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0126-2807 Alfonds Andrew Maramis and Agustinus Ignatius Kristijanto, 2012. Heavy Metals Accumulated by ISSN Paragyractis Sp.

and Hydropsyche Sp. in Kreo River Adjacent to Jatibarang Landfill, Semarang, Indonesia. Volume 7, Number 2: 115-124, June, 2012 T2012 Department of Environmental Engineering Sepuluh Nopember Institute of Technology, Surabaya & Indonesian Society of Sanitary and Environmental Engineers, Jakarta Open Access http://www.trisanita.org/jases
International peer-reviewed journal

This work is licensed under the Creative Commons Attribution 3.0 Unported License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Research Paper

HEAVY METALS ACCUMULATED BY PARAGYRACTIS SP. AND HYDROPSYCHE SP. IN KREO RIVER ADJACENT TO JATIBARANG LANDFILL, SEMARANG, INDONESIA
ALFONDS ANDREW MARAMIS1* and AGUSTINUS IGNATIUS KRISTIJANTO2
of Biology, Faculty of Mathematcis and Natural Sciences, State University of Manado (UNIMA), Campus UNIMA at Tondano, Minahasa, 95618, North of Sulawesi, Indonesia. 2Department of Chemistry, Sciences and Mathematics Faculty, Satya Wacana Christian University, Jl. Diponegoro No. 52-60, Salatiga, 50711, Central of Java, Indonesia.
*Corresponding Author: Phone: +62-431-3306127; E-mail: alfondsmaramis@yahoo.com Received: 9th March 2012; Revised: 20th April 2012; Accepted: 20th April 2012
1Department

Abstract: Benthic macroinvertebrates can accumulate pollutants such as heavy metals from water and sediment of a river. These studies aims to identify the differences in concentration of Cd, Zn, Cu, and Fe in Paragyractis sp. (Insecta: Lepidoptera) and Hydropsyche sp. (Insecta: Trichoptera) that live in Kreo River, before and after the Jatibarang landfill leachate discharge. Another aim was to find out the differences of these metals bioaccumulation factor of two benthic from its environment. To obtain the aims, benthic samples were collected at four stations on the Kreo River. The first station located next to 150 m upstream from the point of discharge of leachate. The second, third, and fourth station respectively to be about 1, 500, and 3000 m downstream from the point. All the samples were analyzed by HACH DREL 2000 spectrophotometer in order to determine the total amounts of Cd, Zn, Cu, and Fe. Bioaccumulation factors (BAF) calculated based on the ratio between heavy metal content in benthic with the metals concentration from their environment. The results showed that the landfill leachate quite a role in increasing the concentrations of heavy metals (except Cu) in Hydropsyche sp., but did not cause increased in Paragyractis sp. Both benthic BAF showed a similar pattern based on the type of environment phase. Metals BAF of Hydropsyche sp. and Paragyractis sp. from water that is sorted from highest to lowest as follows: Cu > Zn > Fe > Cd, while the sediment is: Zn > Cu > Cd > Fe.
Keywords: Benthic macroinvertebrate, heavy metals, bioaccumulation factor, Jatibarang landfill, leachate

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Alfonds Andrew Maramis and Agustinus Ignatius Kristijanto, 2012. Heavy Metals Accumulated by Paragyractis Sp. and Hydropsyche Sp. in Kreo River Adjacent to Jatibarang Landfill, Semarang, Indonesia.

INTRODUCTION Heavy metals can enter into the water bodies of the river through geogenic or anthropogenic processes [1]. Geogenic processes such as changes in the natural cycle of the earth's crust (weathering of rocks and volcanic eruptions), contributes significantly to the entry of heavy metals into the environment [2]. Anthropogenically, heavy metals enter the environment through the process of mining, industrial activity, vehicle fuel emissions, etc.[3]-[5]. Heavy metals have been described as an environmental pollutant when present in quantities causing harmful effects to living organisms in the ecological system [6]. One of the main sources of heavy metal pollution in the environment is landfill leachate. Leachate carries suspended and dissolved materials that are the product of waste degradation [7]. Leachate contains a number of heavy metals in high concentrations [8]. Some studies have reported the effects of heavy metals contained in the leachate to the biotic community of a river [9]-[11]. Benthic macroinvertebrates can accumulate pollutants such as heavy metals from water and sediment of a river. The rate of heavy metals accumulation in benthic macroinvertebrates could represent the level of pollution from the place where these benthic taken [12]. Response of benthic macroinvertebrates to heavy metal contamination has become a major concern because of its function as an indicator of ecological damage. Mechanism of metal tolerance in general have been understood, but expression of these metals on benthic macroinvertebrates and its significance to the effects at the population and community level still can not be determined [13]-[14]. According to Cain and his colleagues [13], which causes differences in bioaccumulation and toxicity of heavy metals between species with one another is the difference in physiological and biochemical processes of each species. Some species may limit bioaccumulation of some heavy metals through absorption and release, thus the species can maintain intracellular metal concentrations in the lower level and to effectively prevent metal poisoning. However, there are many species that are not capable of regulating the bioaccumulation of various types of heavy metals. Buchwalter and Luoma [15] added that a wide variety of physiological and morphological characteristics consistent with a broad taxonomic diversity of aquatic insects. Most of this variation is related to the evolutionary history of insects as secondary aquatic organisms. The total bioaccumulated metal concentration in any organism that is a net accumulator of the metal is informative about metal bioavailability summed across exposure routes. However, there is typically no one universal metal concentration that is indicative of toxicity, especially across species, largely because of interspecies differences in detoxification [14]. The level of bioaccumulation of heavy metals can be determined through calculation of the bioaccumulation factors. Bioaccumulation factor of heavy metal of a species is the ratio between the concentrations of heavy metals in the body of the species with the concentration of heavy metals in the environment where the species was settled [16]. Based on this background, these studies aims to identify differences in concentration of heavy metals (Cd, Zn, Cu and Fe) in Paragyractis sp. (Insecta: Lepidoptera) and Hydropsyche sp. (Insecta: Trichoptera) that live in Kreo River, before and after the Jatibarang landfill leachate discharge. Another aim was to find out the differences of each heavy metals (Cd, Zn, Cu and Fe) bioaccumulation factor of these two benthic macroinvertebrates from its environment (both water and sediment). MATERIALS AND METHODS Site of interest The study area is located in Semarang City, Central of Java (Figure 1). In this city, lies the Kreo River, which originates from Ungaran Mountain, Ungaran Regency [17], flows through 116
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Alfonds Andrew Maramis and Agustinus Ignatius Kristijanto, 2012. Heavy Metals Accumulated by Paragyractis Sp. and Hydropsyche Sp. in Kreo River Adjacent to Jatibarang Landfill, Semarang, Indonesia.

Mijen, Ngaliyan and Gunungpati Subdistricts and emptying into Garang River [18]-[19]. In the lower reaches of Sungai Garang, after joining with the Kreo River, there lies the Regional Water Company of Semarang City [17]. The Kreo, with its catchment area of about 66,60 km2, included in the group of big rivers that flow in Semarang City [20]. On the one side of Kreo River, exactly in the Kedungpane Village, Mijen Subdistrict, there lies Jatibarang landfill (Figure 2). Jatibarang landfill, which is a waste storage site of Semarang resident, has a width of about 460.183 m2 [21]. Waste management of Jatibarang landfill initially use sanitary landfill system, then transformed into an open dumping as a consequence of the ratio of waste disposed volume and storage capacity that was not proportional. The waste storage process produces landfill leachate which seeps in the ground and flowing on the surface soil (landfill runoff). Leachate that flowing on the surface of the soil, enters the shelter pool and then forwarded to the water bodies of Kreo River [22].

Fig. 1: Map of Central Java Province, scale 1:3.000.000 [18]

Fig. 2: Map of the Mijen, Ngaliyan and Gunungpati Subdistricts in Semarang City that separated by the Kreo River, scale 1:65.000 [18]. This map shows the four sampling stations on Kreo River. 117
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Alfonds Andrew Maramis and Agustinus Ignatius Kristijanto, 2012. Heavy Metals Accumulated by Paragyractis Sp. and Hydropsyche Sp. in Kreo River Adjacent to Jatibarang Landfill, Semarang, Indonesia.

Design of the research Experiment to achieve the first goal of the research was designed using randomized block design with the independent variable is the spatial factor (sampling station) and the dependent variable is the concentration of heavy metals (Cd, Zn, Cu and Fe) accumulated by the benthic macroinvertebrate (Paragyractis sp. and Hydropsyche sp.). Benthic macroinvertebrates sampling conducted at four stations (Figure 2). The first station located approximately 150 m upstream from the point of Jatibarang landfill leachate discharge. The second, third, and fourth station respectively to be about 1, 500, and 3000 m downstream from the point of leachate discharge. This research was conducted from September to October 2004, right at the transition between dry and rainy seasons. Experiment to achieve the second goal was also designed using randomized block design with the independent variable is the type of heavy metals and the dependent variable is the heavy metals bioaccumulation factor of benthic macroinvertebrates (Paragyractis sp. and Hydropsyche sp.) from its environment (both water and sediment). Replications for each determination of the dependent variable (both the first and second experiments) performed seven times, once a week as a temporal factor [23]. Benthic macroinvertebrates sampling Samples of benthic macroinvertebrate were taken using modified sampler box that placed on the surface of substratum of the river opposite direction to the flow of rivers. Furthermore, the area of substratum in the box sampler slowly crushed with fingers. Benthic macroinvertebrate that enter into the container of the sampler box is moved to the polyethylene plastic. Then, 10 drops of 0.4% formalin solution was added to the polyethylene plastic [24][25]. Benthic macroinvertebrate then identified using a set of determination tools, such as a stereo microscope, magnifying glass, and books of determination [26]-[29]. Paragyractis sp. and Hydropsyche sp. benthic were separated from the overall benthic collected, for the determination of heavy metals content. Both species were selected as the object of this study because its body-mass that relatively high compared to the other species. Sample handling and heavy metals determination All collected Paragyractis sp. and Hydropsyche sp. were dried in the oven at 105 0C for 24 h. The samples were then homogenized by hand grinding in a mortar. Sample amounts of 100 mg were transferred in a agate vessel and digested with 10 mL of HNO 3 (PA grade, Merck). The vessels were introduced in a electric hot plate for sample digestion under temperature control. The temperature program applied in hot plate dissolution of all samples was 1085 0C for 2 h. Digested benthic samples were filtered on ashless filters of 25 m pore size (Whatman 41, Sigma Aldrich) and then analyzed for metal determination [16]. All the samples were analyzed by HACH DREL 2000 spectrophotometer in order to determine the total amounts of Cd, Zn, Cu, and Fe. Calculation of bioaccumulation factor Bioaccumulation factors (BAF) calculated based on the ratio between heavy metal content in each benthic with the concentrations of heavy metals from their environment (both water and sediment). Heavy metal concentration data in water and sediment using the data of previous studies [22], because it is done in parallel with this research. To evaluate the metal bioaccumulation from water or sediment, the BAF were calculated [16][30]-[34] as: BAF = M TISSUE M SED / WATER 118
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Alfonds Andrew Maramis and Agustinus Ignatius Kristijanto, 2012. Heavy Metals Accumulated by Paragyractis Sp. and Hydropsyche Sp. in Kreo River Adjacent to Jatibarang Landfill, Semarang, Indonesia.

where M TISSUE is the metal concentrations in the tissues of a benthic macroinvertebrate and M SED/WATER is the metal amount in the sediment or water phase. Data analysis To see the effect of Jatibarang landfill leachate against heavy metals content in Paragyractis sp. and Hydropsyche sp., differences in concentration of heavy metals that accumulated by these two benthic inter-stations of sampling were analyzed using one-way analysis of variance ( = 0,05). Previously, the data of heavy metals concentration were tested for normality distribution using Kolmogorov-Smirnov test ( = 0,05), and homogeneity of variance using the Levene test ( = 0,05). After the data are convincing that the content of heavy metals followed the normal distribution and variance which showed a homogeneous, then the data was further analyzed using analysis of variance. Furthermore, post-hoc test was done on this data using Tukey HSD (Honestly Significant Difference, = 0,05) [35]. The difference between metal bioaccumulation factors were analyzed using the Kruskal-Wallis nonparametric test ( = 0,05) [36]-[37]. All statistical tests were applied using SPSS (version 15) software [38]. RESULTS AND DISCUSSION Heavy metals concentration in Paragyractis sp. and Hydropsyche sp. Table 1 presents the data of the Tukeys HSD test results on heavy metal concentrations in Paragyractis sp. (Insecta: Lepidoptera) and Hydropsyche sp. (Insecta: Trichoptera) which taken at four stations on the Kreo River. From these data, qualitatively seen that the concentration of all of the heavy metals in both benthic which taken at the station after the leachate discharge higher than which taken before the leachate discharge (Figure 3). Table 1: Tukeys HSD test on the mean of heavy metal concentration in Paragyractis sp. and Hydropsyche sp. taken at four stations of the Kreo River. Species Heavy Sampling Station Metals I II III IV Paragyractis sp. Cadmium 0.0043 0.0107 0.0107 0.0034 (a) (a) (a) (a) Zinc 16.1604 25.8230 22.8983 20.5075 (a) (a) (a) (a) Copper 6.5783 10.2452 9.9599 8.8903 (a) (a) (a) (a) Iron 5.3645 7.0970 6.4236 6.2207 (a) (a) (a) (a) Hydropsyche Cadmium 0.0043 0.0168 0.0180 0.0086 sp. (a) (b) (b) (ab) Zinc 19.0218 60.3049 56.8677 30.1939 (a) (b) (b) (ab) Copper 9.8399 26.7382 31.0161 23.6909 (a) (a) (a) (a) Iron 4.6514 14.6442 15.8324 8.2320 (a) (ab) (b) (ab)
Note: The numerals followed the same letters indicate no significant difference between sampling stations, whereas the numerals followed by different letters indicate significant differences. All numerals are expressed in units of g.g-1 dry weight (dw) of the body.

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Alfonds Andrew Maramis and Agustinus Ignatius Kristijanto, 2012. Heavy Metals Accumulated by Paragyractis Sp. and Hydropsyche Sp. in Kreo River Adjacent to Jatibarang Landfill, Semarang, Indonesia.

Fig. 3: Bar charts from the mean of Cd, Zn, Cu, and Fe concentration (g.g-1 dw SE) in Paragyractis sp. (left) and Hydropsyche sp. (right) taken at four stations on the Kreo River. However, statistically the concentrations of the four heavy metals in Paragyractis sp. did not differ significantly between sampling stations. Differ with Hydropsyche sp., which showed increased concentrations of heavy metals on the second, third and fourth stations (after leachate discharge) as compared with the first station (before leachate discharge), except for Cu. This fact means that the landfill leachate of Jatibarang quite a role in increasing concentrations of heavy metals (except Cu) in Hydropsyche sp., but did not cause increased concentration of heavy metals in Paragyractis sp. Cain and Luoma [39] states that, spatial patterns in whole body of metals concentrations were generally corresponded to contamination levels measured in the environment. Hydropsyche genus in the river were chronically exposed to biologically available metals and some features of this exposure were not evident from whole body concentrations. From Table 1 and Figure 3 can be seen also that the highest heavy metals that accumulate in the body of Paragyractis sp. that is Zn, followed by Cu, Fe, and the lowest Cd. So far, the concentration of heavy metals in Paragyractis sp. has never been reported. For comparison, Noret et al. [40] reported that Zn and Fe concentrations that can be accumulated by Issoria lathonia butterflies (Lepidoptera: Nymphalidae) are 30 5 and 23 2 g.g-1 dw, respectively. Concentrations of Zn in terrestrial Lepidoptera (I. lathonia), as reported by Noret et al. [40] was 120
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Alfonds Andrew Maramis and Agustinus Ignatius Kristijanto, 2012. Heavy Metals Accumulated by Paragyractis Sp. and Hydropsyche Sp. in Kreo River Adjacent to Jatibarang Landfill, Semarang, Indonesia.

only slightly higher than the concentration of Zn in Paragyractis sp. that found in this study, but the concentration of Fe in I. lathonia about five times higher than in Paragyractis sp. There are some previous studies that reported the concentration of various heavy metals in the body of the Hydropsyche genus. Cain and Luoma [39] have reported the contents of Cd in H. cockerelli and H. occidentalis that live in the bottom of Clark Fork river for four consecutive years (1992-1995) with the means of concentrations of about 0.60 - 2.92 and 0.33 - 2.29 g.g-1 dw, respectively. The concentrations of Cd in both benthic are quite high, although taken approximately 380 km at the downstream of the river, far away from copper mining areas. In another study, Cain and his colleagues [13] reported the contents of Cu and Zn in Hydropsyche spp. that taken in the same place with the previous research [39], with the range of concentration of about 21.99 - 196.99 and 146.45 - 254.98 g.g-1 dw, respectively. So far, there are no studies that reported the content of Fe in the Hydropsyche genus which can be used as a comparison with this research. This research is consistent with previous research that has been reported by Cain and Luoma [39] and Cain et al. [13], indicating that Zn is the highest accumulated, then Cu, and Cd is the lowest accumulated by the benthic of the Hydropsyche genus. The metals bioaccumulation factor of benthic from the environment Table 2 presents data on the results of the Kruskal-Wallis test on the mean rank of four heavy metals bioaccumulation factor of Paragyractis sp. and Hydropsyche sp. from water and sediment of the Kreo River. Kruskal-Wallis test ( = 0.05) results showed that the BAF of Paragyractis sp. and Hydropsyche sp. from water and sediment were significantly different between each type of metal, which is shown by the high value of Chi-square and Asymp Sig are much smaller than 0.05. Both benthic BAF showed a similar pattern based on the type of environment phase. The metals BAF of Paragyractis sp. and Hydropsyche sp. from water that is sorted from highest to lowest as follows: Cu > Zn > Fe > Cd, while the sediment is: Zn > Cu > Cd > Fe (Figure 4). Tabel 2: Kruskal-Wallis test on the mean rank of four heavy metals bioaccumulation factor of Paragyractis sp. and Hydropsyche sp. from water and sediment of the Kreo River. Heavy Metals Species Environment Cadmiu ChiAsymp. Phase m Copper Zinc Iron Square Sig Paragyractis Water 14.67 78.11 84.89 40.33 89.960 0.000 sp. Sediment 39.26 95.74 66.84 17.72 93.485 0.000 Hydropsyche Water 10.50 57.62 67.38 31.00 70.635 0.000 sp. Sediment 31.50 72.02 52.98 11.00 75.617 0.000 The differences of BAF between types of metal can represent the level of benthic sensitivity to each metals. According Buchwalter and Luoma [15], the overall metal sensitivity of a given taxon results from the interplay among parameters that govern exposure (bioaccumulation via aqueous and dietary routes and loss dynamics) as well as detoxification processes, reflected in the internal distribution patterns. Louma and his colleagues [14] added that the bioaccumulated toxic metals in tolerant biomonitors are indicators of metal bioavailability and can be calibrated against metal specific responses in sensitive species, thus creating a tool for defining doseresponse for metals in a field setting. The total bioaccumulated metal concentration in any organism that is a net accumulator of the metal is informative about metal bioavailability summed across exposure routes. 121
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Alfonds Andrew Maramis and Agustinus Ignatius Kristijanto, 2012. Heavy Metals Accumulated by Paragyractis Sp. and Hydropsyche Sp. in Kreo River Adjacent to Jatibarang Landfill, Semarang, Indonesia.

Fig. 4: Bar charts from the mean of bioaccumulation factor of Paragyractis sp. and Hydropsyche sp. from water and sediment of Kreo River based on the type of heavy metals. The data of the bioaccumulation factor in this figure are presented in the form of square root transformation. Table 2 and Figure 4 shows that Paragyractis sp. and Hydropsyche sp., accumulating Cd from water and sediment in the lower level, further Zn, and Cu accumulated in a relatively higher level. The accumulation of these three kinds of heavy metals in Paragyractis sp. and Hydropsyche sp. in line with the pattern of concentration in water and sediment. Unlike the three metals, the accumulation of Fe from the water and sediments showed unique facts, where the concentration of Fe that was accumulated in both benthic is relatively low. This fact is inconsistent with the concentration of Fe in water and sediment [22], where the concentration of Fe in this two environment phase shows very high concentrations compared with the three other metals. In the water phase, the concentration of Fe is 90 times higher compared with Cd, 3.6 times for Zn, and 10 times for Cu. Whereas in the sediment the concentration of Fe is 5300 times higher than Cd, 40 times for Zn, and 30 times for Cu. According to Cain et al. [13], some species may limit bioaccumulation of some metals by uptake and loss, thereby maintaining low intracellular metal concentrations and effectively preventing metal toxicity. However, most species cannot regulate bioaccumulation of many metals, particularly nonessential metals. Buchwalter and Luoma [15] added that, dissolved uptake rates of the metals were not related to gross morphological features such as body size or gill sizes features that influence water permeability and therefore have ionoregulatory importance. Dissolved Cd and Zn uptake rates strongly co-varied among species, suggesting that these metals are transported by similar mechanisms. However, there is typically no one universal metal concentration that is indicative of toxicity, especially across species, largely because of interspecies differences in detoxification [14]. CONCLUSIONS The conclusion that can be drawn from this research is that the leachate of Jatibarang landfill not cause significant increase in the content of Cd, Zn, Cu, and Fe in Paragyractis sp. In contrast, leachate causes significant increase in content of Cd, Zn, and Fe in Hydropsyche sp., but not significant for Cu. Spatial patterns of metal content in the whole body of benthic can be used to represent the content of metals both in water and sediment. Bioaccumulated toxic 122
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Alfonds Andrew Maramis and Agustinus Ignatius Kristijanto, 2012. Heavy Metals Accumulated by Paragyractis Sp. and Hydropsyche Sp. in Kreo River Adjacent to Jatibarang Landfill, Semarang, Indonesia.

metals in tolerant biomonitors is an indicator of metal bioavailability, as shown by the Zn and Cu which have a high bioaccumulation levels in both benthic. The BAF values in this research that are different among the type of metals indicates that there are some species which can limit the amount of metal bioaccumulation, while other species can not regulate the accumulation of certain metals, especially for metals that are not important in metabolism.
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Alfonds Andrew Maramis and Agustinus Ignatius Kristijanto, 2012. Heavy Metals Accumulated by Paragyractis Sp. and Hydropsyche Sp. in Kreo River Adjacent to Jatibarang Landfill, Semarang, Indonesia.

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