Log in

An acute increase in water temperature can increase free amino acid concentrations in the blood, brain, liver, and muscle in goldfish (Carassius auratus)

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

Abstract

Water temperature directly affects the body temperature in fish, so increasing water temperatures in oceans and rivers will lead to increases in fish body temperatures. Whilst a range of responses of fish to increases in water temperature have been measured, amino acid metabolism in a fish under high water temperature (HT) conditions has not been investigated. The aim of this study was to determine the effects of an acute increase in water temperature on oxygen consumption, plasma cortisol concentrations, and free amino acid concentrations in plasma and several tissues in goldfish (Carassius auratus). Oxygen consumption and plasma cortisol concentrations were increased in goldfish exposed to HT (30 ± 1 °C) for 200 min compared with goldfish at a control water temperature (CT 17 ± 1 °C). Oxygen consumption and plasma cortisol concentrations in both groups of fish combined were positively correlated. When goldfish were exposed to HT for 300 min oxygen consumption and plasma concentrations of 15 free amino acids were increased compared with goldish at CT. Concentrations of several free amino acids were increased to varying extents in the brain, liver, and muscle tissues. In conclusion, an acute increase in water temperature affected amino acid metabolism differently in the brain, liver, and muscle tissues. Goldfish will be a useful species for further studies of the possible roles of various amino acids in the brain, muscle, and liver during acute increases in water temperature in fish.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Similar content being viewed by others

References

  • Aragão C, Corte-Real J, Costas B, Dinis MT, Conceição LEC (2008) Stress response and changes in amino acid requirements in Senegalese sole (Solea senegalensis Kaup 1858). Amino Acids 34:143–148

    Article  CAS  PubMed  Google Scholar 

  • Asechi M, Tomonaga S, Tachibana T, Han L, Hayamizu K, Denbow DM, Furuse M (2006) Intracerebroventricular injection of L-serine analogs and derivatives induces sedative and hypnotic effects under an acute stressful condition in neonatal chicks. Behav Brain Res 170:71–77

    Article  CAS  Google Scholar 

  • Baird CH, Niederlechner S, Beck R, Kallweit AR, Wischmeyer PE (2013) L-threonine induces heat shock protein expression and decreases apoptosis in heat-stressed intestinal epithelial cells. Nutrition 29:1404–1411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernier NJ, Peter RE (2001) The hypothalamic-pituitary-interrenal axis and the control of food intake in teleost fish. Comp Biochem Physiol B Biochem Mol Biol 129:639–644

    Article  CAS  PubMed  Google Scholar 

  • Boogers I, Plugge W, Stokkermans YQ, Duchateau AL (2008) Ultra-performance liquid chromatographic analysis of amino acids in protein hydrolysates using an automated pre-column derivatisation method. J Chromatogr A 1189:406–409

    Article  CAS  PubMed  Google Scholar 

  • Brillon DJ, Zheng B, Campbell RG, Matthews DE (1995) Effect of cortisol on energy expenditure and amino acid metabolism in humans. Am J Physiol Endocrinol Metab 268:E501–E513

    Article  CAS  Google Scholar 

  • Bystriansky JS, Frick NT, Ballantyne JS (2007) Intermediary metabolism of Arctic char Salvelinus alpinus during short-term salinity exposure. J Exp Biol 210:1971–1985

    Article  CAS  PubMed  Google Scholar 

  • Carlton ED, Demas GE (2017) Glucose and insulin modulate sickness responses in male Siberian hamsters. Gen Comp Endocrinol 242:83–91

    Article  CAS  PubMed  Google Scholar 

  • Chowdhury VS (2018) Heat stress biomarker amino acids and neuropeptide afford thermotolerance in chicks. J Poult Sci 56:1–11. https://doi.org/10.2141/jpsa.0180024

    Article  Google Scholar 

  • Chowdhury VS, Tomonaga S, Ikegami T, Erwan E, Ito K, Cockrem JF, Furuse M (2014) Oxidative damage and brain concentrations of free amino acid in chicks exposed to high ambient temperature. Comp Biochem Physiol A Mol Integr Physiol 169:70–76

    Article  CAS  PubMed  Google Scholar 

  • Chowdhury VS, Han G, Bahry MA, Tran PV, Do PH, Yang H, Furuse M (2017) L-citrulline acts as potential hypothermic agent to afford thermotolerance in chicks. J Therm Biol 69:163–170

    Article  CAS  PubMed  Google Scholar 

  • Ciji A, Sahu NP, Pal AK, Dasgupta S, Akhtar MS (2012) Alterations in serum electrolytes, antioxidative enzymes and haematological parameters of Labeo rohita on short-term exposure to sublethal dose of nitrite. Fish Physiol Biochem 38:1355–1365

    Article  CAS  PubMed  Google Scholar 

  • Cockrem JF (2013) Individual variation in glucocorticoid stress responses in animals. Gen Comp Endocrinol 181:45–58

    Article  CAS  PubMed  Google Scholar 

  • Cockrem JF, Bahry MA, Chowdhury VS (2018) Cortisol responses of goldfish (Carassius auratus) to air exposure, chasing, and increased water temperature. Gen Comp Endocrinol 270:18–25

    Article  CAS  PubMed  Google Scholar 

  • Costas B, Aragão C, Dias J, Afonso A, Conceição LE (2013) Interactive effects of a high-quality protein diet and high stocking density on the stress response and some innate immune parameters of Senegalese sole Solea senegalensis. Fish Physiol Biochem 39:1141–1151

    Article  CAS  Google Scholar 

  • Cota D, Proulx K, Smith KAB, Kozma SC, Thomas G, Woods SC, Seeley RJ (2006) Hypothalamic mTOR signaling regulates food intake. Science 312:927–930

    Article  CAS  PubMed  Google Scholar 

  • DeTolla LJ, Srinivas S, Whitaker BR, Andrews C, Hecker B, Kane AS, Reimschuessel R (1995) Guidelines for the care and use of fish in research. ILAR J 37:159–173

    Article  PubMed  Google Scholar 

  • Ellis T, James JD, Stewart C, Scott AP (2004) A non-invasive stress assay based upon measurement of free cortisol released into the water by rainbow trout. J Fish Biol 65:1233–1252

    Article  CAS  Google Scholar 

  • Erwan E, Chowdhury VS, Nagasawa M, Goda R, Otsuka T, Yasuo S, Furuse M (2014) Oral administration of D-aspartate, but not L-aspartate, depresses rectal temperature and alters plasma metabolites in chicks. Life Sci 109:65–71

    Article  CAS  PubMed  Google Scholar 

  • Eslamloo K, Akhavan SR, Fallah FJ, Henry MA (2014) Variations of physiological and innate immunological responses in goldfish (Carassius auratus) subjected to recurrent acute stress. Fish Shellfish Immunol 37:147–153

    Article  CAS  PubMed  Google Scholar 

  • Fanouraki E, Papandroulakis N, Pavlidis M (2016) Non-invasive stress indicators in Mediterranean mariculture: effect of fish size on water cortisol release rate. Symposium on Oceanography Fisheries 2009 Proc 9, pp 711–715

  • Gandar A, Laffaille P, Canlet C, Tremblay-Franco M, Gautier R, Perrault A, Gress L, Mormède P, Tapie N, Budzinski H, Jean S (2017) Adaptive response under multiple stress exposure in fish: from the molecular to individual level. Chemosphere 188:60–72

    Article  CAS  PubMed  Google Scholar 

  • Han G, Yang H, Bahry MA, Tran PV, Do PH, Ikeda H, Furuse M, Chowdhury VS (2017) L-leucine acts as a potential agent in reducing body temperature at hatching and affords thermotolerance in broiler chicks. Comp Biochem Physiol A Mol Integr Physiol 204:48–56

    Article  CAS  PubMed  Google Scholar 

  • Han G, Yang H, Bungo T, Ikeda H, Wang Y, Nguyen LT, Eltahan HM, Furuse M, Chowdhury VS (2018) In ovo L-leucine administration stimulates lipid metabolisms in heat-exposed male, but not female, chicks to afford thermotolerance. J Therm Biol 71:74–82

    Article  CAS  PubMed  Google Scholar 

  • Heath AG, Hughes GM (1973) Cardiovascular and respiratory changes during heat stress in rainbow trout (Salmo gairdneri). J Exp Biol 59:323–338

    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

    Article  CAS  PubMed  Google Scholar 

  • Ikegami T, Takemura A, Choi E, Suda A, Tomonaga S, Badruzzaman M, Furuse M (2015) Increase in telencephalic dopamine and cerebellar norepinephrine contents by hydrostatic pressure in goldfish: the possible involvement in hydrostatic pressure-related locomotion. Fish Physiol Biochem 41:1105–1115

    Article  CAS  PubMed  Google Scholar 

  • Ito K, Erwan E, Nagasawa M, Furuse M, Chowdhury VS (2014) Changes in free amino acid concentrations in the blood, brain and muscle of heat-exposed chicks. Br Poult Sci 55:644–652

    Article  CAS  PubMed  Google Scholar 

  • Ito K, Bahry MA, Hui Y, Furuse M, Chowdhury VS (2015) Acute heat stress up-regulates neuropeptide Y precursor mRNA expression and alters brain and plasma concentrations of free amino acids in chicks. Comp Biochem Physiol A Mol Integr Physiol 187:13–19

    Article  CAS  PubMed  Google Scholar 

  • ** G, Kataoka Y, Tanaka M, Mizuma H, Nozaki S, Tahara T, Mizuno K, Yamato M, Watanabe Y (2009) Changes in plasma and tissue amino acid levels in an animal model of complex fatigue. Nutrition 25:597–607

    Article  CAS  PubMed  Google Scholar 

  • Kala M, Nivsarkar M (2016) Role of cortisol and superoxide dismutase in psychological stress induced anovulation. Gen Comp Endocrinol 225:117–124

    Article  CAS  PubMed  Google Scholar 

  • Kim DH, Kim SH, Jeong WS, Lee HY (2013) Effect of BCAA intake during endurance exercises on fatigue substances, muscle damage substances, and energy metabolism substances. J Exerc Nutr Biochem 17:169–180

    Article  Google Scholar 

  • Kraemer WJ, Ratamess NA, Volek JS, Häkkinen K, Rubin MR, French DN, Gómez AL, McGuigan MR, Scheett TP, Newton RU, Spiering BA, Izquierdo M, Dioguardi FS (2006) The effects of amino acid supplementation on hormonal responses to resistance training overreaching. Metab Clin Exp 55:282–291

    Article  CAS  PubMed  Google Scholar 

  • Kurata K, Shigemi K, Tomonaga S, Aoki M, Morishita K, Denbow DM, Furuse M (2011) L-ornithine attenuates corticotropin-releasing factor-induced stress responses acting at GABAA receptors in neonatal chicks. Neuroscience 172:226–231

    Article  CAS  PubMed  Google Scholar 

  • Madeira D, Vinagre C, Diniz MS (2016) Are fish in hot water? Effects of warming on oxidative stress metabolism in the commercial species Sparus aurata. Ecol Indic 63:324–331

    Article  CAS  Google Scholar 

  • Peckins MK, Susman EJ, Negriff S, Noll JG, Trickett PK (2016) Cortisol profiles: a test for adaptive calibration of the stress response system in maltreated and nonmaltreated youth. Dev Psychopathol 28:1563–1564

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Powell EN, Kasschau M, Chen E, Koenig M, Pecon J (1982) Changes in the free amino acid pool during environmental stress in the gill tissue of the oyster, Crassostrea virginica. Comp Biochem Physiol A Mol Integr Physiol 71:591–598

    Article  Google Scholar 

  • Randall DJ, Tsui TKN (2002) Ammonia toxicity in fish. Mar Pollut Bull 45:17–23

    Article  CAS  Google Scholar 

  • Ryan SN (1995) The effect of chronic heat stress on cortisol levels in the antarctic fish Pagothenia borchgrevinki. Experientia 51:768–774

    Article  CAS  Google Scholar 

  • Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89

    CAS  PubMed  Google Scholar 

  • Sejian V, Singh AK, Sahoo A, Naqvi SMK (2014) Effect of mineral mixture and antioxidant supplementation on growth, reproductive performance and adaptive capability of Malpura ewes subjected to heat stress. J Anim Physiol Anim Nutr (Berl) 98:72–83

    Article  CAS  Google Scholar 

  • Sivakumar AVN, Singh G, Varshney VP (2010) Antioxidants supplementation on acid base balance during heat stress in goats. Asian-Australas J Anim Sci 23:1462–1468

    Article  CAS  Google Scholar 

  • Skiba-Cassy S, Geurden I, Panserat S, Seiliez I (2016) Dietary methionine imbalance alters the transcriptional regulation of genes involved in glucose, lipid and amino acid metabolism in the liver of rainbow trout (Oncorhynchus mykiss). Aquaculture 454:56–65

    Article  CAS  Google Scholar 

  • Turnbull AV, Rivier C (1997) Corticotropin-releasing factor (CRF) and endocrine responses to stress: CRF receptors, binding protein, and related peptides. Proc Soc Exp Biol Med 215:1–10

    Article  CAS  PubMed  Google Scholar 

  • Wu H, Ohnuki H, Ota S, Murata M, Yoshiura Y, Endo H (2017) New approach for monitoring fish stress: a novel enzyme-functionalized label-free immunosensor system for detecting cortisol levels in fish. Biosens Bioelectron 93:57–64

    Article  CAS  PubMed  Google Scholar 

  • Yagi M, Kanda T, Takeda T, Ishimatsu A, Oikawa S (2010) Ontogenetic phase shifts in metabolism: links to development and anti-predator adaptation. Proc Biol Sci 277:2793–2801

    Article  PubMed  PubMed Central  Google Scholar 

  • Yahav S (2015) Regulation of body temperature: strategies and mechanisms. In: Scanes CG (ed) Sturkie’s avian physiology, 6th edn. Academic, London, pp 869–890

    Chapter  Google Scholar 

Download references

Acknowledgments

The diligent technical support of Shin Oikawa (Retired Associate Professor, Fishery Research Laboratory, Kyushu University) in the measurement of oxygen consumption in goldfish is gratefully acknowledged.

Funding

This study was supported by JSPS KAKENHI grant numbers JP15K07694 and JP18K19271 to VSC.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Vishwajit S. Chowdhury.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

This study was performed in accordance with the ethical guidelines for animal experiments as described in the materials and methods section.

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

Wang, Y., Han, G., Pham, C.V. et al. An acute increase in water temperature can increase free amino acid concentrations in the blood, brain, liver, and muscle in goldfish (Carassius auratus). Fish Physiol Biochem 45, 1343–1354 (2019). https://doi.org/10.1007/s10695-019-00642-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-019-00642-5

Keywords

Navigation