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Acta Parasitologica

, Volume 64, Issue 3, pp 464–470 | Cite as

Mercury, Lead and Cadmium Concentrations in Talpa occidentalis and in Their Digeneans of the Genus Ityogonimus

  • Roser Adalid
  • Jordi Torres
  • Marcos Miñarro
  • Jordi Miquel
  • Màrius Vicent Fuentes
  • Catarina EiraEmail author
Original Paper
  • 29 Downloads

Abstract

Introduction

Many parasites living in aquatic ecosystems are useful indicators of environmental health. On the other hand, information is scarcer with respect to the use of helminth parasites of vertebrates living in terrestrial ecosystems as monitoring tools for toxic element environmental pollution. The present study evaluates the suitability of the model Talpa occidentalis/Ityogonimus spp. as a bioindicator system for mercury (Hg), lead (Pb) and cadmium (Cd) contamination in agricultural soils from Asturias (Spain).

Methods

Kidney and liver samples collected from T. occidentalis specimens (n = 36) and Ityogonimus spp. samples collected from 14 infected hosts were analyzed by ICP-MS.

Results

The highest mean levels of Hg and Pb were found in Ityogonimus individuals (20.9 and 12.4 µg g−1 wet weight, respectively). Considering renal and hepatic concentrations in T. occidentalis, bioaccumulation factors of Ityogonimus for Hg were 83.7 and 58.6, respectively, whereas concerning Pb bioaccumulation factors were 38.2 and 82.9, respectively. No bioaccumulation was detected in Ityogonimus in the case of Cd.

Conclusions

More studies involving digenean parasites of small mammals are needed, especially when biomonitoring environmental toxic element pollution in terrestrial ecosystems. The present results support the above-mentioned model as a suitable biomonitoring system to evaluate environmental Hg and Pb contamination in terrestrial non-urban Iberian habitats. Similar models involving other species (Talpa spp./Ityogonimus spp.) might be used in a much wider geographical range.

Keywords

Pollution Parasites Talpidae Biomonitoring model Terrestrial ecosystems 

Notes

Acknowledgements

Authors wish to thank personnel of the “Serveis Científico-Tècnics” of the University of Barcelona for their contribution to the analytical process.

Funding

CE was supported by CESAM UID/AMB/50017/2013 (FCT) co-funded by FCT/MEC and FEDER, within PT2020 and Compete 2020. JT and JM are members of the 2017-SGR-1008 research group.

Compliance with Ethical Standards

Ethical Approval

The methods used in this study comply with the current national laws.

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

References

  1. 1.
    Hamers T, van den Berg JHJ, van Gestel CAM, van Schooten FJ, Murk AJ (2006) Risk assessment of metals and organic pollutants for herbivorous and carnivorous small mammal food chains in a polluted floodplain (Biesbosch, The Netherlands). Environ Pollut 144:581–595.  https://doi.org/10.1016/j.envpol.2006.01.020 CrossRefPubMedGoogle Scholar
  2. 2.
    Sánchez-Chardi A, Peñarroja-Matutano C, Oliveira Ribeiro CA, Nadal J (2007) Bioaccumulation of metals and effects of a landfill in small mammals. Part II. The wood mouse, Apodemus sylvaticus. Chemosphere 70:101–109.  https://doi.org/10.1016/j.chemosphere.2007.06.047 CrossRefPubMedGoogle Scholar
  3. 3.
    Al Sayegh Petkovšek S, Kopušar N, Kryštufek B (2014) Small mammals as biomonitors of metal pollution: a case study in Slovenia. Environ Monit Assess 186:4261–4274.  https://doi.org/10.1007/s10661-014-3696-7 CrossRefPubMedGoogle Scholar
  4. 4.
    Sures B, Nachev M, Selbach C, Marcogliese DJ (2017) Parasites responses to pollution: what we know and where we go in ‘Environmental Parasitology’. Parasite Vector 10:65.  https://doi.org/10.1186/s13071-017-2001-3 CrossRefGoogle Scholar
  5. 5.
    Sures B, Scheible T, Bashtar AR, Taraschewski H (2003) Lead concentrations in Hymenolepis diminuta adults and Taenia taeniaeformis larvae compared to their rat host (Rattus norvegicus) sampled from the city of Cairo, Egypt. Parasitology 127:483–487.  https://doi.org/10.1017/S00311822003003901 CrossRefPubMedGoogle Scholar
  6. 6.
    Torres J, Peig J, Eira C, Borrás M (2006) Cadmium and lead concentrations in Skrjabinotaenia lobata (Cestoda: Catenotaeniidae) and in its host, Apodemus sylvaticus (Rodentia: Muridae) in the urban dumping site of Garraf (Spain). Environ Pollut 143:4–8.  https://doi.org/10.1016/j.envpol.2005.11.012 CrossRefPubMedGoogle Scholar
  7. 7.
    Torres J, Eira C, Miquel J, Foronda P, Feliu C (2011) Cadmium and lead concentrations in Moniliformis moniliformis (Acanthocephala) and Rodentolepis microstoma (Cestoda), and in their definitive hosts, Rattus rattus and Mus domesticus in El Hierro (Canary Archipelago, Spain). Acta Parasitol 56:320–324.  https://doi.org/10.2478/s11686-011-0064-4 CrossRefGoogle Scholar
  8. 8.
    Al-Quraishy S, Gewik MM, Abdel-Baki AAS (2014) The intestinal cestode Hymenolepis diminuta as a lead sink for its rat host in the industrial areas of Riyadh, Saudi Arabia. Saudi J Biol Sci 21:387–390.  https://doi.org/10.1016/j.sjbs.2013.09.010 CrossRefPubMedGoogle Scholar
  9. 9.
    Eira C, Torres J, Vingada J, Miquel J (2005) Concentration of some toxic elements in Oryctolagus cuniculus and in its intestinal cestode Mosgovoyia ctenoides in Dunas de Mira (Portugal). Sci Total Environ 346:81–86.  https://doi.org/10.1016/j.scitotenv.2004.11.014 CrossRefPubMedGoogle Scholar
  10. 10.
    Teimoori S, Sabour Yaraghi A, Makki MS, Shahbazi F, Nazmara S, Rokni MB, Mesdaghinia A, Moghaddam AS, Hosseini M, Rakhshanpour A, Mowlavi G (2014) Heavy metal bioabsorption capacity of intestinal helminths in urban rats. Iran J Public Health 4:310–315Google Scholar
  11. 11.
    Sures B, Jürges G, Taraschewski H (1998) Relative concentrations of heavy metals in the parasites Ascaris suum (Nematoda) and Fasciola hepatica (Digenea) and their respective porcine and bovine definitive hosts. Int J Parasitol 28:1173–1178.  https://doi.org/10.1016/S0020-7519(98)00105-2 CrossRefPubMedGoogle Scholar
  12. 12.
    Lotfy WM, Ezz AM, Hassan AAM (2013) Bioaccumulation of some heavy metals in the liver flukes Fasciola hepatica and F. gigantica. Iran J Parasitol 8:552–558PubMedPubMedCentralGoogle Scholar
  13. 13.
    Hutterer R (2005) Order Soricomorpha. In: Wilson DE, Reeder DM (eds) Mammal species of the world: a taxonomic and geographic reference, 3rd edn. Johns Hopkins University Press, Baltimore, pp 220–311Google Scholar
  14. 14.
    Nicolas V, Martínez-Vargas J, Hugot JP (2017) Molecular data and ecological niche modelling reveal the evolutionary history of the common and Iberian moles (Talpidae) in Europe. Zool Scr 46:12–26.  https://doi.org/10.1111/zsc.12189 CrossRefGoogle Scholar
  15. 15.
    Cassola F (2016) Talpa occidentalis. The IUCN Red List of Threatened Species 2016. http://dx.doi.org/10.2305/IUCN.UK.2016-2.RLTS.T41483A2953593.en. Accessed 14 July 2018
  16. 16.
    Ribas A, Casanova JC (2006) Helminth fauna of Talpa spp. in the Palaearctic Realm. J Helminthol 80:1–6.  https://doi.org/10.1079/JOH2005358 CrossRefPubMedGoogle Scholar
  17. 17.
    Pojmańska T (1930) Family Brachylaimidae Joyeux & Foley, 1930. In: Gibson DI, Jones A, Bray RA (eds) Keys to the trematoda, vol 1. CAB International, London, pp 37–43Google Scholar
  18. 18.
    Adalid R, Torres J, Miñarro M, Fuentes MV, Miquel J (2018) First finding of Ityogonimus lorum and I. ocreatus co-infection in the Iberian mole, Talpa occidentalis. Acta Parasitol 63:835–838.  https://doi.org/10.1515/ap-2018-00 CrossRefPubMedGoogle Scholar
  19. 19.
    Sures B, Siddall R, Taraschewski H (1999) Parasites as accumulation indicators of heavy metal pollution. Parasitol Today 15:16–22.  https://doi.org/10.1016/S0169-4758(98)01358-1 CrossRefPubMedGoogle Scholar
  20. 20.
    Tovar-Sánchez E, Cervantes LT, Martínez C, Rojas E, Valverde M, Ortiz-Hernández ML, Mussali-Galante P (2012) Comparison of two wild rodent species as sentinels of environmental contamination by mine tailings. Environ Sci Pollut Res 19:1677–1686.  https://doi.org/10.1007/s11356-011-0680-4 CrossRefGoogle Scholar
  21. 21.
    Sures B, Reimann N (2003) Analysis of trace metals in the Antarctic host-parasite system Notothenia coriiceps and Aspersentis megarhynchus (Acanthocephala) caught at King George Island, South Shetland Islands. Polar Biol 26:680–686.  https://doi.org/10.1007/s00300-003-0538-4 CrossRefGoogle Scholar
  22. 22.
    Rodrigues dos Santos I, Vieira Silva-Filho E, Schaefer C, Sella SM, Silva CA, Gomes V, Passos MJ, Van Ngan P (2006) Baseline mercury and zinc concentrations in terrestrial and coastal organisms of Admiralty Bay, Antartica. Environ Pollut 140:304–311.  https://doi.org/10.1016/j.envpol.2005.07.007 CrossRefGoogle Scholar
  23. 23.
    Niethammer J (1907) Talpa occidentalis Cabrera, 1907. In: Niethammer J, Krapp F (eds) Handbuch der Säugetiere Europas. Band 3/1. Insektenfresser—Insectivora. Herrentiere-primates. Aula Verlag, Wiesbaden, pp 157–161Google Scholar
  24. 24.
    Nahmani J, Hodson ME, Black S (2007) A review of studies performed to assess metal uptake by earthworms. Environ Pollut 145:402–424.  https://doi.org/10.1016/j.envpol.2006.04.009 CrossRefPubMedGoogle Scholar
  25. 25.
    Jelaska ŠL, Jurasović J, Brown DS, Vaughan IP, Symondson WOC (2014) Molecular field analysis of trophic relationships in soil-dwelling invertebrates to identify mercury, lead and cadmium transmission through forest ecosystems. Mol Ecol 23:3755–3766.  https://doi.org/10.1111/mec.12566 CrossRefGoogle Scholar
  26. 26.
    Ma WC, Talmage SS (2001) Insectivora. In: Shore RF, Rattner BA (eds) Ecotoxicology of wild mammals. Wiley, Chichester, pp 123–158Google Scholar
  27. 27.
    Álvarez CR, Moreno MJ, Bernardo FG, Martín-Doimeadios RR, Nevado JB (2014) Mercury methylation, uptake and bioaccumulation by the earthworm Lumbricus terrestris (Oligochaeta). Appl Soil Ecol 84:45–53.  https://doi.org/10.1016/j.apsoil.2014.06.008 CrossRefGoogle Scholar
  28. 28.
    Le Roux S, Baker P, Crouch A (2016) Bioaccumulation of total mercury in the earthworm Eisenia andrei. Springerplus 5:681.  https://doi.org/10.1186/s40064-016-2282-6 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Wren CD (1986) A review of metal accumulation and toxicity in wild mammals: I. Mercury. Environ Res 40:210–244.  https://doi.org/10.1016/S0013-9351(86)80098-6 CrossRefPubMedGoogle Scholar
  30. 30.
    Bull KR, Roberts RD, Inskip MJ, Goodman GT (1977) Mercury concentrations in soil, grass, earthworms and small mammals near an industrial emission source. Environ Pollut 12:135–140.  https://doi.org/10.1016/0013-9327(77)90016-7 CrossRefGoogle Scholar
  31. 31.
    Lewis LA, Poppenga RJ, Davidson WR, Fischer JR, Morgan KA (2001) Lead toxicosis and trace element levels in wild birds and mammals at a firearms training facility. Arch Environ Contam Toxicol 41:208–214.  https://doi.org/10.1007/s002440010239 CrossRefPubMedGoogle Scholar
  32. 32.
    Li L, Xu Z, Wu J, Tian G (2010) Bioaccumulation of heavy metals in the earthworm Eisenia fetida in relation to bioavailable metal concentrations in pig manure. Bioresour Technol 101:3430–3436.  https://doi.org/10.1016/j.biortech.2009.12.085 CrossRefPubMedGoogle Scholar
  33. 33.
    Sager M (1997) Possible trace metal load from fertilizers. Bodenkultur 48:217–223Google Scholar
  34. 34.
    Pan J, Plant JA, Voulvoulis N, Oates CJ, Ihlenfeld C (2010) Cadmium levels in Europe: implications for human health. Environ Geochem Health 32:1–12.  https://doi.org/10.1007/s10653-009-9273-2 CrossRefPubMedGoogle Scholar
  35. 35.
    Riedel T, Hennessy P, Iden SC, Koschinsky A (2015) Leaching of soil-derived major and trace elements in an arable topsoil after the addition of biochar. Eur J Soil Sci 66:823–834.  https://doi.org/10.1111/ejss.12256 CrossRefGoogle Scholar
  36. 36.
    Bigalke M, Ulrich A, Rehmus A, Keller A (2017) Accumulation of cadmium and uranium in arable soils in Switzerland. Environ Pollut 221:85–93.  https://doi.org/10.1016/j.envpol.2016.11.035 CrossRefPubMedGoogle Scholar

Copyright information

© Witold Stefański Institute of Parasitology, Polish Academy of Sciences 2019

Authors and Affiliations

  1. 1.Secció de Parasitologia, Departament de Biologia, Sanitat i Medi ambient, Facultat de Farmàcia i Ciències de l’AlimentacióUniversitat de BarcelonaBarcelonaSpain
  2. 2.Institut de Recerca de la Biodiversitat (IRBio)Universitat de BarcelonaBarcelonaSpain
  3. 3.Servicio Regional de Investigación y Desarrollo Agroalimentario de AsturiasVillaviciosaSpain
  4. 4.Unitat de Parasitologia, Departament de Farmàcia i Tecnologia Farmacèutica i ParasitologiaUniversitat de ValènciaValènciaSpain
  5. 5.CESAM and Department of BiologyUniversity of AveiroAveiroPortugal

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