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Sustainable insect control in vegetables through optimized applications of entomopathogenic nematodes

Bert Beck (UGent)
(2013)
Author
Promoter
(UGent) , (UGent) and David Nuyttens
Organization
Abstract
Due to the potential impact of conventional chemical pesticides on human health and on the environment, governments worldwide are developing policies to reduce the use of these pesticides. Instruments like the EU directive 91/414/EEC, have resulted in the withdrawal of many active ingredients from the market. Furthermore, the new EU directive 2009/128/EC on the sustainable use of pesticides states that non-chemical methods should be given priority wherever possible. To improve the sustainability of agriculture and to avoid resistance development against the receding number of active ingredients remaining on the market, biological alternatives for conventional chemical pesticides are much sought after and even urgently needed. Entomopathogenic nematodes (EPN) are one of those alternatives. They are used for the biological control of an increasing number of insect pests. These bio-insecticides are exceptionally safe for farmers, farm workers, for consumers and for the environment. However, they may have lower efficacy than conventional chemical pesticides. Nonetheless, EPN are equivalent to or even better than conventional chemical insecticides in controlling a number of commercially important pests (e.g., against black vine weevil, citrus root weevil, cranberry girdler, hunting billbug and western corn rootworm). Poor efficacy against other pests can be the result of inappropriate application methods, the use of poor quality products or suboptimal application conditions. This work focused on optimizing the application of EPN in field vegetables. The general aim of this work was to test and, where possible, to improve the control potential of EPN against three difficult to reach pests, described in detail in chapter 1, viz.: the leaf-bound cabbage moth (Mamestra brassicae) in cauliflower, the soil-bound cabbage root fly (Delia radicum) in cauliflower and the cryptic onion thrips (Thrips tabaci) in leek. Depending on the target pest, the experiments described in chapters 2 to 5 examined the effect of (1) adding adjuvants to the spray suspension, (2) altering the application rate of the EPN and (3) adapting the application technique and/or (4) the timing of the application(s). Chapter 2 focused on improving the formulation and application of EPN on leaves using laboratory tests with special attention to one specific pest: the cabbage moth. Suitable adjuvants for EPN spray applications were selected based on the absence of toxic or immobilizing effects on two EPN species: Steinernema feltiae and S. carpocapsae. The selected humectants and dispersants were further screened for their effects on the sedimentation of these EPN species in a tank suspension. Next, the effect of three suitable surfactants and a humectant and the effect of nozzle size on the deposition of S. carpocapsae on hydrophobic cauliflower leaves was investigated. Subsequently, a laboratory experiment verified whether brewer’s yeast extract can be used as an attractant for the cabbage moth larvae, and whether it improves the mortality caused by EPN to cabbage moth larvae. Finally, the effect of the most suitable surfactant and humectant, selected from the deposition test, on the longevity and on the infectivity of S. carpocapsae, is presented. These experiments have shown that all selected alcohol ethoxylates (Synperonic 91/5, Synperonic 91/6, Synperonic 10/6 and Atplus 245) and the selected alkylpolysaccharide (AL-2575) immobilized both S. carpocapsae and S. feltiae when mixed in the spray suspension. Xanthan gum remains the best sedimentation-retarding agent. An ISO 02 standard flat fan nozzle can clog when spraying S. carpocapsae. An ISO 04 standard flat fan nozzle provides a higher relative deposition of different S. carpocapsae-adjuvant suspensions on cauliflower leaves than the bigger ISO 08 standard flat fan nozzle. Three spreading agents (Silwet L-77, SB Plant Invigorator and Addit) roughly doubled the relative EPN deposition with both the ISO 04 and the ISO 08 nozzle when added to the EPN suspension. Addition of xanthan gum did not significantly increase deposition any further. Addition of yeast extract to a foliar spray containing S. carpocapsae significantly increased mortality of the cabbage moth and decreased the amount of leaf damage caused by these caterpillars. And finally, it was shown that adding Addit and xanthan gum to a spray suspension containing S. carpocapsae prolongs the survival of EPN on leaves, and that these adjuvants can cause mortality in larvae of Galleria mellonella. It was however deemed unlikely, and proven in a field test (chapter 3), that Addit and xanthan gum at the used concentrations, would have a significant effect on insect plagues in field conditions. The field experiments described in chapter 3 implemented the results of chapter 2 and aimed to optimize the control of cabbage moth with S. carpocapsae. A spray application tools test, was performed to select a spray application technique that leads to a maximum of spray coverage on specific parts of the cauliflower plant. The targeted spraying areas were: (1) the central part of the plant, where the cabbage moth larvae can cause direct economic damage to the cauliflower head, and (2) the underside of the leaves, where the young larvae hide during the day and feed during the night. The test showed that two spray boom configurations with vertical extensions in the crop covered the lower side of the outer leaves very well, while also securing statistically equal coverage of the underside of the centre leaves, when compared to all other configurations. Therefore, one of these configurations, a spray boom configuration with TeeJet TP 80 04 EVS nozzles mounted on the horizontal spray boom and TeeJet UB 85 04 nozzles mounted 38 cm long vertical extensions, was selected for the field trial with S. carpocapsae. An adjuvant trial, determined whether S. carpocapsae, applied in the field with this technique, could effectively reduce the cabbage moth numbers in a cauliflower crop and/or the damage to this crop. It also tested if these parameters could be further reduced by adding yeast extract and/or Addit and xanthan gum to the tank suspension. An application rate trial and an application technique trial, were set up (1) to test the effect of different application rates of EPN on cabbage moth control and (2) to confirm if the application technique selected in the spray application tools test was indeed better suited than a standard broadcast spray application, for controlling the cabbage moth. In the adjuvant trial, the numbers of damaged cabbage heads clearly demonstrate a protective effect of spraying with a suspension of S. carpocapsae, when combined with Addit and xanthan gum. It was noticeable that Bt applications outperformed all other treatments, although the difference was not always significant. Based on these results, EPN might provide an extra control option against the cabbage moth, if the efficacy of EPN treatments can be further enhanced. Similar to the adjuvant trial, the numbers of cabbage moth larvae were highly variable between individual plants in both the application rate trial and the application technique trial, making it difficult to distinguish statistical differences between the mean number of caterpillars per plant. However, leaf damage measurements and the number of infected plants proved to be much less variable and thus much more reliable than counting numbers of caterpillars for assessing control by S. carpocapsae and Bt treatments in both trials. Only the Bt applications with the adapted spray boom effectively stopped damage development caused by the cabbage moth. Furthermore, the plots that received Bt with the adapted spray boom were the only plots that contained significantly less infected plants than the control plots. The protection against sunlight on the underside of leaves, together with better placement of the Bt spray may explain the better control of the Bt applications with the adapted spray boom compared with the regular spray boom. This chapter shows that there is much room for improvement in the foliar application of EPN against cabbage moth. Control results were probably largely dependent on the temperature. More cold-tolerant species, strains or breeding products of EPN should be searched for, so that they can be used against the cabbage moth, before any conclusions can be drawn on the optimal application rate of the EPN. The deposition measurements in all trials suffered from high variability. This was most probably caused by the plant architecture of cauliflower: due to the overlap of leaves, some areas of the plant are difficult to spray. This variability is a major concern for biocontrol agents like Bt and EPN, since areas that are not sprayed, are not protected against the targeted pest. When a low temperature active EPN species/strain/breeding product, efficacious against the cabbage moth, becomes available, then EPN applications might be fitted into biological control schemes to prevent development of resistance of cabbage moth against Bt. This is of major importance, since cabbage moth already seems to possess some innate resistance against Bt products. Chapter 4 presents three field tests with applications of IJ of S. feltiae against cabbage root fly in cauliflower. These tests focused on finding an optimal application rate (200,000 IJ/plant vs. 50,000 IJ/plant), a suitable application technique (plant tray spraying vs. drench application) and a good timing of the application (application at planting vs. application one week after planting vs. application two weeks after planting, with or without one or two follow-up treatment(s)). The results demonstrated that a plant tray spray with S. feltiae is superior to a drench application in controlling cabbage root fly in cauliflower. Plant tray sprayings with S. feltiae can reduce the percentage of dead plants compared with the non-treated control. The lack of an application rate-effect relationship suggests that it might be possible to further reduce the applied rate of S. feltiae without causing a significant reduction in control. Numbers of cabbage maggots around the plant roots can be temporarily reduced by plant tray sprays with a rate of 200,000 IJ S. feltiae per cauliflower plant. Mortality results of bait tests with wax moth larvae on soil samples taken from around the cauliflower plants, showed that IJ of S. feltiae, applied as a plant tray spray, take one to two weeks to spread into the soil around the roots of cauliflower. These bait tests also showed that the most effective period of IJ of S. feltiae in the soil is limited up to five weeks, which warrants a follow-up treatment. Further research should examine whether the application rate of IJ of S. feltiae in a plant tray spray can be lowered, while maintaining a good control, and whether a follow-up application of S. feltiae, applied three to five weeks after planting with a better suited technique (e.g., injection), would further improve control of cabbage root fly. Chapter 5 presents two field trials in leek set up to determine and, if possible, to improve the effect of spray applications with S. feltiae against onion thrips in leek. The first trial was carried out on an organic farm and focused on selecting a suitable spray application technique and on testing the effect of an attractant on thrips control. The second trial focused on incorporating spray applications of EPN in a conventional insecticide scheme, and on the effect of mixing the surfactant Addit in the spray suspension on the control of onion thrips. The results show that the selected commercial strain of S. feltiae was not effective against the foliar inhabiting life stages of onion thrips in leek. Mixing a thrips attractant in the spray suspension and spraying with adapted spray equipment (band application and row application) did not improve the efficacy. Compared with the traditional spray boom technique, the row application technique ensured a more even EPN deposition on both the upper side and underside of both old and new leek leaves. This technique offers good potential for improving the applications of fungicides and of contact insecticides in leek. The general discussion in chapter 6 links the obtained results, and suggests directions for future research. The described experimental work with EPN against the cabbage moth, cabbage root fly and onion thrips showed that significant control of the first two pests is certainly possible in outdoor vegetables, but it also showed that there’s still a long way to go before EPN will be applied commercially against these pests in outdoor vegetables. Efficient control of insect pests with EPN requires a perfect match between several factors: the EPN species/strain/breeding product, the pest, the crop, the application (in terms of technique, formulation and application rate) and the environmental conditions. Matching these factors requires the screening and breeding of much more EPN species/strains for different properties (e.g., pathogenicity, temperature tolerance, mobility, drought resistance). In the short term, research on EPN applications against greenhouse pests seems to be the most promising area of research in temperate climates. Only when the prices for EPN drop due to more widespread adoption and when new EPN species/strains/breeding products and application techniques become available, will outdoor applications of EPN become commercially viable. Because pest control with EPN is obviously not a one-size fits-all solution, farmers will need appropriate knowledge to obtain successful pest control with EPN. Moreover, the upcoming EU obligation for farmers to use Integrated Pest Management (IPM) methods to protect their crops will further increase the demand for knowledge on IPM methods. Governmental, NGO and corporate advisory networks will need to be strengthened in order to fulfil this demand and to keep European crops healthy.
Keywords
biological control, entomopathogenic nematodes, crop protection, cabbage moth, cabbage root fly, sustainable insect control, onion thrips

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Please use this url to cite or link to this publication:

MLA
Beck, Bert. Sustainable Insect Control in Vegetables through Optimized Applications of Entomopathogenic Nematodes. Ghent University. Faculty of Bioscience Engineering, 2013.
APA
Beck, B. (2013). Sustainable insect control in vegetables through optimized applications of entomopathogenic nematodes. Ghent University. Faculty of Bioscience Engineering, Ghent, Belgium.
Chicago author-date
Beck, Bert. 2013. “Sustainable Insect Control in Vegetables through Optimized Applications of Entomopathogenic Nematodes.” Ghent, Belgium: Ghent University. Faculty of Bioscience Engineering.
Chicago author-date (all authors)
Beck, Bert. 2013. “Sustainable Insect Control in Vegetables through Optimized Applications of Entomopathogenic Nematodes.” Ghent, Belgium: Ghent University. Faculty of Bioscience Engineering.
Vancouver
1.
Beck B. Sustainable insect control in vegetables through optimized applications of entomopathogenic nematodes. [Ghent, Belgium]: Ghent University. Faculty of Bioscience Engineering; 2013.
IEEE
[1]
B. Beck, “Sustainable insect control in vegetables through optimized applications of entomopathogenic nematodes,” Ghent University. Faculty of Bioscience Engineering, Ghent, Belgium, 2013.
@phdthesis{4141988,
  abstract     = {{Due to the potential impact of conventional chemical pesticides on human health and on the environment, governments worldwide are developing policies to reduce the use of these pesticides. Instruments like the EU directive 91/414/EEC, have resulted in the withdrawal of many active ingredients from the market. Furthermore, the new EU directive 2009/128/EC on the sustainable use of pesticides states that non-chemical methods should be given priority wherever possible. To improve the sustainability of agriculture and to avoid resistance development against the receding number of active ingredients remaining on the market, biological alternatives for conventional chemical pesticides are much sought after and even urgently needed. 
Entomopathogenic nematodes (EPN) are one of those alternatives. They are used for the biological control of an increasing number of insect pests. These bio-insecticides are exceptionally safe for farmers, farm workers, for consumers and for the environment. However, they may have lower efficacy than conventional chemical pesticides. Nonetheless, EPN are equivalent to or even better than conventional chemical insecticides in controlling a number of commercially important pests (e.g., against black vine weevil, citrus root weevil, cranberry girdler, hunting billbug and western corn rootworm). Poor efficacy against other pests can be the result of inappropriate application methods, the use of poor quality products or suboptimal application conditions.
This work focused on optimizing the application of EPN in field vegetables. The general aim of this work was to test and, where possible, to improve the control potential of EPN against three difficult to reach pests, described in detail in chapter 1, viz.: the leaf-bound cabbage moth (Mamestra brassicae) in cauliflower, the soil-bound cabbage root fly (Delia radicum) in cauliflower and the cryptic onion thrips (Thrips tabaci) in leek. Depending on the target pest, the experiments described in chapters 2 to 5 examined the effect of (1) adding adjuvants to the spray suspension, (2) altering the application rate of the EPN and (3) adapting the application technique and/or (4) the timing of the application(s). 
Chapter 2 focused on improving the formulation and application of EPN on leaves using laboratory tests with special attention to one specific pest: the cabbage moth. Suitable adjuvants for EPN spray applications were selected based on the absence of toxic or immobilizing effects on two EPN species: Steinernema feltiae and S. carpocapsae. The selected humectants and dispersants were further screened for their effects on the sedimentation of these EPN species in a tank suspension. Next, the effect of three suitable surfactants and a humectant and the effect of nozzle size on the deposition of S. carpocapsae on hydrophobic cauliflower leaves was investigated. Subsequently, a laboratory experiment verified whether brewer’s yeast extract can be used as an attractant for the cabbage moth larvae, and whether it improves the mortality caused by EPN to cabbage moth larvae. Finally, the effect of the most suitable surfactant and humectant, selected from the deposition test, on the longevity and on the infectivity of S. carpocapsae, is presented.
These experiments have shown that all selected alcohol ethoxylates (Synperonic 91/5, Synperonic 91/6, Synperonic 10/6 and Atplus 245) and the selected alkylpolysaccharide (AL-2575) immobilized both S. carpocapsae and S. feltiae when mixed in the spray suspension. Xanthan gum remains the best sedimentation-retarding agent. An ISO 02 standard flat fan nozzle can clog when spraying S. carpocapsae. An ISO 04 standard flat fan nozzle provides a higher relative deposition of different S. carpocapsae-adjuvant suspensions on cauliflower leaves than the bigger ISO 08 standard flat fan nozzle. Three spreading agents (Silwet L-77, SB Plant Invigorator and Addit) roughly doubled the relative EPN deposition with both the ISO 04 and the ISO 08 nozzle when added to the EPN suspension. Addition of xanthan gum did not significantly increase deposition any further. Addition of yeast extract to a foliar spray containing S. carpocapsae significantly increased mortality of the cabbage moth and decreased the amount of leaf damage caused by these caterpillars. And finally, it was shown that adding Addit and xanthan gum to a spray suspension containing S. carpocapsae prolongs the survival of EPN on leaves, and that these adjuvants can cause mortality in larvae of Galleria mellonella. It was however deemed unlikely, and proven in a field test (chapter 3), that Addit and xanthan gum at the used concentrations, would have a significant effect on insect plagues in field conditions.
The field experiments described in chapter 3 implemented the results of chapter 2 and aimed to optimize the control of cabbage moth with S. carpocapsae. A spray application tools test, was performed to select a spray application technique that leads to a maximum of spray coverage on specific parts of the cauliflower plant. The targeted spraying areas were: (1) the central part of the plant, where the cabbage moth larvae can cause direct economic damage to the cauliflower head, and (2) the underside of the leaves, where the young larvae hide during the day and feed during the night.
The test showed that two spray boom configurations with vertical extensions in the crop covered the lower side of the outer leaves very well, while also securing statistically equal coverage of the underside of the centre leaves, when compared to all other configurations. Therefore, one of these configurations, a spray boom configuration with TeeJet TP 80 04 EVS nozzles mounted on the horizontal spray boom and TeeJet UB 85 04 nozzles mounted 38 cm long vertical extensions, was selected for the field trial with S. carpocapsae.
An adjuvant trial, determined whether S. carpocapsae, applied in the field with this technique, could effectively reduce the cabbage moth numbers in a cauliflower crop and/or the damage to this crop. It also tested if these parameters could be further reduced by adding yeast extract and/or Addit and xanthan gum to the tank suspension.
An application rate trial and an application technique trial, were set up (1) to test the effect of different application rates of EPN on cabbage moth control and (2) to confirm if the application technique selected in the spray application tools test was indeed better suited than a standard broadcast spray application, for controlling the cabbage moth.
In the adjuvant trial, the numbers of damaged cabbage heads clearly demonstrate a protective effect of spraying with a suspension of S. carpocapsae, when combined with Addit and xanthan gum. It was noticeable that Bt applications outperformed all other treatments, although the difference was not always significant. Based on these results, EPN might provide an extra control option against the cabbage moth, if the efficacy of EPN treatments can be further enhanced.
Similar to the adjuvant trial, the numbers of cabbage moth larvae were highly variable between individual plants in both the application rate trial and the application technique trial, making it difficult to distinguish statistical differences between the mean number of caterpillars per plant. However, leaf damage measurements and the number of infected plants proved to be much less variable and thus much more reliable than counting numbers of caterpillars for assessing control by S. carpocapsae and Bt treatments in both trials.
Only the Bt applications with the adapted spray boom effectively stopped damage development caused by the cabbage moth. Furthermore, the plots that received Bt with the adapted spray boom were the only plots that contained significantly less infected plants than the control plots. The protection against sunlight on the underside of leaves, together with better placement of the Bt spray may explain the better control of the Bt applications with the adapted spray boom compared with the regular spray boom. This chapter shows that there is much room for improvement in the foliar application of EPN against cabbage moth. Control results were probably largely dependent on the temperature. More cold-tolerant species, strains or breeding products of EPN should be searched for, so that they can be used against the cabbage moth, before any conclusions can be drawn on the optimal application rate of the EPN.
The deposition measurements in all trials suffered from high variability. This was most probably caused by the plant architecture of cauliflower: due to the overlap of leaves, some areas of the plant are difficult to spray. This variability is a major concern for biocontrol agents like Bt and EPN, since areas that are not sprayed, are not protected against the targeted pest.
When a low temperature active EPN species/strain/breeding product, efficacious against the cabbage moth, becomes available, then EPN applications might be fitted into biological control schemes to prevent development of resistance of cabbage moth against Bt. This is of major importance, since cabbage moth already seems to possess some innate resistance against Bt products.
Chapter 4 presents three field tests with applications of IJ of S. feltiae against cabbage root fly in cauliflower. These tests focused on finding an optimal application rate (200,000 IJ/plant vs. 50,000 IJ/plant), a suitable application technique (plant tray spraying vs. drench application) and a good timing of the application (application at planting vs. application one week after planting vs. application two weeks after planting, with or without one or two follow-up treatment(s)).
The results demonstrated that a plant tray spray with S. feltiae is superior to a drench application in controlling cabbage root fly in cauliflower. Plant tray sprayings with S. feltiae can reduce the percentage of dead plants compared with the non-treated control. The lack of an application rate-effect relationship suggests that it might be possible to further reduce the applied rate of S. feltiae without causing a significant reduction in control. Numbers of cabbage maggots around the plant roots can be temporarily reduced by plant tray sprays with a rate of 200,000 IJ S. feltiae per cauliflower plant.
Mortality results of bait tests with wax moth larvae on soil samples taken from around the cauliflower plants, showed that IJ of S. feltiae, applied as a plant tray spray, take one to two weeks to spread into the soil around the roots of cauliflower. These bait tests also showed that the most effective period of IJ of S. feltiae in the soil is limited up to five weeks, which warrants a follow-up treatment.
Further research should examine whether the application rate of IJ of S. feltiae in a plant tray spray can be lowered, while maintaining a good control, and whether a follow-up application of S. feltiae, applied three to five weeks after planting with a better suited technique (e.g., injection), would further improve control of cabbage root fly.
Chapter 5 presents two field trials in leek set up to determine and, if possible, to improve the effect of spray applications with S. feltiae against onion thrips in leek. The first trial was carried out on an organic farm and focused on selecting a suitable spray application technique and on testing the effect of an attractant on thrips control. The second trial focused on incorporating spray applications of EPN in a conventional insecticide scheme, and on the effect of mixing the surfactant Addit in the spray suspension on the control of onion thrips.
The results show that the selected commercial strain of S. feltiae was not effective against the foliar inhabiting life stages of onion thrips in leek. Mixing a thrips attractant in the spray suspension and spraying with adapted spray equipment (band application and row application) did not improve the efficacy. Compared with the traditional spray boom technique, the row application technique ensured a more even EPN deposition on both the upper side and underside of both old and new leek leaves. This technique offers good potential for improving the applications of fungicides and of contact insecticides in leek.
The general discussion in chapter 6 links the obtained results, and suggests directions for future research. The described experimental work with EPN against the cabbage moth, cabbage root fly and onion thrips showed that significant control of the first two pests is certainly possible in outdoor vegetables, but it also showed that there’s still a long way to go before EPN will be applied commercially against these pests in outdoor vegetables. Efficient control of insect pests with EPN requires a perfect match between several factors: the EPN species/strain/breeding product, the pest, the crop, the application (in terms of technique, formulation and application rate) and the environmental conditions. Matching these factors requires the screening and breeding of much more EPN species/strains for different properties (e.g., pathogenicity, temperature tolerance, mobility, drought resistance).
In the short term, research on EPN applications against greenhouse pests seems to be the most promising area of research in temperate climates. Only when the prices for EPN drop due to more widespread adoption and when new EPN species/strains/breeding products and application techniques become available, will outdoor applications of EPN become commercially viable.
Because pest control with EPN is obviously not a one-size fits-all solution, farmers will need appropriate knowledge to obtain successful pest control with EPN. Moreover, the upcoming EU obligation for farmers to use Integrated Pest Management (IPM) methods to protect their crops will further increase the demand for knowledge on IPM methods. Governmental, NGO and corporate advisory networks will need to be strengthened in order to fulfil this demand and to keep European crops healthy.}},
  author       = {{Beck, Bert}},
  isbn         = {{9789059896512}},
  keywords     = {{biological control,entomopathogenic nematodes,crop protection,cabbage moth,cabbage root fly,sustainable insect control,onion thrips}},
  language     = {{eng}},
  pages        = {{XXX, 178}},
  publisher    = {{Ghent University. Faculty of Bioscience Engineering}},
  school       = {{Ghent University}},
  title        = {{Sustainable insect control in vegetables through optimized applications of entomopathogenic nematodes}},
  year         = {{2013}},
}