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III. Effects on Biological Processes

III. Effects on Biological Processes

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6



A. M. IBEKWE



conjugated b-lyase. The alternative proposal was that metam sodium might be

very sensitive to oxidation, forming reactive sulfenic and sulfinic acids, which

might contribute to its toxic action. Assessing the toxicity of metam, its oxidative

and methylated metabolites, and their contribution to the toxicity of MITC on

non-target soil bacteria are complicated by their interconnected detoxification

and bioactivation pathways.



B. SUBSTRATE-INDUCED RESPIRATION

Substrate-induced respiration (SIR) is mainly used to characterize microbial

activity and has been used to estimate the size of the microbial biomass

(Anderson and Domsch, 1978). The wide use of SIR to assess the impact of

pesticides on microbial activity and biomass has been reported in the literature

(Wardle and Parkinson, 1990; Harden et al., 1993; Hart and Brookes, 1996; Lin

and Brookes, 1999; Smith et al., 2000; Chen et al., 2001). Results on the

effects of two fumigants from a 24-h SIR experiment, evaluated as CO2 evolved

(mg g21 dry soil 24 h21), were recently reported (Dungan et al., 2003a). SIR was

markedly inhibited by incremental additions of PBr or 1,3-D to either unamended

or manure-amended soil. Other studies show both enhancement and reduction of

CO2 evolution following pesticide application, while others exhibit no effect on

soil respiratory activity (Simon-Sylvestre and Fournier, 1979). In unamended

soil, at the highest concentration of PBr and 1,3-D, SIR was reduced to 61 and

22% of the control, respectively. In amended soil, SIR was reduced to 50 and

25% of the control, respectively; however, SIR was 1.4 (PBr) and 2.2 (1,3-D)

times higher, on average, than in fumigated unamended soil (Dungan et al.,

2003a). This study demonstrated a significant reduction of the impact of fumigant

on non-target soil bacteria with soil amendments. A study by Chen et al. (2001)

has shown that SIR was unaffected over a 56-day experimental period when

treated with benomyl (a fungicide) at a rate of 125 mg kg21. This showed that

soil microbial activity was stimulated by the addition of amendments, even when

treated with PBr (at 10 and 100 mg kg21) or 1,3-D (at 10 –500 mg kg21). The

effect of metam sodium has also been shown to strongly affect SIR (Macalady

et al., 1998). Soil treated with 1.6 g l21 of metam sodium was reduced to

17 – 29% of the controls with no recovery after 28 days. Also, metam sodium

applied at 16 g l21 eliminated respiration of added glucose for all sampling dates.

The authors concluded that metam sodium had inhibitory effects on soil

parameters measured even after 18 weeks. Sensitivity of soil respiration after

repeated exposure to MITC (Taylor et al., 1996) suggested that fumigation with

metam sodium resulted in long-term changes in the composition and activity of

soil microorganisms.



FUMIGANTS ON NON-TARGET ORGANISMS IN SOILS



7



C. NITROGEN TRANSFORMATION

The work of Rovira (1976) with CP and MeBr showed an increase in

concentration of NHỵ

4 within 28 days after fumigation, followed by a decrease

after 46 days due to increase in activities of nitrifying bacteria. NO3

concentrations in fumigated soil were lower than the untreated soils after 28

days because of a lack of nitrification following fumigation. Malkomes (1995)

also reported that nitrification was inhibited by fumigation for long periods of

time. Metam sodium produced some inhibitory effects on nitrogen transformation

as a result of depression of ammonia-oxidizing activities (Macalady et al., 1998).

These authors showed a decrease in ammonia oxidation potential with increasing

metam sodium dose. In a recent study, the effects of steam sterilization (SS) on

soil microbial properties, including metabolic diversity of the microbial

communities, were examined in a greenhouse study compared to MeBr (Tanaka

et al., 2003). The numbers of nitrifiers, both ammonium-oxidizing bacteria and

nitrite-oxidizing bacteria, were severely affected by the SS and CP treatments,

resulting in their virtual disappearance. The decrease in the levels of microbial

biomass C and N after the treatments suggested that the SS and CP treatments

eradicated the microorganisms more effectively than the MeBr treatment, and

that the influence of the former persisted until the end of the experiment,

4 months after the treatments. Accumulation of NH4-N was observed after the

SS and CP treatments mainly due to the partial decomposition of the dead

microorganisms and the marked decrease in the number of ammonium-oxidizing

bacteria. The numbers of ammonia-oxidizing bacteria were also reduced by more

than four orders of magnitude in soils fumigated with metal sodium and did not

show recovery 105 days later (Toyota et al., 1999). Fumigation decreased the

numbers of nitrite oxidizers by three orders of magnitude, with a slight recovery

after 105 days (still significantly lower than the control). These studies have

shown that several fumigants adversely affect soil N balances through their

temporary inhibition of nitrification.

The process of nitrification involves the conversion of ammonium to nitrite

and to nitrate. The inhibition of this process through the adverse effects of

fumigants on ammonia-oxidizing bacteria may result in some adverse effects on

the overall soil quality. It should also be noted that once the fumigants are

completely dissipated in soil, there is always a regrowth of the bacteria. It has

been shown previously that autotrophic nitrifying bacterium Nitrosomonas

europaea is capable of co-oxidizing numerous halogenated hydrocarbons in the

presence of NHỵ

4 through the action of the ammonia-oxidizing enzyme ammonia

monooxygenase (AMO) (Rasche et al., 1990). As alternative substrates for this

enzyme, these compounds inhibit ammonia oxidation through competitive

effects. At lower concentrations these compounds may serve as an alternative

substrate for AMO, or with higher concentrations bacterial population may

decrease, resulting in less nitrification.



8



A. M. IBEKWE



IV.



EFFECT ON MICROBIAL ACTIVITIES

AND COMPOSITION



A. CHANGES IN COMMUNITY-LEVEL CARBON SOURCE

UTILIZATION BY BIOLOG

The Biolog Gram-negative (GN) microtiter plate assay is often used to analyze

the functional diversity through substrate utilization patterns of soil microorganisms. When the functional abilities of the heterotrophic soil microbial

communities were observed over a 12-week period of time following the

application of fumigants, severe alterations were seen during the first week,

especially with MeBr (Ibekwe et al., 2001a). The PCA plot (Fig. 2) from MeBr,

MITC, 1,3-D, and CP-treated soil microbial communities and the control

accounted for 28% of the variance on the first component, with six PCs

accounting for over 80% of the variation. The control and the 1,3-D-treated soils

separated along PC1 with their coefficients positively correlating to the right of

PC1. Analysis of MeBr communities did not show any pattern of groupings

except that communities from the first week of treatments were positively

correlated along PC2 and grouped with MITC after weeks 8 and 12. Pairwise

comparison showed that the MeBr communities differed significantly ðp , 0:05Þ

from the control and 1,3-D communities. The control and 1,3-D treatments were



Figure 2 Principal component analysis performed on Biolog GN fingerprints of soil extracts

treated with methyl bromide (MeBr), methyl isothiocyanate (MITC), 1,3-dichloropropene (1,3-D),

chloropicrin (CP), and non-fumigated soil (C). 1, 8, and 12 after the symbols indicate weeks 1, 8, and

12 and 1, 2, and 3 after the “-” sign indicates 50% below field application rate, field application, and

1000% above field application rates, respectively.



FUMIGANTS ON NON-TARGET ORGANISMS IN SOILS



9



similar when compared to the other three fumigants, suggesting a lesser effect of

1,3-D on heterotrophic. In another study, effects of SS on soil microbial

properties, including metabolic diversity of the microbial communities, were

examined in a greenhouse study and were compared to MeBr (Tanaka et al.,

2003). The authors found that the richness and average well color development

(AWCD) values in the microbial communities decreased markedly immediately

after treatment with MeBr but showed a rapid recovery, while those treated

with CP continued to decrease until the transplanting of tomato seedlings.

This was in agreement with Ibekwe et al. (2001a) who showed a sharp decrease in

microbial diversity with MeBr, followed by a quick recovery of the community

after 8 weeks when compared to a more sustained effect for a longer period with

CP. The shifts in microbial communities observed in the Biolog assays were due

to the toxic effects of fumigants on rapid growing microorganisms of high

population in the soils. Analysis of microbial communities from the Biolog GN

assay by DGGE confirmed that carbon source utilization profiles obtained with

Biolog GN plates do not necessarily discriminate the numerically dominant

members of the microbial community used as the inoculum (Engelen et al., 1998;

Smalla et al., 1998).

Under field conditions, natural fluctuations in carbon substrate utilizing

activity and community-level physiological profiles of microorganisms in low

input and conventional rice paddy soils were monitored using Biolog GN plates

for 2 years. The purpose was to establish criteria for assessing side effects of

pesticides on soil microbial ecosystems (Itoh et al., 2002). The activity changed

seasonally showing a regular pattern with more activity observed during late

summer. The level of microbial activities seemed to be directly influenced by soil

temperature and/or redox potential. Soil microbial communities grouped into

three clusters, August – December, January – April, and May – August, based on

the sampling season. Many studies have shown the effects of fumigants on

microbial activities and community structure. The effect of metam sodium

fumigation on community structure after a 5- and 18-week incubation showed

a separation of the two communities along the first principal component (PCA)

based on treatment dose (Macalady et al., 1998). There was a signicant

p ẳ 0:001ị dose treatment effect at week 5, whereas at week 18 there was no

dose significant effect p ẳ 0:05ị; but there was a binary variable effect

p ẳ 0:001ị between the treated and untreated samples. Toyota et al. (1999)

compared the AWCD values and richness (number of positive wells) of different

categories of the 95 substrates 105 days after fumigation with metam sodium.

They found that both AWCD and richness in all the substrate groups were

significantly ð p ¼ 0:05Þ lower in the fumigated soils than in the control soils. In

the radish rhizosphere and non-rhizosphere soils fumigated with CP, there was a

significant suppression in AWCD and richness in fumigated soils compared to the

control (Itoh et al., 2002). It was assumed that the bacterial populations with a

high substrate assimilation activity were damaged by CP fumigation and a



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