Skip to main content
Log in

Effect of water temperature on cellular stress responses in meagre (Argyrosomus regius)

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Μeagre (Argyrosomus regius) is a newly introduced species in the aquaculture sector characterized by high growth rates and good nutritional value. However, the optimum conditions such as water temperature for the rearing of this species are still under research. The aim of the present study was to investigate several biochemical responses in the heart, muscle, liver, and intestine of meagre reared under different water temperatures (17, 23, and 26 °C) in comparison to the initial acclimation temperature at 20 °C. To assess its cellular stress response, the molecular markers of Hsp70 and Hsp90 induced levels, p38 MAPK and p44/42 MAPK phosphorylated levels, ubiquitin conjugates, and Bcl-2 levels were determined. Moreover, to investigate its antioxidant defense, the activities of superoxide dismutase, catalase, and glutathione reductase were measured. The obtained results in meagre showed a distinct tissue-specific response regarding the variations observed in the studied parameters under different acclimation temperatures. Specifically, most examined tissues presented a decrease in the levels of the examined markers compared to 20 °C, while in the intestine, an increase of Hsp70 and p38 MAPK levels was observed at 23 and 26 °C. However, data on the final weight and length of the fish lead to the conclusion that high water temperatures such as 26 °C might be the best for the rearing of this species. Therefore, it is assumed that the observed differential molecular responses may act in a cell-protective way at all temperatures, irrespectively of the effect of temperature on growth parameters.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Ahmad I, Hamid T, Fatima M, Chand HS, Jain SK, Athar M, Raisuddin S (2000) Induction of hepatic antioxidants in freshwater catfish (Channa punctatus Bloch) is a biomarker of paper mill effluent exposure. Biochem Biophys Acta 1523:37–48

    CAS  PubMed  Google Scholar 

  • Ali KS, Dorgai L, Abraham M, Hermesz E (2003) Tissue- and stressor-specific differential expression of two hsc70 genes in carp. Biochem Biophys Res Commun 307:503–509

    CAS  PubMed  Google Scholar 

  • Amaeze NH, Adeyemi RO, Adebesin AO (2015) Oxidative stress, heats schock protein and histopathological effects in the gills of African catfish, Clarias gariepinus induced by bridge runoffs. Environ Monit Assess 187(4):172

    PubMed  Google Scholar 

  • Antonopoulou E, Kentepozidou E, Feidantsis K, Roufidou C, Despoti S, Chatzifotis S (2013) Starvation and re-feeding affect Hsp expression, MAPK activation and antioxidant enzymes activity of European Sea bass (Dicentrarchus labrax). Comp Biochem Physiol A 165:79–88

    CAS  Google Scholar 

  • Beamish FWH (1964) Influence of starvation on standard and routine oxygen consumption. Trans Am Fish Soc 93:103–107

    Google Scholar 

  • Beere HM (2004) The stress of dying: the role of heat shock proteins in the regulation of apoptosis. J Cell Sci 117(13):2641–2651

    CAS  PubMed  Google Scholar 

  • Bilden WN, Wang Z, Iserovich P, Reinach PS (2003) Hypertonically induced p38 MAPK activation elicits recovery of corneal epithelial cell volume and layer integrity. J Membr Biol 193:1–13

    Google Scholar 

  • Cara JB, Aluru N, Moyano FJ, Vijayan MM (2005) Food deprivation induces hsp70 and hsp90 protein expression in larval gilthead sea bream and rainbow trout. Comp Biochem Physiol B 142:426–431

    CAS  PubMed  Google Scholar 

  • Carlberg I, Mannervik B (1985) Glutathione reductase assay. Methods in Enzymol, vol 113. Academic press, Orlando FL, pp 484–495

    Google Scholar 

  • Ciechanover A (1998) The ubiquitin–proteasome pathway: on protein death and cell life. EMBO J 17(24):7151–7160

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cohen G, Dembiec D, Marcus J (1970) Measurement of catalase activity in tissue extracts. Anal Biochem 34(1):30–38

    CAS  PubMed  Google Scholar 

  • Currie S, Moyes CD, Tufts B (2000) The effects of heat shock and acclimation temperature on hsp70 and hsp30 mRNA expression in rainbow trout: in vivo and in vitro comparisons. J Fish Biol 56:398–408

    CAS  Google Scholar 

  • Das P, Gupta A, Manna Sanjib K (2005) Heat shock protein 70 expression in different tissues of Cirrhinus mrigala (Ham.) following heat stress. Aquac Res 36:525–529

    CAS  Google Scholar 

  • Deane EE, Woo NYS (2003) Ontogeny of thyroid hormones, cortisol, hsp70 and hsp90 during silver sea bream larval development. Life Sci 72:805–818

    CAS  PubMed  Google Scholar 

  • Deng DF, Wang CF, Lee SH, Bai SC, SSO H (2009) Feeding rates affect heat shock protein levels in liver of larval white sturgeon (Acipenser transmontanus). Aquaculture 287:223–226

    CAS  Google Scholar 

  • Dietz T (1994) Acclimation of the threshold induction temperatures for hsp 70 and hsp 90 in the fish Gyllicthys mirabilis. J Exp Biol 188:333–338

    CAS  PubMed  Google Scholar 

  • El-Shebly AA, MAH E-K, Hussin AB, Hossain Y (2007) Preliminary observations on the pond culture of meagre, Argyrosomus regius (Asso, 1801) (Sciaenidae) in Egypt. J Fish Aquat Sci 2(5):345–352

    CAS  Google Scholar 

  • FAO (Food and Agricultural Organization) (2010–2019) Cultured aquatic species information programme Argyrosomus regius. (http://www.fao.org.fi, accessed date: 20 November 2019)

  • Feder ME, Hofmann G (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282

    CAS  PubMed  Google Scholar 

  • Feidantsis K, Pörtner HO, Lazou A, Kostoglou B, Michaelidis B (2009) Metabolic and molecular stress responses of the gilthead sea bream Sparus aurata during long term exposure to increasing temperatures. Mar Biol 156:797–809

    CAS  Google Scholar 

  • Feidantsis K, Pörtner HO, Markou T, Lazou A, Michaelidis B (2012) Involvement of p38 MAPK in the induction of Hsp70 during acute thermal stress in red blood cells of the gilthead sea bream, Sparus aurata. J Exp Zool A 317:303–310

    CAS  Google Scholar 

  • Feidantsis K, Antonopoulou E, Lazou A, Pörtner HO, Michaelidis B (2013a) Seasonal variations of cellular stress response of the gilthead sea bream (Sparus aurata). J Comp Physiol B 183:625–639

    CAS  PubMed  Google Scholar 

  • Feidantsis K, Anestis A, Michaelidis B (2013b) Seasonal variations of anti-/apoptotic and antioxidant proteins in the heart and gastrocnemius muscle of the water frog Pelophylax ridibundus. Cryobiol 67:175–183

    CAS  Google Scholar 

  • Feidantsis K, Kaitetzidou E, Mavrogiannis N, Michaelidis B, Kotzamanis Y, Antonopoulou E (2014) Effect of taurine enriched diets on the Hsp expression, MAPK activation and the antioxidant defences of the European Sea bass (Dicentrarchus labrax). Aquac Nutr 20:431–442

    CAS  Google Scholar 

  • Feidantsis K, Pörtner HO, Antonopoulou E, Michaelidis B (2015) Synergistic effects of acute warming and low pH on cellular stress responses of the gilthead seabream Sparus aurata. J Comp Physiol B 185:185–205

    CAS  PubMed  Google Scholar 

  • Feidantsis K, Pörtner HO, Vlachonikola E, Antonopoulou E, Michaelidis B (2018) Seasonal changes in metabolism and cellular stress phenomena in the gilthead sea bream (Sparus aurata). Physiol Biochem Zool 91(3):878–895

    PubMed  Google Scholar 

  • Fridovich I (1974) Superoxide dismutases. Adv Enzymol 41:35–97

    CAS  PubMed  Google Scholar 

  • Furné M, García-Gallego M, Hidalgo MC, Morales AE, Domezain A, Domezain J, Sanz A (2009) Oxidative stress parameters during starvation and refeeding periods in Adriatic sturgeon (Acipenser naccarii) and rainbow trout (Oncorhynchus mykiss). Aquac Nutr 15:587–595

    Google Scholar 

  • Glass HJ, NL MD, Moran RM, Stark JR (1989) Digestion of protein in different marine species. Comp Biochem Physiol B 94(3):607–611

    Google Scholar 

  • Goldman D, Sapru MK, Stewart S, Plotkin J, Libermann TA, Wasylyk B, Guan K (1998) Cloning and characterization of GETS-1, a goldfish Ets family member that functions as a transcriptional repressor in muscle. Biochem J 335(2):267–275

    CAS  PubMed  PubMed Central  Google Scholar 

  • Green DR, Reed JC (1998) Mitochondria and apoptosis. Science 281(5381):1309–1312

    CAS  PubMed  Google Scholar 

  • Greenway SC, Storey KB (2000) Activation of mitogen-activated protein kinases during natural freezing and thawing in the wood frog. Mol Cell Biochem 209:29–37

    CAS  PubMed  Google Scholar 

  • Guderley H, Lapointe D, Bédarda M, Jean-Denis Dutil J-D (2003) Metabolic priorities during starvation: enzyme sparing in liver and white muscle of Atlantic cod, Gadus morhua L. Comp Biochem Physiol A 135:347–356

    Google Scholar 

  • Hashimoto H, Yokoyama Y, Matsuo Y, Toyohara H, Kohno M, Sakaguchi M (1998) Existence of two isoforms of extracellular signal regulated kinase in fish. J Biochem (Tokyo) 123:1031–1035

    CAS  Google Scholar 

  • Hashimoto H, Fukuda M, Matsuo Y, Yokoyama Y, Nishida E, Toyohara H, Sakaguchi M (2000) Identification of a nuclear export signal of MKK6, an activator of the carp p38 mitogen activated protein kinases. Eur J Biochem 267:4362–4371

    CAS  PubMed  Google Scholar 

  • Helmuth B (2009) From cells to coastlines: how can we use physiology to forecast the impacts of climate change? J Exp Biol 212:753–760

    PubMed  Google Scholar 

  • Helmuth B, Broitman BR, Yamane L, Gilman SE, Mach K, KAS M, Denny MW (2010) Organismal climatology: analyzing environmental variability at scales relevant to physiological stress. J Exp Biol 213:955–1003

    Google Scholar 

  • Heredia-Middleton P, Brunelli J, Drew RE, Thorgaard GH (2008) Heat shock protein (HSP70) RNA expression differs among rainbow trout (Oncorhynchus mykiss) clonal lines. Comp Biochem Physiol B 149:552–556

    PubMed  Google Scholar 

  • Hermes-Lima M, Storey KB (1996) Relationship between anoxia exposure and antioxidant status in the frog Rana pipiens. Am J Phys Regul Integr Comp Phys 271:R918–R925

    CAS  Google Scholar 

  • Hermes-Lima M, Store KB (1998) Role of antioxidant defences in the tolerance of severe dehydration by anurans. The case of the leopard frog Ranapipiens. Mol Cell Biochem 189:79–89

  • Hoffman J, Katz U (1997) Salt and water balance in the toad Bufo viridis during recovery from two different osmotically stressful conditions. Comp Biochem Physiol A 117(1):147–154

    CAS  Google Scholar 

  • Hofmann GE (2005) Patterns of Hsp gene expression in ectothermic marine organisms on small to large biogeographic scales. Integr Comp Biol 45:247–255

    CAS  PubMed  Google Scholar 

  • Hofmann GE, Somero GN (1996) Interspecies variation in thermal denaturation of proteins in the congeneric mussels Mytilus trossulus and M. galloprovincialis: evidence from the heat-shock response and protein ubiquitination. Mar Biol 126:65–75

    CAS  Google Scholar 

  • Joyner-Matos J, Downs GA, Julian D (2006) Increased expression of stress proteins in the surf clam Donax variabilis following hydrogen sulfide exposure. Comp Biochem Physiol A 145:245–257

    Google Scholar 

  • Ju Z, Dunham RA, Liu Z (2002) Differential gene expression in the brain of channel catfish (Ictalurus punctatus) in response to cold acclimation. Mol Gen Genomics 268(1):87–95

    CAS  Google Scholar 

  • Kamler E (2002) Ontogeny of yolk-feedingfish: an ecological perspective. Rev Fish Biol Fish 12:79–103

    Google Scholar 

  • Kassahn KS, Crozier RS, Pörtner HO, Caley MJ (2009) Animal performance and stress responses and tolerance limits at different levels of biological organisation. Biol Rev 84:277–292

    PubMed  Google Scholar 

  • Kır M, Sunar MC, Altındağ BC (2017) Thermal tolerance and preferred temperature range of juvenile meagre acclimated to four temperatures. J Therm Biol 65:125–129

    PubMed  Google Scholar 

  • Kounna C, Chatzifotis S, Miliou H, Rigos G, Fountoulaki E (2017) Water temperature effects on growth, body and tissue composition, and gastric evacuation in juvenile meagre (Αrgyrosomus regius). Aquaculture Europe 2017 (EAS 2017), 17-20 October 2017, Dubrovnik, Croatia. Abstract p. 621: poster presentation

  • Kroemer G, Galluzzi L, Brenner C (2007) Mitochondrial membrane permeabilization in cell death. Physiol Rev 87(1):99–163

    CAS  PubMed  Google Scholar 

  • Kultz D, Avila K (2001) Mitogen activated protein kinases are in vivo transducers of osmosensory signals in fish gill cells. Comp Biochem Physiol B 129:821–829

    CAS  PubMed  Google Scholar 

  • Kyriakis JM, Avruch J (2001) Mammalian mitogen activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 81:807–869

    CAS  PubMed  Google Scholar 

  • Leal BR, Ribeiro JS, Posser T, Cordova MF, Rigon PA, Filho ZE, DCA B (2006) Modulation of ERK1/2 and p38MAPK by lead in the cerebellum of Brazilian catfish Rhamdia quelen. Aquat Toxicol 77:98–104

    CAS  PubMed  Google Scholar 

  • Lewis TS, Shapiro PS, Ahn NG (1998) Signal transduction through MAP kinase cascades. Adv Cancer Res 74:49–139

    CAS  PubMed  Google Scholar 

  • Lund SG, Lund MEA, Tufts BL (2003) Red blood cell Hsp 70 mRNA and protein as bio-indicators of temperature stress in the brook trout (Salvelinus fontinalis). Can J Fish Aquat Sci 60(4):460–470

    CAS  Google Scholar 

  • Μarshall WS, Ossum CG, Hoffmann GE (2005) Hypotonic shock mediation by p38 MAPK, JNK, PKC, FAK, OSR1 and SPAK in osmosensing chloride secreting cells of killifish opercular epithelium. J Exp Biol 208:1063–1077

  • Monfort MC (2010) Present market situation and prospects of meager (Argyrosomus regius), as an emerging species in Mediterranean aquaculture. FAO Studies and Reviews. General Fisheries Commission for the Mediterranean (GFCM - Session Report), no. 89. Food and Agricultural Organization of the United Nations, Rome

  • Moody CS, Hassan HM (1984) Anaerobic biosynthesis of the manganese-containing superoxide dismutase in Escherichia coli. J Biol Chem 259:12821–12825

    CAS  PubMed  Google Scholar 

  • Morales AE, Pérez-Jiménez A, Hidalgo MC, Abellan E, Cardenete G (2004) Oxidative stress and antioxidant defenses after prolonged starvation in Dentex dentex liver. Comp Biochem Physiol C 139:153–161

    Google Scholar 

  • Nadzialek S, Pigneur LM, Wιron B, Kestemont P (2010) Bcl-2 and caspase 3 mrna levels in the testes of gudgeon, Gobio gobio, exposed to ethinylestradiol (ee2). Aquat Toxicol 98:304–310

    CAS  PubMed  Google Scholar 

  • Paoletti F, Mocali A (1990) Determination of superoxide dismutase activity by purely chemical system based on NAD(P) H oxidation. Methods Enzymol 186:209–220

    CAS  PubMed  Google Scholar 

  • Pascual P, Pedrajas JR, Toribio F, Lopez-Barea J, Peinado J (2003) Effect of food deprivation on oxidative stress biomarkers in fish (Sparus aurata). Chem Biol Interact 145:191–199

    CAS  PubMed  Google Scholar 

  • Place SP, Hofmann GE (2005) Function and expression of the molecular chaperone HSP70 in Antarctic fishes. FASEB J 19:A214–A214

    Google Scholar 

  • Place SP, Zippay ML, Hofmann GE (2004) Constitutive roles for inducible genes: evidence for the alteration in expression of the inducible hsp70 gene in Antarctic notothenioid fishes. Am J Physiol-Regul Integr Comp Physiol 287:R429–R436

    CAS  PubMed  Google Scholar 

  • Poli BM, Parisi G, Zampacavallo G, Iurzan F, Mecatti M, Lupi P, Bonelli A (2003) Preliminary results on quality and quality changes in reared meagre (Argyrosomus regius): body and fillet traits and freshness changes in refrigerated commercial-size fish. Aquac Int 11:301–311

    Google Scholar 

  • Pörtner HO (2001) Climate change and temperature dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88:137–146

    PubMed  Google Scholar 

  • Pörtner HO (2002a) Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comp Biochem Physiol A 132:739–761

    Google Scholar 

  • Pörtner HO (2002b) Physiological basis of temperature-dependent biogeography: trade-offs in muscle design and performance in polar ectotherms. J Exp Biol 205:2217–2230

    PubMed  Google Scholar 

  • Pörtner HO, Farrell AP (2008) Ecology: physiology and climate change. Science 322:690–692

    PubMed  Google Scholar 

  • Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–97

    PubMed  Google Scholar 

  • Pörtner HO, Peck MA (2010) Climate change effects on fishes and fisheries: towards a cause-and-effect understanding. J Fish Biol 77:1745–1779

    PubMed  Google Scholar 

  • Pörtner HO, Marc FC, Book C (2004) Oxygen limited thermal tolerance in fish? Answers obtained by nuclear magnetic resonance techniques. Respir Physiol Neurobiol 141:243–260

    PubMed  Google Scholar 

  • Rafiee P, Shi Y, Pritchard KA, Ogawa H, ALW E, Komorowski RA, Fitzpatrick CM, Tweddell JS, Litwin SB, Mussatto K, Jaquiss RD, Bakre JA (2003) Cellular redistribution of inducible hsp70 protein in human and rabbit heart in response to the stress of chronic hypoxia. J Biol Chem 278:43636–43644

    CAS  PubMed  Google Scholar 

  • Reed JC (1997) Cytochrome c: can’t live with it-can’t live without it. Cell 91(5):559–562

    CAS  PubMed  Google Scholar 

  • Rios FS, Kalinin AL, Rantin FT (2002) The effects of long-term food deprivation on respiration and haematology of the neotropical fish Hoplias malabaricus. J Fish Biol 61:85–95

    Google Scholar 

  • Salach JI (1978) Preparation of monoamine oxidase from beef liver mitochondria. Methods Enzymol 53:495–501

    CAS  PubMed  Google Scholar 

  • Sheikh-Hamad D, Di Mari J, Suki WN, Safirstein R, Watts BA, Rouse D (1998) p38 kinase activity is essential for osmotic induction of mRNAs for hsp70 and transporter for organic solute betaine in Madin-Darby canine kidney cells. J Biol Chem 273:1832–1837

    CAS  PubMed  Google Scholar 

  • Snaar-Jagalska BE, Krens SF, Robina I, Wang LX, Spaink HP (2003) Specific activation of ERK pathways by chitin oligosaccharides in embryonic zebrafish cell lines. Glycobiology 13:725–732

    CAS  PubMed  Google Scholar 

  • Somero NG (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’. J Exp Biol 213:912–920

    CAS  PubMed  Google Scholar 

  • Somero GN (2012) The physiology of global change: linking patterns to mechanisms. Annu Rev Mar Sci 4:39–61

    Google Scholar 

  • Stead D, Park SF (2000) Roles of Fe superoxide dismutase and catalase in resistance of Campylobacter coli to freeze-thaw stress. Appl Environ Microbiol 66:3110–3112

    CAS  PubMed  PubMed Central  Google Scholar 

  • Todgham AE, Hofmann GE (2009) Transcriptomic response of sea urchin larvae Strongylocentrotus purpuratus to CO2-driven seawater acidification. J Exp Biol 212:2579–2594

    CAS  PubMed  Google Scholar 

  • Tomanek L (2010) Variation in the heat shock response and its implication for predicting the effect of global climate change on species’ biogeographical distribution ranges and metabolic costs. J Exp Biol 213:971–979

    CAS  PubMed  Google Scholar 

  • Tomanek L (2012) Environmental proteomics of the mussel Mytilus: implications fro tolerance to stress and change in limits of biogeographic ranges in response to climate change. Integr Comp Biol 114:1–17

    Google Scholar 

  • Tomanek L, Zuzow MJ, Ivanina AV, Beniash E, Sokolova IM (2011) Proteomic response to elevated PCO2 level in eastern oysters, Crassostrea virginica: evidence for oxidative stress. J Exp Biol 214:1836–1844

    CAS  PubMed  Google Scholar 

  • Trostler N, Brady PS, Romsos DR, Leveille GA (1979) Influence of dietary vitamin E on malondialdehyde levels in liver and adipose tissue and on glutathione peroxidase and reductase activities in liver and erythrocytes of lean and obese (ob/ob) mice. L Nutr 109:345–352

    CAS  Google Scholar 

  • Uehara T, Kaneko M, Tanaka S, Okuma Y, Nomura Y (1999) Possible involvement of p38 MAP kinase in hsp70 expression induced by hypoxia in rat primary astrocytes. Brain Res 823:226–230

    CAS  PubMed  Google Scholar 

  • Valavanidis A, Vlahogianni T, Dassenakis M, Scoullos M (2006) Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol Environ Saf 64:178–189

    CAS  PubMed  Google Scholar 

  • Weber TE, Bosworth BG (2005) Effects of 28 day exposure to cold temperature or feed restriction on growth, body composition, and expression of genes related to muscle growth and metabolism in channel catfish. Aquaculture 246:483–492

    CAS  Google Scholar 

  • Widegren U, Wretman C, Lionikas A, Hedin G, Henriksson J (2000) Influence of exercise intensity on ERK/MAP kinase signalling in human skeletal muscle. Pflügers Arch - Eur J Physiol 441:317–322

  • Zambonino Infante JL, Cahu CL (2001) Ontogeny of the gastrointestinal tract of marine fish larvae. Comp Biochem Physiol C 130:477–487

    CAS  Google Scholar 

  • Zarate J, Bradley TM (2003) Heat shock proteins are not sensitive indicators of hatchery stress in salmon. Aquaculture 223:175–187

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Efthimia Antonopoulou.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Antonopoulou, E., Chatzigiannidou, I., Feidantsis, K. et al. Effect of water temperature on cellular stress responses in meagre (Argyrosomus regius). Fish Physiol Biochem 46, 1075–1091 (2020). https://doi.org/10.1007/s10695-020-00773-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-020-00773-0

Keywords

Navigation