Synergistic efficacy of three botanical powders against Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae) in maize grain storage

doi:10.21203/rs.3.rs-4617144/v1

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Synergistic efficacy of three botanical powders against Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae) in maize grain storage

https://doi.org/10.21203/rs.3.rs-4617144/v1

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Sitophilus zeamais Motschulsky infestation causes severe post-harvest losses of grains in Ghana leading to a major reduction in the quality and economic value. The synergistic efficacy of three botanical powders against adult S. zeamais was assessed. The botanical powders of Aframomum melegueta, Pipper nigrum, and Zingiber officinale in unmixed forms as positive controls, and admixed forms and the synergy were evaluated against the adult Sitophilus zeamais in stored maize grains at different dosage rates. The botanical powders in admixed and unmixed forms were used to treat 100g of maize grains infested with 40 adult S. zeamais at dosage rates of 0g, 10g, 20g, and 30g. The treatments were kept in glass jars covered with muslin cloth for 28 days post-exposure. The experiment was laid out in a completely randomized design. The highest mean adult mortality was recorded from admixed alligator pepper + black pepper at 20g and 30g at day 21, followed by the admixed alligator pepper + black pepper at 30g at day 28. The lowest mean maize grain damage in the admixed botanicals was recorded from alligator pepper + black pepper at 30g exposure at day 28. From the results, we found that the admixed powders demonstrated anti-feedant properties. The study found synergy between the admixed botanical powders in affecting adult S. zeamais mortality and the prevention of grain damage. Their effectiveness in affecting adult S. zeamais mortality and maize grain damage is dose dependent. Farmers could apply the botanical powders in admixed forms to exert stronger efficacy against S. zeamais.

maize weevil

alligator pepper

black pepper

ginger

synergy

botanical powders

The world's population is predicted to reach 9.1 billion people by the year 2050, with the fastest expansion occurring in developing countries (FOA 2013). Many of these countries are currently dealing with hunger and are food insecure (Kitinoja et al. 2011). According to Hodges et al. (2011), to meet the food needs of this growing population, an additional 70% of food production would be required to supplement the existing production levels. Maize (Zea mays. L) is one of the most important cereal grain crops and it makes up a significant component of the staple diet for over 1.2 billion people in sub-Saharan Africa and Latin America (IITA 2020; Nuss and Tanumihardjo 2010). It is regarded as a food security crop in Africa in an effort to solve current and future food insecurity challenges as it provides a sizable portion of daily calories (Emily 2010).

Despite its numerous importance as a food security and nutrition crop in different parts of the world, significant postharvest losses in maize grains which include the consumption of grain kernels directly, disposition of exuviae, loss of grain weight, and quality that negatively impact market value and grain wholesomeness affect the world's economy and food security (Adarkwah et al. 2018; Arlian 2002; Ngom et al. 2021). According to Arifuzzaman et al. (2016) and Castro-lvarez et al. (2015), between 20 and 90% of storage grain losses occur annually and are mostly attributable to insect pest damage with the S. zeamais being identified as a major destructive pest in this regard.

The pest has been managed using a variety of strategies, with synthetic chemical insecticides and fumigants being the most widely adopted, particularly, in countries with limited advanced storage facilities (Anankware et al. 2013; Daglish 2008; Singh 2017). The use of a chemical control approach to managing insect pests has had a significant, negative impact on the environment (Boafo and Lyons 2023; Kumar et al. 2024; Yakubu et al. 2023). Chemical pesticides are highly non-selective, and many of them are poisonous to the environment and dangerous to human health (Acharya 2023). The long-term application of synthetic insecticides is unsustainable, due to the negative impact of pollution on the environment, residual accumulation in foods, pesticide resistance development, toxicity to non-target organisms, and the adverse public health impact on humans and the ecosystem (Mossa et al. 2018; Khan et al. 2023). It has, therefore, become necessary to identify new, efficient, and environmentally friendly options for the control of stored grain pests.

In efforts to discover an effective alternative to chemical pest control, bio-prospecting research has become more vigorous to allow countries blessed with natural resources to develop their innate abilities to support economic activities through safer and better agro-product storage against insect pests (Danho et al. 2002). Botanical pesticides are emerging strongly as alternatives to the use of synthetic chemicals for the control of stored product insect pests such as S. zeamais. Botanical pesticides have shown significant promise of being an effective alternative source for pest management because of their biological activity, biodegradability, and little effect on non-target organisms and the environment (Ayilara et al. 2023). This is because they are eco-friendly, safe, and cost-effective with little or no deleterious effect on humans and livestock (Owusu 2001; Sim et al. 2006; Singh 2017). For example, the toxicity of the extracts of turmeric (Curcuma longa), alligator pepper (Aframomum melegueta), and black pepper (Piper nigrum) against the S. zeamais have been widely reported (Abdussalam and Adeniji 2021; Muhammad et al. 2019; Sitaula et al. 2020; Ukeh et al. 2009). However, the synergistic effectiveness of these botanical spices for the control of S. zeamais, has not been well investigated. To enhance the adoption of botanical pesticides by farmers, empirical evidence of their effectiveness; individually and synergistically, against S. zeamais is required in order to establish their efficacy for the control and preservation of maize grain at storage. The study aimed to assess the synergistic efficacy of botanical pesticide (Aframomum melegueta, Pipper nigrum and Zingiber officinale) in their powdered form on adult mortality and grain damage against S. zeamais. The findings of this study will enhance maize storage and limit economic losses incurred by local farmers as well as warehouse operators in Ghana.

Study area, experimental materials and research design

The study was conducted at Goaso in the Asunafo North Municipal in the Ahafo Region of Ghana. The experiment was laid in a completely randomized design to ensure homogeneity with six (6) botanical treatments. Each biological treatment was replicated four (4) times at different dosage rates of 0g, 10g, 20g, and 30g. The botanical plant extracts include alligator pepper powder alone, black pepper powder alone, ginger powder alone, alligator pepper + black pepper powders, alligator pepper + ginger powders, and black pepper + ginger powders. The botanical powders in the unmixed forms served as positive controls.

Sourcing and preparation of plant extracts

The plant materials consisting of alligator pepper (Aframomum melegueta), black pepper (Piper nigrum), and ginger (Zingiber officinale) were obtained from the Goaso local market in the Ahafo Region of Ghana. The seeds of alligator pepper and black pepper were cleaned and sun-dried for 5 days to achieve adequate dehydration and were grinded into a fine powder using a clean, dry mill. The ginger rhizomes were cleaned and sliced into pieces and sun-dried for 10 days, after which it was pulverised into a fine powder with the use of a clean dry mill. The powders were kept separately in labelled containers for three days before use. Sitophilus zeamais infested maize grains were obtained from the Goaso local market in the Ahafo region of Ghana. Untreated maize grains were sourced from local farmers. A magnifying lens (hand-held COMBR 100mm focal length optical convex lens) was acquired for use in the identification of sexes of the S. zeamais. Other materials including a digital weighing scale (Fuzion Digital Gram Scale – 0.01g/500g), muslin cloth, and rubber bands were also acquired locally for the experiment.

Insect Culture

The healthy untreated maize grains obtained from the local farmers were kept in the freezer (Midea HD-172F (N)) for 96 hours at a temperature of 5 ^oC to prevent possible infestations and destroy any micro-organisms. The grains were sun-dried for two days after refrigeration to achieve adequate dehydration. Five hundred grams (500g) of the maize grains were placed in a 250ml glass jar and infested with an unspecified number of unsexed adult S. zeamais. The open end of the glass jar was covered with muslin cloth and fastened with rubber bands. The glass jar was kept for 15 days to allow for oviposition, after which the adult weevils were sieved out using a RETSCH 100mm diameter stainless steel test sieve, and the grains were kept undisturbed to allow for the emergence of the first filial (F₁) progenies that were used for the bioassay. The adult S. zeamais were sexed using the description by Devi et al. (2017).

Bioassay Procedure

One hundred grams (100g) of the maize grains were weighed using an electronic precision weighing scale (Fuzion Digital Gram Scale – 0.01g/500g) and placed in glass jars. Each 100g of maize grains was treated separately with different botanical treatments at the dosage rates of 0g, 10g, 20g, and 30g. The combined botanical powders of alligator pepper and black pepper (AP + BP), alligator pepper and ginger (AP + GP), and black pepper and ginger (BP + GP) were mixed with half rates of the individual powders at a ratio of 1:1. The glass jars were infested with forty (40) F₁ progenies of the S. zeamais. The open ends of the glass jars were covered with muslin cloth and tightened with rubber bands. The containers were kept at a temperature of 26 ± 2°C and relative humidity of 70 ± 5%. The bioassay experiment was repeated two time.

Data Collection

Weevil Mortality Assessment

Insects were assumed dead upon failure to respond to a series of probes with a blunt dissecting probe. Weevil mortalities were assessed at 7-day intervals over 28 days (7d, 14d, 21d, and 28d). A simple count of dead weevils in the treatments was conducted separately and recorded accordingly. Abbott's formula of correctness was used to analyse the mortalities (Abbot 1925).

$$Percentage control= \frac{X-Y}{X} x 100$$

Where X = the percentage living in the control, Y = the percentage living in the treatment: then X - Y = the percentage killed by the treatment.

Grains Damage Assessment

Damage caused by adult maize weevils in each treatment was assessed at a week interval post-exposure (Asawalam et al. 2007). The grains in each treatment were sieved to separate the grains, dust, and plant extracts. Grains were separated into damaged and undamaged grains and were counted and recorded. The percentage of damaged grains was calculated using the formula:

$$Percentage damage= \frac{Number of grains perforated}{Total number of grains} x 100$$

Statistical Analysis

Statistical Analysis was performed with Sigma Plot for Windows Version 15. Data was transformed using the Square Root and subjected to one-way Analysis of Variance (ANOVA). The means were separated using Tukey’s Honestly Significant Difference (Tukey’s HSD) test at 5% level of probability.

The insecticidal efficacy of powdered admixed and unmixed against adult S. zeamais exposed to varying dosages was significant (P < 0.05) different among the various treatments. Maize grains treated with 30g powder of unmixed alligator pepper significantly caused 93.33% mortality of adult S. zeamais (P < 0.01) at 28 days (Fig. 1a). The maize grains treated with 30g unmixed black pepper powder recorded 84.17% mortality of adults whilst unmixed ginger powder recorded 78.33% mortality after 28 days. However, the lowest insecticidal efficacy of the unmixed pepper powders and unmixed ginger powder was recorded when a lower dose was used (Fig. 1b and 1c).

The admixture of alligator pepper powder and black pepper powder demonstrated strong insecticidal efficacy against the adult S. zeamais at different dosage rates. The results revealed that as the concentration of admixture of alligator pepper powder and black pepper powder increases, the mortality of the adult S. zeamais increases and decreases at lower concentrations (Fig. 1d). However, there was no significant difference (P > 0.05) among 20g and 30g of all the botanical powder mixtures. The exposure of the S. zeamais to 30g of the admixed powders of alligator pepper + black pepper significantly caused the highest mortality (99.17%) at day 14 compared to the control. Furthermore, the admixed form of alligator pepper + black pepper at 20g and 30g caused 100% mortality of the adult S. zeamais at day 21 (Fig. 1d). Maize grains treated with 20g and 30g of alligator pepper + ginger in admixed form caused 100% mortality of S. zeamais at day 28 (Fig. 1e). Adult S. zeamais exposed to higher dosage (30g) dosage of admixed powders of black pepper and ginger powders caused 100% mortality at day 28 (Fig. 1f).

The difference in grain damage observed in the treated maize grains at different dosage rates was significantly different among the treatments and the control (Fig. 2). Generally, the admixed powders demonstrated higher efficacy in preventing grain damage compared to the unmixed botanical powders. Maize grains treated with 30g of admixed powders of alligator pepper and black pepper recorded the lowest grain damage (14.6%), followed by the admixture of alligator pepper and ginger powder (20.2%). At 30g dosage rate, the black pepper and ginger admixed showed the least effectiveness among the admixed powders at suppressing damage to grains (23.0%), by the S. zeamais at day 28. Among the powders, the unmixed alligator pepper powder at 30g showed the highest damage suppression (24.3%) caused by S. zeamais, whereas the ginger powder showed the lowest efficacy against grain damage caused by S. zeamais (38.4%) at 30g dosage rate at day 28. It was further noticed that the botanical powders, either in their unmixed forms or as admixtures suppressed grain damage caused by the adult S. zeamais compared to the controls. Generally, the grain damage caused by the adult S. zeamais decreases with increasing dosage rate (i.e. 10g < 20g < 30g).

Postharvest losses caused by insect pests have been a challenge to poor resource farmers in Sub-Saharan African countries (Barau et al. 2023; Hell et al. 2012; Tadesse 2020). We assessed the synergistic efficacy of some common botanical powders with insecticidal properties for the control of adult maize weevils. From our results. The insecticidal efficacy of the bio-pesticide significantly reduced the population of the adult S. zeamais post-exposure at different dosage rates compared to the control. The different botanical powders demonstrated high insecticidal efficacy against adult S. zeamais. This corroborates with the findings of Abdussalam and Adeniji (2021) who reported significant mortality of adult S. zeamais in maize grains treated with Aframomum melegueta and Moringa oleifera extracts. The admixed botanical powders exerted a more comprehensive insecticidal effect against adult S. zeamais. This observation was similar to a study by Okon 2019 who observed higher efficacy of combined botanical extracts, relative to extracts that are applied alone. Generally, synergistic chemical formulations react more quickly than natural unmixed botanical formulations. This is because the lethal effectiveness of combined botanical extracts becomes enhanced through the boosted reactions of the chemical components of the individual extracts. Additionally, the combined action of multiple control chemicals has a benefit in that such tactics reduce the issue of insect populations acquiring resistance (Khaliq et al. 2020; Nigam et al. 2011). The study findings, therefore, highlight the efficacious superiority of the synergy of the botanical powders on adult S. zeamais mortality over the treatments with the powders in their unmixed state. Furthermore, the phytochemicals of majority of synergists block certain metabolic systems of the insect (Nigam et al. 2011), thereby, inhibiting their smooth metabolic activities for effective functioning (Khaliq et al. 2020). The compelling synergistic insecticidal efficacy of admixed botanical powders against the adult S. zeamais could, therefore, provide an alternative effective and safe grain storage. The use of conventional inorganic chemical protection against the S. zeamais, as opposed to the application of botanicals comes with serious residual, resistance development, environmental contamination, and other health public implications (De-Souza et al. 2013).

It could further be argued that the combined effect of the individual extracts in the admixed botanical powders complemented the efficacy of each other to achieve higher insecticidal effectiveness against the adult S. zeamais. The synergy of botanical derivative actions depends on the active components present in them that complement each other for specific actions. According to Gilbert and Alves (2003), synergy may be as a result of the protection of an active substance from degradation by enzymes or the facilitation of transport of an active principle across barriers such as cell and organelle walls. Synergy may also occur as a result of the overcoming of multiple drug resistance mechanisms or the provision of other signals to the host cells that result in higher efficacy of the crude active ingredient compared with the isolated components. This confirms the assertion of Chaudha et al. (2021) and Palombo and Semple (2002) that combined elements could develop synergy between them that may enhance the effectiveness of each other beyond the levels that could be achieved by the individual elements. Although, among the admixed powders, the black pepper and ginger admixed powders were seen as the least effective in insecticidal potency among the admixed group, the complementary effectiveness of the constituent bioactive compounds was observed to have enhanced its ability to exert higher insecticidal effect on the adult S. zeamais than the applications in their unmixed forms. Synergistic interactions in botanical extract bioactivities are of vital importance to explain the challenges in isolating a single active ingredient, and the efficacy of apparently low doses of active constituents in a single botanical product (Chacon et al. 2022; Reddy and Chowdary 2021; Williamson 2001)

The trend of insect mortality also demonstrated that insecticidal effectiveness was dose dependent. In all treatments, the highest mortality was recorded in the higher dosage rate of 30g, followed 20g, and least in the 10g dosage rate. It could, therefore, be deduced that higher dosage rates of botanical extracts exert higher toxicity to the insect to influence higher mortalities. Other studies have similarly reported higher toxicity against storage insect pests at the applications of botanical extracts at higher concentrations (Abdussalam and Adeniji 2021; Sajjad et al. 2014; Sitaula et al. 2020). Mortality was also observed to increase with an increased duration of exposure to the botanical powders.

The observed reduced damage caused by the adult S. zeamais in the mixed botanical powder treatments at different dosage rates, compared to the powders in their unmixed forms, was in conformity with Gemuchie et al. (2013), who observed similar reduced damage caused by the insect pests in mixed plant powders. The phenomenon may be due to the presence of antifeedant and oviposition deterrent properties in the different botanical powder extracts that act in synergy to control grain damage. The treatments with the powders of alligator pepper and ginger in their admixed form provided the second most efficient protection to grains from the damage caused by the adult S. zeamais. The two powders in their unmixed forms provided relatively, lower protection to the grains from the adult S. zeamais damage. This agrees with the conclusions drawn by Okon (2019) that the complementary effect of combined botanical extracts yields higher efficiency in their ability to control pests compared to the application of the extracts in their unmixed form.

The outcome of grain protection provided by the botanical powders, either in their admixed or unmixed forms were highly significant relative to the controls. Similarly, the difference between the admixed and unmixed botanical powders in the protection of grains against the damage caused by the adult S. zeamais were significant. This demonstrates the general efficacy of the botanical powders in grain damage protection, and the superiority of the admixed botanical powder in the protection of grains at storage compared to the extracts in their unmixed form as reported by Okon (2019).

The general trend of grain protection from S. zeamais damage in the various treatments was indicative of dose dependency. The grain damage caused by the adult S. zeamais was higher in lower dose botanical extract treated grains. However, at 20g and 30g concentrations of grain treatment with mixed and the unmixed botanical powders, the differences in grain damage were not significant. This suggests that increasing the dosage over 20g in the treatment of grains would not yield any significant impact in the protection of the grains from the damage inflicted by the adult S. zeamais.

The admixed botanical powders demonstrated the highest efficacy against in adult S. zeamais and limited grain damage over the application of the powders in their unmixed forms. On the basis of this finding, we concluded that synergy exists among the botanical spice powders. This synergistic efficacy has an advantage in achieving higher adult S. zeamais mortality and reduced grain damage in stored maize grains over the use of the powders in their unmixed forms. The admixed powders of alligator pepper and black pepper provided the most effective grain protection efficacy against the S. zeamais. The best dosage rate for application of the botanical powders to achieve the modest insecticidal efficacy and better grain damage protection from the adult S. zeamais, generally, is at the rate of 30g, however, no significant difference existed among 20g and 30g application rates. The use of the identified synergies to control adult S. zeamais in grains at storage could be a major tool for overcoming metabolic resistance or delay in the manifestation of resistance as well as minimize the potential for chemical residue in food chains from the use of synthetic chemical pesticides.

Ethical Approval:

Not applicable.

Consent to Participate:

Not applicableConsent for Publication: All authors agree to the publication of this work.Competing Interests: The authors declare no competing interests.

Author’s contribution

All six authors conceptualized the study. AAA, RRA and SKD collected, analyzed, and wrote the first draft of the manuscript. SA, KGS, and JPA read the first draft and second draft of the manuscript. All the authors were engaged in reviewing the final manuscript

Acknowledgement

The authors would like to thank the Department of Agriculture, Asunafo North Municipal, for allowing their laboratory facility for the study. We would further like to thank Ms. Naomi Yaa Oforiwaa and Mrs. Diana Hayford for their assistance.

Data Availability:

Data would be made available upon reasonable request from the corresponding author.

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Synergistic efficacy of three botanical powders against Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae) in maize grain storage

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Abstract

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Introduction

Materials and Methods

Study area, experimental materials and research design

Sourcing and preparation of plant extracts

Insect Culture

Bioassay Procedure

Data Collection

Weevil Mortality Assessment

Grains Damage Assessment

Statistical Analysis

Results

Discussion

Conclusion

Declarations

Author’s contribution

Acknowledgement

Data Availability:

References

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