Skip to main content
Log in

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

  • Environmental Pollution, Food Contamination, Risk Assessment and Remediation
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aguesse PC, Dussart BH (1956) Sur quelques Crustacés de Camargue et leur écologie. Vie et Milieu 7(2):481–520

    Google Scholar 

  • 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):310–319

    Google Scholar 

  • 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):407–427

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Avery SV (2011) Molecular targets of oxidative stress. Biochem J 434:201–210. https://doi.org/10.1042/BJ20101695

    Article  CAS  Google Scholar 

  • 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 803–804:27–33

    Google Scholar 

  • 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, Romania

  • 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 49:19–27

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Burgeot T, Woll S, Galgani F (1996) Evaluation of the micronucleus test on Mytilus galloprovincialis for monitoring applications along French coasts. Mar Pollut Bull 32:39–46

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Choung CB, Hyne RV, Stevens MM, Hose GC (2013) The ecological effects of a herbicide-insecticide mixture on an experimental freshwater ecosystem. Environ Pollut 172:264–274

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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):953–958

    Google Scholar 

  • CRDA Kairouan (unknown) Etude de réhabilitation du P.I. Sidi Sâad, Fiche d’identification environnementale et sociale. Hydro Plante 1–19

  • 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)

  • 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

    Article  CAS  Google Scholar 

  • 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):488–491

    Google Scholar 

  • 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 96:86–92

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 69:145–154

    CAS  Google Scholar 

  • 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, Leiden

  • 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):1592–1595

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Forget J, Bocquéné G (1999) Partial purification and enzymatic characterization of acetylcholinesterase from the intertidal copepod Tigriopus brevicornis. Comp Biochem Physiol B 132:345–350

    Google Scholar 

  • 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 132:85–92

    Google Scholar 

  • 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):195–204

    CAS  Google Scholar 

  • Fossi MC, Minutoli R, Guglielmo L (2001) Preliminary results of biomarker responses in zooplankton of brackish environments. Mar Pollut Bull 42:745–748

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Galgani F, Bocquené G (1991) Semi-automated colorimetric and enzymatic assays for aquatic organisms using plate readers. Water Res 25:147–150

    CAS  Google Scholar 

  • 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 138:249–269

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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):70–80

    CAS  Google Scholar 

  • 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 33:431–439

    Google Scholar 

  • 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):111–116

    Google Scholar 

  • 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 104:34–42

    CAS  Google Scholar 

  • 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 29:227–247

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 2018

    Google Scholar 

  • 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 472:155–161

    CAS  Google Scholar 

  • Jarvis AL, Bernot MJ, Bernot RJ (2014) The effect of the psychiatric drug carbamazepine on freshwater invertebrate communities and ecosystem dynamics. Sci Total Environ 496:461–470

    CAS  Google Scholar 

  • Jemec A, Tister T, Drobne D, Sepeié K, Jamnik P, Ros M (2008) Biochemical biomarkers in chronically metal-stressed daphnids. Comp Biochem Physiol C147:61–68

    Google Scholar 

  • 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):464–469

    Google Scholar 

  • 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 92:298–293

    Google Scholar 

  • 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):195–202

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 209:28–36

    Google Scholar 

  • 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 4:16–26

    Google Scholar 

  • Lu GH, Liu JC, Sun LS, Yuan LY (2015) Toxicity of perfluorononanoic acid and perfluorooctane sulfonate to Daphnia magna. Water Sci Eng 8(1):40–48

    Google Scholar 

  • Margaritora FG (1985) Cladocera, Fauna d’Italia 23. Calderini, Bologna

    Google Scholar 

  • Minutoli R, Fossi MC, Gugliemo L (2002) Evaluation of acetylcholinesterase activity in several zooplanktonic crustaceans. Mar Environ Res 54:799–804

    CAS  Google Scholar 

  • Mohamed EH (2014) Biochemical response of the Cyclopoda copepod Apocyclops borneoensis exposed to nickel. Jordan J Biol Sci 7(1):41–47

    Google Scholar 

  • 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):731–748

    Google Scholar 

  • 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 87:413–422

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 775-776:20–30

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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, Tunisia

  • 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 190:61–74

    Google Scholar 

  • 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):817–822

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 465:145–150

    CAS  Google Scholar 

  • Pellegri V, Gorbi G, Buschini A (2014) Comet assay on Daphnia magna in eco-genotoxicity testing. Aquat Toxicol 155:261–268

    CAS  Google Scholar 

  • 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 70:340–347

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 29:371–385

    CAS  Google Scholar 

  • 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 83:161–173

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

  • 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 132-133:182–189

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 49:139–143

    CAS  Google Scholar 

  • Schmid W (1976) The micronucleus test for cytogenetic analysis. In: Hollander A (ed) Chemical mutagens 4. Plenum Press, New York, pp 31–53

    Google Scholar 

  • 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 56:999–1007

    Google Scholar 

  • 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 Tunisie

  • 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 218:353–360

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 15:229–236

  • Szalinska E (2010) Reservoirs as a trap for pollutants: the Czorsztyn reservoir. NEAR curriculum in natural environmental science. Terre Environ 88:205–209

    Google Scholar 

  • 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 120:351–356

    CAS  Google Scholar 

  • 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):367–377

    Google Scholar 

  • 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 3:4548–4557

    Google Scholar 

  • 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):658–665

    CAS  Google Scholar 

  • Vincke MMJ (1982) Revue des sites potentiels pour l’aquaculture dans les eaux continentales tunisiennes. http://www.fao.org/docrep/006/q2659f/Q2659F17.htm

  • Wang MH, Wang GZ (2009) Biochemical response of the copepod Tigriopus japonicas Mori experimentally exposed to cadmium. Arch Environ Contam Toxicol 57:707–717

    CAS  Google Scholar 

  • 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):400–409

    CAS  Google Scholar 

  • 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):154–171

    Google Scholar 

  • 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 680:2–6

    CAS  Google Scholar 

  • Žegura B, Štraser A, Metka F (2011) Genotoxicity and potential carcinogenicity of cyanobacterial toxins—a review. Mutat Res 727:16–41

    Google Scholar 

  • 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):30–37

    CAS  Google Scholar 

  • 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 606:135–150

    CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sabria Barka.

Ethics declarations

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.

Additional information

Responsible editor: Philippe Garrigues

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Barka, S., Gdara, I., Ouanes-Ben Othmen, Z. et al. Seasonal ecotoxicological monitoring of freshwater zooplankton in Bir Mcherga dam (Tunisia). Environ Sci Pollut Res 27, 5670–5680 (2020). https://doi.org/10.1007/s11356-019-04271-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-04271-6

Keywords

Navigation