Mercury concentration in larvae of Eustrongylides sp. (Nematoda: Dioctophymatoidea) from fish of the Brazilian Amazon
DOI:
https://doi.org/10.15517/rev.biol.trop..v71i1.55913Abstract
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.
Downloads
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. DOI: https://doi.org/10.1016/j.envpol.2021.117024
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. DOI: https://doi.org/10.1007/s00244-020-00761-8
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. DOI: https://doi.org/10.1017/S0022149X0001141X
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. DOI: https://doi.org/10.1007/s00244-003-0207-1
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. DOI: https://doi.org/10.12873/391barreto
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. DOI: https://doi.org/10.4322/rbcv.2014.267
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. DOI: https://doi.org/10.1590/S1984-29612012000200018
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. DOI: https://doi.org/10.4025/actascibiolsci.v30i2.3608
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. DOI: https://doi.org/10.2307/3284227
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. DOI: https://doi.org/10.1016/j.envint.2020.106223
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. DOI: https://doi.org/10.1016/j.envres.2022.112691
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. DOI: https://doi.org/10.1016/j.ecoenv.2003.07.012
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. DOI: https://doi.org/10.1017/S0022149X17001006
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. DOI: https://doi.org/10.1016/j.fawpar.2016.08.002
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. DOI: https://doi.org/10.1590/s1984-29612016034
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. DOI: https://doi.org/10.18406/2316-1817v1n2200975
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. DOI: https://doi.org/10.1590/0037-8682-0127-2020
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. DOI: https://doi.org/10.1590/S1679-62252011005000023
Lafferty, K. D. (1997). Environmental parasitology: What can parasites tell us about human impacts on the environment? Parasitology Today, 13, 251–255. DOI: https://doi.org/10.1016/S0169-4758(97)01072-7
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. DOI: https://doi.org/10.1590/1809-4392201403995
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. DOI: https://doi.org/10.1016/j.jtemb.2018.04.012
Lopes, I. G., Oliveira, R. G., & Ramos, F. M. (2016). Perfil do consumo de peixes pela população Brasileira. Biota Amazonia, 6, 62–65. DOI: https://doi.org/10.18561/2179-5746/biotaamazonia.v6n2p62-65
MacKenzie, K. (1999). Parasites as pollution indicators in marine ecosystems: A proposed early warning system. Marine Pollution Bulletin, 38, 955–959. DOI: https://doi.org/10.1016/S0025-326X(99)00100-9
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. DOI: https://doi.org/10.1590/S1679-62252013000200015
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. DOI: https://doi.org/10.1590/S1984-29612016024
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. DOI: https://doi.org/10.1007/s00436-014-4285-y
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. DOI: https://doi.org/10.24039/rnh2016102746
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. DOI: https://doi.org/10.1016/0169-4758(92)90090-O
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. DOI: https://doi.org/10.1016/j.pt.2019.01.003
Rozsa, L., Reiczigel, J., & Majoros, G. (2000). Quantifying parasites in samples of hosts. Journal of Parasitology, 2, 228–232. DOI: https://doi.org/10.1645/0022-3395(2000)086[0228:QPISOH]2.0.CO;2
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. DOI: https://doi.org/10.1017/S0022149X08092171
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. DOI: https://doi.org/10.1038/s41598-020-69628-1
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. DOI: https://doi.org/10.1111/j.1095-8649.2009.02489.x
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. DOI: https://doi.org/10.1017/S0031182003003743
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. DOI: https://doi.org/10.1016/j.ecolind.2019.105549
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. DOI: https://doi.org/10.1590/S1519-69842004000300013
Sures, B. (2003). Accumulation of heavy metals by intestinal helminths in fish: An overview and perspective. Parasitology, 126, 53–60. DOI: https://doi.org/10.1017/S003118200300372X
Sures, B. (2006). How parasitism and pollution affect the physiological homeostasis of aquatic hosts. Journal of Helminthology, 80(2), 151–157. DOI: https://doi.org/10.1079/JOH2006346
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. DOI: https://doi.org/10.1051/parasite/2008153434
Sures, B. (2008b). Host-parasite interactions in polluted environments. Journal of Fish Biology, 73, 2133–2142. DOI: https://doi.org/10.1111/j.1095-8649.2008.02057.x
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. DOI: https://doi.org/10.1016/S0020-7519(02)00249-7
Sures, B., Siddall, R., & Taraschewski, H. (1999). Parasites as accumulation indicators of heavy metal pollution. Parasitology Today, 15, 16–21. DOI: https://doi.org/10.1016/S0169-4758(98)01358-1
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. DOI: https://doi.org/10.1007/BF00931792
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. DOI: https://doi.org/10.1080/01966324.1997.10737430
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. DOI: https://doi.org/10.1016/j.envpol.2003.11.011
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. DOI: https://doi.org/10.3390/ijerph18157940
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. DOI: https://doi.org/10.1016/j.pt.2009.11.001
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. DOI: https://doi.org/10.1111/j.1095-8649.2011.02930.x
Williams, H. H., & Mackenzie, K. (2003). Marine parasites as pollution indicators: An update. Parasitology, 126(S7), S27–41. DOI: https://doi.org/10.1017/S0031182003003640
Published
Issue
Section
License
Copyright (c) 2023 Revista de Biología Tropical
This work is licensed under a Creative Commons Attribution 4.0 International License.
Creative Commons Attribution 4.0 License (CC BY 4.0)
Attribution (BY) • (BY) You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work).
