Time-Dependent Responses of Oxidative Stress, Growth, and Reproduction of Daphnia magna Under Thermal Stress

  • Hyungjoon Im
  • Palas Samanta
  • Joorim Na
  • Jinho JungEmail author


The present study evaluated the effects of temperature (20 and 25°C) on the oxidative stress responses and life-history traits of Daphnia magna depending on exposure time. Daphnid exposed to an elevated temperature for 21 days had notably higher activities of the antioxidant enzymes superoxide dismutase, catalase, glutathione peroxidase, and glutathione S-transferase while the enzyme activities did not differ significantly between the two temperature groups for daphnid exposed for 5 days. However, the results of body length were opposite where only the 5 days exposure daphnid had significantly longer bodies at 25°C compared to those at 20°C (p < 0.05). Despite the earlier reproduction for daphnids at 25°C, the cumulative number of offspring per female for 21 days was not significantly different from those at 20°C (p < 0.05). These findings suggest that D. magna undergo strategic changes in oxidative stress response, growth, and reproduction throughout the exposure period of 21 days.


Antioxidant enzyme Body length Fecundity Water flea 



This work was supported by a Korea University Grant and a National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIP) (Grant No. NRF-2016R1A2B4016299).


  1. Angilletta MJ Jr, Dunham AE (2003) The temperature-size rule in ectotherms: simple evolutionary explanations may not be general. Am Nat 162(3):332–342CrossRefGoogle Scholar
  2. Bae E, Samanta P, Yoo J, Jung J (2016) Effects of multigenerational exposure to elevated temperature on reproduction, oxidative stress, and Cu toxicity in Daphnia magna. Ecotoxicol Environ Saf 132:366–371CrossRefGoogle Scholar
  3. Barata C, Navarro JC, Varo I, Riva MC, Arun S, Porte C (2005) Changes in antioxidant enzyme activities, fatty acid composition and lipid peroxidation in Daphnia magna during the aging process. Comp Biochem Physiol B 140(1):81–90CrossRefGoogle Scholar
  4. Becker D, Brinkmann BF, Zeis B, Paul RJ (2011) Acute changes in temperature or oxygen availability induce ROS fluctuations in Daphnia magna linked with fluctuations of reduced and oxidized glutathione, catalase activity and gene (haemoglobin) expression. Biol Cell 103:351–363CrossRefGoogle Scholar
  5. 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 72:248–254CrossRefGoogle Scholar
  6. Coggins BL, Collins JW, Holbrook KJ, Yampolsky LY (2017) Antioxidant capacity, lipid peroxidation, and lipid composition changes during long-term and short-term thermal acclimation in Daphnia. J Comp Physiol B 187(8):1091–1106CrossRefGoogle Scholar
  7. Costantini D (2014) Oxidative stress and hormesis in evolutionary ecology and physiology: a marriage between mechanistic and evolutionary approaches. Springer, BerlinCrossRefGoogle Scholar
  8. Davies KJA (2000) Oxidative stress, antioxidant defenses, and damage removal, repair, and replacement systems. IUBMB Life 50(4–5):279–289CrossRefGoogle Scholar
  9. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. J Biol Chem 249(8):7130–7139Google Scholar
  10. Heugens EHW, Tokkie LTB, Kraak MHS, Hendriks AJ, Van Straalen NM, Admiraal W (2006) Population growth of Daphnia magna under multiple stress conditions: joint effects of temperature, food, and cadmium. Environ Toxicol Chem 25:1399–1407CrossRefGoogle Scholar
  11. Hoefnagel KN, De Vries EHJ, Jongejans E, Verberk WC (2018) The temperature-size rule in Daphnia magna across different genetic lines and ontogenetic stages: multiple patterns and mechanisms. Ecol Evolut 8(8):3828–3841CrossRefGoogle Scholar
  12. Kim KT, Klaine SJ, Cho J, Kim SH, Kim SD (2010) Oxidative stress responses of Daphnia magna exposed to TiO2 nanoparticles according to size fraction. Sci Total Environ 408(10):2268–2272CrossRefGoogle Scholar
  13. Klumpen E, Hoffschröer N, Zeis B, Gigengack U, Dohmen E, Paul RJ (2017) Reactive oxygen species (ROS) and the heat stress response of Daphnia pulex: ROS-mediated activation of hypoxia-inducible factor 1 (HIF-1) and heat shock factor 1 (HSF-1) and the clustered expression of stress genes. Biol Cell 1:1–50Google Scholar
  14. Langford T (1990) Ecological effects of thermal discharges. Springer, BerlinGoogle Scholar
  15. Lee KW, Raisuddin S, Rhee JS, Hwang DS, Yu IT, Lee YM, Park HG, Lee JS (2008) Expression of glutathione S-transferase (GST) genes in the marine copepod Tigriopus japonicus exposed to trace metals. Aquat Toxicol 89:158–166CrossRefGoogle Scholar
  16. Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13–30CrossRefGoogle Scholar
  17. Martínez-Jerónimo F (2012) Description of the individual growth of Daphnia magna (Crustacea: Cladocera) through the von Bertalanffy growth equation. Effect of photoperiod and temperature. Limnology 13:65–71CrossRefGoogle Scholar
  18. Martins A, Guimarães L, Guilhermino L (2013) Chronic toxicity of the veterinary antibiotic florfenicol to Daphnia magna assessed at two temperatures. Environ Toxicol Pharmacol 36:1022–1032CrossRefGoogle Scholar
  19. Messiaen M, De Schamphelaere KAC, Muyssen BTA, Janssen CR (2010) The micro-evolutionary potential of Daphnia magna population exposed to temperature and cadmium stress. Ecotoxicol Environ Saf 73:1114–1122CrossRefGoogle Scholar
  20. Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175Google Scholar
  21. Muyssen BTA, Messiaen M, Janssen CR (2010) Combined cadmium and temperature acclimation in Daphnia magna: physiological and sub-cellular effects. Ecotoxicol Environ Saf 73:735–742CrossRefGoogle Scholar
  22. Organization for Economic Cooperation and Development (OECD) (1996) Guideline for the testing of chemicals: Daphnia sp. Daphnia magna reproduction test no 211. OECD, ParisGoogle Scholar
  23. Organization for Economic Cooperation and Development (OECD) (2004) Guideline for the testing of chemicals: Daphnia spp. acute immobilisation test no 202. OECD, ParisGoogle Scholar
  24. Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70(1):158–169Google Scholar
  25. Perrin N (1995) About Berrigan and Charnov’s life-history puzzle. Oikos 73:137–139CrossRefGoogle Scholar
  26. Pinkhaus O, Schwerin S, Pirow R, Zeis B, Buchen I, Gigengack U, Koch M, Horn W, Paul RJ (2007) Temporal environmental change, clonal physiology and the genetic structure of a Daphnia assemblage (D. galeata-hyalina hybrid species complex). Freshw Biol 52(8):1537–1554CrossRefGoogle Scholar
  27. Radi R, Turrens JF, Chang LY, Bush KM, Crapo JD, Freeman BA (1991) Detection of catalase in rat heart mitochondria. J Biol Chem 266(32):22028–22034Google Scholar
  28. Vandenbrouck T, Dom N, Novais S, Soetaert A, Ferreira ALG, Loureiro S, Soares AMVM, De Coen W (2011) Nickel response in function of temperature differences: effects at different levels of biological organization in Daphnia magna. Comp Biochem Physiol D 6(3):271–281Google Scholar
  29. West AP, Shadel GS, Ghosh S (2011) Mitochondria in innate immune responses. Nat Rev Immunol 11(6):389–402CrossRefGoogle Scholar
  30. Wojtal-Frankiewicz A (2012) The effects of global warming on Daphnia spp. population dynamics: a review. Aquat Ecol 46:37–53CrossRefGoogle Scholar
  31. Yamane L, Gilman SE (2009) Opposite responses by an intertidal predator to increasing aquatic and aerial temperatures. Mar Ecol Prog Ser 393:27–36CrossRefGoogle Scholar
  32. Zera AJ, Harshman LG (2001) The physiology of life history trade-offs in animals. Annu Rev Ecol Syst 32(1):95–126CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Hyungjoon Im
    • 1
  • Palas Samanta
    • 1
  • Joorim Na
    • 1
  • Jinho Jung
    • 1
    Email author
  1. 1.Division of Environmental Science and Ecological EngineeringKorea UniversitySeoulRepublic of Korea

Personalised recommendations