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United States Department of Agriculture

Agricultural Research Service

Research Project: Sustainable Pest Management Strategies for Arid-land Crops

Location: Pest Management and Biocontrol Research

2013 Annual Report

1a. Objectives (from AD-416):
Develop knowledge and control tactics based on the physiology, biochemistry, genetics and vector-pathogen interactions of insect pests. Characterize and exploit interactions among plants, insect pests and natural enemies; investigate the role of arthropod predators and trophic interactions for improved biological control. Characterize flight behavior and dispersal of insect pests and natural enemies; elucidate relationships among landscape structure, pest and natural enemy biology and dispersal behavior. Refine sampling strategies for insect pests and their associated natural enemies; develop and refine economic thresholds for sucking pests in cotton that incorporate biological control potential; support post-eradication detection of pink bollworm populations. Refine insecticide-based management strategies; characterize factors influencing resistance to chemical insecticides and insecticidal proteins in transgenic crops; evaluate insecticide selectivity; support post-eradication pink bollworm resistance monitoring in Bt cotton.

1b. Approach (from AD-416):
Research will build a solid foundation of fundamental tactics for avoiding pest problems and will strengthen prescriptive pest control through refinement of monitoring, decision aids and effective treatment options. Research will explore and exploit the molecular and chemical basis of male-derived factors on female mating inhibition and hormonal factors regulating reproduction and diapause in Lygus. hesperus, the molecular basis of water channel proteins in Bemisia tabaci, the impact of plant virus and plant allelochemical mediated changes on B. tabaci fitness and insecticide resistance, respectively, and the molecular basis of Bt resistance in Pectinophora gossypiella. Further research will exploit semiochemicals and tri-trophic interactions for enhanced biological control, and identify insect and plant based semiochemicals enabling mating disruption and improved monitoring of B. tabaci and L. hesperus. Flight behavior and inter- and intra-crop dispersal of L. hesperus, and source-sink relationships for arthropod predators inhabiting the agro-ecosystem will be quantified, facilitating IPM at the landscape scale. Selective insecticides and improved decision aids that account for natural enemy abundance will be evaluated and developed for B. tabaci in cotton. Research will further support P. gossypiella post-eradication efforts through refinement of pheromone-based monitoring systems and detection of resistance to Bt cotton. Replaces 5347-22620-017-00D, 5347-22620-018-00D and 5347-22620-020-00D (10/10).

3. Progress Report:
Studies of plant bugs (Lygus) identified a new compound transferred from male to female during mating. This compound initially enhances inhibition of mating, but a breakdown product promotes mating. Synthetic versions of male-derived chemicals influenced mating behaviors in assays. Analyses of Lygus male sexual glands showed an increase in the numbers of genes expressed following mating. A Lygus protein receptor similar to those that regulate mating in other species was identified and characterized. Chemicals that promote egg laying but do not influence mating, were identified from brains of Lygus females. The diapause response of Lygus to different daylengths was defined and validation was initiated. Sex pheromones of three Lygus pest species were characterized and assayed. Lygus odorant binding proteins, essential for chemical communications, were analyzed but initial efforts at biochemical interference were inconclusive. The number of known functional aquaporins (proteins controlling internal water balance) was increased to five for Lygus and to seven for the sweetpotato whitefly, which increases the potential for genetic or biochemical-based controls. Botanical extracts influenced aquaporin function in assays, and were insecticidal when fed to the insects. Studies of the whitefly indicated the production of specific detoxification enzymes varied with exposure to different hosts. These results begin to elucidate the complex physiological relationships that must be understood to develop novel biochemically- or ecologically-based management approaches for Lygus and whitefly. Selection experiments produced a new strain of pink bollworm that is highly resistant to the two transgenic bacterial toxins used world-wide in commercial cotton, and the inheritance patterns of this resistance were elucidated. Analyses of pink bollworm from India, which are resistant to the most common transgenic toxin in cotton (Cry1Ac) indicated novel changes to a cell adhesion protein (cadherin). The changes differ from those in the modified cadherin of resistant pink bollworm selected in the laboratory. These results implicate the cadherins as a critically important source of resistance in pink bollworm, and are important in developing strategies to avoid or monitor resistance in the field. Protein markers used to study insect dispersal were improved, and movement patterns of Lygus and natural enemies within cotton were examined in the field. A new insect sampling method utilizing a rapid knockdown insecticide was evaluated. Studies of predator gut contents were conducted to distinguish cannibalism and scavenging from predation. Field studies of biological control-based thresholds for sweetpotato whitefly evaluated use of predator-prey ratios as an addendum to standard thresholds based on whitefly numbers only. Field surveys examined the pest and beneficial arthropod complexes associated with guayule seedlings. Better understanding of intra- and inter-crop diversity, population levels, and dispersion patterns of pests and their natural enemies is essential to successful integration of new management tactics into production systems.

4. Accomplishments
1. An adult transcriptome for the western tarnished plant bug, Lygus hesperus. The western tarnished plant bug is an important crop pest in the western United States for which almost no molecular genetics information exists. ARS scientists at the Arid-Land Agricultural Research Center, Maricopa, Arizona, used next-generation sequencing to construct an adult Lygus transcriptome, which represents a record of gene expression. Compared with better-studied insects, many of the sequences were unique to Lygus. Intriguingly, compared with other insects a higher percentage of sequences were associated with antioxidant activity, which may be important to resisting biotic and abiotic stress. Exposure to high temperatures triggered increased expression of heat shock proteins that are thought to facilitate short-term adaptation to environmental stresses. This information serves as a broad baseline for future research, and will be essential to efforts to identify and develop new species-specific non-insecticidal controls.

2. Identification of Lygus plant bug sex pheromones. Lygus bugs (western tarnished plant bug, tarnished plant bug, and the pale legume bug) are important pests of many field, fruit, and vegetable crops. Elucidation of the chemicals emitted by females to attract males for mating (sex pheromones) has represented an intractable problem. An ARS scientist at the Arid-Land Agricultural Research Center, Maricopa, Arizona, and Israeli collaborators identified the chemical components of the respective Lygus sex pheromones and demonstrated attractiveness to males in field studies. These results provide the opportunity to develop pheromone lures and traps to permit improved population detection and monitoring.

3. Invasive species detection using traps and encounter-rate equations. Although the pink bollworm has been eradicated from several production regions of the United States, this critically important pest of cotton remains a major problem in other parts of the world. Sustainable eradication is dependent upon effective monitoring methods to detect re-invasion. ARS scientists at the Arid-Land Agricultural Research Center, Maricopa, Arizona, developed simulation methods to determine numbers and arrangements of pheromone traps to facilitate efficient monitoring. The methods use estimates of trap attractiveness combined with moth flight distance to instantaneously solve for trap number through modified encounter-rate equations. Estimates from the simulations will be useful to action agencies for optimizing trapping efforts for the pink bollworm. Furthermore, the simulation approach is adaptable to detection and monitoring of other invasive pests.

4. Transgenic crops have no effect on insect predators or parasitoids. Transgenic crops currently produce a number of target-specific insecticidal proteins from Bacillus thuringiensis (Bt) and have been cultivated on millions of hectares globally. Concerns about the ecological risk associated with these crops, specifically to nontarget organisms, continue to be raised. An ARS scientist from the Arid-Land Agricultural Research Center, Maricopa, Arizona, and researchers at Cornell University, ARS in Ames, Iowa, and Agroscope in Zurich, Switzerland, showed that the biology of two common predators (insidious flower bugs and big-eyed bugs) found in cotton and maize were not affected by chronic exposure to several Bt proteins via ingestion of Bt-resistant prey fed on Bt-maize and cotton over two generations. Similarly, the biology of a common parasitoid (Cotesia) of various caterpillar pests was not affected when exposed to Bt proteins through a Bt-resistant host feeding on Bt maize over multiple generations. Use of Bt-resistant prey and hosts instead of susceptible prey overcame a common problem with such assays by ensuring any observed effects were caused by the Bt toxin instead of by poor prey quality. Results are valuable to governmental authorities responsible for regulating transgenic crops, other scientists, and a general public concerned about the environmental effects of biotechnology.

5. Thermal ecology of the western tarnished plant bug (Lygus). Previous descriptions of Lygus development rates were simplistic and used antiquated experimental and statistical methodology. Because the adult reproductive diapause of Lygus in southern regions terminates in early winter, development and survival of immature stages and young adults under winter conditions may be as important to successful overwintering as the diapause. ARS scientists from the Arid-Land Agricultural Research Center, Maricopa, Arizona, and the Yakima Agricultural Research Laboratory, Wapato, Washington, defined the temperature dependence of development and survival for all Lygus life stages. Demonstration of extended development times and host-free survival under low-temperature conditions contradicts earlier reports that place ecological constraints on mechanisms of Lygus overwintering. Ecological interpretation of these results is consistent with field observations of overwintering populations, and quantitative models permit prediction of population phenology given appropriate meteorological inputs. These results will be indispensible to a more complete understanding of Lygus overwintering ecology, and provide important baseline information for ongoing examinations of the physiology and molecular biology of Lygus thermal ecology.

Review Publications
Penick, C.A., Trobaugh, B., Brent, C.S., Liebig, J. 2013. Head butting as an early indicator of reproductive disinhibition in the termite zootermopsis nevadensis. Journal of Insect Behavior. 26:23-24.

Byers, J.A. (2012). Modelling female mating success during mass trapping and natural competitive attraction of searching males or females. Entomologia Experimentalis et Applicata. 145:228-237.

Hartfelder, K., Bitondi, M., Brent, C.S., Guidugli-Lazzarini, K.R., Simoes, Z.L., Stabentheiner, A. 2013. Physiology and biochemistry of honey bees. In:Dietermann, V., Ellis, J.D., Neumann, P.,editors. The COLOSS BEEBOOK, Volume I: Standard methods for Apis mellifera research. South Glamorgan, United Kingdom: Ibra Publications.

Spurgeon, D.W., Cooper, W.R. 2012. Disinfestation of Beauveria bassiana from adult Lygus hesperus using ultraviolet-C radiation. Southwest Entomology. 37(4):449-457.

Hull, J.J., Geib, S.M., Fabrick, J.A., Brent, C.S. 2013. Sequencing and de novo assembly of the western tarnished plant bug (Lygus hesperus) transcriptome. PLoS One. 8:1.

Byers, J.A. 2012. Ecological interactions of bark beetles with host trees. Psyche. 2012:1-3.

Han, B., Zhang, Q.H., Byers, J.A. 2012. Attraction of the tea aphid, Toxoptera aurantii, to combinations of volatiles and colors related to tea plants. Entomologia Experimentalis et Applicata. 144:258-269.

Sivakoff, F.S., Rosenheim, J.A., Hagler, J.R. (2012). Relative dispersal ability of a key agricultural pest and its predators in an annual agroecosystem. Biological Control. 63:296-303

Spurgeon, D.W., Cooper, W.R. 2012. Temperature-dependent reproductive development of Lygus hesperus (Hemiptera: Miridae). Environmental Entomology. 41(4):941-949.

Crowder, D., Ellsworth, P., Naranjo, S.E., Tabashnik, B., Carriere, Y. 2013. Modeling resistance to juvenile hormone analogs: linking evolution, ecology and management. In: Devillers, James, editor. Juvenile Hormones and Juvenoids. Boca Raton, FL: CRC Press. p. 99-126.

Hull, J.J., Hoffmann, E.J., Perera, O.P., Snodgrass, G.L. 2012. Identification of the western tarnished plant bug (lygus hesperus) olfactory co-receptor orco: expression profile and confirmation of atypical membrane topology. Archives of Insect Biochemistry and Physiology. 81(4):179-198.

Asiimwe, P., S.E. Naranjo & P.C. Ellsworth. 2013. Relative influence of plant quality and natural enemies on the seasonal dynamics of bemisia tabaci (Hemiptera: Aleyrodidae) in cotton. Journal of Economic Entomology. 106:1260-1273.

Cooper, W.R., Spurgeon, D.W. 2013. Temperature-dependent egg development of Lygus hesperus (Hemiptera: Miridae). Journal of Economic Entomology. 106(1):124-130.

Tian, J.C., Wang, X.P., Long, L.P., Romeis, J., Naranjo, S.E., Hellmich II, R.L., Wang, P., Earle, E.D., Shelton, A.M. 2013. Bt crops producing Cry1Ac, Cry2Ab and Cry1F do not harm the green lacewing, chrysoperla rufilabris. PLoS One. 8(3):e60125.

Castle, S.J., Prabhaker, N. 2013. Monitoring changes in bemisia tabaci susceptibility to neonicotinoid insecticides in Arizona and California. Journal of Economic Entomology. 106(3):1404-1413.

Tian, J., Collins, H.L., Romeis, J., Naranjo, S.E., Hellmich II, R.L., Shelton, A.M. 2012. Using field-evolved resistance to Cry1F maize in a lepidopteran pest to demonstrate no adverse effects of Cry1F on one of its major predators. Transgenic Research. 21(6):1303-1310.

Dai, H., Hiromasa, Y., Takahashi, D., Vandervelde, D., Fabrick, J.A., Kanost, M.R., Krishnamoorthi, R. (2013). beta-1,3-Glucan recognition by an insect pathogen recognition domain causes self-association of protein: carbohydrate complex. Biochemistry, 52(1):161-170.

Hagler, J.R., Blackmer, F. 2013. Identifying inter-and intraguild predator feeding activity of an anthropod predator assemblage. Ecological Entomology. 38:258-271.

Krugner, R., Hagler, J.R., Groves, R.L., Sisterson, M.S., Morse, J.G., Johnson, M.W. 2012. Plant water stress effects on the net dispersal rate of the insect vector Homalodisca vitripennis (Germar) (Hemiptera: Cicadellidae) and movement of its egg parasitoid, Gonatocerus ashmeadi Girault (Hymenoptera: Mymaridae). Environmental Entomology. 41(6):1279-1289.

Shelton, A., Naranjo, S.E., Romeis, J., Hellmich II, R.L. 2012. Errors in logic and statistics plague a meta-analysis. Environmental Entomology. 41:1047-1049.

Hagler, J.R., Blackmer, F., Krugner, R., Groves, R.L., Morse, J.G., Johnson, M.W. 2013. Gut content examination of the citrus predator assemblage for the presence of Homalodisca vitripennis remains. Biocontrol. 58:341-349.

Kelly, J.L., Hagler, J.R., Kaplan, I. 2012. Employing immunomarkers to track dispersal and trophic relationships of piercing-sucking predator, Podisus maculiventris (Hemiptera: Pentatomidae). Environmental Entomology. 41(6):1527-1533.

Swezey, S.L., Nieto, D.J., Hagler, J.R., Pickett, C.H., Bryer, J.A., Machtley, S.A. 2013. Dispersion, distribution and movement of Lygus spp.(Hemiptera:Miridae)in trap-cropped organic strawberries. Environmental Entomology. 42(4):770-778.

Spurgeon, D.W., Cooper, W.R. 2013. Sweepnet captures of Lygus hesperus (Hemiptera:Miridae) adult genders and age-classes in cotton. Journal of Entomological Science. 48(3):195-205.

Brent, C.S., Klok, C.J., Naranjo, S.E. 2013. Effect of diapause status and gender on activity, metabolism and starvation resistance in the plant bug Lygus hesperus Knight. Entomologia Experimentalis et Applicata. 148(2):152-160.

Cooper, W.R., Spurgeon, D.W. 2013. Response by Lygus hesperus (Hemiptera: Miridae) adults to salivary preconditioning of cotton squares. Journal of Entomological Science. 48(3):261-264.

Last Modified: 05/27/2017
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