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1 Research Article DISTRIBUTION OF FIVE TOXIC HEAVY METALS IN BIOTIC AND ABIOTIC ... PDF

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Sivanantha et al. Sri Lankan J. Biol. 2016, 1(1):1-14 Sri Lankan Journal of Biology Volume 1 Issue 1 Research Article Open Access DISTRIBUTION OF FIVE TOXIC HEAVY METALS IN BIOTIC AND ABIOTIC CONSTITUENTS OF THE NEGOMBO LAGOON, SRI LANKA Sivanantha N.1, Wijesinghe M. R.2* and Wijesekera R. D.1 1Department of Chemistry, University of Colombo, Colombo 03, Sri Lanka. 2Department of Zoology and Environment Sciences, University of Colombo, Colombo 03, Sri Lanka. Abstract The presence of toxic metals in water has become a matter of national concern. This situation is potentially more dangerous when it occurs in lagoons and estuaries which are both highly productive and sensitive in comparison to other natural habitats. In this study, the levels of five toxic heavy metals, As, Cd, Cr, Pb and Hg, present in several abiotic and biotic constituents of the Negombo lagoon, Sri Lanka, were investigated with the objective of assessing the potential risks of accumulation. Sampling, in five locations, was conducted from December 2014 to April 2015. Water, sediment, soil, bark and leaves of the mangrove Bruguiera gymnorhiza, and fauna of selected taxa were collected and heavy metals were analyzed using ICP – OES following microwave digestion. Apart from Cr which was detected at low levels, none of the other metals were detected in the water. Nevertheless, the five heavy metals were present in relatively large amounts in one or more of the other tested constituents, indicating lagoon pollution, depicting an overall trend water < leaves < bark < snails < fish < crab < sediment < soil. Our investigation suggests that As and Cd, due to their high levels of accumulation in soil and sediment, impose the highest potential risks. Trends in accumulation suggest non-point sources for Cd, Cr and Pb. Findings reported here call for continual monitoring and for controlling discharge of contaminated effluents into productive lagoon ecosystems. Key words: accumulation, abiotic, biotic, heavy metals, lagoon *Corresponding author: Tel: 0714406277; E-mail: [email protected] 1 Sivanantha et al. Sri Lankan J. Biol. 2016, 1(1):1-14 Sri Lankan Journal of Biology Volume 1 Issue 1 1. Introduction been well documented. It has been shown that the accumulated metal Heavy metal contamination in the aquatic concentrations in organisms generally environment is a matter of serious reflect, quantitatively or semi- concern due to its adverse impact on quantitatively, the level of environmental humans and other organisms. Although pollution (Dallinger, 1994), allowing them heavy metals in the environment could to be used as bio-indicators of metal arise from natural sources (Chibuike & pollution. Obiora, 2014), the recent increases have, to a large extent, been attributed to The Negombo lagoon in the western anthropogenic activities such as the region of Sri Lanka (7º 09’N 79º 51’ E) discharge of untreated industrial effluents receives fresh water from three sources: and the intense use of agrochemicals the Ja-Ela, Dandugam Oya and the (Dixit et al., 2015). Heavy metals that Hamilton Canal (Gammanpila, 2013). The enter a water body are dispersed area mainly receives rainfall from the throughout its biotic and abiotic southwest monsoon from May to constituents, the levels of occurrence September, while convectional showers being influenced by the condition of the occur during the remaining months of the water at a given time. For instance, acidic year (CEA, 1994). The temperature varies conditions cause heavy metal ions between 24 oC to 30 oC. The Negombo adsorbed to soil and sediment to be lagoon is one of the most productive released into the water increasing their brackish water ecosystems in Sri Lanka in bioavailability in the aquatic medium terms of mangrove vegetation, fauna and (Alghanmi, et al., 2015). Similarly, other inland fishery (Samarakoon & van Zon, factors, such as temperature and the 1991; Jayasiri, 2004; Dahanayaka et al., amount of dissolved oxygen and organic 2008). Previous studies have assessed the matter, also determine the fate of the status of the Negombo lagoon through heavy metals within a water body accumulation of heavy metals in selected (Kuwabara et al., 1996; Croteau et al., constituents (e.g. Indrajith & Pathiratne, 2002). 2006; Indrajith et al., 2008 – water, sediment and fish; Asanthi et al., 2007 – The heavy metals As, Cd, Hg, Pb and Cr water, sediment and algae; Mendis et. al., (VI) are non-essential elements, and they 2015a & b – water and fish). In this paper, induce toxic impacts in biota even at trace the levels of the five heavy metals As, Cd, levels (Tchounwou et al., 2012). The Cr, Hg and Pb were examined potential hazard imposed by these metals simultaneously, in three abiotic (water, to organisms is enhanced due to the bio- sediment and soil) and selected biotic accumulative and non-biodegradable (mangrove, snails, fish and crabs) nature of the elements (Cui et al., 2011; constituents of the Negombo lagoon. In Yu et al., 2013). Furthermore, the ascertaining the levels of these elements potential for accumulated heavy metals to the possibility of bio-concentration of bio-magnify along food chains, ultimately these heavy metals was also investigated. reaching high concentrations in organisms at the top trophic level, has *Corresponding author: Tel: 0714406277; E-mail: [email protected] 2 Sivanantha et al. Sri Lankan J. Biol. 2016, 1(1):1-14 Sri Lankan Journal of Biology Volume 1 Issue 1 2. Material and Methods Faunal species were collected at four of the stations only (other than from station 2.1 Collection of samples C). Collection of faunal species was based on the available taxa. For instance, The present study was conducted samples of Hydrobiid sp. (gastropod) between December 2014 and April 2015 were collected from station A, at five sampling stations: A – bordering Heteropneustus fossilis (Asian stinging cat the National Aquatic Resources, Research fish) from B, Scylla serrata (mud crab) and Development Agency (NARA) from D and Eutroplus suratensis Conservation Centre, B – bordering the (Pearlspot Cichlid) from E. A total of ten main bus station in Negombo, C – samples each of the different taxa, which Dandugam Oya inlet, D – bordering a were sufficient for analysis, were residential area and E – in close proximity collected from the four sampling stations. to the airport (Figure 1). At each station, Snails were collected from the surface of samples were collected at five random the soil/sediment while fish and crabs points separated from each other by a were caught with the aid of fishermen in distance of more than 20 m, yielding a the vicinity of the sampling stations. All total of 25 sampling points. At each of samples were transported to the these points, two samples each of water, laboratory and stored at 4oC until sediment and soil were collected yielding analyses which were carried out typically a total of 50 samples per component. The within 3 days of collection. water was collected from 1 m beneath the surface with a Ruttner Sampler and 2.2 Analysis of heavy metals stored in polypropylene containers for analysis. These containers were washed The procedure employed for analysis of with 10 % HCl and then with de-ionized heavy metals in water was according to water before use. Surface sediment (down APHA 3120 – B (US EPA, 2007). Samples to around 3 cm from the bottom surface) of the water were digested with conc. was scraped off with a scoop and HNO (10 cm3 conc. HNO for 50 cm3 of 3 3 collected into sealable polythene bags, each sample) and further concentration with excess water being drained before was achieved by evaporation. In cases sealing. Soil, within 5 m away from the where NaCl precipitated before the water and to a depth of 3 cm from the soil concentration process, the solutions were surface, was scooped using a deep spoon topped to different volumes using de- and also stored in sealable polythene ionized water. After filtration the solutes bags. Obtaining soil and sediment in this were analyzed using ICP – OES and tested manner increased the likelihood of for heavy metals. Whenever necessary, collecting recent deposits, as opposed to the solute was diluted. Soil and sediment mainly material of geological origin. At (500 g each) and 20 g of each biotic each point bark and mature leaves from a constituent, i.e. bark, leaves and faunal minimum of three trees of the mangrove tissue, were also digested for analysis, as Bruguiera gymnorhiza were collected. described in US EPA (2007). *Corresponding author: Tel: 0714406277; E-mail: [email protected] 3 Sivanantha et al. Sri Lankan J. Biol. 2016, 1(1):1-14 Sri Lankan Journal of Biology Volume 1 Issue 1 Figure 1. Map of the Negombo lagoon showing the five sampling stations Following microwave digestion, the Calibration checks (20 μg/dm3 for Hg and concentrations of As, Cd, Cr, Pb and Hg in 1.00 mg/dm3 for the other metals) were each sample were determined using used for every 20 samples. Certified inductively coupled plasma-optical aqueous reference standards of TMDA emission spectroscopy (ICP-OES) (Varian 64.2 and ICP-OES wavelength calibration 720-ES, Australia). Recovery studies were solutions were obtained from an outside done with spiked samples and certified source and analyzed according to reference materials (CRM). Analyses were instructions provided. The generated conducted in duplicate, and repeated if results were checked to ensure that they the error exceeded 10 %. For the were within the acceptable range. recovery procedure, a known amount of the standard mixture of the five heavy 2.3 Potential risk factors metals was spiked into conc. HNO (10 3 cm3) (blank sample) and digested. The The Contamination Factor (Cf) which CRMs used were 2711a Montana II, 2976 describes the contamination of a given muscle tissue, 1570a spinach and TMDA toxic substance in a water body as 64.2. ICP-OES and VGA. Calibration check suggested by Håkanson (1980) is useful solutions were analyzed to ensure for assessing the potential dangers instrument performance and to validate imposed by the heavy metal loads in a calibration, using the same acid matrix. water body and is derived using the *Corresponding author: Tel: 0714406277; E-mail: [email protected] 4 Sivanantha et al. Sri Lankan J. Biol. 2016, 1(1):1-14 Sri Lankan Journal of Biology Volume 1 Issue 1 formula Cf = CCurrent / CPre-ind. These noteworthy that, with the exception of Cr indices were calculated for the Negombo (recording a maximum of 0.09 mg/ dm3), lagoon. Since data on pre-industrial levels none of the other toxic heavy metals (As, are lacking for any of the tested metals for Cd, Pb, and Hg) were detected in the Sri Lankan systems, the values obtained water. Nevertheless, the detected levels of for a range of European and American the five metals in the other constituents water bodies prior to industrialization, i.e. sediment, soil and the biota, are which have been also widely applied even indicative of heavy metal contamination for tropical estuaries (e.g Vowotor et al., of the Negombo lagoon (Figure 3 and 2014), were used for this purpose. Table 1). Considering sediment and soil, Additionally, the Ecological Risk Factor the highest metal levels recorded were for (Er) based on the Toxicity Response Cr (34.3 and 49.8 mg/kg respectively). Factor (Tr) assigned to each of the metals Both these constituents were also (Håkanson 1980) was calculated using Er relatively rich in Pb, whilst As and Cd = Tr x Cf. were present at low levels. It is significant that Hg was not recorded in sediment or 3. Results soil at any of the sampling stations. Considering heavy metal concentrations The analyses revealed the presence of all recorded in the flora and fauna, apart five toxic heavy metals i.e. As, Cd, Cr, Pb from Cd, all the other toxic heavy metals and Hg in at least one of the biotic or were recorded in one or more of the abiotic constituents analyzed from each of biotic constituents. From among these, as the five sampling stations in the Negombo although not recorded in the mangrove, lagoon. Figure 2 shows the mean levels was seen to reach high levels, with a (+ standard errors) of the metals maximum of 22.5 mg/kg, in crabs. Cr, Hg recorded in the different constituents, and Pb were recorded in comparatively whilst the minimum- maximum ranges high concentrations in both floral and detected for each of the metals are shown faunal components (Figure 2 and Table in Table 1. Some of the salient features 1). evident from the results are set out below. The overall trends of the mean levels of accumulation of the five metals recorded 3.1 Apportionment among constituents in water, sediment, soil, flora and fauna are shown in Figures 3 (a) and (b). The The mean + standard error of the pH graphs show that, apart from subtle values in the water samples recorded for differences, there is a similar overall the five sampling stations were A: 7.79 ± pattern of accumulation for As, Cd, Cr and 0.24, B: 6.55 ± 0.14, C: 5.65 ± 0.10, D: 7.78 Pb with concentrations increasing in the ± 0.04 and E: 7.85 ± 0.12. The one way order water < leaves < bark < snails < fish ANOVA and Tukey pairwise comparison < crab < sediment < soil. Hg was only test revealed significant station-wise recorded from the biotic constituents. Soil differences in pH (p ≤ 0.05), with station C and sediment evidently function as sinks having a significantly lower pH. With of these heavy metals. respect to the heavy metals, it is *Corresponding author: Tel: 0714406277; E-mail: [email protected] 5 Sivanantha et al. Sri Lankan J. Biol. 2016, 1(1):1-14 Sri Lankan Journal of Biology Volume 1 Issue 1 The C and T factors as well as the low (i.e. < 1) and in the order of Pb < Cr < Pre-ind r generated C and E values are given in As < Cd. The Ecological Risk Factors f r Table 2. Accordingly, both concentration increase in the overall order of Cr < Pb < factors for sediment and soil are generally As<Cd. Figure 2. Mean concentrations (± standard error) of the five tested heavy metals in the different biotic and abiotic constituents in the five sampling stations (A to E). (Note: results for water, where only Cr was detected at low levels, are not shown) *Corresponding author: Tel: 0714406277; E-mail: [email protected] 6 Sivanantha et al. Sri Lankan J. Biol. 2016, 1(1):1-14 Sri Lankan Journal of Biology Volume 1 Issue 1 Table 1. The minimum and maximum values of the five selected heavy metals in the different biotic and abiotic constituents in the Negombo lagoon. Constituent As Cd Cr Hg Pb Water (mg /dm3) ND ND ND - 0.09 ND ND (n=50) Sediment (mg ND - 8.65 ND - 1.67 7.64 - 34.30 ND 2.53 - 19.61 /kg) (n=50) Soil (mg /kg) ND - 9.89 ND - 2.63 2.40 - 49.80 ND ND - 20.26 (n=50) Bruguiera Bark (mg /kg) ND ND ND - 1.93 ND - 0.15 ND - 4.09 (n=50) Leaves ND ND ND - 0.69 ND ND (n=50) Snails (mg /kg) 3.46 - 6.25 ND ND - 1.76 0.07 - 0.22 ND (n=10) Fish (mg /kg) 2.90 - 9.23 ND 0.92 - 4.69 0.15 - 0.61 ND - 2.34 (n=20) Crabs (mg /kg) 20.51 - 22.46 ND 1.41 - 2.48 0.05 - 0.26 ND (n=10) ND indicates metal levels below limits of detection; n indicates number of samples analyzed 3.2 Inter-site comparisons higher than the others (metals: p <0.001). Nevertheless, the inter-site differences in To interpret inter-site differences the total metal levels were not significant combined results for water, sediment, (sites: p>0.05), indicating that the total soil, and mangrove bark and leaves for metal loads between sites were each of the metals were considered. somewhat comparable. The interaction Results for fauna were not included due between sites and metals was also not to the disparity in sample sizes between significant (metals x sites: p>0.05) sites. A two way ANOVA indicated that, suggesting that the trends of overall in the Negombo lagoon, there is a accumulation of each of the metals in the significant metal-wise difference, with different sites were nearly consistent. loads of some metals being markedly *Corresponding author: Tel: 0714406277; E-mail: [email protected] 7 Sivanantha et al. Sri Lankan J. Biol. 2016, 1(1):1-14 Sri Lankan Journal of Biology Volume 1 Issue 1 g) 40 g) 0.6 g/ k30 g /k0.5 m m0.4 n (20 n (0.3 o o ntrati10 ntrati00..21 e e nc 0 nc 0 o o C Sed Soil C Bark Leaf Snail Fish Crab As Cr Pb Cd (a) (b) Figure 3. The patterns of accumulation of heavy metals (means) in the different biotic and abiotic constituents of the Negombo lagoon, depicted in two concentration ranges (a) Pb, Cr, As and (b) Cd, Hg. The extent of consistency between sites to similar sources of inputs suggesting the suggests similarity in the sources of likelihood of non-point sources for these contamination and this was examined metals. On the other hand, As and Hg are using the Pearson's correlation coefficient not significantly correlated with any of matrix, following Vowotor et al. (2014). the other metals, nor with each other, The correlation matrix for the five heavy suggesting that these two metals most metals under consideration is given in likely arise from different sources. The Table 3. Interestingly, the significant and localization of Hg also suggests a point strong positive correlations between the source of input. three contaminants; Cd, Cr and Pb, points Table 2. Concentration Pre-industrial (C ), Toxic response factor (T ), Contamination Pre-ind. r Factor (C) and Ecological Risk Factor (E ) values for As, Cd, Cr and Pb. Note: Hg was not f r recorded in sediment and soil. As Cd Cr Pb T* 10 30 2 5 r C Sediment 0.4 0.5 0.2 0.1 f Soil 0.2 0.4 0.2 0.1 E Sediment 4.0 15.0 0.4 0.5 r Soil 2.0 12.0 0.4 0.5 *Source - Håkanson (1980) *Corresponding author: Tel: 0714406277; E-mail: [email protected] 8 Sivanantha et al. Sri Lankan J. Biol. 2016, 1(1):1-14 Sri Lankan Journal of Biology Volume 1 Issue 1 Table 3. Pearson’s Correlation Coefficients showing the consistency in occurrence of the five tested heavy metals in the five sampling sites. Cd Cr Pb As Cr 0.55* p < 0.01 Pb 0.79* 0.90* p < 0.001 p < 0.001 As 0.20 0.25 0.19 p > 0.05 p >0.05 p >0.05 H g -0.11 0.18 0.20 0.36 p >0.05 p >0.05 p >0.05 p = 0.05 *significant association (p<0.01) 4. Discussion transport of heavy metals is the adsorption onto surfaces of solid In the current investigation, the five particulate matter, which results in tested heavy metals (As, Cd, Cr, Pb and lowering levels in the water medium Hg) were recorded at relatively high (Rieuwerts et al., 1998). Usually in levels in one or more of the biotic or lagoons, triggered by acidic conditions, abiotic constituents in the Negombo heavy metals tend to precipitate with lagoon. In the water, however, none of the sulphide, lowering bioavailability in the elements, with the exception of Cr, was water (Simpson & Spadaro, 2016). Such recorded, and that too at relatively low processes give the water body the ability levels. The absence/low concentration of to regulate toxic metals between the biotc the heavy metals in the water reported and abiotic components. In the present here is in conflict with previously study there is some evidence for documented values for the Negombo variability in pH levels across the lagoon. For instance, values reported by sampling stations which may have Indrajith & Pathiratne (2006) and contributed to some extent to the Indrajith et al. (2008) for Cd and Pb, and observed differences in the metal loads by Asanthi et al. (2007) for arsenic, in between the sites, although such water, were as high as 5.70, 2.10 and 2.16 differences were not significant. Two µg/L, respectively. The seemingly other factors that would seriously affect contradictory results obtained in the concentrations of heavy metals and other present study could be viewed in the light contaminants in the water at a given time of the conditions and processes that is the rate of flushing and the residence prevail in the lagoon. One of the most time of water, both of which would have a important processes controlling the major impact on the rate of sedimentation as well as on the water chemistry. The *Corresponding author: Tel: 0714406277; E-mail: [email protected] 9 Sivanantha et al. Sri Lankan J. Biol. 2016, 1(1):1-14 Sri Lankan Journal of Biology Volume 1 Issue 1 rate of water exchange between the although Hg has been previously lagoon and the adjacent ocean occurs recorded in sediment from the Negombo mainly through tidal action and the lagoon (Indrajith et al., 2008), the present quantity of freshwater discharge. The study did not detect this metal in any of Negombo lagoon is reported to feature a the soil or sediment samples. Studies have weak tide (maximum range is about 10 demonstrated that metal ions with similar cm) but it has a strong and variable valance states compete for metal binding freshwater discharge resulting in a sites, i.e. in this case for surfaces of residence time of between 2-14 days organic matter. Thus, there is a possibility (Rydberg & Wickbom, 1996; Rajapaksha, that Hg was displaced upon additional 1997). The intermittent showers in the loadings of other metals such as Pb area during the study period and the high (Holmberg, 2006). The weak association freshwater discharge into the lagoon noted between Hg and Pb observed in the would have facilitated some flushing present study, however, does not provide which most likely resulted in low persuasive evidence that displacement accumulation of heavy metals in the occurred. The present investigation water as observed here. highlights As and Cd as metals with the highest potential to concentrate in soil or In the present study the heavy metal sediment whilst Cd, due to its high loads recorded in sediment and soil were prevailing levels and high potency to much higher than those in water, with soil cause adverse health impacts, shows up and sediment being near equally polluted, as the metal with the higher ecological reiterating the function of these two risk. Although the risks associated with constituents as heavy metal sinks. Soil individual metals are low accordingly to and sediment generally act as sinks of the stated threshold values (see heavy metals primarily due to the organic Hakanson, 1980), the ‘true risk’ to biota fraction that has the capacity to adsorb may arise from the summation of risks these elements, the process being posed by all metals (as well as other considerably influenced by factors such as contaminants) present in the ecosystem pH, metal speciation, ionic strength, and (Hakanson, 1980). other properties that are inherent to the target metal (Lin & Chen, 1998). Flushing What is of considerable interest is that, and the re-suspension of metals through despite concentrations in water being the disturbance of sediment or soil would beyond detectable limits for most of the temporarily cause elevation of metal metals and for the majority of the loads in water at a particular site sampling sites, there were relatively high (Eisenreich et al., 1980). levels of accumulation of those metals in the biotic elements. Usually living Heavy metal levels observed in the organisms take up heavy metals from present study for sediment in the abiotic constituents, i.e. from soil, water Negombo lagoon are similar for Pb and and sediment. The level of accumulation Cr, whilst Cd values are higher than also depends on the particular trophic previously recorded values (Indrajith et position each organism occupies in the al., 2008). It is also noteworthy that food chain. The heavy metals that are *Corresponding author: Tel: 0714406277; E-mail: [email protected] 10

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study, the levels of five toxic heavy metals, As, Cd, Cr, Pb and Hg, present in several abiotic and biotic Key words: accumulation, abiotic, biotic, heavy metals, lagoon . (Pearlspot Cichlid) from E. A total of ten samples each aqueous reference standards of TMDA . adsorption onto surfaces of sol
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