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Implications of stress-mediated environmental sex determination for declining eel populations

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Abstract

We implement a newly developed framework, expressed as a mathematical model that we solve numerically, for understanding environmental sex determination in populations with consistent trends in abundance. Though broadly applicable, the analysis here focuses on the steadily declining North Atlantic eel populations. This enables us to show how the eco-evolutionary dynamics of eels reflect sex-specific and habitat-specific relationships among demographic features. When increasing stress levels resulting from Human-Induced Rapid Environmental Change are imposed on these populations, they become increasingly vulnerable to highly biased sex ratios. Our analysis is both prescriptive (identifying the key components and the priorities for deepening our understanding of them) and predictive (indicating expected qualitative patterns to be tested in future work). Priorities include establishing sex ratios and age/sex structure by habitat, measuring the magnitude and effects of social and individual stress levels, estimating effects of fishing pressure, and investigating reproduction in the Sargasso Sea. Key predictions address expected biases and trends in sex ratios, habitats more likely to be population sources (e.g. river basins) or sinks (e.g. estuary), expected trends in bimaturism (sex-specific maturation times), implications of the relative speed of adaptation and of environmental deterioration, and fitness responses to stress levels, early-stage mortality, and female demographic parameters.

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References

  • Aoyama J (2009) Life history and evolution of migration in catadromous eels (genus Anguilla). Aqua Biosci Monogr 2:1–42

    Article  Google Scholar 

  • Aprahamian MW, Evans DW, Briand C, Walker AM, McElarney Y, Allen M (2021) The changing times of Europe’s largest remaining commercially harvested population of eel Anguilla anguilla L. J Fish Biol 99(4):1201–1221. https://doi.org/10.1111/jfb.14820

    Article  PubMed  PubMed Central  Google Scholar 

  • Arai T, Chino N (2012) Diverse migration strategy between freshwater and seawater habitats in the freshwater eel genus Anguilla. J Fish Biol 81:442–455

    Article  CAS  PubMed  Google Scholar 

  • Arai T, Kotake A, Harrod C, Morrissey M, McCarthy TK (2019) Ecological plasticity of the European eel Anguilla Anguilla in a tidal Atlantic lake system in Ireland. J Mar Biol Assoc UK 99:1189–1195. https://doi.org/10.1017/S0025315419000031

    Article  CAS  Google Scholar 

  • Aschonitis VG, Castaldelli G, Lanzoni M, Merighi M, Gelli F, Giari L, Rossi R, Fano EA (2015) A size-age model based on bootstrapping and Bayesian approaches to assess population dynamics of Anguilla anguilla L. in semi-close lagoons. Ecol Freshw Fish 26:217–232

    Article  Google Scholar 

  • Aschonitis VG, Castaldelli G, Lanzoni M, Rossi R, Kennedy C, Fano EA (2017) Long-term records (1781–2013) of European eel (Anguilla anguilla L.) production in the Comacchio Lagoon (Italy): evaluation of local and global factors as causes of the population collapse. Aquat Conserv Mar Freshwat Ecosyst 27:502–520

    Article  Google Scholar 

  • Astrӧm M, Dekker W (2007) When will the eel recover? A full life-cycle model. ICES J Mar Sci 64:1491–1498

    Article  Google Scholar 

  • Baillon L, Pierron F, Pannetier P, Normandeau E, Couture P, Labadie P, Budzinski H, Lambert P, Bernatchez L, Baudrimont M (2016) Gene transcription profililing in wild and laboratory-exposed eels: effect of captivity and in situ chronic exposure to pollution. Sci Total Environ 571:92–102

    Article  CAS  PubMed  Google Scholar 

  • Ballasch JC, Tort L (2019) Netting the stress responses in fish. Front Endocrinol 10:62

    Article  Google Scholar 

  • Beaulaton L, Briand C, Lambert P, Castelnaud G, Drouineau H, Chapon P-M, Pénil C et al (2014) Report on the eel stock and fishery in France 2013/2014. In: Report of the joint EIFAAC/ICES/GFCM working group on eel, pp 308–362

  • Belpaire C, Hodson P, Pierron F, Freeze M (2019) Impact of chemical pollution on Atlantic eels: Facts, research needs and implications for management. Curr Opin Environ Sci Health 11:26–36

    Article  Google Scholar 

  • Bevacqua D, Melià P, De Leo GA, Gatto M (2011) Intra-specific scaling of natural mortality in fish: the paradigmatic case of the European eel. Oecologia 165:333–339

    Article  PubMed  Google Scholar 

  • Bevacqua D, Melià P, Gatto M, De Leo GA (2015) A global viability assessment of the European eel. Glob Change Biol 21:3323–3335

    Article  Google Scholar 

  • Bevacqua D, Melià P, Schiavina M, Crivelli AJ, De Leo GA, Gatto M (2019) A demographic model for the conservation and management of the European eel: an application to a Mediterranean coastal lagoon. ICES J Mar Sci 76:2164–2178

    Google Scholar 

  • Boeuf G, Payan P (2001) How should salinity influence fish growth? Comp Biochem Physiol C Toxicol Pharmacol 130:411–423

    Article  CAS  PubMed  Google Scholar 

  • Bonhommeau S, Chassot E, Rivot E (2008) Fluctuations in European eel (Anguilla anguilla) recruitment resulting from environmental changes in the Sargasso Sea. Fish Oceanogr 17:32–44

    Article  Google Scholar 

  • Bornarel V, Lambert P, Briand C, Antunes C, Belpaire C, Ciccotti E, Diaz E, Diserud O, Doherty D, Domingos I, Evans D, de Graaf M, O’Leary C, Pedersen M, Poole R, Walker A, Wickström H, Beaulaton L, Drouineau H (2018) Modelling the recruitment of European eel (Anguilla anguilla) throughout its European range. ICES J Mar Sci 75:541–552

    Article  Google Scholar 

  • Briand C, Mounaix B, Fatin D, Feunteun E (2003) The contribution of springtime and autumn glass eels (Anguilla anguilla) to stock: results based on otolith morphometry. Bull Fr De Péche Piscicol 368:27–42

    Article  Google Scholar 

  • Bull JJ (1981) Sex ratio evolution when fitness varies. Heredity 46:9–26

    Article  Google Scholar 

  • Butler ECV (2006) The tail of two rivers in Tasmania: the Derwent and Huon estuaries. In: Wangersky P (ed) Estuaries. Handbook of Environmental Chemistry, vol 5. Springer, New York, pp 1–49

    Google Scholar 

  • Candolin U, Wong BBM (eds) (2012) Behavioural responses to a changing world: mechanisms and consequences. Oxford University Press, Oxford

    Google Scholar 

  • Capel B (2017) Vertebrate sex determination: evolutionary plasticity of a fundamental switch. Nat Rev Genet 18:675

    Article  CAS  PubMed  Google Scholar 

  • Carroll RL (1988) Vertebrate paleontology and evolution. Freeman, New York

    Google Scholar 

  • Casselman JM (2003) Dynamics of resources of the American eel, Anguilla rostrate: declining abundance in the 1990’s. In: Aida K, Tsukamoto K, Yamauchi K (eds) Eel biology. Springer, Tokyo, pp 255–274

    Chapter  Google Scholar 

  • Castaldelli G, Aschonitis V, Lanzoni M, Gelli F, Rossi R, Fano EA (2014) An update of the length–weight and length–age relationships of the European eel (Anguilla anguilla, Linnaeus 1758) in the Comacchio Lagoon, northeast Adriatic Sea, Italy. J Appl Ichthyol 30:558–559

    Article  Google Scholar 

  • Caswell H (2001) Matrix population models, 2nd edn. Sinauer, Sunderland

    Google Scholar 

  • Chapman PM, Wang F, Sofia Caeiro S (2013) Assessing and managing sediment contamination in transitional waters. Environ Int 55:71–91

    Article  CAS  PubMed  Google Scholar 

  • Charlon N, Blanc J-M (1982) Étude des civelles d’Anguilla anguilla L. dans la région du Bassin de l’Adour. 1. Caractéristiques biométriques de longueur et de poids en fonction de la pigmentation. Arch Hydrobiol 93:238–255

    Google Scholar 

  • Charnov EL (1982) The theory of sex allocation. Princeton University Press, Princeton

    Google Scholar 

  • Charnov EL, Bull JJ (1989) Non-fisherian sex ratios with sex change and environmental sex determination. Nature 338:148–150

    Article  Google Scholar 

  • Chiba H, Iwata M, Yakoh K, Satoh R, Yamada H (2002) Possible influence of social stress on seX differentiation in Japanese eel. Fish Sci 68:413–414

    Article  Google Scholar 

  • Chu Y-W, Han Y-S, Wang C-H, You C-F, Tzeng W-N (2006) The sex-ratio reversal of the Japanese eel Anguilla japonica in the Kaoping River of Taiwan: the effect of cultured eels and its implication. Aquaculture 261:1230–1238

    Article  Google Scholar 

  • Claveau J, Monperrus M, Jarry M, Baudrimont M, Gonzalez P, Cavalheiro J, Mesmer-Dudons N, Bolliet V (2015) Methylmercury effects on migratory behavior in glass eels (Anguilla anguilla): an experimental study using isotopic tracers. Comp Biochem Physiol 171:15–27

    CAS  Google Scholar 

  • Conover DO, Heins SW (1987) The environmental and genetic components of sex ratio in Menidia menidia (Pices: Atherinidae). Copeia 1987:732–743

    Article  Google Scholar 

  • Côté CL, Castonguay M, Verreault G, Bernatchez L (2009) Differential effects of origin and salinity rearing conditions on growth of glass eels of the American eel Anguilla rostrata: implications for stocking programmes. J Fish Biol 74:1934–1948

    Article  PubMed  Google Scholar 

  • Côté CL, Castonguay M, Klujnaia MS, Cramb G, Bernatchez L (2014) In absence of local adaptation, plasticity and spatially varying selection rule: a view from genomic reaction norms in a panmictic species (Anguilla rostrata). BMC Genom 15:403

    Article  Google Scholar 

  • Côté CL, Pavey SA, Stacey JA, Pratt TC, Castonguay M, Audet C, Bernatchez L (2015) Growth, female size, and sex ratio variability in American eel of different origins in both controlled conditions and the wild: implications for stocking programs. Trans Am Fish Soc 144:246–257

    Article  Google Scholar 

  • Crowley PH, Labonne J (2021) Theory of environmental sex determination: trending populations in altered environments. Evolution 75:794–805

    Article  PubMed  Google Scholar 

  • D’Ancona U (1959) Distribution of the sexes and environmental influence in the European eel. Archives D’anatomie Microscopique Et De Morphologie Experimentale 48:61–70

    PubMed  Google Scholar 

  • Daverat F, Tomas J (2006) Tactics and demographic attributes of the European eel (Anguilla Anguilla): the case study of the Gironde watershed (Southwest France). Mar Ecol Prog Ser 307:247–257

    Article  Google Scholar 

  • Daverat F, Limburg KE, Thibault I, Shiao JC, Dodson JJ, Caron FO, Tzeng WN, Iizuka Y, Wickstrom H (2006) Phenotypic plasticity of habitat use by three temperate eel species, Anguilla anguilla, A. japonica and A. rostrata. Mar Ecol Prog Ser 308:231–241

    Article  Google Scholar 

  • Daverat F, Beaulaton L, Poole R, Lambert P, Wickström H, Andersson J, Aprahamian M, Hizem B, Elie P, Yalcin-Ozdilek S, Gumus A (2012) One century of eel growth: changes and implications. Ecol Freshw Fish 21:325–336

    Article  Google Scholar 

  • Davey AJH, Jellyman DJ (2005) Sex determination in freshwater eels and management options for manipulation of sex. Rev Fish Biol 15:37–52

    Article  Google Scholar 

  • De Leo GA, Gatto M (1995) A size and age-structured model of the European eel (Anguilla anguilla L.). Can J Fish Aquat Sci 52:1351–1367

    Article  Google Scholar 

  • De Leo GA, Gatto M (1996) Trends in vital rates of the European eel: evidence for density dependence? Ecol Appl 6:1281–1294

    Article  Google Scholar 

  • Degani G, Levanon D (1983) The influence of low density on food adaptation, cannibalism and growth of eels (Anguilla Anguilla (L.)). Bamidgeh 35:53–60

    Google Scholar 

  • Dekker W (2003) Did lack of spawners cause the collapse of the European eel, Anguilla anguilla? Fish Manag Ecol 10:365–376

    Article  Google Scholar 

  • Dekker W (2004) Slipping through our hands—population dynamics of the European eel. Dissertation: Faculteit der Natutuurweten Schappen, Wiskunde an Informatica, The Netherlands

  • Desaunay I, Guerault D (1997) Seasonal and long-term changes in biometrics of eel larvae: a possible relationship between recruitment variation and North Atlantic ecosystem productivity. J Fish Biol 51:317–339

    Article  Google Scholar 

  • Drouineau H, Rigaud C, Daverat F, Lambert P (2014) EvEel (evolutionary ecology-based model for eel): a model to explore the role of phenotypic plasticity as an adaptive response of three temperate eels to spatially structured environments. Can J Fish Aquat Sci 71:1561–1571

    Article  Google Scholar 

  • Drouineau H, Briand C, Lambert P, Beaulaton L (2016) GEREM (Glass Eel Recruitment Estimation Model): a model to estimate glass eel recruitment at different spatial scales. Fish Res 174:68–80

    Article  Google Scholar 

  • Drouineau H, Durif C, Castonguay M, Mateo M, Rochard E, Verreault G, Yokouchi K, Lambert P (2018) Freshwater eels: a symbol of the effects of global change. Fish Fish 19:903–930. https://doi.org/10.1111/faf.12300Edeline

    Article  Google Scholar 

  • Edeline E, Dufour S, Elie P (2005) Role of glass eel salinity preference in the control of habitat selection and growth plasticity in Anguilla anguilla. Mar Ecol Prog Ser 304:191–199

    Article  Google Scholar 

  • Edeline E, Lambert P, Rigaud C, Elie P (2006) Effect of body condition and water temperature on Anguilla anguilla glass eel migratory behavior. J Exp Mar Biol Ecol 331:217–225

    Article  Google Scholar 

  • Enbody ED, Pettersson ME, Sprehn CG, Palm S, Wickström H, Andersson L (2021) Ecological adaptation in European eels is based on phenotypic plasticity. Proc Natl Acad Sci 118(4):e2022620118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fablet R, Daverat F, De Pontual H (2007) Unsupervised Bayesian reconstruction of individual life histories from otolith signatures: case study of Sr: Ca transects of European eel (Anguilla anguilla) otoliths. Can J Fish Aquat Sci 64:152–165

    Article  CAS  Google Scholar 

  • Fenske KH, Wilberg MJ, Secor DH, Fabrizio MC (2011) An age- and sex-structured assessment model for American eels (Anguilla rostrata) in the Potomac River, Maryland. Can J Fish Aquat Sci 68:1024–1037

    Article  Google Scholar 

  • Fernandino JI, Hattori RS, Moreno Acosta OD, Strussmann CA, Somoza GM (2013) Environmental stress-induced testis differentiation: androgen as a by-product of cortisol inactivation. Gen Comp Endocrinol 192:36–44

    Article  CAS  PubMed  Google Scholar 

  • Frank SA, Swingland IR (1988) Sex ratio under conditional sex expression. J Theor Biol 135:415–418

    Article  CAS  PubMed  Google Scholar 

  • Geffroy B, Bardonnet A (2012) Differential effect of behaviour, propensity to migrate and recruitment season on glass eel’s growing performance. Ecol Freshw Fish 21:469–482

    Article  Google Scholar 

  • Geffroy B, Bardonnet A (2016) Sex differentiation and sex determination in eels: consequences for management. Fish Fish 17:375–398

    Article  Google Scholar 

  • Geffroy B, Douhard M (2019) The adaptive sex in stressful environments. Trends Ecol Evol 34:628–640

    Article  PubMed  Google Scholar 

  • Geffroy B, Wedekind C (2020) Effects of global warming on the sex ratios in fishes. J Fish Biol. https://doi.org/10.1111/jfb.14429

    Article  PubMed  Google Scholar 

  • Geffroy B, Guiguen Y, Fostier A, Bardonnet A (2013) New insights regarding gonad development in European eel: evidence for a direct ovarian differentiation. Fish Physiol Biochem 29:1129–1140

    Article  Google Scholar 

  • Geffroy B, Sadoul B, Bardonnet A (2015) Behavioural syndrome in juvenile eels and its ecological implications. Behaviour 152:147–166

    Article  Google Scholar 

  • Geffroy B, Guilbaud F, Amilhat E, Beaulaton L, Vignon M, Huchet E, Rives J, Bobe J, Fostier A, Guiguen Y, Bardonnet A (2016) Sexually dimorphic gene expressions in eels: useful markers for early sex assessment in a conservation context. Sci Rep 6:3404

    Article  Google Scholar 

  • Goikoetxea A, Todd EV, Gemmell NJ (2017) Stress and sex: does cortisol mediate sex change in fish? Reproduction 154:R149–R160

    Article  CAS  PubMed  Google Scholar 

  • Gross MR, McDowall RM (1988) Aquatic productivity and the evolution of diadromous fish migration. Science 239:1291–1293

    Article  CAS  PubMed  Google Scholar 

  • Guimaraes L, Gravato C, Santos J, Monteiro LS, Guilhermino L (2009) Yellow eel (Anguilla anguilla) development in NW Portuguese estuaries with different contamination levels. Ecotoxicology 18:385–402

    Article  CAS  PubMed  Google Scholar 

  • Han YS, Tzeng WN (2007) Sex-dependent habitat use by the Japanese eel Anguilla japonica in Taiwan. Mar Ecol Prog Ser 338:193–198

    Article  Google Scholar 

  • Harrison AJ, Walker AM, Pinder AC, Briand C, Aprahamian MW (2014) A review of glass eel migratory behavior, sampling techniques and abundance estimates in estuaries: implications for assessing recruitment, local production and exploitation. Rev Fish Biol Fish 24:967–983

    Article  Google Scholar 

  • Helfman GS, Facey DE, Hales LS, Bozeman EL Jr (1987) Reproductive ecology of the American eel. Am Fish Soc Symp 1:4256

    Google Scholar 

  • Hodgson EE, Wilson SM, Moore JW (2020) (2020) Changing estuaries and impacts on juvenile salmon: a systematic review. Glob Change Biol 26:1986–2001. https://doi.org/10.1111/gcb.14997

    Article  Google Scholar 

  • Holmgren K, Mosegaard H (1996) Implications of individual growth status on the future sex of the European eel. J Fish Biol 49:910–925

    Article  Google Scholar 

  • Honeycutt JL, Deck CA, Miller SC, Severance ME, Atkins EB, Luckenbach JA, Godwin J (2019) Warmer waters masculinize wild populations of a fish with temperature-dependent sex determination. Sci Rep 9:1–13

    Article  CAS  Google Scholar 

  • Huey RB, Janzen FJ (2008) Climate warming and environmental sex determination in tuatara: the Last of the Sphenodontians? Proc R Soc B 275:2181–2183

    Article  PubMed  PubMed Central  Google Scholar 

  • Ibbotson A, Smith J, Scarlett P, Aprhamian M (2002) Colonisation of freshwater habitats by the European eel Anguilla Anguilla. Freshw Biol 47:1696–1706

    Article  Google Scholar 

  • ICES (2009) Report of the study group on anguillid eels in saline waters (SGAESAW), 16–18 March 2009, Sackville, Canada; 3–5 September 2009, Gothenburg, Sweden. ICES CM/DFC:06

  • ICES (2014) Report of the joint EIFFAC/ICES/GFCM working group on eels, 3–7 November 2014, Rome, Italy. ICES CM 2014/ACOM, 18

  • ICES (2018) Report of the joint EIFFAC/ICES/GFCM working group on eels (WGEEL), 3–10 October 2017, Kavala, Greece. ICES CM 2017/ACOM:15

  • Iglesias T, Lobon-Cervia J (2012) Size and number of male silver eels Anguilla anguilla (L.) in a Cantabrian river over two decades (1990–2011). Fundam Appl Limnol 181:229–239

    Article  Google Scholar 

  • Imbert H, Arrowsmith R, Dufour S, Elie P (2008) Relationship between locomotor behavior, morphometric characters and thyroid hormone levels give evidence of stage-dependent mechanisms in European eel upstream migration. Horm Behav 53:69–81

    Article  CAS  PubMed  Google Scholar 

  • Jacobsen MW, Pujolar JM, Pedersen L, Hansen MM (2018) Single nucleotide polymorphism markers for assessing potential maternal population structure in European eel (Anguilla anguilla). Conserv Genet Resour 10(4):907–909

    Article  Google Scholar 

  • Janzen FJ, Phillips PC (2006) Exploring the evolution of sex determination, especially in reptiles. J Evol Biol 19:1775–1784

    Article  CAS  PubMed  Google Scholar 

  • Jessop BM (1998) Geographic and seasonal variation in biological characteristics of American eel elvers in the Bay of Fundy area and on the Atlantic coast of Nova Scotia. Can J Zool 76:2172–2185

    Article  Google Scholar 

  • Jessop BM, Shiao J-C, Iizuka Y, Tzeng W-N (2006) Migration of juvenile American eels Anguilla rostrata between freshwater and estuary, as revealed by otolith microchemistry. Mar Ecol Prog Ser 310:219–233

    Article  CAS  Google Scholar 

  • Johnson GD, Ida H, Sakaue J, Sado T, Asahida T, Miya M (2012) A “living fossil” eel (Anguilliformes: Protanguillidae, Fam. Nov.) from an undersea cave in Palau. Proc Biol Sci 279:934–943

    PubMed  Google Scholar 

  • Kettle AJ, Vollestad LA, Asbjorn L, Wibig J (2011) Where once the eel and the elephant were together: decline of the European eel because of changing hydrology in southwest Europe and northwest Africa? Fish Fish 12:380–411

    Article  Google Scholar 

  • Krueger WH, Oliveira K (1999) Evidence for environmental sex determination in the American eel, (Anguilla rostrata). Environ Biol Fishes 55:381–389

    Article  Google Scholar 

  • Laffaille P, Acou A, Guioullet J, Mounaix B, Legault A (2006) Patterns of silver eel (Anguilla anguilla L.) sex ratio in a catchment. Ecol Freshw Fish 15:583–588

    Article  Google Scholar 

  • Lambert P, Rochard E (2007) Identification of the inland population dynamics of the European eel using pattern-oriented modelling. Ecol Model 206:166–178

    Article  Google Scholar 

  • Lefebvre F, Crivelli AJ (2012) Salinity effects on anguillicolosis in Atlantic eels: a natural tool for disease control. Mar Ecol Prog Ser 471:193–216

    Article  Google Scholar 

  • Liu H, Labonne J, Coste P, Huechet E, Plagnes-Juan E, Rives J, Veron V, Seilies I, Bolliet V (2019) Looking at the complex relationships between behavior and conditional strategy based on energy metabolism in the European glass eel (Anguilla anguilla) in experimental conditions. Sci Total Environ 696:134039

    Article  CAS  Google Scholar 

  • Liu H, Lamarins A, Labonne J, Monperrus M, Coste P, Huchet E, Rives J, Seiliez I, Bolliet V (2020) New insights into methylmercury induced behavioral and energy-related gene transcriptional responses in European glass eel (Anguilla anguilla). Chemosphere 255:127020

    Article  CAS  PubMed  Google Scholar 

  • Mateo M, Lambert P, Tetard S, Castonguay M, Ernande B, Drouineau H (2017) Cause or consequence? Exploring the role of phenotypic plasticity and genetic polymorphism in the emergence of phenotypic spatial patterns of the European eel. Can J Fish Aquat Sci 74:987–999

    Article  Google Scholar 

  • The MathWorks (2019) MATLAB® 2019b. Natick, MA

  • McLusky DS, Elliott M (2004) The estuarine ecosystem: ecology, threats and management. Oxford University Press, Oxford

    Book  Google Scholar 

  • Miller MJ, Bonhommeau S, Munk P, Castonguay M, Hanel R, McCleave JD (2015) A century of research on the larval distributions of the Atlantic eels: a re-examination of the data. Biol Rev 90:1035–1064

    Article  PubMed  Google Scholar 

  • Moorman BP, Inokuchi M, Yamaguchi Y, Lerner DT, Grau EG, Seale AP (2014) The osmoregulatory effects of rearing Mozambique tilapia in a tidally changing salinity. Gen Comp Endocrinol 207:94–102

    Article  CAS  PubMed  Google Scholar 

  • Newton A, Icely J, Cristina S, Perillo GME, Turner RE, Ashan D, Cragg S, Luo Y, Tu C, Li Y, Zhang H, Ramesh R, Forbes DL, Solidoro C, Béjaoui B, Gao S, Pastres R, Kelsey H, Taillie D, Nhan N, Brito AC, de Lima R, Kuenzer C (2020) Anthropogenic, direct pressures on coastal wetlands. Front Ecol Evol 8:144. https://doi.org/10.3389/fevo.2020.00144

    Article  Google Scholar 

  • Oeberst R, Fladung E (2012) German eel model (GEM II) for describing eel, Anguilla anguilla (L.), stock dynamics in the river Elbe system. https://doi.org/10.3220/Infn59_09-17_2012

  • Oliveira K (1999) Life history characteristics and strategies of the American eel, Anguilla rostrata. Can J Fish Aquat Sci 56:795–802

    Article  Google Scholar 

  • Oliveira K, McCleave J (2000) Variation in population and life history traits of the American eel, Anguilla rostrata, in four rivers in Maine. Environ Biol Fish 59:141–151

    Article  Google Scholar 

  • Pal A, YewHoong G, YuChen L, Reinhard M (2010) Impacts of emerging organic contaminants on freshwater resources: review of recent occurrences, sources, fate and effects. STOTEN 408:6062–6069

    CAS  Google Scholar 

  • Parsons J, Vickers KU, Warden Y (1977) Relationship between elver recruitment and changes in sex-ratio of silver eels Anguilla anguilla L. migrating from Lough Neagh, Northern Ireland. J Fish Biol 10:211–229

    Article  Google Scholar 

  • Pierron F, Daffe G, Lambert P, Couture P, Baudrimont M (2019) Retrotransposon methylation and activity in wild fish (A. anguilla): a matter of size. Environ Pollut 245:494–503

    Article  CAS  PubMed  Google Scholar 

  • Poole WR, Diserud OH, Thorstad EB, Durif CM, Dolan C, Sandlund OTK, Bergesen K, Rogan K, Kelly GS, Vollestad LA (2018) Long-term variation in numbers and biomass of silver eels being produced in two European river systems. ICES J Mar Sci 75:1627–1637

    Article  Google Scholar 

  • Pujolar JM, Jacobsen TDA, Frydenberg J, Munch K, Jónsson B, Jian JB, Cheng L, Maes GE, Bernatchez L, Hansen MM (2014) Genome-wide single-generation signatures of local selection in the panmictic European eel. Mol Ecol 23:2514–2528

    Article  CAS  PubMed  Google Scholar 

  • Ribas L, Valdiveiso A, Diaz N, Piferrer F (2017) Appropriate rearing density in domesticated zebrafish to avoid masculinization: links with the stress response. J Exp Biol 220:1056–1064

    Article  PubMed  Google Scholar 

  • Roncarati A, Melotti P, Mordenti O, Gennari L (1997) Influence of stocking density of European eel (Anguilla anguilla, L.) elvers on sex differentiation and zootechnical performances. J Appl Ichtyol 13:131–136

    Article  Google Scholar 

  • Sadoul B, Geffroy B (2018) Measuring cortisol, the major stress hormone in fishes. J Fish Biol 94:540–555

    Article  Google Scholar 

  • Schmidt J (1925) The breeding places of the eel. Smithson Inst Annu Rep 1924:279–316

    Google Scholar 

  • Schreck CB (2010) Stress and fish reproduction: the roles of allostasis and hormesis. Gen Comp Endocrinol 165:549–556

    Article  CAS  PubMed  Google Scholar 

  • Schwanz LE, Cordero GA, Charnov EL, Janzen FJ (2016) Sex-specific survival to maturity and the evolution of environmental sex determination. Evolution 70:329–341

    Article  PubMed  Google Scholar 

  • Seyle H (1976) The stress of life. McGraw-Hill, New York

    Google Scholar 

  • Sih A (2013) Understanding variation in behavioural responses to human-induced rapid environmental change: a conceptual overview. Anim Behav 85:1077–1088

    Article  Google Scholar 

  • Silva AT, Midwood JD, Aarestrup K, Pottinger TG, Madsen SS, Cooke SJ (2018) The influence of sex, parasitism, and ontogeny on the physiological response of European eels (Anguilla anguilla) to an abiotic stressor. Physiol Biochem Zool 91:976–986

    Article  PubMed  Google Scholar 

  • Simon J, Westerberg H, Righton D, Sjöberg NB, Dorow M (2018) Diving activity of migrating silver eel with and without Anguillicola crassus infection. J Appl Ichthyol 34:659–668

    Article  Google Scholar 

  • Sobol IM (2001) Global sensitivity indices for nonlinear mathematical models and their Monte Carlo estimates. Math Comput Simul 55:271–280

    Article  Google Scholar 

  • Sprengel G, Lüchtenberg H (1991) Infection by endoparasites reduces maximum swimming speed of European smelt Osmerus eperlanus and European eel Anguilla anguilla. Dis Aquat Org 11:31–35

    Article  Google Scholar 

  • Tabouret H, Bareille G, Bareille G, Mestrot A, Caill-Milly N, Budzinski H, Peluhet L, Prouzet P, Donard OFX (2011) Heavy metals and organochlorinated compounds in the European eel (Anguilla anguilla) from the Adour estuary and associated wetlands (France). J Environ Monit 13:1446–1456

    Article  CAS  PubMed  Google Scholar 

  • Tesch F-W (2003) The eel, 5th edn. Wiley, Oxford

    Book  Google Scholar 

  • Trancart T, Tudorache C, van den Thillart GEEJM, Acou A, Carpentier A, Boinet C, Gouchet G, Feunteun E (2015) The effect of thermal shock during diel vertical migration on the energy required for oceanic migration of the European silver eel. J Exp Mar Biol 463:168–172

    Article  Google Scholar 

  • Tsukamoto K (2009) Oceanic navigation and spawning of anguillid eels. J Fish Biol 74:1833–1852

    Article  CAS  PubMed  Google Scholar 

  • Tsukamoto K, Nakai I, Tesch WV (1998) Do all freshwater eels migrate? Nature 396:635–636

    Article  CAS  Google Scholar 

  • Tzchori I, Degani G, Elisha R, Eliyahu R, Hurvitz A, Vaya J, Moav B (2004) The influence of phytoestrogens and oestradiol-17 beta on growth and sex determination in the European eel (Anguilla anguilla). Aquac Res 35:1213–1219

    Article  CAS  Google Scholar 

  • Tzeng WN, Lin HR, Wang CH, Xu SN (2000) Differences in size and growth rates of male and female migrating Japanese eels in Pearl River. Chin J Fish Biol 57:1245–1253

    Article  Google Scholar 

  • Uller T, Pen I, Wapstra E, Beukeboom LW, Komdeur J (2007) The evolution of sex ratios and sex-determining systems. Trends Ecol Evol 22:292–297

    Article  PubMed  Google Scholar 

  • Van Friedland KD, Miller MJ, Knights B (2007) Oceanic changes in the Sargasso Sea and declines in recruitment of the European eel. ICES J Mar Sci 64:519–530

    Article  Google Scholar 

  • Vaughan L, Brophy D, Toole C, Graham C, Maoileidigh N, Poole R (2021) Growth rates in a European eel Anguilla Anguilla (L., 1758) show a complex relationship with temperature over a seven0decade otolith biochronology. ICES J Mar Sci 78:994–1009

    Article  Google Scholar 

  • Vollestad LA, Jonsson B (1988) A 13-year study of the population-dynamics and growth of the European eel Anguilla anguilla in a Norwegian river—evidence for density-dependent mortality, and development of a model for predicting yield. J Anim Ecol 57:983–997

    Article  Google Scholar 

  • Wedekind C (2017) Demographic and genetic consequences of disturbed sex determination. Philos Trans R Soc B Biol Sci 372(1729):20160326

    Article  Google Scholar 

  • Westerberger H, Miller MJ, Wysujack K, Marohn L, Freese M, Pohlmann J-D, Watanabe S, Tsukamoto K, Hanel R (2018) Larval abundance across the European eel spawning area: an analysis of recent and historic data. Fish Fish 19:890–902

    Article  Google Scholar 

  • Wirth T, Bernatchez L (2001) Genetic evidence against panmixia in the European eel. Nature 409:1037–1039

    Article  CAS  PubMed  Google Scholar 

  • Wong BBM, Candolin U (2015) Behavioral responses to changing environments. Behav Ecol 26:665–673

    Article  Google Scholar 

  • Yokouchi K, Daverat F, Miller MJ, Fukuda N, Sudo R, Tsukamoto K, Elie P, Poole WR (2018) Growth potential can affect timing of maturity in a long-lived semelparous fish. Biol Lett 14:20180269

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Vinnie Cassone, Benjamin Geffroy, Étienne Prévost, Charlotte Récapet, and Cédric Tentelier for comments and suggestions on the manuscript. We acknowledge grant support from the Fulbright Foundation to PHC funding his 2019-2020 year in residence at the INRAE field station in St. Pée sur Nivelle, France; he greatly appreciates the warm hospitality and enthusiastic collaboration of the ECOBIOP research group. PHC also acknowledges sabbatical support from the University of Kentucky.

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Authors and Affiliations

  1. Department of Biology, University of Kentucky, Lexington, KY, 40506, USA

    Philip H. Crowley

  2. Université de Pau et des Pays de l’Adour, e2s UPPA, INRAE, ECOBIOP, 64310, St Pée-sur-Nivelle, France

    Philip H. Crowley, Jacques Labonne, Valérie Bolliet, Françoise Daverat & Agnès Bardonnet

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  1. Philip H. Crowley
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  2. Jacques Labonne
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  3. Valérie Bolliet
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  4. Françoise Daverat
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  5. Agnès Bardonnet
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All authors contributed to the study design and discussion; VB, FD, and AB reviewed the literature; PC wrote and ran the computer programs; PC and JL interpreted the model results.

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Correspondence to Philip H. Crowley.

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Crowley, P.H., Labonne, J., Bolliet, V. et al. Implications of stress-mediated environmental sex determination for declining eel populations. Rev Fish Biol Fisheries 32, 1157–1186 (2022). https://doi.org/10.1007/s11160-022-09730-x

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