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Seasonal ecotoxicological monitoring of freshwater zooplankton in Bir Mcherga dam (Tunisia)

  • Sabria BarkaEmail author
  • Imene Gdara
  • Zouhour Ouanes-Ben Othmen
  • Samia Mouelhi
  • Monia El Bour
  • Amel Hamza-Chaffai
Environmental Pollution, Food Contamination, Risk Assessment and Remediation
  • 63 Downloads

Abstract

Dams represent large semi-closed reservoirs of pesticides and various organic and inorganic pollutants from agricultural and human activities, and their monitoring should receive special attention. This study evaluated the environmental health status of Bir Mcherga dam using zooplankton species. The dam has a capacity of 130 Mm3 and its waters are used for irrigation, water drinking supply, and fishery. Copepods and cladocerans (crustaceans) were collected in situ monthly between October and August 2012. Oxidative stress (CAT, MDA), neurotoxicity (AChE), and genotoxicity (micronucleus test) biomarkers were analyzed in two zooplankton species: Acanthocyclops robustus and Diaphanosoma mongolianum. High values of cells with a micronucleus were observed during summer. AChE activities were inhibited during early winter and summer. The high seasonal variability of CAT and MDA levels indicates that zooplankton is continuously exposed to different oxidative stresses. These results suggest that there is an obvious and continuous multi-faceted stress in Bir Mcherga reservoir and, consequently, an urgent monitoring of freshwater environments in Tunisia is needed, particularly those intended for human consumption and irrigation.

Keywords

Bir Mcherga dam Zooplankton Catalase Malondialdehyde Acetylcholinesterase Micronucleus test 

Notes

Acknowledgments

This study was done in the frame of the MOTOX programme Institut National des Sciences et Technologies de la Mer (INSTM-Tunisia). The authors express their gratitude to the Ecotoxicology Unit of INSTM (Monastir) and particularly to Dr. Rym Ben Dhiab and Dr. Hatem Ben Ouada and to the people in charge of Bir Mcherga dam in the district of Zaghouan for their assistance. We also thank Nick Dettman for the English corrections.

Compliance with ethical standards

Conflict of interest

There is no conflict of interest among the co-authors, and the primary author confirms that this original research article is not under consideration for publication anywhere else.

References

  1. Aguesse PC, Dussart BH (1956) Sur quelques Crustacés de Camargue et leur écologie. Vie et Milieu 7(2):481–520Google Scholar
  2. Alimba CG, Bakare AA (2016) In vivo micronucleus test in the assessment of cytogenotoxicity of landfill leachates in three animal models from various ecological habitats. Ecotoxicol 5(2):310–319Google Scholar
  3. Ammar M, Comte K, El Bour M (2015) Seasonal dynamics of phytoplankton and microbiological communities during sporadic fish die-offs in the Bir M’Cherga reservoir (Tunisia). Cryptogam Algol 36(4):407–427Google Scholar
  4. Antão Barboza LG, Russo Vieira L, Branco V, Figueiredo N, Carvalho F, Carvalho C, Guilhermino L (2018) Microplastics cause neurotoxicity, oxidative damage and energy-related changes and interact with the bioaccumulation of mercury in the European seabass, Dicentrarchus labrax (Linnaeus, 1758). Aquat Toxicol 195:49–57.  https://doi.org/10.1016/j.aquatox.2017.12.008 Google Scholar
  5. Avery SV (2011) Molecular targets of oxidative stress. Biochem J 434:201–210.  https://doi.org/10.1042/BJ20101695 Google Scholar
  6. Barka S, Ouanes Z, Gharbi A, Gdara I, Mouelhi S, Hamza-Chaffai A (2016) Monitoring genotoxicity in freshwater microcrustaceans: a new application of the micronucleus assay. Mutat Res 803–804:27–33Google Scholar
  7. Ben Rejeb Jenhani A, Fathalli A, Romdhane MS (2012) Phytoplankton assemblages in Bir Mcherga freshwater reservoir (Tunisia). In: Gâştescu P, Lewis Jr W, Breţcan P (eds) Water resources and wetlands. Conference Proceedings, 14–16 September 2012, Tulcea, RomaniaGoogle Scholar
  8. Bendjoudi D, Zouaoui F, Errahmani MB, Benjeddou K, Chekir N (2013) Measurements of two biomarkers catalase and malondialdehyde in Perna perna and Mytilus galloprovincialis (Mollusca, Bivalvia) following acute contamination by Staphylococcus aureus. Travaux de l’Institut Scientifique, Rabat, Série Zoologie 49:19–27Google Scholar
  9. Bradford MM (1976) Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254.  https://doi.org/10.1016/0003-2697(76)90527-3
  10. Burgeot T, Woll S, Galgani F (1996) Evaluation of the micronucleus test on Mytilus galloprovincialis for monitoring applications along French coasts. Mar Pollut Bull 32:39–46Google Scholar
  11. Cailleaud K, Maillet G, Budzinski H, Souissi S, Forget-Leray J (2007) Effects of salinity and temperature on the expression of enzymatic biomarkers in Eurytemora affinis (Calanoida, Copepoda). Comp Biochem Physiol A147:841–849.  https://doi.org/10.1016/j.cbpa.2006.09.012 Google Scholar
  12. Cailleaud K, Forget-Leray J, Peluhet L, LeMenach K, Souissi S, Budzinski H (2009) Tidal influence on the distribution of hydrophobic organic contaminants in the Seine Estuary and biomarker responses on the copepod Eurytemora affinis. Environ Pollut 157(1):64–71.  https://doi.org/10.1016/j.envpol.2008.07.026 Google Scholar
  13. Choung CB, Hyne RV, Stevens MM, Hose GC (2013) The ecological effects of a herbicide-insecticide mixture on an experimental freshwater ecosystem. Environ Pollut 172:264–274Google Scholar
  14. Cikcikoglu YN, Yildirim N, Danabas D, Danabas S (2014) Use of acetylcholinesterase, glutathione S-transferase and cytochrome P450 1A1 in Capoeta umbla as biomarkers for monitoring of pollution in Uzuncayir Dam Lake (Tunceli, Turkey). Environ Toxicol Pharmacol 37(3):1169–1176.  https://doi.org/10.1016/j.etap.2014.04.001
  15. Cohen D, Nisbett RE, Bowdle BF, Schwartz N (1996) Comparison of hepatic and renal drug-metabolising enzyme activities in sheep given single or two-fold challenge infections with Fasciola hepatica. Int J Parasitol 30(8):953–958Google Scholar
  16. CRDA Kairouan (unknown) Etude de réhabilitation du P.I. Sidi Sâad, Fiche d’identification environnementale et sociale. Hydro Plante 1–19Google Scholar
  17. Daoud A, Djemali K, Goguel B, Leclerc S (2009) Couplage dun évacuateur vanné avec une tranche de laminage, cas du barrage de Sidi Salem en Tunisie. Colloque CFBR-SHF: «Dimensionnement et fonctionnement des évacuateurs de crues», January 20-21, Lyon (France)Google Scholar
  18. De Wit P, Dupont S, Thor P (2016) Selection on oxidative phosphorylation and ribosomal structure as a multigenerational response to ocean acidification in the common copepod Pseudocalanus acuspes. Evol Appl 9(9):1112–1123.  https://doi.org/10.1111/eva.12335 Google Scholar
  19. Di Marzio WD, Castaldo D, Pantani C, Di Gioccio A, Di Lorenzo T, Sàenz ME, Galassi DMP (2009) Relative sensitivity of hyporheic copepods to chemicals. Bull Environ Contam Toxicol 84(2):488–491Google Scholar
  20. Di Marzio WD, Castaldo D, Di Lorenzo T, Di Gioccio A, Sàenz ME, Galassi DMP (2013) Developmental endpoints of chronic exposure to suspected endocrine-disrupting chemicals on benthic and hyporheic copepods. Ecotoxicol Environ Saf 96:86–92Google Scholar
  21. Djemali I, Guillard J, Yule DL (2016) Seasonal and diel effects on acoustic fish biomass estimates: application to a shallow reservoir with untargeted common carp (Cyprinus carpio). Mar Freshw Res 68(3):528–537.  https://doi.org/10.1071/MF15249 Google Scholar
  22. Domingues I, Guilhermino L, Soares AMVM, Nogueira AJA (2007) Assessing dimethoate contamination in temperate and tropical climates: potential use of biomarkers in bioassays with two chironomid species. Chemosphere 69:145–154Google Scholar
  23. Dussart BH, Defaye D (2001) Introduction to the Copepoda. 2nd edition. Guide to the identification of the microinvertebrates of the continental waters of the world. Backhuys Publishers, LeidenGoogle Scholar
  24. El Jourmi L, Amine A, Boutaleb N, Abouakil N, El Antri S (2015) The use of biomarkers (catalase and malondialdehyde) in marine pollution monitoring: spatial variability. J Mater Environ Sci 6(6):1592–1595Google Scholar
  25. Ensibi C, Daly Yahia MN (2017) Toxicity assessment of cadmium chloride on planktonic copepods Centropages ponticus using biochemical markers. Toxicol Rep 1(4):83–88.  https://doi.org/10.1016/j.toxrep.2017.01.005 Google Scholar
  26. Fathalli A, Ben Rejeb Jenhani A, Moreira C, Welker M, Romdhane M, Antunes A, Vasconcelos V (2011) Molecular and phylogenetic characterization of potentially toxic cyanobacteria in Tunisian freshwaters. Syst Appl Microbiol 34:303–310.  https://doi.org/10.1016/j.syapm.2010.12.003 Google Scholar
  27. Forget J, Bocquéné G (1999) Partial purification and enzymatic characterization of acetylcholinesterase from the intertidal copepod Tigriopus brevicornis. Comp Biochem Physiol B 132:345–350Google Scholar
  28. Forget J, Livet S, Leboulenger F (2002) Partial purification and characterization of acetylcholinesterase (AChE) from the estuarine copepod Eurytemora affinis (Poppe). Comp Biochem Physica C 132:85–92Google Scholar
  29. Forget J, Beliaeff B, Bocquené G (2003) Acetylcholinesterase activity in copepods (Tigriopus brevicornis) from the Vilaine River estuary, France, as a biomarker of neurotoxic contaminants. Aquat Toxicol 62(3):195–204Google Scholar
  30. Fossi MC, Minutoli R, Guglielmo L (2001) Preliminary results of biomarker responses in zooplankton of brackish environments. Mar Pollut Bull 42:745–748Google Scholar
  31. Fuzinatto CF, Flohr L, Melegari SP, Matias WG (2013) Induction of micronucleus of Oreochromis niloticus exposed to waters from the Cubatão do Sul River, southern Brazil. Ecotoxicol Environ Saf 98:103–109.  https://doi.org/10.1016/j.ecoenv.2013.09.016 Google Scholar
  32. Galgani F, Bocquené G (1991) Semi-automated colorimetric and enzymatic assays for aquatic organisms using plate readers. Water Res 25:147–150Google Scholar
  33. Gauthier L, Van der Gaag MA, L'Haridon J, Ferrier V, Fernandez M (1993) In vivo detection of waste water and industrial effluent genotoxicity: use of the newt micronucleus test (Jaylet test). Sci Total Environ 138:249–269Google Scholar
  34. Glippa O, Engström-Öst J, Kanerva M, Rein A, Vuori K (2018) Oxidative stress and antioxidant defense responses in Acartia copepods in relation to environmental factors. PLoS One 13(4):e0195981.  https://doi.org/10.1371/journal.pone.0195981 Google Scholar
  35. Goswami AR, Aich A, Pal S, Chattopadhyay B, Datta S, Mukhopadhyay SK (2013) Antioxidant response to oxidative stress in zooplankton thrived in wastewater-fed ponds in East Calcutta Wetland Ecosystem, a Ramsar site. Toxicol Environ Chem 95(4):627–634.  https://doi.org/10.1080/02772248.2013.801142 Google Scholar
  36. Goswami P, Thirunavukkarasu S, Godhantaraman N (2014) Monitoring of genotoxicity in marine zooplankton induced by toxic metals in Ennore estuary, southeast coast of India. Mar Pollut Bull 88(1–2):70–80Google Scholar
  37. Güngördü A, Erkmen B, Kolankaya D (2012) Evaluation of spatial and temporal changes in biomarker responses in the common carp (Cyprinus carpio L.) for biomonitoring the Meriç Delta, Turkey. Environ Toxicol Pharmacol 33:431–439Google Scholar
  38. Gurinder Kaur W, Handa D, Kaur H, Rohit K (2015) Ecotoxicological studies on fish, Labeo rohita exposed to tannery industry effluent by using micronucleus test. Nucleus 58(2):111–116Google Scholar
  39. Guzman-Guillen R, Prieto Ortega AI, Martín-Camean A, Camean AM (2015) Beneficial effects of vitamin E supplementation against the oxidative stress on cylindrospermopsin-exposed tilapia (Oreochromis niloticus). Toxicon 104:34–42Google Scholar
  40. Haddaoui I, Mahjoub O, Mahjoub B, Boujelben A, Bahadir M (2017) Polycyclic aromatic hydrocarbon in conventional and non-conventional water resources used for irrigation in Tunisia. Larhyss J 29:227–247Google Scholar
  41. Hansen BH, Altin D, Vang SH, Nordtug T, Olsen AJ (2008) Effects of naphthalene on gene transcription in Calanus finmarchicus (Crustacea: Copepoda). Aquat Toxicol 86(2):157–165.  https://doi.org/10.1016/j.aquatox.2007.10.009 Google Scholar
  42. Hansen BH, Altin D, Booth A, Vang SH, Frenzel M, Sørheim KR, Brakstad OG, Størseth TR (2010) Molecular effects of diethanolamine exposure on Calanus finmarchicus (Crustacea: Copepoda). Aquat Toxicol 99(2):212–222.  https://doi.org/10.1016/j.aquatox.2010.04.018 Google Scholar
  43. Henricksen EO, Gabrielsen GW, Trudeau S, Wolkers J, Sagerup K, Skaare JU (2000) Organochlorines and possible biochemical effects in glaucous gulls (Larus hyperboreus) from Bjørnøya, the Barents Sea. Arch Environ Contam Toxicol 38:234–243 http://www.historique-meteo.net/afrique/tunisie. Accessed 26 Feb 2018Google Scholar
  44. Humpage AR, Fenech M, Thomas P, Falconer IR (2000) Micronucleus induction and chromosome loss in transformed human white cells indicate clastogenic and aneugenic action of the cyanobacterial toxin, cylindrospermopsin. Mutat Res 472:155–161Google Scholar
  45. Jarvis AL, Bernot MJ, Bernot RJ (2014) The effect of the psychiatric drug carbamazepine on freshwater invertebrate communities and ecosystem dynamics. Sci Total Environ 496:461–470Google Scholar
  46. Jemec A, Tister T, Drobne D, Sepeié K, Jamnik P, Ros M (2008) Biochemical biomarkers in chronically metal-stressed daphnids. Comp Biochem Physiol C147:61–68Google Scholar
  47. Jeyam G, Ramanibal M (2017) Impact of genotoxic contaminants on DNA integrity of copepod from freshwater bodies in Chennai, Tamil Nadu, India. J Environ Anal Toxicol 7(3):464–469Google Scholar
  48. Karadag H, Firat Ö, Firat Ö (2014) Use of oxidative stress biomarkers in Cyprinus carpio L. for the evaluation of water pollution in Atatürk Dam Lake (Adiyaman, Turkey). Bull Environ Contam Toxicol 92:298–293Google Scholar
  49. Karjalainen M, Engström-Ost J, Korpinen S, Peltonen H, Pääkkönen JP, Rönkkönen S, Suikkanen S, Viitasalo M (2007) Ecosystem consequences of cyanobacteria in the northern Baltic Sea. Ambio 36(2–3):195–202Google Scholar
  50. Kim BM, Rhee JS, Jeong CB, Seo JS, Park GS, Lee YM, Lee JS (2014) Heavy metals induce oxidative stress and trigger oxidative stress-mediated heat shock protein (hsp) modulation in the intertidal copepod Tigriopus japonicus. Comp Biochem Physiol C 166:65–74.  https://doi.org/10.1016/j.cbpc.2014.07.005 Google Scholar
  51. Kim H, Kim JS, Kim PJ, Won EJ, Lee YM (2018) Response of antioxidant enzymes to Cd and Pb exposure in water flea Daphnia magna: differential metal and age-specific patterns. Comp Biochem Physiol C 209:28–36Google Scholar
  52. Kushwaha B, Pandey S, Sharma S, Srivastara R, Kumar R, Sahebrao N, Nagpure S, Dabas A, Kumar Srivastara S (2012) In situ assessment of genotoxic and mutagenic potential of polluted river water in Channa punctatus and Mystus vittatus. Int Aquat Res 4:16–26Google Scholar
  53. Lu GH, Liu JC, Sun LS, Yuan LY (2015) Toxicity of perfluorononanoic acid and perfluorooctane sulfonate to Daphnia magna. Water Sci Eng 8(1):40–48Google Scholar
  54. Margaritora FG (1985) Cladocera, Fauna d’Italia 23. Calderini, BolognaGoogle Scholar
  55. Minutoli R, Fossi MC, Gugliemo L (2002) Evaluation of acetylcholinesterase activity in several zooplanktonic crustaceans. Mar Environ Res 54:799–804Google Scholar
  56. Mohamed EH (2014) Biochemical response of the Cyclopoda copepod Apocyclops borneoensis exposed to nickel. Jordan J Biol Sci 7(1):41–47Google Scholar
  57. Mouelhi S, Balvay G, Kraiem M (2000) Branchiopodes (Cténopodes et Anomopodes) et Copépodes des eaux continentales d’Afrique du Nord : inventaire et biodiversité. Zoosystema 22(4):731–748Google Scholar
  58. Mustapha SA, Davies SI, Jha AN (2012) Determination of hypoxia and dietary copper mediated sub-lethal toxicity in carp Cyprinus carpio at different levels of biological organization. Chemosphere 87:413–422Google Scholar
  59. Naïja N, Kestemont P, Chénais B, Haouas Z, Blust R, Helal AN, Marchand J (2017) Cadmium exposure exerts neurotoxic effects in peacock blennies Salaria pavo. Ecotoxicol Environ Saf 143:217–227.  https://doi.org/10.1016/j.ecoenv.2017.05.041 Google Scholar
  60. Obiakor MO, Okonkwo JC, Ezeonyejiaku CD (2014) Genotoxicity of freshwater ecosystem shows DNA damage in preponderant fish as validated by in vivo micronucleus induction in gill and kidney erythrocytes. Mutat Res 775-776:20–30Google Scholar
  61. Ouanes-Ben Othmen Z, Barka S, Ben Adeljelil Z, Mouelhi S, Krifa M, Kilani S, Chekir-Ghedira L, Forget-Leray J, Hamza-Chaffai A (2018) In situ genotoxicity assessment in freshwater zooplankton and sediments from different dams, ponds and temporary rivers in Tunisia. Environ Sci Pollut Res 26:1435–1444.  https://doi.org/10.1007/s11356-018-3703-6 Google Scholar
  62. Ouelhazi H, Talbi R, Methamem M, Charef A (2009) Impact des activités anthropiques sur la qualité des sédiments du littoral de Radès Sud-Est (Tunis). Coastal and Maritime Mediterranean Conference, Edition 1, Hammamet, TunisiaGoogle Scholar
  63. Palagano da Rocha M, Rosa Dourado PL, Lima Cardoso CA, Silvia Cândido L, Gonçalves Pereira J, Pires de Oliveira KM, Barufatti Grisolia A (2018) Tools for monitoring aquatic environments to identify anthropic effects. Environ Monit Assess 190:61–74Google Scholar
  64. Park SY, Choi J (2007) Cytotoxicity, genotoxicity and ecotoxicity assay using human cell and environmental species for the screening of the risk from pollutant exposure. Environ Int 33(6):817–822Google Scholar
  65. Pavan da Silva RR, Pires OR, Grisolia CK (2011) Genotoxicity in Oreochromis niloticus (Cichlidae) induced by Microcystis spp. bloom extract containing microcystins. Toxicon 58:259–264.  https://doi.org/10.1016/j.toxicon.2011.06.005 Google Scholar
  66. Pavlica M, Klobučar GIV, Vetma N, Erben R, Papeš D (2000) Detection of micronuclei in haemocytes of zebra mussel and great ramshorn snail exposed to pentachlorophenol. Mutat Res 465:145–150Google Scholar
  67. Pellegri V, Gorbi G, Buschini A (2014) Comet assay on Daphnia magna in eco-genotoxicity testing. Aquat Toxicol 155:261–268Google Scholar
  68. Perbiche-Neves G, Saito VS, Previattelli D, da Rocha CEF (2016) Cyclopoid copepods as bioindicators of eutrophication in reservoirs: do pattern hold for large spatial extents? Ecol Indic 70:340–347Google Scholar
  69. Pereira AMM, Soares AMV, Gonçalves FJM, Ribeiro R (2009) Test chambers and test procedures for in situ toxicity testing with zooplankton. Environ Toxicol Chem 18(9):1956–1964.  https://doi.org/10.1002/etc.5620180914 Google Scholar
  70. Puerto M, Jos A, Pichardo S, Moyano R, Blanco A, Camean AM (2014) Acute exposure to pure cylindrospermopsin results in oxidative stress and pathological alterations in tilapia (Oreochromis niloticus). Environ Toxicol 29:371–385Google Scholar
  71. Raisuddin S, Kwok KW, Leung KM, Schlenk D, Lee JS (2007) The copepod Tigriopus: a promising marine model organism for ecotoxicology and environmental genomics. Aquat Toxicol 83:161–173Google Scholar
  72. Rebechi-Baggio D, Richardi VS, Vicentini M, Guiloski IC, Silva de Assis HC, Navarro-Silva MA (2016) Factors that alter the biochemical biomarkers of environmental contamination in Chironomus sancticaroli (Diptera, Chironomidae). Rev Bras Entomol 60(4):341–346.  https://doi.org/10.1016/j.rbe.2016.07.002 Google Scholar
  73. Report of the Tunisian Court of Auditors, Tunisian Republic (2014) http://www.courdescomptes.nat.tn/Fr/thematiques_58_4_-1_0_0_0000_0000_traitements-des-eaux-usees-et-leurs-utilisations__215. Accessed 18 May 2018
  74. Rhee JS, Yu IT, Kim BM, Jeong CB, Lee KW, Kim MJ, Lee SJ, Park GS, Lee JS (2013) Copper induces apoptotic cell death through reactive oxygen species-triggered oxidative stress in the intertidal copepod Tigriopus japonicus. Aquat Toxicol 132-133:182–189Google Scholar
  75. Rodriguez LP, Caliani I, Brugnano C, Granata A, Guglielmo R, Guglielmo L, Zagami G, Minutoli R (2017) Biomarkers employment in planktonic copepods for early management and conservation of aquatic ecosystems: the case of the ‘Capo Peloro’ lakes (southern Italy). Reg Stud Mar Sci 18:161–169.  https://doi.org/10.1016/j.rsma.2017.10.002 Google Scholar
  76. Sanchez-Galan S, Linde AR, Ayllon F, Garcia-Vazquez E (2001) Induction of micronuclei in eel (Anguilla Anguilla L.) by heavy metals. Ecotoxicol Environ Saf 49:139–143Google Scholar
  77. Schmid W (1976) The micronucleus test for cytogenetic analysis. In: Hollander A (ed) Chemical mutagens 4. Plenum Press, New York, pp 31–53Google Scholar
  78. Solé M, Lobera G, Lima D, Reis-Henriques MA, Santos MM (2008) Esterases activities and peroxydation levels in muscle tissue of the shanny Lipophrys pholis along several sites from the Portuguese coast. Mar Pollut Bull 56:999–1007Google Scholar
  79. Souga R (2007) La biodiversité des Copépodes, Cladocères et Rotifères dans deux retenues de barrage de la Tunisie Septentrionale: le barrage Bir M’cherga (Zaghouan) et le barrage Oued Hma (Ben Arous). Dissertation, Institut National d’Agronomie de TunisieGoogle Scholar
  80. Sponchiado G, Fortunato de Lucena Reynaldo AM, de Andrade ACB, Carvalho de Vasconcelos E, Adam ML, Ribas de Oliveira CM (2011) Genotoxic effects in erythrocytes of Oreochromis niloticus exposed to nangrams-per-liter concentration of 17β-estradiol (E2): an assessment using micronucleus test and comet assay. Water Air Soil Pollut 218:353–360Google Scholar
  81. Sun H, Wang W, Geng L, Chen Y, Yang Z (2013) In situ studies on growth, oxidative stress responses, and gene expression of juvenile bighead carp (Hypophthalmichthys nobilis) to eutrophic lake water dominated by cyanobacterial blooms. Chemosphere 93(2):421–427.  https://doi.org/10.1016/j.chemosphere.2013.05.022 Google Scholar
  82. Sunderman FW, Marzoul A, Hopfer SM, Zaharia O, Reid MC (1985) Increased lipid peroxidation in tissues of nickel chloride-treated rats. Ann Clin Lab Sci 15:229–236Google Scholar
  83. Szalinska E (2010) Reservoirs as a trap for pollutants: the Czorsztyn reservoir. NEAR curriculum in natural environmental science. Terre Environ 88:205–209Google Scholar
  84. Toumi H, Boumaiza M, Millet M, Radetski CM, Felten V (2015) Is acethylcholinesterase a biomarker of susceptibility in Daphnia magna (Crustacea, Cladocera) after deltamethrin exposure? Chemosphere 120:351–356Google Scholar
  85. Turki S, Rezig M, El Abed A (2004) Biodiversity of the zooplanktonic populations in the Bir M’Cherga reservoir (Zaghouan, Tunisie). Bull Soc Zool Fr 129(4):367–377Google Scholar
  86. Vehmaa A, Hogfors H, Gorokhova E, Brutemark A, Holmborn T, Engström-Öst J (2013) Projected marine climate change: effects on copepod oxidative status and reproduction. Ecol Evol 3:4548–4557Google Scholar
  87. Vicentini M, Morais GS, Rebechi-Baggio D, Richardi VS, Santos GS, Cestari MM, Navarro-Silva MA (2017) Benzo(a)pyrene exposure cuases genotoxic and biochemical changes in the midge larvae of Chironomus sancticaroli Strixino & Strixini (Diptera: Chironomidae). Neotrop Entomol 46(6):658–665Google Scholar
  88. Vincke MMJ (1982) Revue des sites potentiels pour l’aquaculture dans les eaux continentales tunisiennes. http://www.fao.org/docrep/006/q2659f/Q2659F17.htm
  89. Wang MH, Wang GZ (2009) Biochemical response of the copepod Tigriopus japonicas Mori experimentally exposed to cadmium. Arch Environ Contam Toxicol 57:707–717Google Scholar
  90. Wiegand C, Peuthert A, Pflugmacher S, Carmeli S (2002) Effects of microcin SF608 and microcystin-LR, two cyanotobacterial compounds produced by Microcystis sp., on aquatic organisms. Environ Toxicol 17(4):400–409Google Scholar
  91. Wojtal-Frankiewicz A, Bernasinska J, Jurczak T, Gwozdzinski K, Frankiewicz P, Wielane M (2013) Microcystin assimilation and detoxification by Daphnia spp. in two ecosystems of different cyanotoxin concentrations. J Limnol 72(1):154–171Google Scholar
  92. Yin XH, GuoNian Z, Xian Bing L, ShaoYing L (2009) Genotoxicity evaluation of chlorpyrifos to amphibian Chinese toad (Amphibian: Anura) by comet assay and micronucleus test. Mutat Res 680:2–6Google Scholar
  93. Žegura B, Štraser A, Metka F (2011) Genotoxicity and potential carcinogenicity of cyanobacterial toxins—a review. Mutat Res 727:16–41Google Scholar
  94. Zhang D, Li S, Wang G, Guo D, Xing K, Zhang S (2012) Biochemical responses of the copepod Centropages tenuiremis to CO2-driven acidified seawater. Water Sci Technol 65(1):30–37Google Scholar
  95. Zhou Q, Zhang J, Fu J, Shi J, Jiang G (2008) Biomonitoring: an appealing tool assessment of metal pollution in the aquatic ecosystem. Anal Chim Acta 606:135–150Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Sabria Barka
    • 1
    • 2
    Email author
  • Imene Gdara
    • 1
    • 2
  • Zouhour Ouanes-Ben Othmen
    • 1
    • 2
  • Samia Mouelhi
    • 3
  • Monia El Bour
    • 4
  • Amel Hamza-Chaffai
    • 2
  1. 1.Institut Supérieur de Biotechnologie de MonastirMonastirTunisia
  2. 2.Unité de Recherche de Toxicologie Environnementale et Marine, UR 09-03, IPEISSfax UniversitySfaxTunisia
  3. 3.Unité de Recherche de Biologie Animale et Systématique Evolutive 2092, Campus Universitaire, Manar IIFaculté des Sciences de TunisTunisTunisia
  4. 4.Laboratoire de Biotechnologie et Biodiversité AquatiquesNational Institute of Sea Sciences and Technologies INSTMSalammbôTunisia

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