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ARS Home Southeast Area Miami, Florida Subtropical Horticulture Research Research





- Yang, Xiangbing
- Cloonan, Kevin
- Singh, Sukhwinder
- Tabanca, Nurhayat
- 2023
- 2022
- 2021
- Publications
- Crop Protection & Quarantine (304)

Research Project: Mitigation of Invasive Pest Threats to U.S. Subtropical Agriculture **Location:
                            Subtropical Horticulture Research** 2021 Annual Report **Objectives**
                                

1. Identify semiochemicals that mediate the behavior and physiology of exotic insect pests and develop semiochemical-based tools that lead to products for pest detection, behavioral disruption, and surveillance. [NP 304, Component 4, Problem Statement 4A]
1.A. Document behavioral responses and olfactory chemoreception to semiochemicals that have potential application in pest monitoring and control systems.
1.B. Identify and quantify insect semiochemicals; develop improved systems to collect, analyze and identify semiochemicals.
1.C. Develop synthetic and natural product lures based on host location and/or feeding cues that are formulated for effective use in IPM programs.

2. Evaluate ‘next generation’ technologies to advance methods for fruit fly detection and eradication, such as lasers, sonic methods, or nano-technologies. [NP 304, Component 4, Problem Statement 4A]
2.A. Compare available remote trapping systems that can automatically count and identify trapped insects; optimize automated detection systems for adult fruit fly pests.
2.B. Evaluate imaging techniques and non-destructive chemical analysis methods for detection of larval infestation within host fruit.

3. Evaluate essential oils for natural insect pest toxicants and elucidate the physiological mechanisms underlying resistance to conventional pesticides. [NP 304, Component 4, Problem Statement 4A]
3.A. Determine the molecular/physiological basis for development of pesticide resistance in adult fruit flies.
3.B. Identify plant essential oils and plant extracts that have insecticidal, repellent, or oviposition deterrent properties against adult fruit flies and other target pests.
3.C. Determine the specific chemical components responsible for the toxic/repellent effects of essential oils and plant extracts.

4. Integrate tools, technologies and management strategies to reduce the threat of pest establishment and mitigate the impact of exotic pest incursions. [NP 304, Component 4, Problem Statement 4A]
4.A. Develop new approaches to assess efficacy of lures, repellents, and control practices based on spatial statistics and contour analysis of trap captures in the field.
4.B. Develop improved IPM protocols for tephritid fruit flies, ambrosia beetles, and other target pests by integrating semiochemical-based technologies with other management options, such as biological control, judicious alternating use of insecticides to manage pesticide resistance, sanitation and other cultural practices. **Approach**
                                

Research will consist of field and laboratory experiments to investigate aspects of basic biology, physiology and chemical ecology that can be exploited to develop integrated pest management approaches for invasive insects that impact subtropical agriculture. Target species will include pests that threaten to invade or have recently established in south Florida, including fruit flies in the family Tephritidae (Oriental fruit fly, Medfly, and Anastrepha species) and ambrosia beetles that vector fungal pathogens (redbay ambrosia beetle and Euwallacea shot-hole borers). Strategies will include (1) identifying semiochemicals from natural product sources that can alter insect behavior, such as attractants, repellents, and oviposition deterrents; (2) developing new detection and delimitation tools that will include formulated lures, discrete attract-and-kill bait stations, next generation technologies like smart traps for automated pest surveillance, and non-destructive imaging techniques for detection of hidden infestation in agricultural commodities; (3) improving pesticide resistance management by identification of pesticide modes of action and physiological responses of fruit flies to toxicants; (4) evaluating plant essential oils as sources of natural toxicants (biopesticides) with less environmental impact; and (5) developing new approaches to assess efficacy of lures, repellents, and control practices based on spatial statistics and contour analysis of trap captures in the field. **Progress Report**
                                

Progress was made on Sub-objective 1a: Document behavioral responses and olfactory chemoreception to semiochemicals that have potential application in pest monitoring and control systems and Sub-objective 1b: Identify and quantify insect semiochemicals; develop improved systems to collect, analyze and identify semiochemicals. The following research was conducted by ARS researchers in Miami, Florida: 

Redbay ambrosia beetle and Euwallacea shot hole borers are vectors of laurel wilt and Fusarium dieback, two fungal diseases of avocado. Incorporation of beetle repellents into pest management programs may reduce the incidence of these diseases. Previously, ARS researchers in Miami, Florida, identified piperitone as a new repellent for Euwallacea. Subsequent studies compared piperitone to verbenone and a-farnesene. Euwallacea captures in traps baited with lures were compared to captures in traps containing lures plus a repellent. Farnesene was ineffective; however, piperitone and verbenone were equally effective, reducing captures by 50-70% for 10-12 weeks. Field tests in progress indicate that piperitone is also effective against redbay ambrosia beetle. Since piperitone is less expensive than verbenone, the standard beetle repellent, these studies identify an economical alternative for management of both pests. Manuscripts are in preparation to report this work.

The invasive lychee erinose mite (LEM, Aceria litchii), recently introduced to Florida, is a high priority pest with potential to devastate the state’s lychee production. LEM primarily attacks new leaf growth and flower buds, thereby preventing fruit development. At present, there are no attractants for monitoring tools. ARS scientists in Miami, Florida, in collaboration with the University of Florida, initiated research to identify potential host kairomones by comparing volatiles emitted from various lychee tissues (new flush leaves, older leaves, and flower buds). Chromatographic analysis indicated that the attractive tissue samples were rich in sesquiterpenoids. Behavioral assays are ongoing to identify specific kairomones. 

The hibiscus bud weevil (Anthonomus testaceosquamosus) is a new invasive pest that negatively impacts the hibiscus industry in south Florida, resulting in large economic losses. Females oviposit in flower buds and larvae develop inside the bud, causing bud drop prior to flowering. In collaboration with the University of Florida, volatile emissions from leaves, buds, and open flowers from Hibiscus were distilled, analyzed, and identified. Qualitative and quantitative differences were observed in all three samples and saturated and polyunsaturated long-chain fatty acids were the dominant compounds. Work is ongoing to identify the volatile components that attract females to hibiscus buds. 

In collaboration with Odessa National Polytechnic University (Ukraine), research is being conducted with a series of thymol and carvacrol esters (propyl-, butyl, octyl- and benzyl-) to assess relative attraction of medfly. Combining behavioral bioassays with electroantennography to quantify olfactory response, four new male attractants were identified, with benzyl and octyl esters of thymol and carvacrol analogs being the most potent. Chemical analyses identified key structural features (specific functional groups attached to the aromatic ring) associated with attraction. This work increases our understanding of structure-function relationships in insect kairomones, and helps direct future research on development of improved medfly lures. 

Medfly is a serious pest of fruits and vegetables worldwide. Trimedlure is a synthetic male attractant currently used to monitor for this pest. However, APHIS recently identified a need for new male attractants. In collaboration with national and international scientists, ARS researchers in Miami, Florida, evaluated a series of essential oils for potential new attractants, including Tetradenia riparia (native to southern Africa), Magnolia citrata (Vietnam), Tanacetum annuum (Morocco), and three species of Pulicaria (Saudi Arabia). Studies included behavioral bioassays to assess male attraction and gas chromatography-mass spectrometry (GC-MS) analyses to document chemical constituents. Results show that several of these oils are highly attractive to male medfly. This work has been reported in several publications in 2021; however, investigations are still ongoing to identify specific attractive chemicals. Since essential oils are natural plant products, safe to the environment and inexpensive to produce, this research will lead to promising alternatives to Trimedlure for medfly detection and management. 

Black pod disease (Phytophthora palmivora) and insect pests cause a severe reduction in cacao production. Beetle holes were observed on infected pods but not on healthy pods, indicating that pod-boring beetles are likely attracted to lesions. Therefore, research was initiated by ARS researchers in Miami, Florida, to identify potential beetle attractants emitted by Phytophthora. Headspace volatiles were collected using solid-phase microextraction-gas chromatography-mass spectrometry (HS-SPME/GC-MS). However, the spectral complexity of isomers and large number of unknown compounds posed a significant challenge. Several synthetic chemicals were purchased to facilitate identification, but this is still in progress. This study complements data on disease-resistant cacao cultivars and a survey of bark and ambrosia beetles in Ecuador.

The giant African snail (GAS) is an invasive pest that causes feeding damage to a wide variety of agricultural, ornamental, and native plants. In recent years, GAS has established in Florida, prompting an extensive eradication program. Preliminary studies showed that canine dogs can locate GAS on properties where previous human surveys did not. In collaboration with APHIS-PPQ, research was initiated to determine if signature volatiles are emitted from the mucus trails of GAS. If so, these chemical signals could provide the basis for detection of GAS by trained dogs. Although conventional distillation procedures were not successful, modified procedures were able to detect a series of semivolatile aliphatic aldehydes and acids. This project recently was awarded USDA Farm Bill funding.

Caribbean fruit fly is a pest in Florida, the Caribbean, and Central America to over 100 hosts, particularly citrus and guava. Insecticidal baits are the primary method to control this pest. However, intensive insecticide uses can lead to an increase in resistance in pest populations. A protocol was developed to identify the level of resistance in wild flies to insecticides (organophosphate, carbamates etc.). Lab bioassays were conducted on adults (insecticide free strain) to establish baseline susceptibility to insecticide (i.e., methomyl) and compare to susceptibility of F2 generation collected from the field. Tests are ongoing to determine the resistance level of wild flies to various classes of insecticide. 

Progress was made on Sub-objective 3a: Determine the molecular/physiological basis for development of pesticide resistance in adult fruit flies, Sub-objective 3b: Identify and quantify insect semiochemicals; develop improved systems to collect, analyze and identify semiochemicals, and Sub-objective 4b, Develop improved IPM protocols for tephritid fruit flies, ambrosia beetles, and other target pests by integrating semiochemical-based technologies with other management options, such as biological control, judicious alternating use of insecticides to manage pesticide resistance, sanitation and other cultural practices. 

The Caribbean fruit fly is a pest of numerous tropical and subtropical fruits. Extensive use of insecticides has led to environmental concerns and an increase in pesticide resistance. ARS scientists in Miami, Florida, conducted lab research to evaluate anisole, a plant based volatile compound, for toxicity to Caribbean fruit fly. Results showed that anisole was effective against all insect stages: eggs, larvae, pupae, and adults via contact, fumigation, and residue tests. Anisole treatments caused 100% mortality in all tests within 24 hours using appropriate concentrations. Results indicate that anisole has good potential as an environmentally sound alternative to conventional insecticides and fumigants. 

Tephritid fruit flies are serious pests of fruits and vegetables worldwide, causing severe export restrictions. Concerns about the impact of conventional pesticides on the environment and an increase in pesticide resistance in fruit flies have prompted research to identify environmentally sound alternatives. In collaboration with scientists from Turkey, ARS scientist in Miami, Florida, initiated an investigation of Juniperus foetidissima fruit and leaf essential oils for potential toxicity to adult female Caribbean fruit fly (Anastrepha suspensa). Commercial insecticides (i.e., methomyl, fenthion) were also tested as baselines to compare the toxicity of the two oils. Tests are ongoing to determine lethal effect of the oils at different concentrations. 

In collaboration with Animal and Plant Health Inspection Service (APHIS), ARS scientists in Hilo, Hawaii and Miami, Florida, developed postharvest fumigation protocols using ethyl formate to control Oriental fruit fly (Hilo) and Caribbean fruit fly (Miami). The objective is to develop standardized fumigation protocols applicable for multiple tephritid species. Results demonstrated that ethyl formate is effective against immature stages of both species. An additional test combining ethyl formate with anisole (a volatile plant oil) showed a synergistic effect for Caribbean fruit fly. **Accomplishments**
                                

1. Evaluation of synthetic fruit fly lures. The Caribbean fruit fly (Anastrepha suspensa) is a quarantine pest of citrus and a production pest of guava and other specialty fruits in Florida. Early pest detection and management requires effective lures. In collaboration with APHIS, ARS scientist in Miami, Florida, conducted lab and field studies to compare synthetic 2- and 3-component (2C, 3C) cone lures, the current standards for fruit fly monitoring. In field tests, 2C lures captured significantly more flies than 3C lures. Field longevity was 8 weeks for 2C lures and 6 weeks for 3C lures. In addition, scientists used new ion chromatography methods to measure lure emissions and relate levels of ammonia, putrescine, and trimethyl amine with fly attraction observed in the field. This study provides data requested by APHIS and benefits the regulatory agency with design of field monitoring protocols for pest fruit flies. **Review Publications**
                            *Stappen, I., Wanner, J., Tabanca, N., Bernier, U.R., Kendra, P.E. 2021. Blue tansy oil: chemical composition, repellent activity against aedes aegypti and attractant activity for ceratitis capitata. Natural Product Communications. 16(2): 1–8. https://doi.org/10.1177/1934578X21990194.*
                                *Luu-Dam, N., Tabanca, N., Estep Iii, A.S., Nguyen, D., Kendra, P.E. 2021. Insecticidal and attractant activities of magnolia citrata leaf essential oil against two major pests from diptera: aedes aegypti (culicidae) and ceratitis capitata (tephritidae). Molecules. 26(8): 2311. https://doi.org/10.3390/molecules26082311.*
                                *Kendra, P. E., N. Tabanca, W. S. Montgomery, J. Niogret, D. Owens, and D. Carrillo. 2020. Chapter 18. Essential oils as lures for invasive ambrosia beetles. Pp. 495-513 In: K. H. C. Baser and G. Buchbauer (eds.), Handbook of Essential Oils: Science, Technology, and Applications, 3rd edition. CRC Press, Boca Raton, FL. (ISBN 9780815370963)*
                                *Blythe, E.K., Tabanca, N., Demirci, B., Kendra, P.E. 2020. Chemical composition of essential oil from tetradenia riparia and its attractant activity for mediterranean fruit fly, ceratitis capitata  . Natural Product Communications. 15(9): 1–6. https://doi.org/10.1177/1934578X20953955.*
                                *Hoeferi, M., Wanner, J., Tabanca, N., Abbas, A., Gochev, V., Schmidt, E., Kaul, V.K., Singh, V., Jirovetz, L. 2020. Biological activity of matricaria chamomilla essential oils of various chemotypes. Planta Medica International Open. 7: e114–e121. https://doi.org/10.1055/a-1186-2400.*
                                *Kwon, T.H., Park, C.G., Lee, B., Zarders, D.R., Roh, G.H., Kendra, P.E., Cha, D.H. 2020. Ethyl formate fumigation and ethyl formate plus cold treatment combination as potential phytosanitary quarantine treatments of Drosophila suzukii in blueberries. Journal of Asia Pacific Entomology. 24(1):129-135. https://doi.org/10.1016/j.aspen.2020.11.008.*
                                *Cruz, L. F., O. Menocal, P. E. Kendra, and D. Carrillo.  2021.  Phoretic and internal transport of Raffaelea lauricola by different species of ambrosia beetle associated with avocado trees.  Symbiosis. https://doi.org/10.1007/s13199-021-00776-2.*
                                *Al-Massarani, S.M., El-Gamal, A.A., Al-Rehaily, A.J., Al-Sheddi, E.S., Al-Oqail, M.A., Farshoori, N.N., Estep, A.S., Tabanca, N., Becnel, J.J. 2021. Insecticidal activity and free radical scavenging properties of isolated phytoconstituents from the saudi plant nuxia oppositifolia (hochst). Molecules. 26(4):1-8. https://doi.org/10.3390/molecules26040914.*
                                *Tsikolia, M., Opatz, T., Kauhl, U., Tabanca, N., Demirci, B., Tenbroeck, S., Linthicum, K., Bernier, U.R. 2021. Trials for gathering information on an unknown peak in the GC-MS spectra of horse and pony hair extracts. Advances in Entomology. 9(2):100-111. https://doi.org/10.4236/ae.2021.92009.*
                                *Yang, X., Liu, Y.-B. 2021. Anisole is an environmentally friendly fumigant for postharvest pest control. Journal of Stored Products Research. 93. Article 101842. https://doi.org/10.1016/j.jspr.2021.101842.*


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