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Chloride imbalances in soil lysimeters
Chemosphere 52 (2003) 381–389 www.elsevier.com/locate/chemosphere
Chloride imbalances in soil lysimeters € berg M. Rodstedth, C. St ahlberg, P. Sanden, G. O
*
Department of Thematic Research, Environmental Science Programme, Link€opings Universitet, 60174 Norrk€oping, Sweden Received 7 January 2002; received in revised form 7 April 2002; accepted 16 April 2002
Abstract The assumption that soil neither acts as a source or a sink of chloride is evaluated by incubating soil cores in lysimeters in a climate chamber under controlled conditions. Some of the lysimeters acted as a sink while others acted as a source of chloride. Considerable amounts of organic chlorine were lost by leaching. The loss by leaching of organic chlorine could only explain part of the discrepancy in the lysimeters where the soil acted as a sink and it could certainly not explain the cases where the soil acted as a source. The storage of organic chlorine was four times larger than the storage of chloride and comparably small changes in the organic chlorine storage will thus have a considerable influence on the chloride budget. However, the soil was too heterogeneous to determine whether a change in the storage had taken place or not. It is concluded that the observed chloride surplus and also, at least to some extent, the observed chloride deficit, most likely was caused by net-changes in the storage of organic chlorine in soil. An inverse correlation was found between the initial chloride content of the soil and the imbalance in the chloride budget. Dry deposition of chloride is generally assumed to equal the run-off minus the wet deposition. Extrapolation to the field situation suggests that the output of organic chlorine by soil leachate is at risk to cause an underestimation of the dry deposition by about 25%. Ó 2003 Elsevier Science Ltd. All rights reserved. Keywords: Chloride; Conservative; Organic chlorine; Biogeochemical cycling; Budget calculations
1. Introduction Chloride is generally considered to be a conservative element from a hydrological point of view, and soil is not considered to be either a source or a sink for this element (e.g. Schlesinger, 1997). This assumption dates back to at least the 1940s (Conway, 1942), and today is commonly used in hydrological research and biogeochemical modelling as a basis for budget calculations and deposition estimates. The basic assumption of the model is that the output of chloride is equal to the input in a catchment. A prerequisite for the model is that the timescale is sufficiently long (i.e., years) since the amount
*
Corresponding author.
of chloride stored in vegetation changes seasonally. The past years of research has shown that organically bound chlorine is a natural constituent of soil organic matter and that soil thereby contains large amounts of naturally produced organically bound chlorine (Asplund and € berg, Grimvall, 1991; Hjelm et al., 1995; Hjelm, 1996; O 1998; Johansson, 2000; Myneni, 2002). It has also been found that chlorine participates in a complex biogeochemical cycle that encompasses input by dry and wet deposition, output by leaching and volatilisation and transformation through formation and mineralisation of organic chlorine (Neidleman and Geigert, 1986; Gribble, € berg and Gr€ 1996; O on, 1998; Watling and Harper, 1998; Lobert et al., 1999; Winterton, 2000). This suggests that soil may act both as a sink and a source of chloride. It has been found that the storage of organic chlorine in top-soil in Scandinavia is 2–4 times larger than the
0045-6535/03/$ - see front matter Ó 2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S0045-6535(03)00192-9
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storage of chloride (Johansson et al., 2001, 2002), but the size and relation between the fluxes is poorly understood. In this paper, a description is made of the chloride budget of soil cores in lysimeters that are incubated under controlled conditions and it is analysed whether the budget is in balance or not. Furthermore, the influence of the turn-over of organic chlorine on the chloride budget is evaluated and the relative loss of organic chlorine by soil leachate is quantified.
combined to a bulk sample in a polythene plastic bag (1 l). All samples were transported to the laboratory and the reference samples in the polythene bags were weighted and placed in a deep freezer ()18 °C) until further analyses were carried out. The polypropene cylinders containing the undisturbed soil cores were stored in a refrigerator (4 °C) for 7 days and thereafter incubated in a climate chamber as described below. The polypropene cylinders containing the soil cores are hereafter denoted ‘‘lysimeters’’.
1.1. Terminology 2.3. Experimental set-up Throughout the text, we use the term organically bound chlorine, even though the method used is a sum parameter that does not distinguish between chlorine, bromine and iodine. Since chlorine is by far the most abundant halogen in the environment, the discussion is confined to this halogen. However, it should be kept in mind that chlorine has a lower molecular weight than the other halogens that may be detected by the method. Hence, if other halogens than chlorine are present in considerable amounts, the method will cause an underestimation of the mass of organic halogens in the analyzed samples.
2. Material and method 2.1. Sampling site Soil samples were collected at the Stubbetorp catchment (59°440 N; 16°210 E) in SE Sweden in April 2000. The catchment is situated in a forested mountain area with broken topography. The bedrock is poor in chloride and the area is covered by coniferous forest dominated by Norway spruce (Picea abies (L.) Karst.) and pine (Pinus sylvestris (L.)). The approximate altitude is 100 m.a.s.l. The long term annual mean precipitation in the region is approximately 600 mm and the annual mean temperature is about 6 °C (Raab and Vedin, 1995). A more detailed description of the catchment is given by Maxe (1995). The sampling site (200 m2 ) is located at a discharge area in the catchment with a groundwater level around 150 mm. 2.2. Soil sampling procedures Ten undisturbed soil cores were collected within the sampling site to a depth of 150 mm with the aid of polypropene cylinders with an inner-area of 80 cm2 . A stainless-steel tip facilitated penetration of the root system. In addition, reference samples were collected by sampling three smaller soil cores (inner-area 3.8 cm2 , depth 150 mm) adjacent to each place where an undisturbed core had been collected. The three cores were
Lysimeters were constructed by placing thin PE microfilters (43 lm average pore size, 1 mm thickness) on polypropene bottoms with a horizontally placed stainless-steel pipe. The polypropene cylinders, containing the undisturbed soil cores, were then mounted onto the bottoms. An approximately 20 cm long silicon tube (0.6 cm i.d.) was mounted on the stainless-steel pipe in order to lead leachate, that would be formed during incubation, to an Erlenmeyer flask (E-flask, 250 ml). The mouth of the E-flask with the teflon tube was sealed with plastic film and the E-flask was placed such that it was well below the bottom of the cores. The lysimeters were incubated in a dark climate chamber (10 °C, and 90% humidity) from April 26 to August 31 2000 (i.e. over a period of 128 days), and irrigated twice a week with artificial rain. Due to malfunction of the climate chamber, the humidity dropped slightly below 90% at several occasions during the first 40 days of the incubation period. The amounts of artificial rain corresponds to the weekly mean precipitation according to compiled data for the period 1970–1997 from the meteorological station at Simonstorp (58°460 N; 16°070 O). The chemical composition with respect to major cations and anions corresponds to the monthly mean according to compiled data during the period 1983–1999 from the station situated at Sj€ o€ angen (58°460 N; 14°180 O) and run by Swedish Environmental Research Institute (IVL). The E-flasks were emptied once a week and the amount of leachate was determined by weighting the Eflask before and after emptying the leachate into a polythene flask (150 ml, Kebo lab). The pH of the leachate was determined and the samples were then stored in a deep freezer ()18 °C) until further analyses were conducted. The leachate was analysed with respect to the concentration of organic chlorine (AOX), chloride (Cl ) and total organic carbon (TOC). After termination of the experiment, water content, loss-on-ignition, organic chlorine (TOX) and total amount of chlorine (TX) was determined in the incubated soil as well as in the reference samples that had been stored in a deep freezer during the incubation pe-
M. Rodstedth et al. / Chemosphere 52 (2003) 381–389
riod. The concentration of chloride was determined by subtracting the TOX from the TX values. 2.4. Analytical procedures 2.4.1. Chloride in soil leachate The concentration of chloride in the leachate was determined by potentiometric titration using an automatic titrator (Radiometer, Copenhagen). An aliquot of the leachate (15 ml) was mixed with a carrying electrolyte (15 ml; 1 M KNO3 , 0.2 M HNO3 ) and titrated with AgNO3 (5 mM) to the endpoint. The endpoint was calculated from two curves, where a solution of 14 ml Milli-Q water, 15 ml carrying electrolyte and a chloride solution (1 ml, 0.01 M) was titrated with AgNO3 (5 mM). Duplicate analyses were conducted when possible and blanks were analysed twice or more for each round. 2.4.2. Organic carbon in soil leachate (TOC) The total amount of organic carbon (TOC) in the leachate was determined with a Shimadzu 5000 TOC Analyser. An aliquot of the leachate (10 ml) was diluted with Milli-Q water (40 ml). Duplicate analyses were conducted on each sample. Reference-solutions were analysed as follows; first a Milli-Q water sample, followed by two reference samples with 10 mg TC l1 and 10 mg IC l1 , respectively, followed by a Milli-Q water sample. In addition, Milli-Q water was analysed approximately each 10th analysis. 2.4.3. Organic chlorine in soil leachate (AOX) Organic chlorine in the leachate was determined according to the standard procedure for determination of adsorbable organic halogens (AOX; EU 1485, 1996). In short, a sample was diluted with Milli-Q water to a final volume of 100 ml (3:100 or 1:50; V:V) in an Erlenmeyer flask (300 ml). Activated carbon (50 mg), an acidified nitrate solution (5.0 ml, 0.2 M KNO3 , 0.02 M HNO3 ) and approximately seven drops of concentrated HNO3 were added to the flasks and the suspension was placed on a rotary shaker (1 h, 200 rpm). The suspension was filtered through a polycarbonate filter (0.45 lm) and rinsed with an acidic nitrate solution (20 ml 0.01 M KNO3 , 0.001 M HNO3 ), followed by acidified Milli-Q water (20 ml, pH 2, HNO3 ). The filter with the filter cake were then combusted under a stream of oxygen at 1000 °C in an Euroglas AOX-analyser (model 84/85) in which the formed hydrogen halides were determined by microcoulombmetric titration with silver ions. Each sample was analysed in duplicates. The difference between the duplicates was generally smaller than 0.2 lg Clorg . Blanks were analysed by the use of Milli-Q water. All samples were clearly above the detection limit, which was 5 lg Clorg l1 .
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2.4.4. Water content, pH and loss-on-ignition in soil samples The water content was determined by drying the soil to constant weight at 65 °C. The soil was then sieved through a 2 mm sieve and representative samples (2 g) were analysed for pH. Loss-on-ignition was determined in five subsamples (5 g) that were placed in crucibles, combusted for 2 h in 620 °C and stored in an exicator until weighting. The amount of organic carbon was estimated as 50% of the weight loss and the median value of the five replicates was used for the calculations. The coefficient of variation was approximately 10%. The soil was then milled (0.12 mm) and stored in glass bottles until TOX and TX analyses were conducted. 2.4.5. Organic chlorine in soil samples (TOX) The concentration of organic chlorine (TOX) in soil was analysed according to Asplund et al. (1994). In short, 20 mg milled sample was added to an acidic nitrate solution (20 ml, 0.2 M KNO3 , 0.02 M HNO3 ) and shaken on a rotary shaker (200 rpm) for at least 1 h. The suspension was filtered through a 0.45 m polycarbonate filter and the analyses then followed the procedure for AOX-analyses described above. Five to eight replicates of each soil sample were analysed and the median was used for calculations. The coefficient of variation among the replicates was approximately 5%. Blanks were analysed according to the same procedure but without addition of soil. All samples were clearly above the detection limit, which was 0.4 lg Clorg g1 . 2.4.6. Total amount of chlorine in soil samples (TX) The total amount of chlorine (TX) was determined by adding 20 mg milled and sieved soil (0.12 mm) to a small crucible followed by direct combustion in the AOX-analyser. Five replicates of each soil sample were analysed and the median was used for calculations. The coefficient of variation among the replicates was between 5% and 10%. Blanks were analysed by combustion of the crucibles without addition of soil. All samples were clearly above the detection limit, which was approximately 0.2 lg Clorg g1 . Chloride was calculated as TX minus TOX. 2.5. Statistical analyses and budget calculations If not otherwise stated, the central tendency is given as median, and the variation is given as first and third quartile within parenthesis after the median. The soil routine of the HBV-model (Bergstr€ om et al., 1985) was run on the hydrological data in order to check the water balance of the lysimeters.
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the onset of the experiment varied from 56 to 69 mm and increased in most of the lysimeters during the incubation period. The field capacity used in the soil routine of the HBV-model varied between 74 and 101 mm and evaporation was estimated to 38–66 mm. The hydrology of the lysimeters could be well described by the model.
3. Results 3.1. General description of the soil cores The soil cores consisted of a thick organic layer (12– 15 cm) with a mixed in mineral content. The mineral content increased with depth causing a diffuse transition to an organic rich mineral layer. No clear horizons were distinguished. The water content was 59% (54–65%), the pHH2 O was 3.55 (3.66–3.40) and the organic matter content 49% (41–53%).
3.3. Chloride balance The accumulated amount of chloride that was added to each lysimeter as artificial rainwater was 0.48 mg Cl and the accumulated amount that was leached with the soil water was 11 (8.8–14) mg Cl (Table 2). The total amount in the lysimeters at the onset of the experiment was 23 (16–28) mg Cl and the total amount in the lysimeters at termination of the experiment was 9 (8–12) mg Cl . When the chloride balance was calculated it was found that the soil in some cases had acted as a sink and in others as a source of chloride (Table 2). The imbalance varied from a loss of 18 mg Cl , to an increase of
3.2. Water balance The accumulated amount of artificial rain added to each of the lysimeters during the incubation period was 223 mm, which corresponds to a daily mean deposition of 1.7 mm. The cumulated amount of leachate leaving the lysimeters varied from around 134 to 159 mm (Table 1). The amount of water within the lysimeters at
Table 1 Water balance in the lysimeters as observed and predicted by the hydrological modelling Lysimeter
Water content start
Time to first leachate (days)
Artificial rain
Leakage
Water content end
Balance
Model evaporation
Difference
1 2 3 4 5 6 7 8 9 10
59 61 56 69 65 57 56 61 64 57
14 26 7 7 26 28 26 26 26 7
223 223 223 223 223 223 223 223 223 223
134 143 144 159 141 145 143 146 147 154
94 89 70 91 84 79 78 75 88 88
54 52 65 42 63 56 58 63 52 38
55 53 66 43 64 57 59 64 52 38
)0.5 )0.4 )0.8 )0.6 )0.6 )1.1 )0.5 )0.5 )0.5 )0.3
The lysimeters have been incubated at 10 °C and 90% humidity for 128 days in dark climate chambers and irrigated with artificial rainwater. All values in millimeter.
Table 2 Chloride balance of the 10 lysimeters that were incubated during 128 days in dark climate chambers at 10 °C and 90% humidity (all values are given in milligram) Lysimeter
Artificial rain
Initial storage
Lost by leachate
Storage at end
Balance
Clorg lost by leachate
Balance
1 2 3 4 5 6 7 8 9 10
0.48 0.48 0.48 0.48 0.48 0.48 0.48 0.48 0.48 0.48
44 23 24 23 15 21 35 30 5.9 11
17 9.2 15 15 12 6.7 8.7 13 10 6.9
31 12 9.6 8.6 7.7 6.9 11 0.69 3.7 8.5
3.1 )2.9 )0.32 0.97 4.9 )7.8 )15 )17 7.3 4.0
2.52 0.29 1.25 2.16 0.33 0.29 0.47 0.96 0.51 0.34
0.59 )3.19 )1.56 )1.19 4.59 )8.10 )15.55 )18.07 6.75 3.63
M. Rodstedth et al. / Chemosphere 52 (2003) 381–389
Chloride balance (mg)
5
385
0.49
< 0.01
0 -5 -10 -15
16-28
-20 0
10
20
30
52-107
40
Initial amount of chloride (mg) Fig. 1. Chloride balance in 10 soil lysimeters as a function of the initial amount of chloride in the lysimeters.
∆ = -14.3 to -8.0
∆ =?
6.8 mg Cl . A correlation was found between the netbalance and the initial amounts of chloride in the lysimeters (Fig. 1).
3.4. Organic chlorine The concentration of organic chlorine (AOX) in the artificial rainwater was less than 5 lg Clorg l1 , which corresponds to a total deposition of less than 10 lg Clorg . The concentration of organic chlorine in the leachate was 0.40 (0.25–1.0) mg Clorg l1 and the accumulated amount of organic chlorine lost with the leachates was 0.49 (0.11–1.17) mg Clorg . The concentration of organic chlorine in the leachates decreased or was unchanged over the incubation period. The chlorine-to-carbon ratio was 3.2 (3.1–8.5) mg Clorg g1 C with a decreasing pattern over time in all but one of the lysimeters. The leachate from one of the lysimeters had remarkably high chlorine-to-carbon ratios with initial values around 40 mg Clorg g1 C and final values around 20 mg Clorg g1 C. The concentration of organic chlorine in the soil cores collected and analysed at the onset of the experiment was 0.25 (0.19–0.41) mg Clorg g1 dw. The concentration in the soil from the lysimeters at the end of the incubation period was 0.30 (0.17–0.53) mg Clorg g1 dw. The amount of organic chlorine in the lysimeters at the end of the incubation period was 81 (72–92) mg Clorg . If the concentration of organic chlorine determined in the soil cores are combined with dry weight data from the lysimeters at the termination of the experiment, the initial amounts in the lysimeters can be estimated to 84 (52–107) mg Clorg . The overall chlorine budget of the lysimeters is shown in Fig. 2.
Fig. 2. Initial storage of organic chlorine and chloride and change in the storage in 10 soil lysimeters during the incubation in climate chambers for 128 days. The input is the amount added by artificial rain and the output is the amount lost as soil leachate. All units are in mg.
4. Discussion 4.1. Loss of organic chlorine by soil leachate The amount of organic chlorine that was lost from the lysimeters during the incubation period by soil leachate is of the same size as the input of chloride by artificial rain. This suggests that the amount of chlorine lost from the system as soil leachate is of such size that it is likely to influence the chloride balance. The organic chlorine concentrations in the leachate collected from the lysimeters are initially rather high. With time, the system asymptotically approached a fairly stable chlorine-to-carbon ratio around 3 mg Clorg g1 C, indicating that the processes approached some sort of steady state conditions. The observed run-off during 1986–1990 at the Stubbetorp catchment was 230 mm yr1 (Maxe, 1995). If we assume that the transport of organic chlorine by soil leachate during the latter half of the incubation period resembles the transport in the field situation, the annual transport of organic chlorine by soil leachate in the catchment can be estimated to about
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0.1 g Clorg m2 yr1 . The annual mean wet deposition of chloride in the Stubbetorp catchment during 1986– 1990 was estimated to 0.4 g Cl m2 yr1 and the loss by run-off for the same period was found to be 0.71 g Cl m2 yr1 (Maxe, 1995). In accordance with the generally agreed upon procedure, the dry deposition was calculated as the run-off minus the wet deposition and thus estimated to 0.31 g Cl m2 yr1 . However, our experiment suggests that the dry deposition is inclined to be underestimated as it was assumed to equal the run-off minus the wet deposition. Instead, the experiment suggests that the dry deposition ought to be 25–30% larger since it is indicated that about 0.1 g Cl m2 yr1 is lost from the system as organically bound chlorine in the soil leachate. A previous estimate of the loss of organic chlorine by soil leachate has been conducted at a spruce € berg forest soil in Klosterhede in Northwest Denmark (O and Gr€ on, 1998). The estimates from the Danish study gave an annual transport with soil leachate of 0.07 g Clorg m2 , which further strengthens the conclusion that considerable amounts of chlorine is lost by soil leachate in the field situation. This strongly suggests that the loss of organic chlorine by soil leachate must be considered when a chlorine budget is constructed for a catchment.
4.2. Chlorination during degradation? The chlorine-to-carbon ratios in the soil leachate (3.2 (3.1–8.5) mg Clorg g1 C) are rather high as compared to the ratios in the soil as a whole (1.1 (0.85–1.37) mg Clorg g1 C). Previous studies have shown that the chlorine-to-carbon ratio increases about one order of magnitude from the litter layer to the A-horizon (i.e. from around 0.1 to 1 mg Clorg g1 soil dw) and that it increases further to 5 mg Clorg g1 soil dw or even more € berg, 1998). Previous studies in the B- and C-horizons (O have shown that the organic matter that is leached through the soil has been subjected to microbial degradation (Guggenberger and Zech, 1994). Hence, the soil organic matter that has been subjected to microbial attack is transported downwards in the soil horizon and some precipitates during the transport. Other studies indicate that a net-formation of organic chlorine takes € berg place during the degradation of organic matter (O et al., 1996a,b). It has been suggested that the underlying mechanism is microbial formation of reactive chlorine species such as HOCl, which enables degradation of organic matter and renders a formation of organic chlorine as a by-product. This hypothesis was strengthened by a recent study where it was found that lignin that had been subjected to reactive chlorine was more easily degraded by P. Crysosporium (Johansson et al., 2000). In addition to fragmentation and oxidation, an increased chlorine content of the organic matter will certainly make it more hydrophilic. These processes do
certainly provide a plausible explanation to the observed higher chlorine-to-carbon ratio in the soil leachate as compared to the soil as a whole, as well as the increasing chlorine-to-carbon ratios with depth previously observed in soil profiles. This hypothesis finds further support in the fact that the chlorine-to-carbon ratios of the leachates in the present study peak at the second or third sampling occasion and thereafter decreases. This is most likely a result of the experimental set-up and the induced disturbance of the soil system. Even though precaution was taken to keep the soil cores undisturbed, it could not be prevented that roots were cut. Hence, new carbon sources were introduced into the system and the microbial communities were suddenly provided with a new carbon source. Consequently, the sampling procedure probably caused increased microbial activity as well as changes in the community structure. According to the line of reasoning above, increased microbial activity would render a formation of water-soluble chlorinated organic matter, which also is observed. 4.3. The chloride balance of the lysimeters When the chloride budget was calculated and modelled for each of the lysimeters, it was found that the soil in some of the lysimeters acted as a sink whereas others acted as a source of chloride. The imbalance varied from a decrease corresponding to an annual loss of 6.0 g Cl m2 yr1 to an increase corresponding to a gain of 2.6 g Cl m2 yr1 . The hydrology of the lysimeters could be well described by the HBV-model, which strongly indicates that the experimental set-up and the observations made during the study were sound. It is thus not plausible that the observed imbalances in the chloride budgets are due to experimental errors. Loss by leaching can only explain a minor part of the deficit and it can certainly not explain the five cases when the lysimeters acted as chloride sources. For soil to act as a sink of chloride, temporary adsorption and uptake by plants is not likely. Hence, only three mechanisms remain that theoretically find support in the literature; formation of non-volatile chlorinated organic compounds, formation € berg, of volatile chlorinated organic compounds (e.g. O 1998; Lobert et al., 1999; Winterton, 2000) and anion exchange. In the soil type here studied, anion exchange is generally considered to be negligible. 4.3.1. Net-changes in the storage of organic chlorine If we assume that the lionÕs share of the observed net-changes is due to a formation of non-volatile compounds, a corresponding change in the storage of organic chlorine would have taken place. In the present study, the initial organic chlorine content of the incubated soil cores was extrapolated from analyses made on soil samples that had been collected adjacent to the cores
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that were to be incubated. However, it was found that the small scale variation of the organic matter content varied to a large extent. As the organic chlorine content is strongly related to the organic matter content, the extrapolations of the initial values are too uncertain to allow conclusions to be drawn concerning changes in the organohalogen storage at the demanded level. The major reason is that the initial amount in the lysimeters had to be extrapolated from the reference samples. It can thus not be conclusively shown whether or not the imbalance in the chloride budget was followed by a corresponding change in the organochlorine storage. The storage of organic chlorine in the lysimeters at the onset of the experiment was approximately four times larger than the storage of chloride was, which is in line with previous studies of top-soil samples in the region (Johansson et al., 2001). Like other natural constituents of organic matter, organic matter-bound chlorine is mineralised during the degradation of the € berg, 1998; O € berg and Gr€ organic matter (O on, 1998). Organic matter-bound chlorine is in other words easily and continuously degraded in soil. Previous studies of net-changes of the organohalogen content in soil has shown that both a net-increase and a net-decrease may € berg et al., 1996a,b, 1997; Johansson et al., take place (O 2001). This shows that both a mineralisation (release of chloride) and a formation (consumption of chloride) of organic chlorine occur in soil, even though the processes hitherto have not been separated. The leachate data of the present study strongly indicate that a formation was taking place in all lysimeters, also in those that acted as a source of chloride. However, if the mineralisation of organic chlorine is larger than the formation of the same, excess chloride will be formed and the soil will act as a source of chloride. This suggests that the mineralisation rate (release of chloride) was larger than the formation rate (consumption of chloride) in the lysimeters that acted as a source of chloride. Little is known on in situ formation of organic chlorine, but even less is known on the degradation processes that underlie the mineralisation of chlorinated organic matter. 4.3.2. Formation of chlorinated volatiles The formation of volatile compounds was not studied in the present study, but this possible sink still deserves a comment. It has since long been known that natural sources, besides industrial releases, contribute considerably to the volatile chlorinated compounds in the atmosphere, (e.g. Lovelock, 1975). Initially, research mainly focussed on marine sources, but it has become clear that other major sources must exist (e.g. Gan et al., 1998; Rhew et al., 2000; Yokuchi et al., 2000). A number of studies have suggested that terrestrial sources may be an important source. Even though the first report on the issue was published already in 1985 (Harper, 1985), the
387
information is still very scattered. As pointed out by several authors, it is still not possible to reliably quantify the relative contribution from terrestrial sources (e.g. Khalil et al., 1999). The major reason to this is the lack of sound field data why quantification so far mainly have been based on extrapolations from laboratory studies of single species (e.g. Watling and Harper, 1998). The exception is a recent study focussing on the emission of methyl-chloride and bromide from coastal salt marches indicating fluxes of 0.2–1.2 g m2 yr1 (Rhew et al., 2000). Research on the formation of halogenated volatiles from terrestrial sources has shown that common whiterot fungi are able to methylate chloride (Harper, 1985, 1995; Harper et al., 1988; McNally et al., 1990; Watling and Harper, 1998; Khalil et al., 1999). It has also been found that higher plants are able to produce rather high amounts of chloromethane (Harper, 1995; Gan et al., 1998). In addition, there is evidence that the concentration of methyl chloride and chloroform is higher in soil than in the ambient air, which indicates that such compounds are formed there (Laturnus et al., 1995; Hoekstra et al., 2001; Haselmann et al., 2000). Finally, a recent study suggest that an abiotic formation of chloromethane involving redox reactions with organic matter, iron and chloride takes place in soil (Keppler et al., 2000). Hence, it cannot be excluded that part of the loss of chloride from the lysimeters were due to a volatilisation. However, as very little is known on the formation processes and their dependence on environmental factors such as chloride concentration, it is not possible to even make a qualified guess on the quantities of chloride lost from the system through this route.
4.4. Influence of environmental variables A net-mineralisation has previously been observed during the early decomposition of fresh litter, during early summer periods and as a result of carbonate and € berg et al., 1996a,b, 1997; Jonitrogen amendments (O hansson et al., 2001). A net-formation has been observed after amendment of sulphuric acid and during the fall under long term decomposition of litter. This shows that the turn-over of chlorine in soil is influenced by environmental variables and suggests that the differences among the lysimeters was due to differences in crucial parameters. It is interesting to note the correlation between the chloride imbalance and the initial chloride concentrations in the soil (Fig. 2). A study of the spatial distribution of organic chlorine and chloride in Swedish soil showed a clear correlation between the two variables (Johansson et al., 2002). However, it still remains to be elucidated whether the correlation is due to a pseudocorrelation or if the observed correlation actually is due to a connection through underlying processes.
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4.5. A comment on organic chlorine as an indicator of pollution The concentration of organic chlorine observed in the soil leachates of the present study are extremely high when compared with concentrations observed in surface water or even wastewater (Enell et al., 1989; H€as€anen and Manninen, 1989; Troemel et al., 1989; Jokela et al., 1992; Fleming, 1995). The chlorine-to-carbon ratio observed in the soil leachate in the present study is in most cases slightly higher than those found in surface water. However, remarkably high ratios were occasionally observed in the leachate from four of the lysimeters (>10 mg Clorg g C1 ), and in one case the ratio even varied from 20 to 40 mg Clorg g C1 . During the 1980s, it was argued that the concentration of organic chlorine per se could be used as an indicator of pollution. In the late 1980s and the early 1990s, one started to apprehend the dimensions of the natural chlorine cycle and the detection of organic chlorine is nowadays most often used in a more sensible way. However, extreme values (often considered as those above 200 lg Clorg l1 ) are still often taken as a sign of pollution. The results of the present study further stress the importance to thoroughly evaluate organic chlorine concentration data in relation to its context.
Acknowledgements This project has been financed by MISTRA (The Foundation for Strategic Environmental Research), which hereby is acknowledged. The authors are indebted to Lena Lundman, whom has been of inestimable help and support.
References EN (European Norm) 1485, 1996. Water quality––Determination of adsorbable organically bound halogens (AOX) Approved, April 1996. Asplund, G., Grimvall, A., 1991. Organohalogens in nature, more widespread than previously assumed. Environmental Science and Technology 25, 1346–1350. Asplund, G., Grimvall, A., Jonsson, S., 1994. Determination of total and leachable amounts of organohalogens in soil. Chemosphere 28, 1467–1475. Bergstr€ om, S., Carlsson, B., Sandberg, G., Maxe, L., 1985. Integrated modelling of runoff, alkalinity and pH on a daily basis. Nordic Hydrology 2, 89–104. Conway, E.J., 1942. The chemical evolution of oceans. Proceedings of the Royal Irish Academy 48, 161–212. Enell, M., Kaj, L., Wennberg, L., 1989. Long-distance distribution of halogenated organic compounds (AOX). In: Laikari, H. (Ed.), River Basin Management. Pergamon Press PLC, Oxford, pp. 29–36.
Fleming, B.F., 1995. Organochlorines in perspective. Tappi Journal 78, 93–98. Gan, J., Yates, S.R., Ohr, H.d., Sims, J.J., 1998. Production of methyl bromide by terrestrial higher plants. Geophysical Research Letters 25, 3595–3598. Gribble, G.W., 1996. Naturally Occurring Organohalogen Compounds––A Comprehensive Survey. Springer, Wien, New York. Guggenberger, G., Zech, W., 1994. Composition and dynamics of dissolved carbohydrates and lignin-degradation products in two coniferous forests, N.E. Bavaria, Germany. Soil Biology and Biochemistry 26, 19–27. Harper, D.B., 1985. Halomethane from halide ion––a highly efficient fungal conversion of environmental significance. Nature 315, 55–57. Harper, D.B., 1995. The contribution of natural halogenation processes to the atmospheric halomethane burden. In: Grimvall, A., de Leer, E.W.B. (Eds.), Naturally-Produced Organohalogens. Kluwer Academic Publishers, Dordrecht, pp. 21–34. Harper, D.B., Kennedy, J.T., Hamilton, J.T.G., 1988. Chloromethane biosynthesis in poroid fungi. Phytochemistry (Oxf.) 27, 3147–3153. Haselmann, K.F., Ketola, R.A., Laturnus, F., Lauritzen, F.R., Gr€ on, C., 2000. Occurrence and formation of chloroform at Danish forest sites. Atmospheric Environment 34, 187–193. H€as€anen, E., Manninen, P.K.G., 1989. The total organochlorine and organobromine (AOCl, AOBr) concentrations in water courses and in snow in Finland. VDI Berichte 745, 395–400. Hjelm, O., 1996. Organohalogens in coniferous forest soil (Ph.D. Thesis). Department of Water and Environmental Studies. Link€ oping, Link€ opings Universitet. € berg-Asplund, G., 1995. OrganHjelm, O., Johansson, M.B., O ically bound halogens in coniferous forest soil––Distribution pattern and evidence of in situ production. Chemosphere 30, 2353–2364. Hoekstra, E.J., Duyzer, J.H., de Leer, E.W.B., Brinkman, U.A.T., 2001. Chloroform-concentration gradients in soil air and atmospheric air, and emission fluxes from soil. Atmospheric Environment 35 (1), 61–70. Johansson, E., 2000. Organic chlorine and chloride in soil (Ph.D. Thesis). Department of Water and Environmental Studies. Link€ oping, Link€ opings Universitet. € berg, G., Johansson, E., Krantz-R€ ulcker, C., Zhang, B.X., O 2000. Chlorination and biodegradation of lignin. Soil Biology and Biochemistry 32, 102–1032. € berg, G., Johansson, E., Eben a, G., Sanden, P., Svensson, T., O 2001. Organic chlorine and chloride in Swedish spruce forest soil: Influence of nitrogen. Geoderma 10, 1–13. € berg, G., 2002. Spatial distribution Johansson, E., Sanden, P., O of organically bound chlorine and chloride in forest soil, southern Sweden. Chemosphere, in press. Jokela, J., Salkinoja-Salonen, M.S., Elomaa, E., 1992. Adsorbable organic halogens (AOX) in drinking water and the aquatic environment in Finland. Journal of Water Services Research and Technology––Aqua 41, 4–12. Keppler, F., Eiden, R., Niedan, V., Pracht, J., Sch€ oler, H.F., 2000. Halocarbons produced by natural oxidation processes during degradation of organic matter. Nature 403, 298–301.
M. Rodstedth et al. / Chemosphere 52 (2003) 381–389 Khalil, M.A.K., Moore, R.M., Harper, D.B., Lobert, J.M., Erickson, D.J., Koropalov, V., Sturges, W.T., Keene, W.C., 1999. Natural emissions of chlorine-containing gases: reactive chlorine emissions inventory. Journal of Geophysical Research 104, 8333–8346. Laturnus, F., Mehrtens, G., Gr€ on, C., 1995. Haloperoxidaselike activity in spruce forest soil––a source of volatile halogenated organic compounds. Chemosphere 31, 3709– 3719. Lobert, J.M., Keene, W.C., Logan, J.A., Yevich, R., 1999. Global chlorine emissions from biomass burning: reactive chlorine emissions inventory. Journal of Geophysical Research 104, 8373–8389. Lovelock, J.E., 1975. Natural halocarbons in the air and in the sea. Nature 256, 193–194. Maxe, L., 1995. Effects of acidification on groundwater in Sweden. Swedish Environmental Protection Agency: 166. McNally, K.J., Hamilton, J.T.G., Harper, D.B., 1990. The methylation of benzoic and n-butyric acids by chloromethane in Phellinus pomaceus. Journal of General Microbiology 136, 1509–1515. Myneni, S.C.B., 2002. Formation of stable chlorinated hydrocarbons in weathering plant material. Science 295, 1039– 1041. Neidleman, S.L., Geigert, J., 1986. Biohalogenation: Principles, Basic Roles and Applications. Ellis Horwood Limited, Chichester. € berg, G., 1998. Chloride and organic chlorine in soil. Acta O Hydrochemica et Hydrobiologica 26, 137–144. € berg, G., Gr€ O on, C., 1998. Sources of organic halogens in spruce forest soil. Environmental Science and Technology 32, 1573–1579.
389
€ berg, G., B€ O orjesson, I., Samuelsson, B., 1996a. Net change in organically bound halogens in relation to soil pH. Water Air and Soil Pollution 89, 351–361. € berg, G., Nordlund, E., Berg, B., 1996b. In situ formation of O organically bound halogens during decomposition of Norway spruce litter––effects of fertilization. Canadian Journal of Forest Research 26, 1040–1048. € berg, G., Brunberg, H., Hjelm, O., 1997. Production of O organically bound halogens during degradation of birch wood by common white-rot fungi. Soil Biology and Biochemistry 29, 191–197. Raab, B., Vedin, H. (Eds.), 1995. Klimat, sj€ oar och vattendrag. Nationalatlas. Bokf€ orlaget Bra B€ ocker, H€ ogan€as. Rhew, R.C., Miller, B.R., Weiss, R.F., 2000. Natural methyl bromide and methyl chloride emissions from coastal salt marshes. Nature 403, 292–295. Schlesinger, W.H., 1997. Biogeochemistry. An Analysis of Global Change. Academic Press, San Diego. Troemel, G., Muszik, J., M€ uller, F., 1989. Naßfestmittel–– AOX-belastung im Abwasser. Wochenblatt f€ ur Papierfabrikation 17 (2), 63, 66–68. Watling, R., Harper, D.B., 1998. Chloromethane production by wood-rotting fungi and an estimate of the global flux to the atmosphere. Mycological Research 102 (7), 769–787. Winterton, N., 2000. Chlorine: the only green element–– towards a wider acceptance of its role in natural cycles. Green Chemistry 2, 173–225. Yokuchi, Y., Noijiri, Y., Barrie, L.A., Toom-Sauntry, D., Machida, T., Inzuka, Y., Akimoto, H., Li, H.-J., Fujinuma, Y., Aoki, S., 2000. A strong source of methyl chloride to the atmosphere from tropical coastal land. Nature 403, 295– 298.
Chloride imbalances in soil lysimeters € berg M. Rodstedth, C. St ahlberg, P. Sanden, G. O
*
Department of Thematic Research, Environmental Science Programme, Link€opings Universitet, 60174 Norrk€oping, Sweden Received 7 January 2002; received in revised form 7 April 2002; accepted 16 April 2002
Abstract The assumption that soil neither acts as a source or a sink of chloride is evaluated by incubating soil cores in lysimeters in a climate chamber under controlled conditions. Some of the lysimeters acted as a sink while others acted as a source of chloride. Considerable amounts of organic chlorine were lost by leaching. The loss by leaching of organic chlorine could only explain part of the discrepancy in the lysimeters where the soil acted as a sink and it could certainly not explain the cases where the soil acted as a source. The storage of organic chlorine was four times larger than the storage of chloride and comparably small changes in the organic chlorine storage will thus have a considerable influence on the chloride budget. However, the soil was too heterogeneous to determine whether a change in the storage had taken place or not. It is concluded that the observed chloride surplus and also, at least to some extent, the observed chloride deficit, most likely was caused by net-changes in the storage of organic chlorine in soil. An inverse correlation was found between the initial chloride content of the soil and the imbalance in the chloride budget. Dry deposition of chloride is generally assumed to equal the run-off minus the wet deposition. Extrapolation to the field situation suggests that the output of organic chlorine by soil leachate is at risk to cause an underestimation of the dry deposition by about 25%. Ó 2003 Elsevier Science Ltd. All rights reserved. Keywords: Chloride; Conservative; Organic chlorine; Biogeochemical cycling; Budget calculations
1. Introduction Chloride is generally considered to be a conservative element from a hydrological point of view, and soil is not considered to be either a source or a sink for this element (e.g. Schlesinger, 1997). This assumption dates back to at least the 1940s (Conway, 1942), and today is commonly used in hydrological research and biogeochemical modelling as a basis for budget calculations and deposition estimates. The basic assumption of the model is that the output of chloride is equal to the input in a catchment. A prerequisite for the model is that the timescale is sufficiently long (i.e., years) since the amount
*
Corresponding author.
of chloride stored in vegetation changes seasonally. The past years of research has shown that organically bound chlorine is a natural constituent of soil organic matter and that soil thereby contains large amounts of naturally produced organically bound chlorine (Asplund and € berg, Grimvall, 1991; Hjelm et al., 1995; Hjelm, 1996; O 1998; Johansson, 2000; Myneni, 2002). It has also been found that chlorine participates in a complex biogeochemical cycle that encompasses input by dry and wet deposition, output by leaching and volatilisation and transformation through formation and mineralisation of organic chlorine (Neidleman and Geigert, 1986; Gribble, € berg and Gr€ 1996; O on, 1998; Watling and Harper, 1998; Lobert et al., 1999; Winterton, 2000). This suggests that soil may act both as a sink and a source of chloride. It has been found that the storage of organic chlorine in top-soil in Scandinavia is 2–4 times larger than the
0045-6535/03/$ - see front matter Ó 2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S0045-6535(03)00192-9
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storage of chloride (Johansson et al., 2001, 2002), but the size and relation between the fluxes is poorly understood. In this paper, a description is made of the chloride budget of soil cores in lysimeters that are incubated under controlled conditions and it is analysed whether the budget is in balance or not. Furthermore, the influence of the turn-over of organic chlorine on the chloride budget is evaluated and the relative loss of organic chlorine by soil leachate is quantified.
combined to a bulk sample in a polythene plastic bag (1 l). All samples were transported to the laboratory and the reference samples in the polythene bags were weighted and placed in a deep freezer ()18 °C) until further analyses were carried out. The polypropene cylinders containing the undisturbed soil cores were stored in a refrigerator (4 °C) for 7 days and thereafter incubated in a climate chamber as described below. The polypropene cylinders containing the soil cores are hereafter denoted ‘‘lysimeters’’.
1.1. Terminology 2.3. Experimental set-up Throughout the text, we use the term organically bound chlorine, even though the method used is a sum parameter that does not distinguish between chlorine, bromine and iodine. Since chlorine is by far the most abundant halogen in the environment, the discussion is confined to this halogen. However, it should be kept in mind that chlorine has a lower molecular weight than the other halogens that may be detected by the method. Hence, if other halogens than chlorine are present in considerable amounts, the method will cause an underestimation of the mass of organic halogens in the analyzed samples.
2. Material and method 2.1. Sampling site Soil samples were collected at the Stubbetorp catchment (59°440 N; 16°210 E) in SE Sweden in April 2000. The catchment is situated in a forested mountain area with broken topography. The bedrock is poor in chloride and the area is covered by coniferous forest dominated by Norway spruce (Picea abies (L.) Karst.) and pine (Pinus sylvestris (L.)). The approximate altitude is 100 m.a.s.l. The long term annual mean precipitation in the region is approximately 600 mm and the annual mean temperature is about 6 °C (Raab and Vedin, 1995). A more detailed description of the catchment is given by Maxe (1995). The sampling site (200 m2 ) is located at a discharge area in the catchment with a groundwater level around 150 mm. 2.2. Soil sampling procedures Ten undisturbed soil cores were collected within the sampling site to a depth of 150 mm with the aid of polypropene cylinders with an inner-area of 80 cm2 . A stainless-steel tip facilitated penetration of the root system. In addition, reference samples were collected by sampling three smaller soil cores (inner-area 3.8 cm2 , depth 150 mm) adjacent to each place where an undisturbed core had been collected. The three cores were
Lysimeters were constructed by placing thin PE microfilters (43 lm average pore size, 1 mm thickness) on polypropene bottoms with a horizontally placed stainless-steel pipe. The polypropene cylinders, containing the undisturbed soil cores, were then mounted onto the bottoms. An approximately 20 cm long silicon tube (0.6 cm i.d.) was mounted on the stainless-steel pipe in order to lead leachate, that would be formed during incubation, to an Erlenmeyer flask (E-flask, 250 ml). The mouth of the E-flask with the teflon tube was sealed with plastic film and the E-flask was placed such that it was well below the bottom of the cores. The lysimeters were incubated in a dark climate chamber (10 °C, and 90% humidity) from April 26 to August 31 2000 (i.e. over a period of 128 days), and irrigated twice a week with artificial rain. Due to malfunction of the climate chamber, the humidity dropped slightly below 90% at several occasions during the first 40 days of the incubation period. The amounts of artificial rain corresponds to the weekly mean precipitation according to compiled data for the period 1970–1997 from the meteorological station at Simonstorp (58°460 N; 16°070 O). The chemical composition with respect to major cations and anions corresponds to the monthly mean according to compiled data during the period 1983–1999 from the station situated at Sj€ o€ angen (58°460 N; 14°180 O) and run by Swedish Environmental Research Institute (IVL). The E-flasks were emptied once a week and the amount of leachate was determined by weighting the Eflask before and after emptying the leachate into a polythene flask (150 ml, Kebo lab). The pH of the leachate was determined and the samples were then stored in a deep freezer ()18 °C) until further analyses were conducted. The leachate was analysed with respect to the concentration of organic chlorine (AOX), chloride (Cl ) and total organic carbon (TOC). After termination of the experiment, water content, loss-on-ignition, organic chlorine (TOX) and total amount of chlorine (TX) was determined in the incubated soil as well as in the reference samples that had been stored in a deep freezer during the incubation pe-
M. Rodstedth et al. / Chemosphere 52 (2003) 381–389
riod. The concentration of chloride was determined by subtracting the TOX from the TX values. 2.4. Analytical procedures 2.4.1. Chloride in soil leachate The concentration of chloride in the leachate was determined by potentiometric titration using an automatic titrator (Radiometer, Copenhagen). An aliquot of the leachate (15 ml) was mixed with a carrying electrolyte (15 ml; 1 M KNO3 , 0.2 M HNO3 ) and titrated with AgNO3 (5 mM) to the endpoint. The endpoint was calculated from two curves, where a solution of 14 ml Milli-Q water, 15 ml carrying electrolyte and a chloride solution (1 ml, 0.01 M) was titrated with AgNO3 (5 mM). Duplicate analyses were conducted when possible and blanks were analysed twice or more for each round. 2.4.2. Organic carbon in soil leachate (TOC) The total amount of organic carbon (TOC) in the leachate was determined with a Shimadzu 5000 TOC Analyser. An aliquot of the leachate (10 ml) was diluted with Milli-Q water (40 ml). Duplicate analyses were conducted on each sample. Reference-solutions were analysed as follows; first a Milli-Q water sample, followed by two reference samples with 10 mg TC l1 and 10 mg IC l1 , respectively, followed by a Milli-Q water sample. In addition, Milli-Q water was analysed approximately each 10th analysis. 2.4.3. Organic chlorine in soil leachate (AOX) Organic chlorine in the leachate was determined according to the standard procedure for determination of adsorbable organic halogens (AOX; EU 1485, 1996). In short, a sample was diluted with Milli-Q water to a final volume of 100 ml (3:100 or 1:50; V:V) in an Erlenmeyer flask (300 ml). Activated carbon (50 mg), an acidified nitrate solution (5.0 ml, 0.2 M KNO3 , 0.02 M HNO3 ) and approximately seven drops of concentrated HNO3 were added to the flasks and the suspension was placed on a rotary shaker (1 h, 200 rpm). The suspension was filtered through a polycarbonate filter (0.45 lm) and rinsed with an acidic nitrate solution (20 ml 0.01 M KNO3 , 0.001 M HNO3 ), followed by acidified Milli-Q water (20 ml, pH 2, HNO3 ). The filter with the filter cake were then combusted under a stream of oxygen at 1000 °C in an Euroglas AOX-analyser (model 84/85) in which the formed hydrogen halides were determined by microcoulombmetric titration with silver ions. Each sample was analysed in duplicates. The difference between the duplicates was generally smaller than 0.2 lg Clorg . Blanks were analysed by the use of Milli-Q water. All samples were clearly above the detection limit, which was 5 lg Clorg l1 .
383
2.4.4. Water content, pH and loss-on-ignition in soil samples The water content was determined by drying the soil to constant weight at 65 °C. The soil was then sieved through a 2 mm sieve and representative samples (2 g) were analysed for pH. Loss-on-ignition was determined in five subsamples (5 g) that were placed in crucibles, combusted for 2 h in 620 °C and stored in an exicator until weighting. The amount of organic carbon was estimated as 50% of the weight loss and the median value of the five replicates was used for the calculations. The coefficient of variation was approximately 10%. The soil was then milled (0.12 mm) and stored in glass bottles until TOX and TX analyses were conducted. 2.4.5. Organic chlorine in soil samples (TOX) The concentration of organic chlorine (TOX) in soil was analysed according to Asplund et al. (1994). In short, 20 mg milled sample was added to an acidic nitrate solution (20 ml, 0.2 M KNO3 , 0.02 M HNO3 ) and shaken on a rotary shaker (200 rpm) for at least 1 h. The suspension was filtered through a 0.45 m polycarbonate filter and the analyses then followed the procedure for AOX-analyses described above. Five to eight replicates of each soil sample were analysed and the median was used for calculations. The coefficient of variation among the replicates was approximately 5%. Blanks were analysed according to the same procedure but without addition of soil. All samples were clearly above the detection limit, which was 0.4 lg Clorg g1 . 2.4.6. Total amount of chlorine in soil samples (TX) The total amount of chlorine (TX) was determined by adding 20 mg milled and sieved soil (0.12 mm) to a small crucible followed by direct combustion in the AOX-analyser. Five replicates of each soil sample were analysed and the median was used for calculations. The coefficient of variation among the replicates was between 5% and 10%. Blanks were analysed by combustion of the crucibles without addition of soil. All samples were clearly above the detection limit, which was approximately 0.2 lg Clorg g1 . Chloride was calculated as TX minus TOX. 2.5. Statistical analyses and budget calculations If not otherwise stated, the central tendency is given as median, and the variation is given as first and third quartile within parenthesis after the median. The soil routine of the HBV-model (Bergstr€ om et al., 1985) was run on the hydrological data in order to check the water balance of the lysimeters.
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the onset of the experiment varied from 56 to 69 mm and increased in most of the lysimeters during the incubation period. The field capacity used in the soil routine of the HBV-model varied between 74 and 101 mm and evaporation was estimated to 38–66 mm. The hydrology of the lysimeters could be well described by the model.
3. Results 3.1. General description of the soil cores The soil cores consisted of a thick organic layer (12– 15 cm) with a mixed in mineral content. The mineral content increased with depth causing a diffuse transition to an organic rich mineral layer. No clear horizons were distinguished. The water content was 59% (54–65%), the pHH2 O was 3.55 (3.66–3.40) and the organic matter content 49% (41–53%).
3.3. Chloride balance The accumulated amount of chloride that was added to each lysimeter as artificial rainwater was 0.48 mg Cl and the accumulated amount that was leached with the soil water was 11 (8.8–14) mg Cl (Table 2). The total amount in the lysimeters at the onset of the experiment was 23 (16–28) mg Cl and the total amount in the lysimeters at termination of the experiment was 9 (8–12) mg Cl . When the chloride balance was calculated it was found that the soil in some cases had acted as a sink and in others as a source of chloride (Table 2). The imbalance varied from a loss of 18 mg Cl , to an increase of
3.2. Water balance The accumulated amount of artificial rain added to each of the lysimeters during the incubation period was 223 mm, which corresponds to a daily mean deposition of 1.7 mm. The cumulated amount of leachate leaving the lysimeters varied from around 134 to 159 mm (Table 1). The amount of water within the lysimeters at
Table 1 Water balance in the lysimeters as observed and predicted by the hydrological modelling Lysimeter
Water content start
Time to first leachate (days)
Artificial rain
Leakage
Water content end
Balance
Model evaporation
Difference
1 2 3 4 5 6 7 8 9 10
59 61 56 69 65 57 56 61 64 57
14 26 7 7 26 28 26 26 26 7
223 223 223 223 223 223 223 223 223 223
134 143 144 159 141 145 143 146 147 154
94 89 70 91 84 79 78 75 88 88
54 52 65 42 63 56 58 63 52 38
55 53 66 43 64 57 59 64 52 38
)0.5 )0.4 )0.8 )0.6 )0.6 )1.1 )0.5 )0.5 )0.5 )0.3
The lysimeters have been incubated at 10 °C and 90% humidity for 128 days in dark climate chambers and irrigated with artificial rainwater. All values in millimeter.
Table 2 Chloride balance of the 10 lysimeters that were incubated during 128 days in dark climate chambers at 10 °C and 90% humidity (all values are given in milligram) Lysimeter
Artificial rain
Initial storage
Lost by leachate
Storage at end
Balance
Clorg lost by leachate
Balance
1 2 3 4 5 6 7 8 9 10
0.48 0.48 0.48 0.48 0.48 0.48 0.48 0.48 0.48 0.48
44 23 24 23 15 21 35 30 5.9 11
17 9.2 15 15 12 6.7 8.7 13 10 6.9
31 12 9.6 8.6 7.7 6.9 11 0.69 3.7 8.5
3.1 )2.9 )0.32 0.97 4.9 )7.8 )15 )17 7.3 4.0
2.52 0.29 1.25 2.16 0.33 0.29 0.47 0.96 0.51 0.34
0.59 )3.19 )1.56 )1.19 4.59 )8.10 )15.55 )18.07 6.75 3.63
M. Rodstedth et al. / Chemosphere 52 (2003) 381–389
Chloride balance (mg)
5
385
0.49
< 0.01
0 -5 -10 -15
16-28
-20 0
10
20
30
52-107
40
Initial amount of chloride (mg) Fig. 1. Chloride balance in 10 soil lysimeters as a function of the initial amount of chloride in the lysimeters.
∆ = -14.3 to -8.0
∆ =?
6.8 mg Cl . A correlation was found between the netbalance and the initial amounts of chloride in the lysimeters (Fig. 1).
3.4. Organic chlorine The concentration of organic chlorine (AOX) in the artificial rainwater was less than 5 lg Clorg l1 , which corresponds to a total deposition of less than 10 lg Clorg . The concentration of organic chlorine in the leachate was 0.40 (0.25–1.0) mg Clorg l1 and the accumulated amount of organic chlorine lost with the leachates was 0.49 (0.11–1.17) mg Clorg . The concentration of organic chlorine in the leachates decreased or was unchanged over the incubation period. The chlorine-to-carbon ratio was 3.2 (3.1–8.5) mg Clorg g1 C with a decreasing pattern over time in all but one of the lysimeters. The leachate from one of the lysimeters had remarkably high chlorine-to-carbon ratios with initial values around 40 mg Clorg g1 C and final values around 20 mg Clorg g1 C. The concentration of organic chlorine in the soil cores collected and analysed at the onset of the experiment was 0.25 (0.19–0.41) mg Clorg g1 dw. The concentration in the soil from the lysimeters at the end of the incubation period was 0.30 (0.17–0.53) mg Clorg g1 dw. The amount of organic chlorine in the lysimeters at the end of the incubation period was 81 (72–92) mg Clorg . If the concentration of organic chlorine determined in the soil cores are combined with dry weight data from the lysimeters at the termination of the experiment, the initial amounts in the lysimeters can be estimated to 84 (52–107) mg Clorg . The overall chlorine budget of the lysimeters is shown in Fig. 2.
Fig. 2. Initial storage of organic chlorine and chloride and change in the storage in 10 soil lysimeters during the incubation in climate chambers for 128 days. The input is the amount added by artificial rain and the output is the amount lost as soil leachate. All units are in mg.
4. Discussion 4.1. Loss of organic chlorine by soil leachate The amount of organic chlorine that was lost from the lysimeters during the incubation period by soil leachate is of the same size as the input of chloride by artificial rain. This suggests that the amount of chlorine lost from the system as soil leachate is of such size that it is likely to influence the chloride balance. The organic chlorine concentrations in the leachate collected from the lysimeters are initially rather high. With time, the system asymptotically approached a fairly stable chlorine-to-carbon ratio around 3 mg Clorg g1 C, indicating that the processes approached some sort of steady state conditions. The observed run-off during 1986–1990 at the Stubbetorp catchment was 230 mm yr1 (Maxe, 1995). If we assume that the transport of organic chlorine by soil leachate during the latter half of the incubation period resembles the transport in the field situation, the annual transport of organic chlorine by soil leachate in the catchment can be estimated to about
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0.1 g Clorg m2 yr1 . The annual mean wet deposition of chloride in the Stubbetorp catchment during 1986– 1990 was estimated to 0.4 g Cl m2 yr1 and the loss by run-off for the same period was found to be 0.71 g Cl m2 yr1 (Maxe, 1995). In accordance with the generally agreed upon procedure, the dry deposition was calculated as the run-off minus the wet deposition and thus estimated to 0.31 g Cl m2 yr1 . However, our experiment suggests that the dry deposition is inclined to be underestimated as it was assumed to equal the run-off minus the wet deposition. Instead, the experiment suggests that the dry deposition ought to be 25–30% larger since it is indicated that about 0.1 g Cl m2 yr1 is lost from the system as organically bound chlorine in the soil leachate. A previous estimate of the loss of organic chlorine by soil leachate has been conducted at a spruce € berg forest soil in Klosterhede in Northwest Denmark (O and Gr€ on, 1998). The estimates from the Danish study gave an annual transport with soil leachate of 0.07 g Clorg m2 , which further strengthens the conclusion that considerable amounts of chlorine is lost by soil leachate in the field situation. This strongly suggests that the loss of organic chlorine by soil leachate must be considered when a chlorine budget is constructed for a catchment.
4.2. Chlorination during degradation? The chlorine-to-carbon ratios in the soil leachate (3.2 (3.1–8.5) mg Clorg g1 C) are rather high as compared to the ratios in the soil as a whole (1.1 (0.85–1.37) mg Clorg g1 C). Previous studies have shown that the chlorine-to-carbon ratio increases about one order of magnitude from the litter layer to the A-horizon (i.e. from around 0.1 to 1 mg Clorg g1 soil dw) and that it increases further to 5 mg Clorg g1 soil dw or even more € berg, 1998). Previous studies in the B- and C-horizons (O have shown that the organic matter that is leached through the soil has been subjected to microbial degradation (Guggenberger and Zech, 1994). Hence, the soil organic matter that has been subjected to microbial attack is transported downwards in the soil horizon and some precipitates during the transport. Other studies indicate that a net-formation of organic chlorine takes € berg place during the degradation of organic matter (O et al., 1996a,b). It has been suggested that the underlying mechanism is microbial formation of reactive chlorine species such as HOCl, which enables degradation of organic matter and renders a formation of organic chlorine as a by-product. This hypothesis was strengthened by a recent study where it was found that lignin that had been subjected to reactive chlorine was more easily degraded by P. Crysosporium (Johansson et al., 2000). In addition to fragmentation and oxidation, an increased chlorine content of the organic matter will certainly make it more hydrophilic. These processes do
certainly provide a plausible explanation to the observed higher chlorine-to-carbon ratio in the soil leachate as compared to the soil as a whole, as well as the increasing chlorine-to-carbon ratios with depth previously observed in soil profiles. This hypothesis finds further support in the fact that the chlorine-to-carbon ratios of the leachates in the present study peak at the second or third sampling occasion and thereafter decreases. This is most likely a result of the experimental set-up and the induced disturbance of the soil system. Even though precaution was taken to keep the soil cores undisturbed, it could not be prevented that roots were cut. Hence, new carbon sources were introduced into the system and the microbial communities were suddenly provided with a new carbon source. Consequently, the sampling procedure probably caused increased microbial activity as well as changes in the community structure. According to the line of reasoning above, increased microbial activity would render a formation of water-soluble chlorinated organic matter, which also is observed. 4.3. The chloride balance of the lysimeters When the chloride budget was calculated and modelled for each of the lysimeters, it was found that the soil in some of the lysimeters acted as a sink whereas others acted as a source of chloride. The imbalance varied from a decrease corresponding to an annual loss of 6.0 g Cl m2 yr1 to an increase corresponding to a gain of 2.6 g Cl m2 yr1 . The hydrology of the lysimeters could be well described by the HBV-model, which strongly indicates that the experimental set-up and the observations made during the study were sound. It is thus not plausible that the observed imbalances in the chloride budgets are due to experimental errors. Loss by leaching can only explain a minor part of the deficit and it can certainly not explain the five cases when the lysimeters acted as chloride sources. For soil to act as a sink of chloride, temporary adsorption and uptake by plants is not likely. Hence, only three mechanisms remain that theoretically find support in the literature; formation of non-volatile chlorinated organic compounds, formation € berg, of volatile chlorinated organic compounds (e.g. O 1998; Lobert et al., 1999; Winterton, 2000) and anion exchange. In the soil type here studied, anion exchange is generally considered to be negligible. 4.3.1. Net-changes in the storage of organic chlorine If we assume that the lionÕs share of the observed net-changes is due to a formation of non-volatile compounds, a corresponding change in the storage of organic chlorine would have taken place. In the present study, the initial organic chlorine content of the incubated soil cores was extrapolated from analyses made on soil samples that had been collected adjacent to the cores
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that were to be incubated. However, it was found that the small scale variation of the organic matter content varied to a large extent. As the organic chlorine content is strongly related to the organic matter content, the extrapolations of the initial values are too uncertain to allow conclusions to be drawn concerning changes in the organohalogen storage at the demanded level. The major reason is that the initial amount in the lysimeters had to be extrapolated from the reference samples. It can thus not be conclusively shown whether or not the imbalance in the chloride budget was followed by a corresponding change in the organochlorine storage. The storage of organic chlorine in the lysimeters at the onset of the experiment was approximately four times larger than the storage of chloride was, which is in line with previous studies of top-soil samples in the region (Johansson et al., 2001). Like other natural constituents of organic matter, organic matter-bound chlorine is mineralised during the degradation of the € berg, 1998; O € berg and Gr€ organic matter (O on, 1998). Organic matter-bound chlorine is in other words easily and continuously degraded in soil. Previous studies of net-changes of the organohalogen content in soil has shown that both a net-increase and a net-decrease may € berg et al., 1996a,b, 1997; Johansson et al., take place (O 2001). This shows that both a mineralisation (release of chloride) and a formation (consumption of chloride) of organic chlorine occur in soil, even though the processes hitherto have not been separated. The leachate data of the present study strongly indicate that a formation was taking place in all lysimeters, also in those that acted as a source of chloride. However, if the mineralisation of organic chlorine is larger than the formation of the same, excess chloride will be formed and the soil will act as a source of chloride. This suggests that the mineralisation rate (release of chloride) was larger than the formation rate (consumption of chloride) in the lysimeters that acted as a source of chloride. Little is known on in situ formation of organic chlorine, but even less is known on the degradation processes that underlie the mineralisation of chlorinated organic matter. 4.3.2. Formation of chlorinated volatiles The formation of volatile compounds was not studied in the present study, but this possible sink still deserves a comment. It has since long been known that natural sources, besides industrial releases, contribute considerably to the volatile chlorinated compounds in the atmosphere, (e.g. Lovelock, 1975). Initially, research mainly focussed on marine sources, but it has become clear that other major sources must exist (e.g. Gan et al., 1998; Rhew et al., 2000; Yokuchi et al., 2000). A number of studies have suggested that terrestrial sources may be an important source. Even though the first report on the issue was published already in 1985 (Harper, 1985), the
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information is still very scattered. As pointed out by several authors, it is still not possible to reliably quantify the relative contribution from terrestrial sources (e.g. Khalil et al., 1999). The major reason to this is the lack of sound field data why quantification so far mainly have been based on extrapolations from laboratory studies of single species (e.g. Watling and Harper, 1998). The exception is a recent study focussing on the emission of methyl-chloride and bromide from coastal salt marches indicating fluxes of 0.2–1.2 g m2 yr1 (Rhew et al., 2000). Research on the formation of halogenated volatiles from terrestrial sources has shown that common whiterot fungi are able to methylate chloride (Harper, 1985, 1995; Harper et al., 1988; McNally et al., 1990; Watling and Harper, 1998; Khalil et al., 1999). It has also been found that higher plants are able to produce rather high amounts of chloromethane (Harper, 1995; Gan et al., 1998). In addition, there is evidence that the concentration of methyl chloride and chloroform is higher in soil than in the ambient air, which indicates that such compounds are formed there (Laturnus et al., 1995; Hoekstra et al., 2001; Haselmann et al., 2000). Finally, a recent study suggest that an abiotic formation of chloromethane involving redox reactions with organic matter, iron and chloride takes place in soil (Keppler et al., 2000). Hence, it cannot be excluded that part of the loss of chloride from the lysimeters were due to a volatilisation. However, as very little is known on the formation processes and their dependence on environmental factors such as chloride concentration, it is not possible to even make a qualified guess on the quantities of chloride lost from the system through this route.
4.4. Influence of environmental variables A net-mineralisation has previously been observed during the early decomposition of fresh litter, during early summer periods and as a result of carbonate and € berg et al., 1996a,b, 1997; Jonitrogen amendments (O hansson et al., 2001). A net-formation has been observed after amendment of sulphuric acid and during the fall under long term decomposition of litter. This shows that the turn-over of chlorine in soil is influenced by environmental variables and suggests that the differences among the lysimeters was due to differences in crucial parameters. It is interesting to note the correlation between the chloride imbalance and the initial chloride concentrations in the soil (Fig. 2). A study of the spatial distribution of organic chlorine and chloride in Swedish soil showed a clear correlation between the two variables (Johansson et al., 2002). However, it still remains to be elucidated whether the correlation is due to a pseudocorrelation or if the observed correlation actually is due to a connection through underlying processes.
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4.5. A comment on organic chlorine as an indicator of pollution The concentration of organic chlorine observed in the soil leachates of the present study are extremely high when compared with concentrations observed in surface water or even wastewater (Enell et al., 1989; H€as€anen and Manninen, 1989; Troemel et al., 1989; Jokela et al., 1992; Fleming, 1995). The chlorine-to-carbon ratio observed in the soil leachate in the present study is in most cases slightly higher than those found in surface water. However, remarkably high ratios were occasionally observed in the leachate from four of the lysimeters (>10 mg Clorg g C1 ), and in one case the ratio even varied from 20 to 40 mg Clorg g C1 . During the 1980s, it was argued that the concentration of organic chlorine per se could be used as an indicator of pollution. In the late 1980s and the early 1990s, one started to apprehend the dimensions of the natural chlorine cycle and the detection of organic chlorine is nowadays most often used in a more sensible way. However, extreme values (often considered as those above 200 lg Clorg l1 ) are still often taken as a sign of pollution. The results of the present study further stress the importance to thoroughly evaluate organic chlorine concentration data in relation to its context.
Acknowledgements This project has been financed by MISTRA (The Foundation for Strategic Environmental Research), which hereby is acknowledged. The authors are indebted to Lena Lundman, whom has been of inestimable help and support.
References EN (European Norm) 1485, 1996. Water quality––Determination of adsorbable organically bound halogens (AOX) Approved, April 1996. Asplund, G., Grimvall, A., 1991. Organohalogens in nature, more widespread than previously assumed. Environmental Science and Technology 25, 1346–1350. Asplund, G., Grimvall, A., Jonsson, S., 1994. Determination of total and leachable amounts of organohalogens in soil. Chemosphere 28, 1467–1475. Bergstr€ om, S., Carlsson, B., Sandberg, G., Maxe, L., 1985. Integrated modelling of runoff, alkalinity and pH on a daily basis. Nordic Hydrology 2, 89–104. Conway, E.J., 1942. The chemical evolution of oceans. Proceedings of the Royal Irish Academy 48, 161–212. Enell, M., Kaj, L., Wennberg, L., 1989. Long-distance distribution of halogenated organic compounds (AOX). In: Laikari, H. (Ed.), River Basin Management. Pergamon Press PLC, Oxford, pp. 29–36.
Fleming, B.F., 1995. Organochlorines in perspective. Tappi Journal 78, 93–98. Gan, J., Yates, S.R., Ohr, H.d., Sims, J.J., 1998. Production of methyl bromide by terrestrial higher plants. Geophysical Research Letters 25, 3595–3598. Gribble, G.W., 1996. Naturally Occurring Organohalogen Compounds––A Comprehensive Survey. Springer, Wien, New York. Guggenberger, G., Zech, W., 1994. Composition and dynamics of dissolved carbohydrates and lignin-degradation products in two coniferous forests, N.E. Bavaria, Germany. Soil Biology and Biochemistry 26, 19–27. Harper, D.B., 1985. Halomethane from halide ion––a highly efficient fungal conversion of environmental significance. Nature 315, 55–57. Harper, D.B., 1995. The contribution of natural halogenation processes to the atmospheric halomethane burden. In: Grimvall, A., de Leer, E.W.B. (Eds.), Naturally-Produced Organohalogens. Kluwer Academic Publishers, Dordrecht, pp. 21–34. Harper, D.B., Kennedy, J.T., Hamilton, J.T.G., 1988. Chloromethane biosynthesis in poroid fungi. Phytochemistry (Oxf.) 27, 3147–3153. Haselmann, K.F., Ketola, R.A., Laturnus, F., Lauritzen, F.R., Gr€ on, C., 2000. Occurrence and formation of chloroform at Danish forest sites. Atmospheric Environment 34, 187–193. H€as€anen, E., Manninen, P.K.G., 1989. The total organochlorine and organobromine (AOCl, AOBr) concentrations in water courses and in snow in Finland. VDI Berichte 745, 395–400. Hjelm, O., 1996. Organohalogens in coniferous forest soil (Ph.D. Thesis). Department of Water and Environmental Studies. Link€ oping, Link€ opings Universitet. € berg-Asplund, G., 1995. OrganHjelm, O., Johansson, M.B., O ically bound halogens in coniferous forest soil––Distribution pattern and evidence of in situ production. Chemosphere 30, 2353–2364. Hoekstra, E.J., Duyzer, J.H., de Leer, E.W.B., Brinkman, U.A.T., 2001. Chloroform-concentration gradients in soil air and atmospheric air, and emission fluxes from soil. Atmospheric Environment 35 (1), 61–70. Johansson, E., 2000. Organic chlorine and chloride in soil (Ph.D. Thesis). Department of Water and Environmental Studies. Link€ oping, Link€ opings Universitet. € berg, G., Johansson, E., Krantz-R€ ulcker, C., Zhang, B.X., O 2000. Chlorination and biodegradation of lignin. Soil Biology and Biochemistry 32, 102–1032. € berg, G., Johansson, E., Eben a, G., Sanden, P., Svensson, T., O 2001. Organic chlorine and chloride in Swedish spruce forest soil: Influence of nitrogen. Geoderma 10, 1–13. € berg, G., 2002. Spatial distribution Johansson, E., Sanden, P., O of organically bound chlorine and chloride in forest soil, southern Sweden. Chemosphere, in press. Jokela, J., Salkinoja-Salonen, M.S., Elomaa, E., 1992. Adsorbable organic halogens (AOX) in drinking water and the aquatic environment in Finland. Journal of Water Services Research and Technology––Aqua 41, 4–12. Keppler, F., Eiden, R., Niedan, V., Pracht, J., Sch€ oler, H.F., 2000. Halocarbons produced by natural oxidation processes during degradation of organic matter. Nature 403, 298–301.
M. Rodstedth et al. / Chemosphere 52 (2003) 381–389 Khalil, M.A.K., Moore, R.M., Harper, D.B., Lobert, J.M., Erickson, D.J., Koropalov, V., Sturges, W.T., Keene, W.C., 1999. Natural emissions of chlorine-containing gases: reactive chlorine emissions inventory. Journal of Geophysical Research 104, 8333–8346. Laturnus, F., Mehrtens, G., Gr€ on, C., 1995. Haloperoxidaselike activity in spruce forest soil––a source of volatile halogenated organic compounds. Chemosphere 31, 3709– 3719. Lobert, J.M., Keene, W.C., Logan, J.A., Yevich, R., 1999. Global chlorine emissions from biomass burning: reactive chlorine emissions inventory. Journal of Geophysical Research 104, 8373–8389. Lovelock, J.E., 1975. Natural halocarbons in the air and in the sea. Nature 256, 193–194. Maxe, L., 1995. Effects of acidification on groundwater in Sweden. Swedish Environmental Protection Agency: 166. McNally, K.J., Hamilton, J.T.G., Harper, D.B., 1990. The methylation of benzoic and n-butyric acids by chloromethane in Phellinus pomaceus. Journal of General Microbiology 136, 1509–1515. Myneni, S.C.B., 2002. Formation of stable chlorinated hydrocarbons in weathering plant material. Science 295, 1039– 1041. Neidleman, S.L., Geigert, J., 1986. Biohalogenation: Principles, Basic Roles and Applications. Ellis Horwood Limited, Chichester. € berg, G., 1998. Chloride and organic chlorine in soil. Acta O Hydrochemica et Hydrobiologica 26, 137–144. € berg, G., Gr€ O on, C., 1998. Sources of organic halogens in spruce forest soil. Environmental Science and Technology 32, 1573–1579.
389
€ berg, G., B€ O orjesson, I., Samuelsson, B., 1996a. Net change in organically bound halogens in relation to soil pH. Water Air and Soil Pollution 89, 351–361. € berg, G., Nordlund, E., Berg, B., 1996b. In situ formation of O organically bound halogens during decomposition of Norway spruce litter––effects of fertilization. Canadian Journal of Forest Research 26, 1040–1048. € berg, G., Brunberg, H., Hjelm, O., 1997. Production of O organically bound halogens during degradation of birch wood by common white-rot fungi. Soil Biology and Biochemistry 29, 191–197. Raab, B., Vedin, H. (Eds.), 1995. Klimat, sj€ oar och vattendrag. Nationalatlas. Bokf€ orlaget Bra B€ ocker, H€ ogan€as. Rhew, R.C., Miller, B.R., Weiss, R.F., 2000. Natural methyl bromide and methyl chloride emissions from coastal salt marshes. Nature 403, 292–295. Schlesinger, W.H., 1997. Biogeochemistry. An Analysis of Global Change. Academic Press, San Diego. Troemel, G., Muszik, J., M€ uller, F., 1989. Naßfestmittel–– AOX-belastung im Abwasser. Wochenblatt f€ ur Papierfabrikation 17 (2), 63, 66–68. Watling, R., Harper, D.B., 1998. Chloromethane production by wood-rotting fungi and an estimate of the global flux to the atmosphere. Mycological Research 102 (7), 769–787. Winterton, N., 2000. Chlorine: the only green element–– towards a wider acceptance of its role in natural cycles. Green Chemistry 2, 173–225. Yokuchi, Y., Noijiri, Y., Barrie, L.A., Toom-Sauntry, D., Machida, T., Inzuka, Y., Akimoto, H., Li, H.-J., Fujinuma, Y., Aoki, S., 2000. A strong source of methyl chloride to the atmosphere from tropical coastal land. Nature 403, 295– 298.