Aquatic Macroinvertebrate Community Structure Affected by Chromium Contamination in the Monte Alegre Stream (SP): a Historical Comparative Case Study)

Abstract

In 2001, 150 tons of tannery waste was incorporated in the soil as a source of organic matter on the Monte Alegre Farm. This waste, which originates from the tannery industry and contains high chromium concentrations, was irregularly used as a soil fertilizer by farmers to produce mangoes, sugarcane, coffee, oranges, corn and lemons, contaminating the soils. This irregular application of tannery waste also contaminated stream sediment and bioaccumulated in some aquatic macroinvertebrate. The present study aims to collect current information about the aquatic macroinvertebrate community to make a comparison between chromium contamination in the Monte Alegre stream sediment with a study carried out in 2007 in the same place. The aquatic macroinvertebrate community was collected from April to September 2017 using an Ekman-Birge grab at two sampling points: one point at the forested area (Upstream Point) and another near the place of the contaminated soil (Downstream Point). Sediment samples were collected to analyze chromium concentration. The current concentration of chromium in the downstream point (impacted area) was higher than that obtained in 2007. The community metrics confirm that the taxonomic structure and diversity of the aquatic macroinvertebrate community to the Monte Alegre stream were affected by chromium. The results suggest that the environmental impact was maintained after ten years.

Keywords:
tannery waste; community indexes; contamination; aquatic invertebrates; metal

HIGHLIGHTS

• We evaluated the influence of chromium contamination on water quality in ten years.

• Aquatic macroinvertebrate community structure was influenced by land use.

• The area impacted by chromium showed lower macroinvertebrate richness and diversity.

• There were better environmental conditions in 2007 when compared to 2017.

INTRODUCTION

Pollution of aquatic ecosystems by metals has aroused interest in terms of the effects on the environment and aquatic biota [¹-³]. Once adsorbed to the sediment, metals can become bioavailable to the water column, affect aquatic biota and be transferred along the food chain [⁴]. They can also bioaccumulate in toxic concentrations to organisms and cause changes in their structure and distribution [⁵-⁷], interfere with growth, development, reproduction, DNA biosynthesis and even cause mortality [⁸,⁹]. In the aquatic environment, the sediment represents a compartment responsible for metal accumulation [¹⁰].

The aquatic macroinvertebrate community is essential for freshwater ecosystems as they act in ecological processes of nutrient cycling and energy transfer in the environment [¹¹]. These individuals represent the ecological diversity of the environment and can respond to impacts of human activities and have been used as water quality bioindicators and biomonitoring of environmental conditions [¹²-¹⁵]. The presence of copper and zinc from the deposition of urban waste was related to increasing the incidence mentum deformities in Chironomidae [¹⁶]. In another study, aquatic macroinvertebrates as bioindicators were used to detect metal pollution in the Brazilian Cerrado streams [⁶].

On the Monte Alegre farm, located in the municipality of Bueno de Andrada, State of São Paulo, approximately 150 tons of leather waste was disposed of in the soil as a source of organic matter. Near this region, several industries that produced leather gloves irregularly discarded leather shaving waste in the settlement soil, where sugarcane, mangoes, lemons, oranges, tangerines, corn and legumes were grown, which are a source of livelihood for families and commercialization in the region. This discard caused not only soil contamination but also contamination of the aquatic biota and sediment of the Monte Alegre stream, located close to the settlement [¹⁷].

In the study conducted by Santos and coauthors [¹⁷], concentrations of chromium were detected in the soil on the Monte Alegre (SP) farm totaling 30.93 and 55.85 mg kg^-1 in the sugarcane cultivation areas and 40.2 and 567.2 mg kg^-1 in the contaminated soil. This impact led to the accumulation of chromium in the sediment and consequent changes in the aquatic macroinvertebrate community structure of the Monte Alegre (SP) stream, causing a reduction in species diversity and richness in the chromium contaminated area [¹⁸].

Thus, it is believed that chromium contamination can still affect the aquatic macroinvertebrate community of the Monte Alegre stream and that the chromium concentration would decrease over time. Based on this hypothesis, the present study aimed to carry out a historical comparative study 10 years after the study conducted by Corbi and coauthors [¹⁸]. The aim was to analyze the chromium concentrations in the sediment in the Monte Alegre stream and the impacts on the richness and taxonomic diversity of the macroinvertebrate community.

MATERIAL AND METHODS

Study area

The present study was developed in the Monte Alegre stream, located on the Monte Alegre farm, in the municipality of Bueno de Andrada, State of São Paulo, Brazil (Figure 1). The Monte Alegre stream is the low order, it has a has water velocity of 2.0 m s^-1, a depth of 0.8 m, a width of 1.5 m and is located at about 570m altitude, within in the Cerrado area.

Two sampling points were selected close to the collection points in the study by Corbi and coauthors [¹⁸]. Point one was established as the reference (Upstream) and is located above the point of chromium contamination in the coordinates within closed and preserved forest. The other point (Downstream) is located close to the contaminated area by chromium in the coordinates. This point is influenced by agriculture and the presence of the settlement. Sediments and stream macroinvertebrates were collected in two periods, April and September 2017.

Figure 1
Location of the sampling points (Upstream and Downstream) in the Monte Alegre stream (Google Earth, 2021).

Physical and chemical characterization

The physical and chemical water variables of pH, temperature, dissolved oxygen, and electrical conductivity of the water were measured in situ using the Yellow Springs multimeter, model 556, only once period (September 2017).

Sediments for chromium and organic matter analysis were sampled using a standard Ekman-Birge grab (standard area of 225 cm²) in two periods (April and September 2017). Sediment samples (about 2.0 g) for the chromium determination were oven dried at 65 ºC and digested with nitric acid (HNO₃) at 90 ºC on a hot plate [¹⁹]. The solutions of metal were analyzed by atomic absorption spectrophotometry. The organic matter of the sediments was analyzed, in triplicate, by mass loss on ignition (550 ºC, 4 hours) [²⁰].

Community sampling

The aquatic macroinvertebrate community was collected, in triplicate, in two periods, April and September 2017, using an Ekman-Birge grab (standard area of ​​225 cm²). The samples were placed in plastic pots, sent to the laboratory, and then washed in a 0.250 mm mesh sieve. The organisms were selected on a transilluminated tray and fixed in 70% alcohol for taxonomic identification at the family level, based on the keys available from [²¹-²²].

Data analysis

To verify the difference in chromium and organic matter concentrations between the two sampled points, the Kruskal-Wallis test was applied using the PAST Program. The stream macroinvertebrates were analyzed by the participation of each taxonomic group and by the total organisms collected in each sampled point. The following parameters were determined for the macroinvertebrates: Margalef richness index; Shannon diversity index; %EPT (Ephemeroptera, Plecoptera and Trichoptera); EPT/total of families X 100; EPT/Chironomidae X 100; Chironomidae/total X 100; BMWP Biotic Index (Biological Monitoring Working Party) and IBB Biotic Index (Belgian Biotic Index) based on [²³]. To determine the richness index (Margalef) and the diversity index (Shannon), the PAST program (Paleontological Statistics) was used [²⁴]. Afterwards, the results of the present study were compared with the results obtained by Corbi and coauthors [¹⁸].

RESULTS

Physical and chemical characterization

The temperature varied from 19.5 to 21.5ºC. The upstream point showed acidic pH (6.72) and the downstream point was within the tolerable limits for most fauna and flora, which is 5.0 to 9.0 [²⁵]. The dissolved oxygen was low in the two sampled points, varied from 2.3 mg L^-1 to the upstream point and from 0.6 mg L^-1 to the downstream point. The decomposition process of dead organic matter may be related to low concentrations, as chemical processes and anaerobic respiration require a high demand for dissolved oxygen to occur [²⁶]. The low concentration of the downstream point which is related to the characteristics of the location, has stagnant water and low turbulence. The electrical conductivity of the impacted area (338 μS cm^-1) was higher than reference area (22 μS cm^-1).

The organic matter was low, ranging from 17.3% (upstream point) to 31.9% (downstream point). Statistical tests show a significant difference between the two areas (p<0.05). Chromium was detected in higher concentrations in the impacted area, confirming the results obtained in 2011 [¹⁸]. In the reference area, the chromium concentration was 29.62 mg kg^-1 and in the impacted area it was 38.42 mg kg^-1 (Table 1). The Kruskal-Wallis test showed no significant difference between the reference and impacted areas (p value 0.35).

Table 1
Comparison of chromium concentrations in the sediment of the Monte Alegre stream analyzed by the present study and by Corbi and coauthors [¹⁸] for the points equivalent to the reference area and the area impacted by chromium.

	Chromium concentrations (mg.kg-1)
	Present study*	Corbi and coauthors (2011)**
Upstream	29.6 ± 1.5	8.0 - 10.9
Downstream	38.4 ± 11.3	30.1 - 32.4

• *Values averages. ** Minimum and maximum values for the period of study

Aquatic macroinvertebrate community

In this study, a total of 333 organisms were observed, distributed into 12 families (Table 2). The most representative family was Chironomidae (Diptera), found in the two sampled points. The reference area showed greater richness and diversity of families compared to impacted area. The Trichoptera and Ephemeroptera orders had abundance only in the reference area, with the occurrence of the families Leptoceridae, Calamoceratidae and Leptophlebiidae. In impacted area, there were no organisms of these orders and the Ceratopogonidae and Chironomidae families were the most prevalent. In both areas, the presence of the Libellulidae, Ceratopogonidae, Tipulidae, Chironomidae and Oligochaeta families was observed.

Table 2
Macroinvertebrate community of the Monte Alegre stream analyzed for the points equivalent to the reference area (Upstream) and the area impacted by chromium (Downstream)

Taxonomic Group	Upstream	Downstream
Coleoptera
Elmidae	-	2
Syrtidae	1	-
Diptera
Ceratopogonidae	79	20
Chironomidae	138	3
Simuliidae	1	-
Tipulidae	3	1
Ephemeroptera
Leptophlebiidae	1	-
Odonata
Coenagrionidae	5	-
Gomphidae	1	-
Libellulidae	13	2
Oligochaeta	42	1
Trichoptera
Calamoceratidae	14	-
Leptoceridae	6	-
TOTAL	304	29

Concerning community metrics and biotic indexes (Table 3), the upstream point was the one with the largest number of families (11) and downstream point was the smallest, with only 5 families. The Shannon Diversity index and Margalef richness index were higher than the upstream point. The percentage of EPT represented 7% at the upstream point, while at the other point, no such organisms were found. For the ratio of the number of EPT families to the total family and of EPT for Chironomidae, the values ​​of 25 and 0.05 were found, respectively, for the upstream point and zero for the downstream point, due to the absence of organisms in the EPT group. The presence of Chironomidae represented 45% at the upstream point and 10% at the downstream point. The water quality classification for the upstream point was good and moderately polluted for the BMWP index and the IBB index, respectively. On the other hand, the water quality at the downstream point was classified as very poor (BMWP Index) and poor (IBB).

In general, the reference point presented better environmental conditions, such as greater richness and diversity of organisms and good water quality. On the other hand, the community metrics showed evidence of environmental impacts in the downstream point.

Table 3
Comparison of community metrics of the Monte Alegre stream analyzed by the present study and by Corbi and coauthors [¹⁸] for the points equivalent to the reference area and the area impacted by chromium

	Present study1		Corbi and coauthors [18] 1
Community metrics	Upstream	Downstream	Upstream	Downstream
Number of families	11	5	16	15
Dominance	0.15	0.49	0.15	0.20
Shannon Diversity index	2.24	1.16	2.3	2.0
Margalef Richness index	3.50	1.78	3.3	2.9
EPT (%)	7	0	15	16
(Family number EPT/total family) x 100	27	0	32	26
(EPT/Chironomidae) x 100	0.050	0	68	42
(Chironomidae/total) x 100	45	10	25	40
Biotic Index BMWP2	68 (Good)	23 (Very poor)	87 (excellent)	69 (good)
Biotic Index IBB2	5 (Moderately polluted)	4 (Poor)	7 (good)	5 (Moderately polluted)

• ¹
  The sampling methods between the present study and the one Corbi and coauthors (2011) were different and should be analyse with caution [¹⁸]. The present study used an Ekman-Birge grab, Corbi and coauthors (2011) used a D-frame to collect the macroinvertebrates [¹⁸].
• ²
  Water quality classification based on [²³].

DISCUSSION

Our results showed that chromium is still accumulated in the sediment of the Monte Alegre stream after ten years. Studies conducted in sugarcane growing areas have also shown the persistence of chromium in sediments over several years [²⁷]. In streams adjacent to banana plantations, chromium accumulation in sediment was identified, with concentrations ranging from 0.99 mg kg^-1 to 28.99 mg kg^-1 [²⁹]. Concentrations between 45.0 and 161.0 mg kg^-1 were detected in urban occupation areas [³⁰].

The current concentration of chromium in the downstream point (impacted area) was higher than that obtained in 2007. It is known that the occurrence of chromium may also be related to agriculture and waste and sewage deposition [²⁸]. At the downstream point, some plantations and areas occupied by the residents of the settlement were observed, which may have contributed to the increase in chromium concentrations at this point. Note that in this point, the oxygen concentration was very low, the water had low turbulence and there was no presence of EPT, which contributed to the deterioration of the environmental quality of the stream in relation to the upstream point.

The presence of metals in the environment can also cause damage to the aquatic biota. The community metrics confirm that the taxonomic structure and diversity of the aquatic macroinvertebrate community to the Monte Alegre stream were affected by chromium. It can be observed that the section near the chromium contamination point showed less diversity and richness of organisms, showing the sensitivity of some organisms, such as the EPT group, to survive in environmental stress conditions. The Chironomidae community structure and the distribution of richness of EPT species was influenced by exposure to sugarcane and banana plantations [³¹, ³²]. Exposure of Chironomidae larvae to hexavalent chromium and copper showed that these metals significantly affected the endogenous composition of the host bacterium community [³³]. In another study, reproduction and survival of Daphnia magna were affected by exposure to sediments from areas near tanneries [³⁴].

Comparing the current results of the aquatic macroinvertebrate community with the results obtained in 2007, it can be observed that after ten years, the ecological conditions of the stream of the impacted area did not improve due to exposure to chromium. There was an increase in chromium concentrations in the sediment. Although the present study used different methods of sampling the aquatic macroinvertebrate community, results suggest that the environmental impact was maintained after ten years.

Acknowledgments

We are grateful to the National Council for Scientific and Technological Development (CNPq) for financing this research.

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• Funding:

  This research received no external funding.

Edited by

Editor-in-Chief:

Alexandre Rasi Aoki

Associate Editor:

Marcos Pileggi

Publication Dates

• Publication in this collection
  24 Mar 2023
• Date of issue
  2023

History

• Received
  17 Feb 2022
• Accepted
  04 July 2022