Skip to main content
SpringerLink
Log in

Tryptophan supplementation helps totoaba (Totoaba macdonaldi) juveniles to regain homeostasis in high-density culture conditions

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

Abstract

High-density culture brings with it chronic stress situations that affect fish welfare. In order to evaluate the effect of tryptophan (Trp) levels on the response to stress, Totoaba macdonaldi juveniles were stocked at low (13.5 kg m−3) and high (27.0 kg m−3) densities (32.5 and 56.4 kg m−3, respectively, at the end of the experiment) in 100-L tanks and fed for 63 days with experimental diets containing different Trp levels: control diet CD0.42 (0.42%) and three supplemented diets with 0.99, 1.55 and 2.19% (0.99Trp, 1.55Trp and 2.19Trp, respectively) (three tanks × density × diet). The high-density stocking fed with CD0.42 diets showed significantly increased blood parameters. Trp decreased catalase (CAT) activity in low- and high-density stocking, while the superoxide dismutase (SOD) activity showed no difference. Serotonin (5-hydroxytryptamine, 5-HT) content decreased, and the serotonin turnover ratio (5-HIAA:5-HT) increased in the brains of fish fed with the CD0.42 diet. Indeed, Trp-supplemented diets helped to restore homeostasis in high-density growth conditions as evaluated by the hematological and plasma parameters as well as the serotonergic activity. When the fish were provided a diet containing moderate Trp levels, plasma cortisol increased under high-density conditions. However, no differences were observed among stock densities when totoaba were fed with the 2.19Trp diet. Notably, survival was unaffected by both Trp or densities, but weight gain (WG) decreased with the dietary Trp levels in the high density culture. In sum, Trp supplementation decreased the parameter values linked to stress response on totoaba juveniles cultured at high stock densities.

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.

Similar content being viewed by others

References

  • Abdo-de la Parra MI, Rodríguez-Ibarra LE, Campillo-Martínez F, Velasco-Blanco G, García-Aguilar N, Álvarez-Lajonchère LS, Voltolina D (2010) Efecto de la densidad de siembra sobre el crecimiento y supervivencia larval del pargo lunarejo Lutjanus guttatus. Rev Biol Mar Oceanogr 45:141–146

    Google Scholar 

  • Aebi H (1984) Catalase “in vitro”. Methods Enzymol 105:121–126

    CAS  PubMed  Google Scholar 

  • Akhtar MS, Pal AK, Sahu NP, Ciji A, Meena DK, Das P (2013) Physiological responses of dietary tryptophan fed Labeo rohita to temperature and salinity stress. J Anim Physiol Anim Nutr 97:1075–1083

    CAS  Google Scholar 

  • Andrade T, Afonso A, Pérez-Jiménez A, Oliva-Teles A, de las Heras V, Mancera JM, Serradeiro R, Costas B (2015) Evaluation of different stocking densities in a Senegalese sole (Solea senegalensis) farm: Implications for growth, humoral immune parameters and oxidative status. Aquac. 438:6–11

    CAS  Google Scholar 

  • Association of Official Analytical Chemists (2000) Official Methods of Analysis, AOAC, Gaithersburg, MD, USA. p.1018

  • Atencio-García V, Genes-López F, Madariaga-Mendoza D, Pardo-Carrasco S (2007) Hematología y química sanguínea de juveniles de rubio (Salminu saffinis Pisces: Characidae) del río Sinú. Acta Biol Colomb 12:27–40

    Google Scholar 

  • Azouzi S, Santuz H, Morandat S, Pereira C, Côté F, Hermine O, El Kirat K, Colin Y, Le Van Kim C, Etchebest C, Amireault P (2017) Antioxidant and Membrane Binding Properties of Serotonin Protect Lipids from Oxidation. Biophys J 112:1863–1873

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baldwin L (2010) The effects of stocking density on fish welfare. The Plymouth Stud Sci 4:372–383

    Google Scholar 

  • Barcellos LJG, Kreutz LC, Quevedo RM (2006) Previous chronic stress does not alter the cortisol response to an additional acute stressor in jundiá (Rhamdia quelen, Quoy and Gaimard) fingerlings. Aquac. 253:317–321

    CAS  Google Scholar 

  • Bardullas U, Giordano M, Rodríguez VM (2011) Chronic atrazine exposure causes disruption of the spontaneous locomotor activity and alters the striatal dopaminergic system of the male Sprague–Dawley rat. Neurotoxicol Teratol 33:263–272

    CAS  PubMed  Google Scholar 

  • Barrera-Guevara JC (1990) The conservation of Totoaba macdonaldi (Gilbert), (Pisces: Sciaenidae), in the Gulf of California. México J Fish Biol 37:201–202

    Google Scholar 

  • Barton BA (2002) Stress in Fishes: A diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42:517–525

    CAS  PubMed  Google Scholar 

  • Barton BA, Iwama GK (1991) Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Annu Rev Fish Dis 1:3–26

    Google Scholar 

  • Basic D, Schjolden J, Krogdahl Å, Von Krogh K, Hillestad M, Winberg S, Mayer I, Skjerve E, Höglund E (2013) Changes in regional brain monoaminergic activity and temporary down-regulation in stress response from dietary supplementation with L-tryptophan in Atlantic cod (Gadus morhua). Br J Nutr 109:2166–2174

    CAS  PubMed  Google Scholar 

  • Best J, Nijhout HF, Reed M (2010) Serotonin synthesis, release and reuptake in terminals: a mathematical model. Theor Biol Med Model 7:1–26

    Google Scholar 

  • Bisesi JH, Sweet LE, van den Hurk P, Klaine SJ (2016) Effects of an antidepressant mixture on the brain serotonin and predation behavior of hybrid striped bass. Environ Toxicol Chem 35:938–945

    CAS  PubMed  Google Scholar 

  • Blaxhall PC, Daisley PW (1973) Routine hematological methods for use with fish blood. J Fish Biol 5:771–781

    Google Scholar 

  • Boadle-Biber MC (1993) Regulation of serotonin synthesis. Prog Biophys Mol Biol 60:1–15

    CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  PubMed  Google Scholar 

  • Bubenik GA, Pang SF (1997) Melatonin levels in the gastrointestinal tissues of fish, amphibians, and reptile. Gen Comp Endocrinol 106:415–419

    CAS  PubMed  Google Scholar 

  • Cabanillas-Gámez M, López LM, Galaviz MA, True CD, Bardullas U (2017) Effect of L-tryptophan supplemented diets on serotonergic system and plasma cortisol in Totoaba macdonaldi (Gilbert, 1890) juvenile exposed to acute stress by handling and hypoxia. Aquac Res 49:847–857

    Google Scholar 

  • Chen Y, Guillemin GJ (2009) Kynurenine Pathway Metabolites in Humans: Disease and Healthy States. Int J of Tryptophan Res 2:1–19

    Google Scholar 

  • Ciji A, Prasad N, Kumar A, Shahbaz M (2015) Dietary L-tryptophan modulates growth and immuno-metabolic status of Labeo rohita juveniles exposed to nitrite. Aquac Res 46:2013–2024

    CAS  Google Scholar 

  • Costas B, Arangão C, Mancera JM, Dinis MT, Conceição LEC (2008) High stocking density induces crowding stress and affects amino acid metabolism in Senegalese sole Solea senegalensis (Kaup 1858) juveniles. Aquac Res 39:1–9

    CAS  Google Scholar 

  • Coulibaly A, Ouattara IN, Koné T, N'Douba V, Snoeks J, Bi GG, Kouamélan EP (2007) First results of floating cage culture of the African catfish Heterobranchus longifilis Valenciennes, 1840: Effect of stocking density on survival and growth rates. Aquac. 263:61–67

    Google Scholar 

  • De Block M, Stoks R (2008) Compensatory growth and oxidative stress in a damselfly. P Roy Socof Lon B Biol 275:781–785

    Google Scholar 

  • Di Marco P, Priori A, Finoia MG, Massari A, Mandich A, Marino G (2008) Physiological responses of European sea bass Dicentrarchus labrax to different stocking densities and acute stress challenge. Aquac. 275:319–328

    Google Scholar 

  • Diógenes AF, Teixeira C, Almeida E, Skrzynska A, Costas B, Oliva-Teles A, Peres H (2019) Effects of dietary tryptophan and chronic stress in gilthead seabream (Sparus aurata) juveniles fed corn distillers dried grains with solubles (DDGS) based diets. Aquac. 498:396–404

    Google Scholar 

  • DOF (2009) AVISO por el que se informa al público en general que la Comisión Nacional de Áreas Naturales Protegidas ha concluido la elaboración del Programa de Manejo de la Reserva de la Biosfera Alto Golfo de California y Delta del Río Colorado, ubicada en aguas del Golfo de California y en los municipios de Mexicali, Estado de Baja California, y de Puerto Peñasco y de San Luis Río Colorado, Estado de Sonora 113.

  • Dornelles Y, Zafalon-Silva B, Wiegand M, Berteaux R (2015) Leucocyte profile and growth rates as indicators of crowding stress in pejerrey fingerlings (Odontesthes bonariensis). Aquac Res 46:2270–2276

    Google Scholar 

  • Folch J, Lees M, Stanley G (1957) A simple method of the isolation and purification of total lipids from animal tissue. The J of Biol Chem 226:497–509

    CAS  Google Scholar 

  • Galano A, Xian Tan D, Reiter RJ (2011) Melatonin as a naturally against oxidative stress: aphysicochemical examination. J Pineal Res 51:1–16

    CAS  PubMed  Google Scholar 

  • Goldenfarb PB, Bowyer FP, Hall E, Brosious E (1971) Reproducibility in the Hematology Laboratory: The Microhematocrit determination. Am J Clin Pathol 56:35–39

    CAS  PubMed  Google Scholar 

  • Hacışevk A, Baba B (2018) An Overview of Melatonin as an Antioxidant Molecule: A Biochemical Approach. https://doi.org/10.5772/intechopen.79421

    Google Scholar 

  • Herrera M, Ruiz-Jarabo I, Hachero I, Vargas Chacoff L, Amo A, Mancera JM (2012) Stocking density affects growth and metabolic parameters in the brill (Scophthalmus rhombus). Aquac Int 20:1041–1052

    CAS  Google Scholar 

  • Herrera M, Castanheira MF, Conceição LEC, Martins CI (2014) Linking risk taking and the behavioral and metabolic responses to confinement stress in gilthead seabream Sparus aurata. Appl Anim Behav Sci 155:101–108

    Google Scholar 

  • Höglund E, Bakke MJ, Øverli Ø, Winberg S, Nilsson GE (2005) Suppression of aggressive behavior in juvenile Atlantic cod (Gadus morhua) by l-tryptophan supplementation. Aquac. 249:525–531

    Google Scholar 

  • Höglund E, Sørensen C, Bakke MJ, Nilsson GE, Øverli O (2007) Attenuation of stress-induced anorexia in brown trout (Salmo trutta) by pre-treatment with dietary L-tryptophan. Br J Nutr 97:786–789

    PubMed  Google Scholar 

  • Hoseini SM, Hosseini SA (2010) Effect of dietary L-tryptophan on osmotic stress tolerance in common carp, Cyprinus carpio, juveniles. Fish Physiol Biochem 36:1061–1067

    CAS  PubMed  Google Scholar 

  • Hoseini SM, Hosseini SA, Soudagar M (2012) Dietary tryptophan changes serum stress markers, enzyme activity, and ions concentration of wild common carp Cyprinus carpio exposed to ambient copper. Fish Physiol Biochem 38:1419–1426

    CAS  PubMed  Google Scholar 

  • Hoseini SM, Mirghaed AT, Mazandarani M, Zoheiri F (2016) Serum cortisol, glucose, thyroid hormones' and non-specific immune responses of Persian sturgeon, Acipenser persicus to exogenous tryptophan and acute stress. Aquac. 462:17–23

    CAS  Google Scholar 

  • Iguchi K, Ogawa K, Nagae M, Ito F (2003) The influence of rearing density on stress response and disease susceptibility of ayu (Plecoglossu saltivelis). Aquac. 220:515–523

    Google Scholar 

  • Iwama G, Vijayan M, Forsyth R, Ackerman P (1999) Heat Shock Proteins and Physiological Stress in Fish. Am Zool 39:901–909

    CAS  Google Scholar 

  • Iwama GK, Afonso LOB, Todgham A, Ackerman P, Nakano K (2004) Are hsps suitable for indicating stressed states in fish? The J of Exp Biol 207:15–19

    CAS  Google Scholar 

  • Jiang WD, Wen HL, Liu Y, Jiang J (2016) Enhanced muscle nutrient content and flesh quality, resulting from tryptophan, is associated with anti-oxidative damage referred to the Nrf2 and TOR signalling factors in young grass carp (Ctenopharyn godonidella): Avoid tryptophan deficiency or excess. Food Chem 199:210–219

    CAS  PubMed  Google Scholar 

  • Kezuka H, Iigo M, Furukawa K, Aida K, Hanyu I (1992) Effects of photoperiod, pinealectomy and ophthalmectomy on circulating melatonin rhythms in the Goldfish, Carassius auratus. Zool Sci 9:1047–1053

    CAS  Google Scholar 

  • Kpundeh MD, Xu P, Yang H, Qiang J, He J (2013) Stocking densities and chronic zero culture water exchange stress effects on biological performances, hematological and serum biochemical indices of GIFT tilapia juveniles (Oreochromis niloticus). J Aquac Res Develop 4:1–5

    Google Scholar 

  • Krol J, Zakęś Z (2016) Effect of dietary L-tryptophan on cannibalism, survival and growth in pikeperch Sander lucio perca (L.) post-larvae. Aquac Int 24:441–451

    CAS  Google Scholar 

  • Kumar P, Saurabh S, Pal AK, Sahu NP, Arasu ART (2014) Stress mitigating and growth enhancing effect of dietary tryptophan in rohu (Labeo rohita, Hamilton 1822) fingerling. Fish Physiol Biochem 40:1325–1338

    CAS  PubMed  Google Scholar 

  • Laranja JLQ, Quinitio ET, Catacutan MR, Coloso RM (2010) Effects of dietary L-tryptophan on the agonistic behavior, growth and survival of juvenile mud crab Scylla serrata. Aquac. 310:84–90

    CAS  Google Scholar 

  • Le Floc'h N, Seve B (2007) Biological roles of tryptophan and its metabolism: Potential implications for pig feeding. Livest Sci 112:23–32

    Google Scholar 

  • Lepage O, Tottmar O, Winberg S (2002) Elevated dietary intake of L-tryptophan counteracts the stress-induced elevation of plasma cortisol in rainbow trout (Oncorhynchus mykiss). J Exp Biol 205:3679–3687

    CAS  PubMed  Google Scholar 

  • Lepage O, Tarson ET, Mayer I, Winberg S (2005) Tryptophan affects both gastrointestinal melatonin production andinterrenal activity in stressed and non-stressed rainbow trout. J Pineal Res 38:264–271

    CAS  PubMed  Google Scholar 

  • López LM, Flores-Ibarra M, Bañuelos-Vargas I, Galaviz MA, True CD (2015) Effect of fishmeal replacement by soy protein concentrate with taurine supplementation on growth performance, hematological and biochemical status, and liver histology of totoaba juveniles (Totoaba macdonaldi). Fish Physiol Biochem 41:921–936

    PubMed  Google Scholar 

  • Madrid J, Camilo P, Viana MT, Lazo JP (2019) Dietary lysine requirement for juvenile, Totoaba macdonaldi. Aquac. 500:92–98

    CAS  Google Scholar 

  • McCord JM, Fridovich I (1969) Superoxide Dismutase: an enzymatic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049–6055

    CAS  PubMed  Google Scholar 

  • Medeiros LR, Mager EM, Grosell M, McDonald MD (2010) The serotonin subtype 1A receptor regulates cortisol secretion in the Gulf toadfish, Opsanus beta. Gen Comp Endocrinol 168:377–387

    CAS  PubMed  Google Scholar 

  • Minjarez-Osorio C, González-Félix ML, Pérez-Velazquez M (2012) Biological performance of Totoaba macdonaldi in response to dietary protein level. Aquac. 362-363:50–55

    CAS  Google Scholar 

  • Mohsen AT (2012) Effects of dietary protein levels and rearing density on growth performance and stress response of nile tilapia, Oreochromis niloticus (L). Int Aquat Res 4:1–13

    Google Scholar 

  • Montero D, Izquierdo MS, Tort L, Robaina L, Vergara JM (1999) High stocking density produces crowding stress altering some physiological and biochemical parameters in gilthead seabream, Sparus aurata, juveniles. Fish Physiol Biochem 20:53–60

    CAS  Google Scholar 

  • Morandini L, Ramallo MR, Moreira RG, Höcht C, Somoza GM, Silva A, Pandolf M (2015) Serotonergic outcome, stress and sexual steroid hormones, and growth in a South American cichlid fish fed with an L-tryptophan enriched diet. Gen Comp Endocrinol 223:27–37

    CAS  PubMed  Google Scholar 

  • Musumeci G, Loreto C, Trovato FM, Giunta S, Imbesi R, Castrogiovanni P (2014) Serotonin (5HT) expression in rat pups treated with high-tryptophan diet during fetal and early postnatal development. Acta Histochem 116:335–343

    CAS  PubMed  Google Scholar 

  • NOM-062-ZOO, NOM (1999) Especificaciones técnicas para la producción, cuidado y uso de los animales de laboratorio 58.

  • Papoutsoglou SE, Karakatsouli N, Chiras G (2005) Dietary l-tryptophan and tank colour effects on growth performance of rainbow trout (Oncorhynchus mykiss) juveniles reared in a recirculating water system. Aquac Eng 32:277–284

    Google Scholar 

  • Pérez-Jimenez A, Peres H, Cruz-Rubio V, Oliva-Teles A (2012) The effect of dietary methionine and white tea on oxidative status of gilthead sea bream (Sparus aurata). Br J Nutr 108:1202–1209

    PubMed  Google Scholar 

  • Pickering AD (1993) Growth and stress in fish production. Aquac 111(5):l–63

    Google Scholar 

  • Pickering AD, Pottinger TG (1995) Biochemical effects of stress, In: Hochachka, P.W., Mommsen T.P. (Eds), Biochem. Mol. Biol. Fishes. Sci. Direct. 5:349-379.

  • Raicevich S, Minute F, Finoia MG, Caranfa F, Di Muro P, Scapolan L, Beltramini M (2014) Synergistic and antagonistic effects of thermal shock, air exposure, and fishing capture on the physiological stress of Squilla mantis (Stomatopoda). PLoS One 9:1–12

    Google Scholar 

  • Rotllant J, Pavlidis M, Kentouri M, Abad ME, Tort L (1997) Non-specificimmune responses in the red porgy Pagrus pagrus after crowding stress. Aquac. 156:279–290

    Google Scholar 

  • Rueda-López S, Lazo JP, Correa RG, Viana MT (2011) Effect of dietary protein and energy levels on growth, survival and body composition of juvenile Totoaba macdonaldi. Aquac. 319:385–390

    Google Scholar 

  • Ruiz-Durá MF (1985) Recursos pesqueros de las costas de México. Editorial Limunsa, México 1-208.

  • Sánchez P, Ambrosio PP, Flos R (2010) Stocking density and sex influence individual growth of Senegalese sole (Solea senegalensis). Aquac. 300:93–101

    Google Scholar 

  • Satriyo TB, Galaviz MA, Salze G, López LM (2017) Assessment of dietary taurine essentiality on the physiological state of juvenile Totoaba macdonaldi. Aquac Res 48:5677–5689

    CAS  Google Scholar 

  • Stenfors C, Ross SB (2002) Evidence for involvement of protein kinases in the regulation of serotonin synthesis and turnover in the mouse brain in vivo. J Neural Transm 109:1353–1363

    CAS  PubMed  Google Scholar 

  • Taylor BL, Rojas-Bracho L, Moore J, Jaramillo-Legorreta A, VerHoef JM, Cardenas-Hinojosa G, Nieto-Garcia E, Barlow J, Gerrodette T, Tregenza N, Thomas L, Hammond PS (2016) Extinction is imminent for Mexico's endemic porpoise unless fishery by catch is eliminated. Conserv Lett 10:588–595. https://doi.org/10.1111/conl.12331

    Article  Google Scholar 

  • Tejpal CS, Pal AK, Sahu NP, Kumar JA, Muthappa NA, Vidya S, Rajan MG (2009) Dietary supplementation of L-tryptophan mitigates crowding stress and augments the growth in Cirrhinus mrigala fingerling. Aquac. 293:272–277

    CAS  Google Scholar 

  • Tejpal CS, Sumitha EB, Pal AK, Murthy HS, Sahu NP, Siddaiah GM (2014) Effect of dietary supplementation of L-tryptophanon thermal tolerance and oxygen consumption rate in Cirrhinus mrigala fingerlings under varied stocking density. J Therm Biol 41:59–64

    CAS  PubMed  Google Scholar 

  • Thivend P, Mercier C, Guilbot A (1972) Determination of starch with glucoamylase. In: Methods in Carbohydrate Chemistry (ed. by R.L. Whistler & J.N. Bemiller), pp. 100–105. Academic Press, New York, NY, USA.

  • Trejo-Escamilla I, Galaviz MA, Flores-Ibarra M, Álvarez González CA, López LM (2017) Replacement of fishmeal by soya protein concentrate in diets of Totoaba macdonaldi (Gilbert, 1890) juveniles: effect on the growth performance, in vitro digestibility, digestive enzymes and the haematological and biochemistry parameters. Aquac Res 48:4038–4057

    CAS  Google Scholar 

  • True CD (2012) Desarrollo de la biotecnia de cultivo de Totoaba macdonaldi. Universidad Autónoma de Baja California 135 p.

  • True CD, Silva A, Castro N (1997) Acquisition of broodstock of Totoaba macdonaldi: Field handling, decompression, and prophylaxis of an endangered species. Prog Fish Cult 59:246–248

    Google Scholar 

  • Wendelaar-Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625

    CAS  PubMed  Google Scholar 

Download references

Funding

This study was supported by Universidad Autónoma de Baja California (UABC), by the Mexican National Council for Science and Technology (CONACYT) (Stimulus Program for innovation PROINNOVA-2015 no. 220455), and by the fellowship no. 197039 (Miguel A. Cabanillas-Gámez). A reference made to a trademark or a patented product does not represent an endorsement by the Universidad Autónoma de Baja California and does not imply its approval to exclude other products that may also be suitable.

Author information

Authors and Affiliations

  1. Facultad de Ciencias Marinas, Universidad Autónoma de Baja California (UABC), Carretera Tijuana-Ensenada 3917, Playitas, Ensenada, 22860, B.C., México

    Miguel Cabanillas-Gámez, Mario A Galaviz & Lus M López

  2. Facultad de Ciencias, Universidad Autónoma de Baja California (UABC), Carretera Tijuana-Ensenada 3917, Playitas, Ensenada, 22860, B.C., México

    Ulises Bardullas

  3. Unidad de Química en Sisal, Facultad de Química, Universidad Nacional Autónoma de México, Puerto de Abrigo S/N, Sisal, Hunucma, 97356, Yucatán, México

    Sergio Rodriguez

  4. Departamento de Neurobiología Conductual y Cognitiva, Instituto de Neurobiología, Universidad Nacional Autónoma de México, Boulevard Juriquilla 3001, Querétaro, 76230, Querétaro, México

    Verónica M Rodriguez

Authors
  1. Miguel Cabanillas-Gámez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ulises Bardullas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mario A Galaviz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sergio Rodriguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Verónica M Rodriguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lus M López
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lus M López.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

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

Drs.López and Bardullas share co-seniority in this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cabanillas-Gámez, M., Bardullas, U., Galaviz, M.A. et al. Tryptophan supplementation helps totoaba (Totoaba macdonaldi) juveniles to regain homeostasis in high-density culture conditions. Fish Physiol Biochem 46, 597–611 (2020). https://doi.org/10.1007/s10695-019-00734-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-019-00734-2

Keywords

Search

Navigation