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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

2012 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.

3. Progress Report:
Studies of Lygus flight after feeding on cotton, alfalfa, guayule, camelina, and lesquerella were initiated. Understanding host effects on flight may provide insights into Lygus movement among crops. A compound transferred by male lygus during mating that makes females unattractive to other males was shown to change chemically over time, restoring female attractiveness. Five odorant binding proteins were identified from Lygus antennae, and additional components involved in communication are sought. Understanding chemical communications may facilitate mating disruption or other control methods. Lygus overwinter in a state of reduced metabolism (diapause). Studies of the hormonal control of diapause continued. Survival studies showed that diapausing Lygus tolerated environmental stresses better than reproductive Lygus. About 36,000 DNA sequences from Lygus were generated and a subset may be involved in mediation of thermal stress. These results contribute to efforts to develop ecologically-based management strategies for Lygus. Efforts to optimize inexpensive protein markers (egg white, milk protein, soy protein) for studying insect dispersal revealed marker concentrations for effective marking of insects, and indicated a small incidence of inter-insect marker transfer. These results reduce cost and improve effectiveness of mark-recapture studies. Progress was made in developing biological control based thresholds for sweetpotato whitefly in cotton using selective and non-selective insecticides to manipulate pest and natural enemy populations. Whitefly populations were larger in cotton infected with cotton leaf crumple virus than in uninfected cotton, indicating virus infection benefits the whitefly. Studies were initiated to examine effects of prior experience and host plant on parasite effectiveness against the whitefly. Assays showed that whitefly resistance to a commonly used material (imidacloprid) was higher than to three other neonicotinoid insecticides. Studies of effects of plant defensive compounds on whiteflies were started. Field studies showed that Lygus, big-eyed bugs, and collops beetles fed on whitefly, but Lygus and big-eyed bugs also fed on each other. Function of a water channel protein in the whitefly gut, BtAQP1, was confirmed. Treatments to interfere with this protein have yet to affect whitefly fitness. Better methodology, or identification of additional channel proteins, is needed to advance this approach to whitefly control. Collectively, these results shed light on factors controlling whitefly populations, which is essential to improved management. Studies of pink bollworm resistance to Bt cotton revealed a new resistance gene resulting from a mutation. It is the fourth cadherin gene linked to resistance, suggesting the cadherin gene is a primary source of Bt resistance. Examination of field-collected Bt resistant pink bollworm indicated the resistance was from a cadherin gene modified by a mobile DNA element (jumping gene). Models of invasive species detection were developed based on pink bollworm. Progress in understanding Bt resistance and monitoring pink bollworm resistance is critical to eradication efforts.

4. Accomplishments
1. Optimized protein marking for arthropod dispersal research. The protein marking procedure is a powerful method for marking insects for ecological studies. However, first-generation protein marks consist of vertebrate IgG proteins, the expense of which has limited their use. In studies of alternative marking materials including egg white (albumin), milk protein (casein), and soy protein (trypsin), an ARS scientist from the Arid-Land Agricultural Research Center, Maricopa, AZ, identified substitutes more economical than, and in some cases superior to, the IgG proteins. Insect retention of the markers was compared to rabbit IgG, and application rates necessary to mark >90% of the resident arthropod population were determined. Application of these alternative markers to ecological questions facilitates large-scale studies that were previously prohibitively expensive, and increases the availability of this marking methodology to a wider range of potential users.

2. Bt resistance genes in pink bollworm. Transgenic Bt cotton, cotton that makes insecticidal proteins from the bacterium Bacillus thuringiensis, is an essential tool of the Pink Bollworm Eradication Program. Genes conferring resistance to Bt cotton are known to occur in the pink bollworm, and although control failures have not been observed in the U.S., field populations of Bt-resistant pink bollworm have appeared in other countries. An ARS scientist from the Arid-Land Agricultural Research Center, Maricopa, AZ, and collaborators at the University of Arizona, showed that resistance to Bt cotton is genetically linked with changes in the pink bollworm cadherin gene, and that one such cadherin mutation involved an insertion of a mobile DNA element or “jumping gene.” In addition, the ARS scientist identified a new resistance gene from the pink bollworm, bringing the total to four known cadherin mutations genetically linked to Bt resistance. These results implicate changes to the cadherin gene as the predominant mechanism of pink bollworm resistance to Bt cotton, and accentuate the importance of cadherin-based resistance monitoring to preservation of this critically important control technology.

3. An integrated approach to insecticide resistance monitoring. Pest resistance to insecticides remains a major concern to agricultural producers worldwide. Insecticide resistance monitoring programs generally rely on laboratory bioassays to detect changes in susceptibility of target pest populations, but results of these assays are often poor indicators of insecticide field performance. ARS scientists from the Arid-Land Agricultural Research Center, Maricopa, AZ, conducted parallel laboratory and field-based bioassays on adults of the sweetpotato whitefly, Bemisia tabaci, and compared the results to control levels achieved in cantaloupes treated with the insecticide imidacloprid. Whitefly mortality was much higher in the laboratory systemic uptake bioassay compared with the field-based bioassay, whereas control obtained in the cantaloupes was excellent because the insecticide prevented establishment of immature whiteflies in the crop. These results underscore the importance of utilizing a combination of bioassay and field efficacy approaches in support of regulatory and control program decisions regarding insecticide performance.

4. Transgenic crop has no effect on important insect predator. Transgenic crops producing the target-specific insecticidal proteins of Bacillus thuringiensis (Bt) have been widely adopted and cultivated on millions of hectares globally. However, there remain concerns about the ecological risk associated with these crops, specifically to non-target organisms. ARS scientists from the Arid-Land Agricultural Research Center, Maricopa, AZ, and researchers at Cornell University, ARS in Ames, IA, and Agroscope in Zurich, Switzerland showed that the biology of a common predatory lady beetle was not affected by ingestion of Bt-resistant prey fed on Bt-maize over two generations. Use of Bt-resistant prey 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. Comparative impacts of plant quality and natural enemies on pest dynamics in cotton. The sweetpotato whitefly, Bemisia tabaci, and the western tarnished plant bug, Lygus hesperus, are key pests of cotton and other crops in the western U.S. ARS scientists from the Arid-Land Agricultural Research Center, Maricopa, AZ, and collaborators from the University of Arizona demonstrated differential influences of plant quality (manipulated by varying water supplied by irrigation) and natural enemies on these two pest species. Crop water stress reduced Lygus bug populations, compared with unstressed cotton, regardless of insecticide treatments. In contrast, whitefly populations were more influenced by insecticide-induced disruption of generalist predators than by variations in plant quality. For both pests, preservation of natural enemies through use of selective insecticides provided better pest control and enhanced yields compared with broad-spectrum insecticides. These results provide producers information that is essential to conservation of natural enemies, and to improve the efficiency of pest and crop management efforts.

6. A molecular approach to studying arthropod predation. Understanding predator-prey interactions of the arthropod predator community in any given ecosystem is essential for pinpointing the ecosystem services provided by natural enemies. An ARS scientist from the Arid-Land Agricultural Research Center, Maricopa, AZ, developed, optimized, and utilized a suite of prey-specific DNA-based assays to analyze the gut contents of the cotton predator community. The targeted insects included an herbivore pest (sweetpotato whitefly), a strict predator (collops beetle), an omnivorous pest (lygus bug), and an omnivorous predator (big-eyed bug). Gut analyses showed that the strict predator and both omnivores fed substantially on whiteflies. However, the two omnivores also fed on each other, but rarely fed on the collops beetle. The gut assays further revealed that the targeted pests (whitefly and lygus) were more frequently eaten by insect predators than by spiders, whereas the two beneficial species (big-eyed bug and collops beetle) were fed upon by both insect and spider predators. This study serves as a model to demonstrate the utility of DNA-based methods in elucidating complex food web interactions.

Review Publications
Xianchun, L., Degain, B.A., Harpold, V.S., Marcon, P.G., Nichols, R.L., Fournier, A.J., Naranjo, S.E., Palumbo, J.C., Ellsworth, P.C. 2012. Baseline Susceptibilities of B- and Q-biotype Bemisia tabaci to anthranilic diamides. Pest Management Science. 68:83-91.

Fabrick, J.A., Mathew, L.G., Tabashnik, B.E., Li, X. (2011). Insertion of an intact CR1 retrotranspon in a cadherin gene linked with BT resistance in the pink bollworm, Pectinophora gossypiella. Insect Molecular Biology. 20(5):651-665

Rosengaus, R.B., James, L., Hartke, T.R., Brent, C.S. 2011. Mate preference and disease risk in Zootermopsis angusticollis (Isoptera:Termopsidae. Environmental Entomology. 40(6):1554-1565.

Naranjo, S.E., Ellsworth, P.C., Dierig, D.A. 2011. Impact of Lygus spp. (Hemiptera: Miridae) on damage, yield and quality of lesquerella (Physaria fendleri), a potential new oil-seed crop. Journal of Economic Entomology. 104: 1575-1583.

Dolezal, A.G., Brent, C.S., Holldobler, B., Amdam, G. 2012. Worker division of labor and endocrine physiology are associated in the harvester ant, Pogonomyrmex californicus. Journal of Experimental Biology Online. 215:454-460.

Irvin, N.A., Hagler, J.R., Hoddle, M.S. 2012. Laboratory investigation of triple marking the parasitoid Gonatocerus ashmeadi (Hymenoptera: Mymaridae) with a fluorescent dye and two animal proteins. Entomologia Experimentalis et Applicata. 143:1-12.

Gao, Y., Jurat-Fuentes, J., Oppert, B.S., Fabrick, J.A., Lui, C.A., Gao, J., Lei, Z. 2011. Increased toxicity of Bacillus thuringiensis Cry3Aa against Crioceris quatuordecimpunctata, Phaedon brassicae and Colaphellus bowringi by a Tenebrio molitor cadherin fragment. Pest Management Science. 67(9): 1076-1081.

Brent, C.S., Byers, J.A. (2011). Female attractiveness modulated by a male-derived antiaphrodisiac pheromone in a plant bug. Animal Behaviour, 82:937-943.

Carriere, Y., Goddell, P., Ellers-Kirk, C., Dutilleul, P., Naranjo, S.E., Ellsworth, P.E. 2012. Effects of local and landscape factors on population dynamics of a cotton pest. PLoS One. 7(6):e39862.doi:10.1371/journal.pone.0039862.

Booth, W., Brent, C.S., Calleri, D.V., Rosengaus, R.B., Traniello, J.F., Vargo, E.L. 2011. Population genetic structure and colony breeding system in dampwood termites (Zootermopsis angusticollis and Z. nevadensis nuttingi). Insectes Sociaux. 59:127-137.

Naranjo, S.E., Stefanek, M.A. 2012. Feeding Behavior of a Potential Insect Pest, Lygus hesperus, on Four New Industrial Crops for the Arid Southwestern USA.. Industrial Crops and Products. 37:358-361.

Hagler, J.R. 2011. An immunological approach to quantify consumption of protein-tagged Lygus hesperus by the entire cotton predator assemblage. Biological Control. 58 (2011) 337–345.

Lu, R.C., Wang, H.B., Zhang, Z., Byers, J.A., Jin, Y.J., Wen, H.F. 2012. Coexistence and competition between Tomicus Yunnanensis and T. minor (Coleoptera: Scolytidae) in yunnan pine. Psyche. vol.2012,pp.1-6.

Fabrick, J.A., Tabashnik, B.E. 2012. Similar genetic basis of resistance to bt toxin cry1ac in boll-selected and diet-selected strains of pink bollworm. PLoS One. 7(4):e35658

Hagler, J.R., Mueller, S., Teuber, L.R., Van Deynze, A., Martin, J. (2011). A method for distinctly marking honey bees, Apis mellifera originating from multiple apiary locations. Journal of Insect Science. 11:146

Hagler, J.R., Mueller, S., Teuber, L.R., Machtley, S.A., Deynze, A.V. 2011. Foraging range of honey bees, Apis mellifera, in alfalfa seed production fields. Journal of Insect Science. 11:144.

Byers, J.A. 2011. Analysis of vertical distributions and effective flight layers of insects: three-dimensional simulation of flying insects and catch at trap heights. Environmental Entomology. 40(5):1210-1222.

Castle, S.J., Palumbo, J.C. 2011. Cantaloupe Insects: Ecology and Control. Encyclopedia of Pest Management. 10.1081/E-EPM.

Helms Cahan, S., Graves, C.J., Brent, C.S. 2011. Intergenerational effect of juvenile hormone on offspring in Pogonomyrmex harvester ants. Journal of Comparative Physiology. 181(8):991.

Hoffmann, E.J., Castle, S.J. 2012. Imidacloprid in Melon Guttation Fluid: A Mode of Exposure for Pest and Beneficial Organisms. Journal of Economic Entomology. 105(1):67-71.

Penick, C.A., Liebig, J., Brent, C.S. 2011. Reproduction, dominance, and caste: endocrine profiles of queens and workers of the ant Harpegnathos saltator. Journal of Comparative Physiology. 197(11):1063-1071.

Carrière, Y., C.Ellers-Kirk, K. Hartfield, G. Larocque, B. Degain, P. Dutilleul, T. J. Dennehy, S. E. March, D. W. Crowder, X. Li, P. C. Ellsworth, S. E. Naranjo, J. C. Palumbo, A. Fournier, L. Antilla & B. E. Tabashnik. 2012. Large-scale, spatially explicit test of the refuge strategy for delaying insecticide resistance. Proc. Nat. Acad. Sci. (USA)109:775-780.

Lee, J.M., Hull, J.J., Kawai, T., Goto, C., Kurihara, M., Tanokura, M., Nagata, K., Nagasawa, H., Matsumoto, S. 2012. Re-evaluation of the PBAN receptor molecule: characterization of PBANR variants expressed in the pheromone glands of moths. Frontiers in Endocrinology. 3(6):1-12.

Oppert, B.S., Dowd, S.E., Bouffard, P., Li, L., Conesa, A., Lorenzen, M.D., Toutges, M., Marshall, J., Huestis, D., Fabrick, J.A., Oppert, C., Jurat-Fuentes, J. 2012. Transcriptome profiling of the intoxication response of Tenebrio molitor larvae to Bacillus thuringiensis Cry3Aa protoxin. PLoS One. 7(4): e34624. 12pp. Available:

Byers, J.A. 2012. Estimating insect flight densities from attractive trap catches and flight height distributions. Journal of Chemical Ecology 38:592-601.

Lu, R.C., Wang, H.B., Zhang, Z., Byers, J.A., Jin, Y.J., Wen, H.F., Shi, W.J. 2012. Attraction of tomicus yunnanensis (coleoptera: scolytidae) to yunnan pine logs with and without periderm or phloem: an effective monitoring bait. Psyche Vol. 2012, ID 794683, pp.1-5.

Byers, J.A. 2012. A population genetic model of evolution of host-mate attraction and nonhost repulsion in a bark beetle Pityogenes bidentatus. Psyche. 2012:1-9.

Byers, J.A. 2012. Bark beetles, pityogenes bidentatus, orienting to aggregation pheromone avoid conifer monoterpene odors when flying but not when walking. Psyche Vol. 2012, ID 940962, pp.1-10.

Lee, J.M., Hull, J.J., Kawai, T., Tsuneizumi, K., Kurihara, M., Tanokura, M., Nagata, K., Nagasawa, H., Matsumoto, S. 2012. Establishment of Sf9 transformants constitutively expressing PBAN receptor variants: application to functional evaluation. Frontiers in Endocrinology. 3(56):1-8.

Byers, J.A., Birgersson, G. 2012. Host-tree monoterpenes and biosynthesis of aggregation pheromones in the bark beetle ips paraconfusus. Psyche Vol. 2012, ID 539624, pp. 1-10.

Williams III, L.H., Hagler, J.R., Tonkel, K.C. 2011. Retention of immunolabels by Diorhabda carinulata (Coleoptera: Chrysomelidae), a biological control agent of saltcedar. Entomologia Experimentalis et Applicata. 141:154-162.

Slosky, L.M., Hoffmann, E.J., Hagler, J.R. 2012. A comparative study of the retention and lethality of the first and second generation arthropod protein markers. Entomologia Experimentalis et Applicata. 144(2):165-171.

Florence, T., Yun-Gen, M., Bong-Hee, S., Young-Soo, K., Hull, J.J., Fraser, M.J., Lewis, R.V., Jarvis, D.L. 2012. Silkworms transformed with chimeric silkworm/spider silk genes spin composite silk fibers with improved mechanical properties. Proceedings of the National Academy of Sciences. 109(3):923-928.

Wang, Y., Brent, C.S., Fennern, E., Amdam, G.V. 2012. Gustatory perception and fat body energy metabolism are jointly affected by vitellogenin and juvenile hormone in honey bees. PLoS Genetics. 8(6):e1002779.

hRodriguez-Saona, C.R., Byers, J.A., Schiffhauer, D. 2012. Effect of trap color and height on captures of blunt-nosed and sharp-nosed leafhoppers (Hemiptera: cicadellidae) and non-target arthropods in cranberry bogs. Crop Protection 40:132-144.

Last Modified: 2/23/2016
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