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Heavy Metal Accumulation in the Intestinal Tapeworm Proteocephalus macrophallus Infecting the Butterfly Peacock Bass (Cichla ocellaris), from Southeastern Brazil

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Abstract

Here we evaluate the potential of heavy metal accumulation of Proteocephalus macrophallus parasitizing the Butterfly Peacock Bass (Cichla ocellaris). A total of 19 fish specimens were collected. From the hosts, samples of intestine, liver, muscle, and parasites were taken. Heavy metal concentrations (Al, As, Ba, Cd, Cr, Fe, Hg, Mg, Mn, Ni, Pb, Ti, and Zn) were obtained using Atomic Absorption Spectrometry. All analyzed elements was found in higher concentrations in the parasites comparing to its host tissues. The bioconcentration factors were higher in the intestine, varying between 5.91 (Ti) to 8.00 (Ba), followed by the muscle, 1.88 (Mg) to 6.39 (Zn), and liver, 1.67 (Al) to 2.02 (Ba). These results show that at the infection site heavy metal concentrations are reduced, since the elements are absorbed directly from the intestinal wall by the parasites. In general, P. macrophallus presents a reasonable capacity of metal accumulation comparing to its hosts.

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References

  • Baruš V, Šimková A, Prokeš M, Peňáz M, Vetešník L (2012) Heavy metals in two host–parasite systems: tapeworm vs. fish. Acta Vet Brno 81:313–317

    Article  Google Scholar 

  • Benito M, Mosteo R, Rubio E, Laplante D, Ormad MP (2017) GOÑI P. Bioaccumulation of inorganic elements in Dreissena polymorpha from the Ebro River, Spain: could zebra mussels be used as bioindicator of the impact of human activities? River Res Appl 33(5):718–728

    Article  Google Scholar 

  • Brázová T, Hanzelová V, Miklisová D, Šalamún P, Vidal-Martínez VM (2015) Host–parasite relationships as determinants of heavy metal concentrations in perch (Perca fluviatilis) and its intestinal parasite infection. Ecotoxicol Environ Saf 122:551–556

    Article  CAS  Google Scholar 

  • Burger J (2006) Bioindicators: a review of their use in the environmental literature 1970–2005. Envir Bioindic 1:136–144

    Article  Google Scholar 

  • Cunha SC, Pena A, Fernandes JO (2017) Mussels as bioindicators of diclofenac contamination in coastal environments. Environ Pollut 225:354–360

    Article  CAS  Google Scholar 

  • Diaz EC (2007) Environment Issues in the Latin America Region. In: International expert workshop on indigenous peoples and protections of the environment, Russian Federation

  • Dural M, Göksu MZL, Özak AA (2007) Investigation of heavy metal levels in economically important fish species captured from the Tuzla lagoon. Food Chem 102:415–421

    Article  CAS  Google Scholar 

  • Eira C, Torres J, Miquel J, Vaqueiro J, Soares AMVM, Vingada J (2009) Trace element concentrations in Proteocephalus macrocephalus (Cestoda) and Anguillicola crassus (Nematoda) in comparison to their fish host, Anguilla anguilla in Ria de Aveiro, Portugal. Sci Total Environ 407:991–998

    Article  CAS  Google Scholar 

  • Jia Y, Wang L, Qu Z, Wang C, Yang Z (2017) Effects on heavy metal accumulation in freshwater fishes: species, tissues, and sizes. Environ Sci Pollut Res 24:9379–9386

    Article  CAS  Google Scholar 

  • Leite LAR, Pedro NHO, Azevedo RK, Kinoshita A, Gennari RF, Watanabe S, Abdallah VD (2017) Contracaecum sp. parasitizing Acestrorhynchus lacustris as a bioindicator for metal pollution in the Batalha River, southeast Brazil. Sci Total Environ 575:836–840

    Article  CAS  Google Scholar 

  • Moraes PM, Santos FA, Cavecci B, Padilha CCF, Vieira JCS, Roldan PS, Padilha PM (2013) GFAAS determination of mercury in muscle samples of fish from Amazon, Brazil. Food Chem 141:2614–2617

    Article  CAS  Google Scholar 

  • Nachev M, Schertzinger G, Sures B (2013) Comparison of the metal accumulation capacity between the acanthocephalan Pomphorhynchus laevis and larval nematodes of the genus Eustrongylides sp. infecting barbel (Barbus barbus). Parasit Vectors 6:1–8

    Article  CAS  Google Scholar 

  • Nhi TTY, Shazili NAM, Shararom-Harrison FS (2013) Use of cestodes as indicator of heavy metal pollution. Exp Parasitol 133:75–79

    Article  CAS  Google Scholar 

  • Olsson P-E, Kling P, Hogstrand C (1998) Mechanisms of heavy metal accumulation and toxicity in fish. In: Langston WJ, Bebiano MJ (eds) Metal metabolism in aquatic environments, 1st edn. Springer, New York, pp 321–350

    Chapter  Google Scholar 

  • Reid AJ, Carlson AK, Creed IF et al (2019) Emerging threats and persistent conservation challenges for freshwater biodiversity. Biol Rev 94:849–873

    Article  Google Scholar 

  • Santos RS, Roumbedakis K, Marengoni NG, Takahashi HK, Pimenta FDA, Melo CMR, Martins ML (2011) Proteocephalid cestode infection in tucunaré Cichla sp. (Osteichthyes: Cichlidae) from Paraná River, São Paulo. Arq Bras Med Vet Zootec 63:584–590

    Article  Google Scholar 

  • Schludermann C, Konecny R, Laimgruber S, Lewis JW (2003) Fish macroparasites as indicators of heavy metal pollution in river sites in Austria. Parasitology 126:S61–S69

    Article  CAS  Google Scholar 

  • Scholz T (1999) Life cycles of species of Proteocephalus, parasites of fishes in the Paleartic Region: a review. J Parasitol 73:1–19

    Article  CAS  Google Scholar 

  • Silva FA, Neves RCF, Quintero-Pinto LG, Padilha CCF, Jorge SOMA, Barros MM, Pezzato LE, Padilha PM (2007) Determination of selenium by GFAAS in slurries of fish feces to estimate the bioavailability of this micronutrient in feed used in pisciculture. Chemosphere 68:1542–1547

    Article  CAS  Google Scholar 

  • Sures B, Nachev M, Selbach C, Marcogliese DJ (2017) Parasites responses to pollution: what we know and where we go in “Environmental Parasitology”. Parasit Vectors 10(65):1–19

    Google Scholar 

  • Sures B, Siddal R, Taraschewski H (1999) Parasites as accumulation indicators of heavy metal pollution. Parasitol Today 15(1):16–21

    Article  CAS  Google Scholar 

  • Sures B, Siddall R (1999) Pomphorhynchus laevis: the intestinal acanthocephalan as a lead sink for its fish host, chub (Leuciscus cephalus). Exp Parasitol 93:66–72

    Article  CAS  Google Scholar 

  • Sures B, Tarachewski H, Rokicki J (1997) Lead and cadmium content of two cestodes, Monobothrium wageneri and Bothriocephalus scorpii, and their fish hosts. Parasitol Res 83:618–623

    Article  CAS  Google Scholar 

  • Sures B (2003) Accumulation of heavy metals by intestinal helminths in fish: an overview and perspective. Parasitology 126(7):S53–S60

    Article  CAS  Google Scholar 

  • Sures B (2004) Environmental parasitology: relevancy of parasites in monitoring environmental pollution. Trends Parasitol 20:170–177

    Article  CAS  Google Scholar 

  • Sures B (2006) How parasitism and pollution affect the physiological homeostasis of aquatic hosts. J Helminthol 80:151–157

    Article  CAS  Google Scholar 

  • Sures B (2001) The use of fish parasites as bioindicators of heavy metals in aquatic ecosystems: a review. Aquat Ecol 35:245–255

    Article  CAS  Google Scholar 

  • Viarengo A, Canesi L (1991) Mussels as biological indicators of pollution. Aquaculture 94:225–243

    Article  Google Scholar 

  • Voulvoulis N, Georges K (2016) Industrial and agricultural sources and pathways of aquatic pollution. In: McKeown AE, Bugyi G (eds) Impact of water pollution on human health and environmental sustainability, 1st edn. IGI Global, Hershey, pp 29–54

    Chapter  Google Scholar 

  • Zhou Q, Zhang J, Fu J, Shi J, Jiang G (2008) Biomonitoring: an appealing tool for assessment of metal pollution in the aquatic ecosystem. Anal Chim Acta 606:135–150

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the Fundação de Amparo à Pesquisa do Estado de São Paulo (Process No. 2017/00566-5 and 2016/21040-9) for the financial support.

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Authors and Affiliations

  1. Instituto de Biociências, Universidade Estadual Paulista (UNESP), Botucatu, Brazil

    Lucas A. R. Leite & Pedro M. Padilha

  2. Pró-reitoria de Pesquisa e Pós-graduação, Universidade do Sagrado Coração (USC), Bauru, Brazil

    Felipe F. Januário

  3. Programa de Pós-graduação em Análise de Sistemas Ambientais, Centro Universitário CESMAC, Alagoas, Brazil

    Emmyle T. C. do Livramento, Rodney K. de Azevedo & Vanessa D. Abdallah

Authors
  1. Lucas A. R. Leite
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  2. Felipe F. Januário
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  3. Pedro M. Padilha
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  4. Emmyle T. C. do Livramento
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  5. Rodney K. de Azevedo
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  6. Vanessa D. Abdallah
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Correspondence to Lucas A. R. Leite.

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Leite, L.A.R., Januário, F.F., Padilha, P.M. et al. Heavy Metal Accumulation in the Intestinal Tapeworm Proteocephalus macrophallus Infecting the Butterfly Peacock Bass (Cichla ocellaris), from Southeastern Brazil. Bull Environ Contam Toxicol 103, 670–675 (2019). https://doi.org/10.1007/s00128-019-02704-z

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  • DOI: https://doi.org/10.1007/s00128-019-02704-z

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