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Trace element assessment in Neoechinorhynchus agilis (Rudolphi, 1918) (Acanthocephala: Neoechinorhynchidae) and its fish hosts, Mugil cephalus (Linnaeus, 1758) and Chelon ramada (Risso, 1827) from Ichkeul Lagoon, Tunisia

Published online by Cambridge University Press:  02 November 2021

H. Jmii Chine Open the ORCID record for H. Jmii Chine [Opens in a new window] ,
M. Nachev ,
B. Sures  and
L. Gargouri
H. Jmii Chine*
Affiliation:
Faculty of Sciences of Tunis, Laboratory of Diversity, Management and Conservation of Biological Systems, University of Tunis El Manar, LR18ES06, Tunis, Tunisia
M. Nachev
Affiliation:
Department of Aquatic Ecology and Centre for Water and Environmental Research, University of Duisburg-Essen, Universitätsstr. 5, 45141, Essen, Germany
B. Sures
Affiliation:
Department of Aquatic Ecology and Centre for Water and Environmental Research, University of Duisburg-Essen, Universitätsstr. 5, 45141, Essen, Germany
L. Gargouri
Affiliation:
Faculty of Sciences of Tunis, Laboratory of Diversity, Management and Conservation of Biological Systems, University of Tunis El Manar, LR18ES06, Tunis, Tunisia
*
Author for correspondence: H. Jmii Chine, E-mail: halimajmii@hotmail.com
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Abstract

Acanthocephalans belonging to the species Neoechinorhynchus agilis were collected from two mullets, Mugil cephalus and Chelon ramada from Ichkeul Lagoon in northern Tunisia. Collected parasites, as well as tissues of their hosts (muscle, liver and intestine), were analysed for trace elements (silver, arsenic, cadmium, cobalt, copper, iron, manganese, nickel (Ni), lead (Pb), selenium, vanadium (V), zinc) using inductively coupled plasma mass spectrometry. Our results showed different accumulation patterns of trace elements in fish tissues and parasites. Among the host tissues, liver accumulated the highest metal amounts. Acanthocephalans showed Ni, Pb and V in significantly higher concentrations compared to their host's tissues. Further, the calculated bioconcentration factors demonstrated a 390-fold higher Pb accumulation in the parasite compared to fish muscle. This study is the first field survey in Tunisia dealing with elements’ uptake in parasites and their hosts. Our results corroborate the usefulness of the acanthocephalans for biomonitoring of metal pollution in aquatic ecosystems and promote more research in order to understand host–parasite systems in brackish waters of the Mediterranean area.

Keywords

Neoechinorhynchus agilismetal uptakemulletspollutionbrackish water
Type
Research Paper
Information
Journal of Helminthology , Volume 95 , 2021 , e61
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Al-Hasawi, ZM (2019) Environmental parasitology: intestinal helminth parasites of the siganid fish Siganus rivulatus as bioindicators for trace metal pollution in the Red Sea. Parasite 26, 12.CrossRefGoogle ScholarPubMed
Annabi, A, El Mouadeb, R and Herrel, A (2017) Distinctive accumulation patterns of heavy metals in Sardinella aurita (Clupeidae) and Mugil cephalus (Mugilidae) tissues. Environmental Science and Pollution Research 25, 2623–2629.CrossRefGoogle ScholarPubMed
Ben M'barek, N (2001) Etude de l’écosystème du lac Ichkeul et de son bassin versant. 19 Caractéristiques physiques et géochimiques des eaux et des sédiments. Doctoral thesis, Université de Tunis II, Tunisia, 235 pp.Google Scholar
Ben Salem, F, Ben Said, O, Mahmoudi, E, Duran, R and Monperrus, M (2017) Distribution of organic contamination of sediments from Ichkeul Lake and Bizerte Lagoon, Tunisia. Marine Pollution Bulletin 123, 329–338.CrossRefGoogle ScholarPubMed
Birk, S, Chapman, D, Carvalho, L, et al. (2020) Impacts of multiple stressors on freshwater biota across spatial scales and ecosystems. Nature Ecology & Evolution 4, 1060–1068.CrossRefGoogle ScholarPubMed
Bone, Q and Moore, R (2008) Biology of fishes. 3rd edn. Abingdon, Oxon, Taylor & Francis.CrossRefGoogle Scholar
Chouba, L, Kraiem, M, Njimi, W, Tissaoui, CH, Thompson, JR and Flower, RJ (2007) Seasonal variation of heavy metals (Cd, Pb and Hg) in sediments and in mullet, Mugil cephalus (Mugilidae), from the Ghar el Melh Lagoon (Tunisia). Transitional Waters Bulletin 4, 45–52.Google Scholar
Du Laing, G, De Vos, R, Vandecasteele, B, Lesage, E, Tack, FMG and Verloo, MG (2008) Effect of salinity on heavy metal mobility and availability in intertidal sediments of the Scheldt estuary. Estuarine, Coastal and Shelf Science 77, 589–602.CrossRefGoogle Scholar
FAO (1983) Compilation of legal limits for hazardous substances in fish and fishery products. FAO Fishery Circular, Food and Agriculture Organization 464, 5–100.Google Scholar
Fernandes, C, Fontainhas-Fernandes, A, Peixoto, F and Salgado, MA (2007) Bioaccumulation of heavy metals in Liza saliens from the Esomriz Paramos Coastal Lagoon, Portugal. Ecotoxicology and Environmental Safety 66, 426–431.CrossRefGoogle ScholarPubMed
Genç, TO and Yilmaz, F (2017) Metal accumulations in water, sediment, crab (Callinectes sapidus) and two fish species (Mugil cephalus and Anguilla Anguilla) from the Köyceğiz lagoon system-Turkey: an index analysis approach. Bulletin of Environmental Contamination and Toxicology 99(1), 173–181.CrossRefGoogle ScholarPubMed
Hamza-Chaffai, A (2014) Usefulness of bioindicators and biomarkers in pollution biomonitoring. International Journal of Biotechnology for Wellness Industries 3, 19–26.CrossRefGoogle Scholar
Jithendran, KP and Kannappan, S (2010) A short note on heavy infection of acanthocephalan worm (Neoechinorhynchusagilis) in grey mullet, Mugil cephalus. Journal of Parasitological Diseases 34, 99–101.CrossRefGoogle Scholar
Kefi, F, Mleiki, A, Maâtoug Béjaoui, J and Trigui El Menif, N (2016) Seasonal variations of trace metal concentrations in the soft tissue of Lithophaga Lithophaga collected from the Bizerte Bay (Northern Tunisia, Mediterranean Sea). Journal of Aquaculture Research & Development 7, 6.Google Scholar
Merian, E, Anke, M, Ihnat, M and Stoeppler, M (2004) Elements and their compounds in the environment. 2nd edn. Weinheim, Wiley-VCH.CrossRefGoogle Scholar
Nachev, M and Sures, B (2015) Environmental parasitology: parasites as accumulation bioindicators in the marine environment. Journal of Sea Research 113, 45–50.CrossRefGoogle Scholar
Nachev, M, Zimmermann, S, Rigaud, T and Sures, B (2010) Is metal accumulation in Pomphorhynchus laevis dependent on parasite sex or infrapopulation size? Parasitology 137(12), 39–48.CrossRefGoogle ScholarPubMed
Olsson, PE, Kling, P and Hogstrand, C (1998) Mechanisms of heavy metal accumulation and toxicity in fish. pp. 321–350 in Langston, WJ and Bebianno, M (Eds) Metal metabolism in aquatic environments. London, Chapman and Hall.CrossRefGoogle Scholar
Ouchir, N, Ben Aissa, L, Boughdiri, M and Aydi, A (2016) Assessment of heavy metal contamination status in sediments and identification of pollution source in Ichkeul Lake and rivers ecosystem, Northern Tunisia. Arab Journal of Geoscience 9, 539.CrossRefGoogle Scholar
Reynolds, EJ, Smith, DS, Chowdhury, MJ and Hoanga, TC (2018) Chronic effects of lead exposure on topsmelt fish (Atherinops affinis): influence of salinity, organism age, and relative sensitivity to other marine species. Environmental Toxicological Chemistry 37, 2705–2713.CrossRefGoogle ScholarPubMed
Rosenberg, DM and Resh, VH (1993) Introduction to freshwater biomonitoring and benthic macroinvertebrates. pp. 1–9 in Rosenberg, DM and Resh, VH (Eds) Freshwater biomonitoring and benthic macroinvertebrates. New York, Chapman/Hall.Google Scholar
Squadrone, S, Prearo, M, Brizio, P, Gavinelli, S, Pellegrino, M, Scanzio, T, Guarise, S, Benedetto, A and Abete, MC (2013) Heavy metals distribution in muscle, liver, kidney and gill of European catfish (Silurus glanis) from Italian rivers. Chemosphere 90, 358.CrossRefGoogle ScholarPubMed
Stagg, RM and Shuttleworth, TJ (1982) The accumulation of copper in Platichthys flesus L. and its effects on plasma electrolyte concentrations. Journal of Fish Biology 20, 491–500.CrossRefGoogle Scholar
Storelli, MM, Barone, G, Storelli, A and Marcotrigiano, GO (2006) Trace metals in tissues of mugilids (Mugil auratus, Mugil capito, and Mugil labrosus) from the Mediterranean Sea. Bulletin of Environmental Contamination and Toxicology 77, 43–50.CrossRefGoogle ScholarPubMed
Sures, B (2003) Accumulation of heavy metals by intestinal helminths in fish: an overview and perspective. Parasitology 126, 53–60.CrossRefGoogle ScholarPubMed
Sures, B (2004) Environmental parasitology: relevancy of parasites in monitoring environmental pollution. Parasitology 20, 170–177.Google ScholarPubMed
Sures, B (2005) Effects of pollution on parasites, and use of parasites in pollution monitoring. pp. 421–425 in Rohde, K (Ed.) Marine parasitology. Collingwood, CSIRO Publishing.Google Scholar
Sures, B and Reimann, N (2003) Analysis of trace metals in the Antarctic host parasite system Motothenia coriiceps and Aspersentis megarhynchus (Acanthocephala) caught at King George Island, South Shetland Islands. Polar Biology 26, 680–686.CrossRefGoogle Scholar
Sures, B and Siddall, R (1999) Pomphorhynchus laevis: the intestinal acanthocephalan as a lead sink for its fish host, chub (Leuciscus cephalus). Experimental Parasitology 93, 66–72.CrossRefGoogle Scholar
Sures, B and Siddall, R (2001) Comparison between lead accumulation of Pomphorhynchus laevis (Palaeacanthocephala) in the intestine of chub (Leuciscus cephalus) and in the body cavity of goldfish (Carassius auratus auratus). International Journal for Parasitology 31, 669–673.CrossRefGoogle Scholar
Sures, B and Taraschewski, H (1995) Cadmium concentrations of two adult acanthocephalans (Pomphorhinchus leavis, Acanthocephalus lucii) compared to their fish host and cadmium and lead levels in the larvae of A. Lucii compared to their crustacean host. Parasitology Research 81, 494–497.CrossRefGoogle Scholar
Sures, B, Taraschewski, H and Jackwerth, E (1994a) Lead accumulation in Pomphorhynchus laevis and its host. Journal of Parasitology 80, 355–357.CrossRefGoogle Scholar
Sures, B, Taraschewski, H and Jackwerth, E (1994b) Lead content of Paratenuisentis ambiguus (Acanthocephala), Anguillicola crassus (Nematodes) and their host Anguilla anguilla. Diseases of Aquatic Organisms 19, 105–107.CrossRefGoogle Scholar
Sures, B, Taraschewski, H and Rydlo, M (1997) Intestinal fish parasites as heavy metal bioindicators: a comparison between Acanthocephalus lucii (Palaeacanthocephala) and the zebra mussel, Dreissena polymorpha. Bulletin of Environmental Contamination and Toxicology 59, 14–21.CrossRefGoogle ScholarPubMed
Sures, B, Siddall, R and Taraschewski, H (1999) Parasites as accumulation indicators of heavy metal pollution. Parasitology Today 15, 16–21.CrossRefGoogle ScholarPubMed
Sures, B, Zimmermann, S, Sonntag, C, Stüben, D and Taraschewski, H (2003) The acanthocephalan Paratenuisentis ambiguus as a sensitive indicator of the precious metals Pt and Rh emitted from automobile catalytic converters. Environmental Pollution 122, 401–405.CrossRefGoogle Scholar
Sures, B, Nachev, M, Pahl, M, Grabner, D and Selbach, C (2017) Parasites as drivers of key processes in aquatic ecosystems: facts and future directions. Experimental Parasitology 180, 141–147.CrossRefGoogle ScholarPubMed
Tkach, IV, Sarabeev, VL and Shvetsova, LS (2014) Taxonomic status of Neoechinorhynchus agilis (Acanthocephala, Neoechinorhynchidae), with a description of two new species of the genus from the Atlantic and Pacific mullets (Teleostei, Mugilidae). Vestnik Zoologii 48, 291–306.CrossRefGoogle Scholar
Waltham, NJ, Teasdale, PR and Connolly, RM (2013) Use of flathead mullet (Mugil cephalus) in coastal biomonitor studies: review and recommendations for future studies. Marine Pollution Bulletin 69, 195–205.CrossRefGoogle ScholarPubMed
Yazidi, A, Saidi, S, Ben Mbarek, N and Darragi, F (2017) Contribution of GIS to evaluate surface water pollution by heavy metals case of Ichkeul lake (Northern Tunisia). Journal of African Earth Sciences 134, 166–173.CrossRefGoogle Scholar
Yilmaz, AB (2009) The comparison of heavy metal concentrations (Cd, Cu, Mn, Pb and Zn) in tissues of three economically important fish (Anguilla Anguilla, Mugil cephalus and Oreochromis niloticus) inhabiting Köycegiz Lake-Mugla (Turkey). Turkish Journal of Science & Technology 4(1), 7–15.Google Scholar
Zimmermann, S, Sures, B and Taraschewski, H (1999) Experimental studies on lead accumulation in the eel specific endoparasites Anguillicola crassus (Nematoda) and Paratenuisentis ambiguus (Acanthocephala) as compared with their host, Anguilla Anguilla. Archives of Environmental Contamination and Toxicology 37, 190–195.CrossRefGoogle ScholarPubMed
Zimmermann, S, Messerschmidt, J, Von Bohlen, A and Sures, B (2005) Uptake and bioaccumulation of platinum group metals (Pd, Pt, Rh) from automobile catalytic converter materials by the zebra mussel (Dreissena polymorpha). Environmental Research 98, 203–209.CrossRefGoogle Scholar