Marine Pollution Bulletin 87 (2014) 345–351
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Bioaccumulation of trace elements in dominant mesozooplankton group inhabiting in the coastal regions of Indian Sundarban mangrove wetland Bhaskar Deb Bhattacharya a, Jiang-Shiou Hwang b, Li-Chun Tseng b, Santosh Kumar Sarkar a,⇑, Dibyendu Rakshit a, Soumita Mitra a a b
Department of Marine Science, University of Calcutta, 35 Ballygunge Circular Road, Calcutta 700019, India Institute of Marine Biology, National Taiwan Ocean University, Keelung 20224, Taiwan
a r t i c l e
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Article history: Available online 8 August 2014 Keywords: Mesozooplankton Copepods Trace metal Bioaccumulation factor Indian Sundarban
a b s t r a c t Mesozooplankton (Body size 20–200 lm) along with the surface water were collected from coastal regions of Sundarban, northeastern part of Bay of Bengal considering three seasons, namely premonsoon, monsoon and postmonsoon. Samples were analyzed for community structure and the dominant copepod species were further analyzed for trace metal concentration. In total, 50 copepods were identified (22 families and 43 genera). The dominant mesozooplankton species included 9 copepods and an epipelagic chaetognath, exhibited both spatial and seasonal variations. Metal concentration exhibited considerable inter-specific variations for the copepods and the mean concentrations were: Fe, 1350.2–51118.3 lg/g; Al, 647.2–73019.1 lg/g; Ni, 32.4–110.3 lg/g; Mn, 122.8–1066.5 lg/g; Pb, 0.04–97.5 lg/g; Pb, 10.6– 97.5 lg/g; Cd, 4.2–21.6 lg/g; Cu, 17.4–145.1 lg/g; Zn, 225.7–1670.9 lg/g; Cr, 21.7–194.3 lg/g; Co, 1.32–111.1 lg/g. Metal concentrations showed the following order: Sagitta bedoti > Coryceas danae > Oithona sp. > Eucalanus subcrassus > Labidocera euchaeta > Paracalanus parvus > Acartiella tortaniformis > Acartia spinicauda > Pseudocalanus serricaudatus. Ó 2014 Elsevier Ltd. All rights reserved.
Zooplankton play an important role in the biogeochemical cycling of metals in marine systems in general is well known, especially regarding particle-reactive metals in the water column (Fisher et al., 1991; Lee and Fisher, 1994; Stewart et al., 2005). Thus, in several studies macro- and meso-zooplankton organisms have been specifically used as biomonitors for assessment of the bioavailability of elements in marine systems, covering a variety of spatial and temporal scales (Kahle and Zauke, 2003; Ritterhoff and Zauke, 1997; Zauke et al., 1996). Their potential suitability is largely due to their worldwide presence, their major role in the food webs and their high contribution to the total biomass in marine systems. The Indian Sundarban, formed at the estuarine phase of the tidal Hugli River of an area of 9600 km2, is a tide-dominated mangrove wetland belonging to the low-lying coastal zone (Fig. 1). This is one of the most dynamic, complex and vulnerable bioclimatic zone in a typical, tropical geographical location in the northeastern part of the Bay of Bengal. The wetland is characterized by a complex network of tidal creeks, which surround hundreds of tidal islands exposed to different elevations at high and
⇑ Corresponding author. Fax: +91 33 2461 4849. E-mail address: [email protected] (S.K. Sarkar). http://dx.doi.org/10.1016/j.marpolbul.2014.07.050 0025-326X/Ó 2014 Elsevier Ltd. All rights reserved.
low semi-diurnal tides. This coastal environment suffers from environmental degradation due to rapid human settlement, tourism and port activities, and operation of mechanized boats, deforestation and increasing agricultural and aquaculture practices. The ongoing degradation is also related to huge siltation, flooding, storm runoff, atmospheric deposition and other stresses resulting in changes in water quality, depletion of fishery resources, choking of river mouth and inlets, and overall loss of biodiversity as evident in recent years (Sarkar and Bhattacharya, 2003; 2008). A significant ecological change is pronounced in this area due to reclamation of land, deforestation, huge discharges of untreated or semi-treated domestic, municipal and agricultural wastes as well as effluents from multifarious industries (Fig. 1) carried by the rivers as well as contaminated mud disposal from harbor dredging (Sarkar et al., 2007). The upstream of the Hugli River flows through some of the most industrialized (jute mill, textile, tannery, thermal power, oil refinery as shown in Fig. 1) and urbanized (megacity Calcutta and Howrah) regions which make it one of the highly human-impacted rivers in India. The huge discharge of trace metals has a crucial influence on the total load and distribution of elements in the coastal regions of Sundarban. This study has been undertaken to assess the role of mesozooplankton in the biogeochemical cycles. Copepods have been chosen as recommended organisms as they are considered best biomarkers
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Fig. 1. Map of The Indian Sundarban and Sagar Island (enlarged) in details showing the three sampling sites S1, S2 and S3 along N-S direction.
for trace metal monitoring in marine environment because of their huge biomass, limited swimming capacity, vital role in trophic chains, easy availability and sensitivity to trace metal contamination. Three stations have been chosen along south north gradient of high to low salinity for the present study situated in the western flank of Sundarban namely, Lot No. 8 (S1), Chemaguri (S2) and Gangasagar (S3). The selected sampling sites belong to distinctive geographic, geomorphic and hydrological settings with variations of energy domains characterized by wave-tide climate. The sites have diverse human interferences with a variable degree of exposure to trace metal pollution. The surface water and mesozooplankton samples were collected (during 2011 and 2012) seasonally (premonsoon, monsoon and postmonsoon) from three sites distributed on the eastern and western flank of the Sundarban wetland. On each site, water samples (approx. 100 cc.) were filtered through cellulose acetate membrane filter (pore diameter 0.45 lm) and 2 ml 65% nitric acid (Merck) were added after that, water samples were transferred in polyethylene flasks, and they were immediately transported to the laboratory at ±4 °C. The temperature and salinity of water were measured on board, using thermometer (mercury, 0–100 °C) and refractometer respectively. pH of the water was measured by digital pH meter (Model No. 101 E) and turbidity was measured by using turbidity meter (Model no: SYS 304 E). Mesozooplankton samples were collected by towing a Ring Trawl plankton net (mesh size 200-lm). The net was towed obliquely at 1 m below the surface for ten minutes. Zooplankton samples were sorted under a binocular microscope and visually observed to ensure the absence of any foreign particles. On board the plankton samples were sorted and identified up to species level. Copepods were the most abundant taxa in the zooplankton samples followed by chaetognath. Ten dominant mesozooplankton species of diverse feeding guilds such as Bestiolina similis, Paracalanus parvus, Acartia spinicauda, Acartiella tortaniformis, Pseudodiaptomus serricaudatus, Oithona sp., Labidocera euchaeta, Eucalanus subcrassus and Coryceaus danae and the solitary epipelagic chaetognath (Sagitta bedoti) were separated and considered for further analyses of trace metals. Collected plankton samples were divided
into two parts. The first part was transferred to buffered formalin for detailed quantitative analyses and the other part was placed in a small nylon sieve and was thoroughly rinse with Milli-Q water to remove salts. To avoid any possible entrainment of elements on the surface of the zooplanktonic organisms, each zooplankton sample was washed three times with distilled water for elimination of fine particulates of trace elements of terrigenous origin (Demina et al., 2009; Rentería-Cano et al., 2011). Then it was kept deep frozen for trace metals analyses in the laboratory. The concentration of dissolved metals were determined in water by solvent extraction using ammonium pyrrolidine dithiocarbamate (APDC) and methyl isobutyl ketone (MIBK) as a standard method (APHA, 1989). A 1% aqueous solution of APDC (Eastman Chemicals) was prepared daily and purified by shaking with an equal volume of MIBK, separating the phases and filtering the lower aqueous phase. Since APDC is only slightly soluble in MIBK whereas metal complexes are highly soluble, the reagent is easily purified in this manner. Reagent grade MIBK was used throughout without further purification. Ammonium acetate (Sigma, Mumbai) buffer (5N) was prepared and metallic impurities were removed by adding a few milliliters of APDC solution and extracting with MIBK. The dissolved metals were simultaneously extracted from filtered water samples by chelation with APDC followed by MIBK extraction according to method described in literature (Ferrer et al., 2000; Brooks et al., 1967; Koirtyohanm and Wen, 1973; Murakami et al., 1992). All experiments were carried out in a pH range of 2–6. Extractions were done in a separatory funnel shaken for 2 min. by hand with 50 ml of aqueous volume, 1 ml of APDC solution and 10 ml of MIBK. When the highest possible accuracy was required the organic phase was placed in a 10 ml volumetric flask and diluted to volume with water saturated MIBK. This eliminated the error caused by variation in the volume of organic phase lost because of solubility. Concentration of the dissolved metals was measured in a graphite-furnace Atomic Absorption Spectrophotometer (Perkin–Elmer, Graphite Furnace). Standardization was based on a two-point calibration procedure, using a multi element standard (J.T. Backer, Inc. Phillsburg NJ) as the high standard, and double distilled water (zero metal concentration) as the low standard. Standardization of the instrument was
B.D. Bhattacharya et al. / Marine Pollution Bulletin 87 (2014) 345–351 Table 1 Quality assurance using CRM randomly allocated within the determination. Metals
Fe Al Ni Mn Pb Cd Cu Zn Cr Co
DORM-2
TORT-2
Certified values
Measured values
Certified values
Measured values
142 10.90 19.40 3.66 0.065 0.043 2.34 25.60 34.70 0.182
141.07 10.04 19.30 3.49 0.062 0.041 2.29 25.20 34.50 0.179
105 – 2.50 13.60 0.35 26.70 106 180 0.77 0.51
104.80 – 2.30 13.30 0.30 26.30 106 179.70 0.72 0.50
repeated after every three sets of seawater extracts to minimize the effect of instrument drift. Distilled water and a check standard were also included in the analysis sequence. In laboratory, the frozen copepod sample was kept out of the freezer and the water adhering to the samples was removed by placing the sieve on good quality filter paper, without any contamination. The frozen samples were lyophilized and homogenized. Then a 0.5 g sub-sample was taken and subjected to wet digestion (HNO3:HClO4 = 3:1; v/v). Excess of acids was evaporated and the dry residue was dissolved in 10 cm3 of HNO3 (0.1 mol/dm3) solution. Metals, in the so obtained solutions, were analyzed by means of atomic absorption spectrometry (a model Video 11E Thermo Jarrel Ash spectrometer was used). Either electrothermal (Cd, Ni, Cr, Co, Pb) or flame (Fe, Zn, Mn–acetylene/air; Al–acetylene/nitrous oxide) atomization was applied. Blanks were run in parallel with actual samples. Average blanks varied in the range from 0% (for Fe) to 7% (for Cd) of the mean metals concentrations in the analyzed solutions. Quality control was achieved by analyzing DORM 2 and TORT 2 (results shown in Table 1).
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Total 50 mesozooplankton taxonomic groups were identified. Mesozooplankton abundance was higher during the dry season (>1000 ind. m3) than the monsoon season ( Al > Mn > Zn > Ni > Cu > Cr > Co > Pb > Cd. Majority of the metals showed relatively high concentrations during late premonsoon period in comparison to the low flow condition (early postmonsoon) which is attributed to high evaporation rate of surface water followed by elevated temperature (Abdel-Satar, 2001). The negative relationships of Mn with majority of the metals (excepting Cu) were recorded suggesting that Mn-oxide may be only a minor host phase for these metals. Non-significant correlations of Mn with all the metals are due to the different processes like biological effects and external inputs operating in estuarine system (Ray et al., 2006). Significant correlations between Cu with Co (r = 0.69) and Ni (0.76), Ni with Zn (r = 0.514) and Pb (0.638) and Zn with Cd (r = 0.857) indicate the possible enrichment of all these four metals partly through terrigenous origin and partly due to the biological production. The concentrations of trace metals in the 10 dominant species of mesozooplankton collected at all stations are shown in Table 2 and plotted in Fig. 3. The concentrations ranged as follows: Fe, 1350.2– 51118.3 lg/g; Al, 647.2–73019.1 lg/g; Ni, 32.4–110.3 lg/g; Mn, 122.8–1066.5 lg/g; Pb, 0.04–97.5 lg/g; Pb, 10.6–97.5 lg/g; Cd, 4.2–21.6 lg/g; Cu, 17.4–145.1 lg/g; Zn, 225.7–1670.9 lg/g; Cr, 21.7–194.3 lg/g; and Co, 1.32–111.1 lg/g. The average concentration of trace metals in all the analyzed mesozooplankton samples followed the sequence: Fe > Al > Z n > Cu > Mn > Ni > Cr > Cd > Co > Pb. The inter- and intra-variability in concentration turns out to be quite considerable (up to 10–100 fold variations). To compare the trace metal contents in the different copepods species, metal concentrations in each species were normalized to the metal content of B. similis. The sequence of sums of the normalized values of all metals in each species was: S. bedoti > C. danae > Oithona sp. > E. subcrassus > L. euchaeta > P. parvus > A. tortoniformis > A. spinicauda > P. serricaudatus. The highest
Fig. 4. Trace metal bioconcentration factors in copepods obtained in this study.
metal quota was found in S. bedoti which is carnivorous in nature (Hamid et al., 2010; Sarkar et al., 1986). High metal bioavailability results in high concentrations of the corresponding metals in biota through the so-called bioconcentration process. The bioconcentration factor (BCF) can provide knowledge of how enriched organisms are in particular elements, with respect to the surrounding environment. The average order of magnitude of the BCF (Cm/Cw; Cm, and Cw represent the metal concentration in copepods and water, respectively) of copepods for trace metals in the present study ranged from 4.5 to 6.5 (Fig. 4) and followed the sequence:
Znð12:06Þ > Crð2:05Þ > Cuð1:80Þ > Cdð1:76Þ > Coð1:67Þ > Pbð1:62Þ > Nið1:36Þ > Mnð1:31Þ > Alð0:58Þ > Feð0:45Þ
study study study study study Present Present Present Present Present 27.5–61.6 21–55.1 46.7–114.9 25.7–59.8 NR – 74.06 66.4–118.3 42.9–94.8 90.5–194.3 47.6–99.5 0–129.53 333.1–1084.2 283.6–1034.7 571.9–2074.1 288.3–1039.4 0–1382.73 26–68.1 28.1–70.2 60.9–145.1 32.8–74.9 NR – 96.73 8.2–9.2 6.7–7.7 20.4–22.4 13.7–14.7 0–14.93 18.6–35.5 14.1–31 32.9–66.7 18.8–35.7 0–44.46 241–595 181.5–535.5 358.5–1066.5 177–531 Nr – 711 42–71.8 32.5–62.3 69.7–129.3 37.2–67 NR – 73.53 1469.2–51118.3 1409.7–51058.8 2452.4–101,751 1042.7–50691.8 0–67833.7 Sundarban Sundarban Sundarban Sundarban Sundarban Indian Indian Indian Indian Indian
119.7–36,556 67.22–36503.5 466.58–73,019 399.3–36515.5 NR – 48679.3
Co
10 ± 3 NR NR 0.03–69.1 0.1–87.5 0.4–82.3 0.2–91.9 14.5–48.6 13.4–36.1 18.35–35 1.32–25.1 16.42–41.8 NR NR NR 7.2–73.6 6.9–283.5 5.6–98.6 7.1–188.3 19.4–71.3 11.57–37.94 17.9–51.5 11.8–58.2 20.19–61.41
Cr Zn
2570 ± 830 5000 ± 231 5846 ± 7662 25.3–1046.9 21.1–1141.8 11.6–499.1 5.6–825.1 234.1–985.2 225.7–985.2 234.1–985.2 234.1–985.2 195.4–821 NR NR NR 5.8–67.7 9.9–195.5 9.8–99.4 8.3–180 30.2–72.3 17.8–49.2 26.7–58.4 26.7–58.4 28.47–65.12
Cu Cd
22 ± 6 7.1 ± 0.6 8.8 ± 3.2 0.4–132 2.9–92.1 3.4–35.1 1.4–141.8 5.2–6.2 4–9.32 4.9–7.3 3.2–9.4 5.05–6.35 NR NR NR 0.07–34.5 0.62–75 0.09–12.7 0.06–85.9 9.6–26.5 10.58–26.36 11.4–25.9 10.6–27.6 11.15–25.95
Pb Mn
NR NR NR 7.4–407.4 5.6–994.1 6.8–363.1 5.7–325.6 122–476 158–426 176.5–386 176.5–386 149.2–416.75 NR NR NR 15.4–335.7 23.8–517.4 3.1–396.8 2.7–954.9 23–52.8 23–65.1 27.3–49.4 27.3–49.2 27.2–50.35
Ni Al
NR NR NR 25–1384 57–3118 52–2870 20–2571 1350.2–50999.3 458.2–26212.3 1212.7–38587.2 1022.8–38587.2 1281.4–44774.6
Acartia clausi Acartia sp. Temora longicornis Canthocalanus pauper Oncaea venusta Temora discaudata Temora trubinata Bestiolina similis Paracalanus parvus Acartia spinicauda Acartiella tortaniformis Pseudodiaptomus serricaudatus Oithona sp. Labidocera euchaeta Eucalanus subcrassus Coryceaus danae Sagitta bedoti
Fe Location
Mediterranean Sea German Bight German Bight Northern Taiwan Northern Taiwan Northern Taiwan Northern Taiwan Sundarban, India Indian Sundarban Indian Sundarban Indian Sundarban Indian Sundarban
Species
Table 3 The trace metal concentrations in marine copepods (lg/g dry wt) in comparison with previous data NR: not reported.
NR NR NR NR NR NR NR 14.72–36,451 584–36,475 346.8–36587.2 348.1–36,463 180.76–36,457
Reference
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Fisher et al. (2000) Zauke et al. (1996) Zauke et al. (1996) Hsiao et al. (2011) Hsiao et al. (2011) Hsiao et al. (2011) Hsiao et al. (2011) Present study Present study Present study Present study Present study
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Bioaccumulation factors for metals represent the outcome of many processes involved in the bioaccumulation of metals in zooplankton. Hence, the bioaccumulation of metals in zooplankton depends upon bioavailability, the amount of dissolved metal uptake, the physiological efficiency of the organism to excrete metals, as well as on the feeding rate and prey availability (Rainbow, 1997). Differences in the bioaccumulation factors for elements like Co, Ni, Cu, Zn and Cd compared with the essential element Fe and non-essential element Pb, might be related to different physiology of copepods feeding in coastal and offshore waters (Rejomon et al., 2010). Wide fluctuation in the concentration of metals in different groups of zooplankton was observed. This can be attributed to the capacity of each group to concentrate a particular element by different means like direct uptake from seawater or assimilation of metals through ingested food. Probably the large surface to volume ratio of zooplankton leads to differences in the amount of accumulation through adsorption (Martin, 1970). Accumulation strategies vary between pure regulation and net accumulation, depending on the biological species and the chemical element considered (Rainbow et al., 1990). There are an increasing number of studies reporting trace metal contents in marine copepods. Zauke and Schmalenbach (2006) compared the published data from different marine and estuarine environments worldwide and showed that trace metal concentrations in copepods collected from the Farm Strait, the Greenland Sea and the Weddell Sea fell in the following ranges: Cd, 0.27–14.4 lg/ g; Cu, 38–51 lg/g; Pb, 0.09–10.7 lg/g; Ni, 2.1–18 lg/g; and Zn 59– 682 lg/g. Also Hsiao et al. (2011, 2006, 2010) determined the trace metal concentrations in marine dominant copepods from Taiwan coastal waters in details (Table 3). But from the Indian Sundarban coastal waters this study is the very new approach. The coastal and offshore enrichment of trace metals in zooplankton may be attributed to the peculiar hydrology pattern of the Bay of Bengal. The Bay of Bengal has an extensive coastal zone as well as deep basins with different water masses and receives massive freshwater inputs from nearby rivers to the coastal zone. The eastern shelf of the Bay of Bengal gets strongly affected by the entrainment of increased loads of fresh waters during monsoon, originating from the Ganges–Brahamaputra river system which in turn drops the salinity gradient to >8.0 psu in the nearby coastal zones (Prasanna Kumar et al., 2004). The impact of such a huge influx of freshwater discharge results the Bay of Bengal as a trap for trace metals especially in the coastal zone as evident conspicuously from the peaking up of metal content in water and zooplankton at the coastal regions of Sundarban mangrove wetland, which is also comparable to the trace metal content in zooplankton collective from off Vishakapatnam and off Madras coastal areas. The riverine input of dissolved metals are coastally trapped by eddies and also since shelf areas are under a directive influence of increased loads of trace metals from terrestrial sources relative to oceanic waters, it results in an average higher value for all the metals in coastal zooplankton samples, in the Bay of Bengal (Prasanna Kumar et al., 2004; Hydes and Kremling, 1993). Moreover a significant quantity of sediments impregnated with trace metals are also supplied by major rivers along the east coast of India and were constantly moved by coastally trapped waves either towards north or south depending on the direction and angle of wave approach with respect to the coast also results in a net accumulation of metals in coastal zooplankton from the Bay of Bengal (Rengasamy and Jing, 2005). Many studies have shown that chemical pollutants may affect copepods to various degrees ranging from sub-lethal to lethal effects, and thus impact copepods population dynamics (Hook and Fisher, 2001; Lindley, 1998). Hook and Fisher (2001) investigated the effect of exposure route on metal accumulation, tissue distribution, and toxicity in the marine copepods A. hudsonica
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and A. tonsa. Their results show that metals taken up through food can depress egg production in marine copepods when phytoplankton prey were exposed to 1 nM Hg or 5 nM Cd. They also indicate that this effect occurs when the metal burden in copepods increases only a few-fold over background levels. They further suggest that metals interfere with egg production by altering vitellogenesis so as to decrease yolk accumulation in the developing ovary. Similar results have also been reported by Lindley (1998) who examined the viability of copepod resting eggs from British estuaries in which the degree of chemical contamination varied. Their results demonstrate that the highest hatching success (92%) was observed for resting eggs from the estuary having the lowest concentration of PAHs. Conversely, lowest hatching success (14%) occurred in the estuary with the highest concentration of PAHs. The study first investigates a detailed account of heavy metal accumulation mainly in the copepods, the dominant mesozooplankter group, inhabiting in coastal regions of Sundarban wetland. The metal concentration difference within and between the species of copepods can vary many fold, suggesting that the bioaccumulative ability of copepods with respect to metals shows inter- and intra-species variability. Bioconcentration factors of copepods ranged from 4 to 6, confirming that the copepods have a great capacity to accumulate trace metals, and thus can rightly serve a potential indicator to assess metal concentration. Acknowledgements The work was financially supported jointly by the National Science Council of Taiwan (NSC 102-2923-B-019-001-MY3) with Department of Science and Technology (DST) & Confederation of Indian Industry (CII), New Delhi, India under India-Taiwan Programme in Science and Technology (Project Reference No. GITA/ DST/TWN/P-48/2013) as well as Council of Scientific and Industrial Research (CSIR), New Delhi (Sanction no. 09/028(0815)/2010-EMRI). The authors (Bhaskar Deb Bhattacharya and Soumita Mitra) are greatly indebted to the funding organizations (CSIR and DST/CII respectively) for extending them financial assistance. References Abdel-Satar, A.M., 2001. Environmental studies on the impact of the drain effluent upon the southern sector of Lake Manzalah, Egypt. Egyptian J. Aquat. Biol. Fisheries 5 (3), 17–30. APHA, 1989. Standard Methods for the Examination of Water and Wastewater, 17th ed. American Public Health. Association, American Water Works Association and Water Pollution Control Federation, Washington, DC, p. 1467. Brooks, R.R., Presley, B.J., Kaplan, I.R., 1967. APDC-MIBK extraction system for the determination of trace elements in saline waters by atomic absorption spectrophotometry. Talanta 14, 809. Demina, L.L., Galkin, S.V., Shumilin, E., 2009. Bioaccumulation of some trace elements in the biota of the hydrothermal fields of the Guaymas Basin (Gulf of California). Boletín Soc. Geol. Mexicana 61 (1), 31–45. Ferrer, L., Contardi, E., Andrade, S., Asteasuain, R., Pucci, A., Marcovecchio, J., 2000. Environmental cadmium and lead concentrations in the Bahía Blanca Estuary (Argentina). Potential toxic effects of Cd and Pb on crab larvae. Oceanologia 43, 493–504. Fisher, N.S., Nolan, C.V., Fowler, S.W., 1991. Assimilation of metals in marine copepods and its biogeochemical implications. Mar. Ecol. Prog. Ser. 71, 37–43. Fisher, N.S., Stupakoff, I., Sanudo-Wilhelmy, S., Wang, W.X., Teyssie, J.L., Fowler, S.W., Crusius, J., 2000. Trace metals in marine copepods: a field test of a bioaccumulation model coupled to laboratory uptake kinetics data. Mar. Ecol. Progr. Ser. 194, 211–218. Hamid, R., Fatimah, Y.M., Akito, K., 2010. Abundance and distribution of planktonic chaetognaths in the Strait of Malacca. Oceanography 1 (2), 11–19.
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Baseline
Bioaccumulation of trace elements in dominant mesozooplankton group inhabiting in the coastal regions of Indian Sundarban mangrove wetland Bhaskar Deb Bhattacharya a, Jiang-Shiou Hwang b, Li-Chun Tseng b, Santosh Kumar Sarkar a,⇑, Dibyendu Rakshit a, Soumita Mitra a a b
Department of Marine Science, University of Calcutta, 35 Ballygunge Circular Road, Calcutta 700019, India Institute of Marine Biology, National Taiwan Ocean University, Keelung 20224, Taiwan
a r t i c l e
i n f o
Article history: Available online 8 August 2014 Keywords: Mesozooplankton Copepods Trace metal Bioaccumulation factor Indian Sundarban
a b s t r a c t Mesozooplankton (Body size 20–200 lm) along with the surface water were collected from coastal regions of Sundarban, northeastern part of Bay of Bengal considering three seasons, namely premonsoon, monsoon and postmonsoon. Samples were analyzed for community structure and the dominant copepod species were further analyzed for trace metal concentration. In total, 50 copepods were identified (22 families and 43 genera). The dominant mesozooplankton species included 9 copepods and an epipelagic chaetognath, exhibited both spatial and seasonal variations. Metal concentration exhibited considerable inter-specific variations for the copepods and the mean concentrations were: Fe, 1350.2–51118.3 lg/g; Al, 647.2–73019.1 lg/g; Ni, 32.4–110.3 lg/g; Mn, 122.8–1066.5 lg/g; Pb, 0.04–97.5 lg/g; Pb, 10.6– 97.5 lg/g; Cd, 4.2–21.6 lg/g; Cu, 17.4–145.1 lg/g; Zn, 225.7–1670.9 lg/g; Cr, 21.7–194.3 lg/g; Co, 1.32–111.1 lg/g. Metal concentrations showed the following order: Sagitta bedoti > Coryceas danae > Oithona sp. > Eucalanus subcrassus > Labidocera euchaeta > Paracalanus parvus > Acartiella tortaniformis > Acartia spinicauda > Pseudocalanus serricaudatus. Ó 2014 Elsevier Ltd. All rights reserved.
Zooplankton play an important role in the biogeochemical cycling of metals in marine systems in general is well known, especially regarding particle-reactive metals in the water column (Fisher et al., 1991; Lee and Fisher, 1994; Stewart et al., 2005). Thus, in several studies macro- and meso-zooplankton organisms have been specifically used as biomonitors for assessment of the bioavailability of elements in marine systems, covering a variety of spatial and temporal scales (Kahle and Zauke, 2003; Ritterhoff and Zauke, 1997; Zauke et al., 1996). Their potential suitability is largely due to their worldwide presence, their major role in the food webs and their high contribution to the total biomass in marine systems. The Indian Sundarban, formed at the estuarine phase of the tidal Hugli River of an area of 9600 km2, is a tide-dominated mangrove wetland belonging to the low-lying coastal zone (Fig. 1). This is one of the most dynamic, complex and vulnerable bioclimatic zone in a typical, tropical geographical location in the northeastern part of the Bay of Bengal. The wetland is characterized by a complex network of tidal creeks, which surround hundreds of tidal islands exposed to different elevations at high and
⇑ Corresponding author. Fax: +91 33 2461 4849. E-mail address: [email protected] (S.K. Sarkar). http://dx.doi.org/10.1016/j.marpolbul.2014.07.050 0025-326X/Ó 2014 Elsevier Ltd. All rights reserved.
low semi-diurnal tides. This coastal environment suffers from environmental degradation due to rapid human settlement, tourism and port activities, and operation of mechanized boats, deforestation and increasing agricultural and aquaculture practices. The ongoing degradation is also related to huge siltation, flooding, storm runoff, atmospheric deposition and other stresses resulting in changes in water quality, depletion of fishery resources, choking of river mouth and inlets, and overall loss of biodiversity as evident in recent years (Sarkar and Bhattacharya, 2003; 2008). A significant ecological change is pronounced in this area due to reclamation of land, deforestation, huge discharges of untreated or semi-treated domestic, municipal and agricultural wastes as well as effluents from multifarious industries (Fig. 1) carried by the rivers as well as contaminated mud disposal from harbor dredging (Sarkar et al., 2007). The upstream of the Hugli River flows through some of the most industrialized (jute mill, textile, tannery, thermal power, oil refinery as shown in Fig. 1) and urbanized (megacity Calcutta and Howrah) regions which make it one of the highly human-impacted rivers in India. The huge discharge of trace metals has a crucial influence on the total load and distribution of elements in the coastal regions of Sundarban. This study has been undertaken to assess the role of mesozooplankton in the biogeochemical cycles. Copepods have been chosen as recommended organisms as they are considered best biomarkers
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B.D. Bhattacharya et al. / Marine Pollution Bulletin 87 (2014) 345–351
Fig. 1. Map of The Indian Sundarban and Sagar Island (enlarged) in details showing the three sampling sites S1, S2 and S3 along N-S direction.
for trace metal monitoring in marine environment because of their huge biomass, limited swimming capacity, vital role in trophic chains, easy availability and sensitivity to trace metal contamination. Three stations have been chosen along south north gradient of high to low salinity for the present study situated in the western flank of Sundarban namely, Lot No. 8 (S1), Chemaguri (S2) and Gangasagar (S3). The selected sampling sites belong to distinctive geographic, geomorphic and hydrological settings with variations of energy domains characterized by wave-tide climate. The sites have diverse human interferences with a variable degree of exposure to trace metal pollution. The surface water and mesozooplankton samples were collected (during 2011 and 2012) seasonally (premonsoon, monsoon and postmonsoon) from three sites distributed on the eastern and western flank of the Sundarban wetland. On each site, water samples (approx. 100 cc.) were filtered through cellulose acetate membrane filter (pore diameter 0.45 lm) and 2 ml 65% nitric acid (Merck) were added after that, water samples were transferred in polyethylene flasks, and they were immediately transported to the laboratory at ±4 °C. The temperature and salinity of water were measured on board, using thermometer (mercury, 0–100 °C) and refractometer respectively. pH of the water was measured by digital pH meter (Model No. 101 E) and turbidity was measured by using turbidity meter (Model no: SYS 304 E). Mesozooplankton samples were collected by towing a Ring Trawl plankton net (mesh size 200-lm). The net was towed obliquely at 1 m below the surface for ten minutes. Zooplankton samples were sorted under a binocular microscope and visually observed to ensure the absence of any foreign particles. On board the plankton samples were sorted and identified up to species level. Copepods were the most abundant taxa in the zooplankton samples followed by chaetognath. Ten dominant mesozooplankton species of diverse feeding guilds such as Bestiolina similis, Paracalanus parvus, Acartia spinicauda, Acartiella tortaniformis, Pseudodiaptomus serricaudatus, Oithona sp., Labidocera euchaeta, Eucalanus subcrassus and Coryceaus danae and the solitary epipelagic chaetognath (Sagitta bedoti) were separated and considered for further analyses of trace metals. Collected plankton samples were divided
into two parts. The first part was transferred to buffered formalin for detailed quantitative analyses and the other part was placed in a small nylon sieve and was thoroughly rinse with Milli-Q water to remove salts. To avoid any possible entrainment of elements on the surface of the zooplanktonic organisms, each zooplankton sample was washed three times with distilled water for elimination of fine particulates of trace elements of terrigenous origin (Demina et al., 2009; Rentería-Cano et al., 2011). Then it was kept deep frozen for trace metals analyses in the laboratory. The concentration of dissolved metals were determined in water by solvent extraction using ammonium pyrrolidine dithiocarbamate (APDC) and methyl isobutyl ketone (MIBK) as a standard method (APHA, 1989). A 1% aqueous solution of APDC (Eastman Chemicals) was prepared daily and purified by shaking with an equal volume of MIBK, separating the phases and filtering the lower aqueous phase. Since APDC is only slightly soluble in MIBK whereas metal complexes are highly soluble, the reagent is easily purified in this manner. Reagent grade MIBK was used throughout without further purification. Ammonium acetate (Sigma, Mumbai) buffer (5N) was prepared and metallic impurities were removed by adding a few milliliters of APDC solution and extracting with MIBK. The dissolved metals were simultaneously extracted from filtered water samples by chelation with APDC followed by MIBK extraction according to method described in literature (Ferrer et al., 2000; Brooks et al., 1967; Koirtyohanm and Wen, 1973; Murakami et al., 1992). All experiments were carried out in a pH range of 2–6. Extractions were done in a separatory funnel shaken for 2 min. by hand with 50 ml of aqueous volume, 1 ml of APDC solution and 10 ml of MIBK. When the highest possible accuracy was required the organic phase was placed in a 10 ml volumetric flask and diluted to volume with water saturated MIBK. This eliminated the error caused by variation in the volume of organic phase lost because of solubility. Concentration of the dissolved metals was measured in a graphite-furnace Atomic Absorption Spectrophotometer (Perkin–Elmer, Graphite Furnace). Standardization was based on a two-point calibration procedure, using a multi element standard (J.T. Backer, Inc. Phillsburg NJ) as the high standard, and double distilled water (zero metal concentration) as the low standard. Standardization of the instrument was
B.D. Bhattacharya et al. / Marine Pollution Bulletin 87 (2014) 345–351 Table 1 Quality assurance using CRM randomly allocated within the determination. Metals
Fe Al Ni Mn Pb Cd Cu Zn Cr Co
DORM-2
TORT-2
Certified values
Measured values
Certified values
Measured values
142 10.90 19.40 3.66 0.065 0.043 2.34 25.60 34.70 0.182
141.07 10.04 19.30 3.49 0.062 0.041 2.29 25.20 34.50 0.179
105 – 2.50 13.60 0.35 26.70 106 180 0.77 0.51
104.80 – 2.30 13.30 0.30 26.30 106 179.70 0.72 0.50
repeated after every three sets of seawater extracts to minimize the effect of instrument drift. Distilled water and a check standard were also included in the analysis sequence. In laboratory, the frozen copepod sample was kept out of the freezer and the water adhering to the samples was removed by placing the sieve on good quality filter paper, without any contamination. The frozen samples were lyophilized and homogenized. Then a 0.5 g sub-sample was taken and subjected to wet digestion (HNO3:HClO4 = 3:1; v/v). Excess of acids was evaporated and the dry residue was dissolved in 10 cm3 of HNO3 (0.1 mol/dm3) solution. Metals, in the so obtained solutions, were analyzed by means of atomic absorption spectrometry (a model Video 11E Thermo Jarrel Ash spectrometer was used). Either electrothermal (Cd, Ni, Cr, Co, Pb) or flame (Fe, Zn, Mn–acetylene/air; Al–acetylene/nitrous oxide) atomization was applied. Blanks were run in parallel with actual samples. Average blanks varied in the range from 0% (for Fe) to 7% (for Cd) of the mean metals concentrations in the analyzed solutions. Quality control was achieved by analyzing DORM 2 and TORT 2 (results shown in Table 1).
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Total 50 mesozooplankton taxonomic groups were identified. Mesozooplankton abundance was higher during the dry season (>1000 ind. m3) than the monsoon season ( Al > Mn > Zn > Ni > Cu > Cr > Co > Pb > Cd. Majority of the metals showed relatively high concentrations during late premonsoon period in comparison to the low flow condition (early postmonsoon) which is attributed to high evaporation rate of surface water followed by elevated temperature (Abdel-Satar, 2001). The negative relationships of Mn with majority of the metals (excepting Cu) were recorded suggesting that Mn-oxide may be only a minor host phase for these metals. Non-significant correlations of Mn with all the metals are due to the different processes like biological effects and external inputs operating in estuarine system (Ray et al., 2006). Significant correlations between Cu with Co (r = 0.69) and Ni (0.76), Ni with Zn (r = 0.514) and Pb (0.638) and Zn with Cd (r = 0.857) indicate the possible enrichment of all these four metals partly through terrigenous origin and partly due to the biological production. The concentrations of trace metals in the 10 dominant species of mesozooplankton collected at all stations are shown in Table 2 and plotted in Fig. 3. The concentrations ranged as follows: Fe, 1350.2– 51118.3 lg/g; Al, 647.2–73019.1 lg/g; Ni, 32.4–110.3 lg/g; Mn, 122.8–1066.5 lg/g; Pb, 0.04–97.5 lg/g; Pb, 10.6–97.5 lg/g; Cd, 4.2–21.6 lg/g; Cu, 17.4–145.1 lg/g; Zn, 225.7–1670.9 lg/g; Cr, 21.7–194.3 lg/g; and Co, 1.32–111.1 lg/g. The average concentration of trace metals in all the analyzed mesozooplankton samples followed the sequence: Fe > Al > Z n > Cu > Mn > Ni > Cr > Cd > Co > Pb. The inter- and intra-variability in concentration turns out to be quite considerable (up to 10–100 fold variations). To compare the trace metal contents in the different copepods species, metal concentrations in each species were normalized to the metal content of B. similis. The sequence of sums of the normalized values of all metals in each species was: S. bedoti > C. danae > Oithona sp. > E. subcrassus > L. euchaeta > P. parvus > A. tortoniformis > A. spinicauda > P. serricaudatus. The highest
Fig. 4. Trace metal bioconcentration factors in copepods obtained in this study.
metal quota was found in S. bedoti which is carnivorous in nature (Hamid et al., 2010; Sarkar et al., 1986). High metal bioavailability results in high concentrations of the corresponding metals in biota through the so-called bioconcentration process. The bioconcentration factor (BCF) can provide knowledge of how enriched organisms are in particular elements, with respect to the surrounding environment. The average order of magnitude of the BCF (Cm/Cw; Cm, and Cw represent the metal concentration in copepods and water, respectively) of copepods for trace metals in the present study ranged from 4.5 to 6.5 (Fig. 4) and followed the sequence:
Znð12:06Þ > Crð2:05Þ > Cuð1:80Þ > Cdð1:76Þ > Coð1:67Þ > Pbð1:62Þ > Nið1:36Þ > Mnð1:31Þ > Alð0:58Þ > Feð0:45Þ
study study study study study Present Present Present Present Present 27.5–61.6 21–55.1 46.7–114.9 25.7–59.8 NR – 74.06 66.4–118.3 42.9–94.8 90.5–194.3 47.6–99.5 0–129.53 333.1–1084.2 283.6–1034.7 571.9–2074.1 288.3–1039.4 0–1382.73 26–68.1 28.1–70.2 60.9–145.1 32.8–74.9 NR – 96.73 8.2–9.2 6.7–7.7 20.4–22.4 13.7–14.7 0–14.93 18.6–35.5 14.1–31 32.9–66.7 18.8–35.7 0–44.46 241–595 181.5–535.5 358.5–1066.5 177–531 Nr – 711 42–71.8 32.5–62.3 69.7–129.3 37.2–67 NR – 73.53 1469.2–51118.3 1409.7–51058.8 2452.4–101,751 1042.7–50691.8 0–67833.7 Sundarban Sundarban Sundarban Sundarban Sundarban Indian Indian Indian Indian Indian
119.7–36,556 67.22–36503.5 466.58–73,019 399.3–36515.5 NR – 48679.3
Co
10 ± 3 NR NR 0.03–69.1 0.1–87.5 0.4–82.3 0.2–91.9 14.5–48.6 13.4–36.1 18.35–35 1.32–25.1 16.42–41.8 NR NR NR 7.2–73.6 6.9–283.5 5.6–98.6 7.1–188.3 19.4–71.3 11.57–37.94 17.9–51.5 11.8–58.2 20.19–61.41
Cr Zn
2570 ± 830 5000 ± 231 5846 ± 7662 25.3–1046.9 21.1–1141.8 11.6–499.1 5.6–825.1 234.1–985.2 225.7–985.2 234.1–985.2 234.1–985.2 195.4–821 NR NR NR 5.8–67.7 9.9–195.5 9.8–99.4 8.3–180 30.2–72.3 17.8–49.2 26.7–58.4 26.7–58.4 28.47–65.12
Cu Cd
22 ± 6 7.1 ± 0.6 8.8 ± 3.2 0.4–132 2.9–92.1 3.4–35.1 1.4–141.8 5.2–6.2 4–9.32 4.9–7.3 3.2–9.4 5.05–6.35 NR NR NR 0.07–34.5 0.62–75 0.09–12.7 0.06–85.9 9.6–26.5 10.58–26.36 11.4–25.9 10.6–27.6 11.15–25.95
Pb Mn
NR NR NR 7.4–407.4 5.6–994.1 6.8–363.1 5.7–325.6 122–476 158–426 176.5–386 176.5–386 149.2–416.75 NR NR NR 15.4–335.7 23.8–517.4 3.1–396.8 2.7–954.9 23–52.8 23–65.1 27.3–49.4 27.3–49.2 27.2–50.35
Ni Al
NR NR NR 25–1384 57–3118 52–2870 20–2571 1350.2–50999.3 458.2–26212.3 1212.7–38587.2 1022.8–38587.2 1281.4–44774.6
Acartia clausi Acartia sp. Temora longicornis Canthocalanus pauper Oncaea venusta Temora discaudata Temora trubinata Bestiolina similis Paracalanus parvus Acartia spinicauda Acartiella tortaniformis Pseudodiaptomus serricaudatus Oithona sp. Labidocera euchaeta Eucalanus subcrassus Coryceaus danae Sagitta bedoti
Fe Location
Mediterranean Sea German Bight German Bight Northern Taiwan Northern Taiwan Northern Taiwan Northern Taiwan Sundarban, India Indian Sundarban Indian Sundarban Indian Sundarban Indian Sundarban
Species
Table 3 The trace metal concentrations in marine copepods (lg/g dry wt) in comparison with previous data NR: not reported.
NR NR NR NR NR NR NR 14.72–36,451 584–36,475 346.8–36587.2 348.1–36,463 180.76–36,457
Reference
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Fisher et al. (2000) Zauke et al. (1996) Zauke et al. (1996) Hsiao et al. (2011) Hsiao et al. (2011) Hsiao et al. (2011) Hsiao et al. (2011) Present study Present study Present study Present study Present study
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Bioaccumulation factors for metals represent the outcome of many processes involved in the bioaccumulation of metals in zooplankton. Hence, the bioaccumulation of metals in zooplankton depends upon bioavailability, the amount of dissolved metal uptake, the physiological efficiency of the organism to excrete metals, as well as on the feeding rate and prey availability (Rainbow, 1997). Differences in the bioaccumulation factors for elements like Co, Ni, Cu, Zn and Cd compared with the essential element Fe and non-essential element Pb, might be related to different physiology of copepods feeding in coastal and offshore waters (Rejomon et al., 2010). Wide fluctuation in the concentration of metals in different groups of zooplankton was observed. This can be attributed to the capacity of each group to concentrate a particular element by different means like direct uptake from seawater or assimilation of metals through ingested food. Probably the large surface to volume ratio of zooplankton leads to differences in the amount of accumulation through adsorption (Martin, 1970). Accumulation strategies vary between pure regulation and net accumulation, depending on the biological species and the chemical element considered (Rainbow et al., 1990). There are an increasing number of studies reporting trace metal contents in marine copepods. Zauke and Schmalenbach (2006) compared the published data from different marine and estuarine environments worldwide and showed that trace metal concentrations in copepods collected from the Farm Strait, the Greenland Sea and the Weddell Sea fell in the following ranges: Cd, 0.27–14.4 lg/ g; Cu, 38–51 lg/g; Pb, 0.09–10.7 lg/g; Ni, 2.1–18 lg/g; and Zn 59– 682 lg/g. Also Hsiao et al. (2011, 2006, 2010) determined the trace metal concentrations in marine dominant copepods from Taiwan coastal waters in details (Table 3). But from the Indian Sundarban coastal waters this study is the very new approach. The coastal and offshore enrichment of trace metals in zooplankton may be attributed to the peculiar hydrology pattern of the Bay of Bengal. The Bay of Bengal has an extensive coastal zone as well as deep basins with different water masses and receives massive freshwater inputs from nearby rivers to the coastal zone. The eastern shelf of the Bay of Bengal gets strongly affected by the entrainment of increased loads of fresh waters during monsoon, originating from the Ganges–Brahamaputra river system which in turn drops the salinity gradient to >8.0 psu in the nearby coastal zones (Prasanna Kumar et al., 2004). The impact of such a huge influx of freshwater discharge results the Bay of Bengal as a trap for trace metals especially in the coastal zone as evident conspicuously from the peaking up of metal content in water and zooplankton at the coastal regions of Sundarban mangrove wetland, which is also comparable to the trace metal content in zooplankton collective from off Vishakapatnam and off Madras coastal areas. The riverine input of dissolved metals are coastally trapped by eddies and also since shelf areas are under a directive influence of increased loads of trace metals from terrestrial sources relative to oceanic waters, it results in an average higher value for all the metals in coastal zooplankton samples, in the Bay of Bengal (Prasanna Kumar et al., 2004; Hydes and Kremling, 1993). Moreover a significant quantity of sediments impregnated with trace metals are also supplied by major rivers along the east coast of India and were constantly moved by coastally trapped waves either towards north or south depending on the direction and angle of wave approach with respect to the coast also results in a net accumulation of metals in coastal zooplankton from the Bay of Bengal (Rengasamy and Jing, 2005). Many studies have shown that chemical pollutants may affect copepods to various degrees ranging from sub-lethal to lethal effects, and thus impact copepods population dynamics (Hook and Fisher, 2001; Lindley, 1998). Hook and Fisher (2001) investigated the effect of exposure route on metal accumulation, tissue distribution, and toxicity in the marine copepods A. hudsonica
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and A. tonsa. Their results show that metals taken up through food can depress egg production in marine copepods when phytoplankton prey were exposed to 1 nM Hg or 5 nM Cd. They also indicate that this effect occurs when the metal burden in copepods increases only a few-fold over background levels. They further suggest that metals interfere with egg production by altering vitellogenesis so as to decrease yolk accumulation in the developing ovary. Similar results have also been reported by Lindley (1998) who examined the viability of copepod resting eggs from British estuaries in which the degree of chemical contamination varied. Their results demonstrate that the highest hatching success (92%) was observed for resting eggs from the estuary having the lowest concentration of PAHs. Conversely, lowest hatching success (14%) occurred in the estuary with the highest concentration of PAHs. The study first investigates a detailed account of heavy metal accumulation mainly in the copepods, the dominant mesozooplankter group, inhabiting in coastal regions of Sundarban wetland. The metal concentration difference within and between the species of copepods can vary many fold, suggesting that the bioaccumulative ability of copepods with respect to metals shows inter- and intra-species variability. Bioconcentration factors of copepods ranged from 4 to 6, confirming that the copepods have a great capacity to accumulate trace metals, and thus can rightly serve a potential indicator to assess metal concentration. Acknowledgements The work was financially supported jointly by the National Science Council of Taiwan (NSC 102-2923-B-019-001-MY3) with Department of Science and Technology (DST) & Confederation of Indian Industry (CII), New Delhi, India under India-Taiwan Programme in Science and Technology (Project Reference No. GITA/ DST/TWN/P-48/2013) as well as Council of Scientific and Industrial Research (CSIR), New Delhi (Sanction no. 09/028(0815)/2010-EMRI). The authors (Bhaskar Deb Bhattacharya and Soumita Mitra) are greatly indebted to the funding organizations (CSIR and DST/CII respectively) for extending them financial assistance. References Abdel-Satar, A.M., 2001. Environmental studies on the impact of the drain effluent upon the southern sector of Lake Manzalah, Egypt. Egyptian J. Aquat. Biol. Fisheries 5 (3), 17–30. APHA, 1989. Standard Methods for the Examination of Water and Wastewater, 17th ed. American Public Health. Association, American Water Works Association and Water Pollution Control Federation, Washington, DC, p. 1467. Brooks, R.R., Presley, B.J., Kaplan, I.R., 1967. APDC-MIBK extraction system for the determination of trace elements in saline waters by atomic absorption spectrophotometry. Talanta 14, 809. Demina, L.L., Galkin, S.V., Shumilin, E., 2009. Bioaccumulation of some trace elements in the biota of the hydrothermal fields of the Guaymas Basin (Gulf of California). Boletín Soc. Geol. Mexicana 61 (1), 31–45. Ferrer, L., Contardi, E., Andrade, S., Asteasuain, R., Pucci, A., Marcovecchio, J., 2000. Environmental cadmium and lead concentrations in the Bahía Blanca Estuary (Argentina). Potential toxic effects of Cd and Pb on crab larvae. Oceanologia 43, 493–504. Fisher, N.S., Nolan, C.V., Fowler, S.W., 1991. Assimilation of metals in marine copepods and its biogeochemical implications. Mar. Ecol. Prog. Ser. 71, 37–43. Fisher, N.S., Stupakoff, I., Sanudo-Wilhelmy, S., Wang, W.X., Teyssie, J.L., Fowler, S.W., Crusius, J., 2000. Trace metals in marine copepods: a field test of a bioaccumulation model coupled to laboratory uptake kinetics data. Mar. Ecol. Progr. Ser. 194, 211–218. Hamid, R., Fatimah, Y.M., Akito, K., 2010. Abundance and distribution of planktonic chaetognaths in the Strait of Malacca. Oceanography 1 (2), 11–19.
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