Next Article in Journal
Spotted Fever Group Rickettsioses in Central America: The Research and Public Health Disparity among Socioeconomic Lines
Next Article in Special Issue
Lymantria dispar (L.) (Lepidoptera: Erebidae): Current Status of Biology, Ecology, and Management in Europe with Notes from North America
Previous Article in Journal
Mechanical Acaricides Active against the Blacklegged Tick, Ixodes scapularis
Previous Article in Special Issue
Population Fitness of Eupeodes corollae Fabricius (Diptera: Syrphidae) Feeding on Different Species of Aphids
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Insects
Volume 13
Issue 8
10.3390/insects13080673
insects-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Efficacy of Biopesticides in the Management of the Cotton Bollworm, Helicoverpa armigera (Noctuidae), under Field Conditions

by
Lawrence N. Malinga
1,2,* and
Mark D. Laing
3
1
Agricultural Research Council–Industrial Crops, Rustenburg 0300, South Africa
2
South African Sugarcane Research Institute, Mount Edgecombe 4300, South Africa
3
School of Agricultural, Earth and Environmental Sciences, College of Agriculture, Engineering & Science, University of KwaZulu-Natal, Pietermaritzburg 3209, South Africa
*
Author to whom correspondence should be addressed.
Insects 2022, 13(8), 673; https://doi.org/10.3390/insects13080673
Submission received: 9 May 2022 / Revised: 19 July 2022 / Accepted: 20 July 2022 / Published: 27 July 2022
(This article belongs to the Special Issue Integrated Pest Management in Agricultural Crops and Forest Ecosystems)
Browse Figures
Review Reports Versions Notes

Abstract

:

Simple Summary

Cotton remains the most important cash crop in the world. The key insect pests of cotton include the African bollworm Helicoverpa armigera. This pest causes damage to crops estimated at greater than USD 2 billion per year worldwide. Excessive use of insecticides to control this pest has a negative effect on the environment, and is expensive for the farmers. The aim of this study is to explore the field efficacy of different biopesticides as an alternative to control H. armigera. Four biopesticides—namely, Eco-Bb® (Beauveria bassiana), Bb endophyte (Beauveria bassiana), Bolldex® (nucleopolyhedrovirus), and Delfin® (Bacillus thuringiensis)—were evaluated and compared with the pyrethroid Karate® (lambda-cyhalothrin) and an untreated control. Plots treated with Karate® had significantly lower numbers of H. armigera larvae compared to the untreated control, and were comparable to the plots treated with Bolldex®. On average, plots treated with Bolldex® had a high seed cotton yield compared to the other treatments. Biopesticides showed a moderate reduction in the numbers of H. armigera larvae, and could thus be used within an integrated pest management programme.

Abstract

Cotton is one of the most valuable materials in the world, popularly used in the clothing industry and other products. However, its production is limited by the high infestation of insect pests. A study was conducted to evaluate the effects of different biopesticides on the control of the African bollworm (Helicoverpa armigera) under cotton field conditions. Four biopesticides—namely, Eco-Bb® (Beauveria bassiana), Bb endophyte (Beauveria bassiana), Bolldex® (Nucleopolyhedrovirus), and Delfin® (Bacillus thuringiensis)—were evaluated and compared with the pyrethroid Karate® (lambda-cyhalothrin) and an untreated control against H. armigera. Field trials were conducted at the Agriculture Research Council, Rustenburg, in the North West Province of South Africa during the 2017 and 2018 cotton seasons. The results revealed that in plots sprayed with Karate® and Bolldex®, the numbers of H. armigera were significantly reduced compared to the untreated controls. Plots treated with Bolldex® had the lowest number of damaged bolls in 2017, while those treated with Karate® had the lowest number of damaged bolls in 2018. All treated plots had significantly fewer damaged bolls when compared to the controls. A seed cotton yield of 5987 kg/ha was recorded in the plots that were treated with Bolldex®—significantly higher than the yields from plots treated with Eco-Bb®, Delfin®, and Bb endophyte—in 2017. However, the yield in treatments with Eco-Bb®, Delfin®, and Bb endophyte was lower than that from the untreated controls during this season. In 2018, plots treated with Bolldex® had the highest yield, at 6818 kg/ha, which was not different from the other treatments. The highest average seed cotton yield of 6400 kg/ha was recorded in the plots treated with Bolldex®, followed by Karate®. In summary, the efficacy of different biopesticides against H. armigera varied significantly, while the synthetic pesticide (Karate®) and Bolldex® resulted in more consistent control of this pest. The results suggest that biopesticides may, however, have the potential for use in the sustainable control of cotton bollworms as part of integrated pest management programmes, although further work is required to support this hypothesis.

1. Introduction

Cotton, Gossypium hirsutum L. (Malvaceae), remains the most important cash crop in the world [1]. It is a fibre crop grown in more than 80 tropical and subtropical countries [2,3]. Over a century ago, cotton contributed more than 70% of the world’s fibre use—compared to about 30% of current consumption [4]. The decline is due to the development of a high number of synthetic fibres, which increased in the mid-1990s [5]. Furthermore, the decline is also attributed to climate change and pest problems, among other factors [6]. Cotton production is a major economic component in Africa, and is a significant contributor to economic growth [7]. The continent contributes approximately 8% of the cotton produced worldwide from a total of six cotton basins [8], covering over 20 countries in sub-Saharan Africa [9]. In South Africa, cotton is a significant crop produced by 250 commercial and over 2000 small-scale farmers in five provinces, namely, KwaZulu-Natal, Limpopo, Mpumalanga, North West, and Northern Cape [10,11].
The key insect pests of cotton include the African bollworm, Helicoverpa armigera Hübner (Noctuidae: Lepidoptera). This bollworm is an indigenous species considered to be a major pest of fibre crops in Africa [12], and ranks as the most important lepidopteran pest in South Africa [13,14,15]. Four heliothine species are reported as being of economic importance in Africa, but H. armigera is the only species of major economic importance [16]. This pest causes damage to crops estimated at greater than USD 2 billion annually in Asia, Europe, Africa, and Australasia [17]. Unlike most other arthropod pests, H. armigera is a polyphagous pest that infests more than 200 crop species worldwide, and can adapt to new environments [18,19]. It has a very large range of host plants, including cotton, pepper, corn, tomato, lucerne, soybean, sorghum, and tobacco [20,21]. H. armigera is a serious pest because of its polyphagy [22,23], high fecundity [24], high mobility [25], and resistance to chemical insecticides [26,27,28,29,30]. Cotton is mainly attacked by the larval stage of H. armigera [31], which causes high yield loss. Because H. armigera larvae have a habit of entering the fruit, bolls, or pods, the plant affords them good protection against chemical sprays, making control almost impossible [32]. Low economic damage thresholds in cotton require a high level of control [12], resulting in reliance on synthetic insecticides [33,34].
Worldwide, up to 60% of all commercialised insecticides are used in cotton [35]. Chemical pesticides such as pyrethroids, carbamates, and organophosphates are applied to control Helicoverpa pests [36]. Pyrethroids such as Karate® (lambda-cyhalothrin) are non-selective insecticides commonly used against pests—including lepidopterans—in cotton [37,38]. Although chemical pest control is extensively used throughout the world, it has been generally regarded as detrimental to the environment [39]. The use of chemical pesticides to control agricultural pests has resulted in secondary pest outbreaks, as well as reductions in the numbers of beneficial insects and biodiversity [19]. Excessive use of chemicals also causes economic impacts on farmers, and has a negative impact on animals [40]. Before the introduction of Bt cotton with the bacterium Bacillus thuringiensis in 1996 [41], cotton production was costly due to the high application of pesticides [42]. However, with the continuous use of Bt cotton on a large scale, H. armigera has developed resistance to Bt cotton [43,44]. Today, many agricultural chemical pesticides are under pressure to be banned due to their harmful effects, and some farmers have turned to biopesticides [45,46].
Biopesticides are used to control plant pests, and are made from living micro-organisms or natural products [47]. They are known to be economical, environmentally friendly, and target-specific [48]. Biopesticides have the potential to control yield loss without compromising the quality of the crop [49]. The bacterium Bacillus thuringiensis is one of the most used microbial biopesticides. Although Helicoverpa armigera nucleopolyhedrovirus (HearNPV) is generally used against cotton bollworms, little is understood about the interaction between the virus and host insects [50]. The use of biopesticides in Africa is minimal, accounting for only 3% of the world’s market [51]. South Africa and Kenya are the leading countries in the development and use of biopesticides in Africa [52]. By 2019, South Africa had over 30 registered biopesticides, of which 7 are manufactured locally, and mainly comprise different strains of Beauveria bassiana [53].
The idea behind IPM is that combining different practices overcomes the shortcomings of individual practices. The aim is not to eradicate pest populations but, rather, to manage them below levels that cause economic damage [54]. Although biopesticides may not be as rapid as synthetic pesticides, they form part of the crop protection methods used in integrated pest management. Thus, biopesticides are one of the promising alternatives for managing environmental pollution. Integrated control for H. armigera that seeks to minimise insecticide use and impacts on non-target organisms needs to be considered. However, in South Africa, there are very few registered biopesticides for use against H. armigera. Hence, this study confines itself to evaluating the field efficacy of different biopesticides in the control of H. armigera. The importance of this study is to enable scientists to intensify research on the stability of biopesticides under field conditions. This will further provide the bioagents industry with knowledge on biopesticides that have the potential to be registered for use on cotton for the control of H. armigera.

2. Materials and Methods

2.1. Trial Site, Layout, and Planting

The trials were conducted in 2017 and repeated in 2018 at the Agricultural Research Council (25°39.0′ S, 27°14.4′ E) in Rustenburg, North West Province, South Africa. Each plot had 6 rows that were 5 m long, with 1 m spacing between rows, 2 m paths between replications, and 20 cm spacing between plants. The trials were completely randomised block designs, and the treatments were replicated four times. A non-GM cotton cultivar, DeltaOPAL, was hand-planted under irrigated conditions, and weeds were manually removed by hand-hoeing. Thinning of seedlings at the fourth true leaf stage was performed to obtain a plant population density of five plants per metre. The trials were planted late in October.

2.2. Treatments and Application

Based on weekly scouting for bollworms, the administration of treatments started 13 weeks after planting, when the first and second instars were observed. Weekly spray applications were performed until 23 weeks after planting, when the cotton bolls were matured. Ten ground applications were administered around 3–4 p.m. due to the UV sensitivity of the biopesticides [55]. The treatments (Table 1) were applied using knapsack sprayers.

2.3. Data Collection

The efficacy of different treatments was assessed based on in situ counts of H. armigera larvae. From 12 weeks after planting, 12 plants per plot were scouted weekly. The scouting was conducted using a visual examination of plants in representative locations within a plot. The whole plant was inspected for the presence of all H. armigera larval instars, and the total population was counted. The counts were expressed in insect numbers. The seed cotton yields were determined at the end of the season. For accurate yield measurements, and to minimise experimental error, the two middle rows were harvested in each plot. The trials were harvested in May, when over 90% of the bolls had opened. The two middle rows were harvested per plot. Hand-harvesting was performed to ensure that the seed cotton was harvested and weighed accurately.

2.4. Data Analysis

The data were subjected to appropriate analysis of variance (ANOVA). The Shapiro–Wilk test was performed on the standardised residuals to test for deviations from normality [56]. LSDs (least significant differences) were calculated at a 5% significance level to compare the means of significant source effects [57]. The analysis was performed using Genstat Release 18 and SAS version 9.4 statistical software [58]. The seed cotton yields were expressed in percentages (yield in treatment plots–yield in control plots ÷ yield in control plots × 100).

3. Results

In 2017, plots treated with Karate® had significantly lower numbers of H. armigera larvae compared to the untreated controls, and were comparable to the plots treated with Bolldex® and Bb endophyte (Figure 1). The controls had the highest numbers of H. armigera, and this trend was similar for both the 2017 and 2018 seasons. The H. armigera population was significantly lower in all of the treatments compared to the untreated controls during the 2018 season. Plots treated with Karate® had lower numbers of H. armigera larvae, which were comparable to the plots treated with Bolldex® and Eco-Bb®. The results shown in Figure 2 reveal that plots treated with Bolldex® had significantly lower numbers of damaged bolls compared to Bb endophyte and the controls in 2017. However, in 2018, none of the active treatments were different from one another, although plots treated with Karate® had the lowest numbers of damaged bolls, followed by Eco-Bb® and Bolldex®. In both seasons, all of the treatments had significantly lower numbers of damaged bolls when compared to the untreated controls. A seed cotton yield of 5987 kg/ha was recorded in the plots that were treated with Bolldex®—significantly higher than the yields from the plots treated with Eco-Bb®, Delfin®, and Bb endophyte—in 2017 (Table 2). However, none of the treatments showed a significantly higher yield than the untreated controls. In 2018, plots treated with Bolldex® had the highest yield, at 6818 kg/ha, which was not different from the other treatments. The yield from the treatments with Eco-Bb®, Delfin®, and Bb endophyte was lower than that from the untreated controls in 2017. The average seed cotton yield was higher for all treatments in 2018 than in 2017. On average, the plots treated with Bolldex® had a significantly higher seed cotton yield (45%) compared to the untreated controls, followed by Karate®. Plots where Karate® was applied had earlier boll opening than the other treatments in 2017.

4. Discussion

In this study, statistically significant control of H. armigera and increases in yield were obtained with some of the biopesticides when compared to untreated controls. However, none of the biopesticides performed significantly better than the chemical control in the reduction in the numbers of H. armigera. Unlike greenhouse trials under controlled conditions, field trials are affected by different environmental factors [59], which may influence the effectiveness of the biopesticides. This study clearly shows that the insecticidal action of some of the tested biopesticides was comparable to the commercial synthetic insecticide. Bolldex® warrants more attention, because the reduction it caused in the numbers of H. armigera larvae was comparable to that of Karate®. These results demonstrate the potential of biopesticides to reduce H. armigera populations, and that they can be introduced as environmentally friendly pesticides in organic and commercial agriculture. This study demonstrates that both Bolldex® and Karate® significantly reduced H. armigera populations during the two seasons. Biopesticides have been reported to effectively reduce the larval population of H. armigera when combined with parasitoids [60].
Helicoverpa armigera nucleopolyhedrovirus (HaNPV) has been used in several countries and introduced in South Africa for use on several crops [32,61]. Delfin® may have reduced the larval population of H. armigera compared to the control in 2018, but there were no significant differences in 2017. Khalique and Ahmed (2001) [62] reported that the mortality response of H. armigera larvae to a combination of Karate® and B. thuringiensis subsp. kurstaki was synergistic, and that the two products were compatible. While considering the economic injury levels of cotton bollworms per plot [63], the results show that H. armigera larvae exceeded the threshold level of five bollworms for all of the treatments except for the Karate® treatment in 2017, and there were less than four bollworms for all of the treatments except for the untreated controls in 2018.
The lowest number of damaged bolls was observed in plots that were treated with Bolldex® and Karate®. The effects of Bolldex® and Karate® on the reduction in boll damage corresponded with the reduction in the numbers of H. armigera on the plots where these treatments were applied. These results are also in concordance with the observations of Li et al. (2006) [64], who found that more than 60% parasitism of H. armigera decreased boll damage by 80% compared with controls. Joubert (2012) [32] reported that a trial was conducted for the control of H. armigera on peaches, and Bolldex® yielded 99% scar-free fruit.
The data on yield revealed that a significantly higher yield of seed cotton was recorded in the treatments with Bolldex®, followed by Karate®, in 2018. In 2017, all of the treatments had yields that were not significantly different from the untreated controls. This may be related to the insect numbers in 2017 being higher than in 2018. In 1997, Cole et al. [65] reported that Karate® increased cotton yield by 12% and provided good pest control whilst maintaining beneficial populations. This is contrary to the findings of Kumar and Stanley (2010) [66], who reported that although lambda-cyhalothrin enhanced seed cotton yields, it caused mortality in both destructive and useful insect species. Sinno et al. (2021) [67] reported that endophytic fungi have the potential to improve plant development and provide protection against pests. However, in this study, the endophytic treatments Eco-Bb® and Bb endophyte only suppressed the H. armigera population, but had a lower yield compared to untreated controls in one season. Lotfy and Moustafa (2021) [68] investigated the efficacy of two B. bassiana strains against the cotton bollworm, and concluded that B. bassiana was efficient against the pest. They further observed that the fungus significantly reduced the numbers of infested bolls. The present study did not evaluate the impact of the pest complex other than the bollworm.
Plots that were treated with Karate® had earlier boll opening than the other treatments in 2017. The additive effects were probably due to multiple mechanisms that affect the pathogens, as opposed to the fewer control mechanisms provided by a single antagonist. Ali (2016) [69] stated that the average number of open bolls/plant is significantly increased by spraying insecticides and salicylic acid.

5. Conclusions

H. armigera remains a major pest of cotton, and its infestation reduces the yield. The main management tool to control this pest is the application of synthetic pesticides. The overuse of such agents subsequently results in pesticide resistance, and this highlights the importance of IPM strategies that include the use of biopesticides. Although biopesticides are safer to use, there are limitations to their full adoption as a pest management tool. The application of biopesticides under field conditions poses some challenges, as high doses are required for good efficacy. This study provides insight that although Eco-Bb® is currently not registered to control H. armigera, it has a suppressive potential against the population of H. armigera larvae. However, during the first season, the yield in treatments with Eco-Bb®, Delfin®, and Bb endophyte was lower than of untreated controls. Bolldex® provided better control of the pest compared to the untreated controls, and it increased the yield. Although the biopesticides were less effective against the H. armigera larvae compared to the chemical pesticide, they have the potential to be used in conjunction with synthetic pesticides to delay the development of pesticide resistance. However, further research that focuses on the efficacy and persistence of different doses and other products is required. More research on the production and application of biopesticides is needed in order to integrate these biological products into cotton production. It is also essential for public and private stakeholders to support and promote the research on biopesticides. Equally important is the training of farmers in the use of biopesticides for the rapid adoption of this technology.

Author Contributions

L.N.M.: Conceptualisation, Investigation, Methodology, Data Collection and Analysis, Validation, Manuscript Preparation, Writing—Corrections, Project Administration, Resources. M.D.L.: Conceptualisation, Supervision, Methodology, Validation, Visualisation. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

The authors would like to acknowledge the Agricultural Research Council for providing the funding and the field to conduct the trials.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Haider, N.; Ahmed, K.S.; Haidary, A.A.; Afzal, M.; Majeed, M.Z. Field evaluation of different insecticides against spotted bollworm (Earias spp.) and comparative yield assessment for BT and non-Bt cotton. J. Entomol. Zool. Stud. 2015, 4, 33–35. [Google Scholar]
  2. Hussain, M.; Noureen, N.; Fatima, S.; Ghazanfar, M. Cotton mealybug management: A review. Middle-East J. Sci. Res. 2016, 24, 2424–2430. [Google Scholar]
  3. Ma, H.; Meng, C.; Zhang, K.; Wang, K.; Fan, H.; Li, Y. Study on physiological mechanism of using cottonseed meal to improve salt–alkali tolerance of cotton. J. Plant Growth Regul. 2020, 40, 126. [Google Scholar] [CrossRef]
  4. Townsend, T. Cotton and Economic Development. Cotton Analytics. 2017. Available online: http://cottonanalytics.com/category/cotton-and-economic-development/ (accessed on 25 June 2021).
  5. Dhaliwal, J.S. Natural fibers: Applications. In Generation, Development and Modifications of Natural Fibers; Abbas, M., Jeon, H., Eds.; IntechOpen: London, UK, 2019. [Google Scholar]
  6. OECD; FAO. OECD FAO Agricultural Outlook 2019–2028. 2019. Available online: https://doi.org/10.1787/agr_outlook-2019-en (accessed on 25 June 2021). [CrossRef]
  7. Vitale, J. Economic Importance of Cotton in Burkina Faso. Food and Agriculture Organization of the United Nations. 2018. Available online: http://www.fao.org/3/i8330en/I8330EN.pdf (accessed on 2 August 2021).
  8. Amanet, K.; Chiamaka, E.O.; Quansah, G.W.; Mubeen, M.; Farid, H.U.; Akram, R.; Nasim, W. Cotton production in Africa. In Cotton Production; Jabran, K., Chauhan, B.S., Eds.; Wiley: Hoboken, NJ, USA, 2019; pp. 359–369. [Google Scholar] [CrossRef]
  9. IPBO. Cotton in Africa. 2017. Available online: http://www.vib.be/en/about-vib/Documents/vib_fact_CottonAfrican_EN_2017_0901_LR_FINAL.pdf (accessed on 25 June 2021).
  10. Van Jaarsveld, M.J. Geographic Susceptibility of Helicoverpa armigera (Lepidoptera: Noctuidae) to Insecticidal Proteins in Bt-cotton in South Africa. Master’s Thesis, Department of Zoology and Entomology, Rhodes University, Grahamstown, South Africa, 2003. [Google Scholar]
  11. Louw, M. Cotton Farming in South Africa. Field Crops in South Africa. 2020. Available online: http://southafrica.co.za/cotton-farming-in-south-africa.html (accessed on 17 September 2021).
  12. Cherry, A.; Cock, M.; Van den Berg, H.; Kfir, R. Biological control of Helicoverpa armigera in Africa. In Biological Control in IPM Systems in Africa; Neuenschwander, P., Borgemeister, C., Langewald, J., Eds.; CABI Publishing: Wallingford, UK, 2003; pp. 329–346. [Google Scholar]
  13. Moran, V.C. The phytophagous insects and mites of cultivated plants in South Africa: Patterns and pest status. J. Appl. Ecol. 1983, 20, 439–450. [Google Scholar] [CrossRef]
  14. Bell, M.A.; McGeoch, M.A. An evaluation of the pest status and research conducted on phytophagous Lepidoptera on cultivated plants in South Africa. Afr. Entomol. 1996, 4, 161–170. [Google Scholar]
  15. Moore, S.; Kirkman, W. HELICOVIRTM: A virus for the biological control of bollworm. SA Fruit J. 2010, 9, 63–67. [Google Scholar]
  16. Greathead, D.J.; Girling, D.J. Distribution and economic importance of Heliothis and of their natural enemies and host plants in southern and eastern Africa. In Proceedings of the Workshop on Biological Control of Heliothis: Increasing the Effectiveness of Natural Enemies, New Delhi, India, 11–15 November 1985; King, E.G., Jackson, R.D., Eds.; [Google Scholar]
  17. Tay, W.T.; Soria, M.F.; Walsh, T.; Thomazoni, D.; Silvie, P.; Behere, G.T.; Anderson, C.; Downes, S. A brave new world for an old-world pest: Helicoverpa armigera (Lepidoptera: Noctuidae) in Brazil. PLoS ONE 2013, 8, e80134. [Google Scholar] [CrossRef] [Green Version]
  18. Djihinto, A.C.; Katary, A.; Djaboutou, M.C.; Prudent, P.; Menozzi, P.; Atachi, P. Variation in biological parameters of cypermethrin resistant and susceptible strains of Helicoverpa armigera from Benin Republic, West Africa. Int. J. Biol. Chem. Sci. 2012, 6, 940. [Google Scholar] [CrossRef] [Green Version]
  19. Chen, G.; Liu, H.; Mo, B.C.; Hu, J.; Liu, S.Q.; Bustos-Segura, C.; Xue, J.; Wang, X. Growth and development of Helicoverpa armigera (Lepidoptera: Noctuidae) larvae infected by Heliothis virescens ascovirus 3i (HvAV-3i). Front. Physiol. 2020, 5, 93. [Google Scholar] [CrossRef]
  20. Cunningham, J.P.; Zalucki, M.P. Understanding heliothine (Lepidoptera: Heliothinae) pests: What is a host plant? J. Econ. Entomol. 2014, 107, 881–896. [Google Scholar] [CrossRef]
  21. Gu, S.; Han, P.; Ye, Z.; Perkins, L.E.; Li, J.; Wang, H.; Zalucki, M.P.; Lu, Z. Climate change favours a destructive agricultural pest in temperate regions: Late spring cold matters. J. Pest Sci. 2018, 91, 1191–1198. [Google Scholar] [CrossRef]
  22. Achaleke, J.; Brevault, T.; Blondin, L.; Vassal, J.M. Helicoverpa armigera: Truly Polyphagous. Available online: https://agritrop.cirad.fr/549357/1/document_549357.pdf (accessed on 2 February 2021).
  23. Brévault, T.; Nibouche, S.; Achaleke, J.; Carrière, Y. Assessing the role of non-cotton refuges in delaying Helicoverpa armigera resistance to Bt cotton in West Africa. Evol. Appl. 2011, 5, 53–65. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Noor-ul-Ane, M.; Kim, D.; Zalucki, M.P. Fecundity and egg laying in Helicoverpa armigera (Lepidoptera: Noctuidae): Model development and field validation. J. Econ. Entomol. 2018, 111, 2208–2216. [Google Scholar] [CrossRef]
  25. Fitt, G.P. The ecology of Heliothis species in relation to agroecosystems. Annu. Rev. Entomol. 1989, 34, 17–52. [Google Scholar] [CrossRef]
  26. Chaturvedi, I. Status of insecticide resistance in the cotton bollworm, Helicoverpa armigera (Hubner). J. Cent. Eur. Agric. 2007, 8, 171–182. [Google Scholar]
  27. Pretorius, J.D. Status of Resistance of Helicoverpa armigera (Lepidoptera: Noctuidae) and Diparopsis castanea (Lepidoptera: Noctuidae) to Bt Cotton in South Africa. Master’s Thesis, North-West University, Potchefstroom, South Africa, 2011. [Google Scholar]
  28. Yang, Y.; Li, Y.; Wu, Y. Current status of insecticide resistance in Helicoverpa armigera after 15 years of Bt cotton planting in China. J. Econ. Entomol. 2013, 106, 375–381. [Google Scholar] [CrossRef]
  29. Hussain, D.; Saleem, M.; Ghouse, G.; Abbas, M. Insecticide resistance in field populations of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). J. Entomol. Sci. 2015, 50, 119–128. [Google Scholar] [CrossRef]
  30. Tossou, E.; Tepa-Yotto, G.; Kpindou, O.K.; Sandeu, R.; Datinon, B.; Zeukeng, F.; Akoton, R.; Tchigossou, G.M.; Djègbè, I.; Vontas, J.; et al. Susceptibility profiles of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) to deltamethrin reveal a contrast between the Northern and the Southern Benin. Int. J. Environ. Res. Public Health 2019, 16, 1882. [Google Scholar] [CrossRef] [Green Version]
  31. Li, H.; Bouwer, G. Toxicity of Bacillus thuringiensis Cry proteins to Helicoverpa armigera (Lepidoptera: Noctuidae) in South Africa. J. Invertebr. Pathol. 2012, 109, 110–116. [Google Scholar] [CrossRef]
  32. Joubert, R. Biological Bollworm Control. Farmers Weekly: 22 May 2012. Available online: https://www.farmersweekly.co.za/agri-technology/farming-for-tomorrow/biological-bollworm-control/ (accessed on 26 January 2021).
  33. Mensah, R.K. Development of an integrated pest management programme for cotton. Part 1: Establishing and utilizing natural enemies. Int. J. Pest Manag. 2002, 48, 87–94. [Google Scholar] [CrossRef]
  34. Safna, M.; Naik, K.V.; Desai, V.S.; Karmarkar, M.S.; Shinde, B.D.; Raut, P.P. Evaluation of the efficacy of some insecticides against fruit borer, Helicoverpa armigera (Hubner) infesting tomato. Int. J. Chem. Stud. 2018, 6, 1158–1163. [Google Scholar]
  35. Yadav, S.; Dutta, S. Evaluation of organophosphorus pesticide residue in cotton of Tijara Tehsil, Alwar, Rajasthan. Nat. Environ. Pollut. Technol. 2019, 18, 1455–1458. [Google Scholar]
  36. Martin, T.; Ochou, G.O.; Hala-N’klo, F.; Vassal, J.M.; Vaissayre, M. Pyrethroid resistance in the cotton bollworm, Helicoverpa armigera (Hubner), in West Africa. Pest Manag. Sci. 2000, 56, 549–554. [Google Scholar] [CrossRef]
  37. Javaid, I.; Uaine, R.N.; Massua, J. The use of insect growth regulators for the control of insect pests of cotton. Int. J. Pest Manag. 1999, 45, 245–247. [Google Scholar] [CrossRef]
  38. Machado, A.V.A.; Potin, D.M.; Torres, J.B.; Silva Torres, C.S.A. Selective insecticides secure natural enemies action in cotton pest management. Ecotoxicol. Environ. Saf. 2019, 184, 109669. [Google Scholar] [CrossRef]
  39. Szewczyk, B.; Rabalski, L.; Krol, E.; Sihler, W.; de Souza, M.L. Baculovirus biopesticides-safe alternative to chemical protection of plants. J. Biopestic. 2009, 2, 209–216. [Google Scholar]
  40. Patel, S.R.; Patel, K.G.; Ghetiya, L.V. Population dynamics of pod borer (Helicoverpa armigera Hubner) infesting chickpea in relation to abiotic factors. Agres–Int. e-J. 2015, 4, 163–170. [Google Scholar]
  41. James, C. Global Status of Commercialized Biotech/GM Crops: 2016; ISAAA Brief No. 52; ISAAA: Ithaca, NY, USA, 2016. [Google Scholar]
  42. Rocha-Munive, M.G.; Soberón, M.; Castañeda, S.; Niaves, E.; Scheinvar, E.; Eguiarte, L.E.; Mota-Sánchez, D.; Rosales-Robles, E.; Nava-Camberos, U.; Martínez-Carrillo, J.L.; et al. Evaluation of the impact of genetically modified cotton after 20 years of cultivation in Mexico. Front. Bioeng. Biotechnol. 2018, 6, 82. [Google Scholar] [CrossRef]
  43. Ahmad, S.; Cheema, H.M.N.; Khan, A.A.; Khan, R.S.A.; Ahmad, J.N. Resistance status of Helicoverpa armigera against Bt cotton in Pakistan. Transgenic Res. 2019, 28, 199–212. [Google Scholar] [CrossRef]
  44. Zhang, H.N.; Tian, W.; Zhao, J.; Jin, L.; Yang, J.; Liu, C.H.; Yang, Y.; Wu, S.; Wu, K.; Cui, J.; et al. Diverse genetic basis of field-evolved resistance to Bt cotton in cotton bollworm from China. Proc. Natl. Acad. Sci. USA 2012, 109, 10275–10280. [Google Scholar] [CrossRef] [Green Version]
  45. Maghsoudi, S.; Jalali, E. Noble UV protective agent for Bacillus thuringiensis based on a combination of graphene oxide and olive oil. Sci. Rep. 2017, 7, 11019. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Vilas-Boas, G.T.; Peruca, A.P.S.; Arantes, O.M.N. Biology and taxonomy of Bacillus cereus, Bacillus anthracis, and Bacillus thuringiensis. Can. J. Microbiol. 2007, 53, 673–687. [Google Scholar] [CrossRef] [PubMed]
  47. Organisation for Economic Co-Operation and Development. Series on Pesticides No. 448. Report of Workshop on the Regulation of Biopesticides: Registration and Communication Issues. 2009. Available online: http://www.oecd.org/dataoecd/3/Collego55/43056580.pdf (accessed on 5 September 2021).
  48. Kumar, S.; Singh, A. Biopesticides: Present status and the future prospects. J. Fertil. Pestic. 2015, 6, 100–129. [Google Scholar] [CrossRef]
  49. Kumar, J.; Ramlal, A.; Mallick, D.; Mishra, V. An overview of some biopesticides and their importance in plant protection for commercial acceptance. Plants 2021, 10, 1185. [Google Scholar] [CrossRef]
  50. Xing, L.; Yuan, C.; Wang, M.; Lin, Z.; Shen, B.; Hu, Z.; Zou, Z. Dynamics of the interaction between cotton bollworm Helicoverpa armigera and nucleopolyhedrovirus as revealed by integrated transcriptomic and proteomic analyses. Mol. Cell. Proteom. 2017, 16, 1009–1028. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  51. Olson, S. An analysis of the biopesticide market now and where is going. Outlooks Pest Manag. 2015, 26, 203–206. [Google Scholar] [CrossRef]
  52. Akutse, K.S.; Subramanian, S.; Maniania, N.; Dubois, T.; Ekesi, S. Biopesticide research and product development in Africa for sustainable agriculture and food security–Experiences from the International Centre of Insect Physiology and Ecology (icipe). Front. Sustain. Food Syst. 2020, 4, 563016. [Google Scholar] [CrossRef]
  53. Hatting, J.L.; Moore, S.D.; Maland, A.P. Microbial control of phytophagous invertebrate pests in South Africa: Current status and future prospects. J. Invertebr. Pathol. 2019, 165, 54–66. [Google Scholar] [CrossRef]
  54. Chandler, D.; Bailey, A.S.; Tatchell, G.M.; Davidson, G.; Greaves, J.; Grant, W.P. The development, regulation and use of biopesticides for integrated pest management. Philos. Trans. R. Soc. B Biol. Sci. 2011, 366, 1987–1998. [Google Scholar] [CrossRef]
  55. Zhang, L.; Zhang, X.; Zhang, Y.; Wu, S.; Gelbič, I.; Xu, L.; Guan, X. A new formulation of Bacillus thuringiensis: UV protection and sustained release mosquito larvae studies. Sci. Rep. 2016, 6, 39425. [Google Scholar] [CrossRef]
  56. Shapiro, S.S.; Wilk, M.B. An analysis of variance test for normality (complete samples). Biometrika 1965, 52, 591–611. [Google Scholar] [CrossRef]
  57. Snedecor, G.W.; Cochran, W.G. Statistical Methods, 6th ed.; The Lowa State University: Ames, IA, USA, 1967. [Google Scholar]
  58. SAS. SAS/STAT User’s Guide; SAS Institute Inc.: Cary, NC, USA, 1999; Volume 8. [Google Scholar]
  59. Tesfagiorgis, H.B. Studies on the Use of Biocontrol Agents and Soluble Silicon against Powdery Mildew of Zucchini and Zinnia. Ph.D. Thesis, University of KwaZulu-Natal, Durban, South Africa, 2008. [Google Scholar]
  60. Sharma, G.D.; Devi, N.; Raj, D.; Oberoi, C.K. Field efficacy of different insecticides and bio-pesticides against fruit borer (Helicoverpa armigera) and greenhouse whitefly (Trialeurodes vaporariorum). Himachal J. Agric. Res. 2008, 34, 40–46. [Google Scholar]
  61. Madumbi Sustainable Agriculture. Bolldex® Product Label. Available online: http://www.madumbi.co.za/pdf/Bolldex/Bolldex%20Label.pdf (accessed on 24 January 2021).
  62. Khalique, F.; Ahmed, K. Synergistic Interaction between Bacillus thuringiensis (Berliner) and lambda-cyhalothrin (Pyrethroid) against, chickpea pod borer, Helicoverpa armigera (Hübner). Pak. J. Biol. Sci. 2001, 4, 1120–1123. [Google Scholar] [CrossRef] [Green Version]
  63. ARC (Agricultural Research Council). Management Guide for the Cotton Producer, 2nd ed.; ARC-Institute for Industrial Crops: Rustenburg, South Africa, 2004. [Google Scholar]
  64. Li, J.; Yan, F.; Coudron, T.A.; Pan, W.; Zhang, X.; Liu, X.; Zhang, Q. Field release of the parasitoid Microplitis mediator (Hymenoptera: Braconidae) for control of Helicoverpa armigera (Lepidoptera: Noctuidae) in cotton fields in Northwestern China’s Xinjiang Province. Environ. Entomol. 2006, 35, 694–699. [Google Scholar] [CrossRef]
  65. Cole, J.F.H.; Pilling, E.D.; Boykin, R.; Ruberson, J.R. Effects of Karate® insecticide on beneficial arthropods in Bollgard® cotton. In Proceedings of the 1997 Proceedings Beltwide Cotton Conferences, New Orleans, LA, USA, 6–10 January 1997; Dugger, C.P., Richter, D.A., Eds.; Volume 2, pp. 1118–1120. [Google Scholar]
  66. Kumar, K.R.; Stanley, S. Bio-efficacy of microbial and chemical insecticides on major lepidopterous pests of cotton and their (insect) natural enemies in cotton ecosystem in Tamil Nadu. Resist. Pest Manag. Newsl. 2010, 20, 4–7. [Google Scholar]
  67. Sinno, M.; Ranesi, M.; Di Lelio, I.; Iacomino, G.; Becchimanzi, A.; Barra, E.; Molisso, D.; Pennacchio, F.; Digilio, M.C.; Vitale, S.; et al. Selection of endophytic Beauveria bassiana as a dual biocontrol agent of tomato pathogens and pests. Pathogens 2021, 10, 1242. [Google Scholar] [CrossRef]
  68. Lotfy, D.E.; Moustafa, H.Z. Field evaluation of two entomopathogenic fungi; Beauveria bassiana and Metarhizium anisopliae as a biocontrol agent against the spiny bollworm, Earias insulana Boisduval (Lepidoptera: Noctuidae) on cotton plants. Egypt. J. Biol. Pest Control 2021, 31, 78. [Google Scholar] [CrossRef]
  69. Ali, O.S.M. Effect of Salicylic Acid and Its Mixtures with Three Insecticides on Some Cotton Insect Pests. Ph.D. Thesis, Tanta University, Tanta, Egypt, 2016. [Google Scholar]
Insects 13 00673 g001 550
Figure 1. The average number of H. armigera larvae found on different treatments during the 2017 and 2018 seasons. Means with the same letter are not significantly different (p < 0.05). The comparison was carried out using the data from the same year.
Figure 1. The average number of H. armigera larvae found on different treatments during the 2017 and 2018 seasons. Means with the same letter are not significantly different (p < 0.05). The comparison was carried out using the data from the same year.
Insects 13 00673 g001
Insects 13 00673 g002 550
Figure 2. The average number of damaged bolls found on different treatments during the 2017 and 2018 seasons. Means with the same letter are not significantly different (p < 0.05). The comparison was carried out using the data from the same year.
Figure 2. The average number of damaged bolls found on different treatments during the 2017 and 2018 seasons. Means with the same letter are not significantly different (p < 0.05). The comparison was carried out using the data from the same year.
Insects 13 00673 g002
Table
Table 1. List of treatments that were used with their active ingredients, formulations, and concentrations.
Table 1. List of treatments that were used with their active ingredients, formulations, and concentrations.
Trade NameActive IngredientFormulationConcentration
Eco-Bb®Beauveria bassiana (strain R444)2 × 10⁹ spores/gram300 g/ha in 1 g/L water
Bb endophyteBeauveria bassiana2 × 10⁹ spores/gram300 g/ha in 1 g/L water
Bolldex®Nucleopolyhedrovirus (HearNPV)7.5 × 1012 spores/gram200 mL/ha in water
Delfin®Bacillus thuringiensis subspecies kurstaki (Btk)32,000 IU/mg1 kg/ha in 25 L/ha water
Karate®Lambda-cyhalothrin50 g/L120 mL/ha in 200 L/ha water
Table
Table 2. Seed cotton yields from plots with different treatments during the 2017 and 2018 seasons.
Table 2. Seed cotton yields from plots with different treatments during the 2017 and 2018 seasons.
Treatment2017 (kg/ha) *2018 (kg/ha) *
Eco-Bb®3055 ± 139.19 b5961 ± 65.07 ab
Bolldex®5987 ± 86.56 a6818 ± 95.59 a
Delfin®3523 ± 49.24 b5755 ± 109. 21 ab
Bb endophyte3100 ± 66.11 b6409 ± 128.93 a
Karate® 5133 ± 99.34 ab6405 ± 57.64 a
Untreated control4168 ± 143.09 ab4673 ± 124.79 b
LSD (5%)2373.81.6178
CV%37.9451617.88032
p-Value0.12160.1436
* Means with the same letter are not significantly different (p < 0.05). The comparisons were carried out using the data from the same year.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Malinga, L.N.; Laing, M.D. Efficacy of Biopesticides in the Management of the Cotton Bollworm, Helicoverpa armigera (Noctuidae), under Field Conditions. Insects 2022, 13, 673. https://doi.org/10.3390/insects13080673

AMA Style

Malinga LN, Laing MD. Efficacy of Biopesticides in the Management of the Cotton Bollworm, Helicoverpa armigera (Noctuidae), under Field Conditions. Insects. 2022; 13(8):673. https://doi.org/10.3390/insects13080673

Chicago/Turabian Style

Malinga, Lawrence N., and Mark D. Laing. 2022. "Efficacy of Biopesticides in the Management of the Cotton Bollworm, Helicoverpa armigera (Noctuidae), under Field Conditions" Insects 13, no. 8: 673. https://doi.org/10.3390/insects13080673

APA Style

Malinga, L. N., & Laing, M. D. (2022). Efficacy of Biopesticides in the Management of the Cotton Bollworm, Helicoverpa armigera (Noctuidae), under Field Conditions. Insects, 13(8), 673. https://doi.org/10.3390/insects13080673

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop