Natural cortisol production is not linked to the sexual fate of European sea bass.

Cortisol European sea bass Sex determination Sex differentiation Temperature

Journal

Fish physiology and biochemistry
ISSN: 1573-5168
Titre abrégé: Fish Physiol Biochem
Pays: Netherlands
ID NLM: 100955049

Informations de publication

Date de publication:
Aug 2022
Historique:
received: 06 01 2022
accepted: 14 07 2022
pubmed: 3 8 2022
medline: 20 8 2022
entrez: 2 8 2022
Statut: ppublish

Résumé

In this study, we aimed to investigate the relationship between cortisol and the determination of sexual fate in the commercially important European sea bass (Dicentrarchus labrax). To test our hypothesis, we designed two temperature-based experiments (19 ℃, 21 ℃ and 23 ℃, experiment 1; 16 ℃ and 21 ℃, experiment 2) to assess the effects of these thermal treatments on European sea bass sex determination and differentiation. In the fish from the first experiment, we evaluated whether blood cortisol levels and expression of stress key regulatory genes were different between differentiating (149 to 183 dph) males and females. In the second experiment, we assessed whether cortisol accumulated in scales over time during the labile period for sex determination as well as the neuroanatomical localisation of brain cells expressing brain aromatase (cyp19a1b) and corticotropin-releasing factor (crf) differed between males and females undergoing molecular sex differentiation (117 to 124 dph). None of the gathered results allowed to detect differences between males and females regarding cortisol production and regulatory mechanisms. Altogether, our data provide strong physiological, molecular and histochemical evidence, indicating that in vivo cortisol regulation has no major effects on the sex of European sea bass.

Identifiants

pubmed: 35917042
doi: 10.1007/s10695-022-01104-1
pii: 10.1007/s10695-022-01104-1
doi:

Substances chimiques

Hydrocortisone WI4X0X7BPJ

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1117-1135

Subventions

Organisme : European Maritime and Fisheries Fund
ID : 4320175237

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer Nature B.V.

Références

Aerts J, Metz JR, Ampe B et al (2015) Scales tell a story on the stress history of fish. PLoS One 10:e0123411. https://doi.org/10.1371/journal.pone.0123411
doi: 10.1371/journal.pone.0123411 pubmed: 25922947 pmcid: 4414496
Alderman SL, Bernier NJ (2007) Localization of corticotropin-releasing factor, urotensin I, and CRF-binding protein gene expression in the brain of the zebrafish, Danio rerio. J Comp Neurol 502:783–793. https://doi.org/10.1002/cne.21332
doi: 10.1002/cne.21332 pubmed: 17436299
Alfonso S, Sadoul B, Gesto M et al (2019) Coping styles in European sea bass: the link between boldness, stress response and neurogenesis. Physiol Behav 207:76–85. https://doi.org/10.1016/j.physbeh.2019.04.020
doi: 10.1016/j.physbeh.2019.04.020 pubmed: 31047951
Alfonso S, Gesto M, Sadoul B (2021) Temperature increase and its effects on fish stress physiology in the context of global warming. J Fish Biol 98:1496–1508. https://doi.org/10.1111/jfb.14599
doi: 10.1111/jfb.14599 pubmed: 33111333
Bessa E, Sadoul B, Mckenzie DJ, Geffroy B (2021) Group size, temperature and body size modulate the effects of social hierarchy on basal cortisol levels in fishes. Horm Behav 136:105077. https://doi.org/10.1016/j.yhbeh.2021.105077
doi: 10.1016/j.yhbeh.2021.105077 pubmed: 34656822
Bull JJ (1983) Evolution of sex determining mechanisms. The Benjamin/Cummings Publishing Company, Inc
Castañeda Cortés DC, Padilla LFA, Langlois VS et al (2019) The central nervous system acts as a transducer of stress-induced masculinization through corticotropin-releasing hormone B. Development 146:dev172866. https://doi.org/10.1242/dev.172866
doi: 10.1242/dev.172866 pubmed: 30936180
Castelli MA, Whiteley SL, Georges A, Holleley CE (2020) Cellular calcium and redox regulation: the mediator of vertebrate environmental sex determination? Biol Rev 95:680–695. https://doi.org/10.1111/brv.12582
doi: 10.1111/brv.12582 pubmed: 32027076
Castelli M, Georges A, Holleley CE (2021) Corticosterone does not have a role in temperature sex reversal in the central bearded dragon (Pogona vitticeps). J Exp Zool Part A Ecol Integr Physiol 335:301–310. https://doi.org/10.1002/jez.2441
doi: 10.1002/jez.2441
Cerdá-Reverter JM, Zanuy S, Muñoz-Cueto JA (2001a) Cytoarchitectonic study of the brain of a perciform species, the sea bass (Dicentrarchus labrax). I. The telencephalon. J Morphol 247:217–228. https://doi.org/10.1002/1097-4687(200103)247:3%3c217::AID-JMOR1013%3e3.0.CO;2-U
doi: 10.1002/1097-4687(200103)247:3<217::AID-JMOR1013>3.0.CO;2-U pubmed: 11223929
Cerdá-Reverter JM, Zanuy S, Muñoz-Cueto JA (2001b) Cytoarchitectonic study of the brain of a perciform species, the sea bass (Dicentrarchus labrax). II. The diencephalon. J Morphol 247:229–251. https://doi.org/10.1002/1097-4687(200103)247:3%3c229::AID-JMOR1014%3e3.0.CO;2-K
doi: 10.1002/1097-4687(200103)247:3<229::AID-JMOR1014>3.0.CO;2-K pubmed: 11223930
Cerdá-Reverter JM, Muriach B, Zanuy S, Muñoz-Cueto JA (2008) A cytoarchitectonic study of the brain of a perciform species, the sea bass (Dicentrarchus labrax): the midbrain and hindbrain. Acta Histochem 110:433–450. https://doi.org/10.1016/j.acthis.2008.01.001
doi: 10.1016/j.acthis.2008.01.001 pubmed: 18406450
Core Team R (2020) R: a language and environment for statistical computing
Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208:191–364. https://doi.org/10.1016/S0044-8486(02)00057-1
doi: 10.1016/S0044-8486(02)00057-1
Diotel N, Le Page Y, Mouriec K et al (2010) Aromatase in the brain of teleost fish: expression, regulation and putative functions. Front Neuroendocrinol 31:172–192. https://doi.org/10.1016/j.yfrne.2010.01.003
doi: 10.1016/j.yfrne.2010.01.003 pubmed: 20116395
Diotel N, Vaillant C, Kah O, Pellegrini E (2016) Mapping of brain lipid binding protein (Blbp) in the brain of adult zebrafish, co-expression with aromatase B and links with proliferation. Gene Expr Patterns 20:42–54. https://doi.org/10.1016/j.gep.2015.11.003
doi: 10.1016/j.gep.2015.11.003 pubmed: 26611722
Escobar S, Rocha A, Felip A et al (2016) Leptin receptor gene in the European sea bass (Dicentrarchus labrax): cloning, phylogeny, tissue distribution and neuroanatomical organization. Gen Comp Endocrinol 229:100–111. https://doi.org/10.1016/j.ygcen.2016.03.017
doi: 10.1016/j.ygcen.2016.03.017 pubmed: 26979276
Geffroy B, Douhard M (2019) The adaptive sex in stressful environments. Trends Ecol Evol 34:628–640. https://doi.org/10.1016/j.tree.2019.02.012
doi: 10.1016/j.tree.2019.02.012 pubmed: 30952545
Geffroy B (2018) RNA-Seq juvéniles de bar: Projet 3S (Seabass, Sex and Stress)
Geffroy B, Gesto M, Clota F et al (2021b) Parental selection for growth and early-life low stocking density increase the female-to-male ratio in European sea bass. Sci Rep 11:1–14. https://doi.org/10.1038/s41598-021-93116-9
doi: 10.1038/s41598-021-93116-9
Geffroy B, Besson M, Sánchez-Baizán N, Clota F, Goikoetxea A, Sadoul B, Ruelle F, Blanc MO, Parrinello H, Hermet S, Blondeau-Bidet E (2021a) Unraveling the genotype by environment interaction in a thermosensitive fish with a polygenic sex determination system. Proc Natl Acad Sci 118(50). https://doi.org/10.1073/pnas.2112660118
Goikoetxea A, Todd EV, Gemmell NJ (2017) Stress and sex: does cortisol mediate sex change in fish? Reproduction 154:R149–R160. https://doi.org/10.1530/REP-17-0408
doi: 10.1530/REP-17-0408 pubmed: 28890443
Goikoetxea A, Sadoul B, Blondeau-Bidet E et al (2021) Genetic pathways underpinning hormonal stress responses in fish exposed to short- and long-term warm ocean temperatures. Ecol Indic 120:106937. https://doi.org/10.1016/j.ecolind.2020.106937
doi: 10.1016/j.ecolind.2020.106937
Grima L, Chatain B, Ruelle F et al (2010) In search for indirect criteria to improve feed utilization efficiency in sea bass (Dicentrarchus labrax). Aquaculture 302:169–174. https://doi.org/10.1016/j.aquaculture.2010.02.016
doi: 10.1016/j.aquaculture.2010.02.016
Hattori RS, Fernandino JI, Kishii A et al (2009) Cortisol-induced masculinization: does thermal stress affect gonadal fate in pejerrey, a teleost fish with temperature-dependent sex determination? PLoS One 4:e6548. https://doi.org/10.1371/journal.pone.0006548
doi: 10.1371/journal.pone.0006548 pubmed: 19662094 pmcid: 2717333
Hattori RS, Castañeda-Cortés DC, Arias Padilla LF et al (2020) Activation of stress response axis as a key process in environment-induced sex plasticity in fish. Cell Mol Life Sci 77:4223–4236. https://doi.org/10.1007/s00018-020-03532-9
doi: 10.1007/s00018-020-03532-9 pubmed: 32367192
Hayashi Y, Kobira H, Yamaguchi T et al (2010) High temperature causes masculinization of genetically female medaka by elevation of cortisol. Mol Reprod Dev 77:679–686. https://doi.org/10.1002/mrd.21203
doi: 10.1002/mrd.21203 pubmed: 20653000
Holland LZ, Ocampo Daza D (2018) A new look at an old question: when did the second whole genome duplication occur in vertebrate evolution? Genome Biol 19:209. https://doi.org/10.1186/s13059-018-1592-0
doi: 10.1186/s13059-018-1592-0 pubmed: 30486862 pmcid: 6260733
Holleley CE, Sarre SD, O’Meally D, Georges A (2016) Sex reversal in reptiles: reproductive oddity or powerful driver of evolutionary change? Sex Dev 10:279–287. https://doi.org/10.1159/000450972
doi: 10.1159/000450972 pubmed: 27794577
Hudson HA, Brauer PR, Scofield MA (2008) Petzel DH (2008) Effects of warm acclimation on serum osmolality, cortisol and hematocrit levels in the Antarctic fish, Trematomus bernacchii. Polar Biol 31(8):991–997. https://doi.org/10.1007/s00300-008-0438-8
doi: 10.1007/s00300-008-0438-8
Kassambara A, Mundt F (2020) factoextra: extract and visualize the results of multivariate data analyses. 2020 R package version 1.0. 7. Google Sch There is no Corresp Rec this Ref
Kim J-H, Kim SK, Hur YB (2019) Temperature-mediated changes in stress responses, acetylcholinesterase, and immune responses of juvenile olive flounder Paralichthys olivaceus in a bio-floc environment. Aquaculture 506:453–458. https://doi.org/10.1016/j.aquaculture.2019.03.045
doi: 10.1016/j.aquaculture.2019.03.045
Laberge F, Yin-Liao I, Bernier NJ (2019) Temporal profiles of cortisol accumulation and clearance support scale cortisol content as an indicator of chronic stress in fish. Conserv Physiol 7:. https://doi.org/10.1093/conphys/coz052
Madaro A, Folkedal O, Maiolo S et al (2018) Effects of acclimation temperature on cortisol and oxygen consumption in Atlantic salmon (Salmo salar) post-smolt exposed to acute stress. Aquaculture 497:331–335. https://doi.org/10.1016/j.aquaculture.2018.07.056
doi: 10.1016/j.aquaculture.2018.07.056
Martins RST, Gomez A, Zanuy S et al (2015) Photoperiodic modulation of circadian clock and reproductive axis gene expression in the pre-pubertal European sea bass brain. PLoS One 10:e0144158. https://doi.org/10.1371/journal.pone.0144158
doi: 10.1371/journal.pone.0144158 pubmed: 26641263 pmcid: 4671726
Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268
doi: 10.1023/A:1008924418720
Navarro-Martín L, Viñas J, Ribas L et al (2011) DNA methylation of the gonadal aromatase (cyp19a) promoter is involved in temperature-dependent sex ratio shifts in the European sea bass. PLOS Genet 7:e1002447. https://doi.org/10.1371/journal.pgen.1002447
doi: 10.1371/journal.pgen.1002447 pubmed: 22242011 pmcid: 3248465
Olivereau M, Olivereau J (1988) Localization of CRF-like immunoreactivity in the brain and pituitary of teleost fish. Peptides 9:13–21. https://doi.org/10.1016/0196-9781(88)90004-6
doi: 10.1016/0196-9781(88)90004-6 pubmed: 2896342
Olivereau M, Ollevier F, Vandesande F, Verdonck W (1984) Immunocytochemical identification of CRF-like and SRIF-like peptides in the brain and the pituitary of cyprinid fish. Cell Tissue Res 237:379–382. https://doi.org/10.1007/BF00217162
doi: 10.1007/BF00217162 pubmed: 6148147
Ortega-Recalde O, Goikoetxea A, Hore TA, et al (2020) The genetics and epigenetics of sex change in fish. Annu Rev Anim Biosci 8:annurev-animal-021419–083634. https://doi.org/10.1146/annurev-animal-021419-083634
Pavlidis M, Karantzali E, Fanouraki E et al (2011) Onset of the primary stress in European sea bass Dicentrarhus labrax, as indicated by whole body cortisol in relation to glucocorticoid receptor during early development. Aquaculture 315:125–130. https://doi.org/10.1016/j.aquaculture.2010.09.013
doi: 10.1016/j.aquaculture.2010.09.013
Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP (2004) Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper – Excel-based tool using pair-wise correlations. Biotechnol Lett 26:509–515. https://doi.org/10.1023/B:BILE.0000019559.84305.47
doi: 10.1023/B:BILE.0000019559.84305.47 pubmed: 15127793
Piferrer F, Blázquez M, Navarro L, González A (2005) Genetic, endocrine, and environmental components of sex determination and differentiation in the European sea bass (Dicentrarchus labrax L.). Gen Comp Endocrinol 142:102–110. https://doi.org/10.1016/j.ygcen.2005.02.011
doi: 10.1016/j.ygcen.2005.02.011 pubmed: 15862554
Prunet P, Sturm A, Milla S (2006) Multiple corticosteroid receptors in fish: from old ideas to new concepts. Gen Comp Endocrinol 147:17–23. https://doi.org/10.1016/j.ygcen.2006.01.015
doi: 10.1016/j.ygcen.2006.01.015 pubmed: 16545810
Ribas L, Crespo B, Sánchez-Baizán N et al (2019) Characterization of the European sea bass (Dicentrarchus labrax) gonadal transcriptome during sexual development. Mar Biotechnol 21:359–373. https://doi.org/10.1007/s10126-019-09886-x
doi: 10.1007/s10126-019-09886-x
Rosewicz S, McDonald AR, Maddux BA et al (1988) Mechanism of glucocorticoid receptor down-regulation by glucocorticoids. J Biol Chem 263:2581–2584
doi: 10.1016/S0021-9258(18)69104-5
Rousseau K, Prunet P, Dufour S (2021) Special features of neuroendocrine interactions between stress and reproduction in teleosts. Gen Comp Endocrinol 300:113634. https://doi.org/10.1016/j.ygcen.2020.113634
doi: 10.1016/j.ygcen.2020.113634 pubmed: 33045232
Sadoul B, Geffroy B (2019) Measuring cortisol, the major stress hormone in fishes. J Fish Biol 94:540–555. https://doi.org/10.1111/jfb.13904
doi: 10.1111/jfb.13904 pubmed: 30667059
Sadoul B, Alfonso S, Bessa E et al (2018) Enhanced brain expression of genes related to cell proliferation and neural differentiation is associated with cortisol receptor expression in fishes. Gen Comp Endocrinol 267:76–81. https://doi.org/10.1016/j.ygcen.2018.06.001
doi: 10.1016/j.ygcen.2018.06.001 pubmed: 29902473
Saillant E, Fostier A, Haffray P et al (2002) Temperature effects and genotype-temperature interactions on sex determination in the European sea bass (Dicentrarchus labrax L.). J Exp Zool 292:494–505. https://doi.org/10.1002/jez.10071
doi: 10.1002/jez.10071 pubmed: 11857484
Sakae Y, Oikawa A, Sugiura Y, et al (2020) Starvation causes female-to-male sex reversal through lipid metabolism in the teleost fish, medaka (Olyzias latipes). Biol Open 9:. https://doi.org/10.1242/bio.050054
Samaras A, Papandroulakis N, Lika K, Pavlidis M (2018) Water temperature modifies the acute stress response of European sea bass, Dicentrarchus labrax L. (1758). J Therm Biol 78:84–91. https://doi.org/10.1016/j.jtherbio.2018.09.006
doi: 10.1016/j.jtherbio.2018.09.006 pubmed: 30509671
Samaras A, Dimitroglou A, Kollias S et al (2021) Cortisol concentration in scales is a valid indicator for the assessment of chronic stress in European sea bass Dicentrarchus Labrax l. Aquaculture 545:737257. https://doi.org/10.1016/j.aquaculture.2021.737257
doi: 10.1016/j.aquaculture.2021.737257
Sarre SD, Ezaz T, Georges A (2011) Transitions between sex-determining systems in reptiles and amphibians. Annu Rev Genomics Hum Genet 12:391–406. https://doi.org/10.1146/annurev-genom-082410-101518
doi: 10.1146/annurev-genom-082410-101518 pubmed: 21801024
Stelkens RB, Wedekind C (2010) Environmental sex reversal, Trojan sex genes, and sex ratio adjustment: conditions and population consequences. Mol Ecol 19:627–646. https://doi.org/10.1111/j.1365-294X.2010.04526.x
doi: 10.1111/j.1365-294X.2010.04526.x pubmed: 20088884
Thomas JT, Todd EV, Muncaster S et al (2019) Conservation and diversity in expression of candidate genes regulating socially-induced female-male sex change in wrasses. PeerJ 7:e7032. https://doi.org/10.7717/peerj.7032
doi: 10.7717/peerj.7032 pubmed: 31218121 pmcid: 6568253
Timmers RJM, Lambert JGD, Peute J et al (1987) Localization of aromatase in the brain of the male African catfish, Clarias gariepinus (Burchell), by microdissection and biochemical identification. J Comp Neurol 258:368–377. https://doi.org/10.1002/cne.902580305
doi: 10.1002/cne.902580305 pubmed: 3584544
Todd EV, Ortega-Recalde O, Liu H et al (2019) Stress, novel sex genes, and epigenetic reprogramming orchestrate socially controlled sex change. Sci Adv 5:eaaw7006. https://doi.org/10.1126/sciadv.aaw7006
doi: 10.1126/sciadv.aaw7006 pubmed: 31309157 pmcid: 6620101
Uller T, Hollander J, Astheimer L, Olsson M (2009) Sex-specific developmental plasticity in response to yolk corticosterone in an oviparous lizard. J Exp Biol 212:1087–1091. https://doi.org/10.1242/jeb.024257
doi: 10.1242/jeb.024257 pubmed: 19329741
Vallarino M, Fasolo A, Ottonello I, et al (1989) Localization of corticotropin-releasing hormone (CRF)-like immunoreactivity in the central nervous system of the elasmobranch fish, Scyliorhinus canicula. Cell Tissue Res 258:. https://doi.org/10.1007/BF00218865
Vandeputte M, Dupont-Nivet M, Chavanne H, Chatain B (2007) A polygenic hypothesis for sex determination in the European sea bass Dicentrarchus labrax. Genetics 176:1049–1057. https://doi.org/10.1534/genetics.107.072140
doi: 10.1534/genetics.107.072140 pubmed: 17435246 pmcid: 1894574
Vandeputte M, Piferrer F (2018) Genetic and environmental components of sex determination in the European sea bass. Sex Control Aquac 305–325
Vandeputte M, Clota F, Sadoul B et al (2020) Low temperature has opposite effects on sex determination in a marine fish at the larval/postlarval and juvenile stages. Ecol Evol 10:13825–13835. https://doi.org/10.1002/ece3.6972
doi: 10.1002/ece3.6972 pubmed: 33391683 pmcid: 7771145
Vijayan MM, Leatherland JF (1990) High stocking density affects cortisol secretion and tissue distribution in brook charr, Salvelinus fontinalis. J Endocrinol 124:311–318. https://doi.org/10.1677/joe.0.1240311
doi: 10.1677/joe.0.1240311 pubmed: 2155988
Vijayan MM, Raptis S, Sathiyaa R (2003) Cortisol treatment affects glucocorticoid receptor and glucocorticoid-responsive genes in the liver of rainbow trout. Gen Comp Endocrinol 132:256–263. https://doi.org/10.1016/S0016-6480(03)00092-3
doi: 10.1016/S0016-6480(03)00092-3 pubmed: 12812773
Warner DA, Radder RS, Shine R (2009) Corticosterone exposure during embryonic development affects offspring growth and sex ratios in opposing directions in two lizard species with environmental sex determination. Physiol Biochem Zool 82:363–371. https://doi.org/10.1086/588491
doi: 10.1086/588491 pubmed: 19143534
Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625. https://doi.org/10.1152/physrev.1997.77.3.591
doi: 10.1152/physrev.1997.77.3.591 pubmed: 9234959
Xie F, Xiao P, Chen D et al (2012) miRDeepFinder: a miRNA analysis tool for deep sequencing of plant small RNAs. Plant Mol Biol 80:75–84. https://doi.org/10.1007/s11103-012-9885-2
doi: 10.1007/s11103-012-9885-2
Yamaguchi T, Yoshinaga N, Yazawa T et al (2010) Cortisol is involved in temperature-dependent sex determination in the Japanese flounder. Endocrinology 151:3900–3908. https://doi.org/10.1210/en.2010-0228
doi: 10.1210/en.2010-0228 pubmed: 20534725
Yudt MR, Cidlowski JA (2002) The glucocorticoid receptor: coding a diversity of proteins and responses through a single gene. Mol Endocrinol 16:1719–1726. https://doi.org/10.1210/me.2002-0106
doi: 10.1210/me.2002-0106 pubmed: 12145329

Auteurs

Alexander Goikoetxea (A)

MARBEC Univ Montpellier, CNRS, Ifremer, IRD, Palavas-Les-Flots, France. alexandergoikoetxea@gmail.com.

Arianna Servili (A)

Ifremer, IFREMER, Univ Brest, CNRS, IRD, LEMAR, 29280, Plouzané, France.

Camille Houdelet (C)

MARBEC Univ Montpellier, CNRS, Ifremer, IRD, Palavas-Les-Flots, France.

Olivier Mouchel (O)

Ifremer, IFREMER, Univ Brest, CNRS, IRD, LEMAR, 29280, Plouzané, France.

Sophie Hermet (S)

MARBEC Univ Montpellier, CNRS, Ifremer, IRD, Montpellier, France.

Fréderic Clota (F)

MARBEC Univ Montpellier, CNRS, Ifremer, IRD, Palavas-Les-Flots, France.
Université Paris-Saclay, INRAE, AgroParisTech, GABI, Jouy-en-Josas, France.

Johan Aerts (J)

Stress Physiology Research Group, Faculty of Sciences, Ghent University, Ostend, Belgium.

Juan Ignacio Fernandino (JI)

Instituto Tecnológico de Chascomús, INTECH (CONICET-UNSAM), Chascomús, Argentina.

François Allal (F)

MARBEC Univ Montpellier, CNRS, Ifremer, IRD, Palavas-Les-Flots, France.

Marc Vandeputte (M)

MARBEC Univ Montpellier, CNRS, Ifremer, IRD, Palavas-Les-Flots, France.
Université Paris-Saclay, INRAE, AgroParisTech, GABI, Jouy-en-Josas, France.

Eva Blondeau-Bidet (E)

MARBEC Univ Montpellier, CNRS, Ifremer, IRD, Montpellier, France.

Benjamin Geffroy (B)

MARBEC Univ Montpellier, CNRS, Ifremer, IRD, Palavas-Les-Flots, France.

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