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J. Pesticide Sci. 23, 223-229 (1998)

Original Article

Joint Action of Chlorfluazuron with Synergists and in Chlorfluazuron-Susceptible and Resistant Strains of Diamondback Moth, Plutella xylostella

Adel Ramzy FAHMY1 and Tadashi MIYATA

Laboratory of Applied Entomology, School of Agricultural Sciences, Nagoya University, Nagoya 464-8601, Japan

(Received January 22, 1997; Accepted February 27, 1998)

The synergistic action of triphenyl phosphate (TPP) and piperonyl butoxicide (PB) on chlorfluazuron was studied in chlorfluazuron-susceptible and resistant larvae of diamondback moth, Plutella xylostella (L.). Synergistic ratios with TPP and PB were approximately 7 and 4, respectively, in two resistant strains, namely TL-resistant (TL-R) and BK-resistant (BK-R) strains. There was no synergism with TPP and PB in TL-susceptible (TL-S) strain, while there was up to 2-fold with TPP and 3-fold with PB in the BK-susceptible (BK-S) strain. From these results, it is likely that the enhanced degradation of chlorfluazuron by a TPP-sensitive enzyme system is responsible for chlorfluazuron resistance in diamond- back moth. Teflubenzuron at a nontoxic level (

ment of resistance.6,7) INTRODUCTION The significance of synergism studies arises for two Diamondback moth, Plutella xylostella (L.), is a cos- main reasons. The first is that synergists may be used as mopolitan serious pests of crucifer crops. It causes a rapid and reliable method to predict the enzyme severe crop damage in infested areas due to control system(s) responsible for degradation when failure caused by the development of insecticide resist- the proper enzyme inhibitor is used.6,8) The second is ance. This insect pest has developed very high levels of that there is a possibility of improving the performance of resistance and a wide range of multiple-resistance to efficacy of insecticides,9) and also lower insecticide doses almost all the conventional insecticides used for control. might help to reduce the impact of insecticides to the Recently, reports on the development of resistance to environment. When insecticide mixtures show potentia- conventional insecticides, including BT formulations and tion in their joint action and/or if they can retard or insect growth regulators (IGRs) are increasing especially prevent the development of resistance, then application of in South East Asian countries and the U.S.A.1-5) these mixtures could be considered as a possible resist- Unfortunately, it is becoming increasingly difficult to ance management tool. find new compounds which are safe and highly in- In this study, synergism and joint action of seciticidal to overcome the problem of pest resistance to chlorfluazuron with other insecticides were investigated insecticides. Consequently, investigators are directing in chlorfluazuron-susceptible and resistant strains of their efforts to improve the effectiveness of existing prod- diamondback moth. ucts. Practically, this is possible through two ways, first by the use of synergists and second by the use of insecti- MATERIALS AND METHODS cides mixtures which may delay or retard the develop- Insects 1 Present address: Department of Entomology, Faculty of Two Thai strains of diamondback moth, Tup Luang Science, Amn Shams University, Abbasia, Cairo, Egypt. (TL) and Bang Khae (BK), were used for this study. At 224 日本農薬学会誌 第23巻 第3号 平成l0年8月 the time of collection, these two strains were 400- to for synergism studies or in distilled water containing 200 3400-fold resistant to chlorfluazuron and 37,500- to ppm of the spreading agent Linoh(R)for joint action 70,000-fold resistant to teflubenzuorn compared to a experiments. Four replicates were made for each, con- Japanese susceptible (OSS) strain (Sinchaisri et al., centration as well as for the controls. Mortality was unpublished data). These two stains were imported recorded one week after treatment for all mixtures and from Thailand after being reared in the laboratory for BPU or JHA applied singly. On the other hand it was two years without any insecticidal selection pressure. recorded after three days for all the other insecticides. At that time, their resistance ratio (RR) values were as Larvae or pupae which did not respond to pencil tip low as 16-62 to chlorfluazuron and 10-18 to prodding were judged as dead. teflubenzuron comparing to the same OSS strain(Fahmy et al., unpublished data). Subcolonies of the TL and Statistical Treatment of the Data BK strains were selected for chlorfluazuron resistance in Data were analyzed by the probit analysis11 with a the laboratory for 14 and 15 generations out of 21 genera- personal computer NEC PC-9801 VM (Nippon Electric tions. At that time, the RR values of the selected col- Co. Ltd., Tokyo). onies reached 318 and 303, respectively, compared to the Co-toxicity coefficient (CC) values of the binary insec- non-selected colonies. Furthermore, the selected-TL ticide mixtures were estimated using following formula and BK colonies were selected with chlorfluazuron for as proposed by Sun and Johnson.12) another 7 and 8 generations and their RR values reached Actual toxicity index of the mixture/ 570 and 300, respectively. Thus, in this paper, CC= x 100 chlorfluazuron selected and non-selected colonies were heoretical toxicity index of the mixture called TL-R and TL-S, and BK-R and BK-S strains, A CC value significantly higher than 100 indicates respectively. The TL-R and BK-R strains were occa- potentiation, a CC value close to 100 indicated a similar sionally selected with chlorfluazuron to maintain the action and antagonistic action is indicated by CC values resistance level high. The insects were reared at 25oC less than 100. under long-day photoperiod (16 light-8 dark). The rearing technique was the same as described before.10) RESULTS Early third instar larvae were used for experiments. Synergism Studies TPP and PB did not show any insecticidal activity Insecticides and Synergists under experimental conditions. The synergistic effect of Insecticides used in this study were chlorfluazuron TPP and PB on chlorfluazuron was tested in TL and BK (Atabron(R)) 5% EC, teflubenzuron (Nomolt(R)) 5% EC strains of diamondback moth and the results are shown (benzoylphenyl urea, BPU), pyriproxyfen (Sumilarv(R)) in Tables 1 and 2. In the TL-R strain, chlorfluazuron 10% EC (juvenile hormone analog, JHA), phenthoate was synergized more with TPP and PB. The LC50 of the (Elsan(R)) 50% EC (organophosphorus compound), resistant strain dropped from 271 ppm to 38 and 71 ppm fenvalerate (Sumicidin(R)) 20% EC () and with TPP and PB, respectively indicating synergistic thiodicarb (Larvin(R))technical grade 96.2% (1% solution ratio (SR) value of 7.1 and 3.8. On the other hand, no was prepared by dissolving in a mixture of acetone: clear synergism were recognized in the susceptible strain benzene:Newcol 863 at the ratio of 3:3:1, v/v) (car- with either compounds. Also in the BK-R strain, the bamate). Synergists used were triphenyl phosphate drop in the LC50 value was from 249 ppm to 36.5 and (TPP) (95%) and piperonyl butoxicide (PB) (100%). 62.8 ppm with TPP and PB, respectively indicating SR All insecticide preparations were diluted with water value of 6.8 and 3.9. However, PB has also exerted containing 200 ppm spreading agent Linoh(R)(Nihon some synergistic activity in the susceptible strain as Noyaku Co. Ltd., Tokyo) at the desired concentrations. well. Teflubenzuron, at the concentration of less than LC 1, Testing Technique was also tested for synergistic activity to chlorfluazuron. The leaf dipping technique was adopted.10) For It was found that teflubenzuron (at

Table 1 Synergism of chlorfluazuron by different compounds in the TL-S and TL-R strains of diamondback moth.

a) Synergistic ratio=LC of chlorfluazuron/LC of chlorfluazuron+synergist. b) 95% confidential interval.

Table 2 Synergism of chlorfluazuron by different compounds in the BK-S and BK-R strains of diamondback moth.

a) and b) as in Table 1.

Table 3 Susceptibility levels of the TL-S and TL-R strains of diamondback moth to different insecticides and cross-resistance levels.

a) Resistance ratio =LC of the resistant strain/LC of the susceptible strain, b) 95% confidential interval. 226 日本農薬学会誌 第23巻 第3号 平成10年8月

Table 4 Susceptibility levels of the BK-S and BK-R strains of diamondback moth to different insecticides and cross-resistance levels.

a) and b) as in Table 3.

Table 5 Susceptibility levels of the TL-S and TL-R strains of diamondback moth to insecticides mixtures and co-toxicity coefficient value.

a) Co-toxicity coefficient. b) 95% confidential interval. moth to chlorfluazuron have reached 570 and 300, respec- cides tested as clear from the RR values listed in Tables tively, compared with the susceptible (non-selected) 3 and 4. strains. This difference in the RR values between two The TL and BK strains of diamondback moth were strains was partially due to the difference in the suscepti- tested against binary mixtures of insecticides in order to bility levels of the TL-S and BK-S strains since LC5o assess the joint action of these binary mixtures by estimat- values of the TL-R and BK-R strains were very close, 271 ing the CC values of each mixture. The results of this and 249 ppm, respectively (Tables 3 and 4). test are listed in Tables 5 and 6. The TL-R and BK-R strains have shown some cross- Joint action, expressed by the CC values, was only resistance to teflubenzuron with RR values of 31.7 and high with mixtures of chlorfluazuron+teflubenzuron 16.5, respectively (at the LC50 level). Also at the LC95 and chlorfluazuron+pyriproxyfen in both TL and BK level, the RR values were high (37 and 46 for the TL and strains. Joint action was higher in the resistant strains BK strains, respectively). A very low level of cross- than in the susceptible ones. In the TL strain, CC value resistance (at the LC50 level) to pyriproxyfen (JHA) was with chlorfluazuron+teflubenzuron mixture were 692 recognized especially in the TL strain. However, the and 1290 in the susceptible and resistant strains, respec- RR value at the LC95 level for both strains showed no tively. Also for chlorfluazuron+pyriproxyfen, the CC evidence for cross-resistance to this compound. Also values were 1450 and 1940 in the susceptible and resistant there was no cross-resistance to any of the other insecti- strains, respectively. The situation with the BK strains Journal of Pesticide Science 23 (3) August 1998 227

Table 6 Susceptibility levels of the BK-S and BK-R strains of diamondback moth to insecticides mixtures and co-toxicity coefficient value.

a)and b)as in Table 5. was not different from that in the TL strain. The CC that cytochrome P450 monooxygenase is the primary values were 492 and 1080 for the chlorfluazuron+ factor for resistance in these compounds. However teflubenzuron mixture and 926 and 1830 for the addition of MGK 264, another cytochrome P450monoox- chlorfluazuron+pyriproxyfen mixture in the susceptible ygenase inhibitor, was less effective in synergizing and resistant strains, respectively. On the other hand, teflubenzuron in diamondback moth.17) Thus, the exact the CC values for the other mixtures in both strains have situation does not seem to be clear since synergism in the shown similar or independent action with no sign of susceptible strains of the same populations was not tested potentiation evidenced by the CC values being close to or in the last two reports by Pern et al.17) and Cheng et less than 100 as shown in Tables 5 and 6. al.18) Therefore the involvement of these enzyme sys- tems in the resistance mechanisms is not conclusive unless DISCUSSION it is confirmed that the same synergist does not enhance Generally, synergism studies have been reported main- the insecticidal activity in the susceptible individuals. ly as inhibition of metabolic detoxification of Synergism of BPUs in different insect species by different insecticides.13) These studies are usually useful for the compounds is well documented. For example, Prim- prediction of resistance mechanisms to conventional pricar and Georghiou19) stated that was insecticides6,7,13,14)as well as to BPUs.9,15,16)The remark- synergized by PB and , cytochrome P450monoox- able enhancement of the toxicity of chlorfluazuron by ygenase inhibitors, in Musca domestica and the SR TPP in the chlorfluazuron-resistant strains compared values were significantly higher in the diflubenzuron- with susceptible strains suggests the possibility that a resistant strain than in the susceptible strain, indicating a TPP-sensitive enzyme system (s) might be involved in the significant role for cytochrome P450enzymes in resistance chlorfluazuron resistance mechanism in this insect pests. to this compound. TPP is a typical carboxylesterase inhibitor, thus the exact Addition of teflubenzuron at the concentration of less nature and specifications of this enzyme system (s) have than LC 1 level (to eliminate any lethal effect caused by yet to be clarified. Qualitative and/or quantitative teflubenzuron), remarkably increased chlorfluazuron tox- difference in metabolic enzyme systems between the sus- icity. The possible explanation for that might be the ceptible and the resistant insects may explain the higher interference with chlorfluazuron degradation enzyme, synergistic ratios obtained in the resistant strains than in since the SR of teflubenzuron (at

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