Scott M. Salom

Host specificity of Laricobius nigrinus Fender (Coleoptera: Derodontidae), a potential biological control agent of the hemlock woolly adelgid, Adelges tsugae Annand (Homoptera: Adelgidae)

Abstract Host specificity tests of Laricobius nigrinus Fender (Coleoptera: Derodontidae) were conducted under quarantine in Blacksburg, Virginia, to determine the suitability of this beetle as a biological control agent of the hemlock woolly adelgid, Adelges tsugae Annand (Homoptera: Adelgidae), in the eastern United States. Members of the genus Laricobius are known to feed on adelgids. L. nigrinus, native to western North America, was tested on three other adelgids and three non-adelgid species of Homoptera in three families. A. tsugae is an exotic insect pest of eastern (Tsuga canadensis (L.) Carriere) and Carolina (T. caroliniana Engelmann) hemlocks. In paired-choice and no-choice oviposition tests, L. nigrinus females preferred to oviposit in A. tsugae ovisacs over the other test species. Feeding tests showed that L. nigrinus consumed more eggs of A. tsugae than eggs of Adelges piceae (Ratzeburg) and Pineus strobi (Hartig), but not of Adelges abietis (L.). In larval development tests, L. nigrinus only completed development on A. tsugae. These results suggest that L. nigrinus has a narrow host range and that it has potential for biological control of A. tsugae. Based on these results, L. nigrinus has been cleared for field release by USDA APHIS.

Establishment of the hemlock woolly adelgid predator, Laricobius nigrinus (Coleoptera: Derodontidae), in the eastern United States.

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 five 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 fall—early spring and across the range of A. tsugae densities tested were successful.

Development and reproductive biology of Laricobius nigrinus, a potential biological control agent of Adelges tsugae

Biological studies on Laricobius nigrinus Fender (Coleoptera: Derodontidae) were conducted in the laboratory to obtain basic information on this littleknown predator. Laricobius nigrinus is acandidate biological control agent of thehemlock woolly adelgid, Adelges tsugaeAnnand (Homoptera: Adelgidae), an exotic peston eastern (Tsuga canadensis (L.)Carrière) and Carolina (T.caroliniana Engelmann) hemlocks in the easternUnited States. It is univoltine andundergoes an aestival diapause. Post-aestivation activity period was 36.6 and30.8 weeks for males and females, respectively. Adult activity and oviposition are wellsynchronized with the over-wintering generationof A. tsugae. Mean lifetime fecunditywas 100.8 eggs over a mean duration of 13.2weeks oviposition period. Within thetemperature range (12–18°C) studied,development was fastest at 18°C. Meandevelopment time from egg to adult was 88.8,64.8 and 46.6 days at 12, 15 and 18°C,respectively. Laricobius nigrinus hasfour larval instars. Mean larval consumptionwas 225.9 and 252.3 A. tsugae eggs at 12and 18°C, respectively. Thesefindings provide essential data on the rate ofdevelopment and feeding capacity of L. nigrinusat temperatures typical of ambientconditions during late winter/early spring inVirginia. Its rapid development at18°C indicates that it has potential asa biological control agent of A. tsugaebecause of its synchrony with the developmentof the over-wintering generation of A. tsugaein eastern United States.

Lethal and Sublethal Effects of Imidacloprid on Hemlock Woolly Adelgid (Hemiptera: Adelgidae) and Two Introduced Predator Species

ABSTRACT Eastern hemlock, Tsuga canadensis (L.) Carrière, 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 flip 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 in a 6 d LD50 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 significantly 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 flip times were generally not significantly 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.

Propagation, Synchrony, and Impact of Introduced and Native Laricobius spp. (Coleoptera: Derodontidae) on Hemlock Woolly Adelgid in Virginia

Abstract Synchrony and impact of the predators Laricobius nigrinus Fender and Laricobius rubidus LeConte, on hemlock woolly adelgid, Adelges tsugae Annand, were studied in an eastern hemlock field insectary in Virginia. First, a field insectary for propagation of the introduced L. nigrinus was established by planting hemlocks in 2001, infesting them with hemlock woolly adelgid in 2002 and 2003, followed by releasing 258 L. nigrinus in 2003. Initial sampling showed that the native L. rubidus was present in the area. Hemlock woolly adelgid and both Laricobius species populations increased annually, from which 305 F3 L. nigrinus adults were collected and redistributed to forests in 2007. Second, the phenology of hemlock woolly adelgid and Laricobius spp. life cycles were monitored in 2005 and 2006. Adult L. nigrinus (F2) and L. rubidus were active on hemlock from fall through mid-spring and overlapped with second-instar sistentes nymphs through progredientes eggs. The predators’ eggs were oviposited and larvae developed (i.e., F3 L. nigrinus) from late winter to mid-spring on progredientes eggs, indicating synchrony with suitable prey life stages. Third, a predator exclusion experiment was used to examine the relationships between the predators and prey in 2005 and 2006. When exposed to L. nigrinus (F2 adults and F3 larvae) and L. rubidus, hemlock woolly adelgid survival and ovisac density were lower and ovisac disturbance was higher than hemlock woolly adelgid protected in cages. The establishment and production of L. nigrinus at a field insectary, synchronization with, and impacts on hemlock woolly adelgid after a small release 2 yr earlier makes it an important potential biological control agent of hemlock woolly adelgid.

Laboratory Evaluation of Biologically-Based Compounds as Antifeedants for the Pales Weevil, Hylobius pales (Herbst) (Coleoptera: Curculionidae)

Twenty plant-produced compounds or mixtures and one insect-produced semiochemical were evaluated as potential antifeedants for the pales weevil, Hylobius pales (Herbst). Initially, a choice laborat...

Competitive Interactions Among Two Specialist Predators and a Generalist Predator of Hemlock Woolly Adelgid, Adelges tsugae (Homoptera: Adelgidae), in the Laboratory

Abstract Competitive interactions among two specialist predators, Laricobius nigrinus Fender and Sasajiscymnus (Pseudoscymnus) tsugae Sasaji and McClure, and a generalist predator, Harmonia axyridis Pallas, of hemlock woolly adelgid, Adelges tsugae Annand, were studied in the laboratory. The two specialist predators are part of a biological control program that has been initiated for A. tsugae, and the potential for competition among these species and polyphagous established predators is unknown. Laboratory assays were evaluated in environmental chambers at two conditions: (1) early spring, 9:5°C (D:N), 12:12 (L:D) h, and 50–75% RH; and (2) late spring, 18:10°C (D:N), 16:8 (L:D) h, and 75–90% RH. Predator feeding trials using conspecific and heterospecific eggs showed that L. nigrinus and S. tsugae eggs were consumed by all species, and predation was decreased with increased A. tsugae density. Eggs of H. axyridis were eaten almost exclusively by conspecifics, at high rates, regardless of A. tsugae density. Survival, feeding on A. tsugae, and net egg production of single predators and groups of three conspecifics and heterospecifics were also examined. Survival for all species was not significantly affected by the presence of additional predators. In conspecific groupings, only H. axyridis showed significant reductions in feeding on A. tsugae, whereas all species had significantly reduced net egg production with conspecifics. In heterospecific groupings, no significant effects on A. tsugae predation or net egg production were detected. The only significant negative competitive interactions detected in these assays were among conspecifics, whereas heterospecific combinations showed noninterference.

Temperature-Dependent Development of the Specialist Predator Laricobius nigrinus (Coleoptera: Derodontidae)

Abstract The effect of temperature on the duration of egg, larval, prepupal, and pupal development of the predator Laricobius nigrinus Fender was studied at six constant temperatures (6, 9, 12, 15, 18, and 21°C) where Adelges tsugae Annand was used as prey. Developmental time was inversely proportional to temperature between 6 and 18°C. Laricobius nigrinus did not complete development at 21°C. Significant positive linear relationships were observed between developmental rate and temperature for all life stages. Minimum developmental threshold temperatures were estimated at 5.4°C for eggs, 3.2°C for larvae, 2.9°C for prepupae, and 3.1°C for pupae. Median development times for eggs, larvae, prepupae, and pupae were 59.5, 208.3, 217.4, and 212.8 degree-days (DD) above minimum developmental temperatures, respectively. Development from oviposition to adult eclosion required a minimum temperature of 3.7°C and 666.7 DD. A degree-day model, developed in the laboratory for predicting egg hatch, predicted a degree-day value that was within 4 d of the median egg hatch observed at two field sites in 2000. This regression model is a useful predictor of egg hatch in Victoria, British Columbia, Canada. In addition, the lower development threshold from egg to adult for L. nigrinus (3.7°C) is similar to that for the A. tsugae progrediens (spring) generation from second instar to adult (3.9°C), indicating that L. nigrinus and A. tsugae are adapted to similar climatic regimes.

Volatile emissions of eastern hemlock, Tsuga canadensis, and the influence of hemlock woolly adelgid.

The volatile emissions of eastern hemlock, Tsuga canadensis Carriere, were identified and quantified using standard and chiral gas chromatography and mass spectrometry. All of the identified compounds were monoterpenes, and included alpha-pinene, myrcene, tricyclene, camphene, alpha-phellandrene, beta-pinene, limonene, beta-phellandrene, terpinolene, and bornyl acetate. alpha-Pinene, myrcene, and camphene comprised greater than 75% by mass of the total release. Infestation by the exotic insect, hemlock woolly adelgid (HWA, Adelges tsugae Annand), resulted in an increased release rate of monoterpenes from branch tips. Release rate was negatively correlated to the amount of the branch tip sample that was new growth, suggesting that release rate is greater from previous-year foliage. Additionally the percent composition of the volatile profile is slightly altered by infestation, with alpha-pinene comprising 57% of volatiles from infested foliage and 66% from uninfested foliage.

Comparison between a native and exotic adelgid as hosts for Laricobius rubidus (Coleoptera: Derodontidae)

Laricobius rubidus LeConte, native to eastern North America whose primary host is Pineus strobi Hartig, has been observed in association with Adelges tsugae, an exotic and lethal pest of hemlock trees in eastern North America. Pineus strobi and A. tsugae were used to evaluate host preference and suitability of this predatory beetle to determine in part its suitability as a potential biological control agent of A. tsugae. In a paired-choice oviposition test, L. rubidus preferred to oviposit in P. strobi ovisacs over those of A. tsugae. However, in the no-choice oviposition test, there was no significant difference in the mean number of eggs laid by L. rubidus females in P. strobi or A. tsugae ovisacs. There were no significant differences in larval developmental time or survivorship for L. rubidus reared on a diet of either P. strobi or A. tsugae. Laricobius rubidus completed development to the adult stage on A. tsugae indicating that it is a suitable host and therefore has the potential to contribute to biological control of A. tsugae in the eastern United States. The introduction of a congener, Laricobius nigrinus to eastern North America may result in competition with L. rubidus on A. tsugae, but the inability of L. nigrinus to complete development on P. strobi suggests that the two congeners will not compete on the primary host of L. rubidus.