Lethal and Sublethal Effects of Imidacloprid on Hemlock Woolly Adelgid (Hemiptera: Adelgidae) and Two Introduced Predator Species
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FOREST ENTOMOLOGY Lethal and Sublethal Effects of Imidacloprid on Hemlock Woolly Adelgid (Hemiptera: Adelgidae) and Two Introduced Predator Species 1,2 1 1 3 BRIAN M. EISENBACK, SCOTT M. SALOM, LOKE T. KOK, AND ANTHONY F. LAGALANTE J. Econ. Entomol. 103(4): 1222Ð1234 (2010); DOI: 10.1603/EC09270 ABSTRACT Eastern hemlock, Tsuga canadensis (L.) Carrie`re, branchlets were systemically treated with imidacloprid and bioassayed with hemlock woolly adelgid, Adelges tsugae (Annand) (Hemiptera: Adelgidae), and predators. After 10 d, two hemlock woolly adelgid predators, Laricobius nigrinus Fender (Coleoptera: Derodontidae) and Sasajiscymnus tsugae Sasaji & McClure (Coleoptera: Coc- cinellidae), were allowed to feed on remaining hemlock woolly adelgid for 20 d on branches systemically treated with 1, 10, or 100 ppm imidacloprid. Every 5 d, mortality, mobility (measured as ßip time), number of hemlock woolly adelgid consumed, and degree of intoxication of each individual beetle were recorded. Liquid chromatography-mass spectrometry was used to quantify imidacloprid and some of its major metabolites in hemlock wood tissues and in the predator beetles postmortem. Probit analysis of hemlock woolly adelgid mortality and imidacloprid concentrations recovered from branch wood tissues determined the 30 d LC50 to be 242 ppb. A topical application of imidacloprid to the ventral abdomen of individual beetles resulted ina6dLD50 value of 1.8 and 0.71 ng imidacloprid per beetle for L. nigrinus and S. tsugae, respectively. In no-choice tests, L. nigrinus mortality was signiÞcantly higher on hemlock branchlets treated with 100 ppm imidacloprid than on controls, but S. tsugae mortality was not. S. tsugae consumed the same number of adelgids on treated branchlets as on controls, but L. nigrinus consumed fewer adelgids from the 100 ppm branchlets than on controls. In choice tests, beetle mortality and ßip times were generally not signiÞcantly different from controls. At times, both beetle species displayed intoxication symptoms after feeding on adelgids from treated branchlets and imidacloprid was recovered from both beetle species postmortem. These results suggest that systemic imidacloprid displayed both lethal and sublethal effects on these two nontarget predators of the hemlock woolly adelgid. KEY WORDS Tsuga canadensis, Laricobius nigrinus, Sasajiscymnus tsugae, nontarget, prey-mediated effects Hemlock woolly adelgid, Adelges tsugae (Annand) avian species (Reay 1999, Yamasaki et al. 1999, Snyder (Hemiptera: Adelgidae), is an exotic invasive pest of et al. 2002, Tingley et al. 2002, Ross et al. 2003). two hemlock (Tsuga) species in the eastern United Hemlock woolly adelgid feeds on ßuids and nutri- States. Carolina hemlock, Tsuga caroliniana En- ents from parenchyma cells at the base of hemlock gelmann, is a relatively rare species conÞned to moun- needles (McClure 1987, 1991; Shields et al. 1995; tain ridges and isolated stands in the Appalachian Young et al. 1995). Infestation causes desiccation, bud highlands of western North Carolina, Tennessee, and mortality, needle loss, and a reduction of new growth Virginia. Eastern hemlock, Tsuga canadensis (L.) Car- (McClure 1987, McClure et al. 2001) and can lead to rie`re, is common along streams and cool, mountain dieback and tree death in 4Ð10 yr (McClure et al. slopes throughout eastern forests; its range extends 2001). Hemlock woolly adelgid has an anholocyclic from Maine to the southern extent of the Appalachian life cycle with two parthenogenic generations per year chain in northern Georgia and Alabama (Godman and on hemlocks. The asexual sistentes generation is Ϸ1 Lancaster 1990). Eastern hemlocks are an important mm in length and secretes a woolly white ßocculence economic (Rhea 1995, Holmes et al. 2005) and eco- or ovisac. Sistentes Þrst-instar crawlers aestivate on logical species; they provide habitats and nutrients hemlock stems throughout the summer. Breaking aes- that are beneÞcial for many aquatic, terrestrial, and tivation in the fall, they begin feeding and develop through four instars during the winter. Adults mature and lay eggs in March and April, which hatch as either 1 Department of Entomology, Virginia Polytechnic Institute and progredientes or sexuparae. Sexuparae production is State University, Blacksburg, VA 24061. initiated by high densities of sistentes that cause poor 2 Corresponding author: Department of Biology, Bryan College, host nutritional quality (McClure 1991). Sexuparae Dayton, TN 37321 (e-mail: [email protected]). 3 Department of Chemistry, Villanova University, Villanova, PA are winged and sexual; they do not feed on hemlocks 19085. but disperse to search for suitable spruce (Picea) spe- 0022-0493/10/1222Ð1234$04.00/0 ᭧ 2010 Entomological Society of America August 2010 EISENBACK ET AL.: EFFECTS OF IMIDACLOPRID ON HEMLOCK WOOLLY ADELGID 1223 cies to complete an holocyclic life cycle (Havill and 1999). For example, in cotton, Gossypium hirsutum L., Foottit 2007). The progredientes generation is similar metabolites protect the plant from whiteßies even in body morphology to the sistentes. After hatching, after parent compound concentrations declined Þrst instar crawlers disperse, settle, and begin to feed (Nauen et al. 1999). at the base of needles. The progredientes develop Effective control of hemlock woolly adelgid can be rapidly through four instars, mature, and lay eggs. Eggs achieved when imidacloprid is applied by foliar sprays hatch into sistentes crawlers which migrate to new or through systemic trunk or soil injections (McClure growth, settle, and aestivate through the summer. et al. 2001, Doccola et al. 2003, Webb et al. 2003, Laricobius nigrinus Fender (Coleoptera: Derodon- Cowles et al. 2006). Trunk and soil injections are the tidae) and Sasajiscymnus (Pseudoscymnus) tsugae primary control techniques for hemlock woolly adel- Sasaji & McClure (Coleoptera: Coccinellidae) are two gid in large-scale injection programs in national forests predators that have been reared and released as bio- and state parks. The Great Smoky Mountains National logical control agents of hemlock woolly adelgid Park in northeastern Tennessee is an example of a (Cheah and McClure 2002, Cheah et al. 2005, Lamb et current initiative to limit hemlock decline from hem- al. 2006). L. nigrinus is native to the PaciÞc Northwest lock woolly adelgid infestation. In the park, 466,843 and is a specialist predator of hemlock woolly adelgid. S. tsugae and 7,857 L. nigrinus) have been released at It is univoltine, host speciÞc and closely synchronized 32 and 191 sites, respectively, and Ͼ140,000 hemlocks with hemlock woolly adelgidÕs life cycle (Zilahi- have been treated via soil or trunk injections of imi- Balogh et al. 2002, 2003, Mausel et al. 2010). Adults dacloprid as of 2010 (K. Johnson, personal communi- emerge from the soil and begin feeding on sistentes in cation). the fall after the adelgids break aestivation. L. nigrinus In settings where chemical and biological controls feeds throughout the winter. The adults are cold hardy are jointly applied, it is important to determine the and active at temperatures above 0ЊC (Mausel 2007). compatibility of the two control options. High-value In early spring, adults begin laying eggs; larvae develop hemlock stands are often the Þrst candidates for chem- through four instars and feed primarily on hemlock ical control, and these same stands are desired as sites woolly adelgid eggs. In late spring, larvae drop from for biological control predator releases. Often preda- the hemlock branches into the soil where they pupate tor releases are in proximity to chemically treated and aestivate through the summer. L. nigrinus can sites, occupying the same valleys or mountain ridges. survive, oviposit, and reduce hemlock woolly adelgid As predators are released into the environment, it is populations in Þeld cages during winter and spring in important to analyze factors that could affect their southwestern Virginia (Lamb et al. 2005, 2006; Flowers establishment (Mausel 2007). Subsequent relocation et al. 2006). Three generations of L. nigrinus were and dispersal of predators from release sites could recovered from release sites in eastern forests (Lamb possibly result in predators coming into contact with et al. 2006, Mausel et al. 2010). hemlock woolly adelgid on hemlocks that have been S. tsugae is a multivoltine predator that is native to chemically treated. Japan where it is found in association with hemlock Using imidacloprid to control hemlock woolly ad- woolly adelgid (Cheah and McClure 1995). It can feed elgid could impact predators either through direct and develop to maturity on all stages of hemlock exposure or indirectly by changing hemlock woolly woolly adelgid, and its life cycle suggests a seasonal adelgid availability, quality, or distribution. Systemic synchrony with hemlock woolly adelgid progredien- insecticides do not directly expose predators to the tes in the Þeld (Cheah and McClure 1998, 2000). S. degree that foliar applications do (Mizell and Scony- tsugae is less cold tolerant than L. nigrinus and devel- ers 1992); however, nontarget beneÞcials can come ops most rapidly at temperatures from 20 to 25ЊC into contact with systemic toxins by feeding on plant (Cheah and McClure 2000). More than 3 million S. parts, contaminated prey, or through environmental tsugae and Ͼ100,000 L. nigrinus have been released in factors such as contaminated soil (Groot and Dicke eastern forests as of spring 2009. 2002). Predator consumption of