Bioavailability of heavy metals from sewage sludge and some long-term effects on soil microbes in agricultural ecosystems

Metals may affect the growth of plants and soil microbial activity, and soil fertility in the long term. Less is known of their adverse long-term effects on soil micro-organisms than on crop yields and metal uptake. This is not surprising, since their effects when added to soils in sewage sludge are difficult to assess, and few long-term experiments exist. This paper reviews evidence from long-term field experiments with sewage sludges in the United Kingdom, Sweden, Germany, and the United States. Changes in the extractability and uptake by crops of sludge metals in the Woburn experiment (UK), started in 1942, were measured to assess whether Zn and Cd are fixed by the sludge/soil constituents or are released as the sludge organic matter decomposes. Extractability of Zn by 0.1 M CaCl2 as a proportion of the total ranged from 0.5 to 3% and that of Cd from 4 to 18%, and were higher in sludge-amended than in farmyard-manure- or fertilizer-amended soils. Over a 33-year period after 1961, when sludge was last applied, the extractability of both metals fluctuated, but neither decreased nor increased consistently. The relationships between soil- and crop-metal concentrations were linear, with no evidence of a plateau across the concentrations achieved. The slopes of the soil-plant relationships depended on the type of crop or crop part examined, but was generally in the order red beet > sugar beet > carrot > barley. However, there were large seasonal differences in metal concentrations in the crops. It is concluded that up to 33 years after sludge applications ceased, Zn and Cd extractability and bioavailability do not decrease. Adverse effects on microbial activity and populations of cyanobacteria, Rhizobium leguminosarum bv. trifolii, mycorrhiza, and the total microbial biomass have been detected, in some cases below the European Community's maximum allowable concentration limits for metals in sludge-treated soils. For example, N2-fixation by free-living heterotrophic bacteria was found to be inhibited at metal concentrations (mg kg-1) of 127 Zn, 37 Cu, 21 Ni, 3.4 Cd, 52 Cr, and 71 Pb. Fixation by free-living cyanobacteria was reduced by 50% at metal concentrations (mg kg-1) of 114 Zn, 33 Cu, 17 Ni, 2.9 Cd, 80 Cr, and 40 Pb. Numbers of R. leguminosarum bv. trifolii decreased by several orders of magnitude at metal concentrations (mg kg-1) of 130 to 200 Zn, 27 to 48 Cu, 11 to 15 Ni, and 0.8 to 1.0 Cd. Important factors influencing the severity of toxicity were soil texture and pH. Higher pH, clay and organic-C contents reduced metal toxicity considerably. The evidence presented in this review of long-term field experiments suggests that adverse effects on microbial parameters were generally found at modest concentrations of metals in soils. It is concluded that prevention of adverse effects on soil microbial processes, and ultimately soil fertility, should be a factor that influences soil-protection legislation. (author)