Survival and reproduction of Laricobius nigrinus Fender (Coleoptera: Derodontidae), a predator of hemlock woolly adelgid, Adelges tsugae Annand (Homoptera: Adelgidae) in field cages

Biological Control 32 (2005) 200–207 www.elsevier.com/locate/ybcon

Survival and reproduction of Laricobius nigrinus Fender (Coleoptera: Derodontidae), a predator of hemlock woolly adelgid, Adelges tsugae Annand (Homoptera: Adelgidae) in Weld cages A.B. Lamb¤, S.M. Salom, L.T. Kok Entomology Department, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061-0319, United States Received 4 March 2004; accepted 22 September 2004 Available online 5 November 2004

Abstract Laricobius nigrinus Fender (Coleoptera: Derodontidae) is being evaluated as a biological control agent for the hemlock woolly adelgid (HWA), Adelges tsugae Annand (Homoptera: Adelgidae). Predator exclusion studies on survival, reproduction, and impact on HWA populations were investigated over two years in Virginia, US. In year 1, branches were selected to receive one of three treatments: caged hemlock branches with predators; caged hemlock branches without predators; and uncaged hemlock branches. L. nigrinus adults survived from February to April, producing up to 41 progeny per female. Adelgid densities on branches exposed to L. nigrinus exhibited a signiWcantly higher rate of decline than those on branches not exposed to predators. Additionally, the Wnal density of sistens and progrediens was signiWcantly lower on caged branches containing L. nigrinus than on caged and uncaged branches without predators. In year 2, L. nigrinus survival and predation was evaluated over two 10-week sample periods: (November–January and February–April). L. nigrinus survived throughout the 6-month test period, with 89% surviving through January and 55% through April. Between February and April, 38 progeny were produced per beetle. The decrease in adelgids, measured in both numbers of adelgids and percent reduction per branch, was signiWcantly higher (p < 0.0001) on caged branches with L. nigrinus than on those without predators.  2004 Elsevier Inc. All rights reserved. Keywords: Laricobius nigrinus; Adelges tsugae; Biological control; Field evaluation; Predation; Winter survival; Derodontidae; Adelgidae; Tsuga canadensis

1. Introduction Hemlock woolly adelgid (HWA), Adelges tsugae Annand (Homoptera: Adelgidae) is an Asian insect that attacks and kills eastern hemlock, Tsuga canadensis (L.), and Carolina hemlock, T. caroliniana Engelmann, in the eastern United States. The geographic range of eastern hemlock extends from Nova Scotia west to Minnesota and south to northern Alabama (Baumgras et al., 1999). HWA was Wrst observed in Virginia in 1952 and, since

*

Corresponding author. Fax: +1 540 231 3191. E-mail address: [email protected] (A.B. Lamb).

1049-9644/$ - see front matter  2004 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2004.09.016

the 1980’s, has spread quickly, currently infesting 50% of the geographic range of hemlock (Cheah et al., 2004). The rapid dispersal of this pest is facilitated by wind, birds, deer, and humans (McClure, 1990), enabling it to spread up to 25 km per year (Yorks et al., 1999). The adelgid feeds at the base of needles, which causes them to desiccate and fall oV. Loss of needles inhibits the development of shoots and the growth of new needles (McClure, 1996), and may cause complete mortality in aVected stands in as few as four years after initial infestation (McClure et al., 1996). HWA outbreaks are facilitated by the absence of natural enemies, the susceptibility of Tsuga spp. in eastern North America (Cheah and McClure, 1998; Wallace and Hain, 2000),

A.B. Lamb et al. / Biological Control 32 (2005) 200–207

and their ability to survive low temperatures (Parker et al., 1999). HWA has a complex polymorphic life cycle that involves two asexual and one sexual generation annually (McClure, 1987). The overwintering generation (sistens) feeds and develops throughout the fall and winter months. Sistens deposit eggs within woolly ovisacs. Upon hatching, the Wrst instar crawls to and settles at the base of a hemlock needle (McClure, 1987). This second generation develops rapidly through four instars, maturing in June. A proportion of these nymphs develop wings (sexuparae), while the rest remain wingless (progrediens). The wingless adults lay eggs within woolly ovisacs in late spring, which hatch into sistens crawlers that settle at the base of young needles, feed for a short time, and then enter aestivation (summer diapause) (Gray and Salom, 1996; McClure, 1989; Salom et al., 2002). Aestivation lasts for several months, and sistens nymphs resume feeding and development in October (Gray and Salom, 1996; McClure, 1987). The sexuparae develop along side the progrediens, and when mature they disperse to spruce (Picea spp.) (McClure, 1989). There are no suitable spruce hosts in North America (McClure, 1992); therefore, the production of sexuparae constitutes a mortality factor for HWA populations. The proportion of sistens progeny that develops into sexuparae seems to be directly dependent on the density of sistens (McClure, 1991). The life cycle of HWA is similar in Asia and North America, but, the phenology and timing of their life stages and generations vary signiWcantly with elevation, latitude, and weather conditions (McClure et al., 1999). In addition, the sexual generation has not been observed in western North America (Zilahi-Balogh et al., 2003a). A wide temporal overlap of life stages is characteristic of HWA development in North America (Gray and Salom, 1996; McClure, 1987). Although HWA can be eVectively controlled by insecticides in urban settings (McClure, 1987), these applications are not practical in the forest. Biological control may be the only viable option for reducing HWA populations in the forest setting. With asexual reproduction and two generations per year, HWA populations increase at a rapid rate. Several Asian coccinellid species have been evaluated for their potential as biological control agents for HWA in the eastern United States. Sasajiscymnus tsugae Sasaji and McClure was imported from Japan and has been released throughout the eastern States since 1997 (Cheah and McClure, 1998; Cheah et al., 2004). It is thought to be established, although recovery of this insect has been inconsistent. This predator is active in the later spring and primarily attacks the progrediens generation. A Chinese coccinellid, Scymnus ningshanensis Yu et Yao, is currently being laboratory tested and was released

201

for the Wrst time in spring 2004 (Asaro and Montgomery, personal communication). Another predator that may potentially play an important role in controlling HWA is L. nigrinus, a predacious beetle of HWA in western North America, where hemlock trees are not harmed by HWA. Cheah and McClure (1996) suggested that maintenance of HWA below damaging levels in western North American may be attributed to tree resistance and natural enemies. Laricobius nigrinus is found feeding on HWA in Washington, Oregon, Idaho, and British Columbia (Lawrence and Hlavac, 1979). Field studies in British Columbia and investigations in the laboratory revealed that L. nigrinus possesses many qualities considered desirable by HuVaker and Kennett (1969), in successful biological control agents. It feeds selectively on HWA, is unable to complete development on other adelgid and scale species (Zilahi-Balogh et al., 2002), and its life cycle is phenologically synchronous with that of HWA (Zilahi-Balogh et al., 2003a). Laricobius nigrinus is a univoltine species. The adults are active and feed throughout the fall and winter months. In early spring, adults oviposit in adelgid ovisacs and larvae develop through four instars on adelgid eggs laid by the sistens generation (Zilahi-Balogh, 2003b). When mature, the larvae drop to the soil, pupate, and eclose. The adults aestivate in the soil throughout the summer months, emerge in the fall, and migrate back to hemlock trees. Laricobius nigrinus is a winter-active predator and is unlikely to compete with the Asian predators that are active later in the spring. Thus, we believe it to be a potentially complementary and important component of a predator complex. For L. nigrinus to be a viable biological control candidate, it must be able to survive under natural Weld conditions and help reduce HWA density below injurious levels. The most convincing means of documenting the eVect of a predator is by using check methods, where the predator is excluded from prey on certain branches of the host plant, while including them on other branches (HuVaker and Kennett, 1969). The survival of the prey population can then be compared in the presence and absence of predators. Principal draw-backs of the sleeve-cage method are possible modiWcations of the microclimate, interference with predator dispersal, and protection from wind (DeBach et al., 1951). We report the results of two experiments conducted to determine the ability of L. nigrinus to survive in Virginia’s climate and to evaluate its impact on HWA populations in sleeve cages. The speciWc objectives were to investigate the adult survivorship and reproduction of L. nigrinus throughout the winter and spring; and the impact of L. nigrinus adults and larvae on HWA sistens and progrediens populations.

202

A.B. Lamb et al. / Biological Control 32 (2005) 200–207

2. Materials and methods 2.1. Study sites Field studies were conducted over two consecutive winters. The Wrst experiment was conducted at three sites from February to June, 2001. The sites were located in Montgomery and Giles counties in Southwest Virginia. Site 1 was located at Poverty Creek [Universal Transverse Mercator (UTM): 17 542429 N, 4123129 E], Site 2 at Big Stoney Creek [UTM: 17 533985 N, 4140859 E], and Site 3 was established at the Mountain Lake Nature Conservancy [UTM: 17 541017 N, 4134851 E]. The hemlocks at Sites 1 and 2 were young, understory trees (4 and 8 m tall, respectively). The elevation at Site 1 is 602 m and was located near a bottomland stream in young forest dominated by eastern white pine, Pinus strobus L. Site 2 is located on a northwestern slope (720 m elevation) in a forest dominated by tulip poplar, Liriodendron tulipifera L., and eastern white pine, P. strobus. Site 3 is located at 1218 m in elevation and hemlock trees at this site were 28 m tall and dominated the overstory vegetation. Dataloggers (Hobo, Onset, Poasset, MA) were used to record temperatures at each site during both Weld seasons. Sensors were placed outside and within one sleeve cage at each site. The mean temperature recorded at the Mountain Lake Biological Research Station weather station (approximately 1 mile from Site 3) in February and March (2001) was 0.7 °C, with maximum and minimum temperatures of 15 °C and ¡13.6 °C, respectively. The mean temperature during April and May was 11.6 °C, with maximum and minimum temperatures of 24.6 °C and ¡7.4 °C, respectively. During the study, total precipitation was 39.4 cm with several snow and ice storm events. On average, Sites 1 and 2 experienced temperatures approximately 2 °C warmer than Site 3. There was no diVerence in temperature measured inside and outside the sleeve cages. These two trends were also observed in the second Weld season. The second year experiment was conducted from November 2001 to April 2002 at three sites in Giles county, Southwest Virginia. Two sites were located at Big Stoney Creek: Site 4 [UTM: 543738 N, 4142220 E] and Site 5 [544395 N, 4142097 E]. A third (Site 6) was located at Mountain Lake Nature Conservancy [UTM: 542047 N, 4136311 E]. The hemlocks used at Sites 4 and 5 were understory trees (12 m tall) on northwest facing slopes at 919 and 950 m in elevation, respectively. The overstory vegetation at these sites was dominated by oaks, Quercus spp., and hickories, Carya spp. The hemlock trees used at Site 6 (elevation 1213 m) were 15 m tall and dominated the overstory vegetation. The mean temperature measured at Mt. Lake Biological Research Station (Site 6) in November and Decem-

ber 2001 was 4.9 °C with the highest temperature 20 °C and the lowest ¡13.7 °C. The maximum and minimum temperatures experienced in January and February 2002 were 15.8 and ¡16 °C, respectively, whereas the mean temperature during these months was ¡0.5 °C. The mean temperature during March and April 2002 was 7.2 °C with a maximum temperature of 31.1 °C and minimum of ¡14.7 °C. The total precipitation during the months of the study was 195 cm, and included several snow and ice storms. 2.2. Year 1 study Two trees with high densities of HWA and accessible branches were chosen at each site. Twenty-seven branches, heavily infested with HWA, were selected from each tree. The total number of adelgids was determined by directly counting the ovisacs on the terminal 45 cm of each branch. Each branch was then randomly assigned one of three treatments: caged branches with two female adult L. nigrinus; caged branches without predators; and uncaged branches without predators. The latter two treatments served as controls to determine the eVect of cages on the survival of the adelgid. The adults used for these experiments were selected by isolating individual beetles and determining which individuals oviposited on supplied host material, since we are unable to use morphological characteristics to diVerentiate sex (Zilahi-Balogh, 2001). The cages were sewn nylon mesh sleeves (# 110 mesh, Dynamesh, Chicago, IL) (open at one end), attached to the terminal end of each branch with 20 gauge galvanized wire wrapped over rubber foam weatherseal (1.91 cm wide, 1.11 cm thick). Using a randomized complete block experimental design, with each tree serving as a block, the eVect of predators and time on adelgid populations was tested. There were six trees with nine replicates on each tree. One replicate of each treatment was removed from each tree at two-week intervals, and the total number of surviving predators, both adults and progeny, was counted using a microscope. In addition, the total number of surviving adelgids on each branch was determined. Data were analyzed using a 2-factor analysis of variance (ANOVA) with statistical analysis software (SAS) (SAS Institute, 1992) to determine if L. nigrinus had a signiWcant impact on Wnal adelgid densities or rate of decrease in adelgid densities. All means were separated using Fisher’s least signiWcant diVerence (LSD) test in SAS. 2.3. Year 2 study One tree was chosen at each of the three sites. Nine branches, heavily infested with HWA, were selected from each tree, and the total numbers of adelgids were

A.B. Lamb et al. / Biological Control 32 (2005) 200–207

counted on the terminal 45 cm of each branch. Each branch was then caged and randomly assigned one of three treatments: Wve adult L. nigrinus present throughout the study (permanent predators); four adult L. nigrinus replaced with lab-reared adults at each sample period (temporary predators); and no predators. We wanted to test L. nigrinus survival throughout the entire winter using the same individuals. The temporary predator treatment was added to collect feeding data, in case the permanent predators did not survive. Since the cage-eVect on HWA density observed in the Wrst year study was not signiWcant, the uncaged control treatment was excluded in the second year. At each sample period, all branches were removed and returned to the laboratory for closer examination. The number of surviving L. nigrinus adults on each branch was assessed and beetles were re-caged on new branches in the Weld the following day. The numbers of L. nigrinus progeny and surviving adelgids were counted using a microscope. Each sample period lasted 10 weeks, the Wrst from November to January and the second from February to April. This experiment was set up as a randomized block design with trees serving as blocks. A two-factor ANOVA in SAS was used to determine if sample period or predator group had an eVect on predator survival or reproduction and if L. nigrinus had a signiWcant impact on the decrease in number or proportion of total adelgids during each sample period. Proportional decreases were arc-sine transformed to perform the analysis of variance and means were separated using Fisher’s LSD test in SAS.

3. Results and discussion 3.1. Year 1 study Laricobius nigrinus adults survived from February to May, and most oviposition occurred in March and April (Fig. 1). Adult survival and oviposition activity declined over time, most likely because of a shortage of prey inside the cages and natural mortality. The total impact the two females and their progeny had on adelgid populations is illustrated in Fig. 2, which compares the Wnal density of the sistens and progrediens generations across treatments at each sample period. The density of sistens was signiWcantly lower on branches exposed to predators than those without predators in every sample period (F D 46.67, df D 2, 130, P < 0.0001). The density of progrediens was lower on branches with predators than those without in every sample period, and signiWcantly lower in several sample periods (F D 12.53, df D 2, 130, P < 0.0001) (Fig. 2). Caged branches without predators tended to have higher adelgid densities than uncaged

203

Fig. 1. Percentage of L. nigrinus adults and the mean number of L. nigrinus progeny found alive at each sample period (n D 54) in year 1 of study. Two adults were placed in sleeve cages on February 20, 2001 and sampled for the Wrst time on March 7.

branches, but only signiWcantly so in three sample periods. This suggests that cages may aid the survival of adelgids. Although L. nigrinus was not present after midMay, adult and larval feeding on the sistens and the ovisacs they produced had a carry-over eVect that lowered the density of the subsequent generation (progrediens). The diVerence in the total decrease of adelgids on branches with and without predators was attributed to L. nigrinus and was used to calculate adult consumption (Table 1). The branches exposed to L. nigrinus showed a signiWcantly higher rate of decrease in sistens density than branches not exposed to predators (F D 59.14, df D 2, 80, P < 0.0001). In six of the Wrst seven sample periods, branches caged with predators had a signiWcantly higher rate of decrease in sistens density than those without. 3.2. Year 2 study We modiWed our Weld evaluation in the second season in an eVort to determine whether L. nigrinus adults would survive the entire winter (beginning in November) in Virginia and to assess their feeding and oviposition activity while adequate prey were present. Data collected for permanent and temporary predators were pooled, since no diVerences were found between their survival (F D 0.16, df D 1, 131, P D 0.69) or reproduction (F D 0.02, df D 1, 131, P D 0.96). L. nigrinus survival and reproduction were signiWcantly diVerent between sample periods (Table 1). The total decrease in sistens (original count ¡ Wnal count) was signiWcantly greater on branches exposed to L. nigrinus adults than branches not exposed to predators in both sample periods (F D 17.10, df D 1, 46, P < 0.0001). The mean decrease (§SE) in sistens from November to January was 1323 § 85 and 704 § 91 on branches with and without predators, respectively. From February to April, the mean decrease (§SE) in sistens was 1870 § 105 and 962 § 77 on branches with and without L. nigrinus, respectively. Table 1 summarizes the predator activity collected during the two Weld seasons. The diVerence in the total

204

A.B. Lamb et al. / Biological Control 32 (2005) 200–207

Fig. 2. The mean Wnal density of sistens (A) and progrediens (B) per cm branch (§SE) on caged branches, with and without predators, and uncaged branches at each sample period in year 1 of study. Mean densities signiWcantly diVerent at each sample period in (A) and (B) are shown by diVerent letters, with means separated using Fisher’s LSD in SAS (F D 46.67, df D 2, 130, P D 0.0001 and F D 12.53, df D 2, 130, P D 0.0001, respectively). Adult predators and progeny were not observed to be active after May 10th.

Table 1 A summary of L. nigrinus survival, feeding activity, and oviposition estimates in the Wrst and second Weld seasons Sample period Year 1 Study (2001) February–May Year 2 study (2002) November–January February–April

Adult survival % (§SE)

Sistens consumed per day per adult (§SE)

Mean progeny per branch d (§SE)

Mean progeny per adult d (§SE)

Refer to Fig. 1

4.3 § 0.6b

30.4 § 5.3

19.5 § 3.8b

88.9 § 3.2aa 55.3 § 6.9b

3.3 § 1.6c 5.8 § 2.1c

0.9 § 0.3a 93.2 § 8.9b

0.22 § 0.1c 21.5 § 1.9c

a

DiVerent letters within each column indicate signiWcant diVerences between sample periods in 2nd year study (F D 20.29, df D 1, 31, P < 0.001 (adult survival), F D 86.79, df D 1, 31, P < 0.001) (progeny per branch). b All adults are female, units are reported in per female L. nigrinus. c All adults are unsexed, thus units are reported in per adult L. nigrinus. d Progeny includes eggs and larvae.

decrease of sistens on branches with and without predators was attributed solely to L. nigrinus and used to calculate adult feeding rate. In the Wrst Weld season, we estimate that L. nigrinus females consumed an average of 4.3 § 0.6 sistens per day from February to April. In the second Weld season, adults consumed an estimated average of 3.3 § 1.6 sistens per day from November to January and 5.8 § 2.1 sistens per day from February to April. The increased rate of consumption in the spring is likely due to warmer temperatures and the combination of L. nigrinus adult and their late instar progeny feeding. The ovipositional activity of L. nigrinus was comparable in the Wrst and second Weld seasons; the maximum number of progeny per branch was 164 and 152, respectively. The mean number of progeny is higher in the second year (Table 1), but the sample period was longer and there were more adults on the branches than in the Wrst year. One of the drawbacks of starting in November is

that the adults could not be sexed because females were not ovipositing (Zilahi-Balogh et al., 2003b). Therefore, all data for the second year are reported in per beetle units, rather than per female units, as was done in the Wrst year. In addition, predator feeding and oviposition results were increasingly impacted decreasing prey abundance as the Wrst Weld season progressed (Fig. 2). Estimating the total number of adelgids eaten by each predator helps determine the potential feeding capacity of L. nigrinus, but provides little information on its relative impact on a speciWc population of adelgids. Fig. 3 shows the total decrease in sistens as a proportion of the original number, and this may be a better measure of potential level of control by L. nigrinus adults. The proportional decrease in adelgid populations was signiWcantly greater on branches with L. nigrinus adults than branches without L. nigrinus in both sample periods (F D 24.64, df D 2, 46, P < 0.0001). The impact of L. nigrinus

A.B. Lamb et al. / Biological Control 32 (2005) 200–207

Fig. 3. The mean percent reduction in sistens per sample period on sleeved branches with and without L. nigrinus (§SE) in year 2 of study. Means with the same letter, within sample period, are not signiWcantly diVerent from each other (F D 24.64, df D 2, 46, P D 0.0001). Sample period had a signiWcant eVect on mean percent reduction of sistens (F D 45.67, df D 2, 46, P D 0.0001).

on adelgid populations was greater in the February– April sample period than in the November–January sample period (F D 45.67, df D 2, 46, P < 0.0001). This is likely attributable to increased temperatures in the spring and perhaps the additive impact of late instar feeding on sistens. The cause of adelgid mortality on control branches was not determined but is probably due primarily to overwintering mortality. This study indicates that the activity period of L. nigrinus in Virginia is similar to its activity period in its native range (Zilahi-Balogh et al., 2003a) and is well synchronized with the life cycle of HWA in Virginia (Gray and Salom, 1996). L. nigrinus adults were active and fed on sistens nymphs throughout the fall and winter and oviposited in sistens ovisacs in late winter to early spring. Laricobius nigrinus had a signiWcant impact on adelgid populations in both the pre-oviposition period from November to January, and during the oviposition period from February to April. Of special interest is the early season impact (November–March), when no other known biotic mortality agents of HWA are present. Thus, the impact of L. nigrinus adults during the fall and winter should complement the actions of other predators, such as S. tsugae and S. ningshanensis (Coleoptera: Coccinellidae), that become active later in the spring (Cheah and McClure, 2000; Montgomery et al., 2002). S. tsugae adults are present on hemlocks year round, but only become active later in the spring, ovipositing when temperatures rise above 15 °C, resulting in larval activity from May to September (Cheah and McClure, 2000). Butin et al. (2003) found that the period of peak oviposition of S. tsugae diVers from year to year. The Chinese coccinellid, S. ningshanensis, becomes active at temperatures above 7 °C and oviposits for several weeks beginning in May (Butin et al., 2003; Montgomery et al., 2002). In a caged Weld study conducted from May to July, adelgid populations were reduced by S. ningshanensis but increased in cages with S. tsugae (Butin et al., 2003). Other studies indicated that adelgid populations have been reduced following S. tsugae release in the Weld (Cheah and McClure, 1998).

205

A Laricobius species has been employed in a biological control program in the past. Laricobius erichsonii Rosenhauer, a European species, is one of several predators that were introduced into the eastern and western US for the control of balsam woolly adelgid (BWA), Adelges piceae (Ratz.) on Abies spp. Clark and Brown (1958) caged L. erichsonii on Abies spp. to study the impact they had on BWA populations. L. erichsonii reduced adelgid populations by 61%, compared with control cages where BWA populations increased by 186% (Clark and Brown, 1958). Although L. erichsonii performed well in Weld cages and was recovered at most release sites in the following decade, no measurable control of BWA was recorded (BuVam, 1962). The biological control program for BWA is not considered to be successful (Schooley et al., 1984). Many predator species were released prior to screening (Amman and Speers, 1971). With such a diverse array of predator species released, there are many possible causes for their failure to establish. Few species were chosen for release based on their biological attributes. Laboratory studies were conducted on few species released in North Carolina, and of 20+ species, only one hemipteran oviposited on Fraser Wr, Abies fraseri (Pursh) (Amman and Speers, 1971). Some species may have been in competition with each other or were merely unsuited to the environment. In addition, the number of individual predators released was often low; for example, only 1, 700 L. erichsonii were released in North Carolina (BuVam, 1962). Amman and Speers (1971) suggested that most predator species were unable to establish because of important diVerences between the old and new environment, and poor prey acceptance by larvae and ovipositing adults. Adelgid predators can be diYcult to recover from the Weld, but surveys to determine which BWA predators are currently established in eastern North America could be insightful and useful for the present HWA program. The importance of long-term monitoring following release is emphasized by Humble (1994), who documented the establishment of Aphidecta obliterata (L.) (Coleoptera: Coccinellidae) on BWA in western North America more than 20 years after its initial release. Tsuga spp. may have an advantage over balsam Wr, Abies balsamea (L.), and fraser Wr, A. fraseri. Since Tsuga spp. grow in a milder climate than these Abies spp., the environment may be more conducive to predator establishment. In addition, there has been no documentation of HWA injecting toxic saliva into Tsuga spp. (Young et al., 1995) like BWA does in Abies spp. (Hollingsworth et al., 1991; Puritch, 1971). Thus, Tsuga spp. may be able to withstand greater adelgid populations than Abies spp. without incurring injury. Determination and use of predators that provide an additive impact is the most promising way to reduce HWA populations below levels injurious to Tsuga spp.

206

A.B. Lamb et al. / Biological Control 32 (2005) 200–207

A complex of predator species with ecologically distinct requirements will facilitate an additive predator impact and will likely be required to control HWA across the wide geographic range and variable environment in which Tsuga spp. grow. L. nigrinus may be especially important in controlling HWA because it is active so early in the year. The combined eVect of adult consumption of sistens and larval feeding on eggs laid by sistens ultimately reduces the density of the progrediens generation, which will likely complement and enhance the impact of other predators on adelgid populations. The data collected in this study demonstrate that L. nigrinus is a promising biological control agent for HWA. Since this predator can survive, reproduce, and impact adelgid populations in Weld cages, the next phase is to evaluate its impact and ability to establish following open releases.

Acknowledgments The authors are indebted to Holly Gatton and Linda Ferguson for their technical assistance in the laboratory. We thank Drs. Gabriella Zilahi-Balogh, Lee Humble, and Edwin Lewis for helpful discussions and reviewing an earlier version of the manuscript. The Canadian Forest Service is acknowledged for assisting and supporting the collection and importation of L. nigrinus. We are grateful to the Blacksburg Ranger District of the JeVerson and Washington National Forest, the Mountain Lake Nature Conservancy, and the Mountain Lake Biological Station for allowing this work to be conducted on their land. This project was supported Wnancially by the USDA Forest Service, FHP, Special Technology Development Program to S.M.S. and L.T.K.

References Amman, G.D., Speers, C.F., 1971. Introduction and evaluation of predators from India and Pakistan for control of the balsam woolly aphid (Homoptera: Adelgidae) in North Carolina. Can. Entomol. 103, 528–533. Baumgras, J.E., Sendak, P.E., Sonderman, D.L., 1999. Ring shake in eastern hemlock: frequency and relationship to tree attributes. In: McManus, K.A., Shields, K.S., Souto, D.R. (Eds.), Proceedings of the Symposium on Sustainable Management of Hemlock Ecosystems in Eastern North America. USDA For. Serv. Gen. Tech. Rep. NE-267, pp. 156–160. BuVam, P.E., 1962. Observations on the eVectiveness and biology of the European predator Laricobius erichsonii Rosen. (Coleoptera: Derodontidae) in Oregon and Washington. Can. Entomol. 94, 461–472. Butin, E., Elkington, J., Havill, N., Montgomery, M., 2003. Comparison of numerical response and predation eVects of two coccinellid species on hemlock woolly adelgid (Homoptera: Adelgidae). J. Econ. Entomol. 96, 763–767. Cheah, C.A.S.-J., McClure, M.S., 1996. Exotic natural enemies of Adelges tsugae and their prospect for biological control. In: Salom, S.M., Tigner, T.C., Reardon, R.C. (Eds.), Proceedings of the First

Hemlock Woolly Adelgid Review. USDA For. Serv. FHTET 96-10, pp. 103–112. Cheah, C.A.S.-J., McClure, M.S., 1998. Life history and development of Pseudoscymnus tsugae (Coleoptera: Coccinellidae), a new predator of the hemlock woolly adelgid (Homoptera: Adelgidae). Environ. Entomol. 27, 1531–1536. Cheah, C.A.S.-J., McClure, M.S., 2000. Seasonal synchrony of life cycles between the exotic predator, Pseudoscymnus tsugae (Coleoptera: Coccinellidae) and its prey, the hemlock woolly adelgid Adelges tsugae (Homoptera: Adelgidae). Agric. For. Entomol. 2, 241– 251. Cheah, C.A.S.-J., Montgomery, M.S., Salom, S.M., Parker, B., Skinner, M., Reardon, R., 2004. Biological control of the hemlock woolly adelgid. USDA For. Serv. FHTET-2004-04. Clark, R.C., Brown, N.R., 1958. Studies of predators of the balsam woolly aphid, Adelges piceae (Ratz.) (Homoptera: Adelgidae). V. Laricobius erichsonii Rosen. (Coleoptera: Derodontidae), an introduced predator on eastern Canada. Can. Entomol. 90, 657–672. DeBach, P., Fleschner, C.A., Dietrick, C.A., 1951. A biological check method for evaluating the eVectiveness of entomophagous insects. J. Econ. Entomol. 44, 763–766. Gray, D.R., Salom, S.M., 1996. Biology of the hemlock woolly adelgid in the southern Appalachians. In: Salom, S.M., Tigner, T.C., Reardon, R.C. (Eds.), Proceedings of the First Hemlock Woolly Adelgid Review. USDA For. Serv. FHTET 96-10, pp. 26–32. Hollingsworth, R.G., Blum, U., Hain, F.P., 1991. The eVect of adelgidaltered wood on sapwood and conductance of Fraser Wr Christmas trees. IAWA Bull. 12, 235–239. HuVaker, C.B., Kennett, C.E., 1969. Some aspects of assessing eYciency of natural enemies. Can. Entomol. 101, 425–446. Humble, L.M., 1994. Recovery of additional exotic predators of balsam woolly adelgid, Adelges piceae (Ratzeburg) (Homoptera: Adelgidae), in British Columbia. Can. Entomol. 126, 1101–1103. Lawrence, J.F., Hlavac, T.F., 1979. Review of the Derodontidae (Coleoptera: Polyphaga) with new species from North America and Chile. Coleop. Bull. 33, 369–414. McClure, M.S., 1987. Biology and control of hemlock woolly adelgid. Ct. Ag. Exp. Sta. Bull. No. 851. McClure, M.S., 1989. Evidence of a polymorphic life cycle in the hemlock woolly adelgid, Adelges tsugae (Homoptera: Adelgidae). Ann. Entomol. Soc. Am. 82, 50–54. McClure, M.S., 1990. Role of wind, birds, deer, and humans in the dispersal of hemlock woolly adelgid (Homoptera: Adelgidae). Environ. Entomol. 19, 36–43. McClure, M.S., 1991. Density-dependent feedback and population cycles in Adelges tsugae (Homoptera: Adelgidae). Environ. Entomol. 19, 36–43. McClure, M.S., 1992. Hemlock woolly adelgid. Am. Nurseryman 176, 82–86. McClure, M.S., 1996. Natural enemies of adelgids in North America: their prospect for biological control of Adelges tsugae (Homoptera: Adelgidae). In: Salom, S.M., Tigner, T.C., Reardon, R.C. (Eds.), Proceedings of the First Hemlock Woolly Adelgid Review. USDA For. Serv. FHTET 96–10, pp. 89–101. McClure, M.S., Salom, S.M., Shields, K.S., 1996. Hemlock Woolly Adelgid. USDA For. Serv. FHTET 96-35. McClure, M.S., Cheah, A.S.-J., Tigner, T.C., 1999. Is Pseudoscymnus tsugae the solution to the hemlock woolly adelgid problem? an early perspective. In: McManus, K.A., Shields, K.S., Souto, D.R. (Eds.), Proceedings of the Symposium on Sustainable Management of Hemlock Ecosystems in Eastern North America. USDA For. Serv. Gen. Tech. Rep. NE-267, pp. 89–96. Montgomery, M.S., Wang, H., Yao, D., Lu, W., Havill, N., Li, G., 2002. Biology of Scymus ningshanensis (Coleoptera: Coccinellidae): a predator of Adelges tsugae (Homptera: Adelgidae). In: Onken, B., Reardon, R., Lashomb, J. (Eds.), Proceedings: Symposium on the Hemlock Woolly Adelgid in Eastern North America, 5–7 February

A.B. Lamb et al. / Biological Control 32 (2005) 200–207 2002, East Brunswick, New Jersey. USDA For. Serv. Pub., pp. 181–188. Parker, B.L., Skinner, M., Gouli, S., Ashikaga, T., Teillon, H.B., 1999. Low lethal temperature for hemlock woolly adelgid (Homoptera: Adelgidae). Environ. Entomol. 28, 1085–1091. Puritch, G.S., 1971. Water permeability of the wood of grand Wr, Abies grandis Doug. Lindl. in relation to infestation by the balsam woolly aphid, Adelges piceae Ratz. J. Exp. Bot. 22, 936–945. Salom, S.M., Sharov, A.A., Mays, W.T., Gray, D.R., 2002. InXuence of temperature on development of hemlock woolly adelgid (Homoptera: Adelgidae) progrediens. J. Entomol. Sci. 37, 166–176. Schooley, H.O., Harris, J.W.E., Pendrel, B., 1984. Adelges piceae (Ratz.), balsam woolly adelgid (Homoptera: Adelgidae). In: Kelleher, J.S., Hulme, M.A. (Eds.), Biological Control Programmes Against Insects and Weeds in Canada 1969–1980. Commonwealth Agricultural Bureau, Farnham Royal, Slough, UK, pp. 229–234. SAS Institute, 1992. SAS/STAT User’s Guide. SAS Institute, Cary, NC. Wallace, M.S., Hain, F.P., 2000. Field surveys and evaluation of native and established predators of the hemlock woolly adelgid (Homoptera: Adelgidae) in the southeastern United States. Environ. Entomol. 29, 638–644. Yorks, T.E., Jenkins, J.C., Leopold, D.J., Raynal, D.J., Orwig, D.A., 1999. InXuences of eastern hemlock mortality on nutrient cycling. In: McManus, K.A., Shields, K.S., Souto, D.R. (Eds.), Proceedings

207

of the Symposium on Sustainable Management of Hemlock Ecosystems in Eastern North America. USDA For. Serv. Gen. Tech. Rep. NE-267, pp. 126–133. Young, R.F., Shields, K.S., Berlyn, G.P., 1995. Hemlock woolly adelgid (Homoptera: Adelgidae): stylet bundle insertion and feeding sites. Ann. Entomol. Soc. Am. 88, 827–835. Zilahi-Balogh, G.M.G., 2001. Biology of Laricobius nigrinus Fender (Coleoptera: Derodontidae) and its potential as a biological control agent of the hemlock woolly adelgid, Adelges tsugae Annand (Homoptera: Adelgidae) in the eastern United States. PhD dissertation, Virginia Polytechnic Institute and State University, Blacksburg, Virginia. Zilahi-Balogh, G.M.G., Kok, L.T., Salom, S.M., 2002. Host speciWcity tests of Laricobius nigrinus Fender (Coleoptera: Derodontidae), a biological control agent of the hemlock woolly adelgid, Adelges tsugae (Homoptera: Adelgidae). Biol. Control 24, 192–198. Zilahi-Balogh, G.M.G., Humble, L.M., Lamb, A.B., Salom, S.M., Kok, L.T., 2003a. Seasonal abundance and synchrony between Laricobius nigrinus fender (Coleoptera: Derodontidae) and its prey, the hemlock woolly adelgid, Adelges tsugae (Homoptera: Adelgidae) in British Columbia. Can. Entomol. 135, 103–115. Zilahi-Balogh, G.M.G., Salom, S.M., Kok, L.T., 2003b. Development and reproductive biology of Laricobius nigrinus, a potential biological control agent of Adelges tsugae. Biocontrol 48, 293–306.