Research Article |
Corresponding author: Rozane M. Restello ( rrozane@uricer.edu.br ) Academic editor: Carolina Arruda Freire
© 2018 Wanesssa Deliberalli, Rogerio L. Cansian, Albanin A. Mielniczki Pereira, Rafael Chaves Loureiro, Luiz Ubiratan Hepp, Rozane M. Restello.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Deliberalli W, Cansian RL, Mielniczki Pereira AM, Loureiro RC, Hepp LU, Restello RM (2018) The effects of heavy metals on the incidence of morphological deformities in Chironomidae (Diptera). Zoologia 35: 1-7. https://doi.org/10.3897/zoologia.35.e12947
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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 Chironomidae 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.
Biomonitoring, copper, environmental quality, mentum, zinc
Aquatic environments are among the most threatened natural resources of the world, since they are directly affected by what happens in their surroundings (
Metals are amongst the most common pollutants of aquatics ecosystems (
Copper (Cu) and zinc (Zn) are considered essential to aquatic organisms (
The main morphological effects caused by metals in Diptera larvae are deformities in the mentum, a structure in the oral cavity of these immatures (
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,
In regions where urbanization is intense, water bodies are subject to human disturbances that change the quality of the water (
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.
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.
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 (
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
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 (
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
Mean and standard deviation of abiotic variables in four stretches of the River Tigre, Erechim, Rio Grande do Sul.
P1 | P2 | P3 | P4 | |
---|---|---|---|---|
Water temp. (°C) | 16.8 ± 3.5ª | 16.3 ± 2.7ª | 15.9 ± 2.7ª | 15.4 ± 3.2ª |
DO (mg L-1) nnn | 11.5 ± 1.8ª | 8.8 ± 2.9ª | 10.6 ± 2.6ª | 10.4 ± 2.6ª |
pH water | 6.4 ± 0.5ª | 5.5 ± 1.8ª | 5.4 ± 1.5ª | 6.3 ± 0.1ª |
Turbidity (UNT) | 6.9 ± 4.8b | 3.4 ± 1.8b | 17.2 ± 4.2ª | 2.9 ± 0.5b |
EC (mS cm-1) | 0.07 ± 0.01b | 0.16 ± 0.02ª | 0.19 ± 0.04ª | 0.23 ± 0.02ª |
TDS (mg L-1) | 0.04 ± 0.01b | 0.10 ± 0.01ª | 0.12 ± 0.03ª | 0.15 ± 0.01ª |
TOC (mg L-1) | 17.3 ± 1.4ª | 18.5 ± 13.6ª | 19.1 ± 12.6ª | 20.1 ± 1.9ª |
TN (mg L-1) | 2.9 ± 0.2ª | 7.9 ± 0.4b | 9.6 ± 0.8c | 10.1 ± 0.3c |
pH sediment | 8.807 ± 0.11ª | 8.607 ± 0.08b | 8.417 ± 0.07ª,b,c | 7.97 ± 035b,c |
OM (%) | 44.91 ± 2.27ª | 32.65 ± 11.14ª | 61.09 ± 10.21b | 28.35 ± 2.43c |
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.
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
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
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 (
P1 is situated in a small vegetation fragment, which ensures that the aquatic environment is somewhat protected (
High concentrations of organic matter are fundamental for metals to bind, which is of great relevance for their transfer into biological systems (
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 (
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 (
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 (
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.
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).