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Environmental Science and Pollution Research

, Volume 25, Issue 30, pp 30696–30707 | Cite as

Effects of Microcystis aeruginosa on the life history traits and SOD activity of Daphnia similoides sinensis

  • Shuixiu Peng
  • Daogui Deng
  • Ping He
  • Xiaoxue Xu
  • Chenchen Zhang
  • Jie Cao
  • Qi Liu
  • Tingting Zhang
Research Article

Abstract

With water eutrophication and global warming, cyanobacteria blooms have occurred frequently, and the interaction between M. aeruginosa and Daphnia has been widely paid attention by researchers. However, the effects of toxic M. aeruginosa on the SOD activity of Daphnia are poorly known. Six D. similoides sinensis clones collected from Lake Junshan and the offspring of two clones were employed. The effects of toxic M. aeruginosa on the life history traits and SOD activities of D. similoides sinensis in the mother and their offspring were studied. Toxic M. aeruginosa could significantly inhibit the life history traits (e.g., body lengths, offspring numbers at first reproduction, cumulative offspring numbers, and the intrinsic rate of population) and induce higher SOD activities of D. similoides sinensis. Compared with the mother, the effects of toxic M. aeruginosa on the life history traits and SOD activities of D. similoides sinensis in the offspring showed obvious differences. Moreover, the adaptability of the offspring to M. aeruginosa indicated also the differences between two clones. Our results suggested that the mother exposed to toxic M. aeruginosa could enhance the fitness of their offspring to Microcystis by maternal effect and was also affected by the D. similoides sinensis genotypes.

Keywords

Daphnia similoides sinensis Microcystis aeruginosa SOD Life history traits Maternal effect Clone 

Notes

Funding

This program was financially supported by the National Natural Science Foundation of China (No. 31370470; 31870451).

References

  1. Akbar S, Du JJ, Lin H, Kong XS, Sun SC, Tian XJ (2017) Understanding interactive inducible defenses of Daphnia and its phytoplankton prey. Harmful Algae 66:47–56CrossRefGoogle Scholar
  2. Amado LL, Monserrat JM (2010) Oxidative stress generation by microcystins in aquatic animals: why and how. Environ Int 36(2):226–235CrossRefGoogle Scholar
  3. Chen YW, Qin BQ, Teubner K, Dokulil MT (2003) Long-term dynamics of phytoplankton assemblages:Microcystis-domination in Lake Taihu, a large shallow lake in China. J Plankton Res 25(4):445–453CrossRefGoogle Scholar
  4. Chen FZ, Xie P (2003) The effects of fresh and decomposed Microcystis aeruginosa on cladocerans from a subtropic Chinese lake. J Freshw Ecol 18(1):97–104CrossRefGoogle Scholar
  5. Costa SM, Ferrão-Filho AS, Azevedo SMFO (2013) Effects of saxitoxin- and non-saxitoxin-producing strains of the cyanobacterium Cylindrospermopsis raciborskii, on the fitness of temperate and tropical cladocerans. Harmful Algae 28(5):55–63CrossRefGoogle Scholar
  6. Czesak ME, Fox CW (2003) Evolutionary ecology of egg size and number in a seed beetle: genetic trade-off differs between environments. Evolution 57(5):1121–1132CrossRefGoogle Scholar
  7. Dao TS, Ortiz-Rodríguez R, Do-Hong LC, Wiegand C (2013) Non-microcystin and non-cylindrospermopsin producing cyanobacteria affect the biochemical responses and behavior of Daphnia magna. Int Rev Hydrobiol 98(5):235–244Google Scholar
  8. Demott WR (1999) Foraging strategies and growth inhibition in five daphnids feeding on mixtures of a toxic cyanobacterium and a green alga. Freshw Biol 42(2):263–274CrossRefGoogle Scholar
  9. Deng DG, Xie P, Zhou Q, Yang H, Guo LG, Geng H (2008) Field and experimental studies on the combined impacts of cyanobacterial blooms and small algae on crustacean zooplankton in a large, eutrophic, subtropical, Chinese lake. Limnology 9:1–11CrossRefGoogle Scholar
  10. Deng DG, Xie P, Zhou Q, Yang H, Guo LG (2007) Studies on temporal and spatial variations of phytoplankton in Lake Chaohu. J Integr Plant Biol 49(4):409–418CrossRefGoogle Scholar
  11. Ferrão-Filho AS, Silva DAS, Oliveira TA, Pflugmacher S, Silvaet EM (2017) Single and combined effects of microcystins and saxitoxins producer cyanobacteria on the fitness and antioxidant defenses of cladocerans. Environ Toxicol Chem 36(10):2689–2697CrossRefGoogle Scholar
  12. Ger KA, Urrutia-Cordero P, Frost PC, Hansson LA, Sarnelle O, Wilson AE, Lürling M (2016) The interaction between cyanobacteria and zooplankton in a more eutrophic world. Harmful Algae 54:128–144CrossRefGoogle Scholar
  13. Gilbert JJ (1990) Differential effects of Anabaena affinis on cladocerans and rotifers: mechanisms and implications. Ecology 71(5):1727–1740CrossRefGoogle Scholar
  14. Guo NC, Xie P (2011) A study on the effects of food quantity and quality on glutathione S-transferase (GST) activity and growth rate parameters of Daphnia carinata varying in age. Aquat Ecol 45(1):63–73CrossRefGoogle Scholar
  15. Gustafsson S, Hansson LA (2004) Development of tolerance against toxic cyanobacteria in Daphnia. Aquat Ecol 38:37–44CrossRefGoogle Scholar
  16. Gustafsson S, Rengefors K, Hansson LA (2005) Increased consumer fitness following transfer of toxin tolerance to offspring via maternal effects. Ecology 86(10):2561–2567CrossRefGoogle Scholar
  17. Hairston NG, Lampert W, Cáceres CE, Holtmeier CL, Weider LJ, Gaedke U, Fischer JM, Fox JM, Post DM (1999) Rapid evolution revealed by dormant eggs. Nature 401(6752):231–232CrossRefGoogle Scholar
  18. Harney E, Paterson S, Plaistow SJ (2017) Offspring development and life-history variation in a water flea depends upon clone-specific integration of genetic, non-genetic and environmental cues. Funct Ecol 31:1996–2007.  https://doi.org/10.1111/1365-2435.12887 CrossRefGoogle Scholar
  19. He JW, He ZR, Guo QL (1997) The toxicity of Microcystis aeruginosa to fishes and Daphnia. J Lake Sci 9(1):49–56 (in Chinese)CrossRefGoogle Scholar
  20. Hietala J, Reinikainen M, Walls M (1995) Variation in life history responses of Daphnia to toxic Microcystis aeruginosa. J Plankton Res 17(12):2307–2318CrossRefGoogle Scholar
  21. Hu ZQ, Li DH, Liu YD, He GY (2006) Advances in ecotoxicology of microcystins to aquatic organisms. Prog Nat Sci 16(1):14–20 (in Chinese)Google Scholar
  22. Jiang XD, Yang W, Zhao SY, Liang HS, Zhao YL, Chen LQ (2013) Maternal effects of inducible tolerance against the toxic cyanobacterium Microcystis aeruginosa in the grazer Daphnia carinata. Environ Pollut 178(1):142–146CrossRefGoogle Scholar
  23. Jia XY, Chen ZW (2002) The subacute toxicity of cadmium on Carassias auratus. Acta Agric Zhejiangensis 14(3):155–158 (in Chinese)Google Scholar
  24. Kurtz J, Franz K (2003) Innate defence: evidence for memory in invertebrate immunity. Nature 425(6953):37–38CrossRefGoogle Scholar
  25. Lemaire V, Brusciotti S, Gremberghe IV, Vyverman W, Vanoverbeke J, Meester LD (2012) Genotype×genotype interactions between the toxic cyanobacterium Microcystis and its grazer, the waterflea Daphnia. Evol Appl 5(2):168–182CrossRefGoogle Scholar
  26. Li F, Deng DG, Zhang XL, Ji GQ, Huang QF (2014) Combined effects of four Microcystis aeruginosa, strains and Scenedesmus obliquus, concentrations on population dynamics and resting egg formation of two Daphnia species. Limnology 15(3):271–279CrossRefGoogle Scholar
  27. Little TJ, O’connor B, Colegrave N, Watt K, Read AF (2003) Maternal transfer of strain-specific immunity in an invertebrate. Curr Biol 13(6):489–492CrossRefGoogle Scholar
  28. Liu Y, Xie P, Chen FZ, Wu X (2005) Effect of combinations of the toxic cyanobacterium Microcystis aeruginosa PCC7820 and the green alga Scenedesmus on the experimental population of Daphnia pulex. Bull Environ Contam Toxicol 74(6):1186–1191CrossRefGoogle Scholar
  29. Lyu K, Guan H, Wu C, Wang X, Wilson AE, Yang Z (2016) Maternal consumption of non-toxic Microcystis by Daphnia magna induces tolerance to toxic Microcystis in offspring. Freshw Biol 61(2):219–228CrossRefGoogle Scholar
  30. Lyu K, Zhang L, Zhu X, Cui G, Wilson AE, Yang Z (2015) Arginine kinase in the cladoceran Daphnia magna: cDNA sequencing and expression is associated with resistance to toxic Microcystis. Aquat Toxicol 160:13–21CrossRefGoogle Scholar
  31. Monaghan P, Metcalfe NB, Torres R (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol Lett 12:75–92CrossRefGoogle Scholar
  32. Namikoshi M, Rinehart KL (1996) Bioactive compounds produced by cyanobacteria. J Ind Microbiol 17(5–6):373–384Google Scholar
  33. Ortiz-Rodríguez R, Dao TS, Wiegand C (2012) Transgenerational effects of microcystin-LR on Daphnia magna. J Exp Biol 215(16):2795–2805CrossRefGoogle Scholar
  34. Räsänen K, Kruuk LEB (2007) Maternal effects and evolution at ecological time-scales. Funct Ecol 21(3):408–421CrossRefGoogle Scholar
  35. Repka S (1997) Effects of food type on the life history of Daphnia clones from lakes differing in trophic state: I. Daphnia galeata feeding on Scenedesmus and Oscillatoria. Freshw Biol 38(3):675–683CrossRefGoogle Scholar
  36. Rohrlack T, Christoffersen K, Hansen PE, Zhang W, Czarnecki O, Henning M, Fastner J, Erhard M, Neilan BA, Kaebernick M (2003) Isolation, characterization, and quantitative analysis of microviridin J, a new Microcystis metabolite toxic to Daphnia. J Chem Ecol 29(8):1757–1770CrossRefGoogle Scholar
  37. Sarnelle O, Wilson AE (2005) Local adaptation of Daphnia pulicaria to toxic cyanobacteria. Limnol Oceanogr 50(5):1565–1570CrossRefGoogle Scholar
  38. Schwarzenberger A, Kuster CJ, Von Elert E (2012) Molecular mechanisms of tolerance to cyanobacterial protease inhibitors revealed by clonal differences in Daphnia magna. Mol Ecol 21(19):4898–4911CrossRefGoogle Scholar
  39. Schwarzenberger A, Sadler T, Motameny S, Ben-Khalifa K, Frommolt P, Altmüller J, Konrad K, Elert E (2014) Deciphering the genetic basis of microcystin tolerance. BMC Genomics 15(1):776CrossRefGoogle Scholar
  40. Shao YQ, Deng DG, Meng MR, Zhang XL, Li F (2014) Effects of colonial and interspecific competition on the population dynamics and resting egg formation of two cladocerans. J Freshw Ecol 29(2):213–223CrossRefGoogle Scholar
  41. Wilson AE, Sarnell O, Tillmanns AE (2006) Effects of cyanobacterial toxicity and morphology on the population growth of freshwater zooplankton: meta-analyses of laboratory experiments. Limnol Oceanogr 51(4):1915–1924CrossRefGoogle Scholar
  42. Yamaoka K, Edamatsu R, Mori A (1991) Increased SOD activities and decreased lipid peroxide levels induced by low dose X irradiation in rat organs. Free Radic Biol Med 11(11):299–306CrossRefGoogle Scholar
  43. Yang Z, Lyu K, Chen YF, Montagnes (2012) The interactive effects of ammonia and microcystin on life-history traits of the cladoceran Daphnia magna: synergistic or antagonistic? PLoS ONE 7(3): e32285CrossRefGoogle Scholar
  44. Zhang YM, Wang YJ, Yu RL, Zhou M (2008) Effects of heavy metals on ATPase and SOD activities of Hepatopancreas in Misgurnus anguillicaudatus. J Gansu Sci 20(3):55–59 (in Chinese)Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Life Science, Anhui Key Laboratory of Resource and Plant BiologyHuaibei Normal UniversityHuaibeiChina

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