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Chemosphere 107 (2014) 336–343
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Bioturbation/bioirrigation by Chironomus plumosus as main factor controlling elemental remobilization from aquatic sediments? Jörg Schaller ⇑ Institute of General Ecology and Environmental Protection, Technische Universität Dresden, PF 1117, 01737 Tharandt, Germany
h i g h l i g h t s
g r a p h i c a l a b s t r a c t
Chironomus plumosus has a main
impact on elemental mobilization from sediments. DOC, N, Mg, Ca, Sr, Mo and U were highly influenced by bioturbation/ bioirrigation. Al, Fe, Co, Cu, Zn and Ce were affected only at start (larvae dig into sediments). Mn, Ni, As, Cd and Cs mobilization were affected at start and slightly afterwards. Invertebrate bioturbation/ bioirrigation is a main process in element cycling.
a r t i c l e
i n f o
Article history: Received 22 August 2013 Received in revised form 19 December 2013 Accepted 20 December 2013 Available online 20 January 2014 Keywords: Bioaccumulation DOC Macrozoobenthos Mining Nutrients Wetland
a b s t r a c t Aquatic sediments represent a possibly significant sink of soluble inorganic elements/pollutants (metals, metalloids and rare earth elements) in ecosystems. Bioturbation/bioirrigation was shown to affect the remobilization of some elements where others seem to be unaffected. In view of these contrasting results, the effect of bioturbation/bioirrigation was examined using the invertebrate Chironomus plumosus in a laboratory experiment for a broad range (18) of elements. The experiments revealed an impact of invertebrate bioturbation/bioirrigation on elemental remobilization depending on chemical characteristics of the element ranging from strong influence to influence only at start when the larvae dig into the sediments. Three different types of remobilization were found: (i) element mobilization highly influenced by bioturbation/ bioirrigation (DOC, N, Mg, Ca, Sr, Mo and U), (ii) strong element mobilization by bioturbation/bioirrigation at the start of the experiment when the larvae dig into the sediments and afterwards strong decrease, but to higher levels compared to values of treatments without invertebrate impact (Mn, Ni, As, Cd and Cs), and (iii) strong element mobilization by bioturbation/bioirrigation at start when the larvae dig into the sediments and afterwards strong decrease to levels found in treatments without invertebrate impact (Al, Fe, Co, Cu, Zn and Ce). During the experiment a distinct accumulation of most of the elements in C. plumosus was found, where they were not so much bound to the outer surface of C. plumosus but more within the gut system including food and feces. Hence, bioturbation/bioirrigation is certainly a main process controlling mobilization of elements from sediments. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction
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High concentrations of metals and metalloids in water and aquatic sediments are a global problem for freshwater ecosystems (Kraak et al., 1991; Biney et al., 1994; Kouba et al.,
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J. Schaller / Chemosphere 107 (2014) 336–343
2010; Schaller et al., 2013). Metals, metalloids, rare earth elements and radionuclides drain in high amounts from ore deposits, enhanced by mining activity, or industrial waste waters into freshwater ecosystems (Dudka and Adriano, 1997; Moiseenko and Kudryavtseva, 2001). Elements are transported by running water as cations, inorganic complexes, organic complexes of humic and fulvic acids as part of dissolved organic matter (DOC) (Christensen et al., 1999; Alberic et al., 2000) and/or associated with suspended particles (e.g. colloids). The complexes themselves may adsorb to organic and inorganic particles leading to a deposit in freshwater sediments (Schaller et al., 2010b, 2013; Schaller, 2013). A process known to be involved in both element remobilization from these sediments and element fixation from the water body into the sediment, is bioturbation/ bioirrigation (Lewandowski and Hupfer, 2005). Bioturbation/ bioirrigation is generated by the activity of animals within upper sediment layers (Lewandowski and Hupfer, 2005). This process is resulting in an upward transport of chemically reduced sediment particles (Brandes and Devol, 1995). Despite clearly described effects of this process on phosphor (enhanced fixation by sediments due to increased redox potential (Lewandowski and Hupfer, 2005)), data for metals and metalloids contradict. Some studies suggest (Schaller et al., 2011b) or even demonstrate an increased remobilization of some metals by bioturbation/bioirrigation (Lagauzere et al., 2009) where others find no effect (Mermillod-Blondin et al., 2005) or even increased fixation within the sediment (Lewandowski and Hupfer, 2005), which may be due to specific elemental properties. Furthermore, no study exists evaluating the effect of bioturbation/bioirrigation on metal/metalloids remobilization/fixation using sediments with multi-elemental (metals/metalloids/radionuclides/rare earth elements) contamination, outlining the differences between elements. An animal with high bioturbation/bioirrigation potential and high abundance is most suitable for testing these effects. This animal must be able to reduce elemental uptake and/or have available detoxification measures to prevent toxicity effects as shown for other animals (Tigriopus brevicornis and Orchestia gammarellus) (Mouneyrac et al., 2002; Barka et al., 2010). Such an animal is the larvae of Chironomus plumosus (representing the macrozoobenthos), with a very high abundance per m2 in lake sediments (Gallepp, 1979) and low negative effect by high concentration of metals/radionuclides in water and sediment (Vedamanikam and Shazilli, 2008; Liber et al., 2011). Consequently, the aim of this study was to assess the effect of bioturbation/bioirrigation on metal/metalloid/rare earth element remobilization from sediments to water using multi-element (metal/metalloid/radionuclide/rare earth elements) contaminated sediments in batch culture with invertebrate larvae of C. plumosus as bioturbator. Furthermore, the accumulation of the elements within the invertebrates was investigated.
2. Material and methods 2.1. Sediment collection and preparation Organic rich sediments were sampled from a stream in an alder swamp forest at a former uranium mining site in NeuensalzMechelgrün (Germany) (50°290 51.4000 N, 12°140 28.4400 E) as described in Mkandawire et al. (2005). A batch of about 10 L was excavated, homogenized and immediately sieved (nylon sieve with a mesh size of 1000 lm) followed by a draining step (nylon net with a mesh size of 125 lm) to adjust the water content before transfer to laboratory.
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2.2. Experimental setup The test vessels consisted of Plexiglas (12 cm diameter) each filled with 500 g of homogenized sediment, 1 L aqueous medium (lake water with low metal/metalloid concentration, pH = 7.6 and Eh = 200 mV) and one air diffuser with an aeration rate of 0.25 L per minute resulting in a permanently homogenization of the water body. The sediment had a high carbon (11.8% of dry matter) and nitrogen (0.76% of dry matter) content. Two different treatments were used with five replicates each. The first treatment (C+) contained additionally 200 individuals of C. plumosus per vessel, which is at the high end of natural abundance (Gallepp, 1979). The other treatment (control treatment) (C) was set up without invertebrates. The experiments ran for 3 d. The invertebrates were analyzed at the start and end of the experiment. To distinguish between elemental adsorption and real uptake of elements by the used invertebrates, a desorption experiment was conducted as follows. At the start and end of experiment ten specimens were dried at 40 °C. The other 15 specimens were stored in a vessel containing 5 L of tap water to remove metals/metalloids/rare earth elements attached to the body surface by the process of concentration equilibrium, according to Schaller et al. (2011a). The water used had the same pH and hardness as the water at the start of experiment. After this, another five specimens were dried at 40 °C, the gut system was then dissected from the remaining ten specimens. The specimens, gut systems and remaining tissues were dried. 2.3. Sampling, sample preparation and analysis The aqueous medium was sampled at the beginning and 5 h, 24 h, 48 h and 36 h after starting the experiment, always at the same point in the same depth for each test vessel and treatment. Water samples were filtered using 0.45 lm cellulose-acetate filters and subsequently acidified with HNO3. A second sample aliquot was taken for analysis of dissolved organic carbon (DOC). These samples were stored in a freezer at 20 °C. Sediment samples were taken at the beginning and at the end of the experiment and dried afterwards. The pH value (Electrode: Mettler Toledo INLAB 414, unit: Delta 320, Germany), the conductivity and the temperature (both with 95 Lf, WTW, Germany) were measured in permanently (by aeration) mixed water body on a daily basis. Redox potential was measured using platinum redox-electrodes with Ag/AgCl-reference electrode according to Mansfeldt (2003). The determination of elemental concentrations was performed using an inductively coupled plasma mass spectrometer (ICPMS), equipped with a liquid sample introduction system. Water samples were measured directly, sediment samples were digested in a closed vessel microwave system (MARS5 CEM Corp., Matthews, United States) using nitric and hydrochloric acid according to DIN-EN-13346 (2001). Animal samples were also wet digested in a closed vessel system (addition of 3 mL of 65% HNO3 and 2 mL of H2O2). All water samples were acidified and kept at room temperature in conformity with DIN-EN-ISO-5667 (2004). For ICPMS measurement an X-series instrument (Thermo Fisher Scientific Inc., Germany) was used according to DIN-EN-ISO-17294-2 (2004). The instrument was operated in standard mode. Calibration functions were recorded from mixed calibration samples, which were prepared from single element solutions (uranium: Ultra Scientific, Kingstown, UK) and multi-element solutions (Bernd Kraft, Duisburg, Germany). Calibration validity was confirmed with standard reference material GBW7604, poplar leaves (Office of CRM’s, China), digested in the same manner as the sediment samples. Limit of detection (LOD) was calculated as the threefold standard deviation of instrument blank (acidified water).
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experiment, whereas for the comparison of the water and sediment data at start of experiment as well as the different tissues of the invertebrates the t-test was performed using SPSS version 16.01.
Table 1 Elemental content of the used sediments at start of experiment. Values are in mg kg1 DW1 for mean and standard deviation (n = 10). Element
Mean
SD
Mg Al Ca Mn Fe Co Ni Cu Zn As Sr Mo Cd Cs Ce U
6397 36 870 16 872 53 052 28 998 72 312 272 322 406 151 11 8 21 77 89
236 2425 743 1980 1026 1 9 10 11 17 6 1 0 1 2 9
3. Results and discussion 3.1. Experimental performance The sediments used in the experiment showed very high contents of metals/metalloids/rare earth elements at the beginning (Table 1) of the experiment. No significant differences between the two treatments and between start and end were found (for all p > 0.3; data not shown). After 3 d the experiment was terminated to avoid negative effects on invertebrate health and hence an influence on the bioturbation/bioirrigation process due to very high element water content and high conductivity in the water body. Significant differences in conductivity were found between the treatments with (C+) and without (C) bioturbation/bioirrigation (p < 0.001) (Fig. 1). No differences in pH level (pH = 7.6 at start and 8.4 at the end) were found between the treatments during the experiment. The redox measurements at 5 cm sediment depth revealed no differences between the treatments with a constant redox potential of about 200 mV. This can be explained by strong respiration processes due to high temperature and high carbon compounds comparable with shallow lake sediments in summer (Jensen and Andersen, 1992). The temperature increased from 18 to 20 °C, not differing between the treatments. The dissolved organic carbon (DOC) and total nitrogen concentration in the water body increased during the experiment and were significantly higher in treatments with bioturbation/bioirrigation (p < 0.001) (Fig. 1). This can be explained by excretion of the animals (Vanni, 2002) and increasing heterotrophic processes (decomposition of
Dissolved organic carbon (DOC) and total nitrogen (TN) in water samples were determined with a FORMACS HT TC/TN Analyzer (Skalar, Breda, The Netherlands). The analyzer uses a combustion process and the procedure follows DIN-EN-1484 (1997). Calibration samples were prepared from commercial standards (Bernd Kraft, Duisburg, Germany). Carbon and nitrogen contents in the solid samples were measured in a combustion device (Elementar vario el III, Hanau, Germany) according to DIN-ISO-10694 (1995). All chemicals used in the experiment were of analytical grade.
2.4. Statistical analysis Analysis of variance (ANOVA) was used to explore the impact of C. plumosus on elemental mobilization (time series) during the
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sediment organic matter content) within the sediment (Gessner et al., 2010) based on the oxygen input. The organic matter content has its origin in the input of litter from a local alder stand, indicated by the resulting low molar C/N ratio of 15.6 as found previously (Schaller et al., 2011d).
who found the same effect of bioturbation/bioirrigation by tubifex on U remobilization. The Mo data may be explained by either the reverse redox chemistry (like U), by strong binding of Mo to DOC as found previously (Kerr et al., 2008; Schaller et al., 2010a) or by binding to manganese (Mn) and thus release from sediment, if Mn is released from sulfidic sediments, as it has been suggested for such homogenized sediments as used in this experiments (Michaud et al., 2010). For the other elements the increased remobilization may be explained by suspension of sediment particles by bioturbation at start when the larvae dig into the sediments (data not shown), which in turn increases the sediment water contact zone resulting in higher mobilization of some elements (Lewandowski and Hupfer, 2005). A different pattern was found for aluminum (Al), iron (Fe), cobalt (Co), copper (Cu), zinc (Zn) and cerium (Ce) with a strong increase of remobilization within the first 5 h of the experiment in the treatment with invertebrates (C+) (when the larvae dig into the sediments) compared to the treatment without invertebrates (C) followed by a sharp decrease reaching values of the treatment without invertebrates. The strong increase during the first 5 h can be explained by the effects from burying (dig in) of the invertebrates into the sediment and the resulting suspension of sediment particles (see above) (Atkinson et al., 2007). After
3.2. Enhanced elemental remobilization by bioturbation/bioirrigation Significant higher metal/metalloid/rare earth element remobilization (p < 0.001) in the treatment with invertebrate bioturbation/ bioirrigation compared to the treatment without invertebrate impact was found for all elements. However, different patterns of metal/metalloid/rare earth element remobilization between the different elements were found. An increasing metal/metalloid water concentration was found for magnesium (Mg), calcium (Ca), strontium (Sr), molybdenum (Mo) and uranium (U) (Figs. 2–4), which may be due to mineral dissolution of carbonate minerals. For U with reverse redox chemistry compared to metals like Fe and Mn (increased mobilization with increased reduction potential) the enhanced remobilization can be explained by bioturbation/ bioirrigation, and aeration of the sediment (Brookins, 1988; Zheng et al., 2002). These findings confirm with Lagauzere et al. (2009), 35,000
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Fig. 2. Metal mobilization into the overlaying water (mean, min and max) during the experiment for treatments with (C+) and without (C) bioturbation/bioirrigation by C. plumosus.
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completion of this process, the invertebrates seem to have no further impact on the remobilization of Al, Fe, Co, Cu, Zn and Ce. This may be explained by a re-oxidation of the Fe-(oxyhydr)-oxides in the water column with a following precipitation. Hence, these elements will rather be sequestrated by bioturbation as found previously (Lewandowski and Hupfer, 2005). Elements such as Al, Co, Cu, Zn and Ce adsorb onto the surface of the Mn/Fe-(oxyhyd-)oxides and will subsequently be removed from the water column (Goldberg, 1954; Chapman et al., 1998). This is in accordance with Mermillod-Blondin et al. (2005) who found no effect of bioturbation on some metals like copper and zinc. Furthermore, the data does not contradict findings of Lewandowski and Hupfer (2005) that the bioturbation/bioirrigation can result in an increased accumulation of e.g. iron in the sediment. Another pattern to those described above can be seen for Mn, nickel (Ni), arsenic (As), cadmium (Cd) and cesium (Cs). The strong significant remobilization rise during the first 5 h of the experiment in the treatment with invertebrate bioturbation/bioirrigation (when the larvae dig into the sediments), followed by a decrease and after 1 d more or less constant values, is higher compared to the treatment without invertebrates. Hence, Mn, Ni, As, Cd and Cs are affected by burying of the invertebrates into the sediment, aeration of the sediment and suspension of sediment
particles by bioturbation (Lewandowski and Hupfer, 2005; Lagauzere et al., 2011). In the case of Mn it may be explained by the possible sulfidic condition within the sediments (see above). But the effect of aeration of the uppermost sediment layer lead to an immobilization of these metals from the water into the sediment after 1 d of experiment as found previously by others (Lagauzere et al., 2011). The combination of these two processes results in the encountered remobilization pattern. It could be concluded that bioturbation/bioirrigation is a main factor controlling remobilization from sediment into the water column for some elements. The impact of bioturbation/bioirrigation on the remobilization of elements, from sediment into the water body, depends on the chemistry of the elements and conditions within the sediments. 3.3. Minimized metal/metalloid accumulation by C. plumosus A clear increase of elemental content within C. plumosus during the experiment was found, except of aluminum (Table 2). Uptake of the elements can take place via two different pathways, directly via surface and/or via ingestion and uptake in the digestive tract as found for other invertebrates (De Schamphelaere et al., 2004).
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Fig. 3. Metal and metalloid mobilization into the overlaying water (mean, min and max) during the experiment for treatments with (C+) and without (C) bioturbation/ bioirrigation by C. plumosus.
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Fig. 4. Metal mobilization into the overlaying water (mean, min and max) during the experiment for treatments with (C+) and without (C) bioturbation/bioirrigation by C. plumosus.
Table 2 Metal and metalloid content in individuals (mg kg1 DM1) and tissues of C. plumosus. Untreated specimen from start and end of the experiment (n = 10), washed specimen (n = 10), washed specimen with gut system dissected (end washed without gut, n = 5) and gut system including feces from the dissection (gut system with feces, n = 5). (median – bold, minimum and maximum). Significant differences: between start and end of the experiment (all elements (#p < 0.001), except Al ( p < 0.05) and Ca (àp < 0.05), between washed unseparated and washed without gut system (Al, Fe, Ni, Zn, As, Mo, Cd, Cs, Ce and U all (]p < 0.05), between washed unseparated and gut system with feces (Mg, Al, Mn, Fe, Ni, Zn, Sr, and U all (§p < 0.005), Co, Cu and As all ($p < 0.01) and Ca, Mo and Cs all (p < 0.05)) and between washed without gut system and gut system with feces (Mg, Al, Ca, Mn, Fe, Co, Ni, Zn, As, Sr, Cs, Ce and U all (}p < 0.05)). No differences were found between washed and unwashed specimen at the end. Mg
Al
Ca
Mn
Fe
Co
Ni
Cu
Zn
As
Sr
Mo
Start Min Max
1562 1409 1760
183 40 543
2276 1143 5124
25 14 50
1670 1244 2875
