942

Journal of Food Protection, Vol. 75, No. 5, 2012, Pages 942–950 doi:10.4315/0362-028X.JFP-11-397 Copyright G, International Association for Food Protection

Efficacy of Insect Growth Regulators as Grain Protectants against Two Stored-Product Pests in Wheat and Maize

NICKOLAS G. KAVALLIERATOS,1* CHRISTOS G. ATHANASSIOU,2 BASILEIOS J. VAYIAS,3 AND Zˇ ELJKO TOMANOVIC´ 4

1Laboratory of Agricultural Entomology, Department of Entomology and Agricultural Zoology, Benaki Phytopathological Institute, 8 Stefanou Delta str., 2

14561, Kifissia, Attica, Greece; Laboratory of Entomology and Agricultural Zoology, Department of Agriculture, Crop Production and Rural Environment, Downloaded from http://meridian.allenpress.com/jfp/article-pdf/75/5/942/1686621/0362-028x_jfp-11-397.pdf by guest on 27 September 2021 University of Thessaly, Phytokou str., Nea Ionia, 38446, Magnissia, Greece; 3Ministry of Rural Development and Food, General Directorate of Plant Produce, Directorate of Plant Produce Protection, 150 Syggrou Avenue, 17671, Kallithea, Greece; and 4Institute of Zoology, Faculty of Biology, University of Belgrade, Studentski trg 16, 11000, Belgrade, Serbia

MS 11-397: Received 27 August 2011/Accepted 2 December 2011

ABSTRACT Insect growth regulators (IGRs) (two juvenile hormone analogues [ and pyriproxifen], four chitin synthesis inhibitors [, flufenoxuron, , and triflumuron], one ecdysteroid agonist [methoxyfenozide], and one combination of chitin synthesis inhibitors and juvenile hormone analogues [lufenuron plus fenoxycarb]) were tested in the laboratory against adults of Prostephanus truncatus in maize and against adults of Rhyzopertha dominica in wheat. The tested IGRs were applied in maize at three doses (1, 5, and 10 ppm) and assessed at three temperature levels (20, 25, and 30uC) in the case of P. truncatus, while in the case of R. dominica the above doses were assessed only at 25uC in wheat. In addition to progeny production, mortality of the treated adults after 14 days of exposure in the IGR-treated commodities was assessed. All IGRs were very effective (.88.5% suppression of progeny) against the tested species at doses of $5 ppm, while diflubenzuron at 25uCin the case of P. truncatus or lufenuron and in the case of R. dominica completely suppressed (100%) progeny production when they were applied at 1 ppm. At all tested doses, the highest values of R. dominica parental mortality were observed in wheat treated with lufenuron plus fenoxycarb. Temperature at the levels examined in the present study did not appear to affect the overall performance in a great extent of the tested IGRs in terms of adult mortality or suppression of progeny production against P. truncatus in treated maize. The tested IGRs may be considered viable grain protectants and therefore as potential components in stored-product integrated pest management.

Insect growth regulators (IGRs) consist of a group of The use of ecdysteroid agonists generates the premature that disrupt the normal development of insects synthesis of the insect’s cuticle especially close to the area and consequently affect development, reproduction, and of the head, causing feeding inhibition irrespectively of the behavior (40, 42, 44). They are classified as juvenile age or instar of the insect (19, 48, 55). These compounds hormone analogues (JHAs), ecdysteroid agonists, and chitin show chemosterilant activity of females (20), act both synthesis inhibitors (CSIs) (42, 44). Due to their mode of through stomach and contact (19), and can also penetrate the action, IGRs act against the immature stages of insects by insect’s cuticle (48). inhibiting metamorphosis and consequently insect prolifer- CSIs prevent the synthesis of new cuticle, and thus, the ation on the infested commodity (42). These insecticides insects are not capable of proceeding into moulting, or specifically act against insects and have low mammalian they form abnormal cuticle (23, 40). They also affect the toxicity (39, 40, 42, 44). hormonal status of the treated insects and thus several JHAs are responsible for the prolongation of the larval physiological functions (23, 40, 46, 56). stage of insects (36). They act on the metamorphic change The above characteristics have resulted in the classifi- of the treated larvae, producing deformed pupae (40, 42), cation of IGRs as ‘‘low-risk’’ insecticides and raised interest and they also block the completion of embryonic develop- for their evaluation as potential integrated pest management ment (44). Furthermore, they affect the reproduction of (IPM) components (19, 30). So far, only two forms of treated adults by influencing vitellogenesis, development of the IGR (methoprene containing the R and S follicles, protein synthesis in ovaries (29), sexual commu- isomers and s-methoprene containing the S isomer alone) nication (52), or mating performance (49). JHAs may (8) or are used as grain protectants in the United States, with may not (54) reduce the fecundity of adults when they are label doses from 1 to 5 ppm (3, 5, 6, 54). In Australia applied on their larvae or pupae. s-methoprene is registered at the label dose of 0.6 ppm for a 9-month grain protection (11, 13). * Author for correspondence. Tel: z30-2108180215; Fax: z30-2108077506; The IGRs fenoxycarb, pyriproxifen, diflubenzuron, E-mail: [email protected]. flufenoxuron, lufenuron, triflumuron, and methoxyfenozide J. Food Prot., Vol. 75, No. 5 EFFICACY OF INSECT GROWTH REGULATORS AGAINST STORED-PRODUCT PESTS 943 are commercially produced for use against insect pests in the treated diet increased dramatically for doses from 5 to various agroecosystems (31, 33, 34, 37, 45, 50). Several 25 ppm compared with the controls. studies have shown the potentiality of these compounds Prostephanus truncatus (Horn) (Coleoptera: Bostrychi- against stored-grain insect pests. Thind and Edwards (53) dae) and R. dominica are considered as major pests of stored found in laboratory experiments that 1 ppm of fenoxycarb maize and cassava or stored grains, respectively (21, 24). mixed with the food source caused complete inhibition of They are classified as primary pests, a fact that means that adult emergence of -susceptible or -resistant strains they are capable of infesting unbroken grain kernels. of Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae), Although there are reports on the use of IGRs as grain Cryptolestes ferrufineus (Stephens) (Coleoptera: Laemoph- protectants, very little information is available on the loeidae), and Oryzaephilus surinamensis (L.) (Coleoptera: simultaneous evaluation of a wide range of IGRs (i.e., JHAs, Silvanidae) after 10, 8, and 7 weeks of exposure, respectively. CSIs, and ecdysteroid agonists) on both parental adult Later, Edwards et al. (16) showed that 4.2 ppm of fenoxycarb mortality and progeny production of P. truncatus and R. applied on wheat in bins controlled O. surinamensis, dominica. The objective of the present study was to test in the Downloaded from http://meridian.allenpress.com/jfp/article-pdf/75/5/942/1686621/0362-028x_jfp-11-397.pdf by guest on 27 September 2021 Rhyzopertha dominica (F.) (Coleoptera: Bostrychidae), and laboratory the insecticidal efficacy of IGRs, i.e., two JHAs T. castaneum for a period of 2 years. Bu¨chi (7) evaluated (fenoxycarb and pyriproxifen), four CSIs (diflubenzuron, fenoxycarb, mixed with food at 4, 8, and 16 ppm, against flufenoxuron, lufenuron, and triflumuron), one ecdysteroid Liposcelis bostrychophila Badonnel (Psocoptera: Liposcelidi- agonist (methoxyfenozide), and one combination of CSI and dae) and showed that it reduced considerably the adult JHA (lufenuron plus fenoxycarb) as grain protectants against production after 4, 6, and 8 weeks of exposure. However, the P. truncatus in maize in different doses and at different maximum reduction of the number of nymphs was 70.0% after temperature levels. The performance of the above IGRs was 8 weeks of exposure. Furthermore, fenoxycarb caused also evaluated against R. dominica in wheat. reduction in adult fertility and hatching of the eggs of L. bostrychophila. Kostyukovsky et al. (30) reported that 0.1 ppm MATERIALS AND METHODS of pyriproxyfen applied in wheat flour inhibited completely the Insects. The insects tested were P. truncatus and R. dominica. F1 adults of strains of T. castaneum susceptible or resistant to P. truncatus was reared on whole maize, and R. dominica pirimiphos-methyl. At 2.5 ppm, pyriproxifen caused 97% was reared on whole wheat. All species that were used in the reduction of F1 adults of a susceptible strain of Sitophilus experiments were obtained from the laboratory cultures of Benaki oryzae (L.) (Coleoptera: Curculionidae) in treated wheat. Phytopathological Institute at 25uC with 70% relative humidity Athanassiou et al. (4) reported significant reduction on the and continuous darkness. For the bioassays, only adults were used, numbers of adults and nymphs of L. bostrychophila, Liposcelis ,4 weeks old. decolor (Pearman) (Psocoptera: Liposcelididae), and Liposce- lis paeta Pearman (Psocoptera: Liposcelididae) in comparison Formulations. The IGR formulations that were screened in the present study were Admiral EC containing 10% pyriproxyfen as the to the untreated controls 35 days after exposure on concrete 2 active ingredient (AI) (provided by Hellafarm, Amaroussion, Greece), arenas with the label rate of 2.3 mg of active ingredient per m . Cascade DC containing 10% flufenoxuron (AI) (provided by BASF, Desmarchelier and Allen (15) showed that there was no Aghia Paraskevi, Greece), Runner SC containing 24% methoxyfe- progeny of Sitophilus granarius (L.) (Coleoptera: Curculioni- nozide (AI) (provided by Bayer, Amaroussion, Greece), Alsystin SC dae) and S. oryzae adults after their exposure for a second 2- containing 48% triflumuron (AI) (provided by Bayer), Match EC week period in wheat treated with diflubenzuron at concen- containing 5% lufenuron (AI) (provided by Syngenta, Anthousa, trations ranging from 0.6 to 9.0 ppm. Ammar (2) evaluated Greece), Helgar WG containing 25% fenoxycarb (AI) (provided by flufenoxuron against S. oryzae in treated wheat and found that Hellafarm), Lufox EC containing 7.5% fenoxycarb and 3% lufenuron (AI) (provided by Syngenta), and Dimilin WP containing 25% after 8 months posttreatment the F1 progeny reduction was diflubenzuron (AI) (provided by Dupont, Halandri, Greece). 92.9 or 96.3%,whereastheF2 was95.9or100% at 5 or 25 ppm, respectively. Mahanthi (35), testing lufenuron and Commodities. Untreated, clean maize (Zea mays L. var. diflubenzuron as stored-maize protectants, showed that they Dias) and hard wheat (Triticum durum Desf. var. Mexa) were used inhibited completely the adult emergence of S. oryzae and in the tests. The moisture contents of the tested commodities were controlled completely Corcyra cephalonica Stainton (Lepi- 12.1 and 11.2% for maize and wheat, respectively, as determined doptera: Pyralidae). Eisa and Ammar (17) by testing the by a moisture meter (Dickey-John Multigrain CAC II, Dickey-John residual performance of triflumuron, fenoxycarb, and flufe- Co., Auburn, IL) upon the beginning of the tests. noxuron in wheat against S. oryzae found that 50 or 100 ppm of these compounds provided complete control for a period of Bioassay series 1. In the first series of bioassays, the tested 2 years. Triflumuron and flufenoxuron controlled completely IGRs were separately applied as solutions in 1-kg lots of maize at S. oryzae in treated wheat at 1 and 10 ppm for a period of three doses: 1, 5, and 10 ppm. Spraying was carried out on a tray, 9 months, whereas fenoxycarb gave the same results at 10 ppm where 1 kg of maize, spread into a thin layer, was treated with 3 ml of an aqueous solution that contained the appropriate volume of for a 12-month posttreatment period. Oberlander et al. (43) each IGR formulation corresponding to each dose. Spraying was reported that the weight of larvae of Plodia interpunctella carried out with an AG-4 airbrush (Mecafer, Valence, France). (Hu¨bner) (Lepidoptera: Pyralidae) exposed in cereal food Furthermore, an additional 1-kg lot of maize was sprayed with 3 ml source treated with 10 and 25 ppm of methoxyfenozide of distilled water and served as control. After spraying, the maize increased 50% compared with the increase of 400% of the lots were placed into 5-liter glass jars and were manually shaken controls over 3 days. Furthermore, the mortality of the larvae in for 10 min to achieve equal distribution of the insecticide in the 944 KAVALLIERATOS ET AL. J. Food Prot., Vol. 75, No. 5 entire grain mass (25). Next, three samples, each of them weighing P , 0.01; for temperature, F ~ 4.4, df ~ 2, 647, P ~ 0.02) 30 g, were obtained from each treated (or untreated) maize lot and were significant, while all associated interactions (for IGR placed inside glass vials (7.5-cm diameter, 12.5-cm height). The | dose, F ~ 1.7, df ~ 14, 647, P ~ 0.06; for IGR | closure of the vials had a 1.5-cm-diameter hole in the middle temperature, F ~ 1.4, df ~ 14, 647, P ~ 0.13; for dose | covered by gauze for sufficient aeration inside the vial. Thirty temperature, F ~ 1.6, df ~ 4, 647, P ~ 0.18) were not adults of P. truncatus were added in each vial, and the vials were significant for mortality levels of parental P. truncatus inserted in incubators set at 25uC. Following this, all vials were individuals in maize treated with IGRs. Parental mortality of placed in incubators set at the desired level of temperature each P. truncatus in maize treated with the tested IGRs was time. The tested levels of temperature were 20, 25, and 30uC, while relative humidity was maintained at 65% during the entire generally low since it did not exceed 27.5% when experimental period of this bioassay series. Parental mortality flufenoxuron was applied at 10 ppm at 30uC (Table 1). was assessed after a period of 14 days of exposure, while all Temperature did not have significant influence in the parental individuals (dead and alive) were removed from the vials parental mortality of P. truncatus with the exception of and the vials were again placed in the incubators for an additional lufenuron plus fenoxycarb at 5 and 10 ppm, where Downloaded from http://meridian.allenpress.com/jfp/article-pdf/75/5/942/1686621/0362-028x_jfp-11-397.pdf by guest on 27 September 2021 period of 60 days under the same conditions as described above. significantly fewer individuals were killed at 20uC than at Next, the vials were opened again and the adult progeny was 30uC (Table 1). At 1 ppm, the parental mortality did not counted. The entire procedure was repeated three times for each vary significantly inside each tested temperature level species by preparing new maize lots each time. (Table 1). Similarly, at 5 and 10 ppm, the mortality of the Parental mortality rates in control groups were 5.5, 4.2, parental P. truncatus individuals did not vary significantly and 4.9% at 20, 25, and 30uC, respectively. Therefore, parental inside 20 or 25uC and 25uC, respectively. mortality data were transformed according to Abbott’s formula (1). ~ ~ Parental mortality data and progeny production data were subjected All main effects (for IGR, F 57.0, df 7, 647, P , ~ ~ to the same transformations as those used in bioassay series 1. The 0.01; for dose, F 44.7, df 2, 647, P , 0.01; for transformed mortality data were submitted to a three-way analysis temperature, F ~ 51.1, df ~ 2, 647, P ~ 0.02) and their of variance, with IGR, temperature, and dose as main effects. interactions (for IGR | dose, F ~ 2.5, df ~ 14, 647, P , Similarly, the transformed progeny production counts were submitted 0.01; for IGR | temperature, F ~ 5.4, df ~ 14, 647, P , to a three-way analysis of variance, with IGR, temperature, and dose 0.01) were significant, with the exception of dose | as main effects. All analyses were done using the JMP software (47). temperature (F ~ 1.6, df ~ 4, 647, P ~ 0.17), which was Means were separated by the Tukey-Kramer honestly significant not significant for progeny production of P. truncatus in difference (HSD) test with P valuessetat0.05(51). A preliminary maize treated with IGRs. The tested IGRs caused suppres- Dunnett’s test was used to examine the existence of significant sion from 86.4 to 100% of progeny production of P. differences in progeny production between control groups and IGR- truncatus individuals (Table 2). Of the IGRs that were treated maize for each of the tested temperature levels. Since Dunnett’s examined here, diflubenzuron was the most effective since it test showed that control progeny was always statistically higher than almost completely suppressed progeny in all of the tested the progeny that emerged in IGR-treated maize, control groups were not incorporated to the analyses of progeny production data. cases (from 99.4 to 100%) (Table 2). The less effective tested IGRs were lufenuron, lufenuron plus fenoxycarb Bioassay series 2. In the second series of bioassays, the IGRs or triflumuron at 1 ppm, lufenuron or pyriproxifen at 5 were applied in hard wheat and evaluated against R. dominica at ppm, and lufenuron plus fenoxycarb at 10 ppm, causing 25uC following the same procedure as described for bioassay series suppression of progeny production between 89.2 and 94.7% 1. The parental mortality and progeny production counts were (Table 2). Temperature had a significant impact on the recorded as described above. suppression of progeny production when flufenoxuron, Parental mortality in control groups was low and did not exceed pyriproxifen, and triflumuron were applied at 1 and 5 ppm, 5%. However, parental mortality data were corrected according to while it significantly affected the performance of fenoxycarb Abbott’s formula (1). The mortality of parental individuals and when it was applied at 1 ppm (Table 2). When fenoxycarb progeny production data were analyzed separately for each species. or pyriproxifen were applied at 1 ppm, significantly more Prior to analysis, mortality data were arcsine transformed, while progeny were suppressed at 20 C than at 25 or 30 C. In the progeny production data were subjected to log (x z 1) u u transformation in order to achieve homogeneity of variances. The case of flufenoxuron at the same dose, significantly more transformed mortality data were submitted to a two-way analysis of progeny were suppressed at 20 or 25uC than at 30uC, while variance, with IGR and dose as main effects. Similarly, the for triflumuron at the same dose progeny was significantly transformed progeny production counts were submitted to a two- suppressed at 20 or 30uC than at 25uC. The fact that way analysis of variance, with IGR and dose as main effects. All significantly more progeny were recorded at 25uC than at 20 analyses were done using the JMP software (47). Means were or 30uC was also observed when flufenoxuron or triflu- separated by the Tukey-Kramer HSD test with P values set at 0.05 muron was applied at 5 ppm, while when pyriproxifen was (51). Control progeny data were not incorporated in the progeny applied at the same dose significantly more progeny were production analysis because a preliminary Dunnett’s test showed suppressed at 20uC than at 25 or 30uC (Table 2). However, that progeny production in control groups was always significantly when the IGRs were applied at 10 ppm, temperature was not higher than that recorded in the IGR-treated wheat. significantly associated with the progeny suppression in the treated maize (Table 2). RESULTS Bioassay series 1. All main effects (for IGR, F ~ 9.9, Bioassay series 2. All main effects (for IGR, F ~ 18.4, df ~ 7, 647, P , 0.01; for dose, F ~ 35.5, df ~ 2, 647, df ~ 7, 215, P , 0.01; for dose, F ~ 48.9, df ~ 2, 215, J. Food Prot., Vol. 75, No. 5 EFFICACY OF INSECT GROWTH REGULATORS AGAINST STORED-PRODUCT PESTS 945

TABLE 1. Mortality of P. truncatus adults after 14 days of exposure in maize treated with seven IGRs and one combination of IGRs at three doses and at three temperaturesa

Temp (uC):

Dose (ppm) IGR 20 25 30

1 Diflubenzuron 8.6 ¡ 3.1 A a 1.1 ¡ 0.7 A a 2.1 ¡ 1.1 A a Fenoxycarb 3.5 ¡ 1.6 A a 4.8 ¡ 1.5 A a 6.0 ¡ 2.0 A a Flufenoxuron 8.1 ¡ 5.8 A a 3.1 ¡ 1.1 A a 5.6 ¡ 1.7 A a Lufenuron 6.4 ¡ 1.4 A a 4.6 ¡ 1.5 A a 1.8 ¡ 1.1 A a Lufenuron z fenoxycarb 5.6 ¡ 1.9 A a 7.0 ¡ 1.9 A a 8.8 ¡ 2.5 A a Methoxyfenozide 0.9 ¡ 0.9 A a 2.2 ¡ 1.2 A a 1.2 ¡ 0.8 A a Pyriproxyfen 1.7 ¡ 1.3 A a 0.7 ¡ 0.3 A a 3.5 ¡ 2.8 A a Triflumuron 2.6 ¡ 0.9 A a 4.6 ¡ 1.4 A a 2.8 ¡ 1.5 A a Downloaded from http://meridian.allenpress.com/jfp/article-pdf/75/5/942/1686621/0362-028x_jfp-11-397.pdf by guest on 27 September 2021 5 Diflubenzuron 1.7 ¡ 1.3 A a 3.9 ¡ 1.3 A a 5.6 ¡ 1.3 A bc Fenoxycarb 7.3 ¡ 1.8 A a 10.2 ¡ 2.0 A a 9.3 ¡ 2.5 A bc Flufenoxuron 9.0 ¡ 4.2 A a 4.8 ¡ 2.0 A a 10.4 ¡ 2.9 A bc Lufenuron 4.3 ¡ 1.8 A a 9.2 ¡ 1.7 A a 4.6 ¡ 1.3 A ab Lufenuron z fenoxycarb 6.9 ¡ 2.6 A a 8.5 ¡ 3.7 AB a 18.0 ¡ 2.4 B bc Methoxyfenozide 5.2 ¡ 1.3 A a 2.6 ¡ 1.2 A a 0.3 ¡ 0.2 A a Pyriproxyfen 3.0 ¡ 1.7 A a 6.1 ¡ 1.6 A a 8.8 ¡ 1.9 A ab Triflumuron 3.4 ¡ 1.4 A a 3.1 ¡ 1.7 A a 3.8 ¡ 2.3 A ab

10 Diflubenzuron 4.3 ¡ 2.3 A ab 12.4 ¡ 3.3 A a 10.9 ¡ 3.2 A ab Fenoxycarb 9.0 ¡ 2.9 A ab 7.2 ¡ 2.7 A a 10.7 ¡ 3.1 A ab Flufenoxuron 19.3 ¡ 4.1 A b 18.5 ¡ 4.0 A a 27.5 ¡ 6.0 A b Lufenuron 12.0 ¡ 2.8 A ab 13.5 ¡ 4.8 A a 9.1 ¡ 2.7 A ab Lufenuron z fenoxycarb 8.2 ¡ 2.7 A ab 12.4 ¡ 2.4 A a 21.5 ¡ 1.4 B b Methoxyfenozide 6.0 ¡ 2.9 A ab 8.9 ¡ 3.0 A a 10.9 ¡ 2.2 A ab Pyriproxyfen 5.6 ¡ 2.0 A ab 8.1 ¡ 3.8 A a 13.8 ¡ 3.4 A ab Triflumuron 3.9 ¡ 2.2 A a 7.8 ¡ 2.4 A a 3.8 ¡ 1.9 A a a Values are mean percentages ¡ standard errors. For each IGR or combination of IGRs, within each dose, means followed by the same uppercase letter are not significantly different; in all cases, df ~ 2, 26 (Tukey-Kramer HSD test; P ~ 0.05). Within each temperature and dose, means followed by the same lowercase letter are not significantly different; in all cases, df ~ 7, 71 (Tukey-Kramer HSD test; P ~ 0.05).

P , 0.01) and associated interaction (for IGR | dose, F ~ suppression of R. dominica progeny (59.2%) than did the 3.2, df ~ 14, 215, P , 0.01) for mortality levels of parental remainder of the tested IGRs at 1 ppm, suppression of individuals of R. dominica were significant in wheat treated progeny production of this species was not significantly with IGRs. Mortality of treated parental R. dominica adults differentiated inside the 1-ppm dose of the remainder of the ranged from 0.3 to 55.7%, and it was dose dependent. tested IGRs, and it ranged from 88.6 to 100% (Table 4). However, in the cases of fenoxycarb and methoxyfenozide the parental mortality was not significantly differentiated DISCUSSION among the tested doses (Table 3). At all tested doses, Through the use of IGRs, suppression of progeny the highest values of parental mortality were observed in production of stored-product insect pests can be achieved. wheat treated with lufenuron plus fenoxycarb but without For instance, Daglish (10) reported 99.6% suppression significant difference compared with fenoxycarb or lufe- of progeny production of R. dominica in maize treated nuron at 1 ppm; fenoxycarb, lufenuron, or triflumuron at with 10 ml of solution of an emulsifiable concentrate of 5 ppm; and fenoxycarb, flufenoxuron, lufenuron, pyriproxy- methoprene during 6 months of storage, while Kostyu- fen, or triflumuron at 10 ppm (Table 3). kovsky et al. (30) showed complete F1 reduction of a All main effects (for IGR, F ~ 14.5, df ~ 7, 215, P , pirimiphos-methyl–susceptible strain of the same species 0.01; for dose, F ~ 14.0, df ~ 2, 215, P , 0.01) and in wheat treated with 3 ppm of methoprene. Elek and | ~ ~ associated interaction (for IGR dose, F 16.7, df 14, Longstaff (18) reported complete F1 progeny production of 215, P , 0.01) were significant for progeny production of R. the same species after 2 weeks of exposure of parental dominica in wheat treated with IGRs. Progeny production of adults in wheat treated with 0.5 ppm of chlorfluazuron, R. dominica in treated wheat was very low and did not exceed teflubenzuron, and flufenoxuron. In light of the results of one adult per vial when the tested IGRs were applied at 5 or the present study, all IGR treatments were effective at 10 ppm. Fenoxycarb, methoxyfenozide, and triflumuron were doses of $5 ppm against both of the tested species since the least effective IGRs compared with the remainder of the suppression of progeny production was consistently higher tested IGRs when the last two were applied at 5 ppm and than 88.5%. Similar results have been reported by Thind fenoxycarb was applied at 10 ppm (Table 4). Except for and Edwards (53), who found that 5 ppm of fenoxycarb lufenuron plus fenoxycarb, which caused significantly lower mixed with wheat reduced completely the adult emergence 946 KAVALLIERATOS ET AL. J. Food Prot., Vol. 75, No. 5

TABLE 2. Number of P. truncatus adults per vial in maize treated with seven IGRs and one combination of two IGRs at four doses (inclusive of 0 ppm), 60 days after the removal of the parental adults, and percent suppression of P. truncatus adults in comparison with controlsa

Mean no. ¡ SE % suppression

Dose (ppm) IGR 20uC25uC30uC20uC25uC30uC

0 Control 25.0 ¡ 1.6 A 27.2 ¡ 1.2 A 33.8 ¡ 1.8 B

1 Diflubenzuron 0.1 ¡ 0.1 A a 0.0 ¡ 0.0 A a 0.2 ¡ 0.1 A a 99.6 100.0 99.4 Fenoxycarb 0.4 ¡ 0.2 A a 1.6 ¡ 0.2 B bc 2.2 ¡ 0.3 B b 98.4 94.1 93.5 Flufenoxuron 0.6 ¡ 0.2 A a 1.2 ¡ 0.3 A b 1.8 ¡ 0.3 B b 97.6 95.6 94.7 Lufenuron 2.7 ¡ 0.6 A c 3.3 ¡ 0.4 A d 2.4 ¡ 0.4 A b 89.2 87.9 92.9 Lufenuron z fenoxycarb 2.3 ¡ 0.6 A bc 2.8 ¡ 0.3 A c 3.2 ¡ 0.5 A b 90.8 89.7 90.5 ¡ A ¡ A ¡ A Methoxyfenozide 1.0 0.4 ab 1.0 0.3 b 1.9 0.4 b 96.0 96.3 94.4 Downloaded from http://meridian.allenpress.com/jfp/article-pdf/75/5/942/1686621/0362-028x_jfp-11-397.pdf by guest on 27 September 2021 Pyriproxyfen 0.9 ¡ 0.3 A ab 2.8 ¡ 0.4 B c 2.2 ¡ 0.4 B b 96.4 89.7 93.5 Triflumuron 2.2 ¡ 0.3 A bc 3.7 ¡ 0.3 B d 2.1 ¡ 0.4 A b 91.2 86.4 93.8

5 Diflubenzuron 0.0 ¡ 0.0 A a 0.0 ¡ 0.0 A a 0.0 ¡ 0.0 A a 100.0 100.0 100.0 Fenoxycarb 0.7 ¡ 0.3 A a 1.1 ¡ 0.3 A b 1.2 ¡ 0.3 A b 97.2 96.0 96.4 Flufenoxuron 0.0 ¡ 0.0 A a 1.0 ¡ 0.3 B b 0.3 ¡ 0.3 A b 100.0 96.3 99.1 Lufenuron 2.4 ¡ 0.5 A b 2.2 ¡ 0.3 A c 2.3 ¡ 0.4 A b 90.4 91.9 93.2 Lufenuron z fenoxycarb 0.8 ¡ 0.3 A a 1.7 ¡ 0.3 A bc 1.6 ¡ 0.4 A b 96.8 93.8 95.3 Methoxyfenozide 0.9 ¡ 0.4 A a 0.9 ¡ 0.3 A b 1.2 ¡ 0.3 A b 96.4 96.7 96.4 Pyriproxyfen 0.7 ¡ 0.2 A a 2.2 ¡ 0.2 B c 2.3 ¡ 0.5 B b 97.2 91.9 93.2 Triflumuron 0.3 ¡ 0.2 A a 3.1 ¡ 0.1 B d 1.2 ¡ 0.4 A b 98.8 88.6 96.4

10 Diflubenzuron 0.0 ¡ 0.0 A a 0.0 ¡ 0.0 A a 0.0 ¡ 0.0 A a 100.0 100.0 100.0 Fenoxycarb 0.4 ¡ 0.2 A ab 0.9 ¡ 0.3 A abc 1.1 ¡ 0.3 A b 98.4 96.7 96.7 Flufenoxuron 0.0 ¡ 0.0 A a 0.2 ¡ 0.1 A ab 0.9 ¡ 0.4 A ab 100.0 99.3 97.3 Lufenuron 1.0 ¡ 0.5 A b 1.4 ¡ 0.4 A bc 1.3 ¡ 0.3 A b 96.0 94.9 95.9 Lufenuron z fenoxycarb 1.8 ¡ 0.6 A b 2.0 ¡ 0.3 A c 1.8 ¡ 0.2 A b 92.8 92.6 94.7 Methoxyfenozide 0.7 ¡ 0.2 A ab 0.8 ¡ 0.2 A abc 1.2 ¡ 0.2 A b 97.2 97.1 96.4 Pyriproxyfen 0.9 ¡ 0.3 A ab 1.3 ¡ 0.4 A bc 1.3 ¡ 0.2 A b 96.4 95.2 96.2 Triflumuron 0.8 ¡ 0.4 A ab 1.0 ¡ 0.3 A abc 1.1 ¡ 0.3 A b 96.8 96.3 96.7 a Within a specific IGR or combination of IGRs and dose, means followed by the same uppercase letter are not significantly different. For each IGR or combination of IGRs, within dose, means followed by the same uppercase letter are not significantly different; in all cases, df ~ 2, 26 (Tukey-Kramer HSD test; P ~ 0.05). Within each dose and temperature, means followed by the same lowercase letter are not significantly different; in all cases, df ~7, 71 (Tukey-Kramer HSD test; P ~ 0.05). For all temperatures and IGRs or combination of IGRs, progeny in untreated maize was significantly higher than that recorded in treated maize; in all cases, df ~ 1, 17 (Dunnett’s test; P ~ 0.05). of a strain of R. dominica susceptible to insecticides Despite the fact that lufenuron or pyriproxyfen 12 weeks after exposure, whereas in the case of the resistant appeared to be the most effective of the tested IGRs against strain the reduction was 96%. However, for some of the R. dominica, this was not the case when the former was tested IGRs high efficacy levels were recorded even with applied as a mixture with fenoxycarb, where progeny was 1 ppm. In the case of R. dominica, 1 ppm of lufenuron or suppressed only by 59.2% in wheat treated with 1 ppm. pyriproxyfen completely inhibited progeny emergence in Based on our results, a negative interaction between wheat. At the same dose, diflubenzuron caused 98.5% fenoxycarb and lufenuron is apparent in the case of R. suppression of production while in the case of P. truncatus, dominica when these IGRs are applied as a combination in more than 99% suppression in progeny production was wheat at 1 ppm since the effectiveness of this mixture was observed in maize at all three tested temperature levels. significantly lower than that recorded with either lufenuron Similarly, 1 ppm of pyriproxyfen induced 99.7% reduction or fenoxycarb alone. The modes of insecticidal action of of F1 adults of R. dominica in treated wheat (30), whereas lufenuron and fenoxycarb differ because the former is a CSI 1 ppm of diflubenzuron inhibited completely the progeny and the latter is a JHA. Based on the percentage of each production of the same species for a period of 8 months of substance to the tested mixture, this treatment comprised storage (38). 7.5% fenoxycarb and 3% lufenuron, so we could assume that Furthermore, Arthur (3) found that 1 ppm of s- the mode of action of this formulation was based to a greater methoprene was also capable of suppressing completely extent on fenoxycarb than on lufenuron. Although further the F1 progeny of R. dominica in treated wheat for a period investigation is required to test this hypothesis, the fact that from 6 to 18 months after storage. The same reduction of fenoxycarb at 1 ppm showed the lowest performance of the progeny of R. dominica was noted by Mian and Mulla (38) tested IGRs against R. dominica may explain the reduced when wheat was treated with 1 ppm of methoprene for a performance that was also observed in the mixture of period of 10 months posttreatment. fenoxycarb with lufenuron against this species. J. Food Prot., Vol. 75, No. 5 EFFICACY OF INSECT GROWTH REGULATORS AGAINST STORED-PRODUCT PESTS 947

TABLE 3. Mortality of R. dominica adults after 14 days of exposure in wheat treated with seven IGRs and one combination of two IGRs at three dosesa

Mean % mortality ¡ SE at each dose

IGR 1 ppm 5 ppm 10 ppm

Diflubenzuron 0.3 ¡ 0.2 A a 5.6 ¡ 1.5 B ab 13.2 ¡ 1.3 C ab Fenoxycarb 23.3 ¡ 5.3 A c 24.9 ¡ 3.8 A bc 27.2 ¡ 4.9 A abc Flufenoxuron 4.0 ¡ 2.4 A ab 3.9 ¡ 1.8 A a 27.7 ¡ 4.8 B bc Lufenuron 11.0 ¡ 3.5 A bc 40.1 ¡ 5.1 B c 47.4 ¡ 3.5 B bc Lufenuron z fenoxycarb 27.2 ¡ 3.2 A c 46.4 ¡ 4.6 B c 55.7 ¡ 4.6 C c Methoxyfenozide 3.9 ¡ 1.5 A ab 8.2 ¡ 2.7 A ab 8.7 ¡ 2.3 A a Pyriproxyfen 7.2 ¡ 3.2 A ab 12.9 ¡ 3.5 A ab 28.4 ¡ 7.1 B abc Triflumuron 2.2 ¡ 1.3 A ab 17.0 ¡ 4.8 A abc 25.3 ¡ 4.0 B abc Downloaded from http://meridian.allenpress.com/jfp/article-pdf/75/5/942/1686621/0362-028x_jfp-11-397.pdf by guest on 27 September 2021 a For each IGR or combination of IGRs, means followed by the same uppercase letter are not significantly different; in all cases, df ~ 2, 26 (Tukey-Kramer HSD test; P ~ 0.05). Within each dose, means followed by the same lowercase letter are not significantly different; in all cases, df ~ 7, 71 (Tukey-Kramer HSD test; P ~ 0.05).

Contrary to our results, previous studies document dominica and S. oryzae. This finding is interesting because successful combinations of IGRs belonging to different the JHA methoprene and the ecdysteroid agonist RH-5849 groups against stored-product pests, and therefore, general- or applied alone in wheat have shown low izations in terms of the compatibility between different IGRs performance against S. oryzae (30). Similar results were also should be avoided and each case should be examined recorded for RH-5849 and tebufenozide against R. dominica separately. For instance, Daglish and Wallbank (14) reported for doses of 2.5 and 5 ppm, respectively (30). Further- that a mixture of diflubenzuron (1 ppm) and methoprene more, the combination of the JHAs methoprene at 10 ppm (1 ppm) applied in sorghum was very effective against R. and fenoxycarb at 5 ppm with the ecdysteroid agonists

TABLE 4. Number of R. dominica adults per vial in wheat treated with seven IGRs and one combination of two IGRs at four doses (inclusive of 0 ppm), 60 days after the removal of the parental adults, and percent suppression of R. dominica adults in comparison with controlsa

Dose (ppm) IGR Mean no. ¡ SE % suppression

0 Control 20.1 ¡ 2.0

1 Diflubenzuron 0.3 ¡ 0.3 A 98.5 Fenoxycarb 2.3 ¡ 0.8 A 88.6 Flufenoxuron 2.2 ¡ 1.0 A 89.1 Lufenuron 0.0 ¡ 0.0 A 100.0 Lufenuron z fenoxycarb 8.2 ¡ 2.2 B 59.2 Methoxyfenozide 2.1 ¡ 0.8 A 89.6 Pyriproxyfen 0.0 ¡ 0.0 A 100.0 Triflumuron 1.0 ¡ 0.4 A 95.0

5 Diflubenzuron 0.0 ¡ 0.0 A 100.0 Fenoxycarb 1.0 ¡ 0.2 B 95.0 Flufenoxuron 0.0 ¡ 0.0 A 100.0 Lufenuron 0.0 ¡ 0.0 A 100.0 Lufenuron z fenoxycarb 0.1 ¡ 0.1 A 99.5 Methoxyfenozide 0.4 ¡ 0.4 AB 98.0 Pyriproxyfen 0.0 ¡ 0.0 A 100.0 Triflumuron 0.4 ¡ 0.4 AB 98.0

10 Diflubenzuron 0.0 ¡ 0.0 A 100.0 Fenoxycarb 1.0 ¡ 0.5 B 95.0 Flufenoxuron 0.0 ¡ 0.0 A 100.0 Lufenuron 0.0 ¡ 0.0 A 100.0 Lufenuron z fenoxycarb 0.1 ¡ 0.1 A 99.5 Methoxyfenozide 0.1 ¡ 0.1 A 99.5 Pyriproxyfen 0.0 ¡ 0.0 A 100.0 Triflumuron 0.1 ¡ 0.1 A 99.5 a Within each dose, means followed by the same letter are not significantly different; in all cases, df ~ 7, 71 (Tukey-Kramer HSD test; P ~ 0.05). For all IGRs or combination of IGRs, progeny in untreated wheat was significantly higher than that recorded in treated wheat; in all cases, df ~ 1, 17 (Dunnett’s test; P ~ 0.05). 948 KAVALLIERATOS ET AL. J. Food Prot., Vol. 75, No. 5 tebufenozide and methoxyfenozide at 5 or 10 ppm in the Temperature is a key factor in stored-product protection cereal rearing diet of the last instar larvae of P. interpunctella since it often affects the effectiveness of control methods increased their mortality compared with the cases when (25–27) while at the same time influencing the develop- tebufenozide or methoxyfenozide was applied alone (43). mental parameters of stored-product pests (22). Although in IGRs act mainly against the immature developmental a few cases in our study significant differences in the stages and exhibit little or no lethal effect against adults (9, performance of IGRs were observed among the tested 12, 30, 39, 42), but our results seem to contradict the above temperatures, temperature did not appear to affect the statement since all of the tested species exhibited some overall performance of the tested IGRs in terms of adult mortality levels after contact with the IGR-treated com- mortality or suppression of progeny production against P. modities, while mortality for all species was dose truncatus in treated maize. The results of our study suggest dependent. However, this is not the first study in which that IGRs could be considered as temperature-compatible toxic effects of IGRs against adults have been reported. For IPM components at least for the temperature range and for the insect species tested. However, further research is

instance, Letellier et al. (32) reported that mortality of Downloaded from http://meridian.allenpress.com/jfp/article-pdf/75/5/942/1686621/0362-028x_jfp-11-397.pdf by guest on 27 September 2021 Sitophilus zeamais Motschulsky after contact with fenox- required before accepting the stability of IGRs over a broad ycarb-treated grain ranged from 4 to 45.5% following an range of temperatures and species. increase of the fenoxycarb dose from 0.001 to 10 ppm. The tested IGRs have been proposed as potential Ammar (2) reported mortality of parental S. oryzae adults of protectants against several non–stored-product insect pests from 24 to 55% initially after their exposure in wheat treated belonging to different orders. For example, Mendel and with 0.5 to 25 ppm of flufenoxuron and falling to between 2 Rosenberg (37) reported that fenoxycarb inhibited the and 6% 3 months posttreatment. Similar trends were also development of first and second instars of Matsucoccus noted for the IGRs chlorfluazuron and XRD-473. Although josephi Bodenheimer and Harpaz (Hemiptera: Margarodi- Arthur (3) found slight mortality of R. dominica adults after dae), reduced the scale settlement, and caused 98% nymphal contact with a dust formulation of s-methoprene, the author mortality. According to Ludwig and Oetting (34), pyriprox- attributed this fact to the insecticidal properties of the dust yfen and diflubenzuron reduced the adult emergence of Frankliniella occidentalis (Pergande) (Thripidae: Thysa- itself rather than s-methoprene, since in the same study a noptera). Diflubenzuron reduced the longevity of Riptortus liquid formulation of s-methoprene appeared to have no clavatus (Thunberg) (Hemiptera: Alydidae) adults as well as toxic effect against adults of this species. In light of our the number of eggs laid per female (28). Lababidi (31) findings, doses equal to or higher than 5 ppm of fenoxycarb, found that flufenoxuron caused more than 86% mortality of lufenuron, and lufenuron plus fenoxycarb had lethal effects Agonoscena targionii (Lichtenstein) (Hemiptera: Psyllidae) against parental adults of the tested species. Furthermore, R. nymphs in a 2-year experiment. Navarro-Llopis et al. (41) dominica adults were more susceptible than P. truncatus showed that continuous applications of lufenuron on several adults to the IGR treatments tested here. Although we are generations of Ceratitis capitata (Wiedemann) (Diptera: not able to explain the adult mortality that was observed in Tephritidae) were capable of reducing the population of the present study, which in some cases, especially against R. the insect and the fruit damage in citrus orchards during dominica, exceeded 55%, the adulticidal properties of IGRs, a period of 4 years. Shamshad et al. (50) reported that if they do exist, may become a useful tool in stored-product triflumuron was very effective against the third instar larvae management. Those substances may enhance the efficacy of of Lycoriella ingenua Dufour (Diptera: Sciaridae) causing low doses of insecticides and thus provide adequate control 93% mortality at one-half of the recommended dose. of parental adults, preventing also their progeny production at Rodrı´guez-Enrı´quez et al. (45) showed that when larvae of the same time. For example, the combination of - Spodoptera exigua (Hu¨bner) (Lepidoptera: Noctuidae) were methyl at 5 ppm with s-methoprene at 0.6 ppm in wheat fed with an artificial diet mixed with methoxyfenozide, increased significantly the mortality of the parental adults of it resulted in pupae with significantly less weight than a -–resistant strain of T. castaneum the controls, in adult deformities, and in reduction in egg compared with the mortality obtained by treatments with hatching. chlorpyrifos-methyl or s-methoprene alone (11). Also, the In conclusion, application doses of $5 ppm of the combination of these compounds inhibited completely the tested IGRs were of high effectiveness against both species progeny production as in the case of the application of examined in the present study, and therefore, these chlorpyrifos-methyl alone (11). However, the selection of compounds should be considered as potential components each IGR–X insecticide combination requires great care since in stored-product IPM. Screening of the tested IGRs compatibility between these control strategies is not always revealed that efficacy was dose dependent, and in several feasible, especially against insecticide-resistant strains of cases almost complete suppression of progeny production insects, due to cross-resistance development. Kostyukovsky was achieved even with 1 ppm. In contrast, temperature did et al. (30) reported that a pirimphos-methyl–resistant strain of not appear to influence the efficacy of the tested doses to a T. castaneum exhibited cross-resistance to the JHAs metho- great extent. Parental adult mortality was recorded for all prene and pyriproxifen, while in a more recent study Daglish species tested in the present study. Additional studies (11) found that a malathion-resistant strain of S. oryzae and a are required to confirm the above findings and examine malathion-pyrethroid–resistant strain of T. castaneum were mixtures of these compounds with low-risk insecticides also tolerant to s-methoprene treatment alone. aiming to provide long-term protection in stored grains. J. Food Prot., Vol. 75, No. 5 EFFICACY OF INSECT GROWTH REGULATORS AGAINST STORED-PRODUCT PESTS 949

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