Revista de Biología Tropical ISSN Impreso: 0034-7744 ISSN electrónico: 2215-2075

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Mercury concentration in larvae of Eustrongylides sp. (Nematoda: Dioctophymatoidea) from fish of the Brazilian Amazon
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Corrêa, L., Mota Atayde, H., Ferreira Sarrazin, S. L., & Bezerra de Oliveira, R. (2023). Mercury concentration in larvae of Eustrongylides sp. (Nematoda: Dioctophymatoidea) from fish of the Brazilian Amazon. Revista De Biología Tropical, 71(1), E55913. https://doi.org/10.15517/rev.biol.trop.v71i1.55913

Abstract

Introduction: Chemical pollution represents a great concern to aquatic organisms, especially fish. Metals enter the aquatic environment from a variety of sources, including natural biogeochemical cycles and anthropogenic sources such as industrial and residential effluents, mining and atmospheric sources. Objective: To describe the Eustrongylides sp. larvae and the interaction with their fish hosts as indicators of mercury (Hg) contamination in the Brazilian Amazon, and the distribution of Hg in the internal organs of fish species Hoplias malabaricus and Pygocentrus nattereri collected in oxbow lakes on the Tapajós River, in the municipality of Santarém, in the state of Pará. Methods: Total Hg was analyzed using the Direct Hg Analyzer - DMA-80. Concentrations of Hg in Eustrongylides sp. were compared with those found in the tissues/organs of the hosts H. malabaricus and P. nattereri. Hg concentrations in the host/parasite system were statistically compared using Principal Component Analysis. The bioconcentration factor (BCF) was calculated to assess the bioaccumulation capacity of metals in Eustrongylides sp. larvae, comparing the concentration of Hg in the parasite with that accumulated in the musculature of infected hosts. Results: Hg concentrations in all tissues/organs analyzed were higher in the parasitic species Eustrongylides sp. larvae when compared with those found in tissues/organs of H. malabaricus and P. nattereri. There was an inversely proportional relationship, showing that when Eustrongylides sp. larvae are present, the concentration in the parasite is higher than in the musculature of host fish H. malabaricus and P. nattereri. The BCF of Hg was found by comparing Eustrongylides sp. larvae/H. malabaricus muscle and was observed during a flood (BCF Hg = 15 364). Conclusions: The results confirm the greater bioaccumulative capacity of Eustrongylides sp. compared to its host. The data indicated the viability of using Eustrongylides sp. larvae in biomonitoring programs. It is worth mentioning that fish samples for Hg analysis must be free of parasites since their presence can alter the results.

https://doi.org/10.15517/rev.biol.trop..v71i1.55913
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References

Albuquerque, F. E. A., Herrero-Latorre, C., Miranda, M., Barrêto-Júnior, R. A., Oliveira, F. L. C., Sucupira, M. C. A., Ortolani, E. L., Minervino, A. H. H., & López-Alonso, M. (2021). Fish tissues for biomonitoring toxic and essential trace elements in the Lower Amazon. Environmental Pollution, 283, 117024.

Alcala-Orozco, M., Caballero-Gallardo, K., & Olivero-Verbel, J. (2020). Biomonitoring of mercury, cadmium and selenium in fish and the population of Puerto Nariño, at the southern corner of the Colombian Amazon. Archives of Environmental Contamination and Toxicology, 79, 354–370.

Andrews, R. H., Beveridge, I., & Adams, M. (1988). Identification of life cycle stages of the nematode Echinocephalus overstreeti by allozyme electrophoresis. Journal of Helminthology, 62, 153–157.

Barbosa, A. C., De Souza, J., Dórea, J. G., Jardim, W. F., & Fadini, P. S. (2003). Mercury biomagnification in a tropical black water, Rio Negro, Brazil. Archives of Environmental Contamination and Toxicology, 45, 235–246.

Barreto-Sa, A., Baltazar De Oliveira, C. S., Lima, A. A. D. S., Sanches-Borges, B. E., Silva-Santos, G. D. F., Mota-Da-Silva, C. I., Vieira-Da-Silva, M. I. C., & Nascimento-Pinheiro, M. D. C. (2019). Fish consumption frequency and lipid peroxidation in the riverside population of Lower Tocantins. Nutrición Clínica y Dietética Hospitalaria, 39, 64–68.

Barros, L. A., Moraes, J., & Oliveira, R. L. (2006). Nematóides com potencial zoonótico em peixes com importância econômica provenientes do rio Cuiabá. Revista Brasileira de Ciência Veterinária, 13, 55–57.

Benigno, R. N. M., Clemente, S. C., Matos, E. R., Pinto, R. M., Gomes, D. C., & Knoff, M. (2012). Nematodes in Hoplerytrinus unitaeniatus, Hoplias malabaricus and Pygocentrus nattereri (pisces characiformes) in Marajó Island, Brazil. Revista Brasileira de Parasitologia Veterinária, 21, 165–170.

Bialetzki, A., Nakatani, K., Sanches, P. V., Baumgartner, G., Makrakis, M. C., & Taguti, T. L. (2008). Desenvolvimento inicial de Hoplias aff. malabaricus (Bloch, 1794) (Osteichthyes, Erythrinidae) da planície alagável do alto rio Paraná, Brasil. Acta Scientiarum Biological Sciences, 30, 141–149.

Bush, A. O., Lafferty, K. D., Lotz, J. M., & Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology, 83, 575.

Crespo-Lopez, M. E., Augusto-Oliveira, M., Lopes-Araújo, A., Santos-Sacramento, L., Yuki-Takeda, P., Macchi, B. M., do Nascimento, J. L. M., Maia, C. S. F., Lima, R. R., & Arrifano, G. P. (2021) Mercury: What can we learn from the Amazon? Environment International, 146, 106223.

da Silva-Costa, M., Viana, L. F., Lima-Cardoso, C. A., Gonar-Silva-Isacksson, E. D., Silva, J. C., & Florentino, A. C. (2022). Landscape composition and inorganic contaminants in water and muscle tissue of Plagioscion squamosissimus in the Araguari River (Amazon, Brazil). Environmental Research, 208, 112691.

Dórea, J. G., Barbosa, A. C., Souzade, J., Fadini, P., & Jardim, W. F. (2004). Piranhas (Serrasalmus spp.) as markers of mercury bioaccumulation in Amazonian ecosystems. Ecotoxicology and Environmental Safety, 59, 57–63.

Eiras, J. C., Pavanelli, G. C., Takemoto, R. M., & Nawa, Y. (2018). Fish-borne nematodiases in South America: Neglected emerging diseases. Journal of Helminthology, 92, 649–654.

Eiras, J. C., Pavanelli, G. C., Takemoto, R. M., Yamaguchi, M. U., Karkling, L. C., & Nawa, Y. (2016). Potential risk of fish-borne nematode infections in humans in Brazil-Current status based on a literature review. Food Waterborne Parasitology, 5, 1–6.

Fontenelle, G., Knoff, M., Felizardo, N. N., Torres, E. J. L., Matos, E. R., Gomes, D. C., & São-Clemente, S. C. (2016). Anisakid larva parasitizing Plagioscion squamosissimus in Marajó Bay and Tapajós River, state of Pará, Brazil. Revista Brasileira de Parasitologia Veterinária, 25, 492–496.

Freitas, C. E. C., & Siqueira-Souza, F. K. (2009). O uso de peixes como bioindicador ambiental em áreas de várzea da bacia amazônica. Revista Agrogeoambiental, 1, 39–45.

Haddad-Junior, V., de Oliveira, Í. F., Bicudo, N. P., & Marques, M. E. A. (2021). Gnathostomiasis acquired after consumption of raw freshwater fish in the amazon region: A report of two cases in Brazil. Revista da Sociedade Brasileira Medicina Tropical, 54, 1–3.

Heckmann, R. A., Amin, O. M., & Khan, A. (2015). Histopathology of Centrorhynchus globirostris (Acanthocephala: Centrorhynchidae) infecting the intestine of the pheasant crow, Centropus sinensis (Stephens) in Pakistan. Scientia Parasitologica, 16, 151–155.

Jacobina, U. P., Paiva, E., & Dergam, J. A. (2011). Pleistocene karyotypic divergence in Hoplias malabaricus (Bloch, 1794) (Teleostei: Erythrinidae) populations in southeastern Brazil. Neotropical Ichthyology, 9, 325–333.

Lafferty, K. D. (1997). Environmental parasitology: What can parasites tell us about human impacts on the environment? Parasitology Today, 13, 251–255.

Lima, D. P., Santos, C., Silva, R. S., Yoshioka, E. T. O., & Bezerra, R. M. (2015). Contaminação por metais pesados em peixes e água da bacia do rio Cassiporé, Estado do Amapá, Brasil. Acta Amazonica, 45, 405–414.

Lino, A. S., Kasper, D., Guida, Y. S., Thomaz, J. R., & Malm, O. (2018). Mercury and selenium in fishes from the Tapajós River in the Brazilian Amazon: An evaluation of human exposure. Journal of Trace Elements in Medicine and Biology, 48, 196–201.

Lopes, I. G., Oliveira, R. G., & Ramos, F. M. (2016). Perfil do consumo de peixes pela população Brasileira. Biota Amazonia, 6, 62–65.

MacKenzie, K. (1999). Parasites as pollution indicators in marine ecosystems: A proposed early warning system. Marine Pollution Bulletin, 38, 955–959.

Marques, D. F., Santos, F. A., Silva, S. S., Sampaio, I., & Rodrigues, L. R. R. (2013). Cytogenetic and DNA barcoding reveals high divergence within the trahira, Hoplias malabaricus (Characiformes: Erythrinidae) from the lower Amazon River. Neotropical Ichthyology, 11, 459–466.

Melo, F. T. V., Melo, C. S. B., Nascimento, L. C. S., Giese, E. G., Furtado, A. P., & Santos, J. N. (2016). Morphological characterization of Eustrongylides sp. larvae (Nematoda, Dioctophymatoidea) parasite of Rhinella marina (Amphibia: Bufonidae) from Eastern Amazonia. Revista Brasileira de Parasitologia Veterinária, 25, 235–239.

Moravec, F., & Kohn, A. B. M. M. F. (1993). Nematode parasites of fishes of the Paraná River, Brazil. Part 3. Camallanoidea and Dracunculoidea. Folia Parasitologica (Praha), 40, 211–2209.

Morsy, K., Bashtar, A. R., Mostafa, N., El-Deeb, S., & Thabet, S. (2015). New host records of three juvenile nematodes in Egypt: Anisakis sp. (Type II), Hysterothylacium patagonense (Anisakidae), and Echinocephalus overstreeti (Gnathostomatidae) from the greater lizard fish Saurida undosquamis of the Red Sea. Parasitology Research, 114, 1119–1128.

Murrieta-Morey, G. A., & Malta, J. C. O. (2016). Parasites with zoonotic potential in Serrasalmus altispinis Merckx, Jegue & Santos, 2000 (Characiformes: Serrasalmidae) from floodplain lakes in the Amazon, Brasil. Neotropical Helminthology, 10, 249–258.

Nelson, J. (2006). Fishes of the world (4th Ed.). John Wiley and Sons, Inc.

Poulin, R. (1992). Toxic pollution and parasitism in freshwater fish. Parasitology Today, 8, 58–61.

QGIS Development Team. (2020). QGIS Geographic Information System. Open Source Geospatial Foundation Project. http://qgis.osgeo.org

Reiczigel, J., Marozzi, M., Fábián, I., & Rózsa, L. (2019). Biostatistics for parasitologists – A primer to quantitative parasitology. Trends in Parasitology, 35, 277–281.

Rozsa, L., Reiczigel, J., & Majoros, G. (2000). Quantifying parasites in samples of hosts. Journal of Parasitology, 2, 228–232.

Santin, M., Takemoto, R. M., Pavanelli, G. C., Bialetzki, A., & Tavernari, F. C. (2009). Helminths parasitizing larval fish from Pantanal, Brazil. Journal of Helminthology, 83(1), 51–55.

Santoro, M., Iaccarino, D., & Bellisario, B. (2020). Host biological factors and geographic locality influence predictors of parasite communities in sympatric sparid fishes off the southern Italian coast. Scientific Reports, 10, 13283.

Santos, U., Völcker, C. M., Belei, F. A., Cioffi, M. B., Bertollo, L. A. C., Paiva, S. R., & Dergam, J. A. (2009). Molecular and karyotypic phylogeography in the Neotropical Hoplias malabaricus (Erythrinidae) fish in eastern Brazil. Journal Fish Biology, 75, 2326–2343.

Schludermann, C., Konecny, R., Laimgruber, S., Lewis, J. W., Schiemer, F., Chovanec, A., & Sures, B. (2003). Fish macroparasites as indicators of heavy metal pollution in river sites in Austria. Parasitology, 126, 61–69.

Silva, M. A., Aride, P. H. R., Santos, S. M., Araújo, R. L., Pantoja-Lima, J., Braga, T. M. P., & Oliveira, A. T. (2014). Preferências e restrições alimentares de moradores do município de Juruá , Amazonas. Scientia Amazonia, 3, 106–111.

Silva, S. F., Oliveira, D. C., Pereira, J. P. G., Castro, S. P., Costa, B. N. S., & Lima, M. O. (2019). Seasonal variation of mercury in commercial fishes of the Amazon Triple Frontier, Western Amazon Basin. Ecological Indicators, 106, 105549.

Siqueira-Souza, F. K., & Freitas, C. E. C. (2004). Fish diversity of floodplain lakes on the lower stretch of the Solimões River. Brazilian Journal of Biology, 64, 501–510.

Sures, B. (2003). Accumulation of heavy metals by intestinal helminths in fish: An overview and perspective. Parasitology, 126, 53–60.

Sures, B. (2006). How parasitism and pollution affect the physiological homeostasis of aquatic hosts. Journal of Helminthology, 80(2), 151–157.

Sures, B. (2007). Host-parasite interactions from an ecotoxicological perspective. Parasitologia, 49, 173–176.

Sures, B. (2008a). Environmental parasitology. Interactions between parasites and pollutants in the aquatic environment. Parasite, 15, 434–438.

Sures, B. (2008b). Host-parasite interactions in polluted environments. Journal of Fish Biology, 73, 2133–2142.

Sures, B., & Siddall, R. (2003). Pomphorhynchus laevis (Palaeacanthocephala) in the intestine of chub (Leuciscus cephalus) as an indicator of metal pollution. International Journal for Parasitology, 33, 65–70.

Sures, B., Siddall, R., & Taraschewski, H. (1999). Parasites as accumulation indicators of heavy metal pollution. Parasitology Today, 15, 16–21.

Sures, B., & Taraschewski, H. (1995). Cadmium concentrations in two adult acanthocephalans, Pomphorhynchus laevis and Acanthocephalus lucii, as compared with their fish hosts and cadmium and lead levels in larvae of A. lucii as compared with their crustacean host. Parasitology Research, 81, 494–497.

Tanaka, Y., & Mori, Y. (1997). Principal Component Analysis based on a subset of variables: variable selection and sensitivity analysis. American Journal of Mathematics and Management Science, 17(1), 61–89.

Thatcher, V. E., & Brites-Neto, J. (1994). Diagnóstico, prevenção e tratamento das enfermidades de peixes Neotropicais de água doce. Revista Brasileira de Medicina Veterinária, 16, 111–128.

Thielen, F., Zimmermann, S., Baska, F., Taraschewski, H., & Sures, B. (2004). The intestinal parasite Pomphorhynchus laevis (Acanthocephala) from barbel as a bioindicator for metal pollution in the Danube River near Budapest, Hungary. Environmental Pollution, 129, 421–429.

Vasconcellos, A. C. S., Hallwass, G., Bezerra, J. G., Aciole, A. N. S., Meneses, H. N. M., Lima, M. O., Jesus, I. M., Hacon, S. S., & Basta, P. C. (2021). Health risk assessment of mercury exposure from fish consumption in Munduruku indigenous communities in the Brazilian Amazon. International Journal of Environmental Research and Public Health, 18, 7940.

Vazzoler, A. W. M. (1996). Biologia da reprodução de peixes teleósteos, teoria e prática. Eduem.

Vidal-Martínez, V. M., Pech, D., Sures, B., Purucker, S. T., & Poulin, R. (2010). Can parasites really reveal environmental impact? Trends in Parasitology, 26, 44–51.

Vitorino, C. A., Souza, I. L., Rosa, J. N., Valente, G. T., Martins, C., & Venere, P. C. (2011). Molecular cytogenetics and its contribution to the understanding of the chromosomal diversification in Hoplias malabaricus (Characiformes). Journal of Fish Biology, 78, 1239–1248.

Williams, H. H., & Mackenzie, K. (2003). Marine parasites as pollution indicators: An update. Parasitology, 126(S7), S27–41.

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