Author's personal copy

ARTICLE IN PRESS

Crop Protection 26 (2007) 17331746 www.elsevier.com/locate/cropro

Review

Accelerated biodegradation of pesticides: An overview of the phenomenon, its basis and possible solutions; and a discussion on the tropical dimension
Ziv Arbeli, Cilia L. Fuentes
, , Facultad Agronoma, Universidad Nacional de Colombia, Sede Bogota Colombia. A.A. 14490; Bogota DC, Colombia Received 16 February 2007; accepted 16 March 2007

Abstract Accelerated microbial degradation is the name commonly given to the phenomenon associated with a signicant increase in the rate of degradation of a pesticide in soil following a previous application of the same pesticide and also to the closely related phenomenon involving an unexpectedly rapid degradation of a pesticide following a previous application of another pesticide, usually of similar chemical structure. It apparently is caused by an adaptation of one or more species of microorganism present to metabolize the pesticide. In the late 1940s it was recognized that repeated applications of 2,4-D accelerated its degradation. Studies done in the 1970s and 1980s revealed that many pesticides in use were susceptible to the phenomenon and that it was reducing the efcacy of a number of commercial products especially those for which applications at seeding time were expected to provide prolonged pest control. Further work since that time has shown the dynamic nature of the phenomenon as a number of pesticides which were previously shown to be unaffected are now susceptible. The phenomenon can result in signicantly reduced crop yields and coping with it usually involves additional costs. In the following manuscript we give an overview of this phenomenon, its basis and possible solutions; and attempt to predict how should biogeography factors and tropical conditions inuence the phenomena. r 2007 Elsevier Ltd. All rights reserved.
Keywords: Enhanced degradation; Pesticides; Crop protection; Bacterial biogeography; Tropic

Contents 1. 2. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The phenomenon. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Duration of the accelerated degradation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Cross acclimation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Its basis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Evolution of bacterial degradation genes. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Possible solutions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A discussion on the tropical dimension . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Concluding remarks. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1734 1734 1735 1736 1738 1739 1740 1741 1742 1742 1742

3. 4. 5. 6.

Corresponding author. Tel.: +57 1 3165000x19114.

E-mail address: aziv@unal.edu.co (Z. Arbeli). 0261-2194/$ - see front matter r 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.cropro.2007.03.009

Author's personal copy

ARTICLE IN PRESS
1734 Z. Arbeli, C.L. Fuentes / Crop Protection 26 (2007) 17331746 Table 1 Herbicides known to undergo accelerated degradation Pesticide Loss of efcacy + Reference

1. Introduction Microbial degradation of pesticides applied to soil is the principle mechanism which prevents the accumulation of these chemicals in the environment. Yet, when pesticides are degraded too rapidly, pest control may be less effective. One factor that has been shown to increase the rate of microbial degradation of pesticides in soil is one or more previous applications of the same pesticide or another pesticide with a similar chemical structure. This phenomenon is known as accelerated or enhanced degradation (Racke, 1990) and can result in economic losses to farmers. For example, in the UK accelerated degradation of the insecticidal metabolites of phorate, especially phorate sulfone, made it necessary to increase insecticide use three-fold on carrots over the period 19761996 while crop output increased by only a little more than 10% (Suett et al., 1996a). Microbial adaptation to degrade pesticides was recognized soon after their introduction into markets with the pioneer research on the biodegradation of 2,4-D (Audus, 1949). At this time, however, research on pesticides degradation was mainly academic. Soon after, when the potential environmental risk of pesticides was realized, pesticide degradation research was more focused on their persistence. One of the consequences of these studies was the replacement of the recalcitrant pesticides (mainly chlorinated compounds) by new, degradable pesticides (mainly organophosphorus and carbamate compounds). Shortly after, it was reported that some of these pesticides (e.g. diazinon, EPTC and carbofuran) failed to provide adequate control against their target pests (Sethunathan, 1971; Williams et al., 1976; Felsot et al., 1981; Rahman and James, 1983). Detailed research has shown that repeated application of these pesticides, accelerated their degradation and they did not remain in the soil at concentrations that were sufcient to supply crop protection for the length of time required (Roeth et al., 1990; Felsot et al., 1981). The list of pesticides affected by accelerated degradation is long and is constantly growing. It includes herbicides, insecticides, nematicides, fungicides and fumigants (Tables 14). Some pesticides that appeared to be incapable of inducing accelerated degradation at the time previous reviews were published (e.g., atrazine, and chloropyrophos, Suett et al., 1996a) are now known to be degraded rapidly in previously treated soil (Barriuso and Houot, 1996; Robertson et al., 1998). The greatest potential risk for crop protection seems to be with fumigants (Di Primo et al., 2003), nematicides and insecticides (Suett et al., 1996a). Suett et al. (1996a) reported that 12 out of 13 insecticidesnematicides that were available in United Kingdom for soil application could undergo enhanced biodegradation. Now the single exception, which was chloropyrophos, is also susceptible to the phenomenon (Robertson et al., 1998; Singh et al., 2003a).

2,4,-D Alachlor Amitrole Atrazine Bentazon Butylate Carbetamide Chloramben Chlorotoluron Chlorsulfuron Dalapon Diclofopmethyl Diuron Endothall EPTC Isoproturon Isoxaben Linuron MCPA Monolinuron Napropamide Nitralin Pendimethaline Proyzamide Pyrazon Simazine Terbutryn Vernolate

+ +

Audus (1949, 1951); Gray and Joo (1985) Walker and Welch (1991) Riempa (1962) Barriuso and Houot (1996) Wagner et al. (1996) Harvey (1987) Hole et al. (2001) Wildung et al. (1968) Rouchaud et al. (2000) Ravelli et al. (1997) Leasure (1964); Gray and Joo (1985) Piutti et al. (2002) Rouchaud, et al. (2000) Horowitz (1966) Rahman and James (1983) Bending et al. (2001); El-Sebai et al. (2005) Rouchaud et al. (1997) Walker and Welch (1991) Audus (1951) Maier-Bode and Hartel (1981) Walker and Welch (1991) Savage (1973) Kulshrestha et al. (2000) Walker and Welch (1991); Rouchaud et al. (2000) Engvold and Jansen (1969) Albarran et al. (2004); Suett et al. (1996a) Avidov et al. (1985) Wilson (1984); Gray and Joo (1985)

+ +

? +

The discovery of accelerated microbial degradation of pesticides has led to extensive investigation and many reviews have been published (Kaufman et al., 1985; Roeth, 1986; Felsot, 1989; Racke and Coats, 1990a). In the last 10 years, however, publications about accelerated degradation are rather scarce. Do we know all about it? Has the problem been solved? Is it just out of fashion? In this review we have briey summarized the knowledge about accelerated degradation and prepared a list of (almost) all pesticides known to induce accelerated degradation and a list of important pesticides that are susceptible to accelerated degradation induced by other pesticides (cross acclimation). 2. The phenomenon Accelerated degradation sensu stricto can be used to denote all cases in which repeated application of a pesticide results in an increase in the degradation rate of this pesticide. Yet, because of its economic implications, cases in which a signicant loss of efcacy was observed have received major attention. In general, microorganisms are considered as the principal agents of xenobiotic degradation. Since soil harbors high numbers of diverse microbe

Author's personal copy

ARTICLE IN PRESS
Z. Arbeli, C.L. Fuentes / Crop Protection 26 (2007) 17331746 Table 2 Insecticides and nematicides known to undergo accelerated degradation Pesticide Loss of efcacy + + + + + + Reference 1735

Aldicarb Bendiocarb Benfuracarb Cadusafos Carbaryl Carbofuran Carbosulfan Chlorfenvinphos Chlorpropham Chlorpyrifos Cloethocarb Diazinon Ethoprophos Fenamiphos Fensulfothion Fonofos Furathiocarb Isazofos Isofenphos Malathion Mephosfolan Methylparathion Oxamyl Parathion Phorate Terbufos Trimethacarb

+ + + + + + + + +

+ + + +

Smelt et al. (1987) Racke and Coats (1990b) Suett (1987) Karpouzas et al. (2004b) Rodriguez and Dorough (1977) Felsot et al. (1981); Harris et al. (1984) Suett (1987) Suett et al. (1996a, b) Chapman and Harris (1990) Robertson et al. (1998); Singh et al. (2003a) Racke and Coats (1988b) Sethunathan (1971) Smelt et al. (1987) Ou (1991); Johnson (1998) Read (1983); Harris et al. (1988) Racke and Coats (1990b) Suett (1987) Somasundaram et al. (1993) Racke and Coats (1987) Matsumura and Boush (1966) Suett and Jukes (1990) Singh, et al. (1999) Smelt et al. (1987) Singh, et al. (1999) Suett and Jukes (1997) Chapman and Harris (1990); Pattison and Versteeg (2000) Felsot and Tollefson (1990)

Table 3 Fungicides known to undergo accelerated degradation Pesticide Benomyl Carbendazim Dicarboxamide Dicloran Difenoconazole Iprodion Pandorench Vinclozolin Loss of efcacy + + Reference Yarden et al. (1987) Roeth (1986) Walker and Welch (1990) Roeth (1986) Thom et al. (1997) Walker (1987) Spanis et al. (1962) Walker (1987)

when residual of pesticide is important in order to supply prolonged crop protection. Crops for which the commercially important part grows in the soil (e.g. potato, carrots, onion) are more likely to suffer should the phenomenon occur. Nevertheless, loss of pesticide efcacy due to accelerated degradation could adversely affect production of any crop, which requires root protection, protection from weeds or any pest which spends part of his life cycle in the soil. On the national level, economies that rely on few major crops are at higher risk, not only from the well-known risk of keeping all the eggs in one basket, but also from the risk of specialist pests and higher repetition in pesticide application. Corn, which is the main crop in a few states in the USA (the Corn Belt), is vulnerable to loss of protection against weeds (Roeth et al., 1990; Skipper, 1990) and rootworm (Racke and Coats, 1990b) as a result of accelerated degradation. In contrast, crops in Europe, which has a higher diversity of agriculture and uses more frequent crop rotation, are less vulnerable (Suett et al., 1996a). The effect of accelerated degradation of pesticides on pest control can be dramatic. The economic injury level caused by corn rootworm in carbofuran-treated plots increased from 6% during 19691974, just after commercial introduction, to 28% during 19761980 (Felsot, 1989). In a controlled experiment, EPTC could provide excellent weed control following the rst two annual applications, but following the third and subsequent applications corn yield was dramatically reduced, and was around 75% less than for the hand-weeded positive control (Harvey, 1991). Similarly, iprodione could reduce white rot infection by 9399% in the rst 2 years of use. In the third year reduction of white rot infection fell to 31%, while in the fourth and subsequent years, iprodione had completely lost its effectiveness and reduction of white rot infection was normally 0% (Walker and Welch, 1990). 2.1. Duration of the accelerated degradation The duration of accelerated degradation is the time required for the degradation rate of a pesticide in previously treated soils to be restored to that in previously untreated soil. Obviously, if this time is shorter than the time between two applications, accelerated degradation would not be a factor affecting pest control. Knowledge about the duration of the phenomenon is crucial for planning a pest management strategy. The limited data available on duration times indicates that they vary widely among pesticides, soils with different properties and climatic conditions. Anderson and Lafuerza (1992) found that, in tropical regions, fenamiphos degradation rates returned to levels found in previously untreated soils after 1216 months. Roeth (1986) concluded that in temperate zones, fully mature accelerated degradation of thiocarbamate herbicides might persist for 12 years after the last application and partially persist for another year. In

+ +

Table 4 Fumigant known to undergo accelerated degradation Pesticide 1,3-Dichloropropene Dazomet Metam-sodium Loss of Efcacy Reference Smelt et al. (1989) Di Primo et al. (2003) Di Primo et al. (2003)

+ +

species, soil applied pesticides are more likely to both induce and be adversely affected by accelerated degradation. The loss of pesticide efcacy might occur in cases

Author's personal copy

ARTICLE IN PRESS
1736 Z. Arbeli, C.L. Fuentes / Crop Protection 26 (2007) 17331746

contrast, accelerated degradation of the soil-applied pesticides carbofuran and aldicarb was found to persist for more than 5 years (Parekh et al., 1992; Suett et al., 1993). Similarly, the degradation of oxamyl and aldicarb was still accelerated 5 years after the last applications while the degradation rate of ethoprophos at this time had returned to that in previously untreated soil (Smelt et al., 1996). Observed duration times for carbamate insecticides are usually longer than for organophosphorus insecticides and thiocarbamate herbicides. Instances of extended duration of accelerated degradation have interesting implications for microbial population dynamics and turnover in soils. The mechanisms which allow survival of the agents of accelerated degradation for 5 years have not been studied. Theoretically, an extended duration could be attributed to spore formation or other dormant resistant forms; to low concentrations of pesticides that are desorbing slowly from soil and providing a continuous supply of substrate to the microorganisms involved; to other genes on the same plasmid that keep providing higher tness to the host microorganism(s), for example, the atrazine degradation genes of Pseudomonas sp. strain ADP, are located on a plasmid that also contains a functional mercury resistance operon (Martinez et al., 2001); or to the fact that the microorganism(s) involved are able to maintain a sufciently high population by metabolizing other substrates.

2.2. Cross acclimation Cross acclimation involves the accelerated degradation of a pesticide in a soil in which accelerated degradation has been induced by previous application(s) of another pesticide. Usually, cross acclimation is observed with pesticides from the same group of chemicals (Chapman and Harris, 1990; Singh et al., 2005). For example, soil in which accelerated degradation of carbofuran has been induced by previous treatment is known to accelerate the degradation of other carbamate pesticides such as bendiocarb, carbaryl, cloethocarb, isoprocarb and propoxur (Read, 1987; Racke and Coats, 1988b), while no change in degradation rate was observed for several organophosphorus insecticides (Racke and Coats, 1988a), thiocarbamate herbicides (Kaufman and Edwards, 1983) and dithiocarbamate herbicides (Harris et al., 1984). Cross acclimation can be explained by a broad specicity of the degrading enzyme. Microorganisms which posses a degradation gene for the initially applied pesticide would proliferate followed its application. If the enzyme involved can also degrade another pesticide, the effect of this cross acclimation would be observed following the application of the second pesticide. The accelerated degradation rate for the other pesticide would be expected to be slower, if the afnity of degradation enzyme for the originally applied pesticide

Table 5 Cross acclimation of organophosphorus pesticides Pestiside tested Cadusafos Cadusafos Coumaphos Coumaphos Chlorpyrifos Chlorpyrifos Chlorpyrifos Diazinon Diazinon Ethoprophos Ethoprophos Ethoprophos Ethoprophos Ethoprophos Fenamiphos Fenamiphos Fonofos Fonofos Fonofos Isazofos Isazofos Isofenphos Parathion Parathion Phorate Phorate Terbufos Terbufos Soil history Chlorpyrifos Fenamiphos Chlorpyrifos Fenamiphos Fenamiphos Fonofos Isofenphos Chlorpyrifos Fenamiphos Cadusafos Chlorpyrifos Fenamiphos Fonofos Isofenphos Cadusafos Chlorpyrifos Chlorpyrifos Fenamiphos Isofenphos Chlorpyrifos Fenamiphos Fonofos Chlorpyrifos Fenamiphos Fonofos Isofenphos Fonofos Isofenphos Results Negative Negative Positive Negative Negative Negative Negative Positive Negative Positive Negative Negative Negative Negative Negative Negative Negative Negative Negative Positive Negative Negative Positive Negative Negative Negative Negative Negative Reference Singh et al. (2005) Karpouzas et al. (2004a) Singh et al. (2005) Singh et al. (2005) Singh et al. (2005) Racke and Coats (1988a) Racke and Coats (1988a) Singh et al. (2005) Singh et al. (2005) Karpouzas et al. (2004b) Singh et al. (2005) Singh et al. (2005); Karpouzas et al. (2004a) Racke and Coats (1988a) Racke and Coats (1988a) Karpouzas et al. (2004b) Singh et al. (2005) Singh et al. (2005) Singh et al. (2005) Racke and Coats (1988a) Singh et al. (2005) Singh et al. (2005) Racke and Coats (1990b) Singh et al. (2005) Singh et al. (2005) Racke and Coats (1988a) Racke and Coats (1988a) Racke and Coats (1988a) Racke and Coats (1988a)

Author's personal copy

ARTICLE IN PRESS
Z. Arbeli, C.L. Fuentes / Crop Protection 26 (2007) 17331746 1737

were greater than for the second pesticide. If more than one enzyme is involved in the degradation of the initially applied pesticide but only one enzyme can participate in the metabolism of the second pesticide, degradation may be incomplete and partial degradation products may accumulate (Singh et al., 2005). Degradation of several pesticides from the same chemical group has been demonstrated in pure bacterial culture, as well as, by puried enzymes (Karns et al., 1986; Strong et al., 2002; Karpouzas et al., 2005; Shapir et al., 2005). Cases of cross acclimation within important pesticide groups (carbamate and organophosphate) are summarized in Tables 5 and 6. Generally, cross acclimation has been

observed more frequently among carbamate insecticides than among organophosphorus insecticides (Sethunathan and Pathak, 1972; Forrest et al., 1981; Racke and Coats, 1988a, b; Morel-Chevillet et al., 1996). Nevertheless, soil with a history of chloropyrifos application(s) was observed to accelerate the degradation of isazofos, parathion, coumaphos and diazinon, but not fenamiphos, cadusafos, fonofos and ethaprophos (Singh et al., 2005). The four pesticides for which degradation was accelerated have the same phosphate side chain (O,O-diethyl phosphorothioate) while the phosphate side chain of each of the unaffected pesticides is distinct (Singh et al., 2005). This suggests that the organophosphate hydrolase involved is specic

Table 6 Cross acclimation of carbamate pesticides Pesticide tested Aldicarb Aldicarb Aldicarb Bendiocarb Bendiocarb Benfuracarb Bufencarb Bufencarb Carbaryl Carbaryl Carbaryl Carbofuran Carbofuran Carbofuran Carbofuran Carbofuran Carbofuran Carbofuran Carbofuran Carbofuran Carbofuran Carbofuran Carbofuran Carbofuran Carbofuran Carbofuran Carbofuran Carbofuran Carbofuran Carbofuran Carbosulfan Chlorpropham Cloethocarb Cloethocarb Fenobucarb Furathiocarb Furathiocarb Isoprocarb Metolcarb Oxamyl Oxamyl Oxamyl Oxamyl Propoxur Trimethacarb Soil history Carbofuran Carbofuran Oxamyl Carbofuran Cloethocarb Carbofuran Carbofuran Carbofuran Carbofuran Carbofuran Cloethocarb Aldicarb Bendiocarb Benfuracarb Carbaryl Carbosulfan Cloethocarb Chlorpropham Dioxacarb Ethiofencarb Fenobucarb Formetanate Furathiocarb Isoprocarb Methiocarb Metolcarb Pirimicarb Promecarb Propoxur Trimethacarb Carbofuran Carbofuran Carbofuran Carbofuran Carbofuran Carbofuran Carbofuran Carbofuran Carbofuran Aldicarb Carbofuran Carbofuran Cloethocarb Carbofuran Carbofuran Results Negative Positive Positive Positive Positive Positive Negative Positive Negative Positive Positive Positive Positive Positive Positive Positive Positive Negative Positive Positive Positive Negative Positive Positive Positive Positive Negative Positive Positive Positive Positive Negative Negative Positive Positive Negative Positive Positive Positive Positive Negative Positive Positive Positive Positive Reference Read (1987) Chapman and Harris (1990) Smelt et al. (1987) Racke and Coats (1988b) Racke and Coats (1988b); Felsot (1986) Suett (1987) Felsot (1986) Chapman and Harris (1990) Racke and Coats (1988b) Chapman and Harris (1990) Racke and Coats (1988b) Chapman and Harris (1990) Morel-Chevillet et al. (1996) Morel-Chevillet et al. (1996) Morel-Chevillet et al. (1996) Morel-Chevillet et al. (1996) Racke and Coats (1988b) Chapman and Harris (1990) Morel-Chevillet et al. (1996) Morel-Chevillet et al. (1996) Morel-Chevillet et al. (1996) Morel-Chevillet et al. (1996) Morel-Chevillet et al. (1996) Morel-Chevillet et al. (1996) Morel-Chevillet et al. (1996) Morel-Chevillet et al. (1996) Morel-Chevillet et al. (1996) Morel-Chevillet et al. (1996) Morel-Chevillet et al. (1996) Dzantor and Felsot (1989) Suett (1987) Chapman and Harris (1990) Racke and Coats (1988b); Hamm and Thomas (1986) Read (1987); Chapman and Harris (1990) Morel-Chevillet et al. (1996) Chapman and Harris (1990) Suett (1987) Felsot (1986) Morel-Chevillet et al. (1996) Smelt et al. (1987) Read (1987) Chapman and Harris (1990) Chapman and Harris (1990) Read (1987); Chapman and Harris (1990) Felsot (1986); Chapman and Harris (1990)

Author's personal copy

ARTICLE IN PRESS
1738 Z. Arbeli, C.L. Fuentes / Crop Protection 26 (2007) 17331746

for this side chain. A review of biodegradation of organophosphorus compound has recently been published (Singh and Walker, 2006). Cross acclimation was also seen in other pesticide groups such as phenoxyacetic herbicides (Kirkland and Fryer, 1972) and thiocarbamate herbicides (Wilson, 1984; Skipper et al., 1986; Harvey et al., 1986; Tal et al., 1989a), dicarboximides fungicides (Walker and Welch, 1990; Mitchell and Cain, 1996), the isothiocyanates fumigants (Di Primo et al., 2003; Warton et al., 2003) and theoretically it can happens in any group of chemicals. Cross acclimation can limit the possibilities for effective pesticide rotation. Nevertheless for some pesticides, accelerated degradation after cross acclimation is signicantly slower than after self-adaptation which permits them to still be used effectively in rotations. For example, the accelerated degradation rates of EPTC and vernolate were similar following self-adaptation and cross acclimation, whereas the degradation rate of butylate in soils with a history of EPTC and vernolate treatment was increased but to a lesser extent (Wilson, 1984). This is in agreement with the observation that butylate gave acceptable weed control in elds with a history of EPTC treatment and in which EPTC had failed (Obrigawich et al., 1982; Rahman and James, 1983). 3. Its basis The lag phase before microbial growth is well known from the growth curve of pure cultures. This phase is usually explained by the time necessary for cells to synthesize the enzymes essential for growth when they are introduced into a new environment. Similar lag is frequently observed between the time a chemical enters an environment and the time microbial degradation is evident. This period of time has been termed acclimation or adaptation time (Alexander, 1999). It reects the time necessary to accumulate a sufciently high number of degrader microorganisms capable of utilizing a specic chemical as a nutrient or energy source. In the case of accelerated microbial degradation, it appears the high degrader population is maintained from one pesticide application to the following application so the acclimation time becomes shorter with each pesticide application until, in some cases, it is no longer observable. There are more factors which inuence adaptation time, as well as, the subsequent degradation kinetics in the natural soil environment which harbors a complex microbial community than in a pure culture grown under laboratory controlled conditions. As a result the acclimation time and occurrence of accelerated degradation in soil is less predictable. Acclimation times can vary from a few hours to many months (Alexander, 1999), and accelerated degradation can occur after a single application or after several decades (Avidov et al., 1988; Barriuso and Houot, 1996). Theoretically, microbial adaptation to degrade a specic chemical in soil may reect: (1) an increase in

degradation activity of a limited number of microorganisms initially present due to selective gene expression; (2) an increase in the number of degraders initially present due to microbial growth and/or lateral gene transfer; (3) the movement of other microorganisms capable of degradation to the site of application and (4) the evolution of the new enzymes necessary for use of the chemical as an energy source. It has been shown that bacteria are the dominant agents of accelerated degradation of pesticides while fungi have little or no role in the phenomenon (Tal et al., 1989b; Racke and Coats, 1990b). This is in agreement with the fact that in many cases fungal degradation is a co-metabolic reaction by non-specic lignolitic or cytochrome 450 enzymes (Fernando and Aust, 1994; Kullman and Matsumura, 1996; Yadav et al., 2003). In general, every environmental factor which inuences microbial growth (e.g. temperature, pH, availability of nutrients, electron acceptors, the present of competitors or predators) could inuence the acclimation time (e.g. Chapman and Harris, 1990). Similarly, environmental and biological factors that inuence the survival of the degrader population between one pesticide application and another affect the development of accelerated degradation. Many reports indicate that soil pH is the most important factor (e.g. Getzin, 1973; Suett et al., 1996b; Singh et al., 2003a, b; Warton and Matthiessen, 2005). Accelerated degradation also depends on the metabolic gene pool of the microbial community at or near the site of application. In the absence of efcient degradation genes for the specic pesticide, accelerated degradation will not develop unless new microbes possessing the required genes migrate to the site or the required new genes evolve in the microbes already present. The degradation rate and the extent of microbial growth during degradation is also inuenced by the structure of the pesticide. Usually, structurally simple pesticides with high water solubility and low adsorptivity that can easily support microbial growth will develop accelerated degradation more quickly, sometimes even after a single application. The structure of these pesticides is often similar to naturally occurring substances which are currently used as an energy source by the soil microorganisms and, as a result, they are easily degraded by most microbial communities immediately after their introduction to the environment. In contrast, pesticides with a structure that is different from most naturally occurring substances (i.e. xenobiotic compounds) are often degraded slowly since the microorganisms do not possess suitable degradation genes. In these cases, degradation by nonspecic enzymes may still occur at a slow rate. In many of these cases the microorganisms cannot gain nutrients or energy from degradation of the pesticide and thus the degrading population will not grow, and accelerated degradation will not occur (Robertson and Alexander, 1994). This type of reaction is called co-metabolism (Alexander, 1999). Degradation of natural compounds which are readily biodegradable can be signicantly slowed

Author's personal copy

ARTICLE IN PRESS
Z. Arbeli, C.L. Fuentes / Crop Protection 26 (2007) 17331746 1739

by the addition of one or more substituents. These substituents (e.g. Cl, NO2, SO3H, Br, CN, CF3) are known as xenophores (Alexander, 1999) since they are not common substituent in natural occurring organic matter. Additionally pesticides, which have low bioavailability (low solubility in water and/or high adsoptivity) are less susceptible to accelerated degradation as the degradation rate may be limited by the desorption or dissolution rate of the molecule and not by the metabolic rate of microorganisms (Alexander, 1999). 3.1. Evolution of bacterial degradation genes Short generation times and high genomic plasticity allow bacteria to evolve new genes at a relatively high rate. As a consequence, they can degrade nearly all known organic material (Johnson and Spain, 2003). Xenobiotic compounds are molecules that were synthesized by man and did not exist previously in the environment. As a result, bacteria did not have an opportunity to evolve enzymes capable of degrading these compounds. Indeed, the degradation rates of these compounds are often slow and predominantly by nonspecic reactions which do not support microbial growth (co-metabolism) (Seffernick and Wackett, 2001). Nevertheless in some cases, a few years after the introduction of the xenobiotic into the soil environment, the degradation rate seemed to accelerate apparently due to evolution of a new degradation pathway (van der Meer, 1997; Seffernick and Wackett, 2001; Johnson and Spain, 2003). The Darwinian principles of the origin of species (or genes) by the means of natural selection or the preservation of races (or genes) in the struggle for life are still valid (Darwin, 1859). Although soil may contain 10% organic matter, the degradation rate of this carbon, mainly humic and fulvic acids, is rather slow presumably due to limited availability to potential degrading agents (Stevenson, 1982). It is widely assumed that carbon availability is the most common limiting factor for microbial growth in soil (Alden et al., 2001; Koch et al., 2001). Thus the ability to exploit a readily available carbon source in the form of a new molecule would increase bacterial tness. The concept of the selsh gene is especially applicable to degradation genes in bacteria since many of them are mobile either on plasmids or other transposable insertion elements (van der Meer and Sentchilo, 2003; Top and Springael, 2003). In this scenario, a gene with higher tness is expected to proliferate in the environment in different bacterial hosts. These genes can select the most suitable host for a given environment and as a reward would increase the tness of their host. Evolution of degradation genes has occurred spontaneously for dichloropropionic acid in laboratory cultures under selective pressure (Senior et al., 1976). In other cases, a tedious gathering of evidence, employing diverse methods from biochemistry, genetics and bioinformatics was needed to elucidate the evolutionary pathways (e.g. Werlen et al.,

1996; Copley, 2000; Poelarends et al., 2000; Seffernick and Wackett, 2001; Johnson et al., 2002; Muller et al., 2003). Such evidence includes: remnants of genetic material from lateral gene transfer, scattered organization of the genes encoding the enzymes, primitive or inefcient regulation of enzyme synthesis, and poorly adapted degradative enzymes (high Km, low Kcat, low catalytic specicity). Study of the relatively primitive pathways reveals the strategies that bacteria use to evolve new capabilities and provides insight about the origins of the catabolic steps (Johnson and Spain, 2003). Atrazine metabolism is one of the best-studied cases of evolution of degradation genes (Seffernick and Wackett, 2001). During the rst 35 years of atrazine utilization, atrazine and its triazine degradation products were found to accumulate both in natural and laboratory media. Studies with pure and mixed microbial cultures showed that the catabolism of atrazine is mainly via N-dealkylation reactions and there were no reports of microbial dechlorination of atrazine (Seffernick and Wackett, 2001). In 1993, however, Mandelbaum et al. (1993) reported on rapid microbial dechlorination of atrazine. Shortly thereafter bacteria that can dechlorinate atrazine were isolated (e.g. Yanze-Kontchchou and Gschwind, 1994; Mandelbaum et al., 1995; Struthers et al., 1998; Topp et al., 2000a, b; Rousseaux et al., 2001). The transformation of atrazine to cyanuric acid by these bacteria occurs via a novel pathway. Atrazine chlorohydrolase (AtzA), the dechlorinating enzyme, is 98% identical (a difference in nine nucleic acids) to the enzyme melamine deaminase (TriA) which catalyzes the removal of two of the three amino groups from melamine (Seffernick et al., 2001). Melamine (2,4,6triamino-1,3,5-triazine) was introduce to the market 40 years before atrazine (Partington, 1961). Sequence comparison of triA and atzA suggested a lack of silent mutations and the authors suggested that atzA was evolved from triA under strong selective pressure (Seffernick et al., 2001). Attempts to further improve the efciency of the dechlorination associated with this gene by articial evolution (1600 different mutation), resulted in only slightly better activity (1.4 times faster). It implies that atzA has the optimal structure for catalyzing the dechlorination of atrazine and it is highly evolved (Raillard et al., 2001). Although mutations seem to play an important role in the evolution of atzA, gene transfer was the important mechanism for gathering the DNA sequence associated with all six enzymes that are responsible of complete mineralization of atrazine on the same plasmid (Martinez et al., 2001). Based on the GC content, it seems that the different genes evolved in different bacteria (Martinez et al., 2001). These genes (98100% identity) were found in different bacteria from different families and from different geographic regions (de Souza et al., 1998; Rousseaux et al., 2001). It demonstrates the rapid dispersion of the newly evolved genes throughout the world.

Author's personal copy

ARTICLE IN PRESS
1740 Z. Arbeli, C.L. Fuentes / Crop Protection 26 (2007) 17331746

4. Possible solutions One way to cope with the problem of reduced pesticide efcacy due to enhanced microbial degradation would be to increase the amount and/or frequency of application of the pesticide. The increased chemical and application cost and regulatory limits on application rates often restrict this approach. Moreover, increasing the application rate may further increase the population of pesticide degraders, which would result in an even higher degradation rate of the pesticide. Replacing the pesticide with another is a second option. However, this is not always feasible since in some cases all of the available pesticides are prone to accelerated degradation. In addition, the alternatives are, in many cases, more expensive. Thus, the increased difculty of pest control associated with accelerated degradation of pesticides clearly indicates the need for more sophisticated pest management, in another words: Integrated Pest Management (IPM) (Katan, 2000; Way and van Emden, 2000). IPM attempts to reduce pest populations by a variety of means instead of relying only on a chemical whose efcacy is susceptible to the development of pest resistance and accelerated microbial degradation. Although accelerated degradation of pesticides is only one additional reason to adopt IPM, the phenomenon has some characteristics which require special consideration in planning pesticide management. Efforts to incorporate pesticides into IPM programs and deal with the effects of accelerated degradation have followed two main approaches: (1) trying to avoid development of accelerated degradation; and (2) trying to circumvent it after its development (Felsot and Tollefson, 1990). One of the most often suggested strategies is crop and pesticide rotation (e.g. Karpouzas et al., 2004b; Warton et al., 2003). Crop rotation will reduce the build up of pest populations, which are specialized for each crop. Pesticide rotation will reduce the build up of microorganisms that degrade each pesticide due to the longer intervals between applications. Pesticide rotation may be easier to introduce into a crop rotation system which normally requires a different pesticide for each of the major crop specic pests. While designing a pesticide rotation, it should be kept in mind that in many cases microorganisms are able to degrade chemicals which are structurally related and therefore adaptation of these microorganisms to one pesticide could also lead to rapid degradation of the others thereby reducing their usefulness as components of a rotation (see cross acclimation above). Thus, it is desirable to rotate pesticides which are structurally different or are known not to undergo cross acclimation. Another important consideration is the duration of accelerated degradation. It has been demonstrated that the high degradation rates associated with accelerated microbial degradation can still exist up to 5 years after the last pesticide application (Di Primo et al., 2003; Parekh et al., 1992; Suett et al., 1993; Smelt et al., 1996).

One pest control strategy that is particularly vulnerable to the effect of enhanced microbial degradation is a seed furrow application, which is expected to provide prolonged protection for the developing crop. Many important insect pests that this strategy is used to control have complex life cycles in which some stages (often the larva) live in the soil, while other stages (often the adults) live outside of soil. In these cases, it might be more effective to suppress female adults, just before or at the beginning of the egg-laying period, with pesticides that are not applied to soil (Felsot and Tollefson, 1990). Another approach would be to change the time of pesticide application to the soil in order to reduce the need for a prolong effect. Instead of applying the pesticide at a high rate at planting time, the application, possibly at a reduced rate, could be timed to coincide more closely with pest activity thereby reducing the need for prolonged efcacy (Felsot and Tollefson, 1990). Both strategies depend on careful monitoring of elds to detect female adults or larval infection. This is in good agreement with the philosophy of IPM, but requires additional training of farmers and results in additional costs. Pest control problems associated with accelerated degradation could be tackled by inhibiting or killing the microorganisms, which degrade the pesticides. For instance, soil fumigation (methyl bromide) or soil solarization, which is used to control soil born pathogens, has been found to prolong the effective lifetime of terbutryn from 2 to 10 weeks (Avidov et al., 1985). In a similar way, microbial inhibitors (also called extenders) can be added to the pesticide formulation to extend the duration of pest control (Harvey, 1990). Unfortunately, some of the fumigants (e.g. Metam-SodiumDi Primo et al., 2003) and extenders (e.g. dietholateHarvey, 1990) can also suffer from accelerated degradation. Another area of investigation designed to avoid development of accelerated degradation is based on the formulation of the pesticide. Theoretically, a formula, which is an available to microorganisms and can slowly release the pesticide into the soil may be able to provide extended pest control (Pussemier et al., 1996). Felsot and Tollefson (1990) compared the persistence of carbofuran coated on sand (Furdan 15G) and carbofuran in a rollcompacted gypsum granule designed to release the insecticide more slowly. Greater persistence of the insecticide was observed in soils treated with the gypsum formulation both in laboratory and eld experiments. Nevertheless, crop protection was not improved probably because the slow-release formulation failed to provided a sufciently high concentration of carbofuran in the soil. Better results were achieved with a slow-release formulation of aldicarb (Coppedge et al., 1976) which did extend the bioactivity over a longer time. It was concluded that this strategy is more appropriate for highly active pesticides, which are toxic to pests even at low concentrations.

Author's personal copy

ARTICLE IN PRESS
Z. Arbeli, C.L. Fuentes / Crop Protection 26 (2007) 17331746 1741

5. A discussion on the tropical dimension Accelerated microbial degradation of pesticides has been observed in widely separated geographical zones such as Europe (Suett et al., 1996a), the United States (Racke and Coats, 1990a), New Zealand (Rahman and James, 1983), Australia (Robertson et al., 1998), India (Sethunathan, 1971), Israel (Tal et al., 1989a, b) and Costa-Rica (Moens et al., 2004). Most studies on the environmental fate and accelerated microbial degradation of pesticides have been done in temperate zones (i.e. Europe and North America), while studies done in tropical countries are relatively scarce. Hence, in addition to encouraging more studies in tropical zones, it is important to know whether results from experiments done in temperate zones can be extrapolated to the tropics (Racke et al., 1997). In relation to accelerated microbial degradation as it occurs in the tropics, there are three important questions: (1) Are soil bacterial communities in the tropics distinctly different from those in temperate zones and do these differences have an inuence on the functional diversity and intensity of the phenomenon? (2) To what extent do different soils and environmental conditions in the tropics have an inuence on microbial activity associated with pesticide degradation? (3) Do the different agricultural practices of tropical zones inuence the phenomenon? The study of microbial biogeography has gained a lot from the introduction of molecular methods to microbial ecology but the basic question: is everything everywhere? is still under debate (Whiteld, 2005). On the one hand, it is evident that global transport of microorganisms is much easier than that of most macroorganisms. Due to their small size, their high number and their ability to form stable dormant forms, microorganisms can be easily transported across the planet (Finlay, 2002; Kellogg and Grifn, 2006). In accordance with this, a recent study suggests that microbial environmental conditions, especially pH, are far more important than geographical distance in controlling bacterial diversity and community structure (Fierer and Jackson, 2006). On the other hand, recent studies have demonstrated microbial endemism in hot sprigs (Papke et al., 2003; Whitaker et al., 2003) and pristine soils (Cho and Tiedje, 2000; Fulthorpe et al., 2003), at least at the sub-species level. These studies suggest that diversication rate of some bacteria is greater than changes in community diversity resulting from long-distance transport. It is likely that different microbial taxa vary in their dispersal ability according to their population size, their ability to form stable dormant forms, their ability to colonial new habitat and to resist extinction (Martiny et al., 2006). Studies that suggest microbial endemism are based on genetic analysis, while, to the best of our knowledge, there are no studies that deal with biogeographic patterns on the phenotypic level. Hence, it remains possible that the genetic differences which were found among bacteria from distinct geographical zones reect neutral or nearly neutral mutations (Fenchel, 2003).

For accelerated degradation of pesticides, the discussion should concentrate on the phenotypic level in agricultural soils and biogeography of degradation genes. We suggest that difference among degradation phenotype in agriculture soils due to geographical distance is lower than genomic genetic difference (which could represent neutral mutation) among bacteria in pristine environment: (1) agriculture practices such as vegetation removal, soil tillage and commercial seed distribution probably enhance global bacterial transport; (2) many degradation genes, which are associated with transposable elements, may be transported faster than some of the soil bacteria by choosing bacteria with best transport abilities; (3) as was demonstrated by Senior et al. (1976), under strong selective pressure, mutation which lead to improved degradation ability is likely to repeat it self (in different places); (4) convergent evolution due to strong selective pressure to exploit new substrates can act as additional forth which reduce phenotypic difference between different geographical zones. Atrazine is a good case study since it is assumed that atrazine degradation genes have recently evolved (Seffernick and Wackett, 2001). These genes have been found in Europe (Rousseaux et al., 2001; Piutti et al., 2003), North America (de Souza et al, 1998; Topp et al., 2000a, b), New Zealand (Aislabie et al., 2005), China (Cai et al., 2003), Japan (Satsuma, 2006) and Colombia (Arbeli and Fuentes, in preparation). As these recently evolved genes are already widely distributed, it is likely that the difference among ancient metabolic gene in agricultural soil is even lower. Hence it appears that as a general rule, the old paradigm of Baas Becking Everything is everywhere, but, the environment selects (de Wit and Bouvier, 2006) is a good approximation, at least on the functional level. Nevertheless, exceptions might exist, and it is more likely to happens with newly evolve genes which are located on the chromosomes. For example, thus far, accelerated degradation of chloropyrophos was observed only in Australia (Robertson et al., 1998; Singh et al., 2003a), though, it is not clear whether it is due to genetic endemism or lack of sufcient studies. From the previous discussion it appears that environmental conditions and agriculture practice are more likely to inuence accelerated degradation. Tropical soils and climate conditions are diverse but some generalization can be made. The predominant distinguishing parameter between tropical and temperate zones is the low yearround variation of temperature. In addition, temperature in the tropic is usually high though it highly depends on elevation (for more details on the characteristic of tropical climate and soils see Cobley and Steele, 1984; Racke et al, 1997). Tropical zones can be divided according to the amount and distribution of precipitation: (1) the udic regime, closest to the equator, which characterized by large amounts of rainfall all year round; (2) the ustic regimes which receive less precipitations and have one or two dry periods per year; (3) the aridic regimes which characterized by low precipitation resulting in dry or desert conditions.

Author's personal copy

ARTICLE IN PRESS
1742 Z. Arbeli, C.L. Fuentes / Crop Protection 26 (2007) 17331746

Hence, seasonal changes in soil microbial activity in the tropic are mainly inuenced by moisture (Racke et al., 1997). The inuence of environmental condition on pesticide fate in tropical zone has been discussed in detail by Racke et al. (1997). They concluded that under the same environmental conditions, there is no signicant difference in either kinetics or pathway of pesticide degradation by soils from tropical and temperate zones. However, volatilization and the rate of chemical and microbial degradation is favored by high temperature, and dissipation of pesticides is signicantly faster under tropical conditions (Simon et al., 1992; Racke et al., 1997). Hence, the effect of accelerated degradation in tropical zones might be stronger. The effect of the constantly high temperatures that occurs in the tropics on microbial turnover in soil has not been study. This factor could be particularly relevant to accelerated degradation: If under these conditions microbial succession is faster, populations of pesticide degraders may be reduced rapidly and accelerated degradation may not occur or durations may be reduced compared to temperate conditions. In addition, microbial turn over might differ in udic, ustic and aridic regimes (Racke et al., 1997). Agronomical practice is the last factor that could inuence accelerated degradation. Under tropical conditions it is possible to add more crop cycles during a year. In addition, high temperature and moisture all year in the tropics tend to enhance populations of insects, fungi and other pests. This may result in more frequent pesticide applications, which would favor the development of accelerated microbial degradation. In tropical developing countries there may be less awareness of the phenomenon which may result in sub-optimal pesticide management and incorrect diagnosis of pest control problems should accelerated degradation occur. In conclusion, accelerated degradation might be enhanced in the tropics and damage to a crop might be more extensive and costly if pesticide efcacy were reduced by the phenomena. 6. Concluding remarks In the last 10 years, research effort on accelerated microbial degradation of pesticides in soil has declined considerably. The extent of the inuence of accelerated degradation on agricultural practice is still not clear. In the middle of the 1980s, Roeth (1986) concluded in his review that research techniques used to study accelerated degradation should be rened. At the same time molecular methods were introduced to the eld of microbial ecology (Olsen et al., 1986) and they have had a dramatic inuence on our knowledge in this eld (e.g. Hugenholtz et al., 1998; Dabert et al., 2002). Although molecular methods have been applied to the study of pesticide degradation, they were not directly applied to the study of accelerated degradation. These methods have the potential to give a much more accurate view of microbial community dynamics and gene expression that are related to the induction of accelerated

degradation, to the duration of the phenomenon, to cross acclimation, and to the inuence of environmental and climatic conditions, and perhaps suggest new solutions. Acknowledgments We are deeply grateful to Ralph Chapman and Patrice Dion for their helpful comments on the manuscript. This work was supported by the Direccion de Investigacion Sede Bogota (DIB) and the Escuela de Posgrados, Facultad Agronom a, Universidad Nacional de Colombia. References
Aislabie, J., Bej, A.K., Ryburn, J., Lloyd, N., Wilkins, A., 2005. Characterization of Arthrobacter nicotinovorans HIM, an atrazinedegrading bacterium, from agricultural soil New Zealand. FEMS Microbiol. Ecol. 52, 279286. Albarran, A., Celis, R., Hermos n, M.C., Lopez-Pineiro, A., Cornejo, J., 2004. Behaviour of simazine in soil amended with the nal residue of the olive-oil extraction process. Chemosphere 54, 717724. Alexander, M., 1999. Biodegradation and Bioremediation, second ed. Academic Press, New York. Alden, L., Demoling, F., Baath, E., 2001. Rapid method of determining factors limiting bacterial growth in soil. Appl. Environ. Microbiol. 67, 18301838. Anderson, P.E., Lafuerza, A., 1992. Microbiological aspects of accelerated pesticide degradation. In: Anderson, J.P.E., Arnold, D.J., Lewis, F., Torstensson, L. (Eds.), Proceedings of the International Symposium on Environmental Aspects of Pesticide Microbiology. Department of Microbiology, Swedish University of Agricultural Sciences, Uppsala, pp. 184192. Audus, L.J., 1949. Biological detoxication of 2,4-D. Plant Soil 2, 3136. Audus, L.J., 1951. The biological detoxication of hormone herbicides in soil. Plant Soil 3, 170192. Avidov, E., Aharonson, N., Katan, J., Rubin, B., 1985. Persistence of terbutryn and atrazine in soil as affected by soil disinfestation and fungicides. Weed Sci. 33, 457461. Avidov, E., Aharonson, N., Katan, J., 1988. Accelerated degradation of diphenamid in soils and means for its control. Weed Sci. 36, 519523. Barriuso, E., Houot, S., 1996. Rapid mineralization of the S-triazine ring of atrazine in soils in relation to soil management. Soil Biol. Biochem. 28, 13411348. Bending, G.D., Shaw, E., Walker, A., 2001. Spatial heterogeneity in the metabolism and dynamics of IPU-degrading microbial communities in soil. Biol. Fert. Soils 33, 484489. Cai, B., Han, Y., Liu, B., Ren, Y., Jiang, S., 2003. Isolation and characterization of an atrazine-degrading bacterium from industrial wastewater in China. Lett. Appl. Microbiol. 36, 272276. Chapman, R.A., Harris, C.R., 1990. Enhanced degradation of insecticides in soil: Factors inuencing the development and effects of enhanced microbial activity. In: Racke, K.D., Coats, J.R. (Eds.), Enhanced Biodegradation of Pesticides in the Environment. American Chemical Society, Washington, DC, pp. 8296. Cho, J.C., Tiedje, J.M., 2000. Biogeography and degree of endemicity of uorescent Pseudomonas strains in soil. Appl. Environ. Microbiol. 66, 54485465. Cobley, L.S., Steele, W.M., 1984. An Introduction to the Botany of Tropical Crops. Longman, New York. Copley, S.D., 2000. Evolution of a metabolic pathway for degradation of a toxic xenobiotic: the patchwork approach. Trends Biochem. Sci. 25, 261265. Coppedge, J.R., Stokes, R.A., Ridgway, R.L., Kinzer, R.E., 1976. Slowrelease formulation of aldicarb. Modeling of soil persistence. USDA Public. No. ARS-S-103, USDA-ARS, p. 6.

Author's personal copy

ARTICLE IN PRESS
Z. Arbeli, C.L. Fuentes / Crop Protection 26 (2007) 17331746 Dabert, P., Delgenes, J.P., Moletta, R., Godon, J.J., 2002. Contribution of molecular microbiology to the study in water pollution removal of microbial community dynamics. Rev. Environ. Sci. Biotechnol. 1, 3949. Darwin, C.R., 1859. The origin of species by the means of natural selection, or the preservation of races in the struggle for life. Dzantor, E.K., Felsot, A.S., 1989. Effect of conditioning, crossconditioning, and microbial growth on development of enhanced biodegradation of insecticides in soil. J. Environ. Sci. Helth B 24, 569597. de Souza, M.L., Seffernick, J., Martinez, B., Sadowsky, M.J., Wackett, L.P., 1998. The atrazine catabolism genes atzABC are widespread and highly conserved. J. Bacteriol. 180, 19511954. de Wit, R., Bouvier, T., 2006. Everything is everywhere, but, the environment selects; what did Baas Becking and Beijerinck really say? Environ. Microbiol. 8, 755758. Di Primo, P., Gamliel, A., Austerweil, M., Steiner, B., Beniches, M., Peretz-Alon, I., Katan, J., 2003. Accelerated degradation of metamsodium and dazomet in soil: characterization and consequences for pathogen control. Crop Prot. 22, 635646. El-Sebai, T., Lagacherie, B., Cooper, J.F., Soulas, G., Martin-Laurent, F., 2005. Enhanced isoproturon mineralisation in a clay silt loam agricultural soil. Agron. Sustain. Dev. 25, 271277. Engvold, K.C., Jansen, H.L., 1969. Microbiological decomposition of the herbicide pyrazon. Soil Biol. Biochem. 1, 295300. Felsot, A.S., 1986. Effect of conditioning soil for enhanced biodegradation of carbofuran on dissipation of other methyl carbamate insecticides. In: Sixth International Congress of Pesticide Chemistry, Ottawa, Canada; International Union of Pure and Applied Chemistry: Oxford, England, Paper 6B-08. Felsot, A.S., 1989. Enhanced biodegradation of insecticides in soil: implications for agrosystems. Annu. Rev. Entomol. 34, 453476. Felsot, A.S., Tollefson, J.J., 1990. Evaluation of some methods for coping with enhanced biodegradation of soil insecticides. In: Racke, K.D., Coats, J.R. (Eds.), Enhanced Biodegradation of Pesticides in the Environment. American Chemical Society, Washington, DC, pp. 192213. Felsot, A.S., Maddox, J.V., Bruce, W., 1981. Enhanced microbial degradation of carbofuran in soils with histories of furadan use. Bull. Environ. Contamin. Toxicol. 26, 781788. Fenchel, T., 2003. Biogeography for bacteria. Science 301, 295296. Fernando, T., Aust, S.D., 1994. Biodegradation of toxic chemicals by white rot fungi. In: Chaudhry, G.R. (Ed.), Biological Degradation and Bioremediation of Toxic Chemicals. Chapman & Hall, London, pp. 386402. Fierer, N., Jackson, R.B., 2006. The diversity and biogeography of soil bacterial communities. Proc. Nat. Acad. Sci. 103, 626631. Finlay, B.J., 2002. Global dispersal of free-living microbial eukaryote species. Science 296, 10611063. Forrest, M., Lord, K.A., Walker, N., Woodville, H.C., 1981. The inuence of soil treatments on the bacterial degradation of diazinon and other organophosphorus insecticides. Environ. Pollut. Ser. A 24, 93104. Fulthorpe, R.R., Rhodes, A.N., Tiedje, J.M., 2003. High levels of endemicity of 3-chlorobenzoate-degrading soil bacteria. Appl. Environ. Microbiol. 64, 16201627. Getzin, L.W., 1973. Persistence and degradation of carbofuran in soil. Environ. Entomol. 2, 461467. Gray, R.A., Joo, G.K., 1985. Reduction in weed control after repeated application of thiocarbamate and other herbicides. Weed Sci. 33, 698702. Hamm, R.T., Thomas, J.H., 1986. Microbial degradation of cloethocarb and carbofuran in two different soils. In: Sixth International Congress of Pesticide Chemistry, Ottawa, Canada; International Union of Pure and Applied Chemistry: Oxford, England, 1986; Paper 6C-14. Harris, C.R., Chapman, R.A., Harris, C., Tu, C.M., 1984. Biodegradation of pesticides in soil: rapid induction of carbamate degrading factors after carbofuran treatment. J. Environ. Sci. Health Part B B19, 111. 1743 Harris, C.R., Chapman, R.A., Morris, R.F., Stevenson, A.B., 1988. Enhanced microbial degradation of pesticides carbofuran and fensulfothiona factor contributing to the decline in effectiveness of some soil insect control programs in Canada. J. Environ. Sci. Health Part B B23, 301316. Harvey, R.G., 1987. Herbicide dissipation from soils with different herbicide use histories. Weed Sci. 35, 583589. Harvey, R.G., 1990. Systems allowing continued use of carbamothioate herbicides despite enhanced biodegradation. In: Racke, K.D., Coats, J.R. (Eds.), Enhanced Biodegradation of Pesticides in the Environment. American Chemical Society, Washington, DC, pp. 214221. Harvey, R.G., 1991. Effect of herbicide rotations on enhanced herbicide biodegradation and Wild-Proso Millet (Panicum miliaceum) control. Weed Sci. 39, 607613. Harvey, R.G., McNevin, G.R., Albright, J.W., Kozak, M.E., 1986. Wild Proso Millet (Pancium miliaceum) control with thiocarbamate herbicides on previously treated soils. Weed Sci. 34, 773780. Hole, S.J., McClure, N.C., Powles, S.B., 2001. Rapid degradation of carbetamide upon repeated application to Australian soils. Soil Biol. Biochem. 33, 739745. Horowitz, M., 1966. Breakdown of endothall in soil. Weed Res. 6, 168171. Hugenholtz, P., Goebel, B.M., Pace, N.R., 1998. Impact of cultureindependent studies on the emerging phylogenetic view of bacterial diversity. J. Bacteriol. 180, 47654774. Johnson, A.W., 1998. Degradation of fenamiphos in agricultural production soil. J. Nematol. 30, 4044. Johnson, G.R., Spain, J.C., 2003. Evolution of catabolic pathways for synthetic compounds: bacterial pathways for degradation of 2,4dinitrotoluene and nitrobenzene. Appl. Microbiol. Biotechnol. 62, 110123. Johnson, G.R., Jain, R.K., Spain, J.C., 2002. Origins of the 2,4dinitrotoluene pathway. J. Bacteriol. 184, 42194232. Karns, J.S., Mulbry, W.W., Nelson, J.O., Kearney, P.C., 1986. Metabolism of carbofuran by a pure bacterial culture. Pestic. Biochem. Physiol. 25, 211217. Karpouzas, D.G., Hatziapostolou, P., Papadopoulou-Mourkidou, E., Giannakou, I.O., Georgiadou, A., 2004a. The enhanced biodegradation of fenamiphos in soils from previously treated sites and the effect of soil fumigants. Environ. Toxicol. Chem. 23, 20992107. Karpouzas, D.G., Karanasios, E., Menkissoglu-Spiroudi, U., 2004b. Enhanced microbial degradation of cadusafos in soils from potato monoculture: demonstration and characterization. Chemosphere 56, 549559. Karpouzas, D.G., Fotopoulou, A., Menkissoglu-Spiroudi, U., Singh, B.K., 2005. Non-specic biodegradation of the organophosphorus pesticides, cadusafos and ethoprophos, by two bacterial isolates. FEMS Microbiol. Ecol. 53, 369378. Katan, J., 2000. Physical and cultural methods for the management of soil-borne pathogens. Crop Prot. 19, 725731. Kaufman, D.D., Edwards, D.F., 1983. Pesticide/microbe interaction effects on persistence of pesticides in soil. In: Miyamoto, J., Kearney, P.C. (Eds.), Pesticides Chemistry: Human Welfare and Environment. Pergamon, Oxford, England. Kaufman, D.D., Katan, J., Edwards, D.F., Jordan, E.G., 1985. Microbial adaptation and metabolisms of pesticides. In: Hilton, J.L. (Ed.), Agricultural Chemicals of the Future. Rowman & Allanheld, New Jersey, pp. 437451. Kellogg, C.A., Grifn, D.W., 2006. Aerobiology and the global transport of desert dust. Trends Ecol. Evolution 21, 638644. Kirkland, K., Fryer, J.D., 1972. Degradation of several herbicides in a soil previously treated with MCPA. Weed Res. 12, 9095. Koch, B., Worm, J., Jensen, L.E., Hjberg, O., Nybroe, O., 2001. Carbon limitation induces ss-dependent gene expression in Pseudomonas uorescens in soil. Appl. Environ. Microbiol. 67, 33633370. Kullman, S.W., Matsumura, F., 1996. Metabolic pathways utilized by Phanerochaete chrysosporium for degradation of the cyclodiene pesticide endosulfan. Appl. Environ. Microbiol. 62, 593600.

Author's personal copy

ARTICLE IN PRESS
1744 Z. Arbeli, C.L. Fuentes / Crop Protection 26 (2007) 17331746 bacterial strain possessing the gene trzN from bulk- and maize rhizosphere soil. FEMS Microbiol. Lett. 221, 111117. Poelarends, G.J., Kulakov, L.A., Larkin, M.J., Vlieg, J.E.T.V., Janssen, D.B., 2000. Roles of horizontal gene transfer and gene integration in evolution of 1,3 dichloropropene and 1,2-dibromoethane degradative pathways. J. Bacteriol. 182, 21912199. Pussemier, L., Debongnie, P.H., Goux, S., Chiang, C.L., 1996. Preliminary evaluation of alternative methods for the application of carbofuran in adapted soils. Soil Biol. Biochem. 28, 17771782. Racke, K.D., 1990. Pesticides in the soil microbial ecosystem. Enhanced biodegradation of pesticides in the environment. In: Racke, K.D., Coats, J.R. (Eds.), Enhanced Biodegradation of Pesticides in the Environment. American Chemical Society, Washington, DC, pp. 112. Racke, K.D., Coats, J.R., 1987. Enhanced degradation of isofenophos by soil microorganisms. J. Agric. Food Chem. 35, 9499. Racke, K.D., Coats, J.R., 1988a. Comperative degradation of organophosphorus insecticides in soil: specicity of enhanced microbial degradation. J. Agric. Food Chem. 36, 193199. Racke, K.D., Coats, J.R., 1988b. Enhanced degradation and comparative fate of carbamate insecticides in soil. J. Agric. Food Chem. 36, 10671072. Racke, K.D., Coats, J.R. (Eds.), 1990a. Enhanced Biodegradation of Pesticides in the Environment. American Chemical Society, Washington, DC. Racke, K.D., Coats, J.R., 1990b. Enhanced biodegradation of insecticides in Midwestern Corn Soil. In: Racke, K.D., Coats, J.R. (Eds.), Enhanced Biodegradation of Pesticides in the Environment. American Chemical Society, Washington, DC, pp. 6881. Racke, K.D., Skidmore, M.W., Hamilton, D.J., Unsworth, J.B., Miyamoto, J., Cohen, S.Z., 1997. Pesticide fate in tropical soils. Pure Appl. Chem. 69, 13491371. Rahman, A., James, T.K., 1983. Decreased activity of EPTC+R-25788 followed repeated use in some New Zealand soils. Weed Sci. 31, 783789. Raillard, S.A., Krebber, A., Chen, Y., Ness, J.E., Bermudez, E., Trinidad, R., Fullem, R., Davis, C., Welch, M., Seffernick, J.L., Wackett, L.P., Stemmer, W.P.C., Minshull, J., 2001. Novel enzyme activities and functional plasticity revealed by recombining highly homologous enzymes. Chem. Biol. 8, 891898. Ravelli, A., Pantani, O., Calamai, L., Fusi, P., 1997. Rates of chlorsulfuron degradation in three Brazilian oxisols. Weed Res. 37, 5159. Read, D.C., 1983. Enhanced microbial degradation of carbofuran and fensulfothion after repeated application to acid mineral soil. Agric. Ecosyst. Environ. 10, 3746. Read, D.C., 1987. Greatly accelerated microbial degradation of aldicarb in re-treated eld soil in ooded soil, and in water. J. Econ. Entomol. 80, 156163. Riempa, 1962. Preliminary observation on the breakdown of 3amino1,2,4-triazole in soil. Weed Res. 2, 4150. Robertson, B.K., Alexander, M., 1994. Growth-linked and cometabolic biodegradation: possible reason for occurrence or absence of accelerated pesticide biodegradation. Pestic. Sci. 41, 311318. Robertson, L.N., Chandler, K.J., Stickley, B.D.A., Cocco, R.F., Ahmetagic, M., 1998. Enhanced microbial degradation implicated in rapid loss of chlorpyrifos from the controlled-release formulation suSCons Blue in soil. Crop Prot. 17, 2933. Rodriguez, L.D., Dorough, H.W., 1977. Degradation of carbaryl by soil microorganisms. Arch. Environ. Contam. Toxicol. 6, 4756. Roeth, F.W., 1986. Enhanced herbicide degradation in soil with repeat application. Rev. Weed Sci. 2, 4565. Roeth, F.W., Wilson, R.G., Martin, A.R., Shea, P.J., 1990. Enhanced carbamothioate herbicide degradation: research in Nebraska. In: Racke, K.D., Coats, J.R. (Eds.), Enhanced Biodegradation of Pesticides in the Environment. American Chemical Society, Washington, DC, pp. 2336. Kulshrestha, G., Singh, S.B., Lal, S.P., Yaduraju, N.T., 2000. Effect of long-term eld application of pendimethalin: enhanced degradation in soil. Pest Manage. Sci. 56, 202206. Leasure, J.K., 1964. Metabolism of herbicides, the halogenated aliphatic acids. J. Agric. Food Chem. 12, 4043. Maier-Bode, H., Hartel, K., 1981. Linuron and monolinuron. Residue Rev. 77, 1364. Mandelbaum, R.T., Wackett, L.P., Allan, D.L., 1993. Rapid hydrolysis of atrazine to hydroxyatrazine by soil bacteria. Environ. Sci. Technol. 27, 19431946. Mandelbaum, R.T., Allan, D.L., Wackett, L.P., 1995. Isolation and characterization of a Pseudomonas sp. that mineralizes the s-triazine herbicide atrazine. Appl. Environ. Microbiol. 61, 14511457. Martinez, B., Tomkins, J., Wackett, L.P., Wing, R., Sadowsky, M.L., 2001. Complete nucleotide sequence and organization of the atrazine catabolic plasmis pADP-1 from Pseudomonas sp. strain ADP. J. Bacteriol. 183, 56845697. Martiny, J.B.H., Bohannan, B.J.M., Brown, J.H., Colwell, R.K., Fuhrman, J.A., Green, J.L., Horner-Devine, M.C., Kane, M., Adams Krumins, J., Kuske, C.R., Morin, P.J., Naeem, S., Ovreas, L., Reysenbach, A.L., Smith, V.H., Staley, J.T., 2006. Microbial biogeography: putting microorganisms on the map. Nat. Rev. Microbiol. 4, 102112. Matsumura, F., Boush, G.M., 1966. Malathion degradation by Trichoderma viride and a Pseudomonas species. Science 153, 12781280. Mitchell, J.A., Cain, R.B., 1996. Rapid onset of the accelerated degradation of dicarboximide fungicides in a UK soil with a long history of agrochemicals exclusion. Pesticide Sci. 48, 111. Moens, T., Araya, M., Swennen, R., De Waele, D., 2004. Enhanced biodegradation of nematicides after repetitive applications and its effects on root and yield parameters in commercial banana plantations. Biol. Fertil. Soils 39, 407414. Morel-Chevillet, C., Parekh, N.S., Pautrel, D., Fournier, J., 1996. Cross enhancement of carbofuran biodegradation in soil samples previously treated with carbamate pesticides. Soil Biol. Biochem. 28, 17671776. Muller, T.A., Werlen, C., Spain, J., van der Meer, J.R., 2003. Evolution of a chlorobenzene degradative pathway among bacteria in a contaminated groundwater mediated by a genomic island in Ralstonia. Environ. Microbiol. 5, 163173. Obrigawich, T., Roeth, F.W., Martin, A.R., Wilson, R.G., 1982. Addition of R-33865 to EPTC for extended herbicide activity. Weed Sci. 30, 417422. Olsen, G.J., Lane, D.J., Giovannoni, S.J., Pace, N.R., 1986. Microbial ecology and evolution: a ribosomal RNA approach. Annu. Rev. Microbiol. 40, 337365. Ou, L.T., 1991. Interaction of microorganisms and soil during phenamiphos degradation. Soil Sci. Soc. Am. J. 55, 716722. Papke, R.T., Ramsing, N.B., Bateson, M.M., Ward, D.M., 2003. Geographical isolation in hot spring cyanobacteria. Environ. Microbiol. 5, 650659. Parekh, N.R., McKeown, T., Roberts, S.J., Walker, A., Suett, D.L., 1992. Bacterial systems involved in the enhanced degradation of soil-applied pesticides. In: Anderson, J.P.E., Arnold, D.J., Lewis, F., Torstensson, L. (Eds.), Proceedings of the International Symposium on Environmental Aspects of Pesticide Microbiology. Department of Microbiology, Swedish University of Agricultural Sciences, Uppsala, pp. 153158. Partington, J.R., 1961. A History of Chemistry. Macmillan, London, England. Pattison, T., Versteeg, C., 2000. Enhanced biodegradation of terbufos. Bananatopics 29, 1617. Piutti, S., Marchand, A.-L., Lagacherie, B., Martin-Lauret, F., Soulas, G., 2002. Effect of cropping cycles and repeated herbicide applications on the degradation of diclofop-methyl, bentazone, diuron, isoproturon and pendimethalin in soil. Pest. Manage. Sci. 58, 303312. Piutti, S., Semon, E., Landry, D., Hartmann, A., Dousset, S., Lichtfouse, E., Topp, E., Soulas, G., Martin-Laurent, F., 2003. Isolation and characterisation of Nocardioides sp. SP12, an atrazine-degrading

Author's personal copy

ARTICLE IN PRESS
Z. Arbeli, C.L. Fuentes / Crop Protection 26 (2007) 17331746 Rouchaud, J., Neus, O., Bulcke, R., Callens, D., Dekkers, T., 1997. Isoxaben soil biodegradation in pear tree orchard after repeated high dose application. Arch. Environ. Contam. Toxicol. 33, 247251. Rouchaud, J., Neus, O., Bulcke, R., Cools, K., Eelen, H., Dekkers, T., 2000. Soil dissipation of diuron, chlorotoluron, simazine, propyzamide, and diufenican herbicides after repeated applications in fruit tree orchards. Arch. Environ. Contam. Toxicol. 39, 6065. Rousseaux, S., Hartmann, A., Soulas, G., 2001. Isolation and characterization of new gram-negative and gram positive atrazine degrading bacteria from different French soils. FEMs Microbial. Ecol. 36, 211222. Satsuma, K., 2006. Characterisation of new strains of atrazinedegrading Nocardioides sp. isolated from Japanese riverbed sediment using naturally derived river ecosystem. Pest Manage. Sci. 62, 340349. Savage, K.E., 1973. Nitralin and triuralin persistence in soil. Weed Sci. 21, 285288. Seffernick, J.L., Wackett, L.P., 2001. Rapid evolution of bacterial catabolic enzymes: a case study with atrazine chlorohydrolase. Biochemistry 40, 1274712753. Seffernick, J.L., de Souza, M.L., Sadowsky, M.J., Wackett, L.P., 2001. Melanine deaminase and atrazine chlorohydrolase: 98 percent identical but functionally different. J. Bacteriol. 183, 24052410. Senior, E., Bull, T., Slater, J.H., 1976. Enzyme evolution in a microbial community growing on herbicide Dalapon. Nature 263, 476479. Sethunathan, N., 1971. Biodegradation of diazinon in paddy eld as a cause of loss of its efciency for controlling brown planthoppers in rice elds. Pest Articles News Summaries 17, 1819. Sethunathan, N., Pathak, M.D., 1972. Increased biological hydrolysis of diazinon after repeated application in rice paddies. J. Agric. Food Chem. 20, 586589. Shapir, N., Rosendahl, C., Johnson, G., Andreina, M., Sadowsky, M.J., Wackett, L.P., 2005. Substrate specicity and colorimetric assay for recombinant TrzN derived from Arthrobacter aurescens TC1. Appl. Environ. Microbiol. 71, 22142220. Simon, L., Spiteller, M., Wallnofer, P.R., 1992. Metabolism of Fenamiphos in 16 soils originating from different geographic areas. J. Agric. Food Chem. 40, 312317. Singh, B.K., Walker, A., 2006. Microbial degradation of organophosphorus compounds. FEMS Microbiol. Rev. 30, 428471. Singh, B.K., Kuhad, R.C., Singh, A., Lal, R., Tripathi, K.K., 1999. Biochemical and molecular basis of pesticide degradation by microorganisms. Crit. Rev. Biotechnol. 19, 197225. Singh, B.K., Walker, A., Morgan, J.A.W., Wright, D.J., 2003a. Effects of soil pH on the biodegradation of chlorpyrifos and isolation of a chlorpyrifos-degrading bacterium. Appl. Environ. Microbiol. 69, 51985206. Singh, B.K., Walker, A., Morgan, J.A.W., Wright, D.J., 2003b. Role of soil pH in the development of enhanced degradation of fenamiphos. Appl. Environ. Microbiol. 69, 70357043. Singh, B.K., Walker, A., Wright, D.J., 2005. Cross-enhancement of accelerated biodegradation of organophosphorus compounds in soils: Dependence on structural similarity of compounds. Soil Biol. Biochem. 37, 16751682. Skipper, H.D., 1990. Enhanced biodegradation of carbamothionate herbicides in South Carolina. In: Racke, K.D., Coats, J.R. (Eds.), Enhanced Biodegradation of Pesticides in the Environment. American Chemical Society, Washington, DC, pp. 2336. Skipper, H.D., Murdock, E.C., Gooden, D.T., Zublena, J.P., Amakiri, M.A., 1986. Enhanced herbicide biodegradation in South Carolina soils previously treated with butylate. Weed Sci. 34, 558563. Smelt, J.H., Crum, S.J.H., Teunissen, W., Leistra, M., 1987. Accelerated transformation of aldicarb, oxamyl and ethoprophos after repeated soil treatments. Crop Prot. 6, 295303. Smelt, J.H., Teunissen, W., Crum, S.J.H., Leistra, M., 1989. Accelerated 1,3-dichloropropene transformation in loamy soils. Neth. J. Agric. Sci . 37, 173183. Smelt, J.H., Van de Peppel-Groen, A.E., Van der Plas, L.J.T., Dijksterhuis, A., 1996. Development and duration of accelerated 1745 degradation of nematicides in different soils. Soil Biol. Biochem. 28, 17571765. Somasundaram, L., Jayachandran, K., Kruger, E.L., Racke, K.D., Moorman, T.B., Dvorak, T., Coats, J.R., 1993. Degradation of isazofos in the soil environment. J. Agric. Food Chem. 41, 313318. Spanis, W.C., Munnecke, D.E., Solberg, R.A., 1962. Biological breakdown of two organic mercurial fungicides. Phytopathology 52, 455462. Stevenson, F.J., 1982. Humus Chemistry: Genesis, Composition, Reactions. Wiley, New York, p 12. Strong, L.C., Rosendahl, C., Johnson, G., Sadowsky, M.J., Wackett, L.P., 2002. Arthrobacter aurescens TC1 metabolizes diverse s-triazine ring compounds. Appl. Environ. Microbiol. 68, 59735980. Struthers, J.K., Jayachandran, K., Moorman, T.B., 1998. Biodegradation of atrazine by Agrobacterium radiobacter J14a and use of this strain in bioremediation of contaminated soil. Appl. Environ. Microbiol. 64, 33683375. Suett, D.L., 1987. Inuence of treatment of soil with carbofuran on the subsequent performance of insecticides against cabbage root y (Delia radicum) and carrot y (Psila rosae). Crop Prot. 6, 371378. Suett, D.L., Jukes, A.A., 1990. Some factors inuencing the accelerated degradation of mephosfolan in soils. Crop Prot. 9, 4451. Suett, D.L., Jukes, A.A., 1997. The Accelerated biodegradation of phorate in carrot soils in the United Kingdom. Crop Prot. 16, 457461. Suett, D.L., Jukes, A.A., Phelps, K., 1993. Stability of accelerated degradation of soil applied insecticides: laboratory behaviour of aldicarb and carbofuran in relation to their efcacy against cabbage root y (Delia radicum) in previously-treated eld soils. Crop Prot. 12, 431442. Suett, D.L., Fournier, J.C., Papadopoulou-Mourkidou, E., Pussemier, L., Smelt, J., 1996a. Accelerated degradation: the European dimension. Soil Biol. Biochem. 28, 17411748. Suett, D.L., Jukes, A.A., Parekh, N.R., 1996b. Non-specic inuence of pH on microbial adaptation and insecticide efcacy in previouslytreated eld soils. Soil Biol. Biochem. 28, 17831790. Tal, A., Rubin, B., Katan, J., Aharanson, N., 1989a. Accelerated degradation of thiocarbamate herbicides in Israeli soils following repeated use of vernolate. Pesticide Sci. 25, 343353. Tal, A., Rubin, B., Katan, J., Aharanson, N., 1989b. Fate of 14C-EPTC in a soil exhibiting accelerated degradation of carbamothionate herbicides and its control. Weed Sci. 37, 434439. Thom, E., Ottow, J.C.W., Benckiser, G., 1997. Degradation of the fungicide difenoconazole in a silt loam soil as affected by pretreatment and organic matter. Environ. Pollut. 3, 409414. Top, E.M., Springael, D., 2003. The role of mobile genetic elements in bacterial adaptation to xenobiotic organic compounds. Curr. Opin. Biotechnol. 14, 262269. Topp, E., Zhu, H., Nour, S.M., Houot, S., Lewis, M., Cuppels, D., 2000a. Characterization of an atrazine-degrading Pseudaminobacter sp. isolated from Canadian and French agricultural soils. Appl. Environ Microbiol. 66, 27732782. Topp, E., Mulbry, W.M., Zhu, H., Nour, S.M., Cuppels, D., 2000b. Characterization of s-triazine herbicide metabolism by a Nocardioides sp. isolated from agriculture soils. Appl. Environ Microbiol. 66, 31343141. van der Meer, J.R., 1997. Evolution of novel metabolic pathways for the degradation of chloroaromatic compounds. Antonie van Leeuwenhoek 71, 159178. van der Meer, J.R., Sentchilo, V., 2003. Genomic islands and the evolution of catabolic pathways in bacteria. Curr. Opin. Biotechnol. 14, 248254. Wagner, S.C., Zablotowicz, R.M., Gaston, L.A., Locke, M.A., Kinsella, J., 1996. Bentazon degradation in soil: inuence of tillage and history of bentazon application. J. Agric. Food Chem. 44, 15931598. Walker, A., 1987. Further observations on the enhanced degradation of iprodione and vinclozolin in soil. Pesticide Sci. 21, 219231. Walker, A., Welch, S.J., 1990. Enhanced biodegradation of Dicarboximide fungicides in soil. In: Racke, K.D., Coats, J.R. (Eds.), Enhanced

Author's personal copy

ARTICLE IN PRESS
1746 Z. Arbeli, C.L. Fuentes / Crop Protection 26 (2007) 17331746 Whiteld, J., 2005. Biogeography: is everything everywhere? Science 310, 960961. Wildung, R.E., Chesters, G., Amstrong, D.E., 1968. Chloramben (amiben) degradation in soil. Weed Res. 8, 213225. Williams, I.H., Pepin, H.S., Brown, M.J., 1976. Degradation of carbofuran by soil microorganisms. Bull. Environ. Contam. Toxicol. 15, 244249. Wilson, R.G., 1984. Accelerated degradation of thiocarbamate herbicides in soil with prior thiocarbamate herbicides exposure. Weed Sci. 32, 264268. Yadav, J.S., Soellner, M.B., Loper, J.C., Mishra, P.K., 2003. Tandem cytochrome P450 monooxygenase genes and splice variants in the white rot fungus Phanerochaete chrysosporium: cloning, sequence analysis, and regulation of differential expression. Fungal Genet. Biol. 38, 1021. Yanze-Kontchchou, C., Gschwind, N., 1994. Mineralization of the herbicide atrazine as a carbon source by a Pseudomonas strain. Appl. Environ. Microbiol. 60, 42974302. Yarden, O., Aharonson, N., Katan, J., 1987. Accelerated microbial degradation of methyl benzimidazol-2-ylcarbamate in soil and its control. Soil Biol. Biochem. 19, 735739. Biodegradation of Pesticides in the Environment. American Chemical Society, Washington, DC, pp. 5367. Walker, A., Welsh, S.J., 1991. Enhanced degradation of some soil-applied herbicides. Weed Res. 31, 4957. Warton, B., Matthiessen, J.N., 2005. The crucial role of calcium interacting with soil pH in enhanced biodegradation of metamsodium. Pest. Manage. Sci. 61, 856862. Warton, B., Matthiessen, J.N., Shackleton, M.A., 2003. Cross-enhancement: enhanced biodegradation of isothiocyanates in soils previously treated with metham sodium. Soil Biol. Biochem. 35, 11231127. Way, M.J., van Emden, H.F., 2000. Integrated pest management in practicepathways towards successful application. Crop Prot. 19, 81103. Werlen, C., Kohler, H.-P.E., van der Meer, J.R., 1996. The broad substrate chlorobenzene dioxygenase and cis-chlorobenzene dihydrodiol dehydrogenase of Pseudomonas sp. strain P51 are linked evolutionarily to the enzymes for benzene and toluene degradation. J. Biol. Chem. 271, 40094016. Whitaker, R.J., Grogan, D.W., Taylor, J.W., 2003. Geographic barriers isolate endemic populations of hyperthermophilic Archaea. Science 301, 976978.