Skip to main content
SpringerLink
Log in

In situ localization of vasotocin receptor gene transcripts in the brain-pituitary-gonadal axis of the catfish Heteropneustes fossilis: a morpho-functional study

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

Abstract

In the catfish Heteropneustes fossilis, three vasotocin (VT) receptor subtype genes, v1a1, v1a2, and v2a, were cloned and characterized previously. In the present study, using RNA probes, we localized the distribution of the gene transcripts in the brain-pituitary-gonadal (BPG) axis. The V1a-type receptor, v1a1 and v1a2, genes showed similar and overlapping distribution in the brain. The gene paralogs are distributed in the radial glial cells (RGCs) of the telencephalic ventricle and around the third ventricle in the hypothalamus and thalamus, olfactory tract, nucleus preopticus, nucleus lateralis tuberis, nucleus recessus lateralis and posterioris, nucleus saccus vasculosi, thalamic nuclei, habenular nucleus, habenular commissure, basal part of pineal stalk, accessory pretectal nucleus, optic tectum, corpus and valvula of the cerebellum, and facial and vagal lobes. The V2a receptor gene (v2a) has restricted distribution and is largely confined to the anterior subependymal region of the telencephalon. The localization pattern shows that the V1a-type receptors are distributed in major sensorimotor processing centers and the neuroendocrine/reproductive centers of the brain. In the pituitary, the receptor genes were localized differentially in the three divisions with the V1a-type receptor genes strongly expressed in the rostral pars distalis compared to the v2a paralog. In the ovary, the V1a-type receptor genes were localized in the follicular layer while v2a was localized in the oocyte membrane. In the testis, v1a2 and v2a are densely distributed in the interstitial tissue and seminiferous epithelium but the v1a1 is lowly expressed. The results suggest that the VT receptor genes have an extensive but differential distribution in the BPG axis. Future experimental studies are required to correlate the cellular localizations with specific functions of VT in the BPG axis.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • Acharjee A, Chaube R, Joy KP, Cerda J (2011) Hormonal regulation of aquaporin-1ab in Heteropneustes fossilis oocytes in vitro. Indian J Sci Technol 4:165–166

    Google Scholar 

  • Acharjee A, Chaube R, Joy KP (2018) Reproductive stage- and sex-dependant effects of neurohypophyseal nonapeptides on gonadotropin subunit mRNA expression in the catfish Heteropneustes fossilis: an in vitro study. Gen Comp Endocrinol 260:80–89. https://doi.org/10.1016/j.ygcen.2018.01.001

    Article  CAS  PubMed  Google Scholar 

  • Adashi EY, Hsueh AJW (1981) Direct inhibition of testicular androgen biosynthesis by arginine-vasopressin: mediation through pressor-selective testicular recognition sites. Endocrinology 109:1793–1795

    Article  CAS  PubMed  Google Scholar 

  • Adashi EY, Hsueh AJW (1982) Direct inhibition of rat testicular androgen biosynthesis by arginine vasotocin. J Biol Chem 257:1301–1308

    CAS  PubMed  Google Scholar 

  • Almeida O, Gozdowska M, Kulczykowska E, Oliveira RF (2012) Brain levels of arginine–vasotocin and isotocin in dominant and subordinate males of a cichlid fish. Horm Behav 61:212–217

    Article  CAS  PubMed  Google Scholar 

  • Balment RJ, Lu W, Weybourne E, Warne JM (2006) Arginine vasotocin a key hormone in fish physiology and behaviour: a review with insights from mammalian models. Gen Comp Endocrinol 147:9–16

    Article  CAS  PubMed  Google Scholar 

  • Banerjee P, Chaube R, Joy KP (2015) Molecular cloning, sequencing and tissue expression of vasotocin and isotocin precursor genes from Ostariophysian catfishes: phylogeny and evolutionary considerations in teleosts. Front Neurosci 9:166

    Article  PubMed  PubMed Central  Google Scholar 

  • Banerjee P, Chaube R, Joy KP (2016) In situ localization of vasotocin and isotocin precursor mRNA in brain and ovary of the catfish Heteropneustes fossilis and estrogen regulation of the gene expression. J Trans Neurosci 1:1–2

    Google Scholar 

  • Barbeis C, Balestre MN, Jard S, Tribollet E, Arsenijevic Y, DreifussJJ BK, Manning M, Chan WY, Schlosser SS et al (1995) Characterization of a novel, linear radio iodinated vasopressin antagonist: an excellent radio ligand for vasopressin V1a receptors. Neuroendocrinology 62:135–146

    Article  CAS  PubMed  Google Scholar 

  • Barth SW, Saito N, Grossmann R (1997) Gene expression of the neurohypophysial hormone arg-vasotocin in the reproductive system of the hen. Eur J Phys 434 (Suppl. 1) 454 p

  • Bathgate RA, Sernia C (1994) Characterisation and localisation of oxytocin receptors in the rat testis. J Endocrinol 141:343–352

    Article  CAS  PubMed  Google Scholar 

  • Birnbaumer M (2000) Vasopressin receptors. TEM 11:406–410

    CAS  PubMed  Google Scholar 

  • Chaube R, Chauvigne F, Sequeira TA, Joy KP, Acharjee A, Singh V, Cerda J (2011) Molecular and functional characterization of catfish (Heteropneustes fossilis) aquaporin-1b: changes in expression during ovarian development and hormone-induced follicular maturation. Gen Comp Endocrinol 170:162–171

    Article  CAS  PubMed  Google Scholar 

  • Chaube R, Rawat A, Joy KP (2015) Molecular cloning and characterization of brain and ovarian cytochrome P450 aromatase genes in the catfish Heteropneustes fossilis: sex, tissue and seasonal variation in, and effects of gonadotropin on gene expression. Gen Comp Endocrinol 221:120–133

    Article  CAS  PubMed  Google Scholar 

  • Demski LS, Dulka JG (1986) Thalamic stimulation evokes sex–color change and gamete release in a vertebrate hermaphrodite. Experientia 42:1285–1287

    Article  CAS  PubMed  Google Scholar 

  • Diotel N, Le Page Y, Mouriec K, Tong SK, Pellegrini E, Vaillant C, Anglade I, Brion F, Pakdel F, Chung BC, Kah O (2010) Aromatase in the brain of teleost fish: expression, regulation and putative functions. Front Neuroendocrinol 31:172–192

    Article  CAS  PubMed  Google Scholar 

  • Escobar S, Felip A, Gueguen MM, Zanuy S, Carrillo M, Kah O, Servili A (2013) Expression of kisspeptins in the brain and pituitary of the European sea bass (Dicentrarchus labrax). J Comp Neurol 521:933–948

    Article  CAS  PubMed  Google Scholar 

  • Forlano PM, Deitcher DL, Myers DA, Bass AH (2001) Anatomical distribution and cellular basis for high levels of aromatase activity in the brain of teleost fish: aromatase enzyme and mRNA expression identify glia as source. J Neurosci 21:8943–8955

    Article  CAS  PubMed  Google Scholar 

  • Fryer J, Leung E (1982) Neurohypophyseal hormonal control of cortisol secretion in the teleost, Carassius auratus. Gen Comp Endocrinol 48:425–431

    Article  CAS  PubMed  Google Scholar 

  • Goodson JL, Bass AH (2000) Vasotocin innervation and modulation of vocal-acoustic circuitry in the teleost Porichthys notatus. J Comp Neurol 422:363–379

    Article  CAS  PubMed  Google Scholar 

  • Goodson JL, Bass AH (2001) Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates. Brain Res Rev 35:246–265

    Article  CAS  PubMed  Google Scholar 

  • Groves DJ, Batten TFC (1986) Direct control of the gonadotroph in a teleost Poecilia latipinna. II. Neurohormones and neurotransmitters. Gen Comp Endocrinol 62:315–326

    Article  CAS  PubMed  Google Scholar 

  • Hartfuss E, Galli R, Heins N, Gotz M (2001) Characterization of CNS precursor subtypes and radial glia. Dev Biol 229:15–30

    Article  CAS  PubMed  Google Scholar 

  • Hasunuma I, Toyoda F, Kadono Y, Yamamoto K, Namiki K, Kikuyama S (2010) Localization of three types of arginine vasotocin receptors in the brain and pituitary of the newt Cynops pyrrhogaster. Cell Tissue Res 342:437–457

    Article  CAS  PubMed  Google Scholar 

  • Hasunuma I, Toyoda F, Okada R, Yamamoto K, Kadono Y, Kikuyama S (2013) Roles of arginine vasotocin receptors in the brain and pituitary of submammalian vertebrates. Int Rev Cell Mol Biol 304:191–225

    Article  CAS  PubMed  Google Scholar 

  • Hipkin LJ (1970) Gonadotrophin inhibition by the synergistic action of vasopressin and oxytocin. Nature 225:740–742

    Article  CAS  PubMed  Google Scholar 

  • Hirasawa A, Hashimoto K, Tsujimoto G (1994) Distribution and developmental change of vasopressin V1a and V2 receptor mRNA in rats. Eur J Pharmacol 267:163–169

    Article  Google Scholar 

  • Huffman LS, O’Connell LA, Kenkel CD, Kline RJ, Khan IA, Hofmann HA (2012) Distribution of nonapeptide systems in the forebrain of an African cichlid fish Astatotilapia burtoni. J Chem Neuroanat 44:86–97

    Article  CAS  PubMed  Google Scholar 

  • Huffman LS, Hinz FI, Wojcik S, Aubin-Horth N, Hofmann HA (2015) Arginine vasotocin regulates social ascent in the African cichlid fish Astatotilapia burtoni. Gen Comp Endocrinol 212:106–113

    Article  CAS  PubMed  Google Scholar 

  • Iwasaki K, Taguchi M, Bonkowsky JL, Kuwada JY (2013) Expression of arginine vasotocin receptors in the developing zebrafish CNS. Gene Expr 13:335–342

    Article  CAS  Google Scholar 

  • Johnson AE, Audigier S, Rossi F, Jard S, Tribollet E, Barberis C (1993) Localization and characterization of vasopressin binding sites in the rat brain using an iodinated linear AVP antagonist. Brain Res 622:9–16

    Article  CAS  PubMed  Google Scholar 

  • Jordan CL(1999) Glia as mediators of steroid hormone action on the nervous system: an overview. J Neurobiol 40:434–445

  • Joy KP, Agha A (1993) A light-microscopic study on pineal organ structure and innervation in the catfish. J Hirnforsch 34:545–553

    CAS  PubMed  Google Scholar 

  • Joy KP, Chaube R (2015) Vasotocin—a new player in the control of oocyte maturation and ovulation in fish. Gen Comp Endocrinol 221:54–63

    Article  CAS  PubMed  Google Scholar 

  • Joy KP, Sathyanesan AG (1976) Distribution of monoamine oxidase (MAO) in relation to the hypothalamo-hypophyseal system of the teleost Clarias batrachus (L.). J Neural Transm 39:47–61

    Article  CAS  PubMed  Google Scholar 

  • Joy KP, Singh V (2013) Functional interactions between vasotocin and prostaglandins during final oocyte maturation and ovulation in the catfish Heteropneustes fossilis. Gen Comp Endocrinol 186:126–135

    Article  CAS  PubMed  Google Scholar 

  • Joy KP, Manickam P, Sathyanesan AG (1992) Paraformaldehyde and glyoxylic acid histofluorescence studies on monoamine distribution in the hypothalamo-hypophysial system of the catfish, Clarias batrachus (L.). Biol Struct Morphogen (Paris) 4:58–67

    Google Scholar 

  • Jurkevich A, Berghman LR, Cornett LE, Kuenzel WJ (2005) Characterization and immunohistochemical visualization of the vasotocin VT2 receptor in the pituitary gland of the chicken, Gallus gallus. Gen Comp Endocrinol 143:82–91

    Article  CAS  PubMed  Google Scholar 

  • Kanwal JS, Finger TE (1992) Central representation and projections of gustatory systems. In: Hara J (ed), Fish Chemoreception. Chapman & Hall, pp 79–102

  • Kanwal JS, Finger TE, Caprio J (1988) Forebrain connections of the gustatory system in ictalurid catfishes. J Comp Neurol 278:353–376

    Article  CAS  PubMed  Google Scholar 

  • Kasson BG, Rina Meidan S, Aaron J, Hsue W (1985) Identification and characterization of arginine vasopressin-like substances in the rat testis. J Biol Chem 260:5302–5530

    CAS  PubMed  Google Scholar 

  • Kato Y, Igarashi N, Hirasawa A, Tsujimoto G, Kabayashi M (1995) Distribution and developmental changes in vasopressin V2 receptor mRNA in rat brain. Differentiation 59:163–169

    Article  CAS  PubMed  Google Scholar 

  • Kline JR, O’Connell AL, Hofmann AH, Holt JG, Khan IA (2011) The distribution of an AVT V1a receptor in the brain of a sex changing fish Epinephelus adscensionis. J Chem Neuroanat 42:72–88

    Article  CAS  PubMed  Google Scholar 

  • Kline JR, Holt GJ, Khan IA (2015) Arginine vasotocin V1a2 receptor and GnRH-I co-localize in preoptic neurons of the sex changing grouper. Gen Comp Endocrinol 225:33–44

    Article  CAS  PubMed  Google Scholar 

  • Konno N, Kurosawa M, Kaiya H, Miyazato M, Matsuda K, Uchiyama M (2010) Molecular cloning and characterization of a V2-type receptor in two ray-finned fish, gray bichir, Polypterus senegalus and medaka Oryzias latipes. Peptides 3:1273–1279

    Article  CAS  Google Scholar 

  • Lema SC (2010) Identification of multiple vasotocin receptor cDNAs in teleost fish: sequences, phylogenetic analysis, sites of expression, and regulation in the hypothalamus and gill in response to hyperosmotic challenge. Mol Cell Endocrinol 321:215–230

    Article  CAS  PubMed  Google Scholar 

  • Lema SC, Slane MA, Salvesen KE, Godwin J (2012) Variation in gene transcript profiles of two V1a-type arginine vasotocin receptors among sexual phases of bluehead wrasse (Thalassoma bifasciatum). Gen Comp Endocrinol 179:451–464

    Article  CAS  PubMed  Google Scholar 

  • Leung CH, Abebe DF, Earp SE, Goode CT, Grozhik AV, Mididoddi P (2011) Neural distribution of vasotocin receptor mRNA in two species of songbird. Endocrinology 152:4865–4881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lolait SJ, O’Carrol AM, McBride OW, Konig M, Morel A, Brownstein MJ (1992) Cloning and characterization of a vasopressin V2 receptor and possible link to nephrogenic diabetes insipidus. Nature 357:336–339

    Article  CAS  PubMed  Google Scholar 

  • Marsh KE, Creutz LM, Hawkins MB, Godwin J (2006) Aromatase immunoreactivity in the bluehead wrasse brain, Thalassoma bifasciatum: immunolocalization and co-regionalization with arginine vasotocin and tyrosine hydroxylase. Brain Res 1126:91–101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martos-Sitcha JA, Fuentes J, Mancera JM, Martínez-Rodríguez G (2014) Variations in the expression of vasotocin and isotocin receptor genes in the gilthead sea bream Sparus aurata during different osmotic challenges. Gen Comp Endocrinol 197:5–17

    Article  CAS  PubMed  Google Scholar 

  • Maruska KP (2009) Sex and temporal variations of the vasotocin neuronal system in the damselfish brain. Gen Comp Endocrinol 160:194–204

  • Meidan R, Hsueh AJW (1985) Identification and characterization of arginine vasopressin receptors in the rat testis. Endocrinology 116:416–423

    Article  CAS  PubMed  Google Scholar 

  • Mikhailova MV, Mayeux PR, Jurkevich A, Kuenzel WJ, Madison FN, Periasamy A, Chen Y, Cornett LE (2007) Heterooligomerization between vasotocin and corticotropin-releasing hormone (CRH) receptors augments CRH-stimulated 3′,5′-cyclic adenosine monophosphate production. Mol Endocrinol 21:2178–2188

    Article  CAS  PubMed  Google Scholar 

  • Moons L, Cambre M, Batten TFC, Vandesande F (1989) Autoradiographic localization of binding-sites for vasotocin in the brain and pituitary of the sea bass (Dicentrarchus labrax). Neurosci Lett 100:11–16

    Article  CAS  PubMed  Google Scholar 

  • Nagarajan G, Aruna A, Chang CF (2015) Neuropeptide arginine vasotocin positively affects neurosteroidogenesis in the early brain of grouper, Epinephelus coioides. J Neuroendocrinol 27:718–736

    Article  CAS  PubMed  Google Scholar 

  • Northmore D (2011) The optic tectum. In: Farrell A (ed) Encyclopedia of fish physiology: from genome to environment. Elsevier, pp 131–142

  • Orcel H, Tobin VA, Alonso G, Rabie A (2002) Immunocytochemical localization of vasopressin V1a receptors in the rat pituitary gonadotropes. Endocrinology 143:4385–4388

    Article  CAS  PubMed  Google Scholar 

  • Ostrowski NL, Lolait SJ, Young WS 3rd (1994) Cellular localization of vasopressin V1a receptor messenger ribonucleic acid in adult male rat brain, pineal, and brain vasculature. Endocrinology 135:1511–1528

    Article  CAS  PubMed  Google Scholar 

  • Pierson PM, Guibbolini ME, Lahlou B (1996) A V1-type receptor for mediating the neurohypophysial hormone-induced ACTH release in trout pituitary. J Endocrinol 149:109–115

    Article  CAS  PubMed  Google Scholar 

  • Ramallo M, Pandolfi M (2011) Effects of arginine vasotocin on the hypothalamic-pituitary-gonads axis: a behavioural approach. Indian J Sci Technol 4:15–16

    Google Scholar 

  • Ramallo MR, Grober M, Cánepa MM, Morandini L, Pandolfi M (2012) Arginine vasotocin expression and participation in reproduction and social behavior in males of the cichlid fish Cichlasoma dimerus. Gen Comp Endocrinol 179:221–231

    Article  CAS  PubMed  Google Scholar 

  • Rawat A, Chaube R, Joy KP (2015) Molecular cloning, sequencing and phylogeny of vasotocin receptor genes in the air-breathing catfish Heteropneustes fossilis with sex dimorphic and seasonal variations in tissue expression. Fish Physiol Biochem 41:509–532

    Article  CAS  PubMed  Google Scholar 

  • Rawat A, Chaube R, Joy KP (2016) Effects of ovariectomy and estrogen replacement on expression of brain vasotocin receptor subtype genes in the catfish Heteropneustes fossilis. J Trans Neurosci 1:1–4

    Google Scholar 

  • Rawat A, Chaube R, Joy KP (2017) Effects of the fish spawning inducer ovaprim on vasotocin receptor gene expression in brain and ovary of the catfish Heteropneustes fossilis with a note on differential transcript expression in ovarian follicles. Gen Comp Endocrinol 241:24–32

  • Rodriguez M, Specker JL (1991) In vitro effects of arginine vasotocin on testosterone production by testes of rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol 83:249–257

    Article  CAS  PubMed  Google Scholar 

  • Rose JD, Moore FL (2002) Behavioral neuroendocrinology of vasotocin and vasopressin and the sensorimotor processing hypothesis. Front Neuroendocrinol 23:317–341. https://doi.org/10.1016/S0091-3022(02)00004-3

  • Saito N, Kinzler S, Koike TI (1990) Arginine vasotocin and mesotocin levels in the theca and granulosa layers of ovary during the oviposition cycle in hens (Gallus domesticus). Gen Comp Endocrinol 79:54–63

    Article  CAS  PubMed  Google Scholar 

  • Servili A, Le Page Y, Leprince J, Caraty A, Escobar S, Parhar IS, Seong JY, Vaudry H, Kah O (2011) Organization of two independent kisspeptin systems derived from evolutionary-ancient kiss genes in the brain of zebrafish. Endocrinology 152:1527–1540

    Article  CAS  PubMed  Google Scholar 

  • Singh V, Joy KP (2008) Immunocytochemical localization, HPLC characterization, and seasonal dynamics of vasotocin in the brain, blood plasma and gonads of the catfish Heteropneustes fossilis. Gen Comp Endocrinol 159:214–225

    Article  CAS  PubMed  Google Scholar 

  • Singh V, Joy KP (2009) Relative in vitro seasonal effects of vasotocin and isotocin on ovarian steroid hormone levels in the catfish Heteropneustes fossilis. Gen Comp Endocrinol 162:257–264

    Article  CAS  PubMed  Google Scholar 

  • Singh V, Joy KP (2010) An involvement of vasotocin in oocyte hydration in the catfish Heteropneustes fossilis: a comparison with effects of isotocin and hCG. Gen Comp Endocrinol 166:504–512

    Article  CAS  PubMed  Google Scholar 

  • Singh U, Kumar S, Singru PS (2012) Interaction between dopamine- and isotocin-containing neurones in the preoptic area of the catfish, Clarias batrachus: role in the regulation of luteinising hormone cells. J Neuroendocrinol 24:1398–1411

    Article  CAS  PubMed  Google Scholar 

  • Singh RK, Chaube R, Joy KP (2013) Differential and reproductive stage dependent regulation of vasotocin secretion by catecholamines in the catfish Heteropneustes fossilis. Comp Biochem Physiol Part A 166:619–626

    Article  CAS  Google Scholar 

  • Sugimoto T, Saito M, Mochizuki S, Watanabe Y, Hashimoto S, Kawashima H (1994) Molecular cloning and function expression of a cDNA encoding the human V1b receptor vasopressin receptor. J Biol Chem 269:27088–27092

    CAS  PubMed  Google Scholar 

  • Timmers RJM, Granneman JCM, Lambert JGD, van Oordt PG (1988) Estrogen-2-hydroxylase in the brain of the male African catfish, Clarias gariepinus. Gen Comp Endocrinol 72:190–203. https://doi.org/10.1016/0016-6480(88)90202-X

  • Tribollet E, Raufaste D, Maffrand J, Serradeil-Le Gal C (1999) Binding of the non-peptide vasopressin V1a receptor antagonist SR-49059 in the rat brain: an in vitro and in vivo autoradiographic study. Neuroendocrinology 69:113–120

    Article  CAS  PubMed  Google Scholar 

  • Vargas KJ, Sarmiento JM, Ehrenfeld P, Anazco CC, Villanueva C, Carmona PL, Brenet M, Navarro J, Esterl WM, Gonzalez CB (2009) Postnatal expression of V2 vasopressin receptor splice variants in the rat cerebellum. Differentiation 77:377–385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young LJ, Wang Z, Cooper TT, Albers HE (2000) Vasopressin (V1a) receptor binding, mRNA expression and transcriptional regulation by androgen in the Syrian hamster brain. J Neuroendocrinol 12:1179–1185

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported by a research grant of Department of Science and Technology, New Delhi (Grant No. SA/SO/AS-43/2009) to K. P. Joy (Principal Investigator) and Radha Chaube (Co-Investigator), which is gratefully acknowledged.

Author information

Authors and Affiliations

  1. Department of Zoology, Institute of Science, Banaras Hindu University, Varanasi, 221005, India

    Arpana Rawat & Radha Chaube

  2. Department of Biotechnology, Cochin University of Science and Technology, Kochi, 682022, India

    Keerrikkattil P. Joy

Authors
  1. Arpana Rawat
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Radha Chaube
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Keerrikkattil P. Joy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Radha Chaube or Keerrikkattil P. Joy.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rawat, A., Chaube, R. & Joy, K.P. In situ localization of vasotocin receptor gene transcripts in the brain-pituitary-gonadal axis of the catfish Heteropneustes fossilis: a morpho-functional study. Fish Physiol Biochem 45, 885–905 (2019). https://doi.org/10.1007/s10695-018-0590-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-018-0590-1

Keywords

Search

Navigation