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Stylet Bundle Morphology and Trophically Related Enzymes of the Hemlock Woolly Adelgid (Hemiptera: Adelgidae)

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Stylet Bundle Morphology and Trophically Related Enzymes of the Hemlock Woolly Adelgid (Hemiptera: Adelgidae) MORPHOLOGY,HISTOLOGY, AND FINE STRUCTURE Stylet Bundle Morphology and Trophically Related Enzymes of the Hemlock Woolly Adelgid (Hemiptera: Adelgidae) 1 KELLY L. F. OTEN, ALLEN C. COHEN, AND FRED P. HAIN North Carolina State University, Department of Entomology, Campus Box 7613, Raleigh, NC 27695 Ann. Entomol. Soc. Am. 107(3): 680Ð690 (2014); DOI: http://dx.doi.org/10.1603/AN13168 ABSTRACT The hemlock woolly adelgid, Adelges tsugae Annand (Hemiptera: Adelgidae), is a pest of eastern and Carolina hemlocks (Tsuga canadensis (L.) Carrie`re and Tsuga caroliniana Engelmann, respectively) in the eastern United States and has already caused catastrophic changes to eastern forests. As one of the signiÞcant exotic forest pests, it is imperative that the basic biology of hemlock woolly adelgid be understood for use in novel and improved management techniques. Scanning and transmission electron microscopy and enzyme assays were used to elucidate the feeding biology of hemlock woolly adelgid and are discussed in the context of the pestÐplant interactions and the implications for host plant resistance. Morphological characters indicate that hemlock woolly adelgids may use labial sensilla and neural canals within the mandibular stylets to guide their stylets through close-range host acceptance processes. Stylet bundle insertion is likely assisted by external sheath material that secures the stylet bundle to the plant surface and mandibular dentitions that may assist entry into or within plant tissues. In addition, results support the theory that extra-oral digestion is likely used by hemlock woolly adelgid, suggested by both a narrow food canal and the presence of four trophically related enzymes (a trypsin-like enzyme, an amylase-like enzyme, peroxidase, and polyphenol oxidase). The presence of these enzymes also has implications for causing a systemic response in host trees. KEY WORDS Adelges tsugae, digestive enzyme, electron microscopy, feeding biology, hemlock The hemlock woolly adelgid (Adelges tsugae Annand) eralization occurs despite major biological differences (Hemiptera: Adelgidae) is an exotic invasive sucking (e.g., hemlock woolly adelgid are sessile, whereas insect causing extensive mortality to populations of aphids are motile; hemlock woolly adelgid feeds on eastern and Carolina hemlocks (Tsuga canadensis (L.) xylem ray parenchyma cells, whereas aphids feed on Carrie`re and Tsuga caroliniana Engelmann, respec- phloem sap). tively) in the eastern United States. After infestation, The feeding biology of hemlock woolly adelgid was hemlocks decline in health, exhibited by needle drop, originally investigated by Young et al. (1995), and this bud abortion, a lack of new growth, and a drought-like study constitutes most of what is known about hem- physiological reaction that has been likened with a lock woolly adelgid feeding. They described the stylet hypersensitive response (Walker-Lane 2009, Radville bundle insertion point and extensive stylet bundle et al. 2011). Tree death typically follows in 4Ð10 yr, length, a trait also found in the closely related balsam and in most infested stands, 80Ð90% mortality occurs woolly adelgid (Adelges piceae (Ratzeburg); Forbes (Hale 2004, Townsend and Rieske-Kinney 2006). and Mullick 1970). A long stylet bundle is likely as- The status of hemlock woolly adelgid as a signiÞcant sociated with a need to reach its feeding site and to pest of forest and ornamental hemlocks has provoked secure itself to the host plant. Although lacking evi- extensive research focused primarily on management. dence with a cross-section image, Young et al. (1995) Despite being a focus of research for Ͼ20 yr, the basic deduced that the stylet bundle morphology of hem- biology of hemlock woolly adelgid remains poorly lock woolly adelgid is similar to that of aphids and understood. Adelgids belong to the superfamily Aphi- balsam woolly adelgid (Parrish 1967). doidea (along with Aphididae and Phylloxeridae) and As members of Aphidoidea, hemlock woolly adelgid are commonly regarded as “aphid-like” (e.g., Pirone host plant penetration and salivary secretions are 1978, MacKenzie 2002, Speight 2007); because of this thought to be similar to that of aphids. Aphids pierce association, much of the basic biological understand- the plant cuticle with an alternating sawing motion of ing of hemlock woolly adelgid is based on the more four stylets and produce two types of saliva: watery comprehensive knowledge of aphid biology. This gen- saliva and salivary sheath material (Miles 1959, 1968, 1972; Pollard 1973). The watery saliva may contain 1 Corresponding author, e-mail: [email protected]. digestive enzymes that may help establish and main- 0013-8746/14/0680Ð0690$04.00/0 ᭧ 2014 Entomological Society of America May 2014 OTEN ET AL.: STYLETS AND TROPHIC ENZYMES OF Adelges tsugae 681 tain feeding sites, suppress plant defenses, and induce four sides and top. Samples were examined with a changes in plant physiology (Cohen and Hendrix JEOL JSM-5900LV scanning electron microscope 1994, Miles 1999, Will et al. 2007, Mutti et al. 2008). The (JEOL, Tokyo, Japan) at an accelerating voltage of 15 salivary sheath material is produced as a bead at the tip or 20 kV. Measurements were taken with a planimeter of the stylets that hardens upon extrusion, enclosing on printed images. Images were modiÞed for bright- the stylets and acting to stabilize the labium during ness and contrast by adjusting levels, sized, and placed insertion, as a fulcrum for stylet maneuvering, to pro- together to produce Þgures using Adobe Photoshop tect against host plant defenses, and enable stylet 8.0 (Adobe Systems, San Jose, CA). bundle reinsertion following a molt (Miles 1968, 1972, Transmission Electron Microscopy (TEM). Infested 1999; Cohen 1990). eastern hemlock material was sent via overnight mail Understanding digestive enzymes used by hemlock to Charles A. Murphy (U.S. Department of Agricul- woolly adelgid is critical to further the body of knowl- tureÐAgricultural Research Service [USDAÐARS], edge regarding insectÐplant interactions. It has been Beltsville Agricultural Research Center, Beltsville, suggested that the injection of “toxic” saliva by hem- MD), who performed and imaged the TEM portion of lock woolly adelgid induces the systemic response in this study. Tissue was Þxed overnight at room tem- hemlocks (McClure 1995, Young et al. 1995, Shields et perature by immersion in a Þxative comprising 3% al. 1996), but there are no data to support that concept. glutaraldehyde and 2% paraformaldehyde in 0.05 M Young et al. (1995) documented both saliva types in NaCacodylate buffer, pH 7.0. They were washed in a hemlock woolly adelgid using staining methods, but 0.1 M NaCacodylate buffer rinse, six times over 1 h, did not evaluate them for the presence of enzymes. postÞxed in NaCacodylate buffered 2% osmium te- They also suggest that pectinase, an enzyme signiÞ- troxide for2hatroom temperature, dehydrated in an cant in plant penetration, is present in the saliva of acetone series and slowly inÞltrated with Spurrs low- hemlock woolly adelgid, supported only by the pre- viscosity embedding resin. Then, 90-nm gold sections dominantly intercellular stylet pathway within plant of the tissue were cut on a Reichert/AO Ultracut tissue and the indication of protein in the saliva via microtome with a Diatome diamond knife and staining. Later, Kaur (2009) detected a weak presence mounted onto 200-mesh Ni grids (Leica, DeerÞeld, of amylase in hemlock woolly adelgid homogenate but IL). They were stained with 4% uranyl acetate and 3% was unable to draw conclusions on the discovery. lead citrate, and then viewed in a HT-7700 Hitachi The purpose of this research is to augment the microscope (Hitachi Corp., Tokyo, Japan) at 80 kV. current corpus of basic biological knowledge regard- Images were modiÞed for brightness and contrast by ing feeding biology and host plant interactions of hem- adjusting levels, sized, and placed together to produce lock woolly adelgid. SpeciÞcally, the objectives were Þgures using Adobe Photoshop 8.0. to 1) expand our understanding of hemlock woolly Trophically Related Enzymes of Hemlock Woolly adelgid feeding behaviors using electron microscopy, Adelgid. Material Collection for Enzyme Work. Ac- 2) establish and corroborate stylet bundle cross-sec- tively feeding second- and third-instar hemlock tion morphology suggested by Young et al. (1995), and woolly adelgid nymphs used in these enzyme surveys 3) identify trophically related enzymes used by hem- were collected from live eastern hemlock material lock woolly adelgid. An improved understanding of obtained from Laurel Springs, NC, in January 2011. the interaction between hemlock woolly adelgid and The ovisac was teased off with a paintbrush and 10 its hemlock host will lead to a better comprehension individuals were stored per vial at Ϫ80ЊC. Similarly, of the host response, ultimately improving the work neonate Lygus lineolaris (Palisot de Beauvois) toward improved pest management techniques such (Hemiptera: Miridae) were stored 10 individuals per as host plant resistance and induction of resistance by vial at Ϫ80ЊC for use as positive controls in these systemic chemicals. assays. L. lineolaris is a major agricultural pest that feeds on at least 130 economically important plants, including Materials and Methods cotton, cereals, fruits, vegetables, and alfalfa Feeding Behaviors and Stylet Bundle Cross-Section (Snodgrass et al. 1984, Young 1986, Butts and Lamb Morphology. Material Collection.
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