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Evaluation of bioconcentration of trace elements in the Western Mediterranean mouse Mus spretus at two Moroccan wetland sites

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Abstract

Many micromammals were shown to be vulnerable to metallic trace elements and are therefore suitable for biomonitoring. The objective of our research is to assess the concentration level of five trace elements (Cu, Pb, Cr, Fe and Zn) in small rodent Mus spretus organs (liver, kidneys and heart) from two Moroccan sites, Merja Zerga and Dayet Erroumi, threatened by massive fertilizer use. Tissue metal concentrations in this species varied widely with age, sex, sites and organs. The concentration of Cu in the liver was the highest among all the metals and was recorded in adult females of Merja Zerga with a maximum of 60 μg g−1; at Dayet Erroumi, it was around 14 μg g−1. At the same time, we found a similar trend for Fe, Pb, Cr and Zn in the three organs in males and females at the two sites. Highly significant differences between females at the two sites were recorded for the variables weight (W) and head to body length (TL) (t = -3.99; p < 0.001 and t = -2.24, p < 0.05), however, males showed equal values in the two sites. Spatiotemporal monitoring in small mammals must be studied, but requires the application of a non-lethal estimator as part of a multicriteria conservation approach.

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References

  • Abt KF, Bock WF (1998) Seasonal variations of diet composition in farmland field mice Apodemus spp. and bank voles Clethrionomys glareolus. Acta Theriol 43(4):379–389

  • Ainou H (2016) Etude des habitats de la lagune de Moulay Bousselham et actualisation de leur cartographie. Projet de fin d’étude de Master, Université Mohamed V, Rabat

  • Alimohammad Kalhori A, Jafari HR, Yavari AR et al (2012) Evaluation of anthropogenic impacts on soil and regolith materials based on BCR sequential extraction analysis. Int J Environ Res 6(1):185–194. https://doi.org/10.22059/IJER.2011.485

    Article  Google Scholar 

  • Ashraf MA, Maah MJ, Yusoff I (2012) Bioaccumulation of heavy metals in fish species collected from former Tin mining catchment. Int J Environ Res 6(1):209–218. https://doi.org/10.22059/IJER.2011.487

    Article  CAS  Google Scholar 

  • Aulagnier S, Cuzin F, Thévenot M (2017) Atlas des Mammifères sauvages du Maroc: Peuplement, répartition, écologie. SFEPM, broché, 340p / Réf.A24

  • Aunan K, Fang JH, Hu T, Seip HM, Vennemo H (2006) Climate change and air quality - measures with co-benefits in China. Environ Sci Technol 40:4822–4829. https://doi.org/10.1021/es062994k

    Article  PubMed  CAS  Google Scholar 

  • Bazaïri H, Bayed A, Glemarec M, Hily C (2003) Spatial organisation of macrozoobenthic communities in response to environmental factors in a coastal lagoon of the NW African coast (Merja Zerga, Morocco). Oceanol Acta 26:457–471

    Article  Google Scholar 

  • Beernaert J, Scheirs J, Van Den Brande G et al (2008) Do wood mice (Apodemus sylvaticus L.) use food selection as a means to reduce heavy metal intake? Environ Pollut 151(3):599–607. https://doi.org/10.1016/j.envpol.2007.04.001

  • Benabbou A, Benhoussa A, Fekhaoui M et al (2015) Application of multivariate statistical and geochemical methods for assessing of groundwater pollution near controlled Landfill in Oum Azza area, NW Morocco. Int Res J Earth Sci 3(3):9–14

    Google Scholar 

  • Benhoussa A, Dakki M, Qninba A, EL Agbani MA (1999) Habitats d’un site Ramsar côtier du Maroc, la Merja Zerga: approches typologique et cartographique. Humedales Mediterràneos 1:75–82

    Google Scholar 

  • Blagojevic J, Jovanovic V, Stamenkovic G et al (2012) Age differences in bioaccumulation of heavy metals in populations of the black-striped field mouse, Apodemus agrarius (Rodentia, Mammalia). Int J Environ Res 6:1045–1052

    CAS  Google Scholar 

  • Bouarakia O, Denys C, Benhoussa A et al (2019) Biogeographic history of Gerbillus campestris (Rodentia, Muridae) in Morocco as revealed by morphometric and genetic data. Bonn Zool Bull 68(1):97–124. https://doi.org/10.20363/BZB-2019.68.1.097

    Article  Google Scholar 

  • Bounif I, Taouil H, Elanza S et al (2017) Physicochemical study of Dayet Er-Romi Lake water, Khemisset Region. Am J Engin Res 6(3):101–106

    Google Scholar 

  • Boutahar L, Benhoussa A, Bazairi H et al (2019) Biomonitoring environmental status in semi-enclosed coastal ecosystems using Zostera noltei meadows. Ecol Indic 104:776–793. https://doi.org/10.1016/j.ecolind.2019.04.039

    Article  CAS  Google Scholar 

  • Cherkaoui I, Lamrani M (2007) Caractérisation ornithologique des habitats naturels de la lagune de Merja Zerga (Maroc). Ostrich 78(2):533–540

    Article  Google Scholar 

  • Chiffoleau JF, Truquet I (1990) Méthode de dosage de Cd, Pb, Zn, Ni, Co, Cr, Al, Mn, Fe dans les sédiments et les matières en suspension. Rapport interne Ifremer DRO-90–12-MR, 15 pp

  • Damek-Poprawa M, Sawicka-Kapusta K (2003) Damage of the liver, kidney and testis with reference to burden of heavy metals in yellow-necked mice from areas around steel works and zinc smelters in Poland. Toxicology 186:1–10. https://doi.org/10.1016/S0300-483X(02)00595-4

    Article  PubMed  CAS  Google Scholar 

  • Ding AJ, Fu CB, Yang XQ et al (2013) Intense atmospheric pollution modifies weather: a case of mixed biomass burning with fossil fuel combustion pollution in eastern China. Atmos Chem Phys 13:10545–10554

    Article  Google Scholar 

  • Dragun Z, Roje V, Mikac N et al (2009) Preliminary assessment of total dissolved trace metal concentrations in Sava River water. Environ Monit Assess 159:99–110. https://doi.org/10.1007/s10661-008-0615-9

    Article  PubMed  CAS  Google Scholar 

  • El Abidi A, Idrissi L, Taleb H et al (2000) The impact of lead pollution on the environment of Rabat-Sale (Morocco). Anal Chim 90(11–12):695–702

    Google Scholar 

  • Farag M, Hagag M, Saber A, Fayz A (2012) Contamination of cows milk by heavy metal in Egypt. Bull Environ Contam Toxicol 88:611–613. https://doi.org/10.1007/s00128-012-0550-x

    Article  CAS  Google Scholar 

  • Fritsch C, Giraudoux P, Douay F et al (2010) Spatial distribution of metals in smelter-impacted soils of woody habitats: influence of landscape and soil properties and risk for wildlife. Chemosphere 81(2):141–155. https://doi.org/10.1016/j.chemosphere.2010.06.075

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Sevillano MA, Garcia-Berrera T, Abril N et al (2014) Omics technologies and their applications to evaluate metal toxicity in mice M. spretus as a bioindicator. J Proteomics 104:4–23. https://doi.org/10.1016/j.jprot.2014.02.032

    Article  PubMed  CAS  Google Scholar 

  • Gašparík J, Binkowski L, Jahnátek A et al (2016) Levels of metals in kidney, liver, and muscle tissue and their influence on the fitness for the consumption of wild boar from Western Slovakia. Biol Trace Elem Res 177(2):258–266. https://doi.org/10.1007/s12011-016-0884-z

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gdula-Argasinska J, Dabrowski Z, Witkowska-Pelc E et al (2005) Heavy metal content and histopathology of the tissues of the Yellow-Necked mice (Apodemus flavicollis) and Bank Voles (Clethrionomys glareolus) as an exposure indicator of environmental pollution in Malopolska Province. Chemia Inzynieria Ekologiczna 12(11):1213–1220

    CAS  Google Scholar 

  • Ghaderi AA, Abduli MA, Karbassi AR et al (2012) Evaluating the effects of fertilizers on bioavailable metallic pollution of soils, case study of Sistan farms, Iran. Int J Environ Res 6(2):565–570

    CAS  Google Scholar 

  • Hokuto N, Shouta MMN, Balazs O et al (2017) Monitoring lead (Pb) pollution and identifying Pb pollution sources in Japan using stable Pb isotope analysis with kidneys of wild rats. Int J Environ Res Publ Health 14(1):56. https://doi.org/10.3390/ijerph14010056

    Article  CAS  Google Scholar 

  • Ieradi LA, Zima J, Allegra F et al (2003) Evaluation of genotoxic damage in wild rodents from a polluted area in the Czech Republic. Folia Zool 52(1):57–66

    Google Scholar 

  • Jarić I, Višnjić-Jeftić Z, Cvijanović G et al (2011) Determination of differential heavy metal and trace element accumulation in liver, gills, intestine and muscle of sterlet (Acipenser ruthenus) from the Danube River in Serbia by ICP-OES. Microchem J 98:77–81. https://doi.org/10.1016/j.microc.2010.11.008

    Article  CAS  Google Scholar 

  • Kargar M, Khorasani NA, Karami M et al (2012) An investigation on As, Cd, Mo and Cu contents of soils surrounding the Meyduk tailing dam. Int J Environ Res 6(1):173–184

    CAS  Google Scholar 

  • Kljakovic-Gaspic Z, Ujevic I, Baric A (2002) The Mediterranean blue mussel as an environmental indicator of metal pollution in the coastal area of Eastern Adriatic. Fres Environ Bull 11(9):620–625

    Google Scholar 

  • Lai HY, Hseu ZY, Chen TC, Chen BC et al (2010) Health risk-based assessment and management of heavy metals-contaminated soil sites in Taiwan. Int J Environ Res Publ Health 7(10):3595–3614. https://doi.org/10.3390/ijerph7103596

  • Lee CSL, Li XD, Zhang G, Li J et al (2007) Heavy metals and Pb isotopic composition of aerosols in urban and suburban areas of Hong Kong and Guangzhou, South China-Evidence of the long-range transport of air contaminants. Atmosph Environ 41(2):432–447. https://doi.org/10.1016/j.atmosenv.2006.07.035

    Article  CAS  Google Scholar 

  • Li X, Lijuan L, Yugang W et al (2012) Integrated assessment of heavy metal contamination in sediments from a coastal industrial basin, NE China. Plos One 7(6):e39690. https://doi.org/10.1371/journal.pone.0039690

    Article  PubMed  PubMed Central  Google Scholar 

  • Lopes PA, Viegas-Crespo AM, Nunes AC et al (2002) Influence of age, sex, and sexual activity on trace element levels and antioxidant enzyme activities in field mice (Apodemus sylvaticus and Mus spretus). Biol Trace Elem Res 85(227):239. https://doi.org/10.1385/BTER:85:3:227

    Article  Google Scholar 

  • Maanan M, Landesman C, Maanan M, Zourarah B, Fattal P, Sahabi M (2013) Evaluation of the anthropogenic influx of metal and metalloid contaminants into the Moulay Bousselham lagoon Morocco, using chemometric methods coupled to geographical information systems. Environ Sci Pollut Res 20:4729–4741. https://doi.org/10.1007/s11356-012-1399-6

  • Marques CC, Sanchez-Chardi A, Gabriel S et al (2007) How does the greater white-toothed shrew, Crocidura russula, responds to long-term heavy metal contamination? -A case study. Sci Tot Environ 376(1–3):128–133. https://doi.org/10.1016/j.scitotenv.2007.01.061

    Article  CAS  Google Scholar 

  • Metcheva R, Teodorova S, Topashka-Ancheva M (2002) A comparative analysis of the heavy metal loading of small mammals in different regions of Bulgaria I: monitoring points and bioaccumulation features. Ecotoxicol Environ Saf 54(2):176–187. https://doi.org/10.1016/S0147-6513(02)00051-9

    Article  Google Scholar 

  • Mhamdi Alaoui A, Choura M, Maanan M et al (2010) Metal fluxes to the sediments of the Moulay Bousselham lagoon, Morocco. Environ Earth Sci 61:275–286. https://doi.org/10.1007/s12665-009-0341-9

    Article  CAS  Google Scholar 

  • Mzoughi N, Chouba L (2012) Heavy metals and PAH assessment based on mussel caging in the north coast of Tunisia (Mediterranean Sea). Int J Environ Res 6(1):109–118

    CAS  Google Scholar 

  • Nasrabadi T, Nabi Bidhendi GR, Karbassi AR et al (2010) Partitioning of metals in sediments of the Haraz River (Southern Caspian Sea basin). Environ Earth Sci 59:1111–1117. https://doi.org/10.1007/s12665-009-0101-x

    Article  CAS  Google Scholar 

  • Ogundiran MB, Osibanjo O (2008) Heavy metal concentrations in soils and accumulation in plants growing in a deserted slag dumpsite in Nigeria. Afr J Biotechnol 7(17):3053–3060

    CAS  Google Scholar 

  • Okuku EO, Peter HK (2012) Choose of heavy metals pollution biomonitors: A critic of the method that uses sediments total metals concentration as the benchmark. Int J Environ Res 6(1):313–322

    CAS  Google Scholar 

  • ORMVAG (2007) Contrôle de l'impact des engrais et des pesticides sur l'environnement du bassin du Sebou SCET-Maroc. 138:30

  • ORMVAG (2010) Eude de la faisabilité de l’aménagement hydro-agricole de la zone côtière de la troisième tranche d’irrigation du Gharb. Mission 1: Diagnostic de la situation actuelle, Doc n°1367 -S1231 -10 cMarché n° 53/2009/DAM Edition définitive: décembre, 2010 Maroc

  • Pesce S (2006) Effets des pesticides sur l’activité et la diversité des communautés microbiennes d’un milieu lotique récepteur. Etudes in situ et expérimentales. Thèse de doctorat. Université Blaise Pascal, Clermont II, 271 pp

  • Pereira R, Pereira ML, Ribeiro R, Gonçalves F (2006) Tissues and hair residues and histopathology in wild rats (Rattus rattus L.) and Algerian mice (Mus spretus Lataste) from an abandoned mine area (Southeast Portugal). Environ Pollut 139(3):561–575. https://doi.org/10.1016/j.envpol.2005.04.038

  • Prevendar Crnić A, Šuran J, Cipriš Madunić H et al (2015) Cadmium concentrations in the tissues of young wild boar (Sus scrofa L.) from Moslavina and Slavonia in lowland Croatia. Vet Arch 85(3):323–334

  • Qninba A, Benhoussa A, El Agbani MA et al (2006) Etude phénologique et variabilité annuelle d’abondance des charadriidés (Aves, charadrii) dans un site Ramsar du Maroc: La Merja Zerga. Bull Inst Sci Sect Sci De La Vie 28:35–47

    Google Scholar 

  • Quina AS, Durao AF, Munoz F et al (2019) Population effects of heavy metal pollution in wild Algerian mice (Mus spretus). Ecotoxicol Environ Saf 171:414–424. https://doi.org/10.1016/j.ecoenv.2018.12.062

    Article  PubMed  CAS  Google Scholar 

  • Rautio A, Kunnasranta M, Valtonen A et al (2010) Sex, age, and tissue specific accumulation of eight metals, arsenic, and selenium in the European hedgehog (Erinaceus europaeus). Arch Environ Contam Toxicol 59:642–651. https://doi.org/10.1007/s00244-010-9503-8

    Article  PubMed  CAS  Google Scholar 

  • Salvarredy Aranguren MM (2008) Contamination en métaux lourds des eaux de surface et des sédiments du Val de Milluni (Andes Boliviennes) par des déchets miniers Approches géochimique, minéralogique et hydrochimique. Thèse de doctorat de l’Université de Toulouse, 379 pp

  • Sambo F, Haruna M, Idris S et al (2014) Assessment of heavy metals in water and fish from Ibrahim Adamu Lake, Jigawa, Nigeria. Trends Appl Sci Res 9:603–606. https://doi.org/10.3923/tasr.2014.603.606

    Article  Google Scholar 

  • Sanchez-Chardi A, Nadal J (2007) Bioaccumulation of metals and effects of landfill pollution in small mammals. Part I. The greater white-toothed shrew, Crocidura Russula. Chemosphere 68:703–711. https://doi.org/10.1016/j.chemosphere.2007.01.042

    Article  PubMed  CAS  Google Scholar 

  • Serbaji MM, Azri C, Medhioub K (2012) Anthropogenic contributions to heavy metal distributions in the surface and sub-surface sediments of the northern coast of Sfax, Tunisia. Int J Environ Res 6(3):613–626

    CAS  Google Scholar 

  • Stankovic S, Kalaba P, Stankovic R (2014) Biota as toxic metal indicators. Environ Chem Lett 12:63–84. https://doi.org/10.1007/s10311-013-0430-6

    Article  CAS  Google Scholar 

  • Sunjog K, Gačić Z, Kolarević S et al (2012) Heavy metal accumulation and the genotoxicity in barbel (Barbus barbus) as indicators of the Danube River pollution. Sci World J 2012:351074. https://doi.org/10.1100/2012/351074

    Article  CAS  Google Scholar 

  • Tchounwou PB, Yedjou CG, Patlolla AK et al (2012) Heavy metal toxicity and the environment. Experientia Suppl 101:133–164. https://doi.org/10.1007/978-3-7643-8340-4_6

    Article  Google Scholar 

  • Tête N, Afonso E, Crini N et al (2014a) Hair as a non-lethal tool for risk assessment: do the concentrations of cadmium and lead in the hair of wood mice (Apodemus sylvaticus) reflect internal concentrations? Ecotox Environ Saf 108:233–241. https://doi.org/10.1016/j.ecoenv.2014.07.010

  • Tête N, Durfort M, Rieffel D et al (2014b) Histopathology related to cadmium and lead bioaccumulation in chronically exposed wood mice, Apodemus sylvaticus, around a former smelter. Sci Tot Environ 481:167–177. https://doi.org/10.1016/j.scitotenv.2014.02.029

  • Tifarouine L, Benhoussa A, Bazairi H et al (2018) Assessing the use of small mammalians as bioindicators in northern Morocco (Oued Siad/Jbel Moussa) using heavy metal accumulation. J Mater Environ Sci 9(3):834–840. https://doi.org/10.26872/jmes.2018.9.3.92

  • Tifarouine L, Aziz F, El Abidi A, Hichami N, Benmokhtar S, Badaoui B, Rguibi Idrissi H, Fekhaoui M, Benhoussa A (2019) Influence of age on the bioaccumulation of heavy metals in Apodemus sylvaticus at Merja Zerga lagoon, Morocco. Saudi J Biol Sci 26(7):1682–1688. https://doi.org/10.1016/j.sjbs.2018.08.017

  • Touhami F, Bazairi H, Badaoui B, Benhoussa A (2018a) The impact of wader predation on benthic macrofauna in merja Zerga lagoon, Morocco: an exclosure experiment. Wader Study 124(3):225–237. https://doi.org/10.18194/ws.00093

    Article  Google Scholar 

  • Touhami F, Bazairi H, Badaoui B, Benhoussa A (2018b) Vertical distribution of benthic macrofauna in intertidal habitats frequented by Shorebirds at Merja Zerga Lagoon. Thalassas 34(3):255–265. https://doi.org/10.1007/s41208-017-0059-5

    Article  Google Scholar 

  • Udroiu I, Cristaldi M, Ieradi LA et al (2008) Biomonitoring of Danona national park using the Algerian mouse (Mus spretus) as a sentinel species. Fres Environ Bull 17(9b):1519–1525

    CAS  Google Scholar 

  • Wang Q, Sun Y, Xu W et al (2018) Vertically resolved characteristics of air pollution during two severe winter haze episodes in urban Beijing, China. Atmos Chem Phys 18(4):2495–2509. https://doi.org/10.5194/acp-18-2495-2018

    Article  CAS  Google Scholar 

  • Wariaghli F, Tilghman-Sibille A, El Abidi A et al (2013) Anguilla anguilla L.: Evaluation of the degree of heavy metal contamination in the Sebou estuary and in Moulay Bousselham lagoon reserve (Morocco). Int J Aquat Sci 4(2):69–82

  • Yorulmaz B, Yılmaz F, Genç TO (2015) Heavy metal concentrations in European Eel (Anguilla anguilla L., 1758) from Köyceğiz-Dalyan Lagoon System. Fres Environ Bull 24(5):1607–1613

  • Ziętara J, Wierzbowska IA, Gdula-Argasińska J et al (2018) Concentrations of cadmium and lead, but not zinc, are higher in red fox tissues than in rodents pollution gradient study in the Malopolska province (Poland). Environ Sci Pollut Res 26(5):4961–4974. https://doi.org/10.1007/s11356-018-3951-5

    Article  CAS  Google Scholar 

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Acknowledgements

The present study was supported by the Laboratory ‘Biodiversity, Ecology and Genome’ of the Faculty of Sciences of Rabat, we wish to express our gratitude to Pr. Bouabid Badaoui for their help and scientific suggestions.

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Authors and Affiliations

  1. BioBio Research CenterBioEcoGen Laboratory, Faculty of Sciences, Mohammed V University in Rabat, 4 Avenue Ibn Battouta, B.P. 1014 RP, 10106, Rabat, Morocco

    Loubna Tifarouine, Loubna Boutahar, Asmae Benabbou, Hamid Rguibi Idrissi, Salma Benmokhtar & Abdelaziz Benhoussa

  2. Laboratorio de Biología Marina, Departamento de Zoologia, Universidad de Sevilla, Avda. Reina Mercedes 6, 41012, Sevilla, Spain

    Loubna Boutahar

  3. SARChi Chair On Biodiversity Value and Change, University of Venda, Private Bag X5050, Thohoyandou, 0950, Limpopo, South Africa

    Oussama Bouarakia

  4. National Institute of Health, Department of Toxicology, Health Ministry, Rabat, Morocco

    Abdallah El Abidi

  5. Scientific Institute, Zoological Laboratory, Mohammed V University, Rabat, Morocco

    Mohamed Fekhaoui

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  1. Loubna Tifarouine
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Tifarouine, L., Boutahar, L., Benabbou, A. et al. Evaluation of bioconcentration of trace elements in the Western Mediterranean mouse Mus spretus at two Moroccan wetland sites. Biologia 77, 2843–2855 (2022). https://doi.org/10.1007/s11756-022-01110-x

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