Environmental Science and Pollution Research

, Volume 21, Issue 2, pp 1064–1070 | Cite as

Elevated water temperature reduces the acute toxicity of the widely used herbicide diuron to a green alga, Pseudokirchneriella subcapitata

  • Rumana Tasmin
  • Yohei Shimasaki
  • Michito Tsuyama
  • Xuchun Qiu
  • Fatma Khalil
  • Nozomu Okino
  • Naotaka Yamada
  • Shinji Fukuda
  • Ik-Joon Kang
  • Yuji Oshima
Research Article

Abstract

In the actual environment, temperatures fluctuate drastically through season or global warming and are thought to affects risk of pollutants for aquatic biota; however, there is no report about the effect of water temperature on toxicity of widely used herbicide diuron to fresh water microalgae. The present research investigated inhibitory effect of diuron on growth and photosynthetic activity of a green alga Pseudokirchneriella subcapitata at five different temperatures (10, 15, 20, 25, and 30 °C) for 144 h of exposure. As a result, effective diuron concentrations at which a 50 % decrease in algal growth occurred was increased with increasing water temperature ranging from 9.2 to 20.1 μg L–1 for 72 h and 9.4–28.5 μg L–1 for 144 h. The photochemical efficiency of photosystem II (F v/F m ratio) was significantly reduced at all temperatures by diuron exposure at 32 μg L–1 after 72 h. Inhibition rates was significantly increased with decreased water temperature (P < 0.01). Intracellular H2O2 levels as an indicator of oxidative stress were also decreased with increasing temperature in both control and diuron treatment groups and were about 2.5 times higher in diuron treatment groups than that of controls (P < 0.01). Our results suggest water temperatures may affect the toxicokinetics of diuron in freshwater and should therefore be considered in environmental risk assessment.

Keywords

Diuron Pseudokirchneriella subcapitata Water temperature Photosynthetic activity Intracellular H2O2 

Notes

Acknowledgments

The cost of publication was supported in part by the Research Grant for Young Investigators of the Faculty of Agriculture, Kyushu University, Japan. This study was also supported in part by the JSPS Core-to-Core Program (B. Asia-Africa Science Platforms) “Collaborative Project for Soil and Water Conservation in Southeast Asian Watersheds”.

References

  1. Bérard A, Leboulanger S, Pelte T (1999) Tolerance of Oscillatoria limnetica Lemmermann to atrazine in natural phytoplankton populations and in pure culture: influence of season and temperature. Arch Environ Contam Toxicol 37:472–479CrossRefGoogle Scholar
  2. Blanchoud H, Farrugia F, Mouchel JM (2004) Pesticide uses and transfers in urbanised catchments. Chemosphere 55:905–913CrossRefGoogle Scholar
  3. Blasberg J, Hicks SL, Bucksath J (1991) Acute toxicity of diuron to Selenastrum capricornutum Printz. DuPont Study No. AMR-2046-91. ABC Laboratories Inc., Project ID: Final Report #39335. Unpublished study prepared by ABC Laboratories, Inc., Columbia, Missouri. Submitted to the U. S. Environmental Protection Agency. EPA MRID 42218401Google Scholar
  4. Burdon RH, Gill V, Boyd PA, O’Kane D (1994) Chilling, oxidative stress and antioxidant enzyme response in Arabidopsis thaliana. Proc R Soc Edinburg 102B:177–185Google Scholar
  5. Chalifour A, Juneau P (2011) Temperature-dependent sensitivity of growth and photosynthesis of Scenedesmus obliquus, Navicula pelliculosa and two strains of Microcystis aeruginosa to the herbicide atrazine. Aquat Toxicol 103(1–2):9–17CrossRefGoogle Scholar
  6. Coutant CC, Suffern JS (1979) Temperature influences on growth of aquatic organisms. In: Lee SS, Sengupta S (eds) Waste Heat Management and Utilization. Hemisphere Publ Corp, Washington, D.C, pp 113–124Google Scholar
  7. Davison IR (1991) Environmental effects on algal photosynthesis: temperature. J Phycol 27:2–8CrossRefGoogle Scholar
  8. DeLorenzo ME, Scott GI, Ross PE (2001) Toxicity of pesticides to aquatic microorganisms: a review. Environ Toxicol Chemi 20:84–98CrossRefGoogle Scholar
  9. DeLorenzo ME, Danese LE, Baird TD (2011) Influence of increasing temperature and salinity on herbicide toxicity in estuarine phytoplankton. Environ Toxicol. doi: 10.1002/tox.20726 Google Scholar
  10. Dengler D (2002) Testing of toxic effects of the diuron metabolite mCPDMU on the single cell green alga Desmodesmus subspicatus (formerly Scenedesmus subspicatus). Arbeitsgemeinschaft GAB Biotechnologie GmbH & IFU Unweltanalytik GmbH, Germany. Bayer AG, Germany and Griffin LLC, Belgium. Study Code 20001411/01-AADsGoogle Scholar
  11. DeNicola DM (1996) Periphyton responses to temperature at different ecological levels. In: Stevenson RJ, Bothwell ML, Lowe RL (eds) Algal Ecology. Academic, San Diego, pp 149–181CrossRefGoogle Scholar
  12. Desikan R, Hancock JT, Neill SJ (2003) Oxidative stress signalling. Top Curr Genet 4:129–149Google Scholar
  13. Douglas MT, Handley JW (1988) The algistatic activity of diuron technical. Huntingdon Research Centre Ltd, England. DuPont de Nemours (France) SAGoogle Scholar
  14. Ensminger I, Xyländer M, Hagen C, Braune W (2001) Strategies providing success in a variable habitat. III. Dynamic control of photosynthesis in Cladophora glomerata. Pl Cell Environ 24:769–779CrossRefGoogle Scholar
  15. Ferrero A, Tinarelli A (2007) Rice cultivation in the E.U. ecological conditions and agronomical practices, in: Capri E, Karpouzas DG (Eds.), Pesticide risk assessment in rice paddies: theory and practice. Elsevier, ISBN: 978-0-444-53087-5, Amsterdam. pp. 1–24Google Scholar
  16. Field JA, Reed RL, Sawyer TE, Griffith SM, Wigington PJ (2003) Diuron occurrence and distribution in soil and surface and ground water associated with grass seed production. J Environ Qual 32:171–179Google Scholar
  17. Folt CL, Chen CY, Moore MV, Burnaford J (1999) Synergism and antagonism among multiple stressors. Limnol Oceanogr 44:864–877CrossRefGoogle Scholar
  18. Gonen-Zurgil Y, Carmeli-Schwartz Y, Sukenik A (1997) Selective effect of the herbicide DCMU on unicellular algae—a potential tool to maintain monoalgal mass culture of Nannochloropsis. J Applied Phycol 8:415–419CrossRefGoogle Scholar
  19. Guillard RL (1973) Handbook of phycological methods—culture methods and growth measurements. Cambridge University Press 19:289–311Google Scholar
  20. Hess D, Warren F (2002) The herbicide handbook of the Weed Science Society of America 8th Edition 159–161Google Scholar
  21. Holmstrup M, Bindesbøl AM, Oostingh GJ, Duschl A, Scheil V, Köhler HR, Loureiro S, Soares AMVM, Ferreira ALG, Kienle C, Gerhardt A, Laskowski R, Kramarz PE, Bayley M, Svendsen C, Spurgeon DJ (2010) Interactions between effects of environmental chemicals and natural stressors: a review. Sci Total Environ 408(18):3746–3762CrossRefGoogle Scholar
  22. Houghton JT, Ding Y, Griggs DJ, Noguer M, Linden van der PJ, and Xiaosu D, Eds. (2001) Climate change 2001: the scientific basis: contributions of working group I to the third assessment report of the intergovernmental panel on climate change. Cambridge University Press, 881 ppGoogle Scholar
  23. Huang X, Pedersen T, Fischer M, White R, Young TM (2004) Herbicide runoff along highways. 1. Field observations. Environ Sci Technol 38:3263–3271CrossRefGoogle Scholar
  24. Ichimura T (1971) Sexual cell division and conjugation-papilla formation in sexual reproduction of Closterium strigosum, in: Proceedings of the seventh international seaweed symposium. University of Tokyo Press, Tokyo, pp 208–214Google Scholar
  25. Jones RJ, Kerswell AP (2003) Phytotoxicity of photosystem II (PSII) herbicides to coral. Mar Ecol Prog Ser 261:149–159. doi: 10.3354/meps261149 CrossRefGoogle Scholar
  26. Kellogg RL, Nehring R, Grube A, Goss DW and Plotkin S (2000) Environmental indicators of pesticide leaching and runoff from farm fields. Paper presented at Agricultural Productivity: Data, Methods, and Measures, Washington DC, March9-10, 2000Google Scholar
  27. Kimura I, Ichizen N, Matsunaka S (1971) Mode of action of a herbicide, Benthiocarb. J Weed Sci Technol 12:54–59CrossRefGoogle Scholar
  28. Kennedy K, Bentley C , Paxman C , Heffernan A , Dunn A, Kaserzon S and Mueller J (2010) Final report-monitoring of organic chemicals in the Great Barrier Reef Marine Park using time integrated monitoring tools (2009–2010), The University of Queensland, The National Research Centre for Environmental Toxicology (Entox)Google Scholar
  29. Loos R, Gawlik BM, Boettcher K, Locoro G, Contini S, Bidoglio G (2009) Sucralose screening in European surface waters using a solid-phase extraction-liquid chromatography-triple quadrupole mass spectrometry method. J Chromatogr A 1216(7):1126–1131CrossRefGoogle Scholar
  30. Lopez-Rodas V, Agrelo M, Carrillo E, Ferrero LM, Larrauri A, Martín-Otero L, Costas E (2001) Resistance of microalgae to modern water contaminants as the result of rare spontaneous mutations. Europ J Phycol 36(2):179–190CrossRefGoogle Scholar
  31. Malato S, Blanco J, Cáceres J, Fernandez-Alba AR, Aguera A, Rodrigues A (2002) Photocatalytic treatment of water-soluble pesticides by photo-Fenton and TiO2 using solar energy. Catal Today 76:209–220CrossRefGoogle Scholar
  32. Marking LL (1985) Toxicity of chemical mixtures. In: Rand GM, Petrocelli SR (eds) Fundamentals of Aquatic Toxicology. Hemisphere Publishing Corporation, New York, pp 164–176Google Scholar
  33. Marvá F, López-Rodas V, Rouco M, Navarro M (2010) Adaptation of green microalgae to the herbicides simazine and diquat as result of pre-selective mutations. Aquat Toxicol 96(2):130–134CrossRefGoogle Scholar
  34. Mayasich JM, Karlander EP, Terlizzi DE (1986) Growth responses of Nannochloris oculata Droop and Phaeodactylum tricornutum Bohlin to the herbicide atrazine as influenced by light intensity and temperature. Aquat Toxicol 8:175–184CrossRefGoogle Scholar
  35. Muzik TJ, Mauldin WG (1964) Influence of environment on the response of plants to herbicides. Weeds 12:142–145CrossRefGoogle Scholar
  36. Nebeker AV, Schuytema GS (1998) Chronic effects of the herbicide diuron on freshwater cladocerans, amphipods, midges, minnows, worms, and snails. Arch Environ Contam Toxicol 35(3):441–446CrossRefGoogle Scholar
  37. Okamura H (2002) Photodegradation of the antifouling compounds Irgarol 1051 and diuron released from a commercial paint. Chemosphere 48:43–50CrossRefGoogle Scholar
  38. Olofsdotter M, Watson A, Piggin C (1998) Weeds: a looming problem in modern rice production, in: Sustainability of rice in the global food system. Dowling NG, Greenfield SM, Fisher KS (Eds.), Pacific Basin Study Center, International Rice Research Institute, ISBN: 971-22-0107-4, Davis, California, USA; Manila, Philippines pp. 165–173Google Scholar
  39. Oukarroum A, Polchtchikov S, Perreault F, Popovic R (2012) Temperature influence on silver nanoparticles inhibitory effect on photosystem II photochemistry in two green algae, Chlorella vulgaris and Dunaliella tertiolecta. Environ Sci Pollut Res Int 19(5):1755–1762CrossRefGoogle Scholar
  40. Qian H, Li J, Pan X, Jiang H, Sun L, Fu Z (2010) Photoperiod and temperature influence cadmium’s effects on photosynthesis-related gene transcription in Chlorella vulgaris. Ecotoxicol Environ Saf 73(6):1202–1206CrossRefGoogle Scholar
  41. Quinn PJ (1988) Effects of temperature on cell membrane. Symp Soc Exp Biol 42:237–258Google Scholar
  42. R Development Core T (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  43. Reis MO, Necchi O, Colepicolo P, Barros MP (2011) Co-stressors chilling and high light increase photooxidative stress in diuron-treated red alga Kappaphycus alvarezii but with lower involvement of H2O2. Pest Biochem Physiol 99:7–15CrossRefGoogle Scholar
  44. Revitt DM, Ellis JB, Llewellyn NR (2002) Seasonal removal of herbicides in urban runoff. Urban Water 4:13–19CrossRefGoogle Scholar
  45. Risk & Policy Analysts Limited [RPA] (2000) Socio-economic impacts of the identification of priority hazardous substances under the water framework directive. Final report. Prepared for European Commission Directorate-General Environment, Norfolk, UK, 121 ppGoogle Scholar
  46. Sabater C, Carrasco JM (2001) Effects of pyridaphenthion on growth of five freshwater species of phytoplankton. Chemosphere 44:1775–1781CrossRefGoogle Scholar
  47. Shaw M, Furnas MJ, Fabricius K, Haynes D, Carter S, Eaglesham G, Mueller JF (2010) Monitoring pesticides in the great barrier reef. Mar Pollut Bull 60:113–122CrossRefGoogle Scholar
  48. Shen J, Jiang J, Zheng P (2009) Effects of light and monosulfuron on growth and photosynthetic pigments of Anabaena flos-aquae Breb. J Water Resour Prot 6:408–413. doi: 10.4236/jwarp.2009.16049 CrossRefGoogle Scholar
  49. Srivastava AK, Bhargava P, Mishra Y, Shukla B, Rai LC (2006) Effect of pretreatment of salt, copper and temperature on ultraviolet-B-induced antioxidants in diazotrophic cyanobacterium Anabaena doliolum. J Basic Microbiol 46:135–144CrossRefGoogle Scholar
  50. United States Environmental Protection Agency [USEPA] (2003) Registration eligibility decision for diuron list A. Case 0046. Office of Prevention, Pesticides and Toxic Substances. USEPA, Washington, DC, p 22Google Scholar
  51. Van Dam JW, Negri AP, Mueller JF, Altenburger R, Uthicke S (2012) Additive pressures of elevated sea surface temperatures and herbicides on symbiont-bearing foraminifera. PLoS One 7(3):e33900. doi: 10.1371/journal.pone.0033900 CrossRefGoogle Scholar
  52. Vasil’ev IR, Venediktov PS (1993) Effects of pH and chemicals affecting polypeptide conformation on inhibition of reducing and oxidizing sides of photosystem 2 by DCMU in pea chloroplasts. Photosynthetica 29(4):595–602Google Scholar
  53. Vieira LR, Guilhermino L (2012) Multiple stress effects on marine planktonic organisms: influence of temperature on the toxicity of polycyclic aromatic hydrocarbons to Tetraselmis chuii. J Sea Res 72:94–98CrossRefGoogle Scholar
  54. Villeneuve A, Larroud e S, Humbert JF (2011) Herbicide contamination of freshwater ecosystems: impact on microbial communities. In: Pesticides—formulations, effects, fate (ed. Stoytcheva M), pp. 285–312. IntTech,CroatiaGoogle Scholar
  55. Yamamoto H, Nakamura K (2003) Sampling sediment and water in rice paddy fields and adjacent water bodies, in: Lee PW, Aizawa H, Barefoot AC, Murphy JJ (Eds.), Handbook of residue analytical methods for agrochemicals, volumes 1 & 2. Wiley, Chichester, West Sussex, England/Hoboken, NJ, USA, ISBN: 0-4714-9194-2, pp. 892–907Google Scholar
  56. Yebra DM, Kiil S, Dam-Johansen K (2004) Antifouling technology-past, present and future steps towards efficient and environmentally friendly antifouling coatings. Prog Org Coat 50:75–104CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Rumana Tasmin
    • 1
  • Yohei Shimasaki
    • 1
  • Michito Tsuyama
    • 2
  • Xuchun Qiu
    • 1
  • Fatma Khalil
    • 1
  • Nozomu Okino
    • 3
  • Naotaka Yamada
    • 4
  • Shinji Fukuda
    • 5
  • Ik-Joon Kang
    • 1
  • Yuji Oshima
    • 1
  1. 1.Laboratory of Marine Environmental Science, Faculty of AgricultureKyushu UniversityFukuokaJapan
  2. 2.Laboratory of Silviculture, Faculty of AgricultureKyushu UniversityFukuokaJapan
  3. 3.Laboratory of Marine Resource Chemistry, Faculty of AgricultureKyushu UniversityFukuokaJapan
  4. 4.Laboratory of Pesticide Chemistry, Faculty of AgricultureKyushu UniversityFukuokaJapan
  5. 5.Laboratory of Water Environment Engineering, Faculty of AgricultureKyushu UniversityFukuokaJapan

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