Water Science and Engineering 2020, 13(2) 106-115 DOI:   https://doi.org/10.1016/j.wse.2020.06.007  ISSN: 1674-2370 CN: 32-1785/TV

Current Issue | Archive | Search                                                            [Print]   [Close]
Information and Service
This Article
Supporting info
Service and feedback
Email this article to a colleague
Add to Bookshelf
Add to Citation Manager
Cite This Article
Email Alert
Artemisinin sustained-release granules
Aquatic organisms
Toxicity assessment
Median lethal concentration
Antioxidant enzyme activity

Toxic response of aquatic organisms to guide application of artemisinin sustained-release granule algaecide

Li-xiao Ni a,b,*, Na Wang a,b, Xuan-yu Liu a,b, Fei-fei Yue a,b, Yi-fei Wang a,b, Shi-yin Li c, Pei-fang Wang a,b

a Key Laboratory of Integrated Regulation and Resource Development on Shallow Lakes, Ministry of Education, Hohai University, Nanjing 210098, China b College of Environment, Hohai University, Nanjing 210098, China
c School of Environment, Nanjing Normal University, Nanjing 210097, China


In our previous study, we prepared the granules by embedding artemisinin into alginate-chitosan using microcapsule technology. These
granules can release artemisinin sustainably and have a strong inhibitory effect on the growth of both single Microcystis aeruginosa and mixed
algae. To safely and effectively use artemisinin sustained-release granules to control algal blooms, the ecotoxicity was studied by assessing their
acute and chronic toxicity to Daphnia magna (D. magna) and Danio rerio (D. rerio), along with their antioxidant activities. The results showed
that the 48-h median effective concentration (EC50) of pure artemisinin to D. magna was 24.54 mg/L and the 96-h median lethal concentration
(LC50) of pure artemisinin to D. rerio was 68.08 mg/L. Both values were classified as intermediate toxicity according to the Organization for
Economic Co-operation and Development (OECD). The optimal algae inhibitory concentration of artemisinin sustained-release granules (1 g/L)
had low acute toxicity to both D. magna and D. rerio. The sustained-release granules had higher chronic toxicity to D. magna than to D. rerio.
Partial indices of D. magna were inhibited by granules when the concentrations were larger than 0.1 g/L. Low granule concentration had an
inductive effect on antioxidant enzyme activities in D. magna and D. rerio. With the increase of the exposure concentration and time, the enzyme
activity presented a trend of first increasing and then decreasing, and the overall changes were significant. The change trend and range of enzyme
activity indicated that the granules could cause serious oxidative stress to D. magna and D. rerio, and the changes were consistent with the results
of toxicity experimentation.

Keywords Artemisinin sustained-release granules   Aquatic organisms   Toxicity assessment   Median lethal concentration   Antioxidant enzyme activity  
Received 2019-09-20 Revised 2020-04-08 Online: 2020-06-30 
DOI: https://doi.org/10.1016/j.wse.2020.06.007

This work was supported by the National Natural Science Foundation of China (Grants No. 91647206 and 51779079), the Program for Changjiang Scholars and Innovative Research Team at Hohai University (Grant No.IRT13061), the Project Funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD), and the Top-notch Academic Programs Project of Jiangsu Higher Education Institutions (TAPP).

Corresponding Authors: Li-xiao Ni
Email: nilixiao@hhu.edu.cn
About author:


Abdelgawad, Z.A., Khalafaallah, A.A., Abdallah, M.M., 2014. Impact of Methyl jasmonate on antioxidant activity and some biochemical aspects of maize plant grown under water stress condition. Agricultural Sciences 5(12), 1077-1088. https://doi.org/10.4236/as.2014.512117.

Adam, N., Vakurov, A., Knapen, D., Blust, R., 2015. The chronic toxicity of CuO nanoparticles and copper salt to Daphnia magna. Journal of Hazardous Materials 283, 416-422. https://doi.org/10.1016/j.jhazmat.2014.09.037.

Almeselmani, M., Deshmukh, P.S., Sairam, R.K., 2015. High temperature stress tolerance in wheat genotypes: Role of antioxidant defence enzymes. Acta Agronomica Hungarica 57(1), 1-14. https://doi.org/10.1556/aagr.57.2009.1.1.

Barata, C., Campos, B., Rivetti, C., Leblanc, G.A., Eytcheson, S., Mcknight, S., Tobor-Kaplon, M., Buitenweg, S.D.V., Choi, S., Choi, J., et al., 2016. Validation of a two-generational reproduction test in Daphnia magna: An interlaboratory exercise. Science of the Total Environment 579, 1073-1083. https://doi.org/10.1016/j.scitotenv.2016.11.066.

Beauchamp, C., Fridovich, I., 1971. Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry 44(1), 276-287. https://doi.org/10.1016/0003-2697(71)90370-8.

Braunbeck, T., Boettcher, M., Hollert, H., Kosmehl, T., Seitz, N., Lammer, E., Leist, E., Rudolf, M., Seitz, N., 2005. Towards an alternative for the acute fish LC50 test in chemical assessment: The fish embryo toxicity test goes multi-species-An update. Altex 22(2), 87-102.

Camargo, M.M.P., Martinez, C.B.R., 2007. Histopathology of gills, kidney and liver of a Neotropical fish caged in an urban stream. Neotropical Ichthyology 5(3), 327-336. https://doi.org/10.1590/s1679-62252007000300013.

Chadha, R., Gupta, S., Pathak, N., 2012. Artesunate-loaded chitosan/lecithin nanoparticles: Preparation, characterization, and in vivo studies. Drug Development & Industrial Pharmacy 38(12), 1538-1546. https://doi.org/10.3109/03639045.2012.658812.

Cheng, C.W., Chen, L.Y., Chou, C.W., Liang, J.Y., 2015. Investigations of riboflavin photolysis via coloured light in the nitro blue tetrazolium assay for superoxide dismutase activity. Journal of Photochemistry & Photobiology B: Biology 148, 262-267. https://doi.org/10.1016/j.jphotobiol.2015.04.028.

Cheng, F., Cheng, Z.H., 2015. Research progress on the use of plant allelopathy in agriculture and the physiological and ecological mechanisms of allelopathy. Frontiers in Plant Science 6. https://doi.org/10.3389/fpls.2015.01020.

Chiang, I.Z., Huang, W.Y., Wu, J.T., 2010. Allelochemicals of Botryococcus braunii (Chlorophyceae). Journal of Phycology 40(3), 474-480. https://doi.org/10.1111/j.1529-8817.2004.03096.x.

Cortés, E., 2016. Perspectives on the intrinsic rate of population growth. Methods in Ecology & Evolution 7(10), 1136-1145. https://doi.org/10.1111/2041-210X.12592.

Du, Z.K, Zhu, L.S., Dong, M., Wang, J.H., Wang, J., Xie, H., Zhu, S.Y., 2012. Effects of the ionic liquid
[Omim]PF6 on antioxidant enzyme systems, ROS and DNA damage in zebrafish (
Danio rerio). Aquatic Toxicology 124-125, 91-93. https://doi.org/10.1016/j.aquatox.2012.08.002.

Fabrowska, J., Messyasz, B., Pankiewicz, R., Wilińska, P., ??ska, B., 2018. Seasonal differences in the content of phenols and pigments in thalli of freshwater Cladophora glomerata and its habitat. Water Research 135, 66-74. https://doi.org/10.1016/j.watres.2018.02.020.

Feng, R.W., Wei, C.Y., Tu, S.T., 2013. The roles of selenium in protecting plants against abiotic stresses. Environmental & Experimental Botany 87, 58-68. https://doi.org/10.1016/j.envexpbot.2012.09.002.

Giannopolitis, C.N., Ries, S.K., 1977. Superoxide dismutases: II. Purification and quantitative relationship with water-soluble protein in seedlings. Plant Physiology 59, 315-318. https://doi.org/10.1104/pp.59.2.315.

Griffiths, D.J., Saker, M.L., 2003. The Palm Island mystery disease 20 years on: A review of research on the cyanotoxin cylindrospermopsin. Environmental Toxicology 18(2), 78-93. https://doi.org/10.1002/tox.10103.

Griffitt, R.J., Weil, R., Hyndman, K.A., Denslow, N.D., Powers, K., Taylor, D., Barber, D.S., 2007. Exposure to copper nanoparticles causes gill injury and acute lethality in zebrafish (Danio rerio). Environmental Science & Technology 41, 8178-8186. https://doi.org/10.1021/es071235e.

Imlay, J.A., 2013. The molecular mechanisms and physiological consequences of oxidative stress: Lessons from a model bacterium. Nature Reviews Microbiology 11, 443-454. https://doi.org/10.1038/nrmicro3032.

Jung Collard, H.-R., Ji, K., Lee, S., Liu, X., Kang, S., Kho, Y., Ahn, B., Ryu, J., Lee, J., Choi, K., 2013. Toxicity and endocrine disruption in zebrafish (Danio rerio) and two freshwater invertebrates (Daphnia magna and Moina macrocopa) after chronic exposure to mefenamic acid. Ecotoxicology & Environmental Safety 94, 80-86. https://doi.org/10.1016/j.ecoenv.2013.04.027.

Kim, S.J., Yim, E.C., Park, I.T., Kim, S.W., Cho, H., 2011. Comparison of the acute toxicities of novel algicides, thiazolidinedione derivatives TD49 and TD53, to various marine organisms. Environmental Toxicology and Chemistry 30(12), 2810-2816. https://doi.org/10.1002/etc.691.

Krishnaraj, C., Harper, S.L., Yun, S.I., 2015. In vivo toxicological assessment of biologically synthesized silver nanoparticles in adult zebrafish (Danio rerio). Journal of Hazardous Materials 301, 480-491. https://doi.org/10.1016/j.jhazmat.2015.09.022.

Lee, T.Y., Liu, M.S., Huang, L.J., Lue, S.I., Lin, L.C., Yang, R.C., 2013. Bioenergetic failure correlates with autophagy and apoptosis in rat liver following silver nanoparticle intraperitoneal administration. Particle & Fibre Toxicology 10, 40. https://doi.org/10.1186/1743-8977-10-40.

Levente, V., Bud, I., 2010. Effects of hydrogen peroxide on Compsopogon caeruleus (Rhodophycophyta) and two superior plants. Aquaculture, Aquarium, Conservation & Legislation 3(5), 362-372.

Lopes, K.C., Ferrão-Filho, A.S., Santos, E.G.N., Santos, C.P., 2017. First report of neurotoxic effect of the cyanobacterium Cylindrospermopsis raciborskii on the motility of trematode metacercariae. Journal of Helminthology 92(2), 244-249. https://doi.org/10.1017/s0022149x17000281.

Ma, Y.H., Wang, J.K., Peng, C., Ding, Y.Y., He, X., Zhang, P., Li, N., Lan, T., Wang, D.Q., Zhang, Z.H., et al. 2016. Toxicity of cerium and thorium on Daphnia magna. Ecotoxicology & Environmental Safety 134, 226-232. https://doi.org/10.1016/j.ecoenv.2016.09.006.

Malar, S., Shivendra Vikram, S., JC Favas, P., Perumal, V., 2016. Lead heavy metal toxicity induced changes on growth and antioxidative enzymes level in water hyacinths
Eichhornia crassipes (Mart.)]. Botanical Studies 55, 54. https://doi.org/10.1186/s40529-014-0054-6.

Meng, P.P., Pei, H.Y., Hu, W.R., Liu, Z.D., Li, X.Q., Xu, H.Z., 2015. Allelopathic effects of Ailanthus altissima extracts on Microcystis aeruginosa growth, physiological changes and microcystins release. Chemosphere 141, 219-226. https://doi.org/10.1016/j.chemosphere.2015.07.057.

Murray, D., Jefferson, B., Jarvis, P., Parsons, S.A., 2010. Inhibition of three algae species using chemicals released from barley straw. Environmental Technology 31(4), 455-466. https://doi.org/10.1080/09593331003663294.

Ni, L.X., Acharya, K., Hao, X.Y., Li, S.Y., 2012. Isolation and identification of an anti-algal compound from Artemisia annua and mechanisms of inhibitory effect on algae. Chemosphere 88(9), 1051-1057. https://doi.org/10.1016/j.chemosphere.2012.05.009.

Ni, L.X., Acharya, K., Ren, G.X., Li, S.Y., Li, Y.P., Li, Y., 2013. Preparation and characterization of anti-algal sustained-release granules and their inhibitory effects on algae. Chemosphere 91(5), 608-615. https://doi.org/10.1016/j.chemosphere.2012.12.064.

Ni, L.X., Li, D.Y., Hu, S.Z., Wang, P.F., Li, S.Y., Li, Y.P., Li, Y., Acharya, K., 2015. Effects of artemisinin sustained-release granules on mixed alga growth and microcystins production and release. Environmental Science & Pollution Research 22, 18637-18644. https://doi.org/10.1007/s11356-015-5438-y.

Organization for Economic Co-operation and Development (OECD), 2004a. OECD Guidelines for the Testing of Chemicals. OECD. https://doi.org/10.1787/20745753.

Organization for Economic Co-operation and Development (OECD), 2004b. OECD Guidelines for the Testing of Chemicals. Test No. 202: Daphnia sp. Acute Immobilisation Test. OECD. https://doi.org/10.1787/9789264069947-en.

Organization for Economic Co-operation and Development (OECD), 2012. Guideline for the Testing of Chemicals. Test No. 211: Daphnia magna Reproduction Test. OECD. https://doi.org/10.1787/9789264185203-en.

Qian, H.F., Yu, S.Q., Sun, Z.Q., Xie, X.C, Liu, W.P., Fu, Z.W., 2010. Effects of copper sulfate, hydrogen peroxide and N-phenyl-2-naphthylamine on oxidative stress and the expression of genes involved photosynthesis and microcystin disposition in Microcystis aeruginosa. Aquatic Toxicology 99(3), 405-412. https://doi.org/10.1016/j.aquatox.2010.05.018.

Ribeiro, T.P., Fernandes, C., Melo, K.V., Ferreira, S.S., Lessa, J.A., Franco, R.W.A., Schenk, G., Pereira, M.D., Horn Jr., A., 2015. Iron, copper, and manganese complexes with in vitro superoxide dismutase and/or catalase activities that keep Saccharomyces cerevisiae cells alive under severe oxidative stress. Free Radical Biology and Medicine 80, 67-76. https://doi.org/10.1016/j.freeradbiomed.2014.12.005.

Sabullah, M.K., Ahmad, S.A., Shukor, M.Y., Gansau, A.J., Syed, M.A., Sulaiman, M.R., Shamaan, N.A., 2015. Heavy metal biomarker: Fish behavior, cellular alteration, enzymatic reaction and proteomics approaches. International Food Research Journal 22(2), 435-454.

Van Veld, P.A., Patton, J.S., Lee, R.F., 1988. Effect of preexposure to dietary benzo
[a]pyrene (BP) on the first-pass metabolism of BP by the intestine of toadfish (
Opsanus tau): In vivo studies using portal vein-catheterized fish. Toxicology and Applied Pharmacology 92, 255-265. https://doi.org/10.1016/0041-008x(88)90385-7.

Villarroel, M.J., Sancho, E., Andreu-Moliner, E., Ferrando, M.D., 2013. Caloric content of Daphnia magna as reflect of propanil stress during a short-term exposure and its relationship to long-term responses. Environmental Toxicology Pharmacology 35(3), 465-472. https://doi.org/10.1016/j.etap.2013.02.012.

Wu, H., Gao, C., Guo, Y., Zhang, Y., Zhang, J., Ma, E., 2014. Acute toxicity and sublethal effects of fipronil on detoxification enzymes in juvenile zebrafish (Danio rerio). Pesticide Biochemistry & Physiology 115, 9-14. https://doi.org/10.1016/j.pestbp.2014.07.010.

Xiong, D.W., Fang, T., Yu, L.P., Sima, X.F., Zhu, W.T., 2011. Effects of nano-scale TiO2, ZnO and their bulk counterparts on zebrafish: Acute toxicity, oxidative stress and oxidative damage. Science of the Total Environment 409(8), 1444-1452. https://doi.org/10.1016/j.scitotenv.2011.01.015.

Zhang, S.L., Dai, W., Bi, X.D., Zhang, D.J., Xing, K.Z., 2013. Effect of environmental factors on allelopathic inhibition of Microcystis aeruginosa by berberine. Water Science & Technology 68(2), 419-424. https://doi.org/10.2166/wst.2013.243.

Zhang, T.T., Wu, M.H.P., Nie, L.W., 2009. Allelopathic effects of submerged macrophyte Chara vulgaris on toxic Microcystis aeruginosa. Allelopathy Journal 23(2), 391-402.

Zhou, L.H., Chen, X.H., Zheng, T.L., 2010. Study on the ecological safety of algacides: A comprehensive strategy for their screening. Journal of Applied Phycology 22, 803-811. https://doi.org/10.1007/s10811-010-9522-x.

Similar articles

Copyright by Water Science and Engineering