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ARS Home » Pacific West Area » Hilo, Hawaii » Daniel K. Inouye U.S. Pacific Basin Agricultural Research Center » Tropical Crop and Commodity Protection Research » Research » Research Project #429868

Research Project: Detection, Control and Area-wide Management of Fruit Flies and Other Quarantine Pests of Tropical/Subtropical Crops

Location: Tropical Crop and Commodity Protection Research

2017 Annual Report


1a. Objectives (from AD-416):
The goals of our project plan are to conduct foundational research to create the knowledge base necessary to develop innovative control methods and IPM strategies, and to conduct applied research to produce information and products that improve pest control in tropical agriculture. The four major objectives of our program are: Objective 1: Model pest invasion pathways, and investigate the genomics/genetics, physiology/behavior, population dynamics, biology/ecology, and natural enemies of tropical and subtropical fruit flies and other invasive pests to develop technologies to control (contain, suppress, and eradicate) these pests in Hawaii and the Pacific, the U.S. mainland, and elsewhere. 1A: Build an analysis of emerging tephritid fruit fly genomes, including linkage mapping, uniform and consistent gene structural and functional annotation, and comparative genomic analysis. 1B: Conduct surveys on coffee berry borer (CBB) distribution and abundance on Hawaii Island to provide a baseline for a predictive model that integrates GIS, pest insect population dynamics, host plant phenology, weather data and grower practices to drive area-wide management of CBB on Hawaii Island. Objective 2: Determine physiological, genetic, and biological factors limiting the effectiveness of the sterile insect technique (SIT) and natural enemies in control and eradication of fruit flies and other tropical plant pests of quarantine significance. 2A: Improve the effectiveness of mass reared fruit flies for SIT by quantifying the impact of colony infusion on incorporating wild genetics into the SIT colony, and correlating fly performance with genomic markers. 2B: Investigate parasitoid-fruit fly host interactions from the molecular to the field level. Objective 3: To increase export of tropical fruits and vegetables, improve attractants and trapping systems for surveillance and detection, and develop lures, baits, and reduced risk pesticides for area-wide IPM of fruit flies and/or other tropical plant pests of quarantine significance. 3A: Evaluation of C. capitata, B.dorsalis and B. cucurbitae captures in traps baited with solid trimedlure (TML), methyl eugenol (ME) and raspberry ketone (RK) male lure and insecticide dispensers weathered in Hawaii and California. 3B: Evaluation of mixtures, weathering and chemical degradation of SPLAT-spinosad ME and cue-lure (C-L) for fruit fly control under Hawaii and California conditions. 3C: Evaluation of a new attractant system for detection, monitoring and control of the sweetpotato vine borer, a pest of quarantine significance in Hawaii. Objective 4: Provide baseline information for development of low prevalence and/or pest-free zones, for implementation in Hawaii and the U.S. mainland, to promote or allow unimpeded movement of fruit and vegetable exports. 4A: Create area of low pest prevalence (ALPP) as an independent measure of systems approaches for melon fly. 4B: Utilize models to evaluate the sensitivity of trapping grids for detection and control of insect pests such as tephritid fruit flies. 4C. Effectiveness of foliar and bait sprays against C. capitata, B.dorsalis, B. cucurbitae and B. latifrons.


1b. Approach (from AD-416):
Hypothesis 1A: Tephritid genomes have a core set of genes that are related to their proliferation as pests world-wide. If we have trouble generating crosses from a particular species or have issues generating genomic DNA, other species could be sequenced. Approach 1B: Collect baseline data on distribution and abundance of Coffee Berry Borer and associated environmental and climatic data. Then use GIS techniques to produce a region-wide assessment of infestation and economic impact. If this does not work, surveys can be replaced with grower-collected data. Approach 2A: Combine genetic, proteomic and phenotypic data into a synthetic analysis. If portions experiments fail or cannot be integrated, publish portions independently. Approach 2B: Examine tephritid host-parasitoid biology across levels of biological organization to allow integration of foundational knowledge benefiting classical biological control of tephritids. If international releases are impeded by regulatory issues, field work in Hawaii will be done. Hypothesis 3A: Solid male lure wafers with solid insecticidal tape are just as effective, but more convenient and safer to handle than current liquid lure-insecticide formulations used for fruit fly detection programs. If data are inconclusive, chemical analyses of weathered dispensers from trials will at least provide “use pattern” and formulation data for future trials. Hypothesis 3B: Generic combination SPLAT-MAT-spinosad-methyl eugenol/cue-lure mixture will perform as well as Min-U-Gel with naled and ME and C-L separately for fruit fly control/eradication. If the sprayable mixtures are too expensive, recommend addition of small amounts of cue-lure or raspberry ketone to STATIC-spinosad-ME as part of a tank mix. Hypothesis 3C: A binary male attractant system identified with sweetpotato vine borer populations in Vietnam will provide significantly greater male catch in Hawaii populations than male catch in traps baited with an initially identified single compound lure. In cases where low populations are encountered, trials will be shifted to other fields or other time of year where higher populations are present. Hypothesis 4A: Mass trapping using a plant-odor lure, male lure and protein baits can create areas of low pest prevalence (ALPP) in commercial crops and reduce the risk of a mating pair in a consignment when combined with a second measure such as a (less than 99.9986% effective) quarantine treatment. Alternatively, investigate the effects of other independent measures such as poor host status and quarantine treatments. Approach 4B: Develop a biologically-based mathematical model of tephritid traps in a landscape that allows formal quantification of trap network sensitivity. Hypothesis 4C: Current preharvest foliar insecticides being used in IPM systems against other fruit and vegetable pests (e.g., spotted wing drosophila and Asian citrus psyllid) in California and Florida are sufficient to meet quarantine requirements for fruit flies when introduced into Florida and California. Alternatives are to use current practices of either malathion protein bait or GF-120 sprays.


3. Progress Report:
Progress continued for foundational studies and field evaluation of area-wide control strategies for invasive pests of economic importance such as fruit flies, coffee berry borer (CBB) and sweet potato vine borer. Characterization of the genome assembly of melon fly was completed and published. In this manuscript, ARS scientists characterized loci associated with white pupae, providing putative mutations underlying the white pupae trait. Currently validation of this finding is in progress using Clustered Regularly Interspaced Short Palindromic Repeats Associated Protein 9 targeted genome editing. The genome, the Malaysian fruit fly, is now publically available in the National Center for Biotechnology Information (NCBI) in the 5000 Artrhopod Genomes Initiative workspace, and a publication on a linkage map, "Whole genome assembly and functional genomics", is in preparation. Additional Bactrocera and Anastrepha genomes and transcriptome have been sequenced and are currently undergoing analysis. In CBB research, data collection in Kona and Kau continued for the 2017 season, including monitoring of CBB populations, plant phenology, management practices and weather conditions. Geo-referenced data are being collected using an electronic system. A statistically justifiable sampling protocol has been finalized and will be published. Work comparing two methods for detecting coffee from multi-spectral satellite imagery (Maximum likelihood and Object-based image analysis) is complete and has been submitted for publication. In proteomics research, two proteins linked to genetic sexing strains of oriental and Mediterranean fruit flies in the pupal stage were identified and a manuscript published. Proteome profiling across development stages for all four pest fruit fly species in Hawaii was initiated and partially completed. Differentially expressed proteins between parasitized and un-parasitized oriental fruit fly by Diachasmimorpha longicaudata were studied, identified and submitted for publication. Evidence for the role of insect vision in host range expansion for the melon fly was published. The results of these studies demonstrated that, under a variety of conditions, volatiles emitted by the novel host, papaya, did not positively stimulate the behavior of the herbivore; however, vision was the main mechanism driving the exploitation of the novel host. Findings highlight the remarkable role of vision in the host-location process of melon fly and provide empirical evidence for this sensory modality as a potential mechanism involved in host range expansion. In cooperation with the Animal and Plant Health Inspection Service (APHIS), The Compendium of Fruit Fly Host Information (CoFFHI), Edition 2.0, has been released online, providing expanded centralized coverage of what is known, worldwide, about the status of fruits and vegetables as hosts of fruit flies of economic importance. The list of host plants of the melon fly has been updated. Releases and studies of the oriental fruit fly natural enemy, Fopius arisanus, continued in Senegal and Uganda. A chapter on areawide management of fruit flies (Diptera: Tephritidae) in Hawaii which emphasized the importance of biological control, was contributed to the book “Fruit Fly Research and Development in Africa - Towards a Sustainable Management Strategy to Improve Horticulture.” Further studies on the factors that limit abundance of these natural enemies were conducted in Hawaii, Senegal, and Brazil in laboratory studies. A book chapter on The F. arisanus whole genome assembly was released in NCBI and i5k workspace USDA National Agricultural Library, NCBI Bioproject PRJNA258104, and a publication describing this genome was completed. A new species of parasitoid was imported into Hawaii and established in the Pacific Basin Agricultural Research Center Insectary (Fopius ceratitivorus) through a collaboration with University of Hawaii scientist with the goal of releasing it for Mediterranean fruit fly suppression in the Hawaiian Islands. Chemical degradation models for multilure fruit fly trap dispensers were analyzed to determine their potential for use in large California detection programs. Solid three component male lure TMR (trimedlure [TML], methyl eugenol [ME], raspberry ketone [RK]) dispensers impregnated with 2, 2-dichlorovinyl dimethyl phosphate (DDVP) insecticide placed inside Jackson traps were weathered during summer (8 weeks) and winter (12 weeks) in five California citrus growing areas. Dispensers degraded faster during summer than winter. An asymptotic regression model provided a good fit for percent loss (ME, TML, and DDVP) for summer data. Degradation of DDVP in TMR dispensers was similar to degradation of DDVP in insecticidal strips. Based on these chemical analyses and prior bioassay results with wild flies, TMR dispensers could potentially be used in place of three individual male lure traps, reducing costs of fruit fly survey programs. Use of an insecticidal tape would not require TMR dispensers without DDVP to be registered with the U.S. Environmental Protection Agency. This study has generated five peer-reviewed publications over five years of evaluation. Supporting data with recommendations will be sent to federal and state regulatory agencies for possible use in large mainland fruit fly programs after tests in Florida are completed next year. Further progress on tephritid lures and trapping include a paper describing the attraction of melon fly to cue-lure (C-L) published, adding to directly comparable data for oriental fruit fly and Mediterranean fruit fly. Attraction of Queensland fruit fly to a new lure was also tested and reported in a peer reviewed publication. In addition, experiments on fine-scale behavioral response of Mediterranean fruit fly traps was completed and published, yielding information that could be used to improve trapping efficiency. Work has started on integration of trapping model components into the Agent Based Simulation (ABS) “Medfoes” and on extending the ABS to simulate. A significant breakthrough was made on development of Male Annihilation Technique (MAT) against Mediterranean fruit fly based on field trials of mass trapping with the male lure, TML. Although the male lures ME and C-L are routinely recommended worldwide with sanitation and protein baits for Bactrocera species, ARS scientists in Hilo, Hawaii, documented the possible use of TML against Ceratitis species. These results with TML as a MAT treatment are the first field suppression results and deserve further study for use in Integrated Pest Management systems. Their use in large areawide programs is not known, particularly where sterile male flies are used. Further evaluations will continue through 2018. As part of ARS development of systems approaches to alleviate tephritid fruit fly quarantines on the U.S. mainland, data were collected on the efficacy of Asian Citrus Psyllid insecticides against Mediterranean fruit fly, melon fly, and oriental fruit fly and compared to GF-120 Naturalyte Fruit Fly Bait and Malathion + Nulure, two approved field quarantine treatments for fruit flies. The effects of weathering on foliar deposits of promising insecticides against fruit fly adults were conducted by recording adult mortality as a result of exposure to treatments sprayed on guava weathered for 1 and 7 days under Hawaii climatic conditions. Statistical analysis and evaluations to include parasitoid natural enemies of fruit flies will continue in the next fiscal year.


4. Accomplishments
1. Evidence for insect vision in host range expansion. Shortly after introduction into the Hawaiian Islands around 1895, the highly destructive melon fly was provided the opportunity to expand its host range to include a novel host, papaya. Female melon fly rely strongly on vision to locate host fruit. Given that the papaya fruit is visually apparent in the papaya agro-ecosystem, ARS scientists in Hilo, Hawaii, and scientists from Lincoln University, Missouri, hypothesized that female melon flies used vision as the main sensory modality to find and exploit the novel host fruit. Using a comparative approach that involved a series of studies under natural and semi-natural conditions in Hawaii, the ability of female melon flies to locate and lay eggs in papaya fruit using the sensory modalities of olfaction and vision alone and also in combination were assessed. These studies demonstrate that, under a variety of conditions, volatiles emitted by the novel host do not positively stimulate the behavior of the herbivore; however, vision seems to be the main mechanism driving the exploitation of the novel host. Our findings highlight the remarkable role of vision in the host-location process of melon fly and provide empirical evidence for this sensory modality as a potential mechanism involved in host range expansion.

2. The list of host plants of the melon fly (Bactrocera cucurbitae) is available. The list has been updated and published and is also available online at the USDA Compendium of Fruit Fly Host Information (CoFFHI; https://coffhi.cphst.org/). Melon fly causes direct damage to fruits and vegetables through oviposition and larval feeding and restricts movement of commodities across national and international borders. Establishment of appropriate regulatory procedures to prevent further spread of melon fly, however, is dependent on the knowledge of the status of fruits and vegetables as melon fly hosts, and the list of the host plants of melon fly had not been updated for about 30 years. An ARS researcher in Hilo, Hawaii, in collaboration with an Animal Plant Health Inspection Service (APHIS) senior pest risk analyst, developed an updated host list through summarization of worldwide publications. The updated host list identifies 136 fruit-bearing plant taxa, belonging to 62 plant genera in 30 plant families, that have records of field infestation by melon fly and an additional 137 plant taxa, belonging to 80 plant genera in 39 plant families, which are suggested to be hosts, but lack data of infestation in the field. These updated host records will be used in vetting and developing the official USDA list of host plants of the melon fly, which will be published by APHIS as a federal order.

3. The compendium of fruit fly host information (CoFFHI). Edition 2.0, has been released online, providing expanded centralized coverage of what is known, worldwide, about the status of fruits and vegetables as hosts of fruit flies of economic importance. Fruit flies cause direct damage to fruits and vegetables through oviposition and larval feeding and restrict movement of commodities across national and international borders. Establishment of appropriate regulatory procedures, however, is dependent on the knowledge of the status of commodities as hosts for fruit fly species. The online accessible USDA Compendium of Fruit Fly Host Information (CoFFHI; https://coffhi.cphst.org/), developed through collaborative efforts of ARS scientists in Hilo, Hawaii, and Beltsville, Maryland, scientists from the Animal and Plant Health Inspection Service, and scientists from North Carolina State University's Center for Integrated Pest Management (CIPM), provides some host information for over 1000 fruit fly species along with provisional host lists, and additional host documentation for several more. As a primary reference on fruit fly host plants, CoFFHI is designed to serve as a tool to help regulatory scientists and regulatory officials of USDA and various state regulatory agencies design and implement effective detection, monitoring, suppression, and eradication programs against fruit fly species that pose significant threats to U.S. agriculture and natural resources.

4. Improving California trap programs for detection of fruit flies. Chemical degradation models for multiple male lurefruit fly trap dispensers were constructed and analyzed by ARS scientists in Hilo, Hawaii, scientists from the University of California, Davis, and Riverside, and scientists from industry, to determine their potential for use in large multi-million dollar California fruit fly detection programs. Solid three component male lure TMR (trimedlure [TML], methyl eugenol [ME], raspberry ketone [RK]) dispensers placed inside Jackson traps were weathered during summer (for 8 weels) and winter (for 12 weeks) in five citrus growing areas where fruit flies had been captured previously. Percent loss of TML (the male lure for Mediterranean fruit fly), ME (the male lure for oriental fruit fly), and RK (the male lure for melon fly) was measured. Based on regression analyses, TML degraded the fastest followed by ME, while degradation of the more chemically stable RK was discontinuous, did not fit a regression model, but degradation followed similar seasonal patterns. There were few location differences for all three male lures and dispensers degraded faster during summer than winter. TMR dispensers used in place of three individual male lure traps could reduce the costs of survey programs by more than sixty-six percent.


Review Publications
Manoukis, N., Jang, E.B., Dowell, R.V. 2017. Survivorship of male and female Bactrocera dorsalis in the field and the effect of male annihilation technique. Entomologia Experimentalis et Applicata. 162:243-250.

Manoukis, N., Mangine, T.E. 2016. Response of the pearly eye melon fly Bactrocera cucurbitae (Coquillett) (Diptera:Tephritidae) mutant to host-associated visual cues. Hawaiian Entomological Society Proceedings. 48:15-20.

McQuate, G.T., Nicanor, L.J., Nakamichi, K. 2017. Annotated world bibliography of host plants of the melon fly, Bactrocera cucurbitae (Cocquillett) (Diptera:Tephritidae). Insecta Mundi. 0527:1-339.

Chang, C.L. 2016. Proteomic identification of a potential sex biomarker for 2 fruit fly species at pupal stage. Journal of Asia Pacific Entomology. doi:10.1016/j.aspen2016.11.005.

Vargas, R.I., Leblanc, L., McKenney, M.P., Mackey, B.E., Badji, K. 2016. Rearing Fopius arisanus (Sonan) (Hymenoptera: Braconidae) on Mediterranean fruit fly and its introduction into Senegal against Oriental fruit fly (Diptera: Tephritidae). Hawaiian Entomological Society Proceedings. 48:85-94.

Pinero, J.C., Souder, S., Vargas, R.I. 2017. Vision-Mediated exploitation of a novel host plant by a tephritid fruit fly. PLoS One. doi:10.1371/journal.pone.0174636.

Vargas, R.I., Souder, S., Morse, J.G., Grafton-Cardwell, E.E., Haviland, D.R., Kabashima, J.N., Faber, B.A., Mackey, B.E., Nkomo, E., Cook, P., Stark, J.D. 2017. Chemical degradation of TMR multi-lure dispensers for fruit fly detection weathered under California climatic conditions. Journal of Economic Entomology. doi:10.1093/jee/tox159.

Siderhurst, M.S., Park, S.J., Suttles, C.N., Jamie, I.M., Manoukis, N., Jang, E.B., Taylor, P.W. 2016. Raspberry Ketone Trifluoroacetate, a new attractant for the Queensland fruit fly (Bactrocera tryoni (Froggatt)). Journal of Chemical Ecology. 42:156-162.

McQuate, G.T., Sylva, C.D., Liquido, N.J. 2017. Natural field infestation of Mangifera casturi and M.lalijiwa by oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae). International Journal of Insect Science. 9:1-7.

Liquido, N.J., McQuate, G.T., Suiter, K.A. 2016. Compendium of fruit fly host information (CoFFHI), edition 2.0. USDA CPHST Online Database. Available: https://coffhi.cphst.org/.

Follett, P.A., McQuate, G.T., Sylva, C.D., Swedman, A.L. 2016. Sensitivity of the quarantine pest rough sweetpotato weevil, Blosyrus asellus to postharvest irradiation treatment. Hawaiian Entomological Society Proceedings. 48:23-28.

Sim, S., Geib, S.M. 2017. A Chromosome-scale assemby of the Bactrocera cucurbitae genome provides insight to the genetic basis of white pupae. G3, Genes/Genomes/Genetics. doi:10.1534/g3.117.040170.

Goncalves, R., Manoukis, N., Nava, D.E. 2017. Effect of Fopius arisanus Sonan oviposition experience on parasitization of Bactrocera dorsalis Hendel. Biocontrol. 62(5):595-602. https://doi: 10.1007/s10526-017-9827-7.

Geib, S.M., Guang Hong, L., Sim, S.B., Murphy, T. 2017. Whole genome sequencing of the Braconid parasitoid wasp Fopius arisanus, an important biocontrol agent of pest Tepritid fruit flies. G3, Genes/Genomes/Genetics. doi:10.1534/g3.117.040741.