More widespread than previously assumed
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1346 Environ. Sci. Technol.. Vol. 25, NO. 8, 1991
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001 3-936)(/91/0925-1346$02.50/00 1991 American Chemical Society
Gunilla Asplund Anders Grimvall Linkoping University S-581 83 Linkoping Sweden Although the natural production of organohalogens has been observed in several studies, it is generally assumed to be much smaller than the industrial production of these compounds ( I , 21. Nevertheless, two important natural sources have been known since the 1970s: red algae in marine ecosystems produce large amounts of brominated compounds (31, and methyl halides of natural origin are present in the atmosphere ( 4 , 5). During the past few years it has been shown that organohalogens are so widespread in groundwater, surface water, and soil (6-10) that all samples in the studies ref e r r e d to c o n t a i n m e a s u r a b l e amounts of adsorbable organohalogens [AOXI. In addition, the quantities found often exceed the amount that can be explained by human activities in surrounding areas. We will document the widespread occurrence of organohalogens in “unpolluted” soil and water and discuss possible sources of these compounds. It has been suggested that these organohalogens originate from long-range atmospheric transport of industrially produced compounds ( 1 1 ) . We will review existing evidence of enzymatically mediated halogenation of organic matter in soil and show that, most probably, natural halogenation in the terrestrial environment is the largest source. Occurrence in soil and water To document the natural occurrence of organohalogens, we conducted a survey of 1 3 5 lakes in southern Sweden and found concentrations of AOX ranging from 11 to 185 pg CIlL (Figure 1).This corresponds well with the results of the studies referred to above, which indicate that all surface waters contain organohalogens. The highest concentrations in our survey were found in humic-rich, oligotrophic lakes in remote areas where the AOX concentrations were shown to be comparable with those in industrially polluted waters, such as the Rhine River; along a profile from the source of this river to the Dutch border, AOX concentrations varied from 5 to 200 pg CllL (12). To document further the global occurrence of organohalogens in
terrestrial environments, we analyzed soils from different parts of the world (Table 1).We found that all samples contained organohalogens and that the ratio of organohalogens to organic carbon was remarkably stable (0.22-2.8 mg Cllg C). Moreover, the data presented in Table 1 show that the occurrence of halogenated compounds in soil is not a phenomenon peculiar to Swedish soils; on the contrary, organohalogens seem to occur worldwide. The variability of the orgauohalogen-to-organic-carbon ratio for surface water samples (0.84-14.5 mg Cllg C) was larger, and the median was almost 10 times higher than for soil samples (Figure 2). In our surveys of AOX in water and soil, we analyzed the water samples according to the German standard procedure (13). For soil samples, however. there is no stan-
many, a survey of rainwater samples resulted in a mean value of 20 pg CllL ( 1 0 ) . The total annual deposition of organohalogens in Sweden (3700 metric tons [tonnesI/year),measured as bulk precipitation, approximately equals the total annual riverine loading ( 1 1 ) . However, mass balance calculations for selected river basins strongly indicate that sources other than atmospheric deposition dominate. Large local variations exist between adjacent streams and rivers, and the concentration of AOX in runoff sometimes is 10 times higher than in precipitation ( 1 1 , 14). Furthermore, as was shown in a mass balance study of a raised bog in Sweden, there must be substantial amounts of naturally produced AOX in soil and water (9); local anthropogenic sources of AOX in the study area were negligib
d
-d The quantities detected often exceed the amount that can be explained by human activities in the surrounding areas
dard method. Nevertheless, a special study of the procedure used in the present investigation gave satisfactory results; the measured AOX concentrations in soil are reproducible, and we found no evidence of artifacts that could jeopardize our conclusion about the widespread occurrence of organically bound halogens in soil. A nonindustrial source The prevalence of AOX in remote areas implies that local sources of pollution are not the major explanation for observed concentrations in soil and water. A more substantial contribution could be made by the long-range atmospheric transport of naturally or industrially produced compounds. In Sweden, for example, the average AOX concentration in bulk precipitation has been estimated to be 15 pg CllL ( 1 1 ) ; in Ger-
and the total pool of AOX in the bog (> 1200 tonnes) was found to be more than 300 times larger than the annual atmospheric deposition (< 3.8 tonnes). To summarize, these observations indicate that local pollution and atmospheric deposition are responsible for only part of the widespread occurrence of AOX. Natural halogenation processes in terrestrial or limnic (lake and river) environments also must contribute substantially to the AOX in soil and water. Production in fresh water unlikely Outflows from lakes seem to have lower concentrations of organohalogens than do the lakes’ tributaries ( 1 4 ) . In addition, the highest concentrations in rivers most often are found downstream from peat bogs and in other areas having elevated concentrations of organic matter. Environ. Sci. Technol., Vol. 25, No. 8.1991 1347
This indicates that the halogenated organic compounds are more likely leached from surrounding soils than produced in the water. Furthermore, a large number of terrestrial organisms such as fungi, lichens, bacteria, and higher plants are known to produce halometabolites ( Z ) , whereas very few limnic suecies have been reuorted to have this capacity. Thus no evidence is available that strengthens the hypothesis of a net production of organohalogens in fresh water. However, it cannot be totally ruled out that biological production, which is masked by sedimentation, evaporation, or degradation, occurs in lakes. Terrestrial production
FIGURF ?
Ratio of adsorbable organohalogens (AOX) to total organic carbon (TOC) in surface water, soil, and fulvic acids'
H
Fulvic acids ( n = 3)
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I 1348 Envimn. Sci. Tedlnol., Vol. 2.5,
No. 8, 1991
According to Engvild (15), more than 80 plants are known to produce halometabolites. It also has been shown that the concentration of organohalogens in rain falling through spruce trees sometimes is more than 10 times higher than levels in free precipitation ( 1 4 ) . These compounds may originate from dry deposition, photochemical oxidation on the needles, or biohalogenation in the tree or on the needles. Studies recently performed in climate chambers in our laboratory show that organohalogens can be continuously washed from spruce trees. This indicates that such compounds are produced by the tree or possibly by biological or chemical processes on the surface of the needles. Consequently, plants might contribute to the organohalogens in the environment, although further investigations are needed to determine the extent of and the mechanisms behind such production. Several studies have shown that many soil organisms are known to produce halometabolites (2, 16). In addition, as mentioned above, all soils seem to contain organohalogens. Thus, a natural production in soil is another hypothesis that calls for investigation. Is enzyme action a mechanism? Haloperoxidases constitute a group of enzymes that catalyze the halogenation of many organic substances in the presence of hydrogen peroxide and halide ion 121. Chloroperoxidases (CPO),which oxidize chloride, bromide, and iodide, have been thoroughly investigated mainly through studies of a specific enzyme [the enzyme EC 1.11.1.10, CPO) from the fungus Coldoriomyces fumago ( 1 71.
,
Concentration of adsorbable organohalogens (AOX) in soil samples obtained worldwide Sampling site
Mochudi. Botswana
Mochudi, Botswana Manaos, Brazil Marondera, Zimbabwe N. E. Alberta, Canada N. E. Albelta, Canada N. E. Alberta, Canada Ayer Itam. Malaysia Penang Hill. Malaysia Penang Hill. Malaysia Mount Kintoki. Japan Cockle Park Farm, Great Britain Cockle Park Farm, Great Britain Klcckrike, Sweden Vallmo. Sweden Axsjon. Sweden Snogerupsan, Sweden Snogerupsan. Sweden Horby. Sweden Herby, Sweden Dalir, Iceland Dalir, Iceland Dalir, Iceland Antalya. Turkey Antalya, Turkey Antalya, Turkey
AOX lvg Cllg d.w.4
Vegetatlon
Steppe Steppe Campmaranad Savanna Peat bog, 0-10 cm Peat bog, 1040 cm Peat bog, 40-50 cm Deciduous forest Deciduous forest Deciduous forest Bamboo forest Meadow
5 4
.
Standard
devlatlon
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..
Meadow Garden Pasture Pine tree forest Creek bank Field Beech forest. 5-10 cm Beech forest. 35-40 cm Arctic heath Arctic heath Arctic heath, brook ravine Aleppo pine forest, 0-5 cm Aleppo pine forest, 5-10 cm Aleppo pine forest, 10-20 cm
Dry weight. bLoss on ignition.
CCalculaledvalues of the ralio of AOX 10 total organic carbon (AOW0.5 x L-0-1). 10,000and it is active only in the presence of hydrogen peroxide. The activity is pH-dependent with a pH-optimum close to %. . that of CPO which, under the labo: ratory conditions of the study, was & ,+.e 3.54.In addition, the activity of the .a* soil extract and CPO is inhibited by the addition of specific organic compounds. This implies that enzymatically mediated halogenation of organic matter could be the mechanism that produces organohalogens in soil. tion of total organic carbon (TOC) tiansen (19)showed that iodoperoxidase catalyzes the incorporation of (11). In another study, Wigilius et The role of humic substances al. (7)showed, by size exclusion radioactive iodide into humic acids. Studies of Swedish surface waters chromatography, that halogenated Furthermore, fulvic acids isolated previously have shown that the compounds in surface water are from groundwater wells have been concentration of AOX often is posi- present in the same fractions as shown to contain AOX (9). In our survey of 135 lakes in tively correlated to the concentra- most of the humic material. Chris-
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Environ. Sci. Technol.. Vol. 25, No. 8, 1991 1349
southern Sweden, a positive relationship can be seen between the concentration of AOX and w a t e r color (Figure 31, but the correlation between the concentration of AOX and that of TOC is less pronounced (Figure 4). The lakes with a high TOC and a low concentration of organohalogens are eutrophic, w h i c h implies that only a minor part of the
organic matter in these lakes consists of humic material. This suggests that the organohalogens in surface water are related to h u m i c matter, rather than to organic matter in general. We are indebted to Dr. David Hopkins and Dr. Anthony G. O'Donell, University of Newcastle-upon-T ne, U.K.; Dr. Larry W. Turchenek, Allerta Research Council; and Prof. Steve Hrudey, University of Alberta, Canada, for providing us with soil samples.
17(10), 1985-94.
Gron, C. Dissertation, Institute of Applied Geology, Technical University of Denmark, 1989. (9) Asplund, G.Sci. Total Envimn. 1989, 81/82, 239-48. (101
von Klopp, R.; Kornatzki, K-H. Z. Wasser- Abwasser- Forsch. 1987, 20, 160-67.
.1111, Enell. M. et al. In River Basin Manore,
~~~~~~~~~
~
~~~~~~~~~~~~
D~
ment-K Laikari, H., Ed.; Pergamon Press PLC Oxford, 1989; pp. 29-36. (12) Keller, M. Vom Wasserl98S, 72,199210.
(Deutsche lndustrie Normen); DIN 38409, Teil 14; Beuth-Verlag: Berlin, 1985. (14) Grimvall, A. et al. Presented at the 6th European Symposium on Oxanic Micropollutants in the Aquatic Environment, May 22-24,1990, Lisbon. (15) Engvild, K.C. Phytochemistly 1986, 25,781-91.
(16) Siuda, 1. F.;de Bernardis, J. F. Woydia 1973, 36, 107-43.
References
Hewson, W. D.; Hager, L. P. In The Porphyrins, Vol. VU, Biochemistry, Part B: Dolphin, D., Ed.; Academic Press: New York, 1979; pp. 295-332. (18) Asplund, G. et a]. In Lecture Notes in Earth Sciences; Allard, 8.; BorBn, H.; Grimvall, A,, Eds.; Springer Verlag: Berlin, 1991; pp. 475-83. (19) Christiansen, I. Dissertation, RisB-M-
(171
Hoffman,H-I. et al. Vom Wasser1988, .71., 175-24 .- ..
Neidleman, S. L.; Geigert, J. Endeavour, New Series 1986, 1 1 , 5-15. (3) Fenical, W. In Elsevier Oceanography Series, 31: Marine Organic Chemistry: Duursma, E. K.; Dawson, R., Eds.; Elsevier: Amsterdam. 1981; pp. 375-93.
(2)
2851, Risn National Laboratory, Denmark, 1990.
(8)
(13) DIN
Acknowledgments
(11
Lovelack, 1. E. Nature 1975,256,193-94. Harper, D. B. Nature 1985,315,55-57. ( 6 ) Stevens, A. A. et al. 1. A m . Water Works Assoc. 1985, 77, 146-54. (7) Wigilius, B. et a]. Chemosphere 1988.
(41 (51
Cunilla Asplund IS a 1'h.D. itudi!nt in n a t r r a n d environmenral siud,ec at Linkoping l.'niiwnity. She will prrsrnt a thesis on the natiiral production o/ halogenated organic compounds in the terri:strial environment iaithin a yeur. Asplund holds ri B.Sc. degree In biology ond tem~striolecologv from Linkoping Ilniversitv. t l r r rrsearch interests am in the origin und q p c t s of organohologens und cnvimnmentol policy ancl).s,s. Anders Grimvull is u projessor of r n v ronmcnfal ccitwres in the departrriant of water and erii.ironmmta1 itudirs at Linkoping I'nivercify. He holds a P1i.D in probobilitv and statistics from fhP Universih. of (;btehorg. Sweden 11;s research IniereI'ts include orguni(. pollutants in ivutcr. wtrophicalion of surface ivuters, and thr, statistical anolysis ofenvironmental monrforing dutu.
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