Chronic exposure to tebuconazole alters thyroid hormones and plumage quality in house sparrows (Passer domesticus).

Agroecosystem Body condition Fungicides Passerine birds Sperm quality Sublethal effects Thyroid hormones

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:
26 Jun 2023
Historique:
received: 10 03 2023
accepted: 10 06 2023
medline: 27 6 2023
pubmed: 27 6 2023
entrez: 26 6 2023
Statut: aheadofprint

Résumé

Triazoles belong to a family of fungicides that are ubiquitous in agroecosystems due to their widespread use in crops. Despite their efficiency in controlling fungal diseases, triazoles are also suspected to affect non-target vertebrate species through the disruption of key physiological mechanisms. Most studies so far have focused on aquatic animal models, and the potential impact of triazoles on terrestrial vertebrates has been overlooked despite their relevance as sentinel species of contaminated agroecosystems. Here, we examined the impact of tebuconazole on the thyroid endocrine axis, associated phenotypic traits (plumage quality and body condition) and sperm quality in wild-caught house sparrows (Passer domesticus). We experimentally exposed house sparrows to realistic concentrations of tebuconazole under controlled conditions and tested the impact of this exposure on the levels of thyroid hormones (T3 and T4), feather quality (size and density), body condition and sperm morphology. We found that exposure to tebuconazole caused a significant decrease in T4 levels, suggesting that this azole affects the thyroid endocrine axis, although T3 levels did not differ between control and exposed sparrows. Importantly, we also found that exposed females had an altered plumage structure (larger but less dense feathers) relative to control females. The impact of tebuconazole on body condition was dependent on the duration of exposure and the sex of individuals. Finally, we did not show any effect of exposure to tebuconazole on sperm morphology. Our study demonstrates for the first time that exposure to tebuconazole can alter the thyroid axis of wild birds, impact their plumage quality and potentially affect their body condition. Further endocrine and transcriptomic studies are now needed not only to understand the underlying mechanistic effects of tebuconazole on these variables, but also to further investigate their ultimate consequences on performance (i.e. reproduction and survival).

Identifiants

pubmed: 37365357
doi: 10.1007/s11356-023-28259-5
pii: 10.1007/s11356-023-28259-5
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Andreu-Sánchez O, Paraíba LC, Jonsson CM, Carrasco JM (2012) Acute toxicity and bioconcentration of fungicide tebuconazole in zebrafish (Danio rerio). Environ Toxicol 27(2):109–116. https://doi.org/10.1002/tox.20618
doi: 10.1002/tox.20618
Angelier F, Prouteau L, Brischoux F, Chastel O, Devier M-H, Le Menach K, Martin S, Mohring B, Pardon P, Budzinski H (2023) High contamination of a sentinel vertebrate species by azoles in vineyards: a study of common blackbirds (Turdus merula) in multiple habitats in western France. Environ Pollut 316:120655. https://doi.org/10.1016/j.envpol.2022.120655
doi: 10.1016/j.envpol.2022.120655
Bartholomew GA, Cade TJ (1963) The water economy of land birds. Auk 80(4):504–539. https://doi.org/10.2307/4082856
doi: 10.2307/4082856
Becher R, Wirsel SGR (2012) Fungal cytochrome P450 sterol 14α-demethylase (CYP51) and azole resistance in plant and human pathogens. Appl Microbiol Biotechnol 95(4):825–840. https://doi.org/10.1007/s00253-012-4195-9
doi: 10.1007/s00253-012-4195-9
Bellot P, Dupont SM, Brischoux F, Budzinski H, Chastel O, Fritsch C, Lourdais O, Prouteau L, Rocchi S, Angelier F (2022) Experimental exposure to tebuconazole affects metabolism and body condition in a passerine bird, the house sparrow (Passer domesticus). Environ Toxicol Chem 41(10):2500–2511. https://doi.org/10.1002/etc.5446
doi: 10.1002/etc.5446
Bernabò I, Guardia A, Macirella R, Sesti S, Crescente A, Brunelli E (2016) Effects of long-term exposure to two fungicides, pyrimethanil and tebuconazole, on survival and life history traits of Italian tree frog (Hyla intermedia). Aquat Toxicol 172:56–66. https://doi.org/10.1016/j.aquatox.2015.12.017
doi: 10.1016/j.aquatox.2015.12.017
Bernabò I, Guardia A, Macirella R, Sesti S, Tripepi S, Brunelli E (2020) Tissues injury and pathological changes in Hyla intermedia juveniles after chronic larval exposure to tebuconazole. Ecotoxicol Environ Safety 205:111367. https://doi.org/10.1016/j.ecoenv.2020.111367
doi: 10.1016/j.ecoenv.2020.111367
Bianco AC, Kim BW (2006) Deiodinases: implications of the local control of thyroid hormone action. J Clin Invest 116(10):2571–2579. https://doi.org/10.1172/JCI29812
doi: 10.1172/JCI29812
Binev R, Simeonov R, Todorov R, Nikolov Y (2005) Pathomorphological studies following experimental acute intoxication with the triazole fungicide triticonazole in pigs. Bulgarian J Vet Med 8(3):193–198
Brischoux F, Beaugeard E, Mohring B, Parenteau C, Angelier F (2020) Short-term dehydration influences baseline but not stress-induced corticosterone levels in the house sparrow (Passer domesticus). J Exp Biol 223(3):jeb216424. https://doi.org/10.1242/jeb.216424
doi: 10.1242/jeb.216424
Capel PD, Giger W, Reichert P, Wanner O (1988) Accidental input of pesticides into the Rhine River. Environ Sci Technol 22(9):992–997. https://doi.org/10.1021/es00174a001
doi: 10.1021/es00174a001
Capen CC (1998) Correlation of mechanistic data and histopathology in the evaluation of selected toxic endpoints of the endocrine system. Toxicol Lett 102-103:405–409. https://doi.org/10.1016/S0378-4274(98)00244-6
doi: 10.1016/S0378-4274(98)00244-6
Chastel O, Lacroix A, Kersten M (2003) Pre-breeding energy requirements: thyroid hormone, metabolism and the timing of reproduction in house sparrows Passer domesticus. J Avian Biol 34(3):298–306. https://doi.org/10.1034/j.1600-048X.2003.02528.x
doi: 10.1034/j.1600-048X.2003.02528.x
Cherel Y, Leloup J, Maho L, Yvon. (1988) Fasting in king penguin. II. Hormonal and metabolic changes during molt. Am J Physiol-Reg Integr Compar Physiology 254(2):R178–R184
doi: 10.1152/ajpregu.1988.254.2.R178
Cherel Y, Durant JM, Lacroix A (2004) Plasma thyroid hormone pattern in king penguin chicks: a semi-altricial bird with an extended posthatching developmental period. Gen Compar Endocrinol 136(3):398–405. https://doi.org/10.1016/j.ygcen.2004.02.003
doi: 10.1016/j.ygcen.2004.02.003
Daum G, Lees ND, Bard M, Dickson R (1998) Biochemistry, cell biology and molecular biology of lipids of Saccharomyces cerevisiae. Yeast 14(16):1471–1510. https://doi.org/10.1002/(SICI)1097-0061(199812)14:16<1471::AID-YEA353>3.0.CO;2-Y
doi: 10.1002/(SICI)1097-0061(199812)14:16<1471::AID-YEA353>3.0.CO;2-Y
Davis J, Davis BS (1954) The annual gonad and thyroid cycles of the English sparrow in Southern California. Condor 56(6):328–345. https://doi.org/10.2307/1365019
doi: 10.2307/1365019
Dawson A, Hinsley SA, Ferns PN, Bonser RHC, Eccleston L (2000) Rate of moult affects feather quality: a mechanism linking current reproductive effort to future survival. Proc Royal Soc London Series B: Biol Sci 267(1457):2093–2098. https://doi.org/10.1098/rspb.2000.1254
doi: 10.1098/rspb.2000.1254
De Cock M, de Boer MR, Lamoree M, Legler J, van de Bor M (2014) Prenatal exposure to endocrine disrupting chemicals in relation to thyroid hormone levels in infants – a Dutch prospective cohort study. Environ Health 13(1):106. https://doi.org/10.1186/1476-069X-13-106
doi: 10.1186/1476-069X-13-106
Decuypere E, Verheyen G (1986) Physiological basis of induced moulting and tissue regeneration in fowls. World’s Poultry Sci J 42(1):56–68. https://doi.org/10.1079/WPS19860006
doi: 10.1079/WPS19860006
Dentice M, Salvatore D (2011) Local impact of thyroid hormone inactivation. J Endocr 209(3):273–282. https://doi.org/10.1530/JOE-11-0002
doi: 10.1530/JOE-11-0002
Désert M, Ravier S, Gille G, Quinapallo A, Armengaud A, Pochet G et al (2018) Spatial and temporal distribution of current-use pesticides in ambient air of Provence-Alpes-Côte-d’Azur Region and Corsica, France. Atmos Environ 192:241–256. https://doi.org/10.1016/j.atmosenv.2018.08.054
doi: 10.1016/j.atmosenv.2018.08.054
DesRochers DW, Reed JM, Awerman J, Kluge JA, Wilkinson J, van Griethuijsen LI, Aman J, Romero LM (2009) Exogenous and endogenous corticosterone alter feather quality. Compar Biochem Physiol Part A: Mol Integr Physiol 152(1):46–52. https://doi.org/10.1016/j.cbpa.2008.08.034
doi: 10.1016/j.cbpa.2008.08.034
Draskau MK, Boberg J, Taxvig C, Pedersen M, Frandsen HL, Christiansen S, Svingen T (2019) In vitro and in vivo endocrine disrupting effects of the azole fungicides triticonazole and flusilazole. Environ Pollut 255:113309. https://doi.org/10.1016/j.envpol.2019.113309
doi: 10.1016/j.envpol.2019.113309
Elliott KH, Welcker J, Gaston AJ, Hatch SA, Palace V, Hare JF, Speakman JR, Anderson WG (2013) Thyroid hormones correlate with resting metabolic rate, not daily energy expenditure, in two charadriiform seabirds. Biol Open 2(6):580–586. https://doi.org/10.1242/bio.20134358
doi: 10.1242/bio.20134358
Fernández-Vizcaíno E, Fernández de Mera IG, Mougeot F, Mateo R, Ortiz-Santaliestra ME (2020) Multi-level analysis of exposure to triazole fungicides through treated seed ingestion in the red-legged partridge. Environ Res 189:109928. https://doi.org/10.1016/j.envres.2020.109928
doi: 10.1016/j.envres.2020.109928
Fernández-Vizcaíno E, Ortiz-Santaliestra ME, Fernández-Tizón M, Mateo R, Camarero PR, Mougeot F (2022) Bird exposure to fungicides through the consumption of treated seeds: a study of wild red-legged partridges in Central Spain. Environ Pollut 292:118335. https://doi.org/10.1016/j.envpol.2021.118335
doi: 10.1016/j.envpol.2021.118335
Fisher MC, Henk D, A., Briggs, C. J., Brownstein, J. S., Madoff, L. C., McCraw, S. L., & Gurr, S. J. (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484(7393):186–194. https://doi.org/10.1038/nature10947
doi: 10.1038/nature10947
Girndt A, Cockburn G, Sánchez-Tójar A, Løvlie H, Schroeder J (2017) Method matters: experimental evidence for shorter avian sperm in faecal compared to abdominal massage samples. PLoS One 12(8):e0182853. https://doi.org/10.1371/journal.pone.0182853
doi: 10.1371/journal.pone.0182853
Girndt A, Cockburn G, Sánchez-Tójar A, Hertel M, Burke T, Schroeder J (2019) Male age and its association with reproductive traits in captive and wild house sparrows. J Evol Biol 32(12):1432–1443. https://doi.org/10.1111/jeb.13542
doi: 10.1111/jeb.13542
Goetz AK, Ren H, Schmid JE, Blystone CR, Thillainadarajah I, Best DS, Nichols HP, Strader LF, Wolf DC, Narotsky MG, Rockett JC, Dix DJ (2007) Disruption of testosterone homeostasis as a mode of action for the reproductive toxicity of triazole fungicides in the male rat. Toxicol Sci 95(1):227–239. https://doi.org/10.1093/toxsci/kfl124
doi: 10.1093/toxsci/kfl124
Groscolas R, Cherel Y (1992) How to molt while fasting in the cold: the metabolic and hormonal adaptations of emperor and king penguins. Ornis Scand 23(3):328. https://doi.org/10.2307/3676657
doi: 10.2307/3676657
Groscolas R, Leloup J (1986) The endocrine control of reproduction and molt in male and female emperor (Aptenodytes forsteri) and adelie (Pygoscelis adeliae) penguins. Gen Compar Endocr 63(2):264–274. https://doi.org/10.1016/0016-6480(86)90164-4
doi: 10.1016/0016-6480(86)90164-4
Grote K, Niemann L, Selzsam B, Haider W, Gericke C, Herzler M, Chahoud I (2008) Epoxiconazole causes changes in testicular histology and sperm production in the Japanese quail (Coturnix coturnix japonica). Environ Toxicol Chem 27(11):2368. https://doi.org/10.1897/08-048.1
doi: 10.1897/08-048.1
Hahn TP, Swingle J, Wingfield JC, Ramenofsky M (1992) Adjustments of the prebasic molt schedule in birds. Ornis Scand:314–321
Hall R, Amos J, Garry R, Buxton RL (1970) Thyroid-stimulating hormone response to synthetic thyrotrophin-releasing hormone in man. BMJ 2(5704):274–277. https://doi.org/10.1136/bmj.2.5704.274
doi: 10.1136/bmj.2.5704.274
Harris ARC, Christianson D, Smith MS, Fang S-L, Braverman LE, Vagenakis AG (1978) The physiological role of thyrotropin-releasing hormone in the regulation of thyroid-stimulating hormone and prolactin secretion in the rat. J Clin Investig 61(2):441–448. https://doi.org/10.1172/JCI108955
doi: 10.1172/JCI108955
Helfenstein F, Podevin M, Richner H (2010) Sperm morphology, swimming velocity, and longevity in the house sparrow Passer domesticus. Behav Ecol Sociobiol 64(4):557–565. https://doi.org/10.1007/s00265-009-0871-x
doi: 10.1007/s00265-009-0871-x
Hennin HL, Legagneux P, Bêty J, Williams TD, Grant Gilchrist H, Baker TM, Love OP (2015) Pre-breeding energetic management in a mixed-strategy breeder. Oecologia 177(1):235–243. https://doi.org/10.1007/s00442-014-3145-x
doi: 10.1007/s00442-014-3145-x
Huang T, Zhao Y, He J, Cheng H, Martyniuk CJ (2022) Endocrine disruption by azole fungicides in fish: a review of the evidence. Sci Total Environ 822:153412. https://doi.org/10.1016/j.scitotenv.2022.153412
doi: 10.1016/j.scitotenv.2022.153412
Humann-Guilleminot S, Clément S, Desprat J, Binkowski ŁJ, Glauser G, Helfenstein F (2019a) A large-scale survey of house sparrows feathers reveals ubiquitous presence of neonicotinoids in farmlands. Sci Total Environ 660:1091–1097. https://doi.org/10.1016/j.scitotenv.2019.01.068
doi: 10.1016/j.scitotenv.2019.01.068
Humann-Guilleminot S, Tassin de Montaigu C, Sire J, Grünig S, Gning O, Glauser G, Vallat A, Helfenstein F (2019b) A sublethal dose of the neonicotinoid insecticide acetamiprid reduces sperm density in a songbird. Environ Res 177:108589. https://doi.org/10.1016/j.envres.2019.108589
doi: 10.1016/j.envres.2019.108589
Jacobsen PR, Axelstad M, Boberg J, Isling LK, Christiansen S, Mandrup KR, Berthelsen LO, Vinggaard AM, Hass U (2012) Persistent developmental toxicity in rat offspring after low dose exposure to a mixture of endocrine disrupting pesticides. Reprod Toxicol 34(2):237–250. https://doi.org/10.1016/j.reprotox.2012.05.099
doi: 10.1016/j.reprotox.2012.05.099
Jenni L, Winkler R (2020) The biology of moult in birds. Bloomsbury Publishing
Jenni-Eiermann S, Jenni L, Piersma T (2002) Temporal uncoupling of thyroid hormones in Red Knots: T3 peaks in cold weather, T4 during moult. J Ornithol 143(3):331–340. https://doi.org/10.1046/j.1439-0361.2002.02011.x
doi: 10.1046/j.1439-0361.2002.02011.x
Jenni-Eiermann S, Helfenstein F, Vallat A, Glauser G, Jenni L (2015) Corticosterone: effects on feather quality and deposition into feathers. Methods Ecol Evol 6(2):237–246. https://doi.org/10.1111/2041-210X.12314
doi: 10.1111/2041-210X.12314
Kahle M, Buerge IJ, Hauser A, Müller MD, Poiger T (2008) Azole fungicides: occurrence and fate in wastewater and surface waters. Environ Sci Technol 42(19):7193–7200. https://doi.org/10.1021/es8009309
doi: 10.1021/es8009309
Kalogridi EC, Christophoridis C, Bizani E, Drimaropoulou G, Fytianos K (2014) Part II: temporal and spatial distribution of multiclass pesticide residues in lake sediments of northern Greece: application of an optimized MAE-LC-MS/MS pretreatment and analytical method. Environ Sci Pollut Res 21:7252–7262. https://doi.org/10.1007/s11356-014-2794-y
doi: 10.1007/s11356-014-2794-y
Kuenzel WJ (2003) Neurobiology of molt in avian species. Poultry Sci 82(6):981–991
doi: 10.1093/ps/82.6.981
Kjærstad, M. B., Taxvig, C., Hass, U., Axelstad, M., Metzdorff, S., & Vinggaard, A. M. (2007). Effects of azole fungicides on the function of sex and thyroid hormones.
Kvalnes T, Ringsby TH, Jensen H, Sæther B-E (2013) Correlates of egg size variation in a population of house sparrow Passer domesticus. Oecologia 171(2):391–402. https://doi.org/10.1007/s00442-012-2437-2
doi: 10.1007/s00442-012-2437-2
Li S, Wu Q, Sun Q, Coffin S, Gui W, Zhu G (2019) Parental exposure to tebuconazole causes thyroid endocrine disruption in zebrafish and developmental toxicity in offspring. Aquatic Toxicol 211:116–123. https://doi.org/10.1016/j.aquatox.2019.04.002
doi: 10.1016/j.aquatox.2019.04.002
Liang X, Yu L, Gui W, Zhu G (2015) Exposure to difenoconazole causes changes of thyroid hormone and gene expression levels in zebrafish larvae. Environ Toxicol Pharm 40(3):983–987. https://doi.org/10.1016/j.etap.2015.10.005
doi: 10.1016/j.etap.2015.10.005
Lopez-Antia A, Ortiz-Santaliestra ME, Mougeot F, Mateo R (2013) Experimental exposure of red-legged partridges (Alectoris rufa) to seeds coated with imidacloprid, thiram and difenoconazole. Ecotoxicology 22(1):125–138. https://doi.org/10.1007/s10646-012-1009-x
doi: 10.1007/s10646-012-1009-x
Lopez-Antia A, Feliu J, Camarero PR, Ortiz-Santaliestra ME, Mateo R (2016) Risk assessment of pesticide seed treatment for farmland birds using refined field data. J Appl Ecol 53(5):1373–1381. https://doi.org/10.1111/1365-2664.12668
doi: 10.1111/1365-2664.12668
Lopez-Antia A, Ortiz-Santaliestra ME, Mougeot F, Camarero PR, Mateo R (2018) Brood size is reduced by half in birds feeding on flutriafol-treated seeds below the recommended application rate. Environ Pollut 243:418–426. https://doi.org/10.1016/j.envpol.2018.08.078
doi: 10.1016/j.envpol.2018.08.078
Lopez-Antia A, Ortiz-Santaliestra ME, Mougeot F, Camarero PR, Mateo R (2021) Birds feeding on tebuconazole treated seeds have reduced breeding output. Environ Pollut 271:116292. https://doi.org/10.1016/j.envpol.2020.116292
doi: 10.1016/j.envpol.2020.116292
Machado-Neves M, Neto MJO, Miranda DC, Souza ACF, Castro MM, Sertorio MN, Carvalho TF, Matta SLP, Freitas MB (2018) Dietary exposure to tebuconazole affects testicular and epididymal histomorphometry in frugivorous bats. Bull Environ Cont Toxicol 101(2):197–204. https://doi.org/10.1007/s00128-018-2377-6
doi: 10.1007/s00128-018-2377-6
McNabb FMA (2007) The hypothalamic-pituitary-thyroid (HPT) axis in birds and its role in bird development and reproduction. Cri Rev Toxicol 37(1-2):163–193. https://doi.org/10.1080/10408440601123552
doi: 10.1080/10408440601123552
Mohanty B, Pandey SP, Tsutsui K (2017) Thyroid disrupting pesticides impair the hypothalamic-pituitary-testicular axis of a wildlife bird, Amandava amandava. Reprod Toxicol 71:32–41. https://doi.org/10.1016/j.reprotox.2017.04.006
doi: 10.1016/j.reprotox.2017.04.006
Nolan V, Ketterson ED, Ziegenfus C, Cullen DP, Chandler CR (1992) Testosterone and avian life histories: effects of experimentally elevated testosterone on prebasic molt and survival in male dark-eyed juncos. Condor 94(2):364–370. https://doi.org/10.2307/1369209
doi: 10.2307/1369209
Ortiz-Santaliestra ME, Alcaide V, Camarero PR, Mateo R, Mougeot F (2020) Egg overspray with herbicides and fungicides reduces survival of red-legged partridge chicks. Environ Sci Technol 54(19):12402–12411. https://doi.org/10.1021/acs.est.0c04203
doi: 10.1021/acs.est.0c04203
Pandey SP, Mohanty B (2015) The neonicotinoid pesticide imidacloprid and the dithiocarbamate fungicide mancozeb disrupt the pituitary–thyroid axis of a wildlife bird. Chemosphere 122:227–234. https://doi.org/10.1016/j.chemosphere.2014.11.061
doi: 10.1016/j.chemosphere.2014.11.061
Pelosi C, Thiel P, Bart S, Amossé J, Jean-Jacques J, Thoisy J-C, Crouzet O (2021) The contributions of enchytraeids and earthworms to the soil mineralization process in soils with fungicide. Ecotoxicology 30(9):1910–1921. https://doi.org/10.1007/s10646-021-02452-z
doi: 10.1007/s10646-021-02452-z
Pereira VR, Pereira DR, de Melo Tavares Vieira KC, Ribas VP, Constantino CJL, Antunes PA, Favareto APA (2019) Sperm quality of rats exposed to difenoconazole using classical parameters and surface-enhanced Raman scattering: classification performance by machine learning methods. Environ Sci Pollut Res 26:35253–35265. https://doi.org/10.1007/s11356-019-06407-0
doi: 10.1007/s11356-019-06407-0
Pérez JH, Meddle SL, Wingfield JC, Ramenofsky M (2018) Effects of thyroid hormone manipulation on pre-nuptial molt, luteinizing hormone and testicular growth in male white-crowned sparrows (Zonotrichia leuchophrys gambelii). Gen Compar Endocr 255:12–18. https://doi.org/10.1016/j.ygcen.2017.09.025
doi: 10.1016/j.ygcen.2017.09.025
Pirahanchi Y, Toro F, Jialal I (2018) Physiology, thyroid stimulating hormone. StatPearls Publishing, StatPearls.  http://www.ncbi.nlm.nih.gov/books/NBK499850/
Poulsen R, Luong X, Hansen M, Styrishave B, Hayes T (2015) Tebuconazole disrupts steroidogenesis in Xenopus laevis. Aquatic Toxicol 168:28–37. https://doi.org/10.1016/j.aquatox.2015.09.008
doi: 10.1016/j.aquatox.2015.09.008
Raby M, Maloney E, Poirier DG, Sibley PK (2019) Acute effects of binary mixtures of imidacloprid and tebuconazole on 4 freshwater invertebrates. Environ Toxicol Chem 38(5):1093–1103. https://doi.org/10.1002/etc.4386
doi: 10.1002/etc.4386
Ribas e Ribas RAD, Spolti P, Del Ponte EM, Donato KZ, Schrekker H, Fuentefria AM (2016) Is the emergence of fungal resistance to medical triazoles related to their use in the agroecosystems? A mini review. Brazil J Microbiol 47(4):793–799. https://doi.org/10.1016/j.bjm.2016.06.006
doi: 10.1016/j.bjm.2016.06.006
Rico A, Sabater C, Castillo M-Á (2016) Lethal and sub-lethal effects of five pesticides used in rice farming on the earthworm Eisenia fetida. Ecotoxicol Environ Safety 127:222–229. https://doi.org/10.1016/j.ecoenv.2016.02.004
doi: 10.1016/j.ecoenv.2016.02.004
Robinson RA (2004) The diet of seed-eating birds on lowland farmland. Bri Birds 97(9):464–467
Rokbani O, Fattouch S, Chakir A, Roth E (2019) Heterogeneous oxidation of two triazole pesticides (diniconazole and tebuconazole) by OH-radicals and ozone. Sci Total Environ 694:133745. https://doi.org/10.1016/j.scitotenv.2019.133745
doi: 10.1016/j.scitotenv.2019.133745
Sancho E, Villarroel MJ, Fernández C, Andreu E, Ferrando MD (2010) Short-term exposure to sublethal tebuconazole induces physiological impairment in male zebrafish (Danio rerio). Ecotoxicol Environ Safety 73(3):370–376. https://doi.org/10.1016/j.ecoenv.2009.09.020
doi: 10.1016/j.ecoenv.2009.09.020
Saxena AK, Devillers J, Bhunia SS, Bro E (2015) Modelling inhibition of avian aromatase by azole pesticides. SAR and QSAR Environ Res 26(7-9):757–782. https://doi.org/10.1080/1062936X.2015.1090749
doi: 10.1080/1062936X.2015.1090749
Siefferman L, Liu M, Navara KJ, Mendonça MT, Hill GE (2013) Effect of prenatal and natal administration of testosterone on production of structurally based plumage coloration. Physiol Biochem Zool 86(3):323–332. https://doi.org/10.1086/670383
doi: 10.1086/670383
Stoehr AM, Hill GE (2001) The effects of elevated testosterone on plumage hue in male house finches. J Avian Biol 32(2):153–158. https://doi.org/10.1034/j.1600-048X.2001.320208.x
doi: 10.1034/j.1600-048X.2001.320208.x
Stoker TE, Ferrell JM, Laws SC, Cooper RL, Buckalew A (2006) Evaluation of ammonium perchlorate in the endocrine disruptor screening and testing program’s male pubertal protocol: ability to detect effects on thyroid endpoints. Toxicology 228(1):58–65. https://doi.org/10.1016/j.tox.2006.08.026
doi: 10.1016/j.tox.2006.08.026
Strange RN, Scott PR (2005) Plant disease: a threat to global food security. Ann Rev Phytopathol 43(1):83–116. https://doi.org/10.1146/annurev.phyto.43.113004.133839
doi: 10.1146/annurev.phyto.43.113004.133839
Swaddle JP, Witter MS, Cuthill IC, Budden A, McCowen P (1996) Plumage condition affects flight performance in common starlings: implications for developmental homeostasis, abrasion and moult. J Avian Biol 27(2):103. https://doi.org/10.2307/3677139
doi: 10.2307/3677139
Swaileh KM, Sansur R (2006) Monitoring urban heavy metal pollution using the house sparrow (Passer domesticus). J Environ Monitor 8(1):209–213. https://doi.org/10.1039/B510635D
doi: 10.1039/B510635D
Taxvig C, Hass U, Axelstad M, Dalgaard M, Boberg J, Andeasen HR, Vinggaard AM (2007) Endocrine-disrupting activities in vivo of the fungicides tebuconazole and epoxiconazole. Toxicol Sci 100(2):464–473. https://doi.org/10.1093/toxsci/kfm227
doi: 10.1093/toxsci/kfm227
Tokumoto J, Danjo M, Kobayashi Y, Kinoshita K, Omotehara T, Tatsumi A, Hashiguchi M, Sekijima T, Kamisoyama H, Yokoyama T, Kitagawa H, Hoshi N (2013) Effects of exposure to clothianidin on the reproductive system of male quails. J Vet Med Sci 75(6):755–760. https://doi.org/10.1292/jvms.12-0544
doi: 10.1292/jvms.12-0544
Vézina F, Gustowska A, Jalvingh KM, Chastel O, Piersma T (2009) Hormonal correlates and thermoregulatory consequences of molting on metabolic rate in a northerly wintering shorebird. Physiol Biochem Zool 82(2):129–142
doi: 10.1086/596512
Voitkevich, A. A. E. (1966). The feathers and plumage of birds. The feathers and plumage of birds.
Warrilow AG, Parker JE, Kelly DE, Kelly SL (2013) Azole affinity of sterol 14α-demethylase (CYP51) enzymes from Candida albicans and Homo sapiens. Antimicr Agents Chemother 57(3):1352–1360. https://doi.org/10.1128/AAC.02067-12
doi: 10.1128/AAC.02067-12
Wilson AC, Farner DS (1960) The annual cycle of thyroid activity in white-crowned sparrows of Eastern Washington. Condor 62(6):414–425. https://doi.org/10.2307/1365589
doi: 10.2307/1365589
Yang H, Zhang W, Kong Q, Liu H, Sun R, Lin B, Zhang H, Xi Z (2013) Effects of pubertal exposure to thiazole-Zn on thyroid function and development in female rats. Food Chem Toxicol 53:100–104. https://doi.org/10.1016/j.fct.2012.11.003
doi: 10.1016/j.fct.2012.11.003
Yang J-D, Liu S-H, Liao M-H, Chen R-M, Liu P-Y, Ueng T-H (2018) Effects of tebuconazole on cytochrome P450 enzymes, oxidative stress, and endocrine disruption in male rats. Environ Toxicol 33(8):899–907. https://doi.org/10.1002/tox.22575
doi: 10.1002/tox.22575
Yu L, Chen M, Liu Y, Gui W, Zhu G (2013) Thyroid endocrine disruption in zebrafish larvae following exposure to hexaconazole and tebuconazole. Aquat Toxicol 138-139:35–42. https://doi.org/10.1016/j.aquatox.2013.04.001
doi: 10.1016/j.aquatox.2013.04.001
Zarn JA, Brüschweiler BJ, Schlatter JR (2003) Azole fungicides affect mammalian steroidogenesis by inhibiting sterol 14 alpha-demethylase and aromatase. Environ Health Persp 111(3):255–261. https://doi.org/10.1289/ehp.5785
doi: 10.1289/ehp.5785
Zhang W, Chen L, Xu Y, Deng Y, Zhang L, Qin Y, Wang Z, Liu R, Zhou Z, Diao J (2019) Amphibian (Rana nigromaculata) exposed to cyproconazole: changes in growth index, behavioral endpoints, antioxidant biomarkers, thyroid and gonad development. Aquat Toxicol 208:62–70. https://doi.org/10.1016/j.aquatox.2018.12.015
doi: 10.1016/j.aquatox.2018.12.015
Zubrod JP, Bundschuh M, Arts G, Brühl CA, Imfeld G, Knäbel A, Payraudeau S, Rasmussen JJ, Rohr J, Scharmüller A, Smalling K, Stehle S, Schulz R, Schäfer RB (2019) Fungicides: an overlooked pesticide class? Environ Sci Technol 53(7):3347–3365. https://doi.org/10.1021/acs.est.8b04392
doi: 10.1021/acs.est.8b04392

Auteurs

Pauline Bellot (P)

Centre d'Etudes Biologiques de Chizé, UMR 7372, CNRS-La Rochelle Université, 79360, Villiers en Bois, France. Pauline.bellot@cebc.cnrs.fr.

François Brischoux (F)

Centre d'Etudes Biologiques de Chizé, UMR 7372, CNRS-La Rochelle Université, 79360, Villiers en Bois, France.

Hélène Budzinski (H)

CNRS-EPOC, UMR 5805, LPTC Research Group, University of Bordeaux, 33400, Talence, France.

Sophie M Dupont (SM)

BOREA, MNHN, CNRS 8067, SU, IRD 207, UCN, UA, 97233, Schoelcher, Martinique, France.
LIENSs, UMR 7266 CNRS-La Rochelle Université, 2 Rue Olympe de Gouges, 17000, La Rochelle, France.

Clémentine Fritsch (C)

Laboratoire Chrono-Environnement, UMR 6249, CNRS/Université de Franche-Comté, F-25000, Besançon, France.

Sydney F Hope (SF)

Centre d'Etudes Biologiques de Chizé, UMR 7372, CNRS-La Rochelle Université, 79360, Villiers en Bois, France.

Bruno Michaud (B)

Centre d'Etudes Biologiques de Chizé, UMR 7372, CNRS-La Rochelle Université, 79360, Villiers en Bois, France.

Marie Pallud (M)

Centre d'Etudes Biologiques de Chizé, UMR 7372, CNRS-La Rochelle Université, 79360, Villiers en Bois, France.

Charline Parenteau (C)

Centre d'Etudes Biologiques de Chizé, UMR 7372, CNRS-La Rochelle Université, 79360, Villiers en Bois, France.

Louise Prouteau (L)

CNRS-EPOC, UMR 5805, LPTC Research Group, University of Bordeaux, 33400, Talence, France.

Steffi Rocchi (S)

Laboratoire Chrono-Environnement, UMR 6249, CNRS/Université de Franche-Comté, F-25000, Besançon, France.

Frédéric Angelier (F)

Centre d'Etudes Biologiques de Chizé, UMR 7372, CNRS-La Rochelle Université, 79360, Villiers en Bois, France.

Classifications MeSH