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Efficacy of some microbial control agents and inorganic insecticides against red flour beetle Tribolium castaneum and confused flour beetle, Tribolium confusum (Coleoptera: Tenebrionidae)

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The efficacy of three fungal pathogens, Isaria fumosorosea, Nomuraea rileyi and Verticillium lecanii alone and their combination with natural diatomaceous earth (DE) and silicagel-O-500 and silica-O-750 evaluated against Tribolium castaneum and
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   Integrated Protection of Stored Products  IOBC-WPRS Bulletin Vol. 98, 2014  pp. 193-201 193 Efficacy of some microbial control agents and inorganic insecticides against red flour beetle Tribolium castaneum   and confused flour beetle, Tribolium confusum (Coleoptera: Tenebrionidae) Magda Sabbour  Pests and Plant Protection Department, National Research Centre, El-Behouth St., P.O. Box 12622, Dokki, Cairo, Egypt e-mail:  sabbourm9@yahoo.com  Abstract:  The efficacy of three fungal pathogens,  Isaria fumosorosea ,  Nomuraea rileyi and Verticillium lecanii alone and their combination with natural diatomaceous earth (DE) and silicagel-O-500 and silica-O-750 evaluated against Tribolium castaneum and Tribolium confusum .   Results showed that modified diatoms with Calcium hydroxide (Ca-DE) and modified diatoms with Sodium hydroxide (Na-DE) were the most effective treatments against the two tested insects and achieved the highest mortality percentages. T. castaneum achieved the highest tolerant to tested DEs. Cab-O-Sil-750 gave highest mortality against T.   castaneum  reached to 89, 50 and 12% at concentrations 1, 0.5 and 0.25 g/kg wheat, respectively . The fungus  I. fumosorosea  was the most effective alone against T. castaneum . Ca-DE and Na-DE treatments strongly enhanced the potency of the tested fungi  I. fumosorosea  and  N  .  rileyi . Results showed that T. castaneum was susceptible to  N. rileyi . Larvae of T. castaneum  were more tolerant to V. lecanii  alone. In most cases, DE combinations with tested fungi had synergistic effects, while in T. castaneum  modified diatoms with aluminium hydroxide (Al-DE) decreased the efficacy of V. lecanii . Both silica gel and diatoms protected wheat better. The egg  production was highly suppressed by   combination of Ca-DE followed by Na-DE with tested fungi in comparison to untreated control. The combination of Ca-DE/  I. fumosorosea  strongly suppressed the number of deposited eggs of T. castaneum  (87.5 ± 9.6 eggs/female) in comparison to untreated control (277.0 ± 5.9 eggs/female). The most effective DEs modifications were Ca-DE and Na-DE with insecticidal, repellency or ovicidal effects against T. castaneum  and had synergistic effects on the  potency of tested fungi. Key words:    Isaria fumosorosea ; Nomuraea riley, Verticillium lecanii, Tribolium castaneum , Tribolium confusum , Cab-O-Sil-750, Cab-O-Sil-500 , diatomaceous earths Introduction Both silica gel and diatomaceous earths (DEs) kill insects by absorbing the oily or waxy outer cuticle layer by direct contact. When the thin waterproof layer of the epicuticle is lost then the insect loses water and dies. Several DE formulations and silica have been successfully evaluated as grain protectants against different stored grain pests (Athanassiou et al  ., 2003, 2004, 2005a, 2005b; Athanassiou and Kavallieratos, 2005; Kavallieratos et al  ., 2005; Athanassiou et al  ., 2006; Palyvos et al  ., 2006; Vayias et al  ., 2006a, 2006b; Athanassiou et al. , 2007; Kavallieratos et al  ., 2007a, 2007b; Athanassiou et al  ., 2008a, 2008b; Iatrou et al  ., 2010; Athanassiou et al  ., 2013). They are not toxic, can be easily removed from the grains and  possibly recycled in storage bins. The entomopathogenic fungi are promising for the control of stored product insects as environmentally safe and with low mammalian toxicity. The fungus attaches and penetrates through the insect’s cuticle, causing the insect’s death (Cox and Wilking, 1996). Entomopathogenic fungi have been experimented with success against  194 several stored product insect species in both laboratory and field tests (Moore et al  ., 2000; Akbar et al  ., 2004; Batta 2004; Kavallieratos et al  ., 2006; Michalaki et al  ., 2006; Sabbour and Abd El-Aziz, 2007a, 2007b, 2010; Kavallieratos et al  ., 2014). This work aims to evaluate the efficacy of DEs alone or in combination with three fungal pathogens:  Isaria farinosa   (Holmskjold) Fries (=  Paecilomyces farinosus  (Holmskjold) Brown and Smith),  Nomuraea rileyi (Farlow) Sampson (Ascomycota: Hypocreales) and  Lecanicillium lecanii  Zare and Gams (Ascomycota: Eurotiales) (= Verticillium lecanii  (Zimmermann)) against two stored  products  , Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae)   and Tribolium confusum  Jacquelin du Val (Coleoptera: Tenebrionidae). Material and methods Insects Larvae of T. castaneum  and T. confusum were used in the experiments. The target insects were reared under laboratory conditions on semi-artificial diet (fine wheat with some adherent endosperm) with 20% glycin and 5% yeast powder. All cultures and experiments were held at 26 ± 2 °C and 70-80% r.h. with 16 hours light and 8 hours dark. DEs    A natural DE, three DE modifications and two silica gels were tested alone or in combinations with the fungi. The natural DE was chemically modified by different mono-, di-, tri- valent metal hydroxides (MOH, M = Na, Ca, Al) according to (Abd-El-Aziz and Sherief, 2010). The DEs were treated at the application rates of 0.25, 0.5 and 1 g/kg wheat. Isolation of fungi    The tested fungi species,  I. fumosorosea ,  N. rileyi  and V. lecanii  were isolated from the dead and/or infected larvae and pupae of the tested insects (Sabbour and Sahab, 2005) and were identified at Microbiology Department, NRC. Bioassays The insecticidal efficacy of DEs were tested at three dose rates, 0.25, 0.50 and 1 g/kg wheat against the 3 rd  instar larvae of T. castaneum and  T. confusum (Coleoptera: Tenebrionidae). For each case, four glass jars as replicates were used. Each replicate was treated individually with the respective DE quantity and then shaken manually for one minute to achieve equal distribution of the DE. Subsequently, ten 3 rd  instar larvae of the three tested species were introduced into each glass jar and covered with muslin for sufficient ventilation. Twelve replicates glass jars containing untreated wheat served as control. Mortality was assessed after 7 d of exposure in the treated and untreated jars. Mortality was corrected according to Abbott (1925). All tests were conducted at 27 ± 2 °C and 65 ± 5% relative humidity (RH). For the insecticidal efficacy of tested fungi alone or with DEs, six concentrations (in percent of v/v) for each tested fungi (16, 8, 4, 2, 1, 0.5 x 10 7  spores/ml) were prepared. The target insects were fed with semi-artificial diet contaminated with the different fungi rates. Mortalities were calculated after 7 d. Mortality was corrected according to (Abbott, 1925). Also, LC 50  variance, 95% confidence limits, were calculated according to Finney (1964). The tested fungi were tested at 0.5 x 10 7  spores/kg wheat for conducting the combination tests with DEs formulations at 0.5 g/kg wheat. Ten 3 rd  instars larvae from each insect species were kept in a glass jar (15 x 5 cm 2 ) fed on a diet containing prescribed treatments. For each case, four jars as replicates were prepared. All the experiments were repeated three times. The ovipositional  195 deterrent effects of DEs alone or in combination with the fungi were also tested. The fungi were tested at 0.5 x 10 7 spores/kg wheat in combination with DEs at 0.5 g/kg wheat. The DEs alone were used at the rate of 1 g/kg wheat. Four replicates of 100 g wheat for each treatment were used. Each replicate was treated individually with the formulations for 1 min and put inside glass jars. Four replicates in jars containing untreated wheat served as control. Subsequently, one paired of newly emerged adults were introduced into each jar. The number of deposited eggs on treated or untreated wheat/female was counted and the percent repellency values were calculated according to the equation of Lwande et al  . (1985), D = (1 - T/C) x 100, where: T and C represent the mean number of deposited eggs per female of the treated and check set, respectively. Results and discussion Data in Table 1 show that the efficacy of DEs earth against the target insect pests. After treatments with Cab-O-sil 750 at 1.0%, the percentage of mortality significantly decreased to 89 and 91% for T. castaneum and T. confusum , respectively, as compared to 49 and 55% for the same pests when treated with DE. At lower concentrations the higher percentage of mortality recorded when the target insect pests treated with CA-DE and Cab-O-Sil 750 (Table 1). Similar results obtained by Sabbour et al.  (2012) who found that Ca-DE was the most effective DE and achieved the highest mortality percentages. Ca-DE and Na-DE were the highlight treatments against  Ephestia cautella  (Walker) (Lepidoptera: Pyralidae),  Plodia interpunctella (Hübner) (Lepidoptera: Pyralidae)   and  Ephestia kuehniella  Zeller (Lepidoptera: Pyralidae)   at 5% conc., and achieved the highest mortality percentages (78, 77 and 72%) and (76, 76 and 75%), respectively. This results stands in agreement with Korunic and Mackay (2000) who reported that the treated wheat with 0.5 and 0.75 g of Protect-It ® /kg wheat, reduced the population of Sitophilus oryzae (L.) (Coleoptera: Coleoptera), T. castaneum  and  Rhyzopertha dominica (F.) (Coleoptera: Bostrychidae) by 98 to 100% with respect to controls due to the repellent properties of DE, and probably had very good dispersal capacity in the grain mass. The application of Ca-DE caused the complete mortality of Callosobruchus maculatus  (F.) (Coleoptera: Chrysomelidae) compared to the other tested DEs after 7 and 14 d interval (Abd-El-Aziz and Sherief, 2010). The efficacy of the bioinsecticides were evaluated alone and with the combinations with DE in Table 2. Data show that LC 50  of  I. fumosorosea alone were   140 and 149 spores/ml for T. castaneum and  T. confusum , respectively. The corresponding LC 50  significantly decreased to 99 and 113 spores/ml Table 2. In all treatments the LC 50  for T. castaneum and  T. confusum  were significantly decreased to 111 and 119 spores/ml when  N. rileyi combined with NA-DE (Table 2). The presence of DE favors the insecticidal efficacy of  Beauveria bassiana  (Balsamo) Vuillemin (Ascomycota: Hypocreales) against larvae of  R. dominica  Lord (2005). The addition of many inert dust types such as charcoal, ash or DE increased the potency of  M. anisopliae  against S. oryzae  (Batta, 2004; Kavallieratos et al  ., 2006). Akbar et al.  (2004) mentioned that DE significantly increased the attachment of  B. bassiana  conidia on the cuticle of T. castaneum  larvae. This attachment resulted to damage the epicuticle lipids of insects (Moore et al  ., 2000). Būda and Pečiulytė (2008) tested the effect of four fungal isolates, (  B. bassiana ,  L. lecanii, M. anisopliae  var  . anisopliae  and  I. farinosa ) on adults of  P. interpunctella  and one species tested on mature larvae of the pest. Table 3 shows the ovipositional deterrent effect of DE applied alone and with combination with the fungi The mean number of deposited eggs per female (egg  production) of each tested species was greatly affected by the DEs/fungi combinations (Tables 3, 4). The combination of Ca-DE and Na-DE with tested fungi highly suppressed the  196 moths’ egg production in comparison to untreated with highly significant differences. The number of eggs laid/female of T. castaneum was significantly decreased to 97.6 ± 5.9 individuals when  I. fumosorosea combined with DE   as compared to 298.6 ± 9.4 individuals in the control. The combination of Ca-DE and Na-DE with tested fungi highly suppressed the moths’ egg production in comparison to untreated with highly significant differences. A moderate effect on suppressing the moths’ egg production was recorded in case of DE and Al-DE with tested fungi. T. castaneum was the most susceptible moth to DE/fungi combinations followed by T. confusum moths (Tables 3, 4). The combination of Cab-O-Sil 750/  I. fumosorosea  strongly suppressed the number of deposited eggs of T. castaneum (Table 3). These results meet with Sabbour et al  . (2012) who found that in all tested insects there were significant differences between DEs alone compared to untreated control. The combination of Ca-DE and Na- DE with tested fungi highly suppressed the moths’ egg  production in comparison to untreated with highly significant differences. A moderate effect on suppressing the moths’ egg production was recorded in case of DE an d Al-DE with tested fungi.  P. interpunctella  was the most susceptible moth to DE/fungi combinations followed by  E. cautella  and  E. kuehniella  (Tables 3-5). The combination of Ca-DE/  B. bassiana  strongly suppressed the number of deposited eggs of  P. interpunctella  (54.6 ± 5.8 eggs/female), in comparison to untreated control (288.3 ± 3.4 eggs/female), with highly significant differences. Abd-El-Aziz and Sherief (2010) tested the insecticidal effects of modified DE with different hydroxides against C. maculatus  on stored cowpea grains. Ca-DE had insecticidal, repellent and ovicidal effects against C. maculatus . These effects are due to the modification by using Ca-DE (divalent metal hydroxide) and had the biggest surface area (12.6 m 2 /g) followed by  Na-DE (11.4 m 2 /g), which can absorb more lipid from insect bodies. Also, Ca-DE showed the highest number of crystals. Table 1. Mortality % of tested insect’s larvae on wheat treated with DE, silica gel and three DE modifications at three rates. Treatments concentration % of larval mortality T. castaneum T. confusum  DE 1.0 0.5 0.25 49 30 1 55 34 4  NA-DE 1.0 0.5 0.25 85 39 5 91 40 10 AL-DE 1.0 0.5 0.25 39 20 1 28 18 0 CA-DE 1.0 0.5 0.25 89 40 10 95 49 11 Cab-O-Sil 500 1.0 0.5 0.25 59 30 1 65 33 3 Cab-O-Sil 750 1.0 0.5 0.25 89 50 12 91 54 15  197 Table 2. Efficacy of tested fungi alone or combined with DEs and silica gel against the target insects. Treatments DEs LC 50 of T. castaneum T. confusum    I. fumosorosea DE  NA-DE AL-DE CA-DE Cab-O-Sil 500 Cab-O-Sil 750 138 99 154 100 110 101 166 113 169 117 129 115  I. fumosorosea alone 140 149  N. rileyi  DE  NA-DE AL-DE CA-DE Cab-O-Sil 500 Cab-O-Sil 750 144 111 159 113 122 108 150 119 167 128 130 113  N. rileyi alone 151163  L. lecanii DE  NA-DE AL-DE CA-DE Cab-O-Sil 500 Cab-O-Sil 750 167 140 166 142 104 114 177 155 170 147 109 117 V. lecanii alone 177 190 Table 3. Ovipostional deterrent effect of tested DEs applied alone or in combination with tested fungi against T. castaneum . Treatment Mean number of eggs/female ± SE of T castaneum  DE/fungi combination DE alone DE/  I. fumosorosea  DE/  N. rileyi  DE/  L. lecanii  DE 277.0 ± 5.9 146 ± 7.7 146.1 ± 2.4 199.3 ± 6.3  Na-DE 145.0 ± 8.6 87.5 ± 9.6 88.6 ± 4.4 163.2 ± 3.9 AL-DE 201.0 ± 3.1 146.7 ± 8.7 156.7 ± 6.5 198.9 ± 8.9 CA-DE 157.0 ± 9.9 99 ± 5.3 101 ± 8.7 164.3 ± 2.9 Cab-O-Sil 500 174.1 ± 3.6 102.8 ± 2.8 114.8 ± 7.6 176.6 ± 8.9 Cab-O-Sil 750 134.4 ± 8.4 97.6 ± 5.9 102.9 ± 9.3 165.6 ± 6.8 Control 298.6 ± 9.4 F LSD (0.05) 32.31 19.17
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