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Fish parasites as indicators of organic pollution in southern Brazil

Published online by Cambridge University Press:  01 June 2017

A.C.F. Lacerda ,
K. Roumbedakis ,
J.G.S. Bereta Junior ,
A.P.O. Nuñer ,
M.M. Petrucio  and
M.L. Martins
A.C.F. Lacerda*
Affiliation:
Laboratory of Hydrology, Microbiology and Parasitology (LAHMP), Postgraduate Program in Biological Sciences (PPGCB), Federal University of Paraíba (UFPB), 58051-900, João Pessoa, PB, Brazil Postgraduate Program in Ecology (POSECO), Federal University of Santa Catarina (UFSC), 88040-900, Florianópolis, SC, Brazil
K. Roumbedakis
Affiliation:
Department of Aquaculture, Federal University of Santa Catarina (UFSC), Rod. Admar Gonzaga, 1346, 88040-900, Florianópolis, SC, Brazil
J.G.S. Bereta Junior
Affiliation:
Department of Aquaculture, Federal University of Santa Catarina (UFSC), Rod. Admar Gonzaga, 1346, 88040-900, Florianópolis, SC, Brazil
A.P.O. Nuñer
Affiliation:
Postgraduate Program in Ecology (POSECO), Federal University of Santa Catarina (UFSC), 88040-900, Florianópolis, SC, Brazil
M.M. Petrucio
Affiliation:
Postgraduate Program in Ecology (POSECO), Federal University of Santa Catarina (UFSC), 88040-900, Florianópolis, SC, Brazil
M.L. Martins
Affiliation:
Department of Aquaculture, Federal University of Santa Catarina (UFSC), Rod. Admar Gonzaga, 1346, 88040-900, Florianópolis, SC, Brazil
*
*E-mail: acflacerda@dse.ufpb.br
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Abstract

Increasing urbanization along riverbanks is a constant source of stressors to the aquatic community, and the use of bioindicators is suitable to detect and monitor the effect of each stressor. We investigated the parasites of the ‘cará’ fish (Geophagus brasiliensis) as potential bioindicators in a river whose banks are subject to increasing anthropogenic pressure. Samples were taken at four points of the Sangradouro River, in Florianópolis, southern Brazil, bimonthly for 12 months. Water temperature, pH, dissolved oxygen, conductivity and salinity were measured at each point and water samples were taken for nutrient analysis (total nitrogen, nitrite, total ammonia nitrogen, total phosphorus, phosphate), and total and faecal coliforms. A generalized linear model (GLM) was constructed using the abundance of each parasite species as the response variable and biometric characteristic of the fish and water variables as possible predictors. Among the 137 fish examined, 114 (83.2%) were parasitized by at least one parasite species. Two species of ectoparasites (Sciadicleithrum guanduensis and Neascus-type metacercariae) and two species of endoparasites (Pandosentis aff. iracundus and Homalometron pseudopallidum) were observed. This is the first record of the genus Pandosentis in Brazilian waters and the first record of the species G. brasiliensis as a host for this parasite. Among the analysed groups of parasites, monogeneans and acanthocephalans proved to be the most sensitive to the concentrations of dissolved oxygen, faecal coliforms and total ammonia nitrogen in the water. Our study suggests that the abundance of both monoxenic and heteroxenous parasites can be negatively affected by organic pollution in the aquatic environment, reinforcing the potential of fish parasites as indicators of water quality.

Type
Research Paper
Information
Journal of Helminthology , Volume 92 , Issue 3 , May 2018 , pp. 322 - 331
Copyright
Copyright © Cambridge University Press 2017 

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References

Adams, S.M. & Greeley, M.S. (2000) Ecotoxicological indicators of water quality: using multi-response indicators to assess the health of aquatic ecosystems. Water, Air, and Soil Pollution 123, 103–115.Google Scholar
Adams, S.M., Bevelhimer, M.S., Greeley, M.S., Levine, D.A. & The, S.T. (1999) Ecological risk assessment in a large river-reservoir: 6. Bioindicators of fish population health. Environmental Toxicology and Chemistry 18, 540–628.Google Scholar
Appleby, C. & Mo, T.A. (1997) Population dynamics of Gyrodactylus salaris (Monogenea) infecting Atlantic salmon, Salmo salar, in the river Batnfjordselva, Norway. Journal of Parasitology 83, 23–30.Google Scholar
Arthur, J.W., West, C.W., Allen, K.N. & Hedtke, S.F. (1987) Seasonal toxicity of ammonia to five fish and nine invertebrate species. Bulletin of Environmental Contamination and Toxicology 38, 324–331.Google Scholar
Azevedo, T.M.P., Martins, M.L., Bozzo, F.R. & Moraes, F.R. (2006) Haematological and gill responses in parasitized tilapia from Valley of Tijucas River, SC, Brazil. Scientia Agricola 63, 115–120.Google Scholar
Bastos, R.F., Condini, V., Varela Junior, A.S. & Garcia, A.M. (2011) Diet and food consumption of the pearl cichlid Geophagus brasiliensis (Teleostei: Cichlidae): relationships with gender and sexual maturity. Neotropical Ichthyology 9, 825–830.Google Scholar
Bellay, S., Ueda, B.H., Takemoto, R.M., Lizama, M.A.P. & Pavanelli, G.C. (2012) Fauna parasitária de Geophagus brasiliensis (Perciformes: Cichlidae) em reservatórios do estado do Paraná, Brasil. Brazilian Journal of Biosciences 10, 74–78.Google Scholar
Blanar, C.A., Munkittrick, K.R., Houlahan, J., MacLatchy, D.L. & Marcogliese, D.J. (2009) Pollution and parasitism in aquatic animals: a meta-analysis of effect size. Aquatic Toxicology 93, 18–28.CrossRefGoogle ScholarPubMed
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, 575–583.Google Scholar
Camargo, J.A. & Alonso, A. (2005) Nitrate toxicity to aquatic animals: a review with new data for freshwater invertebrates. Chemosphere 58, 1255–1267.Google Scholar
Camargo, J.A. & Alonso, A. (2006) Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystems: a global assessment. Environment International 32, 831–849.Google Scholar
Carvalho, A.R., Tavares, L.E.R. & Luque, J.L. (2010) Variação sazonal dos metazoários parasitos de Geophagus brasiliensis (Perciformes: Cichlidae) no Rio Guandu, Estado do Rio de Janeiro, Brasil. Acta Scientiarum Biological Sciences 32, 159–167.Google Scholar
Cezar, A.D. & Luque, J.L. (1999) Metazoan parasites of the Atlantic Spadefish, Chaetodipterus faber (Teleostei: Ephippidae) from the coastal zone of the State of Rio de Janeiro, Brazil. Journal of Helminthology 66, 14–20.Google Scholar
Chubb, J.C. (1979) Seasonal occurrence of helminths in freshwater fishes. Part II. Trematoda. Advances in Parasitology 17, 141–313.Google Scholar
Eiras, J.C. (1994) Elementos de Ictioparasitologia. 339 pp. Portugal, Fundação Eng. Antônio de Almeida.Google Scholar
Eiras, J.C., Takemoto, R.M. & Pavanelli, G.C. (2006) Métodos de estudo e técnicas laboratoriais em parasitologia de peixes. 199 pp. Maringá, Eduem.Google Scholar
Eiras, J.C., Takemoto, R.M. & Pavanelli, G.C. (2010) Diversidade dos Parasitos de Peixes de Água Doce do Brasil. 278 pp. Maringá, Chicletec.Google Scholar
Gannicott, A.M. & Tinsley, R.C. (1998) Environmental effects on transmission of Discocotyle sagittata (Monogenea): egg production and development. Parasitology 117, 499–504.Google Scholar
Garcia, A.M., Raseira, M.B., Vieira, J.P., Winemiller, K.O. & Grim, A.M. (2003) Spatiotemporal variation in shallow-water freshwater fish distribution and abundance in large subtropical coastal lagoon. Environmental Biology of Fishes 68, 215–228.Google Scholar
Golterman, H.L., Clymo, R.S. & Ohnstad, M.A.M. (1978) Methods for chemical analysis of freshwater. 213 pp. Oxford, Blackwell Scientific Publications.Google Scholar
Gomiero, L.M. & Braga, F.M. (2007) Reproduction of a fish assemblage in the state of São Paulo, southeastern Brazil. Brazilian Journal of Biology 67, 283–292.Google Scholar
Hudson, P.J., Dobson, A.P. & Lafferty, K.D. (2006) Is a healthy ecosystem one that is rich in parasites? Trends in Ecology and Evolution 21, 381–385.Google Scholar
International Organization for Standardization. (2006) ISO 4831:2006. Microbiology of food and animal feeding stuffs – horizontal method for the detection and enumeration of coliforms – most probable number technique. Geneva, Switzerland, International Organization for Standardization.Google Scholar
Jansen, P.A. & Bakke, T.A. (1991) Temperature-dependent reproduction and survival of Gyrodactylus salaris Malmberg, 1957 (Platyhelminthes: Monogenea) on Atlantic salmon (Salmo salar L.). Parasitology 102, 105–112.Google Scholar
Kennedy, C.R. (2006) Ecology of the Acanthocephala. Cambridge, Cambridge University Press.Google Scholar
Kornacki, J.L. & Johnson, J.L. (2001) Enterobacteriaceae, coliforms and Escherichia coli as quality and safety indicators. pp. 69–82 in Downes, F.P. & Ito, K. (Eds) Compendium of methods for the microbiological examination of foods. 4th edn. Washington DC, American Public Health Association.Google Scholar
Koroleff, F. (1976) Determination of nutrients. pp. 117–181 in Grasshoff, K. (Ed.) Methods of sea water analysis. Weinhein, Verlag Chemie.Google Scholar
Lafferty, K.D. (1997) Environmental parasitology: what can parasites tell us about human impact on the environment? Parasitology Today 13, 251–255.CrossRefGoogle Scholar
Lagrue, C. & Poulin, R. (2015) Measuring fish body condition with or without parasites: does it matter? Journal of Fish Biology 87, 836–847.Google Scholar
Landsberg, J.H., Blakesley, B.A., Reese, R.O., Mcrae, G. & Forstchen, P.R. (1998) Parasites of fish as indicators of environmental stress. Environmental Monitoring and Assessment 51, 211–232.Google Scholar
Le Cren, E.D. (1951) The length–weight relationship and seasonal cycle in gonadal weight condition in the perch Perca fluviatilis. Journal of Animal Ecology 20, 201–209.Google Scholar
Lewis, J. & Hoole, D. (2003) Parasitism and environmental pollution: parasites and hosts as indicators of water quality. Parasitology 126, S1–S3.Google Scholar
Lima-Junior, S.E., Cardone, I.B. & Goitein, R. (2002) Determination of a method for calculation of Allometric Condition Factor of fish. Acta Scientiarium 24, 397–400.Google Scholar
Lizama, M.A.P., Takemoto, R.M. & Pavanelli, G.C. (2006) Parasitism influence on the hepato, splenosomatic and weight/length relation and relative condition factor of Prochilodus lineatus (Valenciennes, 1836) (Prochilodontidae) of the upper Paraná River floodplain, Brazil. Revista Brasileira de Parasitologia Veterinária 15, 116–122.Google Scholar
Madanire-Moyo, G.N., Luus-Powell, W.J. & Olivier, P.A. (2012) Diversity of metazoan parasites of the Mozambique tilapia, Oreochromis mossambicus (Peters, 1852), as indicators of pollution in the Limpopo and Olifants River systems. The Onderstepoort Journal of Veterinary Research 16, 1–9.Google Scholar
Madi, R.R. & Ueta, M.T. (2009) O papel de Ancyrocephalinae (Monogenea: Dactylogyridae), parasito de Geophagus brasiliensis (Pisces: Cichlidae), como indicador ambiental. Revista Brasileira de Parasitologia Veterinária 18, 38–41.Google Scholar
Markert, B.A., Breure, A.M. & Zechmeister, H.G. (2003) Bioindicators and biomonitors: Principles, concepts and applications. 997 pp. Oxford, Elsevier.Google Scholar
Martins, M.L., Fujimoto, R.Y. & Moraes, F.R. (2000) Prevalence and seasonality of Diplectanum piscinarius Kritsky and Thacher 1984 (Monogenoidea) in the gills of Plagioscion squamosissimus Heckel 1840 (Scianidae) from Volta Grande reservoir, Minas Gerais, Brazil. Revista Brasileira de Parasitologia Veterinária 9, 105–107.Google Scholar
Nachev, M. & Sures, B. (2016) Seasonal profile of metal accumulation in the acanthocephalan Pomphorhynchus laevis: a valuable tool to study infection dynamics and implications for metal monitoring. Parasites & Vectors 9. doi: 10.1186/s13071-016-1576-4.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). Parasites & Vectors 6, 21.Google Scholar
Overstreet, R.M. (1997) Parasitological data as monitors of environmental health. Parassitologia 39, 169–175.Google Scholar
Pavanelli, G.C., Eiras, J.C. & Takemoto, R.M. (1998) Doenças de peixes. Profilaxia, Diagnóstico e Tratamento. 3rd edn. 311 pp. Maringá, Eduem.Google Scholar
Piedras, S.R.N., Oliveira, J.L.R., Moraes, P.R.R. & Bager, A. (2006) Toxicidade aguda da amônia não ionizada e do nitrito em alevinos de Cichlasoma facetum (Jenyns, 1842). Ciência e Agrotecnologia 30, 1008–1012.CrossRefGoogle Scholar
Poulin, R. (1992) Toxic pollution and parasitism in freshwater fish. Parasitology Today 8, 58–61.Google Scholar
Poulin, R. (1999) Body size vs abundance among parasite species: positive relationships? Ecography 22, 246–250.Google Scholar
Rábago-Castro, J., Sánchez-Martínez, J.G., Loredo-Osti, J., Gomez-Flores, R., Tamez-Guerra, P. & Ramírez-Pfeiffer, C. (2011) Temporal and spatial variations of ectoparasites on cage-reared channel catfish, Ictalurus punctatus, in Tamaulipas, Mexico. Journal of the World Aquaculture Society 42, 406–411.Google Scholar
Rassier, G.L., Pesenti, T.C., Pereira Junior, J., Silva, D.S., Wendt, E.W., Monteiro, C.M. & Aires Berne, M.E. (2015) Metazoan parasites of Geophagus brasiliensis (Perciformes: Cichlidae) in Patos Lagoon, extreme south of Brazil. Brazilian Journal of Veterinary Parasitology 24, 447–453.Google Scholar
R Development Core Team (2010) A language and environment for statistical computing. Vienna, Austria, R Foundation for Statistical Computing. Available at http://www.R-project.org, 2010 (accessed 22 November 2016).Google Scholar
Strickland, J.D.H. & Parsons, T.R. (1960) A manual of seawater analysis. Bulletin of the Fisheries Research Board of Canada 125, 1–18.Google Scholar
Sures, B. (2003) Accumulation of heavy metals by intestinal helminths in fish: an overview and perspective. Parasitology 126, S53–S60.Google Scholar
Sures, B. (2004) Environmental parasitology: relevancy of parasites in monitoring environmental pollution. Trends in Parasitology 20, 170–177.Google Scholar
Valderrama, J.C. (1981) The simultaneous analysis of total nitrogen and phosphorus in natural waters. Marine Chemistry 10, 1109–1122.Google Scholar
Winger, A.W., Kanck, M., Kristoffersen, K. & Knudsen, R. (2008) Seasonal dynamics and persistence of Gyrodactylus salaris in two riverine anadromous Arctic charr populations. Environmental Biology of Fishes 83, 117–123.Google Scholar