Abstract
Gill anomalies in two fish species (Geophagus brasiliensis and Astyanax bimaculatus) were compared among three freshwater systems with different water quality: one eutrophic river, one eutrophic reservoir, and one oligotrophic reservoir. The raised hypotheses are that reservoirs with low water quality (eutrophic) have fish with more gills anomalies compared with reservoirs with high water quality (oligotrophic), and that the more stable environmental conditions of eutrophic rivers have fish with better healthy conditions than eutrophic reservoirs that have lesser stable environmental conditions. Gills of 36 adult individuals of G. brasiliensis and 23 of A. bimaculatus collected during the winter 2008 and winter 2009 were examined, and the proportions of occurrence of nine histological alterations were compared for the two species among the three systems using a binomial t test for independent samples. Histological changes in fish gills that are reversible and unspecific, such as epithelial lifting, interstitial edema, leukocyte infiltration, hyperplasia of the epithelial cells, lamellar fusion, and vasodilatation were common in both fish species in the three systems. However, lamellar aneurism, which is a more serious and often irreversible anomaly, and lamellar blood congestion occurred only in fish from the two reservoirs. Alternatively, necrosis occurred more in fish from the river. Fish gill anomalies in both species did not differ between the two reservoirs, despite having different water quality. We rejected the hypothesis that reservoirs with lower water quality have fish with more gill injuries compared with high water quality reservoirs. Moreover, the eutrophic river seems to affect differently the healthy condition of fish species, compared with the eutrophic reservoir.
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Abel, P. D. (1976). Toxic action of several lethal concentrations of an anionic detergent on the gills of the brown trout (Salmo trutta L.). Journal of Fish Biology, 9, 441–446.
Albinati, A. C. L., Moreira, E. L. T., Albinati, R. C. B., Carvalho, J. V., de Lira, A. D., Santos, G. B., et al. (2009). Histological biomarkers—Chronic toxicity for roundup in Piauçu (Leporinus macrocephalus). Arquivos Brasileiro de Medicina Veterinária e Zootecnia, 61, 621–627.
Araújo, F. G., Pinto, B. C. T., & Teixeira, T. P. (2009). Longitudinal patterns of fish assemblages in a large tropical river in southeastern Brazil: Evaluating environmental influences and some concepts in river ecology. Hydrobiologia, 618, 89–107.
Arellano, J. M., Storch, V., & Sarasquete, C. (1999). Histological changes and copper accumulation in liver and gills of the Senegales Sole, Solea senegalensis. Ecotoxicology and Enviroronmental Safety, 44, 62–72.
Branco, C. W. C., Rocha, M. I. A., Pinto, G. F. S., Gômara, G. A., & de Filippo, R. (2002). Limnological features of Funil Reservoir (R.J., Brazil) and indicator properties of rotifers and cladocerans of the zooplankton community. Lakes & Reservoir: Research and Management, 7, 87–92.
Carvalho, C. E. V., & Torres, J. P. M. (2002). The ecohydrology of the Paraíba do Sul river, Southeast Brazil. In M. E. McClain (Ed.), The ecohydrology of South American rivers and wetlands (pp. 179–191). Venice, Italy: The IAHS Series of Special Publications.
Coutinho, C., & Gokhale, K. S. (2000). Selected oxidative enzymes and histopathological changes in the gills of Cyprinus carpio and Oreochromis mossambicus cultured in secondary sewage effluent. Water Research, 34, 2997–3004.
Evans, D. H., Piermarini, P. M., & Choe, K. P. (2005). The multifunctional fish gill: Dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiological Reviews, 85, 97–177.
Franchini, A., Alessandrini, F., & Fantin, A. M. B. (1994). Gill morphology and ATPase activity in the goldfish Carassius carassius var. auratus exposed to experimental lead intoxication. Bollettino di Zoologia, 61, 29–37.
Garcia-Santos, S., Monteiro, M., Carrola, J., & Fontaínhas-Fernandes, A. (2007). Histopathological lesions of tilapia Oreochromis niloticus gills caused by cadmium. Brazilian Journal of Veterinary Animal Sciences, 59, 376–381.
Garmendia, L., Soto, M., Cajaraville, M. P., & Marigómez, I. (2010). Seasonality in cell and tissue-level biomarkers in Mytilus galloprovincialis: Relevance for long-term pollution monitoring. Aquatic Biology, 9(3), 203–219.
Giari, L., Manera, M., Simoni, E., & Dezfuli, B. S. (2006). Changes to chloride and rodlet cells in gills, kidney and intestine of Dicentrarchus labrax (L.) exposed to reduced salinities. Journal of Fish Biology, 69, 590–600.
Gomes, J. H. C., Dias, A. C. I. M., & Branco, C. C. (2008). Fish assemblage composition in three reservoirs in the State of Rio de Janeiro. Acta Limnologica Brasisliensis, 20, 373–380.
Heath, A. G. (1995). Water pollution and fish physiology. Boca Raton: CRC.
Hinton, D. E., & Laurén, D. J. (1990). Liver structural alterations accompanying chronic toxicity in fishes: Potential biomarkers of exposure. In J. F. McCarthy & R. L. Shugart (Eds.), Biomarkers of environmental contamination (pp. 51–65). Boca Raton: Lewis Publishers.
Hughes, G. M., & Perry, S. F. (1976). Morphometric study of trout gills: A light microscopic method for the evaluation of pollutant action. Journal of Experimental Biology, 63, 447–460.
Leino, R. L. (2001). Seasonal increases of rodlet cells and other cell-types in percid gills: Association with parasitic infections. In S. D. Bahram (Ed.), Proceedings of the First International Rodlet Cell (Workshop) Ferrara: Italy.
Lima, F. B., Braccini, M. D. C., Díaz, A. O., Junior, C. P., & Guimarães, A. C. G. (2009). Morphology of the gills of Steindachnerina brevipinna (Eigenmann & Eigenmann, 1889) (Characiformes, Curimatidae). Biotemas, 22, 87–92.
Matthaei, C. D., Uehlinger, U., & Frutiger, A. (1997). Response of benthic invertebrates to natural versus experimental disturbance in a Swiss prealpine river. Freshwater Biology, 37, 61–77.
Mazon, A. F., Cerqueira, C. C., & Fernandes, M. N. (2002). Gill cellular changes induced by copper exposure in the South American tropical freshwater fish Prochilodus scrofa. Environmental Research, 88, 52–63.
Monteiro, S. M., Rocha, E., Mancera, J. M., Fontaínhas-Fernandes, A., & Sousa, M. (2008). A stereological study of copper toxicity in gills of Oreochromis niloticus. Ecotoxicology and Enviroronmental Safety, 72, 213–223.
Motter, M. D. S., Silva, L. D., Borges-de-Oliveira, R., Yamada, A. T., Santos, S. C., & Sabóia-Morais, S. M. T. (2004). Índice mitótico em células epiteliais da brânquia de Guaru (Poecilia vivipara) tratados com frações da casca do caule e da folha de Pequi (Caryocar brasiliensis). Brazilian Journal of Veterinary Research and Animal Sciences, 41, 221–227.
Nogueira, D. J., Castro, S. C., & Sá, O. R. (2008). Evaluation of water quality in the Reservoir UHE Furnas-MG, using gills from Pimelodus maculatus (Lacepède, 1803) as a biomarker of environmental pollution. Ciência et Práxis, 1, 15–20.
Pacheco, M., & Santos, M. A. (2002). Biotransformation, genotoxic and histopathological effects of environmental contaminants in European eel (Anguilla anguilla L.). Ecotoxicology and Enviroronmental Safety, 53, 331–347.
Cetesb (São Paulo) (2009). Report on freshwater water quality of the state of São Paulo. São Paulo 538 p. (Ser technical reports). Available in http://www.cetesb.sp.gov.br/tecnologia-ambiental/laboratorios/61-publicacoes-e-relatorios---relatorios-de-qualidade in 14 February 2011.
Pfeiffer, W. C., Fiszman, M., Malm, O., & Azcue, J. M. (1986). Monitoring heavy metals pollution by the critical pathway analysis in the Paraíba do Sul River. Science of the Total Environment, 58, 73–79.
Poltronieri, C., Laurà, R., Bertotto, D., Negrato, E., Simontacchi, C., Guerrera, M. C., et al. (2009). Effects of exposure to overcrowding on rodlet cells of the teleost fish Dicentrarchus labrax (L.). Veterinary Research Communications, 33, 619–629.
Reis, A. B., Sant’Ana, D. M. G., Azevedo, J. F., Merlini, L. S., & Araújo, E. J. A. (2009). The influence of the aquatic environment in tanks sequentially interconnected with PVC pipes on the gill epithelium and lamellas of tilapia (Oreochromis niloticus). Pesquisa Veterinaria Brasileira, 29, 303–311.
Santos, A. F. G. N., Santos, L. N., & Araújo, F. G. (2004). Water level influences on body condition of Geophagus brasiliensis (Perciformes, Cichlidae) in a Brazilian oligotrophic reservoir. Neotropical Ichthyology, 2, 151–156.
Scrimgeour, G. J., Davidson, R. J., & Davidson, J. M. (1988). Recovery of benthic macroinvertebrate and epilithic communities following a large flood, in an unstable, braided, New Zealand river. New Zealand Journal of Marine and Freshwater Research, 22, 337–344.
Soares, M. S. S., Marinho, M. M., Huszar, V. L. M., Branco, C. W. C., & Azevedo, S. M. F. O. (2008). The effects of water retention time and watershed features on the limnology of two tropical reservoirs in Brazil. Lakes & Reservoir: Research and Management, 13, 257–269.
StatSoft, Inc. (2005). Statistica (data analysis software system), version 7.1. www.statsoft.com.
Talling, J. C., & Lemoalle, J. 1998. Ecological dynamics of tropical inland waters. Cambridge, UK: Cambridge University. 441pp.
Tietge, J. E., Johnson, R. D., & Bergman, H. L. (1988). Morphometric changes in gill secondary lamellae of brook trout (Salvelinus fontalis) after long-term exposure to acid and aluminum. Canadian Journal of Fisheries and Aquatic Sciences, 45, 1643–1648.
Tundisi, J. G., Matsumura-Tundisi, T., Pereira, K. C., Luzia, A. P., Passerini, M. D., Chiba, W. A. C., et al. (2010). Cold fronts and reservoir limnology: an integrated approach towards the ecological dynamics of freshwater ecosystems. Brazilian Journal of Biology, 70(3), 815–824.
Vannote, R. L., Minshall, G. W., Cummins, K. W., Sedell, J. R., & Gushing, E. (1980). The river continuum concept. Canadian Journal of Fisheries and Aquatic Sciences, 37, 130–137.
Acknowledgement
We thank Nathália das Neves Cardoso and Danielle Alcantara Vieira from the Laboratory of Histological Techniques, University Federal Rural of Rio de Janeiro, for helping in field and laboratory work. CNPq (Brazilian Research Funding Agency) and FAPERJ (Rio de Janeiro State Research Funding Agency) provided partial funding for Araújo.
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Gomes, I.D., Nascimento, A.A., Sales, A. et al. Can fish gill anomalies be used to assess water quality in freshwater Neotropical systems?. Environ Monit Assess 184, 5523–5531 (2012). https://doi.org/10.1007/s10661-011-2358-2
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DOI: https://doi.org/10.1007/s10661-011-2358-2