International Journal of Tropical Insect Science Vol. 30, No. 4, pp.

207–213, 2010 q icipe 2010

doi:10.1017/S1742758410000378

Biological efficacy of CalneemTM oil against the tropical warehouse moth Ephestia cautella (Lepidoptera: Pyralidae) in stored maize
Ali Shehu1*†, Daniel Obeng-Ofori2 and Vincent Yao Eziah2
1

African Regional Postgraduate Programme in Insect Science (ARPPIS), University of Ghana, Legon, Ghana: 2Crop Science Department, University of Ghana, Legon, Ghana
(Accepted 22 October 2010)

Abstract. The tropical warehouse moth Ephestia cautella (Walker) is an important storage pest of maize grain. The control of this major moth pest relies heavily on the use of synthetic insecticides. We assessed the biological efficacy of a commercial neem oil (Calneem oil) against E. cautella in the laboratory, using the common grain protectant Actellic as a positive control. Contact toxicity, repellency, effects on oviposition, development and grain damage were assessed. The assays were conducted by treating 100 g of maize grains with Calneem oil concentrations of 3, 5 and 7 ml/l; and Actellic at 2 ml/l. Calneem oil significantly (P, 0.05) reduced oviposition rate, development of eggs and immature stages, and emergence rate of E. cautella progeny in maize grains. Grains treated with Calneem oil had significantly (P, 0.05) reduced grain damage in storage, and the oil had a repellency of 53 –70% compared with the negative control. Calneem oil protected maize grain against damage by E. cautella for 10 weeks, compared with 20 weeks protection by Actellic. There was no resistance development to the oil for three generations of E. cautella. The insects that survived treatment with the LC90 concentration (12.2 ml/l) of the Calneem oil laid fewer eggs, and some of their progeny were deformed. Calneem oil provided a good level of protection to maize grains against infestation by E. cautella, and may therefore be a suitable substitute for Actellic. Key words: Ephestia cautella, stored maize, Calneem oil, azadirachtin, toxicity, repellency, persistence, resistance, actellic

Introduction Maize (Zea mays L., Poaceae) is an important cereal grain that is widely cultivated in the tropics, both for human consumption and as livestock feed. It is the most important cereal in the world after wheat and rice, in terms of area under cultivation and total production (Purseglove, 1992).
*E-mail: alijeshehu@yahoo.com † Present address: Department of Agricultural Technology, Yobe State College of Agriculture, Gujba, P.M.B. 1104, Damaturu, Yobe State, Nigeria.

Insect damage to stored grain is a serious problem in the developing countries in the tropics, primarily due to favourable climate conditions and poor storage (Bekele et al., 1997). Important losses are incurred due to the tunnelling activity of adults and larvae of many storage pests, including moths like the tropical warehouse moth Ephestia cautella (Walker) (Lepidoptera: Pyralidae) whose larvae attack and consume the grain germ. Contamination of the infested commodity also occurs from the large quantity of webbing this moth spins over the surface of the grains (FAO, 1992).

Thus the whole experiment lasted 6 weeks. Toxicity to larvae One hundred grams of maize grains were put into five glass jars and infested with 20 E. Three of the jars were treated with Calneem oil (3. foreign exchange constraints and fluctuations lead to ever-rising cost and erratic supply of the chemicals (Obeng-Ofori et al. 48. 1999. The control was treated with water. and each treatment was replicated four times in a completely randomized design. 5 and 7 ml/l) and Actellic (2 ml/l) were applied to the dorsal surface of the thorax of each larva using a microapplicator. and each treatment was replicated four times. was used as a positive control. and 1 ml of three concentrations of Calneem oil (3. Furthermore. 1999). 96 and 120 h. affecting over 300 species of insects. Mortality was recorded after 24. nematodes. which are readily available. and sieved out after 1 week of oviposition. 5 and 7 ml/l). 72. a common storage grain protectant. The need for products that effectively protect stored produce. Contact toxicity via topical application Twenty fifth-instar E. Effect of Calneem oil on oviposition One hundred grams of maize were weighed into five glass jars. cautella adults were used to infest the maize grains in each jar. Thus the whole experiment lasted 6 weeks. Insect pest control in stored produce relies heavily on the use of fumigants and residual contact insecticides. 2007). 2007). a local nongovernmental organization called Aqua Agric Community Project (AACP) has started producing neem oil and cake in Dawhenya for pest control and other agricultural uses. their utilization as pesticides is still limited in Africa (Obeng-Ofori. Neem products are relatively harmless to most beneficial arthropods. cautella from the stock culture were placed separately in Petri dishes. affordable. 5 and 7 ml/l) and Actellic (2 ml/l) after 4 days of infestation. Each treatment was replicated four times. cautella (2 – 4 days old) of mixed sexes were introduced into the jars. Emerging adults were counted and recorded for 5 days. Legon. including the re-evaluation of traditional botanical pest control agents (Talukder and Howse. Water was used as a control. Materials and methods Culturing of insects Ephestia cautella moths were obtained from the Crop Science Department of the University of Ghana. and has stimulated interest in alternative control strategies. The control was treated with water. . as well as mites. cautella in stored maize. To promote the adoption and utilization of neem-based pesticides in Ghana. fungi. cautella adults. bacteria and viruses (Schmutterer. However.208 A. Pesticides derived from neem (Azadirachta indica) are broad spectrum in their activity. Toxicity of Calneem oil on immature stages Toxicity to eggs One hundred grams of maize grains were put into each of five glass jars. However. 5 and 7 ml/l) and Actellic at 2 ml/l after 2 weeks of infestation. The infested grains were treated with Calneem oil (3. Shehu et al. Many botanical pesticides are effective against pests as antifeedants. laboratory and field bioassays were used to evaluate the efficacy of Calneem oil produced by AACP for the control of the tropical warehouse moth E. and are less hazardous than synthetic pesticides to people and the environment (Obeng-Ofori. The treated grain was left for 3 h to allow the water to evaporate. The grains were treated with Calneem oil (3. and 20 E. by which time larvae had emerged. The emerging generations of moths of nearly same age (1 – 4 days) were used to set up subsequent rearing cultures. Insects that did not move or respond to probing three times with a blunt probe were considered dead. The adults that emerged were counted and recorded for 5 days. Adult insects were sieved out after the oviposition period of 4 days. in developing countries. 1995). In this study. These include different plant materials used by resource-poor farmers in developing countries to protect stored grains against pest infestation. The parent adults were removed after 7 days of infestation. indiscriminate use of synthetic insecticides to control storage pests causes the serious problems of toxic residues in grains. Actellice (pirimiphos-methyl). With the aid of an aspirator. and each treatment was replicated four times.. are biodegradable and appear less likely to build up genetic resistance in target pests (Obeng-Ofori. is therefore acute. environment hazards and the development of resistant insect strains. repellents or toxicants. in spite of the highly positive benefits derived from the use of neem products. The eggs were sieved onto a cardboard paper and counted. one treated with Actellic (2 ml/l) and the other treated with water as a control. 1997). 40 unsexed moths were transferred into poultry mash (poultry mash þ honey þ glycerine). 20 adults of E. With the aid of an aspirator. 1985). relatively less poisonous and less detrimental to the environment.

The experiment lasted 3 weeks. Differences between means were separated by determining the least significant difference whenever ANOVA indicated a significant difference.Biological efficacy of Calneem oil 209 Toxicity to pupae Twenty fifth-instar E. The second set of grain was infested in the second month. cautella were placed in separate Petri dishes. Adult moths that emerged were counted and recorded. Percentage weight loss was calculated using the method of FAO (1985) as: % weight loss ¼ UNd 2 DNu £ 100. and 1 ml of nine different concentrations of Calneem oil (6 – 14 ml/l) was applied to the dorsal surface of the thorax of each insect with a micro-applicator. Sixty unsexed E. The LC90 concentration of the oil was determined using Probit analysis. and the control was treated with acetone. 5 and 7 ml/l) and another with Actellic (2 ml/l) to serve as treatments and positive control. and all negative PR values were treated as zero (Obeng-Ofori et al. After 3 days. while the other jar had untreated maize as a control. cautella adults (3 –5 days old) were introduced into the nylon mesh tube through the hole. Persistence of Calneem oil in the field Four sets of treatments were set up. cautella was assessed in the laboratory at 27 ^ 2 8C and 68 – 72% relative humidity. Twenty-five adults of the E. using the method described by Obeng-Ofori and Reichmuth (1997). The PR data Data analysis Data were corrected for mortality in the control using Abbott’s formula (1925) and subjected to ANOVA. Acetone was used as the control. 1997). where U is the weight of undamaged grains in the sample. Repellent effect The repellent action of the Calneem oil on E. The treated grains were left for 1 h to allow the water to evaporate completely. cautella adults aged 3 –5 days were used to infest the first set of treated grains. respectively. and the survivors were used to infest another set of grains so as to obtain the F2 generation. Mortality was recorded after 48 h. The poultry mash was carefully removed leaving 15 pupae in each Petri dish. Grains were sampled for damage assessment after 5 weeks of infestation. one jar contained treated grains. after which grain samples were taken for damage assessment as described above. The grains were treated with either Calneem oil (5 ml/l) or Actellic (2 ml/l). mortality and number of eggs laid were counted and recorded. Twenty-five E. The pupae in each dish were treated with 1 ml each of Calneem oil (3. The number of damaged grains (with characteristic holes) and undamaged grains was counted and weighed. each consisting of 10 kg of maize grains placed in three (40 £ 25 cm) jute sacks. and the number of insects present in the control (Nc) and in treated grains (Nt) was recorded after 30 min. Samples of maize grain (100 g) were treated with Calneem oil (3. with the aid of a funnel. and Nd is the number of damaged grains in the sample. Effects on resistance development Twenty 2. Each treatment was replicated four times. F2 and F3 generations of the insects were also treated as above. A thousand grains were used as sample in calculating damage to grains stored in a crib. The bioassay consisted of two glass jars connected together at their rims by means of a nylon mesh tube with a small hole in its middle. Each treatment was replicated four times. 5 and 7 ml/l) and Actellic (2 ml/l) using a microapplicator. insects that did not move or respond to probing three times with a blunt probe were considered dead.to 5-day-old unsexed fifth instars of E. The emerging F1 generation of the insects was treated with the above LC90 concentration. . and the control was treated with water. cautella were transferred into a Petri dish containing poultry mash and allowed to pupate. In each case.. D is the weight of damaged grains in the sample. In each set-up. UðNd þ NuÞ were analysed using analysis of variance (ANOVA). with each treatment replicated three times. Nu is the number of undamaged grains in the sample. Damage assessment Damage assessment was carried out by taking samples of 100 grains from the control grains used in progeny assessment assays. and each treatment was replicated four times. eggs laid were counted and then transferred onto poultry mash for development into adults. Percentage repellency (PR) values for both tests were computed as: PR ¼ ½ðN c 2 N t Þ=ðN c þ N t ފ £ 100. which were then stored in a crib for 5 weeks. the third set in the third month and the fourth set in the fourth month. cautella that survived the LC90 treatment were used to infest maize grains.

with weight losses of 0.0 ^ 6.0a 33. cautella that emerged from treated grains were deformed (Fig.73c 9.8 ^ 2.11 120 0. cautella emergence from grains treated with different concentrations of Calneem oil and Actellic was not significantly different. cautella compared with untreated controls.0 ^ 0. Repellent effects Calneem oil was moderately repellent to E. cautella 5 and 10 weeks posttreatment. Damage assessment Calneem oil gave good protection to treated grains against damage by E. Some of the adults of E.45 48 0.22% after 2 months of storage (Fig.0 ^ 0.0 ^ 3.0 ^ 4.44b 18. cautella adults from treated grain containing larvae (Table 2).25e 13.8 ^ 2. there were no significant differences among the different concentrations of the oil on E.0 Actellic 2.05) difference between the insecticidal treatments and the control.8 ^ 3. There was a significant (P.0 ^ 7. There was a significant (P. respectively (Table 3). least significant difference. Effect on oviposition Oviposition data of E.0 ^ 2.5 ^ 4. Persistence in the field Calneem oil at the 5 ml/l concentration gave significantly higher (P.0 LSD (P. There was a significant (P. 0. cautella. Shehu et al.0a 0.08c 65. Actellic had 40% repellency (Fig. Results Contact toxicity via topical application Mortality of E.0 ^ 0. and also between the Calneem oil and Actellic treatments. after 120 h.15b 50.05) difference between the number of eggs laid on the treated grains versus the control. There was a significant (P.0a 5. The number of eggs laid decreased with increasing concentration.5 ^ 3. with weight losses of 0.69 LSD. cautella on grain treated with different concentrations of Calneem oil and 2 ml Actellic are summarized in Fig.54b 33.89ab 10.8 ^ 4. 0.07d 12. but E.0 ^ 0. Contact toxicity of Calneeme oil to Ephestia cautella adults % Mean mortality (^ SE) with time (h)+ Treatment (ml/l) Control Calneem oil 3.5 ^ 3.0 7.79b 6. Toxicity to larvae Calneem oil reduced the emergence of E. LSD test.8 ^ 6. but no significant differences were observed between the Calneem oil (7 ml/l) and Actellic. 0. 0.11% to E.05) difference between the insecticidal treatments and the control. but none between Calneem oil and Actellic.68 72 0.39d 6.05) protection to grains than the untreated control. 4).0 ^ 0.210 A. cautella adults from treated grain containing pupae (Table 2).15b 47.12d 93.23c 90. The toxicity of the oil increased with increasing concentration and with time. cautella following treatment of grains containing eggs (Table 2).5 ^ 1. Toxicity to immature stages Toxicity to eggs Calneem oil significantly reduced the emergence of E. 0.0 5.8 ^ 3. There was no emergence of E.0a 0. with a concentration-dependent repellency ranging from 53 to 70%.0a 22. 0. Means in a column followed by different letter(s) are significantly different at P. cautella following topical application of Calneem oil is summarized in Table 1.0a 0.39c 63.0 ^ 0. .05) between the insecticidal treatments and the control. 0. Within 48 h.99 – 2.0 ^ 0. but none between the protectant ability of the Calneem oil and Actellic Table 1. 2).15c 23. cautella from grains treated with Calneem oil (7 ml/l) and Actellic.0 ^ 0.05) difference between the insecticidal treatments and the control. 3).24 and 1.23b 28.89ab 5.0 ^ 2.05) þ 24 0.53 96 0. Toxicity to pupae Calneem oil reduced the emergence of E. 1. cautella. 0.05.8 ^ 3. The highest mortality (65%) was recorded at the highest concentration used.0a 12. There was a significant difference (P.0a 22. In contrast. There was no emergence from grains treated with Calneem oil (7 ml/l) or Actellic.

cautella indicates a possible contact action of the major active constituent of the oil (azadirachtin). The toxicity of the oil results in its protectant effect against insect damage to stored grain.0 ^ 0.0 5. However.0 ^ 0. 2 and 1% concentrations of neem oil produced negligible mortality after 24 and 48 h of treatment.0 ^ 0.05. 0.87a 3. Oviposition rates in grain treated with all three concentrations of the oil (3.85bc 0. . Laying fewer eggs could Eggs 13 ^ 1. 0. Means in a column followed by different letter(s) are significantly different at P.05. indica acts as a strong growth inhibitor.84 Pupae 80 Mean % repellency 10 ^ 0. no significant (P.5b 2. corroborating our observations. 5 and 7 ml/l) were significantly (P.71b 2.63b 2.0 ^ 0. 2. and can cause death before or during moulting (Mordue and Blackwell. Bars followed by different letter(s) are significantly different at P .85b 2. Raguraman and Singh (1997) reported that topical application at the rate of 0.05) different from the control.0 LSD (P. is acutely toxic and an active feeding deterrent against two lepidopteran species.05) differences between mortalities in the three generations of E.02 Larvae 13 ^ 1. 0. Thus resistance development had not set in by the F3 generation treated with Calneem. Calneem oil was effective in reducing the number of eggs laid by E. LSD test. Discussion Calneem oil applied to the dorsal surface of E.. cautella within 5 days.5 ml per insect Table 2. 0. cautella.0 ^ 0. Mean percentage repellency of Calneem oil against Ephestia cautella.0 ^ 0. At this concentration. cabbage looper Trichoplusia ni and the armyworm Pseudaletia unipuncta (Akhtar et al.05. which ranged from 90.4 to 95.0 ^ 1.0c 0. Effect of Calneeme oil on adult emergence from 20 immatures each of Ephestia cautella Mean adult emergence (^ SE)þ Treatment (ml/l) Control Calneem oil 3. 2008). Effect of Calneem oil on oviposition of Ephestia cautella. Azadirachtin prevents both ecdysis and apolysis. 0. 0. there were no significant (P.0 ^ 0.0 ^ 0.8a 2. Bars followed by different letters are significantly different at P. The effectiveness of the oil against E.0b 2. Fig. cautella is summarized in Fig. cautella was toxic to the moths.0 ^ 0. Deformed progeny of Ephestia cautella following Calneem oil treatment Effects on resistance development Contact toxicity of Calneem oil to three generations of E.05) þ at 3. Crude seed extract of A.0 ^ 0. cautella. the protectant effect of Calneem oil appeared to decline with time.Biological efficacy of Calneem oil Mean number of eggs laid 1200 1000 800 600 400 200 0 Control Calneem oil 3 Calneem oil 5 Calneem oil 7 Treatment (ml/l) Actellic 2 b c d e a 211 Fig.8a 4. Fig.2b 2.7b 0.0c 3.0b 0.114 b a a c 60 40 20 0 Calneem oil 3 Calneem oil 5 Calneem oil 7 Actellic 2 Treatment (ml/l) LSD.2 ml/l. LSD test.02b 2.6%. Using Probit analysis. 0. 1993). 5. Mortality increased with increasing dosage and time. with low mortality observed within the first 24 h of treatment. least significant difference. Therefore.0 Actellic 2. LSD test.05) differences between the oil treatment and the control were seen after 15 weeks of treatment. 10 weeks post-treatment. 1. 3.0 ^ 0.0 7. the LC90 concentration of Calneem oil was 12. Calneem oil at 7 ml/l induced about 65% mortality on fifth-instar E.

1995. 0. cautella. Contact toxicity of LC90 concentration of Calneem oil on Ephestia cautella over three generations.0 Actellic 2. Effect of Calneeme oil on weight loss due to Ephestia cautella on stored maize grain Mean % weight loss (^ SE) with duration (weeks)þ Treatment (ml/l) Control Calneem oil 5. as also reported by Sunarti (2003).18a 1. The complete inhibition of egg development and the inhibition of development in immature stages contribute to Calneem oil’s action as a grain protectant. cautella compared with the control.15b 0. 1993). 1996. cautella following three generations of selection.24 ^ 0. the oil remained effective for 10 weeks. Means in a column followed by different letter(s) are significantly different at P.11ab 1. 2000).03b 0. Neem oil is not an instant killer (Raguraman and Singh. LSD test. LSD test. 1993). post-embryonic. hydroxyfuran. This is a significant merit for its use against various pests (Aslam and Naqvi. decalin is reported to have regulatory effects on growth and development. while hydroxyfuran has antifeedant effects (Ascher.15 ^ 0.47a 1.18 ^ 0. the oil caused complete inhibition of the development of eggs and larvae of E. 5. Ascher (1993) observed developmental. larvae and pupae of E.66 ^ 0. 2006).11 ^ 0.32a 1. The oil was moderately repellent to E. 2002.15b 0. which potentially act as repellents (Ascher. who showed that application of neem oil to cocoa beans deterred feeding by E. 0.05.05) þ 5 2.39 ^ 0. 4.0 LSD (P. 1994).05 ^ 0.63 ^ 0.20 ^ 0.817 15 2. Shehu et al. Calneem oil inhibited the development of eggs.212 Mean % damage caused 7 6 5 4 3 2 1 0 Control Calneem oil 3 Calneem oil 5 Calneem oil 7 Treatment (ml/l) b b b b a A. 0. cautella to cocoa beans for more than 3 months of storage. Salako. Capinera. Some of the emerging adults were deformed. 0. Fig.01b 0. The persistency test of the oil and Actellic confirmed that at a concentration of 5 ml/l. cautella larvae 92% and observed only 10% normal adult emergence from the neem oil-treated larvae. with repellency ranging from 50 to 75% compared with the 40% repellency of Actellic.962 20 2. Neem oil contains a complex mixture of active ingredients that limit the ability of pests to develop resistance (Ellis et al. Bars followed by different letter(s) are significantly different at P . Nimbin and salinnin are reported to have a potential sterilizing effect on eggs (Ascher.02b 0. AFR. be due to the fact that neem oil can cause sterility in adult insects (Schmutterer.809 10 3. Inhibition of the development of immature stages of the insect by the oil could be due to the presence of the decalin.. 2008). At a concentration of 7 ml/l. . which repels many species of insects. nimbin and salinnin fragments of azadirachtin. Table 3.41 ^ 0. No significant difference was observed in the mortality of E. LSD test. The oil contains many sulphur compounds. cautella.40a 0. Calneem oil and Actellic significantly reduced the damage caused by larvae of E.698 LSD.20b 1. including moths. cautella. 99 Mean % mortality 96 93 90 87 F1 a a a F2 Generation F3 Actellic 2 Fig. Effect of Calneem oil and Actellic on damage caused by Ephestia cautella to stored grains. Sunarti (2003) reported that the application of neem oil deterred E. cautella. 1993.26ab 1. reproductive and growthinhibitory effects of neem oil. Means followed by different letter(s) are significantly different at P . Blum and Roitberg (1999) reported that one of the most frequently used natural insect repellents is margosa oil (neem oil).05. least significant difference. This action of Calneem oil increases its value as a grain protectant against insect pests.23 ^ 0. which caused malformation and mortality in insects in a dosedependent manner.03 ^ 0. Sclar. cautella larval feeding by 92% and prevented damage by E. 1997) but has strong ovicidal and antifeedant effects that inhibit the development of eggs and larvae of E.05.

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