Introduction

Industrial effluent discharge comprises one of the most significant pollution sources in fresh waters because the release of chemicals in rivers is often done without previous treatment (Rajaram & Das, 2008). In between the discharge and the deposition into river sediments, many compounds can bind with other particles and undergo chemical changes that may, in turn, enhance or decrease their toxicity. Numerous chemicals are also incorporated into the aquatic food webs via benthic organisms (Araujo, Zagatto, & Bertoletti, 2006).

Benthic macroinvertebrates are organisms that offer useful information for water quality assessments, providing data on past and present environmental conditions (Pratt & Coler, 1976). This is possible because impacts can change invertebrate community structure and composition, and also modify their vital functions. The evaluation of the environmental quality of an ecosystem requires information on abiotic and biotic attributes related to ecosystem functioning (Silva, Galvíncio, & Almeida, 2010).

Aquatic insect larvae are the most abundant and diverse benthic macroinvertebrates in running waters (Hynes, 1970; Lake, 1990). Their distribution is related to habitat physical, chemical and structural characteristics, as well as to food resource availability and to the habits of each species (Resh & Rosenberg, 1984; Boltovskoy, Tell, & Dadon, 1995; Merrit & Cummins, 1996). Aquatic insects are used to detect environmental disturbance for presenting low mobility and high abundance, besides being relatively easy to sample and identify, features that make them good candidates to compose biotic indices for water quality assessments (Roque & Trivinho-Strixino, 2000; Queiroz, Trivinho-Strixino, & Nascimento, 2000).

Currently, aquatic environments are undergoing continuous change due to natural disasters, abusive degradation, and overexploitation by human activities. As a result, researchers and organizations have been pursuing strategies for their recovery (Lopes & Pacagnan, 2014). Thus, this study and identification of bentonic macroinvertebrates in the Coutinho River will make possible to ascertain the environmental quality of this environment and to identify possible environmental problems caused by industrial effluent discharges, since the river may be used in the future district (Secretaria Estadual de Meio Ambiente [Sema], 2008).

Material and methods

Study area

The Coutinho River is located in Guarapuava city, Paraná State, Brazil (Figure 1) and its source is placed in the Palmeirinha district. It presents alluvial soil and is affluent of the right margin of the Jordão basin, which is inserted in the Médio Iguaçu tributary hydrographic unit (Paraná, 2006). The riparian zone was largely replaced by agricultural areas, except for a few fragment remnants of native Mixed Ombrophilous Forest, and the river is also surrounded by an industrial hub near the urban area of Guarapuava (Sema, 2008).

The Paraná State is the fastest growing Brazilian state in industrial production (Instituto Paranaense de Desenvolvimento Econômico e Social [Ipardes], 2018). The Guarapuava city industrial hub includes timber exploitation, machinery, packages, and furniture production, the last with 40 industries (Grzeszczeszyn & Machado, 2010). The chemicals in effluents that industries launch into rivers can kill several organisms and can also be harmful to the local population when heavy rainfall and floods occur (Buss & Vitorino, 2010).

Samplings

Three sampling points (Figure 1) were established along the Coutinho River according to their position relative to the industrial effluent discharge site: one upstream (P1) 25º 19' 47" S and 51º 29' 41" W), by the PR 460 road, the other (P2) (25º 21' 5" S and 51º 30' 45" W) nearby, and the third (P3) (25º 22' 58" S and 51º 35' 5" W) downstream, by the BR 277 road (Figure 1).

The three points were sampled in September/2013, November/2013, January/2014, and March/2014. In each sampling occasion, water physical and chemical parameters measured included temperature, pH, turbidity, phosphate, and dissolved oxygen. Water analyses were performed at the Novatec Analysis Center of the Universidade Estadual do Centro-Oeste (Unicentro). Sediment and benthic macroinvertebrates were collected with three throws of a Petersen dredge (0.02 m² area) in each point. Sediment composition was classified according to the Wentworth (1922) granulometric scale.

Samples were washed at the lab using sieves of 1 and 250 mm mesh size. Macroinvertebrates retained in the sieves were kept in 70% ethanol solution, sorted, and identified to the lowest taxonomic level possible with the specific keys: Merritt and Cummins (1984); Roldan-Pérez (1988); Trivinho-Strixino, and Strixino (1995); Epler (2001); Fernandez and Dominguez (2001); Costa, Souza, and Oldrini (2004); Lecci and Froehlich (2007).

Data analyses

The structure of the community of benthic macroinvertebrates was evaluated using density values (Welch, 1948) and the diversity indices of Shannon-Wiener (H’) and equitability Pielou (J). These indices were calculated using the Dives 3.0 software (Rodrigues, 2014).

We applied two visual assessment protocols to characterize environmental and ecological attributes of river reaches, one by Hannaford, Barbour, and Resh (1997) and the other by Ohio Environmental Protection Agency (EPA, 1987), both modified by Callisto, Ferreira, Moreno, Goulart, and Petrucio (2002).We then applied the Biological Monitoring Working Party (BMWP) biotic index, adapted by Loyola (2000), to evaluate the water quality of the Coutinho River. This index attributes scores for each taxon based on their tolerance to organic impacts. The BMWP-ASPT (Average Score Per Taxon) was calculated by dividing the BMWP result by the number of scored families in the sample (Walley & Hawkes, 1997). Finally, we applied the Family Biotic Index (FBI), which attributes values of tolerance to organic pollution for macroinvertebrate families, to verify water pollution levels (Hilsenhoff, 1987).

A Canonical Correspondence Analysis (CCA) was performed in the PAST program (Hammer, Harper, & Ryan, 2001), to verify if there were links between the environmental variables and the macroinvertebrates sampled at each point.

Results and discussion

The application of habitat assessment protocols evidenced that the three Coutinho River reaches (P1 = 45 points; P2 = 50 points; P3 = 46 points) were altered by anthropogenic actions that led to habitat disruption along the river, such as deforestation by agricultural enterprises. Although the three reaches were classified accordingly, the P2 reach received the highest score (50 points) and evidenced local degradation. According to Dudgeon (1996), the suppression of the riparian forest decreases the reproductive success of aquatic and semi-aquatic species that need appropriate sites for mating and laying eggs.

The water quality results (Table 1) revealed that the dissolved oxygen, pH, and turbidity values were the lowest at the P2 reach, which is located near the effluent discharge site of the industrial area of Guarapuava. The lowest phosphate concentration (0.1 mg L^-1) was found in P3. Temperature varied little among sampling points, and turbidity was the highest at P1 (Table 1).

All pH values registered were below six, evidencing an acidified environment. According to Siqueira et al. (2012), pH can influence species distribution and biological interactions by hindering the performance of the physiology of aquatic organisms.

The National Council of Environment (Conselho Nacional do Meio Ambiente [Conama], 2005) establishes minimum Dissolved Oxygen (DO) values of 5 mg L^-1 for Class II water bodies. However, only the P1 reach was within this limit (Table 1), being the P2 (1.85 mg L^-1) and the P3 (3.35 mg L^-1) below minimum quality. Sperling (2005) states that DO concentration can indicate pollution effects of organic wastes in freshwaters: when DO values range between 4 and 5 mg L^-1, sensitive fish species die out; when DO is 2 mg L^-1, nearly all fish species die out, and when DO drops to 0 mg L^-1, anaerobic conditions take place.

Phosphate values of P2 and P3 were within the range pre-established by Conama (2005) (i.e, ≤ 0.1 mg L^-1). Values of P1 were above this limit (0.16 mg L^-1), likely due to agricultural runoff from adjacent areas, which may include phosphate and organophosphate fertilizers.

Sediment evaluation revealed that the P2 presented, on average, the highest percentage of sand (85.1%), followed by P3 (83.7%) and P1 (81.9%). Finer sediment as clay and silt were less representative, being the highest average value registered at P1 (18.1%) (Figure 2). The sediment granulometry can be indicative of anthropic actions that cause siltation and change the physical nature of sediments in lotic ecosystems, consequently influencing the benthic fauna (Bryce, Lomnicky, & Kaufmann, 2010).

Fifteen taxa were identified (Table 2), being Oligochaeta and Chironomidae the most abundant. These two taxa are considered resistant and tolerant to environmental impacts, likely because they present morphological adaptions and generalist habits that allow their survival in oxygen-poor environments (Merrit & Cummins, 1996). Oligochaetes represented 100% of the benthic community assemblage of P3 (September/2013 and January/2014). The presence of Oligochaeta indicates the existence of organic matter in the environment and poor water quality (Bruno et al., 2012; Kamada, De-Lucca, & De-Lucca, 2012).

Chironomidae are generally found in sediments with decaying organic matter (Amorim & Castillo, 2009) and therefore have the characteristic of being tolerant to variations in the aquatic environment. The Chironomus midge represented 74% of the macroinvertebrate fauna of P1 in January/2014, 76% of the P2 fauna in January/2014, and 71% in March/2014. Chironomus is related to water degradation, as it is abundant in eutrophic places, besides supporting low values of dissolved oxygen in the environment (Trivinho-Strixino & Strixino, 1995; Ceretti & Nocentini, 1996; Marques, Ferreira, & Barbosa, 1999).

The P1 reach presented the highest taxonomic richness (10 taxa in September/2013) and the orders Ephemeroptera (3%) and Trichoptera (3%) were exclusive to P1. According to Rosenberg and Resh (1993), insects of these orders are ecologically important for environmental assessments in lotic ecosystems for their sensitivity to disturbances and occurrence in good-quality waters. In this context, their occurrence in P1 was likely associated with the higher levels of dissolved oxygen observed therein.

Hirudinea and Bivalvia also presented high relative abundance. The highest relative abundance of bivalve mollusks (80%) was found in P1 in March/2014, and that of Hirudinea (60%) was found in P2 in September and November/2013. The presence of these organisms is favored in environments with high levels of organic pollution (Barnes, 1984; Amorim & Castillo, 2009; Rodrigues, 2013; Bruno et al., 2012).

The high density of the few taxa observed in the Coutinho River (Figure 3), along with low overall richness, indicate degradation. In P1, the Chironomus presented the highest density observed, with 161 ind. m^-2 (January/2013), followed by Oligochaeta, with 89 ind. m^-2 (November/2013) and Bivalvia, with 50 ind. m^-2(September/2013). In P2, Chironomus (128 ind. m^-2 in March/2014) and Hirudinea (39 ind. m^-2 in March/2014) were the most abundant, whereas in P3 the highest density registered was that of Oligochaeta, with 27 ind. m^-2 in March/2014.

The P1 reach presented the highest diversity (H' = 0.78), equitability (J = 0.70) and richness (S = 13 taxa), while the P3 presented the lowest values for these metrics. The equitability values differed in all sampling points, indicating taxa dominance. Moreover, these metrics tended to decrease along the river continuum, from P1 to P3 (Table 3), as observed for water physical and chemical parameters as well, indicating increased environmental degradation from P2 onwards.

Based on the FBI scores, the three sites of the Coutinho River were classified as presenting poor water quality and significant organic pollution. The BMWP and BMWP-ASP indices showed differences among reaches, being the P1 classified as polluted (BMWP) or with moderate pollution (BMWP-ASPT), and the P2 and P3 classified as strongly polluted (BMWP), or with severe pollution (BMWP-ASPT). Ruaro, Agustini, and Orssatto (2010) obtained similar values for the Clarito River, in the state of Paraná, which also receives pollution from industrial sources along its course. In São Paulo State, the Pequerê River of Cubatão city also underwent degradation and riparian forest removal, being classified as presenting very poor water quality (Amorim & Castillo, 2009). On the other hand, the preserved riparian cover of the Correntoso River (Aquidauana, State Mato Grosso do Sul) ensured all sampling points presented good water quality results of biotic indices (FBI, BMWP, and BMWP-ASPT) (Silva, Favero, Sabino, & Garnés, 2011).

The CCA between the physicochemical parameters of the water and the macroinvertebrates present in the Coutinho River (Figure 4, axis 1 - 79.8 and axis 2 - 20.2%) at three sampling points showed a possible association of Oligochaeta with increased turbidity levels. This group usually lives in environments with high electrical conductivity and turbidity (Alves, Marchese, & Escarpinati, 2006; Gorni & Alves, 2015).

Conclusion

The use of benthic macroinvertebrates for the Coutinho River environmental quality assessment was efficient and enabled the diagnostic of local limnological variations. Our results indicate that the sampled reaches are impacted by both agricultural runoff from adjacent areas and industrial effluent discharges. Evidence includes the higher taxonomic richness found upstream from the industrial area together with the high density of tolerant taxa (as Oligochaeta and Chironomus) downstream from it.

All biotic indices (FBI, BMWP, and BMWP-ASPT) point to moderate-towards-severe pollution along the Coutinho River. Thus, our results should serve as an environmental degradation warning and a call for continuous monitoring of the Coutinho River water quality and impact mitigation actions.

References

Alves, R. G., Marchese, M. R., & Escarpinati, S. C. (2006). Oligochaeta (Annelida, Clitellata) in lotic environments in the State of São Paulo, Brazil. Iheringia, 96(4), 431-435. doi: 10.1590/S0073-47212006000400007

Amorim, A. C. F., & Castillo, A. R. (2009). Macroinvertebrados bentônicos como bioindicadores da qualidade da água do baixo Rio Perequê, Cubatão, São Paulo, Brasil. Biodiversidade Pampeana, 7(1), 16-22.

Araujo, R. P. A., Zagatto, P. A., & Bertoletti, E. (2006). Avaliação da qualidade de sedimentos. In P. A. Zagatto, & E. Bertoletti (Eds.), Ecotoxicologia aquática – princípios e aplicações (p. 69-286). São Carlos, SP: RiMa.

Barnes, R. D. (1984). Zoologia dos invertebrados (4a ed.). São Paulo, SP: Roca.

Boltovskoy, D., Tell, G., & Dadon, R. (1995). Afinidad entre comunidades bentônicas de un ambiente lótico. In E. C. Lopretto, & G. Tell (Eds.), Ecosistemas de águas continentales: metodologias para su estudio (p. 203-214). Buenos Aires, AR: Sur. Tomo I.

Bruno, C. G. C., Batista, J. E., Souza, J. R., Paula, S. M., Brito, B. A., Camelo, F. R. B., & Jacobucci, G. B. (2012). Comparação entre a eficiência de amostragem de dois tipos de substratos artificiais instalados em córregos do Cerrado. Revista Brasileira de Zoociência, 14(1-3), 123-134.

Bryce, S. A., Lomnicky, G. A., & Kaufmann, P. R. (2010). Protecting sediment-sensitive aquatic species in mountain streams through the application of biologically based streambed sediment criteria. Journal of the North American Benthological Society, 29(2), 657-672. doi: 10.1899/09-061.1

Buss, D. F., & Vitorino, A. S. (2010). Rapid bio assessment protocols using benthic macroinvertebrates in Brazil: evaluation of taxonomic sufficiency. Journal of the North American Benthological Society, 29(2), 562-571. doi: 10.1899/09-095.1

Callisto, M., Ferreira, W. R., Moreno, P., Goulart, M., & Petrucio, M. (2002). Aplicação de um protocolo de avaliação rápida da diversidade de habitats em atividades de ensino e pesquisa (MG-RJ). Acta Limnologica Brasiliensia, 14(1), 91-98.

Ceretti, G., & Nocentini, A. M. (1996). Notes on the distribution of some macrobenthonic populations (Oligochaeta and Diptera Chironomidae) in the littoral of a few small lakes in northern Italy. Memorie dell´Istituto Italiano di Idrobiologia dott Marco de Marchi, 54, 109-124.

Conselho Nacional do Meio Ambiente [Conama]. (2005). Resolução Conama n. 357 de 17 de março de 2005. Brasília, DF: Conama.

Costa, J. M., Souza, L. O. I., & Oldrini, B. B. (2004). Chave para identificação das famílias e gêneros das larvas conhecidas de Odonata do Brasil: Comentários e registros bibliográficos (Insecta, Odonata). Publicações Avulsas do Museu Nacional, 99, 3-42.

Dudgeon, D. (1996). Anthropogenic influences on Hong Kong streams. GeoJournal, 40(1-2), 53-61. doi: 10.1007/BF00222531

Epler, J. H. (2001). Identification manual for the larval Chironomidae (Diptera) of North and South Carolina. Raleigh, NC: Department of Environmental and Natural Resources – Division of Water Quality.

Fernandez, H. R., & Dominguez, E. (2001). Guía para la determinación de los artrópodos bentônicos sudamericanos. Buenos Aires, AR: Universidad Nacional de Tucumán.

Gorni, G. R., & Alves, R. G. (2015). Influência de variáveis ambientais sobre a comunidade de oligoquetos (Annelida: Clitellata) em um córrego neotropical. Biotemas, 28(1), 59-66. doi: 10.5007/2175-7925.2015v28n1p59

Grzeszczeszyn, G., & Machado, H. P. V. (2010). Políticas públicas para o desenvolvimento local: o caso de fomento às indústrias de móveis de Guarapuava, Paraná. Interações, 11(1), 81-92. doi: 10.1590/S1518-70122010000100008

Hammer, Ø., Harper, D. A. T., & Ryan, P. D. (2001). PAST - Palaeontological statistics software package for education and data analysis. Palaeontologia Electronica, 4(1), 1-9.

Hannaford, M. J., Barbour, M. T., & Resh, V. H. (1997). Training reduces observer variability in visual – based assessments of stream habitat. Journal of the North American Benthological Society, 16(4), 853-860. doi: 10.2307/1468176

Hilsenhoff, W. L. (1987). An improved index of organic pollution. The Great Lakes Entomologist, 20(1), 31-39.

Hynes, H. B. N. (1970). The ecology of running waters. Liverpool, GB: Liverpool University Press.

Instituto Paranaense de Desenvolvimento Econômico e Social [Ipardes]. (2018). Indústria do Paraná fecha o ano com crescimento acima de 5%. Recovered from: http://www.ipardes.gov.br/index.php?pg_conteudo=1&cod_noticia=908

Kamada, M. D. L., De-Lucca, G. M., & De-Lucca, J. V. (2012). Utilização dos macroinvertebrados bentônicos como indicadores da qualidade da água no córrego Retiro Saudoso, em Ribeirão Preto – SP. Periódico Eletrônico Fórum Ambiental da Alta Paulista, 8(2), 250-261. doi: 10.17271/19800827822012256

Lake, P. S. (1990). Disturbing hard and soft bottom communities: a comparison of marine and freshwater environments. Australian Journal of Ecology, 15(4), 477-488. doi: 10.1111/j.1442-9993.1990.tb01472.x.

Lecci, L. S., & Froehlich, C. G. (2007). Plecoptera. In C. G. Froehlich (Org.), Guia online: identificação de larvas de insetos aquáticos do Estado de São Paulo (p. 1-10). Recovered on June, 8, 2014, from http://sites.ffclrp.usp.br/ /aguadoce/guiaonline

Lopes, V. N., & Pacagnan, M. N. (2014). Marketing verde e práticas socioambientais nas indústrias do Paraná. Revista de Administração, 49(1), 116-128. doi: 10.5700/rausp1135

Loyola, R. G. N. (2000). Atual estágio do IAP no uso de índices biológicos de qualidade. In V Simpósio de Ecossistemas Brasileiros de Conservação (p. 46-52). São Paulo, SP: Aciesp.

Marques, M. G. S. M., Ferreira, R. L., & Barbosa, F. A. R. (1999). A comunidade de macroinvertebrados aquáticos e características limnológicas das lagoas Carioca e da Barra, Parque Estadual do rio Doce, MG. Revista Brasileira de Biologia, 59(2), 203-210. doi: 10.1590/S0034-71081999000200004

Merrit, R. W., & Cummins, K. W. (1984). An introduction to the aquatic insects of North America (2nd ed.). Dubuque, IA: Kendall Hunt Publishing.

Merrit, R. W., & Cummins, K. W. (1996). An introduction to the aquatic insects of North America (3rd ed.). Dubuque, IA: Kendall Hunt Publishing.

Ohio Environmental Protection Agency [EPA]. (1987). Biological criteria for the protection of aquatic life: User’s manual for biological field assessment of Ohio surface waters (Vol. II). Columbus, OH: Division of water quality monitoring and assessment.

Paraná. (2006). Resolução n. 49 CERH/PR, de 20 de dezembro de 2006. Dispõe sobre a instituição de regiões hidrográficas, bacias hidrográficas e unidades hidrográficas de gerenciamento de recursos hídricos do estado do Paraná. Curitiba, PR: Diário Oficial do Estado.

Pratt, J. M., & Coler, R. A. (1976). A procedure for the routine biological evaluation of urban runoff in small rivers. Water Research, 10(11), 1019-1025. doi: 10.1016/0043-1354(76)90083-X

Queiroz, J. F., Trivinho-Strixino, S., & Nascimento, V. M. C. (2000). Organismos bentônicos bioindicadores de qualidade de água da bacia do médio São Francisco. Embrapa Meio Ambiente, 3, 1-4.

Rajaram, T., & Das, A. (2008). Water pollution by industrial effluents in India: discharge scenarios and case for participatory ecosystem specific local regulation. Futures, 40(1), 56-59. doi: 10.1016/j.futures.2007.06.002

Resh, V., & Rosenberg, D. (1984). The ecology of aquatic insects. New York, NY: Praeger.

Rodrigues, V. C. R. (2013). Rio Fervença: efeitos da perturbação no ecossistema (Dissertação de Mestrado). Escola Superior Agrária de Bragança, São Paulo, SP.

Rodrigues, W. C. (2014). DivES – diversidade de espécies. Versão 3.0. Software e guia do usuário. Recovered from http://www.ebras.vbweb.com.br

Roldan-Pérez, G. R. (1988). Guía para el estudo de los macroinvertebrados acuáticos del Departamento de Antioquia. Medelín, CO: Universidade de Antioquia.

Roque, F. O., & Trivinho-Strixino, S. (2000). Avaliação preliminar da qualidade da água dos córregos do município de Luiz Antônio (SP) utilizando macroinvertebrados bentônicos como bioindicadores: subsídios para o monitoramento ambiental. Ciências Biológicas e do Ambiente, 2(1), 21-34.

Rosenberg, D. M., & Resh, V. H. (1993). Introduction to freshwater biomonitoring and benthic macroinvertebrates. In D. M. Rosenberg, & V. H. Resh (Eds.), Fresh water biomonitoring and benthic macroinvertebrates (p. 1-9). New York, NY: Chapman & Hall.

Ruaro, R., Agustini, M. A. B., & Orssatto, F. (2010). Avaliação da qualidade da água do rio Clarito no município de Cascavel (PR), através do índice BMWP adaptado. SaBios - Revista de Saúde e Biologia, 5(1), 5-12.

Secretaria Estadual de Meio Ambiente [SEMA]. (2008). Bacia hidrográfica do rio Jordão fase 1 – diagnóstico. Curitiba, PR: Sema.

Silva, D. F., Galvíncio, J. D., & Almeida, H. R. R. C. (2010). Variabilidade da qualidade de água na Bacia Hidrográfica do Rio São Francisco e atividades antrópicas relacionadas. Qualit@s Revista Eletrônica, 9(3), 1-17. doi: 10.18391/qualitas.v9i3.687

Silva, F. H., Favero, S., Sabino, J., & Garnés, J. A. (2011). Índices bióticos para avaliação da qualidade ambiental em trechos do rio Correntoso, Pantanal do Negro, Estado do Mato Grosso do Sul, Brasil. Acta Scientiarum. Biological Sciences, 33(3), 289-299. doi: 10.4025/actascibiolsci.v33i3.1478

Siqueira, T., Bini, L. M., Roque, F. O., Marques, C. S. R., Trivinho-Strixino, S., & Cottenie, K. (2012). Common and rare species respond to similar niche processes in macroinvertebrate metacommunities. Ecography, 35(2), 183-192. doi: 10.1111/j.1600-0587.2011.06875

Sperling, M. V. (2005). Introdução à qualidade das águas e ao tratamento de esgotos (3 ed.). Belo Horizonte, MG: Universidade Federal de Minas Gerais.

Trivinho-Strixino, S., & Strixino, G. (1995). Larvas de Chironomidae (Diptera) do Estado de São Paulo: guia de identificação de diagnose dos gêneros. São Carlos, SP: Universidade Federal de São Carlos.

Walley, W. J., & Hawkes, H. A. (1997). A computer-based development of the Biological Monitoring Working Party score system incorporating abundance rating, site type and indicator value. Water Research, 31(2), 201-210. doi: 10.1016/S0043-1354(96)00249-7

Welch, P. S. (1948). Limnological methods. Philadelphia, PA: Blakiston Co.

Wentworth, C. K. (1922). An scale of grade and class terms for clastic sediments. Journal of Geology, 30(5), 377-392.