Environ. Sci. Technol. 1992,26,834-836
Evidence for an Increase in the Cadmium Content of Herbage since the 1860s Kevin C. Jones,"*+Andrew Jackson,*,§ and A. E. Johnston11 Institute of Environmental and Biological Sciences, Lancaster University, Lancaster, LA 1 4YQ, UK, Department of Geography and Earth Sciences, Queen Mary and Westfield College, University of London, Mile End Road, London, E l 4NS, UK, and Institute of Arable Crops Research, Rothamsted Experimental Station, Harpenden, Hertfordshire, AL5 2JQ, UK
Introduction Atmospheric deposition is a major source of heavy metals to agroecosystems in industrialized countries (1). Long-term deposition has resulted in the accumulation of some elements (notably Cd and Pb) in soils, so that the burden in contemporary surface horizons is considerably above the historical background level (2-4). Direct surface contamination of atmospherically-derived metals onto vegetation may also be important as a source of metals to foliage, even in rural locations (5-7). Atmospheric emissions of heavy metals from anthropogenic activities have increased substantially worldwide over the last century (8), so inputs to crop plants will have changed through time (4). We report here that Cd concentrations in herbage from a semirural permanent pasture plot in the United Kingdom have increased over the last century, from 102-152 pg/kg between 1861 and 1920 to values consistently above 200 pg/kg between 1940 and 1989. This has important implications for long-term changes in human exposure to Cd, since plant-based foods are the most important source of Cd in the human diet (9). Humans are exposed to Cd from various sources. Dietary intake of Cd in plant-based foodstuffs makes the largest contribution to the general population, but absorption through the lungs from cigarette smoking or ingestion of offal and seafood are significant routes of exposure for many individuals (9, 10). In turn, Cd may enter crops and livestock following uptake from the soil or direct atmospheric deposition onto the foliar portion of plants. Using the principle of isotope dilution, Hovmand et al. (5) showed that between 20 and 60% of grassland foliar Cd at a rural site in Denmark was atmospherically-derived. Atmospheric Cd may also be absorbed into and transported throughout the plant (11). Although most research has emphasized the inputs of Cd in sewage sludges (12) and phosphate fertilizers (13) to agricultural land, atmospheric deposition makes an extremely important contribution nationally or regionally (1,14,15). Deposition and phosphate fertilizers can both result in an underlying long-term increase in soil Cd, with average inputs calculated at ca. 3 g of Cd ha-' year-l to European agricultural soils (14,15),compared to average inputs of ca. 80 g of Cd ha-l year-l to the small percentage of all agricultural land which receives sewage sludge (11, 14). These rates of input are greater than losses by crop offtake, leaching, etc., so mass balance calculations suggest that soil Cd concentrations will tend to increase over time (15). Evidence for this has been obtained by analysis of archived and contemporary soils from several long-term field experiments (3,12,13,15).We have shown previously that soil plough layer (0-23 cm) Cd concentrations at Rothamsted Experimental Station, a semirural site in southeast England, have increased by between 25 and 55% solely as a result of cumulative atmospheric deposition + Lancaster University. t University
of London. Present address: Environmental Resources Limited, 106 Gloucester Place, London W1H 3DB, UK. 1' Rothamsted Experimental Station. 834
Environ. Sci. Technol., Vol. 26, No. 4, 1992
Table I. Comparison between C d Measured b y AAS and
NAA
sample
AAS
NAA
sample
AAS
NAA
1861-1865 1876-1880 1896-1900 1921-1925
109 144 133 170
103 f 7 171 f 9 132 f 8 164 f 8
1936-1940 1956-1960 1981-1985
252 182
250 k 10 180 f 10 217 f 8
221
"Units, pg/kg dry weight.
inputs since the 1840s (3),while Steinnes has demonstrated large-scale long-term regional contamination of Norwegian surface soils with Cd due to atmospheric deposition ( 2 ) . Since the behavior of Cd in the soil is mainly governed by reversible sorption processes (15),increasing soil concentrations will presumably lead to higher plant concentrations. The data presented here provide the first unequivocal evidence for a long-term increase in plant Cd concentrations. Experimental Section The herbage samples were archived annually over the last 130 years from Park Grass, one of the long-term classical experiments at Rothamsted (16). These samples have recently been analyzed for P b with a view to indirectly monitoring changes in the atmospheric loading of P b over the last century (6),particularly since the recent decline in air P b concentrations following reductions in the P b content of gasoline (17). The control plot at this site has never received fertilizer additions and has been undisturbed (i.e., unploughed) for over 300 years. Soils in the control plot had a Cd content of -0.19 mg/kg in 1876, which had increased to -0.29 mg/kg a century later (3),a value typical of contemporary U.K. surface soils. The soil has a pH of 5.3 and is -5% organic matter. Herbage samples have also been sampled from a separate subplot, limed since 1903 to pH 7.1. The pH of the control plot has varied very little over the last century (18). The change in soil pH due to liming has affected the botanical composition and yield of the mixed population of grasses, clovers, and other species growing on the plots (16). Herbage has been harvested twice each year, in June and September, and was unwashed prior to storage and analysis. The June samples only have been bulked and homogenized for 5-year intervals and analyzed "blind in duplicate or triplicate for Cd using autoprobe electrothermal atomization atomic absorption spectrophotometry, along with blanks, reference materials, and spiked samples. Six replicate analyses of samples from 1985-1989 gave a coefficient of variation of 4.8%, indicating a low scatter on the data. Some samples were cross-checked by a neutron activation analysis method (19),which gave excellent agreement (see Table I). Recoveries of spiked samples by AAS were consistently high, averaging 88.5%, while the method gave excellent agreement with certified values for reference materials. Results and Discussion The full data set for the pH 5.3 plot is shown in Figure 1. As noted in previous publications on temporal trends
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-
. j 200 0 I
150 100
50
...
1
. i
D m
1
0 1860
I
1880
1900
1920
1940
1960
1980
Flgure 1. Temporal trends in the Cd content of herbage at Park &ms, Rothamsted. U.K.
in herbage (6, 17, 19), yield can be an important confounding factor which makes it difficult to study trends in concentrations. Concentration increases are of concern because of the implications for increased Cd in the human food chain. Yields on the control plot have varied between 0.70 (in 1936-1940) and 2.30 t/ha between 1861 and 1989, generally decreasing slightly in the first 20-30 years of the experiment, but not changing systematically since that time. Cadmium offtakes (i-e.,concentration X yield) have varied between -50 and 350 mg of Cd ha-l year-l and are subject to greater “noise” than the concentration data alone. Figure 1 shows a clear increase in Cd concentrations since the start of the experiment. Three “phases” appear in the control plot (soil pH 5.3) data: (i) reasonably steady values of between 102 and 152 pg of Cd/kg between 1861 and 1920, (ii) a sharp increase in concentrations between 1920 and 1940 up to 250 pg/kg, and (iii) a “plateau” between 1940 and 1989 consistently above 200 pglkg. Increasing soil pH is known to result in decreased plant Cd uptake (15,20). Not surprisingly, therefore, the Cd content of herbage from the limed plot has been consistently lower, on average about half that on the unlimed control. Concentrations since liming began in 1916 have varied between 72 and 191 pg of Cd/kg, with the trends broadly mirroring those in the unlimed control. There was a decline in Cd concentrations in the most recent samples (1986-1989), but it is too early to say whether this is part of a more general decline, such as that observed in dated lake sediment (21) and ice cores (22) from rural and remote sites in the Northern Hemisphere. The long-term underlying increase in soil Cd concentrations at this site due to the cumulative effect of atmospheric deposition inputs may at least partially account for the increase in herbage Cd concentrations, since there is a clear positive correlation between soil and plant Cd concentrations in acid soils (11,15,20). However, inputs of atmospherically-derived Cd directly onto the herbage are also likely to be important in contributing to the increase (4,5,11). The major contemporary sources of Cd to the U.K. atmosphere are thought to be municipal waste incineration (5 t of Cd/year), nonferrous metal production (3.7 t of Cd/year), iron and steel production (2.3 t of Cd/year), and fossil fuel combustion (1.9 t of Cd/year) (14). Releases to the U.K. atmosphere from municipal waste incineration are likely to have increased over recent decades, while the other sources have probably declined (23). Air Cd concentrations will vary widely through the country. Typical rural values are -0.5-4 ng of Cd/m3,
those in urban areas 1-50 ng of Cd/m3. Rothamsted is a semirural site, suggesting that the temporal trends observed here may be broadly mirrored elsewhere in the United Kingdom. Plant-based foodstuffs, particularly cereals and leafy vegetables, are the major source of human Cd exposure in the general population (9). The increases in herbage concentrations reported here will presumably have occurred, to a greater or lesser extent, in other plants. In particular, leafy vegetables tend to take up higher concentrations of Cd and are more affected by direct deposition of Cd onto edible portions (11, 12, 19). The intake of Cd by livestock grazing on herbage (and hence levels in offal) is also likely to have increased over recent decades. The typical level of Cd intake by the general population (-20 pg/day in the United Kingdom; between -15 and 55 pg/day in Europe, North America, and Japan) (9) is below the WHO recommended maximum intake of 1pg (kg of body weight)-l day-l (equivalent to 54 and 70 pg of Cd/day for a typical adult woman and man, respectively) (24),although the limit may be approached or exceeded by smokers and individuals eating a high proportion of certain Cd-rich foodstuffs (9, 10, 12, 15, 25). It seems likely that human intake of Cd derived from environmental sources is higher now than a century ago. This is undesirable, given that Cd is a cumulative poison which causes kidney dysfunction in middle age above certain concentrations (26,27). It would be prudent to take steps to reduce further inputs of Cd to agroecosystems, since metals are very persistent in surface soils (2,28)and soil Cd appears to remain bioavailable in the long term (28). Ultimately this will limit the major sources of human exposure (15). Given the diffuse nature of atmospheric sources (8,23),reductions to soil nationally can perhaps be achieved most economically by reducing the Cd content of P fertilizers during their manufacture (9, 29), or by judicious use of those sources of rock phosphate which are inherently low in Cd. Registry No. Cadmium, 7440-43-9.
Literature Cited (1) Nriagu, J. 0.;Pacyna, J. M. Nature 1988, 333, 134-137. (2) Steinnes, E.; Solberg, W.; Petersen, H. M.; Wren, C. D. Water, Air, Soil, Pollut. 1989, 45, 207-218. (3) Jones, K. C.; Symon, C.; Johnston, A. E. Sci. Total Environ. i987,67,75-89. (4) Jones, K. C. Enuiron. Pollut. 1991, 69, 311-325. (5) Hovmand, M. F.; Tjell, J. C.; Mosbaek, H. Enuiron. Pollut. 1983, 30, 27-38. (6) Jones, K. C.; Johnston, A. E. Enuiron. Sci. Technol. 1991, 25, 1174-1178. (7) Chamberlain, A. C. Atmos. Environ. 1983, 17, 693-706. (8) Nriagu, J. 0. Nature 1979, 279, 409-411. (9) Hutton, M. Cadmium in the European Community. Technical Report No. 26; Monitoring and Assessment Research Centre, University of London, 1982. (10) Sharma, R. P.; Kjellstrom, T.; McKenzie, J. M. Toxicology 1983,29, 163-171. (11) Harrison, R. M.; Chirgawi, M. B. Sci. Total Enuiron. 1989, 83, 47-62. (12) Davis, R. D. Experientia 1984, 40, 117-126. (13) Mortvedt, J. J. J. Enuiron. Qual. 1987, 16, 137-142. (14) Hutton, M.; Symon, C. Sci. Total Enuiron. 1986, 57, 129-150. (15) Christensen, T. C.; Tjell, J. C. In Heavy Metals in the Environment; Farmer, J. G., Ed.; CEP Consultants: Edinburgh, 1991; Vol. 1, pp 40-49. (16) Thurston, J. M.; Williams, E. D.; Johnston, A. E. Ann. Agron. 1976,27, 1043-1082. (17) Jones, K. C.; Symon, C.; Taylor, P. J. L.; Walsh, J.; Johnston, A. E. Atmos. Enuiron. 1991,25A, 361-369. Environ. Sci. Technol., Vol. 26, No. 4, 1992 835
Environ. Sci. Technol. 1992, 26, 836-837
(18) Johnston, A. E.; Goulding, K. W. T.; Poulton, P. R. Soil Use Manag. 1986,2, 3-10. (19) Jones, K. C.; Johnston, A. E. Environ. Pollut. 1989, 57, 199-216. (20) Adriano, D. C. Trace Elements in the Terrestrial Environment; Springer Verlag: Berlin, 1985. (21) Sanders, G.; Jones, K. C.; Hamilton-Taylor, J.; Dorr, H. submitted for publication in Environ. Toxicol. Chem. (22) Boutron, C. F.; Gorlach, U.; Candelone, J.-P.; Bolshov, M. A.; Delmas, R. J. Nature 1991, 353, 153-156. (23) Hutton, M. Sei. Total Environ. 1983, 29, 29-47. (24) W.H.O. Tech. Rep. Ser. 1972, No. 505. (25) Ministry of Agriculture Fisheries and Food. Survey of Cadmium in Food; Food Surveillance Paper No. 12; HMSO: London, 1983.
(26) Hutton, M. Evaluation of the Relationships Between Cadmium Exposure and Indicators of Kidney Function. Technical Report No. 29; Monitoring and Assessment Research Centre, University of London, 1983. (27) Ellis, K. J.; Yuen, K.; Yasumura, S.; Cohn, S. H. Environ. Res. 1984, 33, 216-226. (28) McGrath, S. P. In Pollutant Transport and Fate in Ecosystems; Coughtrey, P. J., Martin, M. H., Unsworth, M. H., Eds.; Blackwell: Oxford, U.K., 1987; pp 301-317. (29) Sauerbeck, D. Plant Res. Dev. 1984, 19, 24-34.
Received for review October 22, 1991. Revised manuscript received December 19,1991. Accepted December 26,1991. K.C.J. is grateful to the Agricultural and Food Research Council for financial support.
CORRESPONDENCE Comment on "Human Exposure to Volatile Organic Compounds in Household Tap Water: The Indoor Inhalation Pathway "
on the species being transferred. By analogy with early theoretical work on heat transfer in a laminar boundary layer, Nu can be shown to vary with the 1 / 3 power of Sc ( 4 ) . McKone uses this theoretical relationship in order to describe the dependence of the mass-transfer coefficient on the diffusivity of the transferring species, or
SIR In a research paper (1) that appeared in this journal, McKone provided an assessment of the impact on indoor air quality of the release of volatile organic compounds (VOCs) from household water. Due to a lack of mass-transfer data, a relationship was derived which adjusts the measured transfer efficiency for radon to that for VOCs such as 1,2-dibromo-3-chloropropane (DBCP) using the Henry's law constant and liquid and gas diffusivities. Subsequent publications have repeated the derivation (2) and used the result to test hypotheses concerning mass transfer in showers (3). Although the relationship was only intended to be approximate, there is an error in the derivation which casts doubt on its reliability, especially when applied to compounds of low volatility. McKone's derivation is first briefly reviewed. The overall mass-transfer coefficient K (m/s) at the air-water interface reflects the resistance through both the liquid and gas phases
NuL a ScL1l3
(4)
NuG
(5)
om
\-I
where KL and KG are the liquid-phase and gas-phase mass-transfer coefficients (m/s), respectively, R is the gas constant (0.0624Torr m3/mol.K), T i s absolute temperature (K), and H is the Henry's law constant (Torr m3/mol). The liquid- and gas-phase mass-transfer coefficients may be expressed in terms of the Nusselt number, or KL = DLNuL/LL (2) KG = DGNuG/LG
(3)
where DL and DG are the diffusion coefficients (m2/s)of the compound, NUL and NuG are Nusselt numbers, and LL and L G are characteristic lengths (m) in water and air, respectively. Dimensional analysis of convective mass transfer suggests that the Nusselt number is a function of the Reynolds number (Re) and the Schmidt number (Sc) ( 4 ) . Of these two dimensionless groups, only Sc depends 636 Environ. Sci. Technol., Voi. 26, No. 4, 1992
a
ScGli3
where ScL = vL/DL and SCG= vG/DG are the Schmidt numbers in water and air, respectively, vL is the viscosity of water (9.82X lo-' mz/s at 20 "C), and vG is the viscosity of air (1.56 X loy5mz/s at 20 "C). McKone then combines eqs 2-5 and finds KL = O . ~ ( D L ~ / ~ / D G ~ / ~ ) K G (6) which he substitutes into eq 1 to obtain (7)
where /3 is presented as a dimensionless constant that depends upon the physical situation, but is independent of the species under consideration (1). From dimensional considerations, it is apparent that the constant P given in eq 7 cannot be dimensionless. Of greater concern, however, is eq 6, which must include a constant of proportionality, a, or KL = ~ u ( D L ~ ~ ~ / D G ~ ~ ~ ) O . ~(8) KG The proportionality constant a will be carried through to eq 7 resulting instead in
(9) where a = ALG/BLLand p* = AvG1i3/LL.A and B are the constants of proportionality in eqs 4 and 5,respectively, and are related to the Reynolds number of the appropriate phase. The constant p* has the correct dimensions and depends only on the hydrodynamic conditions. Equation 9 has the same form as eq 7 , except for the dimensionless a which appears in the term relating to the gas-phase resistance. Therefore, unless a has a value of unity,
0013-936X/92/0926-0836$03.00/0
0 1992 American Chemical Society
