The effects of heavy metals on the incidence of morphological deformities in Chironomidae (Diptera)

Wanessa Deliberalli Rogério L. Cansian Albanin A. M. Pereira Rafael C. Loureiro Luiz U. Hepp Rozane M. Restello About the authors

ABSTRACT

Streams in urban areas are strongly impacted by the input of organic matter and metals, for instance copper (Cu) and zinc (Zn). These metals are essential for the aquatic biota, but when absorbed in excess they are toxic. In Chiro nomidae larvae, the deleterious effects of heavy metals can be ascertained by analyzing the morphological deformities of the larval mentum, a structure of the oral cavity. In this study, we evaluated I) the bioavailability of Cu and Zn in urban stream sediments and II) the relationship between Cu and Zn concentrations and the incidence of deformities in the mentum of Chironomus larvae. Chironomid flies were collected from four locations in two streams at an urban area in southern Brazil. They were identified and the incidence of deformities in the mentum was quantified. Sediment samples were collected at the same locations where larvae were collected, to quantify the bioavailable fractions of Cu and Zn. The concentrations of Cu in the sediment were similar between the collection sites. However, Zn concentrations varied among sites, being greater in the stretch directly influenced by the input of the organic waste. In total, 2,895 Chironomid larvae were collected. The incidence of deformities in the mentum was above 30% and was correlated with the concentrations of Cu (r = 0.68) and Zn (r = 0.87). This correlation indicates that the municipal waste that is thrown into the city’s streams has influenced the occurrence of deformities.

KEY WORDS:
Biomonitoring; copper; environmental quality; mentum; zinc

INTRODUCTION

Aquatic environments are among the most threatened natural resources of the world, since they are directly affected by what happens in their surroundings (Machado et al. 2015Machado NG, Nassarden DCS, Santos F, Boaventura ICG, Perrier G, Souza FSC, Martins EL, Biudes MS (2015) Chironomus larvae (Chironomidae: Diptera) as water quality indicators along an environmental gradient in a neotropical urban stream. Revista Ambiente e Água 10(2): 298-309. https://doi.org/10.4136/ambi-agua.1533
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). Among the many substances that contaminate rivers and lakes, heavy metals are critical. They are not biodegradable and can have long-term toxic effects (Mahlangeni et al. 2016Mahlangeni NT, Moodley R, Jonnalagadda SB (2016) Heavy metal distribution in Laportea peduncularis and growth soil from the eastern parts of KwaZulu-Natal, South Africa. Environmental Monitoring Assessment 188(2): 76. https://doi.org/10.1007/s10661-015-5044-y
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). Heavy metals in aquatic environments can originate from natural sources (e.g. weathering of rocks) or anthropogenic contamination (e.g. urban, industrial or agricultural waste) (Maldonado and Wendling 2009Maldonado ACD, Wendling B (2009) Manejo de ecossistemas aquáticos contaminados por Metais pesados. Revista Agropecuária Técnica 30(1): 21-32. http://periodicos.ufpb.br/index.php/at/article/view/3237 [Accessed: October 2016]
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). Among the waste generated by human activities, urban effluents may vary in their chemical composition, with a high load of organic matter, nutrients and metals (Baird 2002Baird C (2002) Química Ambiental. Editora Artmed, Porto Alegre, 622 pp.).

Metals are amongst the most common pollutants of aquatics ecosystems (Ali et al. 2013Ali Z, Malik RN, Qadir A (2013) Heavy metals distribution and risk assessment in soilsaffected by tannery effluents. Chemistry and Ecology 29(8): 646-692. https://doi.org/10.1080/02757540.2013.810728
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). When released into water bodies, can form ions. These ions either remain as suspended particles, or they settle in limnic sediments (Tuna et al. 2007Tuna AL, Yilmaz F, Demirak A, Ozdemir N (2007) Sources and distribution of trace metals in the Saricay stream basin of southwestern Turkey. Environmental Monitoring and Assessment 125(1-3): 47-57. https://doi.org/10.1007/s10661-006-9238-1
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), which act as a sink for heavy metals and other pollutants (Sharley et al. 2008Sharley DJ, Hoffmann AA, Pettigrove P (2008) Effects of sediment quality on macroinvertebrates in the Sunraysia region of the Murray-Darling Rivers, Australia. Environmental Pollution 156(3): 689-698. https://doi.org/10.1016/j.envpol.2008.06.014
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). After heavy rains, these metals are re-suspended in the water, contaminating the food chain, and adversely affecting the water column and water communities (Pitt 1995Pitt RE (1995) Effects of urban runoff on aquatic biota. In: Hoffmann DJ, Rattner BA, Burton GA Jr, Cairns J Jr (Eds) Handbook of Ecotoxicology. Lewis Publishers, Boca Raton, 609-630., Linnik and Zubenko 2000Linnik PM, Zubenko IB (2000) Role of bottom sediments in the secondary pollution of aquatic environments by heavy-metal compounds. Lakes and Reservoirs Research Management 5(1): 11-21. https://doi.org/10.1046/j.1440-1770.2000.00094.x
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, Simpson et al. 2005Simpson SL, Batley GE, Chariton AA, Stauber JL, King CK, Chapman JC, Hyne RV, Gale SA, Roach AC, Maher WA (2005) Handbook for Sediment Quality Assessment. CSIRO, Bangor, 126 pp.).

Copper (Cu) and zinc (Zn) are considered essential to aquatic organisms (Torres et al. 2008Torres AM, Barros PM, Campos GCS, Pinto E, Rajamani S, Sayre T, Colepicolo P (2008) Biochemical biomarkers in algae and marine pollution: a review. Ecotoxicology and Environmental Safety 71(1): 1-15. https://doi.org/10.1016/j.ecoenv.2008.05.009
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). However, they can become toxic when absorbed (e.g. food intake) and/or adsorbed (e.g. contact with contaminated water) in excess (Tüzen 2009Tüzen M (2009) Toxic and essential trace elemental contents in fish species from the Black Sea, Turkey. Food and Chemical Toxicology 47(8): 1785-1790. https://doi.org/10.1016/j.fct.2009.04.029
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). According to Magalhães et al. (2015Magalhães DP, Marques MRC, Baptista DF, Buss DF (2015) Metal bioavailability and toxicity in freshwater. Environmental Chemistry Letters 13(1): 68-87. https://doi.org/10.1007/s10311-015-0491-9
https://doi.org/10.1007/s10311-015-0491-...
), feeding is the main source of exposure to these metals. Large amounts of metal can cause physiological or morphological effects (Al-Shami et al. 2010Al-Shami S, Rawi CS, Nor SA, Ahmad AH, Ali A (2010) Morphological deformities in Chironomus spp. (Diptera: Chironomidae) larvae as a tool for impact assessment of anthropogenic and environmental stresses on three rivers in the Juru river system, Penang, Malaysia. Environmental Entomology 39(1): 210-222. https://doi.org/10.1603/EN09109
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, Planelló et al. 2013Planelló R, Servia MJ, Gomez-Sande P, Herrero O, Cobo F, Morcillo G (2013) Transcriptional Responses, Metabolic Activity and Mouthpart Deformities in Natural Populations of Chironomus riparius Larvae Exposed to Environmental Pollutants. Environmental Toxicology 30(4): 383-395. https://doi.org/10.1002/tox.21893
https://doi.org/10.1002/tox.21893...
).

The main morphological effects caused by metals in Diptera larvae are deformities in the mentum, a structure in the oral cavity of these immatures (Brinkhurst et al. 1968Brinkhurst RO, Hamilton AL, Herrington HB (1968) Components of the Botton Fauna of the St. Lawrence Great Lakes. Great Lakes Institute, University of Toronto, 33-50., Di Veroli eta al. 2012Di Veroli A, Selvaggi R, Goretti E (2012) Chironomid mouthpart deformities as indicator of environmental quality: a case study in Lake Trasimeno (Italy). Journal of Environmental Monitoring 14(5): 1473-1478. https://doi.org/10.1039/c2em10882h
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, Sensolo et al. 2012Sensolo D, Hepp LU, Decian VS, Restello RM (2012) Influence of landscape on assemblages of Chironomidae in Neotropical streams. Annales deLimnologie 48: 391-400. https://doi.org/10.1051/limn/2012031
https://doi.org/10.1051/limn/2012031...
). Larvae of Chironomus Meigen, 1804 (Diptera: Chironomidae) are very prone to heavy metal contamination for two reasons. First, they feed from detritus (Armitage 1995Armitage PD (1995) Behaviour and ecology of adults. In: Armitage PD, Cranston PS and Pinder LCV (Eds) The Chironomidae: Biology and Ecology of Non-Biting Midges. Champman and Hall, London, 194-224. https://doi.org/10.1007/978-94-011-0715-0_9
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); second, they remain in direct contact with the limnic sediment (Odume et al. 2012Odume ON, Muller WJ, Palmer CG, Arimoro FO (2012) Mentum deformities in Chironomidae communities as indicators of anthropogenic impacts in Swartkops River. Physics and Chemistry of the Earth 50: 140-148. https://doi.org/10.1016/j.pce.2012.08.005
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, Corbi and Froehlich 2010Corbi JJ, Froehlich CG (2010) Bioaccumulation of metals in aquatic insects of streams located in areas with sugar cane cultivation. Química Nova 33(3): 644-648. https://doi.org/10.1590/S0100-40422010000300030
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).

The cause of deformity in some Chironomidae is still complex and not fully understood. Some studies on the effect of heavy metals on the incidence of deformities in Chironomus have been conducted. In Malaysia, Al-Shami et al. (2010Al-Shami S, Rawi CS, Nor SA, Ahmad AH, Ali A (2010) Morphological deformities in Chironomus spp. (Diptera: Chironomidae) larvae as a tool for impact assessment of anthropogenic and environmental stresses on three rivers in the Juru river system, Penang, Malaysia. Environmental Entomology 39(1): 210-222. https://doi.org/10.1603/EN09109
https://doi.org/10.1603/EN09109...
) investigated the influence of agricultural, industrial and anthropogenic stressors on the incidence of deformities in Chironomidae. Di Veroli et al. (2014Di Veroli A, Santoro F, Pallottini M, Selvaggi R, Scardazza F, Cappelletti D, Goretti E (2014) Deformities of Chironomid larvae and heavy metal pollution: From laboratory to field studies. Chemosphere 11(2): 9-17. https://doi.org/10.1016/j.chemosphere.2014.03.053
https://doi.org/10.1016/j.chemosphere.20...
) documented the morphological deformities in Chironomus in a lake contaminated with heavy metals, including Cu and Zn. Žunić et al. (2015Žunić M, Živić I, Stanković M, Stojanović K, Marković Z (2015) Morphological deformities of mouthparts in genus Chironomus (Diptera: Chironomidae) induced by heavy metals. VII International Conference “Water & Fish”, Belgrade (Serbia), June 2015. Conference Proceedings, 540-544.) stated that Chironomus larvae exposed to high concentrations of Cu and Pb showed a higher rate of deformities. Some studies have reported that the percentages of changes in the oral cavity may range from zero to 8%, even when minimally impacted streams were analyzed (Warwick 1988Warwick WF (1988) Morphological deformities in Chironomidae (Diptera) larvae as biological indicators of toxic stress. In: Evans MS (Ed.) Toxic Contaminants and Ecossystem Health: a Great Lakes Focus. New York, Wiley and Sons, 281-320., Nazarova et al. 2004Nazarova LB, Riss WH, Kahlheber A, Werding B (2004) Some observations of buccal deformities in chironomid larvae (Diptera: Chironomidae) from the Ciénaga Grande de Santa Marta, Colombia. Caldasia 26(1): 275-290. http://www.jstor.org/stable/23641799
http://www.jstor.org/stable/23641799...
, Ochieng et al. 2008Ochieng H, Steveninck ES, Wanda FM (2008) Mouthparts deformities in Chironomidae (Diptera) as indicators of heavy metal pollution in northern Lake Victoria, Uganda. African Journal of Aquatic Science 33(2): 135-142. https://doi.org/10.2989/AJAS.2008.33.2.4.501
https://doi.org/10.2989/AJAS.2008.33.2.4...
).

In regions where urbanization is intense, water bodies are subject to human disturbances that change the quality of the water (Milesi et al. 2008Milesi SV, Biasi C, Restello RM, Hepp LU (2008) Efeito de metais sobre a comunidade de macroinvertebrados bentônicos em riachos do Sul do Brasil. Acta Scientiarum Biological Science (30)3: 283-289. https://doi.org/10.4025/actascibiolsci.v30i3.677
https://doi.org/10.4025/actascibiolsci.v...
). In this study, we evaluated I) the bioavailability of Cu and Zn in urban streams and II) the relationship between the concentration of these metals with the incidence of deformities in the mentum of Chironomus larvae. The following hypotheses were tested: I) the sites with the greatest influence of municipal waste will have higher bioavailable concentrations of Cu and Zn in the sediment and hence, II) in places with higher bioavailable concentrations of Cu and Zn there will be higher incidence of deformities in the mentum of Chironomus larvae.

MATERIAL AND METHODS

This study was conducted in streams located at the basin of the Tigre River in Erechim, southern Brazil (27°29’6” to 27°47’10”S, 52°21’33” to 52°08’43”W, Fig. 1). The local climate is classified as Cfb under Köppen’s classification, subtropical temperate. The annual average temperature is 17.6 °C and rainfall is well distributed throughout the year, with an average rainfall of 1912.3 mm (Alvares et al. 2013Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G (2013) Koppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22(6): 711-728. https://doi.org/10.1127/0941-2948/2013/0507
https://doi.org/10.1127/0941-2948/2013/0...
). The vegetation is characterized by a mixture of seasonal evergreen Araucaria forest and semi-deciduous forest (Oliveira-Filho et al. 2015Oliveira-Filho AT, Budke JC, Jarencow JA, Eisenlohr PV, Neves DRM (2015) Delving into the variations in tree species composition and richness across South American subtropical Atlantic and Pampean forests. Journal of Plant Ecology 8(3): 242-260. https://doi.org/10.1093/jpe/rtt058
https://doi.org/10.1093/jpe/rtt058...
). Urban use comprises 86% of the total area of the drainage area where the studied streams are situated (Budke et al. 2012Budke JC, Hepp LU, Decian VS, Zanin EM (2012) Influência dos usos da terra sobre a composição e funcionalidade de comunidades de macroinvertebrados bentônicos: integrando processos entre paisagens, interface ribeirinha e comunidades biológicas In: Santos JE, Zanin EM, Moschini LE (Eds) Faces da Polissemia da Paisagem: Ecologia, Planejamento e Percepção. RiMa, São Carlos, 311-322.).

Figure 1
Geographic location of the collection sites by the Tigre River, Erechim, RS, Brazil.

The collection sites were located within the boundaries of the city and were characterized as follows: the first site (P1) has riparian vegetation on both sides, extending to about 20 to 30 m. The bed is composed of stones, leaves and sand, with consistent water flow, facilitating oxygenation. The second site (P2) is located upstream of a housing complex. The waste generated by the houses is released directly into the riverbed. There is about 5 to 10 m of riparian vegetation on both banks, where the substrate is rocky. The third site (P3) is located about 2 km from P2 and its substrate is composed of rocks. The vegetation of the margin is low and there is a small community over the stretch. The fourth site (P4) is located about 4 km from P3. It has about 2 m of riparian vegetation on both banks, and a rocky substrate. On one of the banks there is a concrete factory. Every site at the river is shallow (some stretches reach 1 m, but most are <1 m deep).

Organisms were collected over four stretches of the streams (Fig. 1), between August and September 2015, using a Surber sampler (two sub-samples/stretch, mesh: 250 μm, area: 0.09 m2) and fixed in the field with 80% ethanol. For identification of larvae, semi-permanent slides with Hoyer solution (Trivinho-Strixino and Strixino 1995Trivinho-Strixino S, Strixino G (1995) Larvas de Chironomidae (Diptera) do estado de São Paulo: Guia de identificação de diagnose dos gêneros. Departamento de Hidrobiologia, Laboratório de Entomologia Aquática, Universidade Federal de São Carlos, São Carlos , 229 pp.) were made for observation of the organisms in optical microscopy with 1000x magnification. Identification to genus level was done using key of the Trivinho-Strixino (2011Trivinho-Strixino S (2011) Larvas de Chironomidae: Guia de identificação. Universidade Federal de São Carlos, São Carlos, 371 pp.).

The incidence of deformities in the mentum of Chironomus larvae for each sample collected was analyzed. The larvae that had deformities of the mentum were separated and photographed to better visualize abrasions, additions or deletions in their teeth. We considered any change in the normal pattern of the mentum, such as wear, addition, fusion and absence of teeth (Sanseverino and Nessimian 2008Sanseverino AM, Nessimian JL (2008) Assimetria flutuante de organismos aquáticos e sua aplicação para avaliação de impactos ambientais. Oecologia Brasiliensis 12(3): 382-405. https://doi.org/10.4257/oeco.2008.1203.03
https://doi.org/10.4257/oeco.2008.1203.0...
) as deformities. The identified bodies were listed and deposited in the Benthic Invertebrate Collection of MuRAU (Regional Museum of the Alto Uruguay) URI Campus de Erechim.

To characterize the quality of the water at the stretches studied, some physical-chemical characteristics of the water and sediment were measured. Throughout the four sites, some abiotic variables were also measured. The following variables were quantified: water temperature, turbidity, electrical conductivity, total dissolved solids, pH and dissolved oxygen with a multiparameter analyser (Horiba® U50). Water samples for the concentration analysis of total organic carbon and total nitrogen in total organic carbon fixer with a nitrogen detector TOC-VCSH (Shimadzu) were collected. The methods for the analysis of these parameters are described in APHA (1998APHA (1998) Standard methods for the examination of water. American Public Health Association, Water Environmental Federation, Washington, DC, 20th ed., 1180 pp.).

In each stretch, we collected sediment samples with a corer sampler (70 mm diameter) at a depth of 5 to 10 cm. In the laboratory, we dried the samples in an oven (60 °C/48 h) and sifted them (62 μm mesh) to separate the grain size fraction intended for the extraction of metals. The potentially bioavailable fraction of Cu and Zn in the sediment was extracted from 0.5 g of sediment and 10 mL of HCl 0.1 mol L-1 for 24 h at room temperature (20 ± 2 °C). Subsequently, the samples were filtered in 25 mL volumetric flask and the total volume was measured with HNO3 1 mol L-1. The metals were quantified by atomic absorption spectrophotometry on an atomic absorption spectrophotometer (Varian AA55).

To verify the incidence of deformities in organisms, we calculated the percentage of larvae with a deformed mentum. To verify the differences between the abiotic variables along the sampling sections, we used a Repeated Measures Analysis of Variance (RM-ANOVA) followed by a posteriori Tukey test (p < 0.05). To evaluate the relationship between Cu and Zn concentration in the sediment and the incidence of deformities in the larvae, we used Pearson’s linear correlation analysis. The deformity percentage values and the concentrations of the obtained metals were transformed into log (x+1) to avoid distortions caused by outliers and homogenization of the variances. The analyses were conducted using the BioEstat 5.3 program (Ayres et al. 2007Ayres M, Ayres-Júnior M, Ayres DL, Santos AA (2007) BIOESTAT: Aplicações estatísticas nas áreas das ciências bio-médicas. Ong Mamiraua, Belém, 364 pp.).

RESULTS

The average water temperature was 15.7 ± 2.6 °C. The pH was slightly acidic (5.9 ± 1.1) and the water was well-oxygenated (10.4 ± 2.3 mg L-1). The electrical conductivity (F(3,11) = 40.6, p < 0.001), turbidity (F(3,11) = 23.1, p < 0.001), total dissolved solids (F(3,11) = 41.2, p < 0.001) and total nitrogen (F(3,11) = 297.1, p <0.001) differed among the collection sites. The electrical conductivity, total dissolved solids and total nitrogen presented higher values in the downstream sections (P3 and P4), while turbidity was higher only in P3 (Table 1). The pH and percentage of organic matter in the sediment differed between the sites (F(3,11) = 23.9, p < 0.001; F(3,11) = 19.8, p < 0.001, respectively) (Table 1). The pH was higher in P1 (8.8 ± 0.1), while the organic matter (61.1 ± 10.2) was higher in P3.

Table 1
Mean and standard deviation of abiotic variables in four stretches of the River Tigre, Erechim, Rio Grande do Sul.

The bioavailable concentrations of Cu in the sediment were similar between the collection sites (F(3,11) = 1.9, p = 0.17). On the other hand, the bioavailable concentrations of Zn varied between sites (F(3,11) = 45.4, p < 0.001), with P2 being the site with the highest concentration (115 ± 6.9 mg kg-1, Fig. 2).

Figure 2
Zinc concentration (mean ± standard error) and copper at the collection sites of Tigre River, Erechim, RS, Brazil.

In total, 2895 Chironomus larvae were sampled. Site P3 had a greater count of organisms (62.5% of the total, 1808 organisms) followed by site P4 (32.1%, 930 organisms). Of the total number of larvae identified, 881 (30.4%) had deformities of the mentum (Figs 3-6). The majority of deformities observed were by attrition and deletion of the mentum.

Figures 3-6
Deformities in the mentum of Chironomus (oral cavity): (3) standard mentum; (4) deformed mentum (deletion of teeth); (5) deformed mentum (addition of teeth); (6) deformed mentum (tooth wear).

Sites P3 and P4 were the sites with the highest percentage of larvae with deformity of the mentum (31.8% and 31.7%, respectively). The concentrations of Cu and Zn were positively correlated with the incidence of such deformities in Chironomus larvae. The relationship between deformities and Zn concentrations was greater than that of Cu concentrations (r = 0.87, p < 0.001; r = 0.68, p = 0.03, respectively) (Figs 7-8).

Figures 7-8
Pearson’s linear correlation between Copper (7) and zinc (8) concentrations and the incidence of deformities in the mentum of Chironomus (oral cavity) Chironomus.

DISCUSSION

The electrical conductivity, turbidity and total dissolved solids varied among the collection sites. Urban effluents are significant sources of chlorides in the water surface, which influence the variation in electrical conductivity (Santos 2010Santos VO (2010) Análise físico-química da água do Rio Itapetininga-SP: Comparação entre dois pontos. Revista Eletrônica de Biologia 3(1): 99-115. http://revistas.pucsp.br/index.php/reb/article/view/7
http://revistas.pucsp.br/index.php/reb/a...
, Hepp et al. 2013Hepp LU, Restello RM, Milesi, SV, Biasi C, Molozzi J (2013) Distribution of aquatic insects in urban headwater streams. Acta Limnologica Brasiliensia 25(1): 1-9. https://doi.org/10.1590/S2179-975X2013005000014
https://doi.org/10.1590/S2179-975X201300...
). Similarly, as solids dissolved in water indicate the presence of salts, a correlation between dissolved solids and electrical conductivity is expected (Porto et al. 1991Porto MFA, Branco SM, Luca SJ (1991) Caracterização e alterações da qualidade da água. In: Porto RL (Ed.) Hidrologia Ambiental. São Paulo, Editora da Universidade de São Paulo, Associação Brasileira de Recursos Hídricos, 27-66.). Moreover, in places with large suspended matter, colloids and dissolved and particulate organic matter (which can be generated by urban environments), the water tends to be significantly turbid (Medeiros et al. 2015Medeiros PRP, Cavalcante GH, Magalhães EMM (2015) Comportamento da turbidez e material em suspensão, em um rio com vazão regularizada por sistema de barragens em cascata: Rio São Francisco (NE, Brasil). Geochimica Brasiliensis 29(1): 35-44. https://doi.org/10.21715/gb.v29i1.415
https://doi.org/10.21715/gb.v29i1.415...
). The variation of these variables indicates a contamination gradient of the water body (spring-mouth).

P1 is situated in a small vegetation fragment, which ensures that the aquatic environment is somewhat protected (Hepp et al. 2010Hepp LU, Milesi SV, Biasi C, Restello RM (2010) Effects of agricultural and urban impacts on macroinvertebrates assemblages in streams (Rio Grande do Sul, Brazil). Revista Brasileira de Zoologia 27(1): 106-113. https://doi.org/10.1590/S1984-46702010000100016
https://doi.org/10.1590/S1984-4670201000...
, Miserendino et al. 2011Miserendino ML, Casaux R, Archangelsky M, Di Prinzio CY, Brand C, Kutschker AM (2011) Assessing land-use effects on water quality, in-stream habitat, riparian ecosystems and biodiversity in Patagonian northwest streams. Science of The Total Environment 409(1): 612-624. https://doi.org/10.1016/j.scitotenv.2010.10.034
https://doi.org/10.1016/j.scitotenv.2010...
). In addition, its drainage area does not have any source of organic matter of anthropogenic origin. Riparian vegetation does not always guarantee water quality if there is a source of contamination at the site. The great problem of urban water bodies lies in the fact that they receive domestic waste in natura (Hepp et al. 2013Hepp LU, Restello RM, Milesi, SV, Biasi C, Molozzi J (2013) Distribution of aquatic insects in urban headwater streams. Acta Limnologica Brasiliensia 25(1): 1-9. https://doi.org/10.1590/S2179-975X2013005000014
https://doi.org/10.1590/S2179-975X201300...
). In this case, the domestic effluents are dumped directly into the river under study, since in P2 there is an upstream housing complex, which explains the high concentrations of Zn.

High concentrations of organic matter are fundamental for metals to bind, which is of great relevance for their transfer into biological systems (Campbell et al. 1988Campbell PGC, Lewis AG, Champman PM, Crowder AA, Fletcher WK, Imber B, Lumosa SN, Stokes PM, Winfrey M (1988) Biologically available metals in sediments. National Research Council Canada, Conseil National de Recherches Canada, Ottawa, 298 pp.). In our study, we observed that increased concentrations of organic matter were positively associated with Cu concentrations.

Although the concentration of Zn did not increase in the nascent-mouth direction of the stream, the sites with the greatest influence of urban waste (P2 and P3) presented the highest concentrations of Zn, corroborating our first hypothesis.

The incidence of deformities in the mentum if Chironomus was positively correlated with the concentrations of Cu and Zn, thus corroborating our second hypothesis.

Chemical compounds can accumulate in the sediment and are the main cause of morphological alterations in the mentum of Chironomus larvae (Macdonald and Taylor 2006Macdonald EE, Taylor BR (2006) Incidence of mentum deformities in midge larvae (Diptera: Chironomidae) from Northern Nova Scotia, Canada. Hydrobiologia 563(1): 277-287. https://doi.org/10.1007/s10750-006-0012-8
https://doi.org/10.1007/s10750-006-0012-...
), making these immatures suitable indicators of water quality (Janssens and Gerhardt 2003Janssens BL, Gerhardt A (2003) Chironomidae (Diptera, Nematocera) fauna in three small streams of Skania, Sweden. Environmental Monitoring and Assessment 83: 89-102. https://doi.org/10.1023/A:1022494222666
https://doi.org/10.1023/A:1022494222666...
, Ochieng et al. 2008Ochieng H, Steveninck ES, Wanda FM (2008) Mouthparts deformities in Chironomidae (Diptera) as indicators of heavy metal pollution in northern Lake Victoria, Uganda. African Journal of Aquatic Science 33(2): 135-142. https://doi.org/10.2989/AJAS.2008.33.2.4.501
https://doi.org/10.2989/AJAS.2008.33.2.4...
).

Some studies have reported that the oral cavity of Chironomus larvae may present changes in up to 8% of the individuals even in minimally impacted streams (Warwick 1988Warwick WF (1988) Morphological deformities in Chironomidae (Diptera) larvae as biological indicators of toxic stress. In: Evans MS (Ed.) Toxic Contaminants and Ecossystem Health: a Great Lakes Focus. New York, Wiley and Sons, 281-320., Ochieng et al. 2008Ochieng H, Steveninck ES, Wanda FM (2008) Mouthparts deformities in Chironomidae (Diptera) as indicators of heavy metal pollution in northern Lake Victoria, Uganda. African Journal of Aquatic Science 33(2): 135-142. https://doi.org/10.2989/AJAS.2008.33.2.4.501
https://doi.org/10.2989/AJAS.2008.33.2.4...
). This is considered normal and is a consequence of the natural wear and tear caused by the dietary habits of these larvae. In this study, we observed more than 30% of the larvae with deformities in the mentum (wear, deletion and extra teeth). This high percentage of deformed larvae (four times more than expected from natural wear) is indicative of the effect of chemical stressors dissolved in the water. According to Wiederholm (1984Wiederholm T (1984) Incidence of deformed Chironomid larvae (Diptera: Chironomidae) in Swedish lakes. Hydrobiologia 109(3): 243-249. https://doi.org/10.1007/BF00007742
https://doi.org/10.1007/BF00007742...
) and Odume et al. (2012Odume ON, Muller WJ, Palmer CG, Arimoro FO (2012) Mentum deformities in Chironomidae communities as indicators of anthropogenic impacts in Swartkops River. Physics and Chemistry of the Earth 50: 140-148. https://doi.org/10.1016/j.pce.2012.08.005
https://doi.org/10.1016/j.pce.2012.08.00...
), in heavily polluted environments, 30-40% of Chironomidae larvae present deformities in their mouth parts. Martinez et al. (2002Martinez EA, Moore BC, Schaumloffel J, Dasgupta N (2002) The potential association between menta deformities and trace elements in Chironomidae (Diptera) taken from a heavy metal contaminated river. Archives of Environmental Contamination and Toxicology 42(3): 286-291. https://doi.org/10.1007/s00244-001-0190-0
https://doi.org/10.1007/s00244-001-0190-...
) found that 3.8% to 10.3% of Chironomus larvae presented morphological deformities associated with sediments impacted with high levels of Cd, Cu, Pb and Zn. Biasi and Restello (2010Biasi C, Restello RM (2010) Incidência de deformidades morfológicas em larvas de Chironomidae (Insecta: Diptera) como ferramenta de avaliação da qualidade de água em riachos de Erechim - RS. Vivências 6: 136-148. http://www.reitoria.uri.br/~vivencias/Numero_009/artigos/artigos_vivencias_09/n9_ic4.pdf [Accessed: 12/11/2016]
http://www.reitoria.uri.br/~vivencias/Nu...
) observed 12.2% of Chironomus larvae with deformities in the mentum.

The high incidence of deformities in larvae collected at sites P3 and P4 is directly correlated with the high concentrations of Cu and Zn. Organisms exposed to a stressor (e.g. metals) may have their adaptive responses suppressed to the extent that it decreases their chances of survival (Karouna-Renier and Zehr 2003Karouna-Renier NK, Zehr JP (2003) Short-term exposures to chronically toxic copper concentrations induce HSP70 proteins in midge larvae (Chironomus tentans). Science of The Total Environment 312(1): 267-272. https://doi.org/10.1016/S0048-9697(03)00254-7
https://doi.org/10.1016/S0048-9697(03)00...
). High levels of incidence of deformities at site P3 and site P4 may be directly related to environmental stressors, such as the high concentrations of metals in the sediment.

In conclusion, our study indicates that the presence of Cu and Zn from the deposition of waste from urban environments causes deterioration in the quality of water and the sediment of streams, thus increasing the incidence of deformities in Chironomidae. Although we did not observe variations in the concentrations of Cu between the sections, the high incidence of deformities may be caused by this metal in the presence of certain components. As the relationship between Zn concentrations and the incidence of deformities was higher, we are led to believe that the association of Cu and Zn enhances the negative effects of the release of organic residues on aquatic organisms. Another important conclusion of our study is related to the observed morphological effects. Most studies on the use of bioindicators of water quality have indicated that environmental degradation affects aquatic populations and communities. In this study, we showed that the morphological and physiological structure of organisms is impacted, resulting in even greater damage to aquatic communities. Therefore, the use of biological assessment approaches, such as studies of morphological variations in the presence of pollutants, are excellent tools for assessing the health of aquatic environments, serving as important information for water resource management.

ACKNOWLEDGEMENTS

We thank the team of the Laboratory of Biomonitoring of URI Erechim, for the help in the chemical analyses. WD received a scholarship from the PIIC/URI Program. RCL received a scholarship from the PROSUP/CAPES Program.RMR received financial support from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq process 409685/2016-0).

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Publication Notes

  • Available online (first publication):

    April 23, 2018
  • Zoobank Register:

    http://zoobank.org/9CE10538-6D74-4D93-9626-EFB27ABDA130
  • Publisher:

    © 2018 Sociedade Brasileira de Zoologia. Published by Pensoft Publishers at https://zoologia.pensoft.net

Publication Dates

  • Publication in this collection
    28 May 2018
  • Date of issue
    2018

History

  • Received
    03 Apr 2017
  • Reviewed
    12 June 2017
  • Accepted
    18 June 2017
  • Published
    23 Apr 2018
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