (2012) Effects of copper and cadmium spiked-sediments on embryonic development of Japanese medaka (Oryzias latipes). Ecotox Environ Safe 79:272–282. https://doi.org/10.1016/j.ecoenv.2012.01.011
doi: 10.1016/j.ecoenv.2012.01.011
Barone AN, Hayes CE, Kerr JJ, Lee RC, Flaherty DB (2019) Acute toxicity testing of TiO2-based vs. oxybenzone-based sunscreens on clownfish (Amphiprion ocellaris). Environ Sci Pollut Res 26:14513–14520. https://doi.org/10.1007/s11356-019-04769-z
doi: 10.1007/s11356-019-04769-z
Barrionuevo WR, Burggren W (1999) O2 consumption and heart rate in developing zebrafish (Danio rerio): influence of temperature and ambient O2. Am J Phys 276:505–513
Blüthgen N, Meili N, Chew G, Odermatt A, Fent K (2014) Accumulation and effects of the UV-filter octocrylene in adult and embryonic zebrafish (Danio rerio). Sci Total Environ 476–477:207–217. https://doi.org/10.1016/j.scitotenv.2014.01.015
doi: 10.1016/j.scitotenv.2014.01.015
Burggren WW (2005) Developing animals flout prominent assumptions of ecological physiology. Comparat Biochem Physiol, Part A 141:430–439
doi: 10.1016/j.cbpb.2005.03.010
Cannas M, Atzori F, Rupsard F, Bustamante P, Loizeau V, Lefrançois C (2012) PCB contamination does not alter aerobic metabolism and tolerance to hypoxia of juvenile sole (Solea solea). Aquat Toxicol 127:54–60
doi: 10.1016/j.aquatox.2012.04.017
Chen L, Li X, Hong H, Shi D (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.2017.11.008
doi: 10.1016/j.aquatox.2017.11.008
Claireaux G, Lefrançois C (2007) Linking environmental variability and fish performance: integration through the concept of scope for activity. Phil Trans R Soc 2031–2041. https://doi.org/10.1098/rstb.2007.2099
Claireaux G, Davoodi F (2010) Effect of exposure to petroleum hydrocarbons upon cardio-respiratory function in the common sole (Solea solea). Aquat Toxicol 98(2):113–119. https://doi.org/10.1016/j.aquatox.2010.02.006
doi: 10.1016/j.aquatox.2010.02.006
Clark TD, Donaldson MR, Pieperhoff S, Drenner SM, Lotto A, Cooke SJ, Hinch SG, Patterson DA, Farrell AP (2012) Physiological benefits of being small in a changing world: responses of Coho salmon (Oncorhynchus kisutch) to an acute thermal challenge and a simulated capture event. PLoS ONE 7:e39079
doi: 10.1371/journal.pone.0039079
Coronado M, De Haro H, Deng X, Rempel MA, Lavado R, Schlenk D (2008) Estrogenic activity and reproductive effects of the UV-filter oxybenzone (2-hydroxy-4-methoxyphenyl- methanone) in fish. Aquat Toxicol 90:182–187. https://doi.org/10.1016/j.aquatox.2008.08.018
doi: 10.1016/j.aquatox.2008.08.018
Downs CA, Kramarsky-Winter E, Fauth JE, Segal R, Bronstein O, Jeger R, Lichtenfeld Y, Woodley CM, Pennington P, Kushmaro A, Loya Y (2014) Toxicological effects of the sunscreen UV filter, benzophenone-2, on planulae and in vitro cells of the coral, Stylophora pistillata. Ecotox 23(2):175–191
doi: 10.1007/s10646-013-1161-y
Downs CA, Kramarsky-Winter E, Segal R, Fauth J, Knutson S, Bronstein O, Ciner FR, Jeger R, Lichtenfeld Y, Woodley CM, Pennington P, Cadenas K, Kushmaro A, Loya Y (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 70:265–288. https://doi.org/10.1007/s00244-015-0227-7
doi: 10.1007/s00244-015-0227-7
Esperanza M, Seoane M, Rioboo C, Herrero C, Cid Á (2019) Differential toxicity of the UV- filters BP-3 and BP-4 in Chlamydomonas reinhardtii: A flow cytometric approach. Sci Total Environ 669:412–420. https://doi.org/10.1016/j.scitotenv.2019.03.116
doi: 10.1016/j.scitotenv.2019.03.116
Fagervold SK, Rodrigues AMS, Rohée C, Roe R, Bourrain M, Stien D, Lebaron P (2019) Occurrence and environmental distribution of 5 UV filters during the summer season in different water bodies. Water Air Soil Pollut 230:172–172
doi: 10.1007/s11270-019-4217-7
Fent K, Zenker A, Rapp M (2010) Widespread occurrence of estrogenic UV-filters in aquatic ecosystems in Switzerland. Environ Pollut 158(5):1817–1824
doi: 10.1016/j.envpol.2009.11.005
Gao L, Yuan T, Zhou C, Cheng P, Bai Q, Ao J, Wang W, Zhang H (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. https://doi.org/10.1016/j.chemosphere.2013.09.041
doi: 10.1016/j.chemosphere.2013.09.041
Giokas DL, Sakkas VA, Albanis TA, Lampropoulou DA (2005) Determination of UV-filter residues in bathing waters by liquid chromatography UV-diode array and gas chromatography–mass spectrometry after micelle mediated extraction-solvent back extraction. J Chromatogr A 1077(1):19–27
doi: 10.1016/j.chroma.2005.04.074
He T, Tsui MMP, Tan CJ, Ma CY, Yiu SKF, Wang LH, Chen TH, Fan TY, Lam PKS, Murphy MB (2019) 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.2018.11.029
doi: 10.1016/j.envpol.2018.11.029
Hicken CE, Linbo TL, Baldwin DH, Willis ML, Myers MS, Holland L, Incardona JP (2011) Sub-lethal exposure to crude oil during embryonic development alters cardiac morphology and reduces aerobic capacity in adult fish. Proc Acad Sci 108:7086–7090
doi: 10.1073/pnas.1019031108
Hill AJ, Teraoka H, Heideman W, Peterson RE (2005) Zebrafish as a model vertebrate for investigating chemical toxicity. Toxicol Sci 86(1):6–19
doi: 10.1093/toxsci/kfi110
Incardona JP, Collier TK, Scholz NL (2004) Defects in cardiac function precede morphological abnormalities in fish embryos exposed to polycyclic aromatic hydrocarbons. Toxicol Appl Pharmacol 196:191–205
doi: 10.1016/j.taap.2003.11.026
Incardona JP, Carls MG, Teraoka H, Sloan CA, Collier TK, Scholz NL (2005) Aryl hydrocarbon receptor-independent toxicity of weathered crude oil during fish de- velopment. Environ Health Perspect 113:1755–1762
doi: 10.1289/ehp.8230
Incardona JP, Linbo TL, Scholz NL (2011) Cardiac toxicity of 5-ring polycyclic aromatic hydrocarbons is differentially dependent on the aryl hydrocarbon receptor 2 isoform during zebrafish development. Toxicol Appl Pharmacol 257:242–249
doi: 10.1016/j.taap.2011.09.010
Jourdan-Pineau H, Dupont-Prinet A, Claireaux G, McKenzie DJ (2010) An investigation of metabolic prioritization in the European Sea Bass, Dicentrarchus labrax. Physiol Biochem Zool 83:68–77
doi: 10.1086/648485
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):1576–1576. https://doi.org/10.1016/j.envpol.2011.02.055
doi: 10.1016/j.envpol.2011.02.055
Kaiser D, Sieratowicz A, Zielke H, Oetken M, Hollert H, Oehlmann J (2012) Ecotoxicological effect characterisation of widely used organic UV filters. Environ Pollut 163(84):90–90. https://doi.org/10.1016/j.envpol.2011.12.014
doi: 10.1016/j.envpol.2011.12.014
Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of Embryonic Development of the Zebrafish. Dev Dyn 203:253–310
doi: 10.1002/aja.1002030302
Kinnberg KL, Petersen GI, Albrektsen M, Minghlani M, Awad S, Holbech B, Green J, Bjerregaard P, Holbech H (2015) Endocrine-disrupting effect of the ultraviolet filter benzophenone 3 in zebrafish, Danio rerio. Environ Toxicol Chem 34:2833–2840
doi: 10.1002/etc.3129
Lammer E, Carr GJ, Wendler K, Rawlings JM, Belanger SE, Braunbeck T (2009) Is the fish embryo toxicity test (FET) with the zebrafish (Danio rerio) a potential alternative for the fish acute toxicity test? Comp Biochem Physiol, Part C 149:196–209
Lannig G, Flores JF, Sokolova IM (2006) Temperature-dependent stress response in oysters, Crassostrea virginica: pollution reduces temperature tolerance in oysters. Aquat Toxicol 79:278–287
doi: 10.1016/j.aquatox.2006.06.017
Lawrence C (2007) The husbandry of zebrafish (Danio rerio): a review. Aquaculture 269:1–20
doi: 10.1016/j.aquaculture.2007.04.077
Le Bihanic F, Morin B, Cousin X, Le Menach K, Budzinski H, Cachot J (2014a) Developmental toxicity of PAH mixtures in fish early life stages. Part I: adverse effects in rainbow trout. Environ Sci Pollut Res Int 21:13720–13731. https://doi.org/10.1007/s11356-014-2804-0
doi: 10.1007/s11356-014-2804-0
Le Bihanic F, Perrichon P, Landi L, Clérandeau C, Le Menach K, Budzinski H, Cousin X, Cachot J (2014b) Development of a reference artificial sediment for chemical testing adapted to the MELA sediment contact assay. Environ Sci Pollut Res Int 24:13689–13702. https://doi.org/10.1007/s11356-014-2607-3
doi: 10.1007/s11356-014-2607-3
Lee J, Kim S, Park YJ, Moon HB, Choi K (2018) Thyroid hormone-disrupting potentials of major benzophenones in two cell lines (GH3 and FRTL-5) and embryo-larval zebrafish. Environ Sci Technol 52(15):8858–8865
doi: 10.1021/acs.est.8b01796
Lefrançois C, Claireaux G (2003) Influence of ambient oxygenation and temperature on metabolic scope and scope for heart rate in the common sole Solea solea. Mar Ecol Prog Ser 259:273–284
doi: 10.3354/meps259273
Li AJ, Law JCF, Chow CH, Huang Y, Li Leung KSY (2018) Joint effects of multiple UV filters on zebrafish embryo development. Environ Sci Technol 52:9460–9467
doi: 10.1021/acs.est.8b02418
Lin CC, Hui MN, Cheng SH (2007) Toxicity and cardiac effects of carbaryl in early developing zebrafish (Danio rerio) embryos. Toxicol Appl Pharmacol 222(2):159–168
doi: 10.1016/j.taap.2007.04.013
Liu H, Sun P, Liu H, Yang S, Wang L, Wang Z (2015) Hepatic oxidative stress biomarker responses in freshwater fish Carassius auratus exposed to four benzophenone UV filters. Ecotox Envir Safe 119:116–122. https://doi.org/10.1016/j.ecoenv.2015.05.017
doi: 10.1016/j.ecoenv.2015.05.017
Lozano C, Givens J, Stien D, Matallana-Surget S, Lebaron P (2020) Bioaccumulation and toxicological effects of UV-filters on marine species. The Handbook of Environmental Chemistry. Springer, Berlin, Heidelberg. https://doi.org/10.1007/698_2019_442
doi: 10.1007/698_2019_442
Lucas J, Schouman A, Lyphout L, Cousin X, Lefrancois C (2014a) Allometric relationship between body mass and aerobic metabolism in zebrafish Danio rerio. J Fish Biol 84(4):1171–1178. https://doi.org/10.1111/jfb.12306
doi: 10.1111/jfb.12306
Lucas J, Perrichon P, Nouhaud M, Audras A, Leguen I, Lefrancois C (2014b) Aerobic metabolism and cardiac activity in the descendants of zebrafish exposed to pyrolytic polycyclic aromatic hydrocarbons. Environ Sci Pollut Res 21(24):13888–13897. https://doi.org/10.1007/s11356-014-3116-0
doi: 10.1007/s11356-014-3116-0
Mao F, He Y, Kushmaro A, Gin KYH (2017) Effects of benzophenone-3 on the green alga Chlamydomonas reinhardtii and the cyanobacterium Microcystis aeruginosa. Aquat Toxicol 193:1–8. https://doi.org/10.1016/j.aquatox.2017.09.029
doi: 10.1016/j.aquatox.2017.09.029
Martins D, Monteiro MS, Soares AMVM, Quintaneiro C (2017) Effects of 4-MBC and triclosan in embryos of the frog Pelophylax perezi. Chemosphere 178:325–332
doi: 10.1016/j.chemosphere.2017.03.038
McCormick MI, Nechaev IV (2002) Influence of cortisol on developmental rhythms during embryogenesis in a tropical damselfish. J Exp Zool 293(5):456–466
doi: 10.1002/jez.10138
Molins-Delgado D, Máñez M, Andreu A, Hiraldo F, Eljarrat E, Barceló D, Díaz-Cruz MS (2017) A potential new threat to wild life: presence of UV filters in bird eggs from a preserved area. Environ Sci Technol 51(19):10983–10990
doi: 10.1021/acs.est.7b03300
Montes-Grajales D, Fennix-Agudelo M, Miranda-Castro W (2017) Occurrence of personal care products as emerging chemicals of concern in water resources: a review. Sci Total Environ 595:601–614
doi: 10.1016/j.scitotenv.2017.03.286
Nesan DM, Vijayan M (2012) Embryo exposure to elevated cortisol level leads to cardiac performance dysfunction in zebrafish. Mol Cell Endocrinol 363:85–91. https://doi.org/10.1016/j.mce.2012.07.010
doi: 10.1016/j.mce.2012.07.010
OCDE (1998), Test No. 212: fish, short-term toxicity test on embryo and sac-fry stages, OECD Guidelines for the Testing of Chemicals, Section 2, Éditions OCDE, Paris, https://doi.org/10.1787/9789264070141-en .
OCDE (2013) Test No. 236: fish embryo acute toxicity (FET) test, OECD Guidelines for the Testing of Chemicals, Section 2, Éditions OCDE, Paris, https://doi.org/10.1787/9789264203709-en .
Perrichon P, Le Bihanic F, Bustamante P (2014) Influence of sediment composition on PAH toxicity using zebrafish (Danio rerio) and Japanese medaka (Oryzias latipes) embryo-larval assays. Environ Sci Pollut Res 21:13703–13719. https://doi.org/10.1007/s11356-014-3502-7
doi: 10.1007/s11356-014-3502-7
Perrichon P, Le Menach K, Akcha F, Cachot J, Budzinski H, Bustamante P (2016) Toxicity assessment of water-accommodated fractions from two different oils using a zebrafish (Danio rerio) embryo-larval bioassay with a multilevel approach. Sci Total Environ 568:952–966. https://doi.org/10.1016/j.scitotenv.2016.04.186
doi: 10.1016/j.scitotenv.2016.04.186
Pirotta G (2016) The encyclopedia of allowed sunfilters in the world. Skin Care—Househ. Pers Care Today 11:19–21
Quintaneiro C, Teixeira B, Benedé JL, Chisvert A, Soares AMVM, Monteiro MS (2019) Toxicity effects of the organic UV-filter 4-methylbenzylidene camphor in zebrafish embryos. Chemosphere 218:273–281. https://doi.org/10.1016/j.chemosphere.2018.11.096
doi: 10.1016/j.chemosphere.2018.11.096
Ramos S, Homem V, Alves A, Santos L (2015) Advances in analytical methods and occurrence of organic UV-filters in the environment — a review. Sci Total Environ 526:278–311
doi: 10.1016/j.scitotenv.2015.04.055
Ramos S, Homem V, Alves A, Santos L (2016) A review of organic UV-filters in wastewater treatment plants. Environ Int 86:24–44
doi: 10.1016/j.envint.2015.10.004
Sánchez-Quiles D, Tovar-Sánchez A (2015) Are sunscreens a new environmental risk associated with coastal tourism? Environ Int 83:158–170. https://doi.org/10.1016/j.envint.2015.06.007
doi: 10.1016/j.envint.2015.06.007
Schreurs R, Lanser P, Seinen W, Van der Burg B (2002) Estrogenic activity of UV filters determined by an in vitro reporter gene assay and an in vivo transgenic zebrafish assay. Arch Toxicol 76:257–261
doi: 10.1007/s00204-002-0348-4
Schurmann H, Steffensen JF (1997) Effects of temperature, hypoxia and activity on the metabolism of juvenile Atlantic cod. J Fish Biol 50:1166–1180
Sieratowicz A, Kaiser D, Behr M, Oetken M, Oehlmann J (2011) Acute and chronic toxicity of four frequently used UV filter substances for Desmodesmus subspicatus and Daphnia magna. J Environ Sci Health Part A 46:1311–1319. https://doi.org/10.1080/10934529.2011.602936
doi: 10.1080/10934529.2011.602936
Schlenk D, Sapozhnikova Y, Irwin MA, Xie L, Hwang W, Reddy S, Brownawell BJ, Armstrong J, Kelly M, Montagne DE, Kolodziej EP, Sedlak D, Snyder S (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. https://doi.org/10.1897/05-116R.1
doi: 10.1897/05-116R.1
Spitsbergen JM, Kent ML (2003) The state of the art of the zebrafish model for toxicology and toxicologic pathology research: advantages and current limitations. Toxicol Pathol 31:62–87. https://doi.org/10.1080/01926230390174959
doi: 10.1080/01926230390174959
Steffensen JF, Bushnell PG, Schurmann H (1994) Oxygen consumption in four species of teleosts from Greenland: no evidence of metabolic cold adaptation. Polar Biol 14:49–54
doi: 10.1007/BF00240272
Stien D, Clergeaud F, Rodrigues AMS, Lebaron K, Pillot R, Romans P, Fagervold S, Lebaron P (2019) Metabolomics reveal that octocrylene accumulates in Pocillopora damicornis tissues as fatty acid conjugates and triggers coral cell mitochondrial dysfunction. Anal Chem 91:990–995. https://doi.org/10.1021/acs.analchem.8b04187
doi: 10.1021/acs.analchem.8b04187
Thorel E, Clergeaud F, Jaugeon L, Rodirgues A, Lucas J, Stien D, Lebaron P (2020) Effect of 10 UV Filters on the Brine Shrimp Artemia salina and the Marine Microalga Tetraselmis sp. Toxics 8:29. https://doi.org/10.3390/toxics8020029
doi: 10.3390/toxics8020029
Torres T, Cunha I, Martins R, Santos MM (2016) Screening the toxicity of selected personal care products using embryo bioassays: 4-MBC, propylparaben and triclocarban. Int J Mol Sci 17:1762. https://doi.org/10.3390/ijms17101762
doi: 10.3390/ijms17101762
Tovar-Sanchez A, Sanchez-Quiles D, Basterretxea G, Benede JL, Chisvert A, Salvador A et al (2013) Sunscreen products as emerging pollutants to coastal waters. PLoS One 8(6):e65451
doi: 10.1371/journal.pone.0065451
Tsui MMP, Leung HW, Wai TC, Yamashita N, Taniyasu S, Liu W, Lam PKS, Murphy MB (2014a) 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.2014.09.013
doi: 10.1016/j.watres.2014.09.013
Tsui MMP, Leung HW, Lam PKS, Murphy MB (2014b) Seasonal occurrence, removal efficiencies and preliminary risk assessment of multiple classes of organic UV filters in wastewater treatment plants. Water Res 53:58–67
doi: 10.1016/j.watres.2014.01.014
Tsui MMP, Leung HW, Kwan BKY, Ng KY, Yamashita N, Taniyasu S, Lam PKS, Murphy MB (2015) Occurrence, distribution and ecological risk assessment of multiple classes of UV filters in marine sediments in Hong Kong and Japan. J Hazard Mater 292:180–187
doi: 10.1016/j.jhazmat.2015.03.025
Vicquelin L, Leray-Forget J, Peluhet L, LeMenach K, Deflandre B, Anschutz P, Etcheber H, Morin B, Budzinski H, Cachot J (2011) A new spiked sediment assay using embryos of the Japanese medaka specifically designed for a reliable toxicity assessment of hydrophobic chemicals. Aquat Tox 105(3–4):235–245. https://doi.org/10.1016/j.aquatox.2011.06.011
doi: 10.1016/j.aquatox.2011.06.011
Waldman RA, Grant-Kels JM (2019) The role of sunscreen in the prevention of cutaneous melanoma and nonmelanoma skin cancer. J Am Acad Dermat 80(2):574–576. https://doi.org/10.1016/j.jaad.2018.06.069
doi: 10.1016/j.jaad.2018.06.069
Zucchi S, Oggier DM, Fent K (2011) Global gene expression profile induced by the UV-filter 2-ethyl-hexyl-4-trimethoxycinnamate (EHMC) in zebrafish (Danio rerio). Environ Pollut 159:3086–3096. https://doi.org/10.1016/j.envpol.2011.04.013
doi: 10.1016/j.envpol.2011.04.013

Auteurs

Julie Lucas (J)

Sorbonne Université, CNRS, Laboratoire de Biodiversité et Biotechnologie Microbiennes, LBBM, Observatoire Océanologique, 66650, Banyuls-sur-Mer, France. julie.lucas@obs-banyuls.fr.

Valentin Logeux (V)

Sorbonne Université, CNRS, Fédération de Recherche, Observatoire Océanologique, 66650, Banyuls-sur-Mer, France.

Alice M S Rodrigues (AMS)

Sorbonne Université, CNRS, Laboratoire de Biodiversité et Biotechnologie Microbiennes, LBBM, Observatoire Océanologique, 66650, Banyuls-sur-Mer, France.

Didier Stien (D)

Sorbonne Université, CNRS, Laboratoire de Biodiversité et Biotechnologie Microbiennes, LBBM, Observatoire Océanologique, 66650, Banyuls-sur-Mer, France.

Philippe Lebaron (P)

Sorbonne Université, CNRS, Laboratoire de Biodiversité et Biotechnologie Microbiennes, LBBM, Observatoire Océanologique, 66650, Banyuls-sur-Mer, France.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH