Resumen
Introducción: La contaminación química del hábitat acuático representa un gran peligro para organismos acuáticos, especialmente para peces. Los metales ingresan al ambiente acuático desde una variedad de fuentes, incluidos los ciclos biogeoquímicos naturales y fuentes antropogénicas, como efluentes industriales y residenciales, minería y fuentes atmosféricas. Objetivo: Describir las especies de Eustrongylides sp. y la interacción con sus peces hospederos como indicadores de contaminación por mercurio en la Amazonía brasileña, y la distribución en los órganos internos de las especies de peces Hoplias malabaricus y Pygocentrus nattereri recolectadas en cochas del Río Tapajós, en el municipio de Santarém, del estado de Pará. Métodos: El Hg total se analizó utilizando el Direct Hg Analyzer - DMA-80. Las concentraciones de Eustrongylides sp. se compararon con las encontrados en los tejidos/órganos de los hospederos H. malabaricus y P. nattereri. Las concentraciones en el sistema hospedero/parásito se compararon estadísticamente utilizando el análisis de componentes principales. Se calculó el factor de bioconcentración (BCF) para evaluar la capacidad de bioacumulación de metales en larvas de Eustrongylides sp., comparando la concentración en el parásito con la acumulada en la musculatura de los hospederos infectados. Resultados: Las concentraciones de Hg en todos los tejidos/órganos analizados fueron mayores en las larvas de la especie parasitaria Eustrongylides sp. en comparación con las encontradas en los tejidos/órganos de H. malabaricus y P. nattereri. Hubo una relación inversamente proporcional, mostrando que cuando las larvas de Eustrongylides sp. están presentes, la concentración en el parásito es mayor que en la musculatura de los peces hospederos H. malabaricus y P. nattereri. El BCF de Hg se encontró comparando Eustrongylides sp. larvas/ músculo H. malabaricus y se observó durante una inundación (BCF Hg = 15 364). Conclusiones: Los resultados confirman la mayor capacidad bioacumulativa de Eustrongylides sp. en comparación con su hospedero. Los datos indicaron la viabilidad de utilizar larvas de Eustrongylides sp. en programas de biomonitoreo. Cabe mencionar que las muestras de pescado para análisis de Hg deben estar libres de parásitos ya que su presencia puede alterar los resultados.
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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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