Environ. Sci. Technol. 1996, 30, 252-259
Bioaccumulation of Hydrophobic Chemicals in Agricultural Food Chains MICHAEL S. MCLACHLAN* Ecological Chemistry and Geochemistry, University of Bayreuth, 95440 Bayreuth, Germany
The bioaccumulation of polychlorinated biphenyls, dibenzo-p-dioxins, dibenzofurans, and hexachlorobenzene in an air-plant/soil-cow-human food chain was examined using field data collected in southern Germany. The fugacity of many compounds was similar in air, soil, and plants, suggesting near-equilibrium partitioning with somewhat higher fugacities in cows’ milk indicative of moderate biomagnification. However, the fugacities of the more involatile, hydrophobic compounds decreased by up to several orders of magnitude from air to plants to cows’ milk. This phenomenon, termed biodilution, can be explained by the kinetically limited uptake of less volatile compounds in plants and the reduced absorption of very hydrophobic compounds in cows. Biodilution due to metabolism of certain compounds in cows was also observed. Strong biomagnification was observed in humans as indicated by 20-50 times higher fugacities in human milk compared to cows’ milk.
Introduction The bioaccumulation of hydrophobic organic chemicals in aquatic ecosystems has been the subject of intense research during the last 20 years. However, there has been remarkably little study of bioaccumulation in terrestrial ecosystems and, in particular, in agricultural food chains. Foods of agricultural origin, most especially animal fat, account for the majority of the exposure of most Europeans and North Americans to a range of persistent, toxic, environmental contaminants such as polychlorinated biphenyls (PCBs), dibenzo-p-dioxins, and dibenzofurans (PCDD/Fs) (1-5). Hence, bioaccumulation in agricultural food chains determines human risk, making this a particularly important aspect of the environmental chemistry of these compounds. The study of aquatic ecosystems has shown that one useful way of studying food chain bioaccumulation is through fugacity quotients (6, 7). Fugacity quotients offer the advantage of being able to use a single currency to compare levels of contamination in different organisms in a food chain. The approach is to divide the fugacity of the compound in a particular organism by the fugacity in the water that it lives in. While the fugacity quotient cannot exceed 1 if only bioconcentration occurs, biomagnification through food ingestion can result in the fugacity of an * Telephone: 49-921-552254; fax: 49-921-552334.
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organism being much higher than the fugacity of the water. For instance, fugacity quotients of 100 have been reported for PCBs in fish-eating birds (7). In this paper, the fugacity quotient concept is used to examine bioaccumulation in agricultural food chains. Field data collected in northeastern Bavaria are used to calculate the fugacities of a range of hydrophobic organic chemicals in different food chain compartments. The resulting fugacity quotients are discussed in terms of chemical behavior in agricultural environments. For the terrestrial environment, bioconcentration is defined as bioaccumulation leading to equal fugacities in two media, while biomagnification refers to bioaccumulation resulting in an increase in fugacity. The term biodilution is introduced to describe bioaccumulation phenomena yielding a decrease in fugacity. Note that bioconcentration is not defined as uptake from the surrounding ambient phase (air).
Structure of Agricultural Food Chains Agricultural food chains tend to be less complicated than many wildlife food chains. The atmosphere is the source of most environmental chemicals entering the ecosystem. Chemicals in the gaseous phase can partition onto particulate matter in the air. The chemicals are deposited through either dry gaseous, dry particle-bound, or wet deposition to soil and plants, the first trophic level in the food chain. The plants are harvested with a certain amount of soil contamination and are either directly consumed by humans or fed to livestock. In some cases, the livestock consume the plants directly. The livestock then serve as food for humans, in both the form of meat and the form of eggs and dairy products. This paper will focus on the air/soil-plant-cow-milkhuman food chain. It is the most important food chain for human exposure to PCBs and PCDD/Fs (1, 2, 4, 5), and the principles of chemical behavior observed here can be applied to other agricultural food chains.
Definition of Fugacity Quotients In order to calculate the fugacity quotients, it is first necessary to obtain the fugacities. The fugacity f (Pa) of a compound in a particular phase can be calculated from the concentration C (g m-3) using the equation (8)
f ) C/ZM
(1)
where M is the molecular mass (g mol-1) and Z is the fugacity capacity of the phase for the compound (mol m-3 Pa-1). Hence, if the fugacity capacities are known, then the fugacities can be calculated from measured concentrations (the concentration must be on a volume basis). Terrestrial ecosystems are immersed in the medium air and hence the airsnot the watersfugacity is the appropriate reference for examining bioaccumulation in terrestrial food chains. The fugacity capacity of air is by definition (8)
ZA ) 1/RT
(2)
R being the gas constant and T being the absolute temperature. There is relatively little experimental data on the fugacity capacities of plants. It has been suggested that one could
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1995 American Chemical Society
TABLE 1
Abbreviations and Physical-Chemical Properties of the Chemicals chemical
abbrev
H (Pa m3 mol-1) at 25 °C
log KOW at 25 °C
log KOA (calcd)e at 25 °C
hexachlorobenzene 2,4,4′-Cl3biphenyl 2,2′,5,5′-Cl4biphenyl 2,2′,4,5,5′-Cl5biphenyl 2,2′,4,4′,5-Cl5biphenyl 2,2′,4,4′,5,5′-Cl6biphenyl 2,2′,3,4,4′,5′-Cl6biphenyl 2,2′,3,4,4′,5,5′-Cl7biphenyl 2,2′,3,3′,4,4′,5,5′-Cl8biphenyl 2,3,7,8-Cl4DD 1,2,3,7,8-Cl5DD 1,2,3,4,7,8-Cl6DD 1,2,3,6,7,8-Cl6DD 1,2,3,7,8,9-Cl6DD 1,2,3,4,6,7,8-Cl7DD Cl8DD 2,3,7,8-Cl4DF 1,2,3,7,8-Cl5DF 2,3,4,7,8-Cl5DF 1,2,3,4,7,8-Cl6DF 1,2,3,6,7,8-Cl6DF 1,2,3,7,8,9-Cl6DF 2,3,4,6,7,8-Cl6DF 1,2,3,4,6,7,8-Cl7DF 1,2,3,4,7,8,9-Cl7DF Cl8DF
HCB 3B 4B 5B1 5B2 6B1 6B2 7B 8B 4D 5D 6D1 6D2 6D3 7D 8D 4F 5F1 5F2 6F1 6F2 6F3 6F4 7F1 7F2 8F
131a 28.9b 32.3b 24.9b 25.3b 16.7b 13.2b 10.9b 6.8b 3.337c 0.266c 1.084c 1.084c 1.084c 1.273c 0.684c 1.461c 0.505c 0.505c 1.454c 0.741c 0.741c 0.741c 1.425c 1.425c 0.191c
5.5a 5.67d 5.84d 6.38d 6.39d 6.92d 6.83d 7.36d 7.80d 6.8c 7.4c 7.8c 7.8c 7.8c 8.0c 8.2c 6.1c 6.5c 6.5c 7.0c 7.0c 7.0c 7.0c 7.4c 7.4c 8.0c
6.78 7.60 7.73 8.38 8.38 9.09 9.10 9.72 10.36 9.67 11.37 11.16 11.16 11.16 11.29 11.76 9.33 10.19 10.19 10.23 10.52 10.52 10.52 10.64 10.64 12.11
a From ref 14. b From ref 15. c From ref 16, where values for just one structural isomer were available the same values were assigned to the other isomers. d From ref 17. e To calculate KOA, H was converted to a dimensionless air/water partitioning coefficient by dividing by RT.
model the fugacity capacities of plants for hydrophobic compounds by viewing the plant as a certain volume of lipid (9-11), much as fish are treated in aquatic systems. Riederer proposed that one could estimate the Z value of a plant by calculating the total lipid and cutin content and modeling this as octanol (10). This is described by
ZP ) vLKOAZA
(3)
where vL is the volume fraction of the lipids and cutin in the fresh plant material and KOA is the octanol/air partition coefficient, which can be calculated as the quotient of the octanol/water and air/water partition coefficients. In a recent study, Z values were measured for rye grass, an important pasture grass in Germany, and it was found that eq 3 satisfactorily predicted the experimental data based on the estimated vL of 0.01 and applying KOA values measured at 25 °C to air/plant partitioning data obtained at 18 °C (12). The fugacity capacity of soils is commonly modeled using the equation (8)
ZS ) fOCpSKOCZW
(4)
where fOC is the fraction of organic carbon in the soil, pS is the soil density (in g mL-1):
ZW ) 1/H
(5)
and KOC, the organic carbon/water partition coefficient, is defined according to Karickhoff (13):
KOC ) 0.41KOW
(6)
Since this model was derived for solutions of soils in water,
there are some doubts as to whether it is valid for dry soils. However, it should provide a rough estimate of soil fugacity capacity. Animals and humans can be treated in the same manner as fish in aquatic ecosystems. The fat in the tissue is modeled as octanol, and for hydrophobic compounds, the capacity of other tissue components can generally be neglected. The equation is
ZF ) ZO ) vFKOAZA
(7)
Since tissue concentrations are generally given on a fat basis and not a whole body basis, it is usually not necessary to calculate the volume fraction of fat vF.
Chemical Concentrations in the Agricultural Food Chain The concentration data employed in this study were collected primarily around Bayreuth, a city of 70 000 located in a rural region in northeastern Bavaria. Data from just one area were used as far as possible to help assure the comparability of the levels in different matrices. The air and soil concentrations of the chemicals studied are among the lowest found in the literature, and hence we consider the Bayreuth area to represent a terrestrial environment with low-level contamination. Data were available for hexachlorobenzene (HCB), PCBs, and PCDD/Fs. The compounds included in the data set are listed in Table 1 along with their abbreviations and the physical-chemical properties used to calculate the fugacity capacities. The environmental concentrations are summarized in Table 2. The air data were obtained from a study in 1989 in which the gaseous and particle-bound fractions were continuously collected during the second half of the growing season using
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TABLE 2
Chemical Concentrations in the Agricultural Food Chain chemical
gaseousa (pg/m3)
particlea (pg/m3)
soilb (pg/g dw)e
HCB 2,4,4′-Cl3biphenyl 2,2′,5,5′-Cl4biphenyl 2,2′,4,5,5′-Cl5biphenyl 2,2′,4,4′,5-Cl5biphenyl 2,2′,4,4′,5,5′-Cl6biphenyl 2,2′,3,4,4′,5′-Cl6biphenyl 2,2′,3,4,4′,5,5′-Cl7biphenyl 2,2′,3,3′,4,4′,5,5′-Cl8biphenyl 2,3,7,8-Cl4DD 1,2,3,7,8-Cl5DD 1,2,3,4,7,8-Cl6DD 1,2,3,6,7,8-Cl6DD 1,2,3,7,8,9-Cl6DD 1,2,3,4,6,7,8-Cl7DD Cl8DD 2,3,7,8-Cl4DF 1,2,3,7,8-Cl5DF 2,3,4,7,8-Cl5DF 1,2,3,4,7,8-Cl6DF 1,2,3,6,7,8-Cl6DF 1,2,3,7,8,9-Cl6DF 2,3,4,6,7,8-Cl6DF 1,2,3,4,6,7,8-Cl7DF 1,2,3,4,7,8,9-Cl7DF Cl8DF
460 15 27 29 4.1 20 14 4.2 0.13 0.0027 0.0017 0.0016 0.0020 0.0011
