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Effects of increased temperature on metabolic activity and oxidative stress in the first life stages of marble trout (Salmo marmoratus)

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Abstract

Climate change may result in future alterations in thermal regime which could markedly affect the early developmental stages of cold water fish due to their expected high sensitivity to increasing temperature. In the present study, the effect of temperature increase of 2, 4 and 6 °C on the oxygen consumption rate (R), the activity of respiratory electron transport system (ETS) and oxidative stress have been studied in four developmental stages of the marble trout (Salmo marmoratus)—eyed eggs, yolk-sac larvae and juveniles of 1 and 3 months. Oxygen consumption rate and ETS activity increased with level of development and with temperature in all four stages. ETS/R ratios decreased during development and correlated with temperature in eyed eggs, larvae and juveniles of 1 month, but not in juveniles of 3 months. Low ETS/R ratios at higher temperatures indicate stress response in eyed eggs, the most temperature sensitive developmental stage. Catalase (CAT) and glutathione reductase (GR) activities increased during development, but responded differently to elevated temperature in the different developmental stages. Stress in eyed eggs, caused by higher temperatures, resulted in increased oxygen consumption rate and increased activities of CAT and GR. Larvae were sensitive to increased temperature only at the highest experimental temperature of 16 °C. Increased temperature did not stress the metabolism of the juveniles, since they were able to compensate their metabolic activity. The earlier developmental stages of marble trout are thus more sensitive to temperature increase than juveniles and therefore more endangered by higher water temperatures. This is the first report connecting oxygen consumption, ETS activity and ETS/R ratio with the activities of antioxidant enzymes in relation to increased temperature in salmonids.

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References

  • Abele D, Puntarulo S (2004) Formation of reactive species and induction of antioxidant defence systems in polar and temperate marine invertebrates and fish. Comp Biochem Physiol (A) 138:405–415

    Article  Google Scholar 

  • Abele D, Heise K, Pörtner HO, Puntarulo S (2002) Temperature-dependence of mitochondrial function and production of reactive oxygen species in the intertidal mud clam Mya arenaria. J Exp Biol 205:1831–1841

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Akhtar MS, Pal AK, Sahu NP, Ciji A, Mahanta PC (2013) Thermal tolerance, oxygen consumption and haemato-biochemical variables of Tor putitora juveniles acclimated to five temperatures. Fish Physiol Biochem 39:1387–1398

    Article  CAS  PubMed  Google Scholar 

  • Angilletta MJ Jr (2009) Thermal sensitivity. In: Angilletta MJ Jr (ed) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, New York, pp 35–87

    Chapter  Google Scholar 

  • Bagnyukova TV, Chahrak OI, Lushchak VI (2006) Coordinated response of goldfish antioxidant defenses to environmental stress. Aquat Toxicol 78:325–331

    Article  CAS  PubMed  Google Scholar 

  • Bagnyukova TV, Lushchak OV, Storey KB, Lushchak VI (2007) Oxidative stress and antioxidant defense responses by goldfish tissues to acute change of temperature from 3 to 23 °C. J Therm Biol 32:227–234

    Article  CAS  Google Scholar 

  • Bamstedt U (1980) ETS activity as an estimator of respiratory rate of zooplankton populations. The significance of variations in environmental factors. J Exp Mar Biol Ecol 42:267–283

    Article  Google Scholar 

  • Barton BA, Schreck CB (1987) Metabolic cost of acute physical stress in juvenile steelhead. Trans Am Fish Soc 116:257–263

    Article  Google Scholar 

  • Bayir A, Sirkecioglu AN, Bayir M, Haliloglu HI, Kocaman EM, Aras NM (2011) Metabolic responses to prolonged starvation, food restriction, and refeeding in the brown trout, Salmo trutta: oxidative stress and antioxidant defences. Comp Biochem Physiol (B) 159:191–196

    Article  Google Scholar 

  • Carlberg C, Mannervik B (1985) Glutathione reductase. In: Meister A (ed) Meth enzymology, vol 113. Academic Press, New York, pp 488–495

    Google Scholar 

  • Davidson JF, Schiestl RH (2001) Mitochondrial respiratory electron carriers are involved in oxidative stress during heat stress in Saccharomyces cerevisiae. Mol Cell Biol 21:8483–8489

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dockray JJ, Reid SD, Wood CM (1996) Effects of elevated summer temperatures and reduced pH on metabolism and growth of juvenile rainbow trout (Oncorhynchus mykiss) on unlimited ration. Can J Fish Aquat Sci 53:2752–2763

    Article  Google Scholar 

  • Doucet-Beaupré H, Dubé C, Breton S, Pörtner HO, Blier PU (2010) Thermal sensitivity of metabolic enzymes in subarctic and temperate freshwater mussels (Bivalvia: Unionoida). J Therm Biol 35:11–20

    Article  Google Scholar 

  • Gopalan G, Madon SP, Culver DA, Pappas PW (1996) Measurement of metabolism in free ranging juvenile fishes using the electron transport system (ETS) enzyme assays. In: MacKinlay D, Nelson J (eds) High performance fish II. International congress on the biology of fishes. pp 21–30

  • Hegazi MM, Attia ZI, Ashour OA (2010) Oxidative stress and antioxidant enzymes in liver and white muscle of Nile tilapia juveniles in chronic ammonia exposure. Aquat Toxicol 99:118–125

    Article  CAS  PubMed  Google Scholar 

  • Ikeda T (1989) Estimated respiration rate of myctophid fish from the enzyme activity of the electron-transport-system. J Oceanogr 45:167–173

    Google Scholar 

  • Intergovernmental Panel on Climate Change (IPCC) (2013) Climate change 2013: the physical science basis. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia J, Bex V, Midgley PM (eds) Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, p 1535

    Google Scholar 

  • Jeppesen E, Mehner T, Winfield IJ, Kangur K, Sarvala J, Gerdeaux D, Rask M, Malmquist HJ, Holmgren K, Volta P, Romo S, Eckmann R, Sandström A, Blanco S, Kangur A, Stabo HR, Tarvainen M, Ventelä A-M, Søndergaard M, Lauridsen TL, Meerhoff M (2012) Impacts of climate warming on the long-term dynamics of key fish species in 24 European lakes. Hydrobiologia 694:1–39

    Article  CAS  Google Scholar 

  • Kamler E, Keckeis H, Bauer-Nemeschkal E (1998) Temperature-induced changes of survival, development and yolk partitioning in Chondrostoma nasus. J Fish Biol 53:658–682

    Google Scholar 

  • Kenner RA, Ahmed SI (1975) Measurements of electron transport activities in marine phytoplankton. Mar Biol 33:119–127

    Article  CAS  Google Scholar 

  • Killen SS, Brown JA, Gamperl AK (2008) Lack of metabolic thermal compensation during the early life stages of ocean pout Zoarces americanus (Bloch and Schneider): a benthic, cold-water marine species. J Fish Biol 72:763–772

    Article  Google Scholar 

  • Lampert W (1984) The measurement of respiration. In: Downing JA, Rigler FH (eds) A manual on methods for the assessment of secondary productivity in fresh water. IPB Handbook 17. Blackwell Scientific Publications, Oxford, pp 413–468

    Google Scholar 

  • Li X-Y, Huang H-H, Hu K, Liu Y, Jiang W-D, Jiang J, Li S-H, Feng L, Zhou X-Q (2014) The effects of dietary thiamin on oxidative damage and antioxidant defence of juvenile fish. Fish Physiol Biochem 40:673–687

    Article  CAS  PubMed  Google Scholar 

  • Linton TK, Morgan IJ, Walsh PJ, Wood CM (1998) Chronic exposure of rainbow trout (Oncorhynchus mykiss) to simulated climate warming and sublethal ammonia: a year-long study of their appetite, growth, and metabolism. Can J Fish Aquat Sci 55:576–586

    Article  CAS  Google Scholar 

  • Lukančič S, Žibrat U, Mezek T, Jerebic A, Simčič T, Brancelj A (2010) A new method for early assessment of effects of exposing two non-target crustacean species, Asellus aquaticus and Gammarus fossarum, to pesticides, a laboratory study. Tox Indus Health 26:217–228

    Article  Google Scholar 

  • Lushchak VI, Bagnyukova TV (2006) Temperature increase results in oxidative stress in goldfish tissues. 2. Antioxidant and associated enzymes. Comp Biochem Physiol (C) 143:36–41

    Google Scholar 

  • Lyytikäinen T, Jobling M (1998) The effect of temperature fluctuation on oxygen consumption and ammonia excretion of underyearling Lake Inari Arctic charr. J Fish Biol 52:1186–1198

    Google Scholar 

  • Macy WK III, Durbin AG, Durbin EG (1999) Metabolic rate in relation to temperature and swimming speed, and the cost of filter feeding in Atlantic menhaden, Brevoortia tyrannus. Fish Bull 97:282–293

    Google Scholar 

  • Martínez-Álvarez RM, Morales AE, Sanz A (2005) Antioxidant defenses in fish: biotic and abiotic factors. Rev Fish Biol Fish 15:75–88

    Article  Google Scholar 

  • McCarthy ID, Houlihan DF (1997) The effect of temperature on protein metabolism in fish: the possible consequences for wild Atlantic salmon (Salmo salar L.) stocks in Europe as a result of global warming. In: Wood CM, McDonald DG (eds) Global warming: implications for freshwater and marine fish. Cambridge University Press, Cambridge, pp 51–78

    Chapter  Google Scholar 

  • McCullough DA, Bartholow JM, Jager HI, Beschta RL, Cheslak EF, Deas ML, Ebersole JL, Foott JS, Johnson SL, Marine KR, Mesa MG, Petersen JH, Souchon Y, Tiffan KF, Wurtsbaugh WA (2009) Research in thermal biology: burning questions for coldwater stream fishes. Rev Fish Sci 17:90–115

    Article  Google Scholar 

  • Mota M, Sousa R, Araújo J, Braga C, Antunes C (2014) Ecology and conservation of freshwater fish: time to act for a more effective management. Ecol Freshw Fish 23:111–113

    Article  Google Scholar 

  • Muskó IB, Tóth GL, Szábo E (1995) Respiration and respiratory electron transport system (ETS) activity of two amphipods: Corophium curvispinum G. O. Sars and Gammarus fossarum Koch. Pol Arch Hydrobiol 42:547–558

    Google Scholar 

  • Myrick CA, Cech JJ Jr (2000) Temperature influences on California rainbow trout physiological performance. Fish Physiol Biochem 22:245–254

    Article  CAS  Google Scholar 

  • Neyfakh AA, Abramova NB (2014) Biochemical embryology of fishes. In: Florkin M, Sheer BT (Eds.), Chemical zoology, deuterostomians, cyclostemes and fishes. pp 275–283. www.books.google.hu/books?isbn=0323163343

  • Packard TT (1971) The measurement of respiratory electron- transport activity in marine phytoplankton. J Mar Res 29:235–244

    Google Scholar 

  • Pfeiler E, Govoni JJ (1993) Metabolic rates in early life history stages of elopomorph fishes. Biol Bull 185:277–283

    Article  Google Scholar 

  • Pörtner HO (2002) 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

    Article  Google Scholar 

  • Povž M (1995) Status of freshwater fishes in the Adriatic catchment of Slovenia. Biol Conserv 72:171–177

    Article  Google Scholar 

  • Rocha MJ, Rocha E, Resende AD, Lobo-da-Cunha A (2003) Measurement of peroxisomal enzyme activities in the liver of brown trout (Salmo trutta), using spectrophotometric methods. BMC Biochem 4:2

    Article  PubMed Central  PubMed  Google Scholar 

  • Roche H, Bogé G (1996) Fish blood parameters as a potential tool for identification of stress caused by environmental factors and chemical intoxication. Mar Environ Res 41:27–43

    Article  CAS  Google Scholar 

  • Rombough PJ (1988) Respiratory gas exchange, aerobic metabolism, and effects of hypoxia during early life. In: Hoar WS, Randall DJ (eds) Fish physiology, The physiology of developing fish; Eggs and larvae, vol 11., part A. Academic Press, London, pp 59–161

    Chapter  Google Scholar 

  • Rombough PJ (1997) The effects of temperature on embryonic and larval development. In: Wood CM, McDonald DG (eds) Global warming: Implications for freshwater and marine fish. Cambridge University Press, Cambridge, pp 177–223

    Chapter  Google Scholar 

  • Rudneva II (1999) Antioxidant system of Black Sea animals in early development. Comp Biochem Physiol (C) 122:265–271

    CAS  Google Scholar 

  • Simčič T (2005) Respiratory electron transport system (ETS) activity and respiration rate in cold-stenothermal and eurythermal chironomid larvae from high-mountain lakes. Arch Hydrobiol 162:399–415

    Article  Google Scholar 

  • Simčič T, Brancelj A (1997) Electron transport system (ETS) activity and respiration rate in five Daphnia species at different temperatures. Hydrobiologia 360:117–125

    Article  Google Scholar 

  • Simčič T, Brancelj A (2007) The effect of light on oxygen consumption in two amphipod crustaceans: the hypogean Niphargus stygius and the epigean Gammarus fossarum. Mar Freshw Behav Physiol 40:141–150

    Article  Google Scholar 

  • Simčič T, Lukančič S, Brancelj A (2005) Comparative study of electron transport system activity and oxygen consumption of amphipods from caves and surface habitats. Freshw Biol 50:494–501

    Article  Google Scholar 

  • Simčič T, Pajk F, Vrezec A, Brancelj A (2012) Size scaling of whole-body metabolic activity in the noble crayfish (Astacus astacus) estimated from measurements on a single leg. Freshw Biol 57:39–48

    Article  Google Scholar 

  • Smith JC, Chong CK (1982) Body weight activities of cytochrome oxidase and electron transport system in the liver of American plaice Hippoglossoides platessoides can these activities serve as indicators of metabolism? Mar Ecol Prog Ser 9:171–179

    Article  CAS  Google Scholar 

  • Stackley KD, Beeson CC, Rahn JJ, Chan SSL (2011) Bioenergetic profiling of zebrafish embryonic development. PLoS ONE 6(9):e25652. doi:10.1371/journal.pone.0025652

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tóth GL (1999) Aktivität des Elektronentransportsystems. In: von Tümpling W, Friedrich G (eds) Biologische Gewässeruntersuchung. Methoden der Biologischen Wasseruntersuchung 2, Gustav Fischer Verl., Jena, Stuttgart, Lübeck, Ulm, pp 465–473

  • Tóth GL, Szábo M, Webb D (1995) Adaptation of the tetrazolium reduction test for the measurement of the electron transport system (ETS) activity during embryonic development of medaka. J Fish Biol 46:835–844

    Article  Google Scholar 

  • Vinagre C, Madeira D, Narciso L, Cabral HN, Diniz M (2012) Effect of temperature on oxidative stress in fish: lipid peroxidation and catalase activity in the muscle of juvenile seabass, Dicentrarchus labrax. Ecol Indicat 23:274–279

    Article  CAS  Google Scholar 

  • Vincenzi S, Crivelli AJ, Jesensek D, De Leo GA (2008) Total population density during the first year of life as a major determinant of lifetime body-length trajectory in marble trout. Ecol Freshw Fish 17:515–519

    Article  Google Scholar 

  • Welker AF, Campos EG, Cardoso LA, Hermes-Lima M (2012) Role of catalase on the hypoxia/reoxygenation stress in the hypoxia-tolerant Nile tilapia. Am J Physiol Regul Integr Comp Physiol 302:R1111–R1118

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors thank Roger Pain for suggestions on an earlier draft of this manuscript and the English revision of the text, and two anonymous reviewers for their constructive comments on the manuscript. The authors acknowledge financial support by the Slovenian Research Agency (Research Programme P1-0255).

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. National Institute of Biology, Večna pot 111, 1000, Ljubljana, Slovenia

    Tatjana Simčič & Anton Brancelj

  2. Tolmin Angling Association, Tolmin, Slovenia

    Dušan Jesenšek

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  1. Tatjana Simčič
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Simčič, T., Jesenšek, D. & Brancelj, A. Effects of increased temperature on metabolic activity and oxidative stress in the first life stages of marble trout (Salmo marmoratus). Fish Physiol Biochem 41, 1005–1014 (2015). https://doi.org/10.1007/s10695-015-0065-6

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