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Alligator pepper, Aframomum melegueta, and ginger, Zingiber officinale, reduce stored maize infestation by the maize weevil, Sitophilus zeamais in traditional African granaries
Crop Protection 32 (2012) 99e103
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Crop Protection journal homepage: www.elsevier.com/locate/cropro
Alligator pepper, Aframomum melegueta, and ginger, Zingiber officinale, reduce stored maize infestation by the maize weevil, Sitophilus zeamais in traditional African granaries Donald A. Ukeh a, b, c, Sylvia B.A. Umoetok a, Alan S. Bowman b, A. Jennifer Mordue (Luntz) b, John A. Pickett c, Michael A. Birkett c, * a b c
Department of Crop Science, University of Calabar, PMB 1115, Calabar, Nigeria School of Biological Sciences, University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK Biological Chemistry Department, Rothamsted Research, Harpenden, Herts AL5 2JQ, UK
a r t i c l e i n f o
a b s t r a c t
Article history: Received 11 May 2011 Received in revised form 18 October 2011 Accepted 19 October 2011
Alligator pepper, Aframomum melegueta (Roscoe) K. Schum, and ginger, Zingiber officinale Roscoe were tested for their efficacy in protecting stored maize cobs (Zea mays L.) against the maize weevil, Sitophilus zeamais Motschulsky, in traditional maize storage barn conditions, from November 2006 to February 2007, and November 2009 to February 2010 in Obudu, Southeast Nigeria. A randomised complete block design was used in each storage barn with four treatments (maize, maize plus A. melegueta, maize plus Z. officinale, maize plus A. melegueta and Z. officinale) replicated 4 times. When used in combination with stored maize cobs at a level of 10% (w/w), A. melegueta and Z. officinale significantly reduced S. zeamais populations from cobs (P < 0.001), as did a combination of A. melegueta and Z. officinale (5% w/w each, P < 0.001). Furthermore, significantly higher seed germination was observed in treated cobs compared with the untreated cobs in both trials (P < 0.001). Protection of cereals with such repellent materials has important practical applications in parts of the world where insecticides are expensive or in short supply, and where these materials are cheap and readily available for local use by resource-poor farmers. In addition, the use of repellents to protect stored maize grains has the potential for minimising the requirement for broad-spectrum toxic insecticides, thereby reducing the development of insecticide resistance. Crown Copyright Ó 2011 Published by Elsevier Ltd. All rights reserved.
Keywords: Aframomum melegueta Zingiber officinale Zea mays Sitophilus zeamais Storage African granaries
1. Introduction Maize, Zea mays L. (Poaceae), one of the most important food crops, is cultivated globally by resource-poor farming regions on more than 25 million ha in sub-Saharan Africa (Khan et al., 2010), and is widely grown across the different ecological zones of Nigeria, ranging from the rain forest belt in the south to the northern Guinea savannah. Maize serves as a major source of food, feed and raw material for agro-allied industries worldwide (Ishaya et al., 2008). After harvest, inadequate infrastructure, and lack of economic means, constrains smallholder farmers to store the maize crop either shelled or unshelled using traditional storage structures and procedures (Markham et al., 1994), such as cribs, baskets, jute bags, and earthen ware or in the open (Ukeh, 2008). Of all these
* Corresponding author. E-mail address: [email protected] (M.A. Birkett).
methods, the latter approach allows air to flow freely through the grain, which enhances the drying process, but also makes the store vulnerable to attack by insect pests (Holst et al., 2000). One of the major primary and economic pests of stored maize is the maize weevil, Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae), an internal feeder on grains, with great adaptation to withstand periods of starvation (Rees, 2004; Ukeh, 2008). Maize yield losses due to S. zeamais infestation of over 30% have been reported in West Africa after a few months of storage (Kossou and BosqueBerez, 1998), with similar losses (20%) in Ghana (Obeng-Ofori and Amiteye, 2005) and in the western highlands of Cameroon (12e44%) during the first 6 months of storage (Bouda et al., 2001). Apart from weight losses, the feeding damage caused by the larvae and adults of S. zeamais leads to reductions in aesthetic and market value, germination and nutritive value of maize from this region (Ukeh, 2008). Control of S. zeamais is achieved in intensive, large scale production systems with chemical contact insecticides and
0261-2194/$ e see front matter Crown Copyright Ó 2011 Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.cropro.2011.10.013
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fumigants such as pirimiphos methyl, phosphine and methyl bromide. However, for smallholder farmers, regulatory reasons, control failures, financial and technical constraints and development of resistance in some stored product insects to insecticides (Lorini et al., 2007; Ukeh and Mordue, 2009), has necessitated the need for the application of alternative approaches such as biopesticides (Umoetok et al., 2009). Adequate protection of harvested grains from pest infestation during storage using locally available materials could improve the quantity and quality of farm products for food and planting during the next farming season. In view of the potential of natural plant products (Isman, 2006; Rajendran and Sriranjini, 2008) in small-scale farm holdings typical of bulk grain production in sub-Sahara Africa, there has been growing interest in evaluating their efficacies and elucidating the basis of their protective action (Bouda et al., 2001; Tapondjou et al., 2002; Rattan, 2010). Previous ethnobotanical considerations suggested that two plant species, alligator pepper, Aframomum melegueta (Roscoe) K. Schum, and ginger, Zingiber officinale Roscoe (both Zingiberaceae), found in Southeast Nigeria, have the ability to control stored grain insect pests (Ofuya, 1990). With the aim of providing underpinning science for wide scale use of these materials in S. zeamais control by resource-poor farmers, laboratory based studies confirmed that A. melegueta seeds and Z. officinale rhizomes were directly repellent to adult S. zeamais, even in the presence of maize seeds (Ukeh et al., 2009, 2010). Prior to the wide scale application of the repellent materials in stored maize protection, demonstration of activity under controlled field conditions must be presented, in order to determine and optimise the parameters for application. Thus, the aim of this study was to evaluate the efficacy of A. melegueta and Z. officinale against S. zeamais in traditional storage facilities in Southeast Nigeria.
2. Materials and methods 2.1. Site description and construction of traditional storage barns Experiments were carried out in the rural farming district of Bebuatsuan (comprising eight villages) in Obudu Local Government Area of Cross River State, Nigeria (latitude 6 390 and 43 380 North and longitude 9 090 and 10 010 East, elevation of 194.16 m) from November 2006 to February 2007, and repeated from November 2009 to February 2010. Cross River has a humid tropical climate with total annual rainfall of 1500e3000 mm, humidity of 65e90%, ambient temperatures of 22.2 Ce23.8 C minimum, and 27 Ce40 C maximum (FRN Gazette, 2007). Four square-shaped storage barns were constructed with each barn measuring 2.5 2.5 m 3 m in height and were set 20 m apart. All barns were constructed using wooden poles, thatch roof and bamboo walls in accordance with the local storage pattern, whereby up to 80% of local farmers store their products in this manner (Ukeh, 2008).
2.2. Seeding of the field experiment site At each storage barn at the time of this study, the environment was seeded with the local strain of S. zeamais, cultured on white maize collected from the department of Crop Science, University of Calabar, Nigeria, to boost the weevil population at the study site. Five hundred unsexed S. zeamais were sprinkled around each barn at a distance of 3 m away from the walls. Seeding was carried out at 18:00 h local time following the methods of Ukeh (2008) to avoid predation of seeded weevils by local poultry reared by the resource-poor farmer as a part of the farm enterprise.
2.3. Plant material collection and processing Aframomum melegueta fruits and Z. officinale rhizomes were collected over a period of 2 weeks from fields around Akamkpa Local Government Area and some supplied by local farmers of Bebuatsuan community where the study was conducted. A. melegueta fruits were sun dried for 2e3 days, after which the seeds were extracted and Z. officinale rhizomes were sliced, dried in the shade for 5 days. The dried plant materials were pounded to powdered form using a local wooden mortar and pestle, and sieved through a mesh of <2 mm diameter. Several batches of fresh local ‘Ikom white’ maize variety cobs were bought from the Cassava and Maize Growers’ Cooperative Society in Obudu Local Government Area of Cross River State, Nigeria in 2006 and 2009 respectively. The ripe maize cobs were dehusked and sun-dried for 2e3 days before being used for the field experiment. 2.4. Trial design and protocol Before setting up the trials, a total of 10 whole, dehusked cobs of maize were randomly selected from the samples, shelled and assessed for S. zeamais infestation, in order to obtain baseline information of pre-existing pest infestation. In each of the four storage barns, 4 baskets containing 18 kg of shelled maize cobs and 10% (w/w) test plant materials (at a distance of approximately 2 m apart) were set up as described below: Treatment 1: 18 kg of maize þ 2 kg A. melegueta seed material; Treatment 2: 18 kg of maize þ 2 kg Z. officinale rhizome material; Treatment 3: 18 kg of maize þ 1 kg A. melegueta seed material þ 1 kg Z. officinale rhizome material; Treatment 4: Control (18 kg of maize alone). Earlier laboratory investigation showed that 10% plant material combined with maize grains (w/w) gave adequate protection against the maize weevil comparable to 33% plant material (Ukeh et al., 2010). The required quantities of each plant material were mixed with the maize cobs manually in baskets. All the baskets were covered with dried banana leaves, in order to protect them from dust. The treatments were laid out in a randomised complete block design in each storage barn, and each treatment was replicated 4 times. Treatments were sampled weekly, and at each sampling occasion 2 ears were randomly taken from each basket, shelled, the grain sieved, and the weevils counted (Ukeh, 2008). Data on other insect species were discarded because they were beyond the scope of this study. 2.5. Assessment of seed germination Two cobs were randomly selected from each replicate at 12 weeks post-treatment, shelled and 50 seeds from each replicate were again randomly picked for the germination test. The seeds were soaked in distilled water for about 30 min after which time the seeds were removed and placed in labelled Petri dishes lined with Fisherbrand QL 100 filter paper and then covered and moistened daily with distilled water. Four days later, germination was assessed by calculating the number of seeds germinated out of the total of 50 in each Petri dish. 2.6. Data analysis Data generated on the counts of S. zeamais per 2 cobs sampled per treatment per time interval were subjected to statistical analysis using repeated measures ANOVA. Measurements on the same treatment were taken over twelve consecutive weeks, imposing
D.A. Ukeh et al. / Crop Protection 32 (2012) 99e103
Germination % ¼
Mean no: of sprouted seeds 100 Total No: of seeds in Petri dish
3. Results
Mean no. of weevils /2 cobs
a
5
Maize + A. melegueta Maize + Z. officinale
4
Maize + A. melegueta + Z. officinale Control
3
2
1
0
0
b
5
3
4
5
6
7
8
9
10
11
12
8
9
10
11
12
Maize + A. melegueta Maize + Z. officinale
4
Maize + A. melegueta + Z. officinale Control
3
2
1
0
Table 1 Mean standard error (SE) number of adult maize weevils, Sitophilus zeamais, counted 12 weeks post treatment, found in maize cobs either untreated, or treated with A. melegueta and Z. officinale materials in traditional storage barns in Nigeria.
Maize cobs plus A. melegueta Maize cobs plus Z. officinale Maize cobs plus A. melegueta þ Z. officinale Untreated maize cobs (Control) P-value F Df (156)
2
0
The mean number of S. zeamais adults found in stored maize cobs 12 weeks post harvest was significantly lower (P < 0.001) for cobs that were treated with A. melegueta, Z. officinale, and both plant materials, compared to the untreated maize cobs stored alone (Table 1). However, the number of S. zeamais in stored cobs was not significantly different between maize plus A. melegueta, maize plus Z. officinale and maize plus A. melegueta and Z. officinale (P > 0.05) during the two trials (Table 1). Analysis of the weekly population levels revealed that S. zeamais populations in maize cobs were reduced soon after treatment with A. melegueta and Z. officinale, but increased gradually after the first week after treatment up to the 10th week (Fig. 1a, b). There were significant differences in the mean weekly weevil population (F12, 36 ¼ 21.43; P < 0.001), and treatment main effects (F3, 36 ¼ 95.49; P < 0.001), between the treated maize cobs and untreated maize cobs in 2006/2007 trials (Fig. 1a). Similarly, there were significant differences in the weekly S. zeamais population
Treatments
1
Time (weeks)
Mean no. of weevils /2 cobs
a higher correlation between measurements at two consecutive weeks than between measurements far apart in time. Accounting for this, an ante-dependence model of first order (Gabriel, 1962) was fitted using residual maximum likelihood (REML) methods (Patterson and Thompson, 1971). An ante-dependence model states that a measurement at a particular week depends on the previous ones, with the degree of dependence decaying with time lag. The order of the ante-dependence model establishes how far back in time a measurement made at present depends on the preceding ones. The purpose of this analysis was to examine the effects of the four treatments described above on counts of S. zeamais, the effects of time and the interaction between treatment and time. The response variable was subjected to square root transformation (Ox þ 0.05) in order to stabilise the variance (where x ¼ count of S. zeamais). The fixed component of the ante-dependence model was set to the product between time (indicating the week when the insect counts took place and ranging from 0 to 12) and treatment (indicating the treatments applied; A. melegueta, Z. officinale, A. melegueta þ Z. officinale and Control). The random component was set to corn.time, where factor corn indicated the plant that provided the count. All analyses were done using Genstat for Windows, thirteenth edition (Genstat 13, 2010). Data on seed germination were converted to simple percentages after analysis of variance (ANOVA) as follows;
101
1
2
3
4
5
6
7
Time (weeks) Fig. 1. Mean standard error (SE) weekly population levels of S. zeamais per 2 stored maize cobs, either untreated, or treated with A. melegueta and Z. officinale materials, in traditional storage facilities in Nigeria (1a ¼ 2006/2007; 1b ¼ 2009/2010). Data were analysed using repeated measures analysis of variance (ANOVA) with treatment, time and treatment x time as fixed effects.
main effects (F12, 36 ¼ 23.82; P < 0.001) and main effects for treatments (F3, 36 ¼ 54.37; P < 0.001) between maize cobs treated with plant products and the untreated cobs during the 2009/2010 field trials (Fig. 1b). However, there were no significant interactions between time and treatments (F36 ¼ 1.43; P ¼ 0.070) during 2006/ 2007 and (F36 ¼ 0.88; P ¼ 0.659) in 2009/2010 respectively. The percentage germination of seeds in the various treatments was significantly higher in the treated cobs in 2006/2007 (F3, 12 ¼ 12.44, P < 0.001) and 2009/2010 (F3, 12 ¼ 19.48, P < 0.001) compared to the untreated cobs during both trials. The highest seed germination was observed in maize cobs treated with a combination of A. melegueta and Z. officinale (Fig. 2a and b).
4. Discussion
Mean no. of S. zeamais/2 cobs 2006/2007
2009/2010
1.07 0.05b 1.21 0.05b 0.97 0.05b
1.21 0.05b 1.22 0.05b 1.18 0.05b
2.03 0.05a 0.001 95.49 3
1.89 0.05a 0.001 54.37 3
Means in the same column followed by the same letter are not significantly different at the 0.05 level.
The application of plant materials to protect stored products from pest attack is an ancient practice in Africa and Asia (Poswal and Akpa, 1991). The results presented in this study show unequivocally that two local plant species, A. melegueta and Z. officinale, are able to reduce the adult S. zeamais populations in stored maize under storage granary conditions. This is in line with earlier laboratory studies, which demonstrated repellency in behavioural studies, and which also identified the compounds (S)-2-heptanol, (S)-2-heptyl acetate and (R)-linalool from A. melegueta, and 1,8-cineole, neral and geranial from Z. officinale as
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a
100
Mean % germination
a
a
a
80
b 60
40
20
0 A. melegueta
b
A. melegueta + Z. officinale
Control
100
a Mean % germination
Z. officinale
a
a
80
60
b
40
20
0 A. melegueta
Z. officinale
A. melegueta + Z. officinale
Control
Fig. 2. Mean standard error (SE) percentage germination of maize seeds collected from cobs either untreated or treated with A. melegueta and Z. officinale, after field trials in Nigeria (2a ¼ 2006/2007; 2b ¼ 2009/2010 trials). Bars with the same letter are not significantly different at the 0.05 level.
responsible for repellent activity (Ukeh et al., 2009). The plant materials were effective in reducing S. zeamais populations from stored maize, when compared with control untreated maize, at 10% (w/w) and a combination of 5% (w/w) of each plant material. A combination of the two plant materials did not produce any significant synergistic or additive effect on their repellency against S. zeamais. It was observed that the mean number of visiting weevils to treated maize cobs fell one week after the admixture with the repellent materials, while the number of insects in the untreated maize cobs continued to increase week by week. Maize cobs were significantly protected by these treatments from pest infestation up to 10 weeks in traditional storage granaries. Furthermore, the higher germination percentages of treated cobs presumably reflected the smaller amount of seed damage by weevils, and suggest that the biological activity of A. melegueta and Z. officinale suppressed oviposition by S. zeamais. This result is consistent with the findings of Bekele et al. (1995) who reported the repellent effect of dried ground leaves (25 g/250 g of maize seeds) and essential oil (0.3 mg/250 g of maize seeds) of Ocimum kilimandscharicum (Labiatae) against S. zeamais, Rhyzopertha dominica (Fabricius) and Sitotroga cerealella (Oliv.) resulting in lower weight loss and number of damaged maize seeds compared with untreated grains. Adedire and Akinneye (2004) also demonstrated the insecticidal activity of Tithonia diversifolia (Asteraceae) powder and extract against Callosobruchus maculatus (F.) resulting to reduced oviposition and adult emergence in southwest Nigeria. The result is also in agreement with Derbalah and Ahmed (2011) who reported that the powder and oil of Mentha viridis (Lamiaceae) caused significant adult S. oryzae (L.) mortality and reduced
progeny emergence. Under small-scale farmer conditions, as is the case in this study, botanically-derived materials may protect stored grains for several weeks at a time, suggesting that such materials have potential for use in resource-poor and traditional farm storage conditions, in developing and under-developed countries (Weaver and Subramanyam, 2000; Nikpay, 2007; Mulungu et al., 2007). Generally, since plant products are bioactive against specific pest species, biodegradable in the environment, non-toxic to natural enemies and potentially suitable for use in integrated pest management programmes (Isman, 2006; Ukeh and Mordue, 2009), they could be exploited for use as safer stored-product pest control agents. This study was carried out in close association with resource poor farmers in rural farming communities of Obudu in southern Nigeria, with a view to strengthening the capacity of farmers to increase productivity and income in a low-cost, sustainable and environmentally friendly manner. Similar studies have been conducted in western Kenya where rural farmers adopted the low economic input push-pull approach to control stem borers and parasitic weeds in African cereals, with the resulting increase in maize grain yields, improved fodder and milk productivity (Khan et al., 2008, 2010). However, since S. zeamais populations started to-establish after several weeks, this suggests that S. zeamais is gradually able to overcome the efficacy of A. melegueta and Z. officinale in the absence of an alternative suitable food source. It is therefore vitally important to develop a pull component, comprising a trapping system containing attractive kairomones, in order to remove the weevil population once repelled from stored maize by A. melegueta and Z. officinale. Further studies are underway to identify the attractive kairomones from stored maize seed, with a view to deployment in suitable trapping systems in storage houses. In summary, this study along with our previous investigations (Ukeh et al., 2009, 2010) provides underpinning science for use of repellent or antifeedant plant materials in stored product pest control, and provides chemical markers for quality assurance and control if the envisaged control system breaks down. As highlighted above, these plant materials could be used as a push component, in conjunction with a pull component in traps to capture pest species. From an economic perspective, farmers could also be encouraged to expand the existing cultivation of A. melegueta and Z. officinale, thereby not only providing economic and social benefits through enhanced stored maize production, but also by generating income from new products. Acknowledgements This study was funded by a Commonwealth Scholarship award to Donald Ukeh for a PhD at the University of Aberdeen. The research was carried out in collaboration with the Biological Chemistry Department, Rothamsted Research, Harpenden, UK. Rothamsted Research receives grant-aided support from the Biotechnology and Biological Sciences Research Council (BBSRC) of the United Kingdom. The authors are grateful to Dr. Elisa Loza of Rothamsted Research for statistical advice. References Adedire, C.O., Akinneye, J.O., 2004. Biological activity of tree marigold, Tithonia diversifolia, on cowpea seed bruchids, Callosobruchus maculatus (Coleoptera: Bruchidae). Ann. Appl. Biol. 144, 185e189. Bekele, J., Obeng-Ofori, D., Hassanali, A., 1995. Products derived from the leaves of Ocimum kilimandscharicum (Labiatae) as post-harvest grain protectants against the infestation of three major stored product insect pests. Bull. Entomol. Res. 85, 361e367. Bouda, H., Tapondjou, L.A., Fontem, D.A., Gumedzoe, M.Y.D., 2001. Effects of essential oils from leaves of Ageratum conyzoides, Lantana camara and
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Alligator pepper, Aframomum melegueta, and ginger, Zingiber officinale, reduce stored maize infestation by the maize weevil, Sitophilus zeamais in traditional African granaries Donald A. Ukeh a, b, c, Sylvia B.A. Umoetok a, Alan S. Bowman b, A. Jennifer Mordue (Luntz) b, John A. Pickett c, Michael A. Birkett c, * a b c
Department of Crop Science, University of Calabar, PMB 1115, Calabar, Nigeria School of Biological Sciences, University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK Biological Chemistry Department, Rothamsted Research, Harpenden, Herts AL5 2JQ, UK
a r t i c l e i n f o
a b s t r a c t
Article history: Received 11 May 2011 Received in revised form 18 October 2011 Accepted 19 October 2011
Alligator pepper, Aframomum melegueta (Roscoe) K. Schum, and ginger, Zingiber officinale Roscoe were tested for their efficacy in protecting stored maize cobs (Zea mays L.) against the maize weevil, Sitophilus zeamais Motschulsky, in traditional maize storage barn conditions, from November 2006 to February 2007, and November 2009 to February 2010 in Obudu, Southeast Nigeria. A randomised complete block design was used in each storage barn with four treatments (maize, maize plus A. melegueta, maize plus Z. officinale, maize plus A. melegueta and Z. officinale) replicated 4 times. When used in combination with stored maize cobs at a level of 10% (w/w), A. melegueta and Z. officinale significantly reduced S. zeamais populations from cobs (P < 0.001), as did a combination of A. melegueta and Z. officinale (5% w/w each, P < 0.001). Furthermore, significantly higher seed germination was observed in treated cobs compared with the untreated cobs in both trials (P < 0.001). Protection of cereals with such repellent materials has important practical applications in parts of the world where insecticides are expensive or in short supply, and where these materials are cheap and readily available for local use by resource-poor farmers. In addition, the use of repellents to protect stored maize grains has the potential for minimising the requirement for broad-spectrum toxic insecticides, thereby reducing the development of insecticide resistance. Crown Copyright Ó 2011 Published by Elsevier Ltd. All rights reserved.
Keywords: Aframomum melegueta Zingiber officinale Zea mays Sitophilus zeamais Storage African granaries
1. Introduction Maize, Zea mays L. (Poaceae), one of the most important food crops, is cultivated globally by resource-poor farming regions on more than 25 million ha in sub-Saharan Africa (Khan et al., 2010), and is widely grown across the different ecological zones of Nigeria, ranging from the rain forest belt in the south to the northern Guinea savannah. Maize serves as a major source of food, feed and raw material for agro-allied industries worldwide (Ishaya et al., 2008). After harvest, inadequate infrastructure, and lack of economic means, constrains smallholder farmers to store the maize crop either shelled or unshelled using traditional storage structures and procedures (Markham et al., 1994), such as cribs, baskets, jute bags, and earthen ware or in the open (Ukeh, 2008). Of all these
* Corresponding author. E-mail address: [email protected] (M.A. Birkett).
methods, the latter approach allows air to flow freely through the grain, which enhances the drying process, but also makes the store vulnerable to attack by insect pests (Holst et al., 2000). One of the major primary and economic pests of stored maize is the maize weevil, Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae), an internal feeder on grains, with great adaptation to withstand periods of starvation (Rees, 2004; Ukeh, 2008). Maize yield losses due to S. zeamais infestation of over 30% have been reported in West Africa after a few months of storage (Kossou and BosqueBerez, 1998), with similar losses (20%) in Ghana (Obeng-Ofori and Amiteye, 2005) and in the western highlands of Cameroon (12e44%) during the first 6 months of storage (Bouda et al., 2001). Apart from weight losses, the feeding damage caused by the larvae and adults of S. zeamais leads to reductions in aesthetic and market value, germination and nutritive value of maize from this region (Ukeh, 2008). Control of S. zeamais is achieved in intensive, large scale production systems with chemical contact insecticides and
0261-2194/$ e see front matter Crown Copyright Ó 2011 Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.cropro.2011.10.013
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fumigants such as pirimiphos methyl, phosphine and methyl bromide. However, for smallholder farmers, regulatory reasons, control failures, financial and technical constraints and development of resistance in some stored product insects to insecticides (Lorini et al., 2007; Ukeh and Mordue, 2009), has necessitated the need for the application of alternative approaches such as biopesticides (Umoetok et al., 2009). Adequate protection of harvested grains from pest infestation during storage using locally available materials could improve the quantity and quality of farm products for food and planting during the next farming season. In view of the potential of natural plant products (Isman, 2006; Rajendran and Sriranjini, 2008) in small-scale farm holdings typical of bulk grain production in sub-Sahara Africa, there has been growing interest in evaluating their efficacies and elucidating the basis of their protective action (Bouda et al., 2001; Tapondjou et al., 2002; Rattan, 2010). Previous ethnobotanical considerations suggested that two plant species, alligator pepper, Aframomum melegueta (Roscoe) K. Schum, and ginger, Zingiber officinale Roscoe (both Zingiberaceae), found in Southeast Nigeria, have the ability to control stored grain insect pests (Ofuya, 1990). With the aim of providing underpinning science for wide scale use of these materials in S. zeamais control by resource-poor farmers, laboratory based studies confirmed that A. melegueta seeds and Z. officinale rhizomes were directly repellent to adult S. zeamais, even in the presence of maize seeds (Ukeh et al., 2009, 2010). Prior to the wide scale application of the repellent materials in stored maize protection, demonstration of activity under controlled field conditions must be presented, in order to determine and optimise the parameters for application. Thus, the aim of this study was to evaluate the efficacy of A. melegueta and Z. officinale against S. zeamais in traditional storage facilities in Southeast Nigeria.
2. Materials and methods 2.1. Site description and construction of traditional storage barns Experiments were carried out in the rural farming district of Bebuatsuan (comprising eight villages) in Obudu Local Government Area of Cross River State, Nigeria (latitude 6 390 and 43 380 North and longitude 9 090 and 10 010 East, elevation of 194.16 m) from November 2006 to February 2007, and repeated from November 2009 to February 2010. Cross River has a humid tropical climate with total annual rainfall of 1500e3000 mm, humidity of 65e90%, ambient temperatures of 22.2 Ce23.8 C minimum, and 27 Ce40 C maximum (FRN Gazette, 2007). Four square-shaped storage barns were constructed with each barn measuring 2.5 2.5 m 3 m in height and were set 20 m apart. All barns were constructed using wooden poles, thatch roof and bamboo walls in accordance with the local storage pattern, whereby up to 80% of local farmers store their products in this manner (Ukeh, 2008).
2.2. Seeding of the field experiment site At each storage barn at the time of this study, the environment was seeded with the local strain of S. zeamais, cultured on white maize collected from the department of Crop Science, University of Calabar, Nigeria, to boost the weevil population at the study site. Five hundred unsexed S. zeamais were sprinkled around each barn at a distance of 3 m away from the walls. Seeding was carried out at 18:00 h local time following the methods of Ukeh (2008) to avoid predation of seeded weevils by local poultry reared by the resource-poor farmer as a part of the farm enterprise.
2.3. Plant material collection and processing Aframomum melegueta fruits and Z. officinale rhizomes were collected over a period of 2 weeks from fields around Akamkpa Local Government Area and some supplied by local farmers of Bebuatsuan community where the study was conducted. A. melegueta fruits were sun dried for 2e3 days, after which the seeds were extracted and Z. officinale rhizomes were sliced, dried in the shade for 5 days. The dried plant materials were pounded to powdered form using a local wooden mortar and pestle, and sieved through a mesh of <2 mm diameter. Several batches of fresh local ‘Ikom white’ maize variety cobs were bought from the Cassava and Maize Growers’ Cooperative Society in Obudu Local Government Area of Cross River State, Nigeria in 2006 and 2009 respectively. The ripe maize cobs were dehusked and sun-dried for 2e3 days before being used for the field experiment. 2.4. Trial design and protocol Before setting up the trials, a total of 10 whole, dehusked cobs of maize were randomly selected from the samples, shelled and assessed for S. zeamais infestation, in order to obtain baseline information of pre-existing pest infestation. In each of the four storage barns, 4 baskets containing 18 kg of shelled maize cobs and 10% (w/w) test plant materials (at a distance of approximately 2 m apart) were set up as described below: Treatment 1: 18 kg of maize þ 2 kg A. melegueta seed material; Treatment 2: 18 kg of maize þ 2 kg Z. officinale rhizome material; Treatment 3: 18 kg of maize þ 1 kg A. melegueta seed material þ 1 kg Z. officinale rhizome material; Treatment 4: Control (18 kg of maize alone). Earlier laboratory investigation showed that 10% plant material combined with maize grains (w/w) gave adequate protection against the maize weevil comparable to 33% plant material (Ukeh et al., 2010). The required quantities of each plant material were mixed with the maize cobs manually in baskets. All the baskets were covered with dried banana leaves, in order to protect them from dust. The treatments were laid out in a randomised complete block design in each storage barn, and each treatment was replicated 4 times. Treatments were sampled weekly, and at each sampling occasion 2 ears were randomly taken from each basket, shelled, the grain sieved, and the weevils counted (Ukeh, 2008). Data on other insect species were discarded because they were beyond the scope of this study. 2.5. Assessment of seed germination Two cobs were randomly selected from each replicate at 12 weeks post-treatment, shelled and 50 seeds from each replicate were again randomly picked for the germination test. The seeds were soaked in distilled water for about 30 min after which time the seeds were removed and placed in labelled Petri dishes lined with Fisherbrand QL 100 filter paper and then covered and moistened daily with distilled water. Four days later, germination was assessed by calculating the number of seeds germinated out of the total of 50 in each Petri dish. 2.6. Data analysis Data generated on the counts of S. zeamais per 2 cobs sampled per treatment per time interval were subjected to statistical analysis using repeated measures ANOVA. Measurements on the same treatment were taken over twelve consecutive weeks, imposing
D.A. Ukeh et al. / Crop Protection 32 (2012) 99e103
Germination % ¼
Mean no: of sprouted seeds 100 Total No: of seeds in Petri dish
3. Results
Mean no. of weevils /2 cobs
a
5
Maize + A. melegueta Maize + Z. officinale
4
Maize + A. melegueta + Z. officinale Control
3
2
1
0
0
b
5
3
4
5
6
7
8
9
10
11
12
8
9
10
11
12
Maize + A. melegueta Maize + Z. officinale
4
Maize + A. melegueta + Z. officinale Control
3
2
1
0
Table 1 Mean standard error (SE) number of adult maize weevils, Sitophilus zeamais, counted 12 weeks post treatment, found in maize cobs either untreated, or treated with A. melegueta and Z. officinale materials in traditional storage barns in Nigeria.
Maize cobs plus A. melegueta Maize cobs plus Z. officinale Maize cobs plus A. melegueta þ Z. officinale Untreated maize cobs (Control) P-value F Df (156)
2
0
The mean number of S. zeamais adults found in stored maize cobs 12 weeks post harvest was significantly lower (P < 0.001) for cobs that were treated with A. melegueta, Z. officinale, and both plant materials, compared to the untreated maize cobs stored alone (Table 1). However, the number of S. zeamais in stored cobs was not significantly different between maize plus A. melegueta, maize plus Z. officinale and maize plus A. melegueta and Z. officinale (P > 0.05) during the two trials (Table 1). Analysis of the weekly population levels revealed that S. zeamais populations in maize cobs were reduced soon after treatment with A. melegueta and Z. officinale, but increased gradually after the first week after treatment up to the 10th week (Fig. 1a, b). There were significant differences in the mean weekly weevil population (F12, 36 ¼ 21.43; P < 0.001), and treatment main effects (F3, 36 ¼ 95.49; P < 0.001), between the treated maize cobs and untreated maize cobs in 2006/2007 trials (Fig. 1a). Similarly, there were significant differences in the weekly S. zeamais population
Treatments
1
Time (weeks)
Mean no. of weevils /2 cobs
a higher correlation between measurements at two consecutive weeks than between measurements far apart in time. Accounting for this, an ante-dependence model of first order (Gabriel, 1962) was fitted using residual maximum likelihood (REML) methods (Patterson and Thompson, 1971). An ante-dependence model states that a measurement at a particular week depends on the previous ones, with the degree of dependence decaying with time lag. The order of the ante-dependence model establishes how far back in time a measurement made at present depends on the preceding ones. The purpose of this analysis was to examine the effects of the four treatments described above on counts of S. zeamais, the effects of time and the interaction between treatment and time. The response variable was subjected to square root transformation (Ox þ 0.05) in order to stabilise the variance (where x ¼ count of S. zeamais). The fixed component of the ante-dependence model was set to the product between time (indicating the week when the insect counts took place and ranging from 0 to 12) and treatment (indicating the treatments applied; A. melegueta, Z. officinale, A. melegueta þ Z. officinale and Control). The random component was set to corn.time, where factor corn indicated the plant that provided the count. All analyses were done using Genstat for Windows, thirteenth edition (Genstat 13, 2010). Data on seed germination were converted to simple percentages after analysis of variance (ANOVA) as follows;
101
1
2
3
4
5
6
7
Time (weeks) Fig. 1. Mean standard error (SE) weekly population levels of S. zeamais per 2 stored maize cobs, either untreated, or treated with A. melegueta and Z. officinale materials, in traditional storage facilities in Nigeria (1a ¼ 2006/2007; 1b ¼ 2009/2010). Data were analysed using repeated measures analysis of variance (ANOVA) with treatment, time and treatment x time as fixed effects.
main effects (F12, 36 ¼ 23.82; P < 0.001) and main effects for treatments (F3, 36 ¼ 54.37; P < 0.001) between maize cobs treated with plant products and the untreated cobs during the 2009/2010 field trials (Fig. 1b). However, there were no significant interactions between time and treatments (F36 ¼ 1.43; P ¼ 0.070) during 2006/ 2007 and (F36 ¼ 0.88; P ¼ 0.659) in 2009/2010 respectively. The percentage germination of seeds in the various treatments was significantly higher in the treated cobs in 2006/2007 (F3, 12 ¼ 12.44, P < 0.001) and 2009/2010 (F3, 12 ¼ 19.48, P < 0.001) compared to the untreated cobs during both trials. The highest seed germination was observed in maize cobs treated with a combination of A. melegueta and Z. officinale (Fig. 2a and b).
4. Discussion
Mean no. of S. zeamais/2 cobs 2006/2007
2009/2010
1.07 0.05b 1.21 0.05b 0.97 0.05b
1.21 0.05b 1.22 0.05b 1.18 0.05b
2.03 0.05a 0.001 95.49 3
1.89 0.05a 0.001 54.37 3
Means in the same column followed by the same letter are not significantly different at the 0.05 level.
The application of plant materials to protect stored products from pest attack is an ancient practice in Africa and Asia (Poswal and Akpa, 1991). The results presented in this study show unequivocally that two local plant species, A. melegueta and Z. officinale, are able to reduce the adult S. zeamais populations in stored maize under storage granary conditions. This is in line with earlier laboratory studies, which demonstrated repellency in behavioural studies, and which also identified the compounds (S)-2-heptanol, (S)-2-heptyl acetate and (R)-linalool from A. melegueta, and 1,8-cineole, neral and geranial from Z. officinale as
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a
100
Mean % germination
a
a
a
80
b 60
40
20
0 A. melegueta
b
A. melegueta + Z. officinale
Control
100
a Mean % germination
Z. officinale
a
a
80
60
b
40
20
0 A. melegueta
Z. officinale
A. melegueta + Z. officinale
Control
Fig. 2. Mean standard error (SE) percentage germination of maize seeds collected from cobs either untreated or treated with A. melegueta and Z. officinale, after field trials in Nigeria (2a ¼ 2006/2007; 2b ¼ 2009/2010 trials). Bars with the same letter are not significantly different at the 0.05 level.
responsible for repellent activity (Ukeh et al., 2009). The plant materials were effective in reducing S. zeamais populations from stored maize, when compared with control untreated maize, at 10% (w/w) and a combination of 5% (w/w) of each plant material. A combination of the two plant materials did not produce any significant synergistic or additive effect on their repellency against S. zeamais. It was observed that the mean number of visiting weevils to treated maize cobs fell one week after the admixture with the repellent materials, while the number of insects in the untreated maize cobs continued to increase week by week. Maize cobs were significantly protected by these treatments from pest infestation up to 10 weeks in traditional storage granaries. Furthermore, the higher germination percentages of treated cobs presumably reflected the smaller amount of seed damage by weevils, and suggest that the biological activity of A. melegueta and Z. officinale suppressed oviposition by S. zeamais. This result is consistent with the findings of Bekele et al. (1995) who reported the repellent effect of dried ground leaves (25 g/250 g of maize seeds) and essential oil (0.3 mg/250 g of maize seeds) of Ocimum kilimandscharicum (Labiatae) against S. zeamais, Rhyzopertha dominica (Fabricius) and Sitotroga cerealella (Oliv.) resulting in lower weight loss and number of damaged maize seeds compared with untreated grains. Adedire and Akinneye (2004) also demonstrated the insecticidal activity of Tithonia diversifolia (Asteraceae) powder and extract against Callosobruchus maculatus (F.) resulting to reduced oviposition and adult emergence in southwest Nigeria. The result is also in agreement with Derbalah and Ahmed (2011) who reported that the powder and oil of Mentha viridis (Lamiaceae) caused significant adult S. oryzae (L.) mortality and reduced
progeny emergence. Under small-scale farmer conditions, as is the case in this study, botanically-derived materials may protect stored grains for several weeks at a time, suggesting that such materials have potential for use in resource-poor and traditional farm storage conditions, in developing and under-developed countries (Weaver and Subramanyam, 2000; Nikpay, 2007; Mulungu et al., 2007). Generally, since plant products are bioactive against specific pest species, biodegradable in the environment, non-toxic to natural enemies and potentially suitable for use in integrated pest management programmes (Isman, 2006; Ukeh and Mordue, 2009), they could be exploited for use as safer stored-product pest control agents. This study was carried out in close association with resource poor farmers in rural farming communities of Obudu in southern Nigeria, with a view to strengthening the capacity of farmers to increase productivity and income in a low-cost, sustainable and environmentally friendly manner. Similar studies have been conducted in western Kenya where rural farmers adopted the low economic input push-pull approach to control stem borers and parasitic weeds in African cereals, with the resulting increase in maize grain yields, improved fodder and milk productivity (Khan et al., 2008, 2010). However, since S. zeamais populations started to-establish after several weeks, this suggests that S. zeamais is gradually able to overcome the efficacy of A. melegueta and Z. officinale in the absence of an alternative suitable food source. It is therefore vitally important to develop a pull component, comprising a trapping system containing attractive kairomones, in order to remove the weevil population once repelled from stored maize by A. melegueta and Z. officinale. Further studies are underway to identify the attractive kairomones from stored maize seed, with a view to deployment in suitable trapping systems in storage houses. In summary, this study along with our previous investigations (Ukeh et al., 2009, 2010) provides underpinning science for use of repellent or antifeedant plant materials in stored product pest control, and provides chemical markers for quality assurance and control if the envisaged control system breaks down. As highlighted above, these plant materials could be used as a push component, in conjunction with a pull component in traps to capture pest species. From an economic perspective, farmers could also be encouraged to expand the existing cultivation of A. melegueta and Z. officinale, thereby not only providing economic and social benefits through enhanced stored maize production, but also by generating income from new products. Acknowledgements This study was funded by a Commonwealth Scholarship award to Donald Ukeh for a PhD at the University of Aberdeen. The research was carried out in collaboration with the Biological Chemistry Department, Rothamsted Research, Harpenden, UK. Rothamsted Research receives grant-aided support from the Biotechnology and Biological Sciences Research Council (BBSRC) of the United Kingdom. The authors are grateful to Dr. Elisa Loza of Rothamsted Research for statistical advice. References Adedire, C.O., Akinneye, J.O., 2004. Biological activity of tree marigold, Tithonia diversifolia, on cowpea seed bruchids, Callosobruchus maculatus (Coleoptera: Bruchidae). Ann. Appl. Biol. 144, 185e189. Bekele, J., Obeng-Ofori, D., Hassanali, A., 1995. Products derived from the leaves of Ocimum kilimandscharicum (Labiatae) as post-harvest grain protectants against the infestation of three major stored product insect pests. Bull. Entomol. Res. 85, 361e367. Bouda, H., Tapondjou, L.A., Fontem, D.A., Gumedzoe, M.Y.D., 2001. Effects of essential oils from leaves of Ageratum conyzoides, Lantana camara and
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