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ARS Home » Southeast Area » Gainesville, Florida » Center for Medical, Agricultural and Veterinary Entomology » Insect Behavior and Biocontrol Research » Research » Research Project #430081

Research Project: Improved Biologically-Based Methods for Insect Pest Management of Crop Insect Pests

Location: Insect Behavior and Biocontrol Research

2019 Annual Report

Objective 1. Develop new transgenic conditional lethal strains for sexing and sterility in tephritid and drosophilid fruit flies to be used in the sterile insect technique, produce redundant lethality systems for ecological safety, and transgenic technology for emerging pest species such as the Asian citrus psyllid. Objective 2. Develop paratransgenic strains that eliminate the ability of host populations to vector plant disease by using Wolbachia cytoplasmic incompatibility to drive pathogen immunity throughout populations of key pests such as Asian citrus psyllid, glassy-winged sharpshooter, and potato/tomato psyllid. Objective 3. Develop automated acoustic methods for improved surveillance and detection of hidden and invasive pests such as red palm and citrus root weevils and Asian long-horned beetle that will facilitate more rapid information collection/processing by use of big data technologies. Objective 4. Develop improved visual-cue trap systems for surveillance of invasive and outbreak insect pests such as Asian citrus psyllid and corn silk fly, and improve strategies for detecting and predicting the dispersal of these pests by understanding the role of visual and other stimuli in affecting their behavior. Objective 5. Develop predictive models for fall armyworm migration pathways that are shifting due to climate change, and improve area-wide landscape management tactics for these pests by developing cover crop and biological control strategies to control them. Sub-objective 5.A. Develop genetic methods to monitor fall armyworm population behavior and air transport models to describe and predict its migration pathways and potential changes in infestation patterns due to climate change. Sub-objective 5.B. Improve area-wide landscape management tactics by developing cover crop and other strategies to mitigate pest populations such as fall armyworm, and attract or support natural enemies and pollinators.

The experimental approaches to achieve these objectives is multidisciplinary and integrates genetics, ecology, behavior, and engineering to address various stages of control, from molecular genetics leading to autocidal strain development to predicting changes in pest migration in response to global climate change. These approaches will apply, initially, to high priority invasive fruit flies, beetles, psyllids, fall armyworm and corn silk flies, and will include studies for development of molecular genetics methods for gene discovery and manipulation to develop genetically-modified pest strains to suppress wild populations, or eliminate their ability to vector pathogens of plant disease; development of detection and surveillance methods for optimization of acoustic, chemical and visual-cue detectors for detection and surveillance of hidden, invasive and outbreak pests; and biological control studies to develop predictive models to target shifting migrations of noctuid pests in response to climate change, and development of improved area-wide landscape management tactics to mitigate pest populations and attract natural enemies and pollinators.

Progress Report
The research efforts by the Insect Behavior and Biocontrol Research Unit resulted in significant progress towards the five objectives and subobjectives for this project. Major progress was made under Objective 1 to understand the stability of genetic sterile male strains for Sterile Insect Technique (SIT). The natural breakdown of genetic elements used to create tetracycline-suppressible sterile males was characterized as a critical step in determining the long-term usage of these strains. After screening 1.2 million zygotic progeny under non-permissive conditions for embryonic lethality (tetracycline-free diet), heritable survival to adulthood was discovered demonstrating breakdown of the genetic element. Under Objective 2, in vitro cultured insect cells infected with Wolbachia were microinjected into larvae of the fall armyworm and persisted to the adult stage and were vertically transmitted from the females to offspring. Under Objective 3, in collaboration with University researchers, acoustic technology was used to disrupt the mating of the Asian citrus psyllid. Movement of males towards disruptive signals is minimal and high-energy disruptive signals reduced mating activity in treated trees. Under Objective 4, studies on the relative importance of intensity vs hue of reflected light on attraction of Asian citrus psyllids and corn silk flies were field tested to examine enhancement of responses to the colors. Traps using multiple modes of stimuli are being prepared for field deployment. Major contribution was made under Objective 5A where the previously developed systems to monitor fall armyworm migration were employed to assess the recent introduction of fall armyworm into sub-Saharan Africa and its subsequent spread. In this study an international collaboration of scientists led by researchers at USDA-ARS (Gainesville) provided genetic analysis information on the migratory potential, strain behavior, and invasion history of the pest in Africa, which is critical for future efforts to monitor, predict, and control the spread of this invasive pest in the Eastern Hemisphere. The findings provide insights into invasive moths relevant to understanding similar events in the United States. Under Objective 5B, field assessments of the establishment of a fall armyworm specific parasitoid were made for use as biocontrol agents of this pest moth.

1. Migration of pest and invasive insects. The introduction of invasive pest species and/or deleterious traits (i.e., pesticide resistance) into domestic pest populations poses a continuing threat to agriculture. This is exemplified by the recent introduction of fall armyworm into Africa, India and Asia. The subsequent spread throughout most of sub-Saharan Africa of the fall armyworm pose a significant threat to African agriculture and potent problem for the Eastern Hemisphere because it is a voracious feeder and has long-distance flight behaviors. ARS researchers in Gainesville, Florida, led an international collaboration of scientists to investigate the migratory potential, behavior, and invasion history of the fall armyworm in Africa, information critical to monitor and control the spread of this pest in the Eastern Hemisphere. The findings provide insights into invasive moths relevant to understanding similar events in the United States.

2. Genetic breakdown of embryonic conditional lethality systems. The stability of genetic sterile male strains for Sterile Insect Technique (SIT) must be validated before long-term usage of these strains. ARS researchers in Gainesville, Florida, collaborated with those at national and international universities to assess the natural breakdown of genetic elements used to create tetracycline-suppressible sterile males. Heritable survivability was discovered in offspring by screening 1.2 million zygotic progeny under non-permissive conditions for embryonic lethality. DNA sequence deletions were found in both the primary-site and in second-site maternal effect genetic modifiers. We expect that descendants of the primary-site mutations should remain susceptible to control by the lethality system; however, the second-site modifier lines are likely to be resistant to further conditional lethal control resulting in a resistant population in the field. This new knowledge indicates that use of a conditional lethality system in the field may require the use of a secondary redundant lethality system to prevent survival of individuals resistant to either system.

3. Enhanced attraction of Asian citrus psyllids to visual targets. The Asian citrus psyllid which serves as a vector of the pathogen causing citrus greening disease or Huanglongbing, is one of the most serious citrus pests worldwide with particularly devastating impacts on the Florida citrus industry. While yellow sticky traps are the standard surveillance method and critical for guidance of pest management strategies, they are not effective when psyllid populations are low. ARS researchers in Gainesville, Florida, have determined optimal paint pigments that enhance attraction of Asian citrus psyllids in the laboratory. One pigment enhanced psyllid attraction over the yellow sticky traps in the field when used by ARS researchers at Ft. Pierce, Florida. These results provide potential for enhancement of current surveillance capabilities for this vector species.

4. Acoustic disruption of Asian citrus psyllids mating. The Asian citrus psyllid which serves as a vector of the pathogen causing citrus greening disease or Huanglongbing, is one of the most serious citrus pests worldwide with particularly devastating impacts on the Florida citrus industry. The males of the Asian citrus psyllid are attracted to sounds produced by females. ARS researchers in Gainesville, Florida, in collaboration with University researchers, assessed acoustic technology to disrupt the mating of the Asian citrus psyllids. Movement of males towards disruptive signals is minimal and high-energy disruptive signals reduced mating activity in treated trees. Widespread use of such devices could help reduce the use of pesticides for management of Asian citrus psyllids.

5. Gene editing of toxin transporter genes in the Indian meal moth. Resistance to toxin-based insecticides has become a major issue for biologically engineered crops. ARS researchers in Gainesville, Florida, used gene editing in the Indian meal moth and the fall armyworm to create mutations in genes that produce transport proteins that are targets of toxin resistance. Gene editing of these transporter genes resulted in white eyed moths and effected Bt resistance. Using this gene editing system, various pesticide resistance genes can be mutated, and the effects studied to find mechanisms to avoid or reverse pesticide resistance.

6. Egg parasitoids reduce fall armyworm populations. The fall armyworm moth is a major pest of corn and grass in North America. The moth must overwinter in the most Southern regions and then migrate each spring to repopulate the Northern regions. ARS researchers in Gainesville, Florida, have assessed the distribution and use of an exotic parasitoid attacking fall armyworm egg masses. Collections of the parasitoid were successful in north central and central Florida, but currently the parasitoid has not been found in south Florida. Egg masses that were 24 hours old and attached to corn leaves had the highest parasitism rate. New techniques to attach egg masses to survey flags has the potential to search for the parasitoid in habitats without corn production.

Review Publications
Mankin, R.W., Burman, H., Menocal, O., Carrillo, D. 2018. Acoustic detection of Mallodon dasystomus (Coleoptera: Cerambycidae) in Persea americana (Laurales: Lauraceae) branch stumps. Florida Entomologist. 101(2):321-323.
Mankin, R.W., Stanaland, D.R., Haseeb, M., Rohde, B., Menocal, O., Carrilo, D., Wignall, A.E. 2018. Assessment of plant structural characteristics, health, and ecology using bioacoustic tools. Proceedings of Meetings on Acoustics (POMA).
Njoroge, A.W., Mankin, R.W., Smith, B., Baributsa, D. 2019. Effects of hypoxia on acoustic activity of two stored-product pests, adult emergence and grain quality. Journal of Economic Entomology. 112(4):1989-1996.
Njoroge, A.W., Affognon, H., Richter, U., Hensel, O., Rohde, B., Chen, Mankin, R.W. 2019. Acoustic, pitfall trap, and visual surveys of stored product insect pests in Kenyan warehouses. Insects. 10(4):1-12.
Turnipseed, R.K., Moran, P.J., Allan, S.A. 2018. Behavioral response of gravid Culex quinquefasciatus, Aedes aegypti, and Anopheles quadrimaculatus (Diptera: Culicidae) to aquatic macrophyte volatiles. Journal of Vector Ecology. 43(2):252-260.
Gillett-Kaufman, J.L., Allan, S.A., Buss, L.J. 2015. Manduca rustica (Lepidoptera: Sphingidae) damage on olive (Olea europaea;Lamiales:Oleaceae) trees in Florida. Florida Entomologist. 98(4):1260-1261.
Nagoshi, R.N., Fleischer, S., Meagher Jr, R.L. 2017. Demonstration and quantification of restricted mating between fall armyworm host strains in field collections by SNP comparisons. Environmental Entomology. 110(6):2568-2575.
Lopez-Martinez, G., Meagher Jr, R.L., Jeffers, L., Bailey, W., Hahn, D. 2016. Low oxygen atmosphere enhances post-irradiation survival of Trichoplusia ni (Lepidoptera: Noctuidae). Florida Entomologist. 99(2):24-33.
Jeger, Michael, Bragard, C., Caffier, D., Candressee, T., Chatzivassiliou, E., Dehnen-Schmutz, K., Gilioli, G., Gregiore, J., Anton, J., Miret, J., Navarro, M., Niere, B., Parnell, S., Potting, R., Rafoss, T., Rossi, V., Urek, G., Van Bruggen, A., Van Der Werf, W., West, J., Winter, S., Day, R., Early, R., Hruska, A., Nagoshi, R.N., Gardi, C., Musbach-Schultz, O., Macleod, A. 2018. Pest risk assessment of Spodoptera frugiperda for the European Union. European Food Safety Authority (EFSA) Journal. 16(8):5351,120pp.
Allan, S.A. 2018. Behavior-based control of insect crop pests. In: Cordoba-Aguilar, A., Gonzales-Tokman, D., and Gonzalez-Santoyo, I. editors. Insect Behavior. New York, NY: Oxford University Press Mexico. p. 309-331.
Weeks, E.N., Baniszewski, J., Gezan, S.A., Allan, S.A., Cuda, J.P., Stevens, B.R. 2018. Methionine as a safe and effective novel biorational mosquito larvicide. Pest Management Science. 75(2):346-355.
Nagoshi, R.N., Dhanani, I., Asokan, R., Mahadevaswamy, H.M., Kalleshwaraswamy, C.M., Sharanabasappa, Meagher Jr, R.L. 2019. Genetic characterization of fall armyworm infesting South Africa and India indicate recent introduction from a common source population. PLoS One. 14(5):e0217755.
Schetelig, M.F., Yan, Y., Zhao, Y., Handler, A.M. 2018. Genomic targeting by recombinase-mediated cassette exchange in the spotted wing drosophila, Drosophila suzukii. Insect Molecular Biology. 28(2):187-195.
Li, J., Handler, A.M. 2019. CRISPR/Cas9-mediated gene editing in an exogenous transgene and an endogenous sex determination gene in the Caribbean fruit fly, Anastrepha suspensa. Gene. 691:160-166.
Meagher Jr, R.L., Agboka, K., Tounou, A.K., Koffi, D., Agbevohia, K.A., Amouze, T., Adjevi, K., Nagoshi, R.N. 2019. Comparison of pheromone trap design and lures for Spodoptera frugiperda (Lepidoptera: Noctuidae) in Togo and genetic characterisation of moths caught. Entomologia Experimentalis et Applicata. 167(6):507-516.
Yang, L., Hu, X.P., Allan, S.A., Alborn, H.T., Bernier, U.R. 2019. Electrophysiological and behavioral responses of the kudzu bug, Megacopta cribrari (Hemiptera: Plataspidae to volatile compounds identified from, kudzu and soybean plants. Journal of Agricultural and Food Chemistry. 67(15):4177-4183.
Owusu, F.A., Tanga, C.M., Paris, T.M., Allan, S.A., Mohamed, S.A., Khamis, F.M., Setamou, M., Borgemeister, C., Ekesi, S. 2018. Size and shape analysis of Trioza erytreae Del Guercio (Hemiptera: Triozidae), vector of citrus huanglongbing disease. Pest Management Science. 75(3):760-771.
Lyu, Q., Guo, M., Ma, M., Mankin, R.W. 2019. External prior learning and internal mean sparse coding for image denoising. Journal of Electronic Imaging. 28(3):033014.
Gauo, M., Ma, Y., Yang, X., Mankin, R.W. 2019. Detection of damaged wheat kernels using an impact acoustic signal processing technique based on Gaussian modelling and an improved extreme learning machine algorithm. Biosystems Engineering. 184:37-44.
Teets, N.M., Dias, V., Pierce, B., Schetelig, M.F., Handler, A.M., Hahn, D.A. 2019. Overexpression of an antioxidant enzyme improves male mating performance after stress in a lek-mating fruit fly. Proceedings of the Royal Society B. 286(1904):20190898.
Tavares, W., Legaspi, J.C., De Castro, A., Haseeb, M., Meagher Jr, R.L., Kanga, L.H., Zanuncio, J.C. 2019. Turmeric powder and its derivatives of Curcuma longa and black mustard oil of Brassica nigra affecting interactions among Spodoptera exigua and its natural Cotesia flavipes and Podisus maculiventris. Dose Response.
De Castro, A.A., Legaspi, J.C., Tavares, W.S., Meagher Jr, R.L., Miller, N.W., Kanga, L., Haseeb, M., Serrao, J.E., Wilckep, C.F., Zanuncio, J.C. 2018. Lethal and behavioral effects of synthetic and organic insecticides Spodoptera exigua and its predator Podisus maculiventris. PLoS One. 13(11):e0206789.
Meagher Jr, R.L., Watrous, K., Fleischer, S., Nagoshi, R.N., Brown, J.T., Bowers, K.E., Miller, N.W., Hight, S.D., Legaspi, J.C., Westbrook, J.K. 2019. Documenting potential sunn hemp (Crotallaria juncea L.) (Fabaceae) pollinators in Florida. Environmental Entomology. 48(2):343-350.
Doherty, E.M., Meagher Jr, R.L., Dale, A.G. 2019. Turfgrass cultivar diversity provides associational resistance in the absence of pest resistant cultivars. Environmental Entomology. 48(3):623-632.
Johnson, D.M., Weeks, E.N., Lovullo, E.D., Shirk, P.D., Geden, C.J. 2018. Mortality effects of three bacterial pathogens and Beauveria bassiana when topically applied or injected into house flies (Diptera: Muscidae). Journal of Medical Entomology. 56(3):774-783.
Wu, K., Shirk, P.D., Taylor, C.E., Furlong, R.B., Shirk, B.D., Pinheiro, D.H., Siegfried, B.D. 2018. CRISPR/Cas9 mediated knockout of the abdominal-A homeotic gene in fall armyworm moth (Spodoptera frugiperda). PLoS One. 13(2):e0208647.
Guo, M., Xuehua, S., Zichen, Z., Miao, M., Wu, X., Mankin, R.W. 2018. Identification and classification of damaged corn kernels with impact acoustics multi-domain patterns. Computers and Electronics in Agriculture. 150:152-161.
Nagoshi, R.N., Goergen, G., Du Plessis, H., Van Den Berg, J., Meagher Jr, R.L. 2019. Genetic comparisons of fall armyworm populations from 11 countries spanning sub-Saharan Africa provide insights into strain composition and migratory behaviors. Nature Scientific Reports. 9(1):8311.
Nagoshi, R.N. 2019. Evidence that a major subpopulation of fall armyworm found in the Western Hemisphere is rare or absent in Africa, which may limit the range of crops at risk of infestation. PLoS One. 14(4):e0208966.