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ABSTRACT OTEN, KELLY LYNN FELDERHOFF. Host-Plant Selection by the Hemlock Woolly Adelgid, Adelges tsugae Annand: Sensory Systems and Feeding Behavior in Relation to Physical and Chemical Host-Plant Characteristics. (Under the direction of Dr. Fred P. Hain). The hemlock woolly adelgid (HWA), Adelges tsugae Annand (Hemiptera: Adelgidae), is an invasive insect causing extensive mortality to hemlocks in the eastern United States. It has become increasingly important to understand the insect-plant interactions of this system for management and eventual hemlock restoration. Insect-plant interactions were observed using light, scanning and transmission electron microscopy. HWA may exploit alternative stylet insertion sites during high infestation (typical insertion site is between the pulvinus and the stem, below the abscission layer). Five dentitions occur at the tip of the mandibular stylets. Stylet bundle cross-section reveal separate salivary (0.24 - 0.54 µm in diameter, n=11) and food canals (0.48 - 1.0 µm in diameter, n=11), typical of Hemiptera, and single stylet innervation. Sensilla of the labium appear mechanosensory and an antennal sensorium is present, indicating that morphology and chemical host characteristics may play roles in host-plant acceptance. Tarsal setae are likely used in adhesion to surfaces. Feeding biology was further investigated in an enzymatic survey. We detected the presence of trypsin-like protease, amylase, peroxidase, and polyphenol oxidase. HWA had four times lower protease activity (0.259 BAEE U µg protein-1 min-1) and eight times lower amylase-like activity (0.1088 mU protein-1 min-1) than L. lineolaris, the positive control. The presence of protease and amylase suggests that, if injected into the plant, it could be used for digestion of insoluble plant proteins and starches. HWA had twice as much peroxidase (0.2323 mU µg protein-1 min-1) and three times as much polyphenol oxidase activity (0.0569 abs µg protein-1 min-1) compared to L. lineolaris, signifying the possibility of plant defense detoxification. Hemlocks were scrutinized for differences in morphology and chemical composition of the epicuticle. Comparisons were made between species using low temperature-scanning electron microscopy and related to known HWA resistance. Trichomes likely do not relate to host-plant acceptance by HWA, as species that lack and are covered with trichomes are both colonized. Cuticle thickness is significantly thinner at the stylet insertion point than at other locations of the pulvinus. A thinner cuticle may facilitate tissue penetration, potentially the reason for specificity in insertion site. In addition, cuticle thickness at this point is significantly different between species, with the hybrid, Carolina, southern Japanese, and northern Japanese hemlocks possessing the thickest cuticles; therefore, cuticle thickness may confer some resistance to HWA. Wax structures were generally smoother in eastern and Carolina hemlocks, hypothesized to facilitate sheath adhesion to the plant surface. Because there are many factors that contribute to wax morphology, this research should be pursued further. Extractable lipids of the hemlock surface were analyzed with gas chromatography- mass spectrometry. Results indicate inter- and intraspecific variation. In addition, an unidentified compound appears in the resistant species. This compound should be further scrutinized, both in its identification and its association to HWA behavior. Interspecific variation in resistance among eastern, Carolina, and western hemlock was assessed in the field. Two of five blocks were artificially infested, two blocks were untreated, and one block was chemically treated. A binary assessment of HWA infestation revealed that eastern hemlock was 36 times more likely and Carolina hemlock was half as likely to become infested as western hemlock. Infestation rates declined significantly in subsequent years as a result of winter temperatures. Cutting success was also studied at the species level and propagation methods are suggested for hardwood rooted cuttings for all species except western hemlock. Rooted cuttings offer a viable option for clonal propagation, which will be useful in breeding programs for resistance screening. In addition, the establishment of a common-garden is discussed and will be useful for ongoing and future research in the field. Host-Plant Selection by the Hemlock Woolly Adelgid, Adelges tsugae Annand: Sensory Systems and Feeding Behavior in Relation to Physical and Chemical Host-Plant Characteristics by Kelly Lynn Felderhoff Oten A dissertation submitted to the Graduate Faculty of North Carolina State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Entomology Raleigh, North Carolina 2011 APPROVED BY: _______________________________ ______________________________ Fred P. Hain John Frampton Committee Chair Minor Representative ________________________________ ________________________________ Allen C. Cohen John S. King ________________________________ ________________________________ John F. Monahan Robert M. Jetton DEDICATION I would like to dedicate this dissertation to my niece and nephew, Evelyn Grace and Corbin Ray. May you grow up with love and respect for the natural world around you and appreciate the majestic forests of the world in which we live. ii BIOGRAPHY Kelly Lynn Felderhoff was born in Texas on April 16, 1983. Second of four children, she was raised in College Station, TX by her parents, Chris and Sandy Felderhoff. Throughout her childhood, it was apparent that she had a fascination with insects. She was involved in 4-H, with entomology as her main project and may have been the only fourth- grader to bring an insect collection for show-and-tell. While in high school, Kelly worked in the Texas A&M University Insect Collection. She graduated from A&M Consolidated High School in 2001, knowing she wanted to pursue Entomology as a career. In August 2001, Kelly enrolled at Texas A&M University to study entomology. While pursuing her degree, she worked on undergraduate research projects in the field of forensic entomology with Dr. Jimmy Olson. Her project results revealed the importance of using proper preservation techniques in forensic collections in order to calculate an accurate post-mortem interval; her data were used as preliminary results for a research proposal. She also participated in the Texas Integrated Pest Management Internship Program, and experienced the agricultural side of entomology. In addition, she evaluated the effectiveness of the program since its inception, resulting in her first publication. Kelly graduated with her B.S. in Entomology in August 2005. The day following graduation, Kelly moved to Knoxville, TN to pursue her M.S. degree in entomology at the University of Tennessee. Under the direction of Dr. Ernest Bernard, her thesis included a revision of the family Tomoceridae (Collembola) in Great Smoky Mountains National Park. Using morphological and molecular techniques, she iii described two new species, resurrected one species, and identified two species complexes. She graduated in December 2007. In January 2008, Kelly began her doctoral program in entomology with a minor in forestry at North Carolina State University. Under the direction of Dr. Fred P. Hain, she studied the feeding biology of the hemlock woolly adelgid and investigated mechanisms of host-plant resistance between hemlock species; this dissertation presents her findings. While a student, she participated in the Preparing the Professoriate Program, which gave her the opportunity to teach her own course. This experience convinced her that teaching in some context must be a part of her career. In the spring semester following graduation, she will teach the undergraduate forest entomology course at NCSU. iv ACKNOWLEDGMENTS Throughout this journey towards my doctoral degree, I am conscious that my accomplishments could not have been possible without the support of many people. First, I would like to thank Fred Hain for having faith in my ability to successfully complete this program. He played an integral role in my professional development and encouraged me to take on things that I may not have otherwise. Under his guidance, I grew as an individual personally and professionally, and I view him as a friend and a significant influence as a young scientist. I hope to implement many of his qualities when I become a mentor myself someday. I am grateful to John Frampton as well, who challenged me and supported me throughout my project. Thanks go to my committee members for their guidance and encouragement: John King, Robert Jetton, John Monahan, and Allen Cohen. I especially want to thank Allen Cohen, for his friendship, his unwavering interest in my research, and for always making the time to meet with me. His insight was invaluable and his patience endless. Allen’s wife, Jackie, was also extremely supportive and always a friendly face. I also want to thank the Cohens for my wonderful lab mate, Spotty, who kept me company during long hours of dissertation writing. I express gratitude to sources of funding for my project, the USDA Forest Service, Northern Research Station and Forest Health Protection in Region 8. In addition, support from the NCSU Department of Entomology made this project possible. I thank the department for taking me on. I am very grateful for the time, enthusiasm, and ideas from John Strider. He was always willing to help me with my research, whether it include
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