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Chapter 1. Effects of Fumigants on Nin-Target Organism in Soils

Chapter 1. Effects of Fumigants on Nin-Target Organism in Soils

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A. M. IBEKWE

the development of healthy soils. In the southwestern United States,

fumigation is used to control pathogens such as Verticillium dahliae,

Pythium, Rhizoctonia, or Cylindrocarpon spp. In addition to pathogen

control, fumigation can also result in enhanced growth response of the

plant by reducing weed pressure. The continued use of fumigants in

agriculture will require more investigations of the different types of

fumigants, soils, environmental conditions, and biological/microbial

communities to establish both the effectiveness on target organisms and

safety to the general public.

q 2004 Elsevier Inc.



I. INTRODUCTION

Agricultural soils are typically treated with pesticides to provide effective

control of nematodes, soil-borne pathogens, and weeds in preparation for

planting high value cash crops. Fumigants are a class of pesticide with broad

biocidal activity and affect many non-target soil organisms (Parr, 1974;

Domsch et al., 1983; Anderson, 1993). Currently, only four registered

fumigants are available in the Unites States: 1,3-dichloropropene (1,3-D),

methyl isothiocyanate (MITC), chloropicrin (CP), and methyl bromide

(MeBr). Methyl iodide (MeI, iodomethane) is another fumigant yet to be

registered that is considered being a promising alternative to MeBr for soilborne pest control in high value cash crops. While most fumigants are known

to have broad biocidal activity, their effects on non-target soil microbial

communities are largely unknown, due to the lack of appropriate methods to

describe microbial soil community composition. Soil microorganisms play

one of the most critical roles in sustaining the health of natural and

agricultural soil systems. They are a significant component of nutrient

cycling, especially of C and N, which are essential for proper plant

nutrition and agricultural productivity. Changes in the microbial

community composition as a result of fumigant applications may lead to

changes in the functional diversity of that community and ultimately, the

overall soil quality.

Because of the strong relationships between microbial diversity and

ecosystem function, soil microorganisms are recognized as sensitive indicators

of soil health. MeBr has the ability to destroy stratospheric ozone (Yung et al.,

1980; Prather et al., 1984) and a ban on its production and importation is to be

completed by 2005 in the United States (USEPA, 1995). 1,3-D, MITC, and CP

have been proposed as the most likely chemical alternatives to MeBr. Since little

ecotoxicological information exists with respect to these (and many other



FUMIGANTS ON NON-TARGET ORGANISMS IN SOILS



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fumigants), it is essential that fumigant effects on non-target microorganisms be

examined.



II. MODE OF ACTION

Fumigants are extensively used to grow strawberries, tomatoes, and other

high valued cash crops in California and Florida. Many studies have

documented the chemistry and air pollution potential of these fumigants in

the environment (Baker et al., 1996; Gan et al., 1998a,b). There are only

four registered chemical fumigants available in the United States: The first is

1,3-D, which is marketed under the trade name Telone and contains an equal

ratio of cis-1,3-D and trans-1,3-D. The second, MITC, is a primary product

of metam sodium (sodium methyldithiocarbamate) metabolism. CP, a third

fumigant also known as trichloronitromethane, is often formulated with

Telone and metam sodium. MeBr is the last fumigant available in the United

States. 1,3-D, MITC, and CP have been proposed as the most likely chemical

alternatives to MeBr. Figure 1 shows the structural formula of metam

sodium, MITC, cis- and trans-1,3-D, CP, and MeBr.

Compared to other pesticides, fumigants were found to have little or no

detectable effects on soil microorganisms at field application rates (Hicks et al.,

1990; Anderson, 1993). Their effects on non-target soil microorganisms at the

field application rate are largely unknown until recently, mainly due to lack of

appropriate methodology to describe the non-target population (Elliot et al.,

1996; Macalady et al., 1998; Ibekwe et al., 2001a; Dungan et al., 2003a).

Fumigants should only be toxic to the target organisms, be biodegradable, and

should not leach into the groundwater, though this is not always the case.

The widespread use of fumigants in the warm climate regions of the United

States is of increasing concern. The mode of action of different classes of

pesticides differs. Some pesticides are designed to affect specific or general

processes in the target organisms and are more suitable for a specific target

population. Fumigants are generally designed to provide effective control of

nematodes and soil-borne pathogens, such as fungi and weeds. Metam

sodium and 1,3-D may be very effective as fungicides, and thus may be

expected to affect non-targeting soil flora. The most used fungicide in

Denmark is fenpropimorph, which specifically inhibits two enzymes

involved in ergosterol biosynthesis (Johnsen et al., 2001). This fungicide

was designed to target leaf-associated fungi and subsequently may have some

effects on the soil fungi. Degradation of fenpropimorph also produces an

intermediate metabolite, fenpropimorphic acid, and it has been shown that

saprotrophic fungi were substantially affected by this intermediate



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A. M. IBEKWE



Figure 1 The chemical structure of cis- and trans-1,3-dichloropropene (1,3-D), metam sodium,

methyl isothiocyanate (MITC), chloropicrin (CP), and methyl bromide (MeBr).



compound, indicating that the biological activity of the fungicide may be

attributed to both mother compound and the more mobile metabolites

(Bjørnlund et al., 2000).

Changes in the microbial composition as a result of fumigant application may

lead to changes that interfere with the functional diversity and overall soil quality.

The strong relationships between microbial diversity, ecosystem sustainability,

and function are being increasingly recognized as sensitive indicators of soil

health (Turco et al., 1994). Ultimately, the linking of information between

microbial community structure/diversity and crop production will be an

important step in being able to predict soil fertility. There is a significant gap

in information on the effects of fumigants on soil bacterial and their impact on

major soil processes, such as organic matter transformation and pollutant

degradation. This review will elaborate on the most up-to-date data available in

the literature on this topic and describe some of the techniques in microbial

ecology that may be helpful in understanding different processes in soil that are

significantly affected by fumigants.



FUMIGANTS ON NON-TARGET ORGANISMS IN SOILS



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III. EFFECTS ON BIOLOGICAL PROCESSES

A. ENZYME ACTIVITIES

The effect of fumigants on enzyme activities was previously reported by Ladd

et al. (1976) and has been shown to have an inhibitory effect on dehydrogenase

activities (DHAs) (Anderson, 1978; Smith and Pugh, 1979; Tu, 1992).

Fumigation of a field soil with MeBr and CP, either individually or in

combination, decreased soil enzyme activities (Ladd et al., 1976). DHA is an

indicator for potential non-specific intracellular enzyme activity of the total

microbial biomass. Fumigants appear to disturb the membrane-bound processes

of active cells. As noted by Ladd (1978), DHA measurements may be influenced

not only by enzyme concentrations, but also by the nature and concentration of

added C substrates, and of alternative electron acceptors, such as NO2

3 . Zelles

et al. (1997) conducted an extensive study with seven enzymes to determine the

effects of chloroform fumigation on their activities and found that enzymes

bound to the active microorganisms were nearly inhibited completely

(dehydrogenase) or strongly reduced (arginine deaminase). These authors also

reported that fumigation of soil did not change the activities of xylase,

b-glucosidase and saccharase and only induced a low reduction in phosphatase

activity. Recently, Dungan et al. (2003a) showed that the incorporation of

compost manure to agricultural soils significantly increased the DHA of the soil

over a 12-week incubation period when compared to unamended soils. When

these soils were treated with two fumigants, propargyl bromide (PBr) and 1,3-D,

they observed a higher rate of fumigant degradation in the amended soils,

corresponding well with the increased enzyme activity in the amended soil

treatments. When treated with PBr at 10 mg kg21 or 1,3-D at 10 and

100 mg kg21, the DHA in unamended and amended soils was not significantly

reduced. At 100 mg kg21, PBr was more toxic than 1,3-D, as indicated by the

reduced DHA at this concentration. At 500 mg kg21 of PBr and 1,3-D, DHA was

significantly repressed, but by week 8 in the amended soil treatments, DHA had

recovered to levels similar to that of the control. DHA in unamended soils spiked

with 500 mg kg21 of 1,3-D or PBr did not demonstrate significant recovery after

12 weeks. This confirmed the inhibitory effects of fumigants on DHA as

previously reported (Anderson, 1978; Smith and Pugh, 1979; Tu, 1992).

Decreases in DHA, in both unamended and amended soils, were probably a direct

result of the adverse effects of PBr and 1,3-D on soil microbial populations.

Fumigants such as metam sodium may interfere with respiratory enzymes such as

pyruvate dehydrogenase due to their chelating effects on metal cations such as Cu

(Corbett et al., 1984) or to toxic degradation products such as MITC (Staub et al.,

1995). These authors showed that MITC is metabolized to S-methyl metam,

probably by formation of S-(N-methylthiocarbamoyl)cysteine, by cysteine



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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.



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