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Establishment of the Hemlock Woolly Adelgid Predator, Laricobius Nigrinus (Coleoptera: Derodontidae), in the Eastern United States

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Establishment of the Hemlock Woolly Adelgid Predator, Laricobius Nigrinus (Coleoptera: Derodontidae), in the Eastern United States BIOLOGICAL CONTROL-PARASITOIDS AND PREDATORS Establishment of the Hemlock Woolly Adelgid Predator, Laricobius nigrinus (Coleoptera: Derodontidae), in the Eastern United States 1 D. L. MAUSEL, S. M. SALOM, L. T. KOK, AND G. A. DAVIS Department of Entomology, Virginia Tech, 216A Price Hall MC 0319, Blacksburg, VA 24061-0002 Environ. Entomol. 39(2): 440Ð448 (2010); DOI: 10.1603/EN09088 ABSTRACT The hemlock woolly adelgid, Adelges tsugae Annand (Hemiptera: Adelgidae), native to western North America and Asia, was accidentally introduced from Japan to the eastern United States. To potentially establish biological control of A. tsugae, we released a predator endemic to western North America, Laricobius nigrinus Fender (Coleoptera: Derodontidae), from 2003 to 2005, in 22 localities from Georgia to Massachusetts. Release sites spanned the invasive range of the adelgid across Þve United States Department of Agriculture plant hardiness zones (5a to 7a). Release sizes were 75, 150, 300, 600, or 1,200 adult L. nigrinus per site in the fall, winter, early spring, or sequentially (i.e., fall or winter and early spring). We monitored establishment by annual sampling for L. nigrinus adults with beat sheets and for L. nigrinus larvae by branch clipping. At the end of 3 yr, L. nigrinus was established in 13 of the 22 sites. The following variables were evaluated for their correlation with the numbers of L. nigrinus larvae and adults recovered and for their effect on establishment (scored as F3 presence/absence): (1) Minimum winter temperature at the release site, (2) A. tsugae density at the time of release, (3) release size, and (4) release season. Only minimum winter temperature was correlated with larval recoveries and no variables were correlated with adult recoveries. Logistic regression modeling found that establishment was positively related to minimum winter temperature and release size. We recommend smaller release sizes in warm areas where establishment probability was high (i.e., zones 7a, 6b, and 6a) and larger release sizes in cold areas where establishment probability was low (i.e., zones 5b and 5a). Releases during fallÐearly spring and across the range of A. tsugae densities tested were successful. KEY WORDS Tsuga canadensis, Adelges tsugae, Laricobius nigrinus, release strategy, establishment To improve the establishment rate of classical biolog- mott et al. (1998) discovered that releases of Ͻ100 ical control agents, better understanding is needed of gorse thrips, Sericothrips staphylinus (Haliday) (Thys- variables that affect colonization (Memmott et al. anoptera: Thripidae), on gorse were superior to 1,000, 1998). Climate in particular is recognized frequently the size formerly advocated. as an important variable, whose inßuence can be pre- Classical biological control is the option of primary dicted through the use of climate-matching methods interest for suppression of the hemlock woolly adel- (Sutherst et al. 2004). An issue of practical importance gid, Adelges tsugae Annand (Hemiptera: Adelgidae), is the optimal number of individuals to release per site. in native eastern hemlock, Tsuga canadensis (L.) Since the relative importance of demographic stochas- Carrie`re, and Carolina hemlock, T. caroliniana En- ticity (e.g., sex ratio), environmental variability (e.g., gelmann, forests of the eastern United States (Cheah temperature), and Allee effects (e.g., mate Þnding in et al. 2004). The adelgid is native to northwestern small populations) are typically unclear during ex- North America and Asia and was discovered in Rich- ploratory releases, a mixed release strategy has been mond, VA, in the 1950s after accidental introduction advocated (Shea and Possingham 2000). A mixed strat- from Japan (Havill et al. 2006). It has spread widely egy is one using a structured set of different release (Anonymous 2009) and caused extensive mortality of approaches, which can facilitate a better understand- hemlock trees (Orwig and Foster 1998, Eschtruth et al. ing of variables that inßuence establishment and im- 2006). Methods exist for monitoring A. tsugae (Costa prove efÞciency and success of subsequent releases and Onken 2006, Fidgen et al. 2006), chemically con- (Campbell 1976, Grevstad 1999). For example, Mem- trolling it (Steward and Horner 1994), and ameliorat- ing hemlock forest decline (Ward et al. 2004). Unfor- tunately, there does not appear to be any effective 1 Current address: Department of Plant, Soil, and Insect Sciences, natural enemies of A. tsugae in eastern United States University of Massachusetts, Agricultural Engineering Bldg., 250 Natural Resources Road, Amherst, MA 01003-9295 (e-mail: dmausel@ forests (Wallace and Hain 2000). However, Laricobius psis.umass.edu). rubidus LeConte (Coleoptera: Derodontidae), an ex- 0046-225X/10/0440Ð0448$04.00/0 ᭧ 2010 Entomological Society of America April 2010 MAUSEL ET AL.: ESTABLISHMENT OF Laricobius nigrinus 441 tant predator of the native pine bark adelgid, Pineus Effective biological control agents typically estab- strobi (Hartig), has recently been discovered com- lish easily and show some impact within three gener- pleting development on A. tsugae (Zilahi-Balogh et al. ations (Clausen 1951). Those that do not establish 2005, Mausel et al. 2008). Foreign explorations in Asia easily or show impact within this period often have and northwestern North America have identiÞed sev- little chance of success, but exceptions occur (Debach eral predators as potential biological control agents of and Rosen 1991). Centered on this theory, our objec- A. tsugae (Sasaji and McClure 1997, Yu et al. 2000, Yu tive was to use a mixed release strategy and determine and Montgomery 2007, Zilahi-Balogh et al. 2007, how well adult L. nigrinus releases in A. tsugae-infested Kohler et al. 2008). Three coccinellids from Asia and eastern hemlock forests established based on 3 yr of Laricobius nigrinus Fender from northwestern North systematic postrelease monitoring. To potentially in- America have been released (Cheah et al. 2004). crease the success rate of subsequent releases, the Surveys of western hemlock, Tsuga heterophylla following variables were evaluated for their associa- (Raf.) Sargent, have shown that L. nigrinus is wide- tion with the numbers of L. nigrinus larvae and adults spread and feeds on A. tsugae, at both low and high recovered, and for their effects on establishment density infestations in northwestern North America (scored as F3 presence/absence): Minimum winter (Kohler et al. 2008). Adults and larvae feed on A. temperature at the release site, A. tsugae density at the tsugae eggs, nymphs, and adults at the base of needles. time of release, release size, and release season. L. nigrinus eggs are laid in late winterÐearly spring in sistens ovisacs (summerÐearly spring A. tsugae gener- Materials and Methods ation), which contain progrediens eggs (spring A. tsugae generation). Larvae develop through four in- Selection of Release Sites and Trees. Releases were stars feeding on A. tsugae eggs and fourth instars drop made in eight states throughout the invasive range of A. tsugae in the eastern United States (Table 1; Fig. 1). to the forest ßoor to pupate. After eclosion, adults Ͼ undergo aestival diapause in the soil during summer Stands of 10 ha with a hemlock component, where and emerge in fall, synchronized with sistens Þrst A. tsugae density was low to moderate (1Ð75% of instars breaking aestival diapause. They feed on de- shoots infested), and crown health was not severely veloping adelgid nymphs and adults in fallÐwinter compromised (i.e., off color, premature needle loss, and branch tip dieback) were selected. Individual (Zilahi-Balogh et al. 2003). trees that L. nigrinus were released on had high live Because L. nigrinus feeds, oviposits, and undergoes crown ratios (Ͼ95%) to enable access to branches larval development during fall, winter, and early from the ground for beat sheet sampling. spring, cold temperature is likely an important abiotic Release Procedures. The L. nigrinus adults released mortality factor during the critical establishment were laboratory-reared from parents collected from phase when releases occur in the eastern United an A. tsugae-infested western hemlock seed orchard States. Survival of A. tsugae itself is positively related near Victoria, BC, Canada (48.48 N, 123.36 W) in late to minimum winter temperature (Trotter and Shields winter 2003. They were reared using established 2009). Winters are mild in the marine west coast cli- methods (Lamb et al. 2005b). Reared adults emerging mate of Victoria, BC, Canada (i.e., the source location after aestival diapause from soil Þlled containers in of L. nigrinus in this study) but are considerably colder fall 2003Ð2005. (i.e., F1 laboratory generation) were in many areas of A. tsugaeÕs invasive range in the placed in 3.8-liter containers in groups of up to 50 on eastern United States. Summers are also cooler and A. tsugae-infested eastern hemlock. Depending on the dryer in Victoria, BC; however, L. nigrinus is dormant season, adults were maintained at 2Ð10ЊC, seasonally in earthen soil cells at this time and unlikely to be adjusted photoperiods, and 70Ð90% RH in environ- affected by potentially higher soil temperatures and mental chambers before release. They were screened moisture. for missing appendages, poor-color, or small size. L. nigrinus was imported into the eastern United Three sub-samples of adults were examined for ento- States from Victoria, BC, for evaluation and was de- mopathogens before release by Dr. L. Solter, IL Nat- termined to be host-speciÞc (Zilahi-Balogh et al. ural History Survey; Dr. A. Lawrence, Mississippi State 2002). Subsequent to Federal and State approval for University; and Dr. J. Becnel, USDA-ARS Gainesville environmental release of L. nigrinus, several Þeld stud- and all results were negative. ies were carried out in southwest Virginia. Adults L. nigrinus adults were given fresh A. tsugae every 2 demonstrated high winter survival in sleeve cages, wk until they were released. A cluster of 10Ð15 A. signiÞcant feeding, and oviposition on A. tsugae (Lamb tsugae-infested eastern hemlock twigs (10 cm length) et al. 2005a).
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