Biological Control of Pests in Forests of Eastern United States

 

 

HEMLOCK WOOLLY ADELGID
(Adelges tsugae)

Mike Montgomery, USDA FS, Northern Forest Unit, Hamden, Connecticut memontgomery@fs.fed.us

Scott Salom, L. T. Kok, David Mausel, Ashley Lamb, Virginia Tech, Blacksburg, VA, salom@vt.edu; Ltkok@vt.edu; dmausel@vt.edu; aslamb@vt.edu

Joe Elkinton, Roy Van Driesche, University of Massachusetts, Amherst elkinton@ent.umass.edu, vandries@nre.umass.edu

Range in North America and Pest Origin

Hemlock woolly adelgid (HWA) (Adelges tsugae Annand) (Adelgidae) occurs in two separate parts of North America. In the the Pacific Northwestern states of the USA and in western Canada, the species is likely to be native, being first noted in the 1920s (Annand, 1924). In the eastern USA, the species is found from Georgia to Massachusetts (Fig. 2). In this area, the species is invasive and its range is expanding. It has not yet reached the western and northern portions of the range of eastern hemlock, and is limited in the north by lack of tolerance to extreme winter cold. Voucher specimens in the United States National Museum indicate that HWA was first collected in eastern North America in Richmond, Virginia in 1951, where is was collected on ornamental hemlocks. While HWA is native to both the western USA, Japan and China, the strain found in the eastern USA has been shown by DNA analyses to have come from Japan (Havill et al., 2006)

Fig. 2. Range of hemlock woolly adelgid in the eastern United States (as of 2006) (USDA Forest Service, Northeastern Area, Hamden, Connecticut;Forestryimages.org)

Damage

In western North America, HWA is not damaging to forest hemlock stands. In the eastern United States, HWA kills hemlocks and has degraded hemlock health severely from Connecticut, southward along the Appachians to at least South Carolina. Loss of hemlock deprives species dependent on cool forest conditions of critical habitat. Ecological effects of hemlock loss on other species have been studied in the Delaware Water Gap National Recreation Area in New Jersey and Pennsylvania (Evans, 2002). With loss of hemlock, stands shift to decidous trees less able to mantain cool habitats and cool stream temperatures. This leads to losses of some species dependent on such habitats and a decline in native trout in associated streams.

Resident Natural Enemies

Adeligids as a group lack parasitoids (Zilahi-Balogh et al., 2002a), but are attacked by a set of specialized predators in the Coccinellidae (Scymnus spp.), Derodontidae (Laricobius spp.), and Chamaemyiidae (Leucopis spp.). Also, generalist predators such as other coccinellids (e.g., Harmonia axyridis), syrphids, cecidomyiids (Aphidoletes, Lestodiplosis) and chrysopids are present in the eastern United States on hemlock foliage and might consume some HWA life stages.

Surveys for native or previously established imported natural enemies of HWA have been conducted by McClure (1987) and Montgomery and Lyon (1996) in Connecticut and by Wallace and Hain (2000) in North Carolina and Virginia. Species of Cecidomyiidae, Syrphidae, and Chrysopidae were found associated with HWA by McClure (1987), but densities were too low to reduce adelgid populations.  Surveys by Montgomery and Lyon (1996) on HWA-infested eastern hemlock growing together with eastern white pine and Scotch pine (Pinus sylvestris L.) recovered Scymnus suturalis Thunberg (Coleoptera: Coccinellidae), Laricobius rubidus, and a brown lacewing (Hemerobiidae). On Pineus strobi-infested eastern white pine, S. suturalis and Laricobius rubidus, Leucopis (Neoleucopis) sp. (Chamaemyiidae), and a Tetraphleps sp. (Anthocoridae) were recovered.  Both S. suturalis and L. rubidus were abundant on pine and hemlock (Montgomery and Lyon, 1996).  Scymnus suturalis is of European origin and was introduced into Michigan in the 1960s (Montgomery and Lyon, 1996). Surveys by Wallace and Hain (2000) in three forested sites over two years in northern North Carolina and southern Virginia on HWA-infested eastern hemlock recovered Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae); Chrysoperla harrisii (Fitch) (Chrysopidae); Hemerobius humulinus L. and Hemerobius sp.  (Hemerobiidae); Aphidoletes abietis Kieffer, Aphidoletes aphidimyza Rondani, Aphidoletes sp., Lestodiplosis sp., and Trisopsis sp. (Diptera: Cecidomyiidae); Leucopis sp.; species of Syrphidae; and L. rubidus.  Predators were collected in very low numbers in both years. Overall, H. axyridis, Neuroptera, and Cecidomyiidae were most abundant.  Cage exclusion experiments indicated that these predators had no significant effects on the density of HWA populations (Wallace and Hain, 2000).

Biological Control Efforst Against the Pest

Because HWA is extremely damaging to the ecology of hemlock communities and because native or previously introduced natural enemies in the eastern U.S. have shown little ability to reduce HWA populations, a project of classical biological control was begun to introduce additional promising species of predators from western North America and Asia to the eastern United States.  Since the early 1990s, several coccinellids and derodontid beetles have been investigated (and some species introduced to the eastern United States) that have potential as biological control agents of HWA (Cheah and McClure, 1998; McClure et al., 2000; Montgomery et al., 2000; Lu and Montgomery, 2001; Zilahi-Balogh et al., 2002b; 2003ab). Natural enemies that have been imported previously and an assessment of their status follows.

Sasajiscymnus tsugae (Sasaji and McClure). This species (Fig. 3) is associated with HWA populations in Japan but also occurs in marshes (McClure, 1995; Sasaji and McClure, 1997). Its original genus name, Pseudoscymnus, was subsequently noted to be occupied, and was subsequently changed to Sasajiscymnus (Vandenberg, 2004). This species is multivoltine and relatively easy to mass rear. It has been released in most HWA-infested states from Georgia to New Hampshire and is considered to be established in seven states (McClure et al., 2000; Palmer and Sheppard, 2002; Blumenthal, 2002). In sleeve cages, it was found to have little impact on HWA population increase compared with Scymnus ningshanensis Yu et Yao (Butin et al., 2003ab). Between year impact on HWA densities in the field has not been demonstrated (Casagrande et al., 2002; Cheah and McClure, 2002), despite some positive indications of impact during the year of release at some sites (Casagrande et al., 2002; McClure et al., 2000). Some improvement in hemlock health has occurred at release sites but high winter mortality of HWA may be the cause (Cheah et al., 2005). To date more than one million of this species has been released and while it is clearly established  further monitoring is needed to determine if its impact is significant.

Fig. 3. Sasajiscymus tsugae (photo by Carol Cheah, CT Agric. Exp Station; Forestryimages.org)

Laricobius nigrinus Fender (Fig. 4) was described from specimens found in the Pacific Northwest (Oregon and interior British Columbia) (Fender, 1945).  It is presumed to be a native species in long association with HWA. In British Columbia, L. nigrinus exhibits good synchrony with the life cycle of HWA, aestivating when HWA aestivates and resuming activity in the fall in time for adult L. nigrinus to feed on developing sistens through the winter (Zilahi-Balogh et al., 2003ab).  Subsequently, single eggs are deposited into sistens’ ovisacs (Fig. 5) as progrediens’ eggs are oviposited, and hatching predator larvae feed on the eggs.  In laboratory host specificity tests, L. nigrinus showed a preference to oviposit in HWA ovisacs and in feeding tests consumed more eggs of HWA than of other test species (except for Adelges abietis [L.]) (Zilahi-Balogh et al., 2002b). This predator completed its development only on HWA.  Methods for moderate scale, efficient mass rearing have been developed (Lamb et al., 2005a). Cage studies have documented survival and reproduction of this predator on HWA under field conditions in the eastern United States (Lamb et al., 2005b). Field releases were begun in fall 2003 in Virginia. This species has established at at least half of 25 release sites, and reproduction through as many as four generations has been observed (Mausel, unpub.). This species is now clearly established and spreading in the Appalachian region of the Middle Atlantic states (Georgia to Pennsylvania). This biotype of L. nigrinus (designated as the martime strain, reflecting its collection point near Seattle, Washington) may lack tolerance of winter temperatures in the northern parts of HWA's range. Another population of this species has been identified in northern Idaho (Mausel, unpub.) that may be better adapted to temperatures in New England. Its collection and release in Massachusetts and Connecticut is anticipated.

Fig. 4. Laricobius nigrinus (Photo by Ashley Lamb, Virginia Tech; Forestryimages.org)

Fig. 5. Laricobius nigrinus egg (yellow) amid wool and red eggs of HWA (Photo by Ashley Lamb, Virginia Tech; Forestryimages.org)

Laricobius species from Asia. Several apparently new and undescribed species in this genus have been recovered from HWA-infested hemlocks in Asia.  In 1994, 62 specimens of a new species were collected in Kaohsing County, Taiwan in late May (Murphy, 1995).  These were shipped to the Forest Service Quarantine Laboratory in CT but were all dead shortly after arrival.  The high numbers collected in a few hours indicate that this is an important predator. Two new Laricobius beetles were also recovered in Sichuan Province, China in 2002 and 2004 (Zilahi-Balogh et al., 2007). Although not as abundant, these merit further study because this genus specializes on Adelgidae. In 2006, another new Laricobius species was collected in Japan from HWA-infested hemlock and is currently in culture in Viriginia (Lamb, unpub). Host range assessments are underway, with the intention of introducing this Japanese species as soon as possible.

Scymnus species from China. Many species (> 50) of coccinellids have been found on hemlock in China in association with HWA, of which at least nine are known to feed considerably on HWA (Montgomery et al., 2000; Yu et al., 2000; Yu, 2001).  Three species (in the subgenus Neopullus) have been studied extensively: Scymnus camptodromus, S. sinuanodulus (Ss) , and S. ningshanensis (Sn) .  Based on abundance and observed adelgid specificity in their native habitat, these species have been imported for further study, and two (Ss and Sn) have been released.

(a) Scymnus camptodromus (Sc). This was the first species studied and imported from China. It feeds voraciously on HWA in the laboratory in China (Zhao et al., 1998). Laboratory colonization has been difficult because of an egg diapause (Lu and Montgomery, 2000).  This problem as recently been resolved and future release of this species is anticipated, as it seems to have several advantages, including an earlier larval feeding period than other Scymnus species under study (leading to potentially higher impacts of HWA).

(b) Scymnus sinuanodulus (Ss) . This univoltine species (Fig. 6), which feeds on several HWA life stages, especially eggs, was the most common predator found in association with HWA in surveys in China (Montgomery et al., 1998). Its larvae and pupae have been described by Lu et al. (2002). It was imported into USDA Forest Service Quarantine Laboratory in 1996 and parameters of its fecundity and development rate have been quantified (Lu and Montgomery, 2001). Eggs are laid early in the spring with a second peak later in the season. It was widely distributed in three counties in Lijiang Prefecture, Yunnan Province with an average of 0.7 beetles per 0.5 m of HWA-infested hemlock branch in some areas.  It was found most frequently on HWA-infested hemlock but was also found in association with Pineus armandi on white pine. This beetle was not found in association with various aphids, scales, and other Homoptera, suggesting host specificity to adelgids.  In laboratory host range tests, it showed a clear preference for HWA but also fed on eggs and nymphs of the adelgid Pineus strobi (Hartig) and nymphs of the aphid Myzocallis tiliae (L.) (Montgomery et al., 1998).  Field sleeve cage studies suggest that the species can significantly reduce HWA population increase (Montgomery et al., 2003). This species was released into the environment for the first time in Georgia in 2004 (Montgomery, pers. comm.), with additional releases subsequently.

Fig. 6. Scymnus sinuanodulus adult (Photo by Guoyue Yu)

(c) Scymnus ningshanensis (Sn) . This species (Fig. 7) is univoltine and feeds on eggs and other stages of HWA (Fig. 8) (Wang et al., 2000). It was collected at sites further north in China, where the climate is more comparable to that of CT (Montgomery et al., 2002).  Its host range has been assessed (Butin et al., 2002) and is relatively narrow (mostly adelgids, limited feeding on aphids). In sleeve cage trials, this species suppressed HWA population growth under conditions where S. tsugae failed to do so (Butin et al., 2003ab). Field releases of this species in field cages were made in Massachusetts in 2006 and open field releases are planned for April of 2007 in Massachusetts and Connecticut.

Fig. 7. Scymnus ningshanensis adults mating (Photo by Lynn Jones and Nathan Havill; Forestryimages.org)

Fig. 8. Scymnus ningshanensis larva feeding on HWA (Photo by Lynn Jones and Nathan Havill; Forestryimages.org)

Hemiptera.  Tetraphleps parallelus, T. galchanoides, and Anthocoris alpinus (Anthocoridae) were recorded as predators of HWA in China in 1997 (Wang et al. 1998).  In a shipment of HWA-infested hemlock foliage sent from Niba Gou Forestry Farm near Quiaoji, Baoxing, Co., Sichuan to VA Tech in fall, 2002, approximately 40 early instar nymphs of T. galchanoides were found feeding on HWA (McAvoy et al., 2007).  Ten of these nymphs (9 males and 1 female) completed development on HWA under laboratory conditions.  No F1 generation was produced.  Additionally, Montgomery has observed feeding by a Deraeocoris sp. (Miridae) on HWA in China.  These predacious Hemiptera partially consume HWA nymphs, leaving a characteristic carcass and based on this indicator, Deraeocoris sp. predation rates during the fall on dense populations of HWA in China exceeded 80%.  Tests with alternate prey in China revealed that these Hemiptera at first rejected live aphids when encountered, but would readily consume aphids once feeding on an immobilized aphid had occurred.  The Tetraphleps, Deraecoris, and perhaps other Hemiptera species merit further study, which must include careful evaluation of host specificity.

Diptera.  In Oregon, where HWA is native, the second most abundant predator group found associated with HWA is species of Leucopis flies (Chamaemyiidae) (Ross et al., unpublished).

Current Status

The natural enemies of HWA that have been imported and released in the eastern United States now include Sasajiscymnus tusgae, Scymnus sinuanodulus, Scymnus ningshanensis, and Laricobius nigrinus (maritime source population). Of these, S. tsugae has been widely released by the tens of thousands over many locations. These releases have led to apparent establishment of this species, but no clear evidence of its population increase or impact on HWA exist, apart from some evidence of improvement in tree health. Releases of L. nigrinus from 2003 to present have resulted in establishment at about 50% of all release sites, with evidence of small increases in predator numbers each year following release. HWA densities at release sites has not yet been reduced by L. nigrinus but a monitoring program is underway measuring impacts at a series of sites (Salom laboratory, Virginia Tech). Small, limited releases of Scymnus sinuanodulus began  in 2004 the southern Appalachian Mountains and of Scymnus ningshanensis in 2007 in Massachusetts and Connecticut. These releases will be evaluated over the next few years. Several species of lady beetles and Laricobius beetles are currently in quarantine for evaluation of host range and biology.

References Cited

Annand, P. N. 1924. A new species of Adelges (Hemiptera: Phylloxeridae). Pan-Pacific Entomologist 1: 79-82.

Blumenthal, E. M. 2002. Report: Pseudoscymnus tsugae in Pennsylvania forests, pp. 166-169. In: B. Onken, R. Reardon, and J. Lashomb (eds.). Proceedings: Hemlock Woolly Adelgid in the Eastern United States Symposium, February 5-7, 2002, East Brunswick, New Jersey.  USDA Forest Service and New Jersey Agricultural Experiment Station Publication.

Butin, E., M. Montgomery, N. Havill, and J. Elkinton. 2002. Pre-release host range assessment for classical biological controls: experience with predators for the hemlock woolly adelgid, pp. 205-213. In: B. Onken, R. Reardon, and J. Lashomb (eds.). Proceedings: Hemlock Woolly Adelgid in the Eastern United States Symposium, February 5-7, 2002, East Brunswick, New Jersey.  USDA Forest Service and New Jersey Agricultural Experiment Station Publication.

Butin, E., J. Elkinton, N. Havill, and M. E. Montgomery. 2003a. Comparison of numerical response and predation effects of two coccinellid species on hemlock woolly adelgid (Homoptera: Adelgidae). Journal of Economic Entomology 96: 763-767.

Butin, E., J. Elkinton, N. Havill, and M. E. Montgomery. 2003b. Comparative impact of Scymnus ningshanensis and Pseudoscymnus tsugae (Coleoptera: Coccinellidae) on the hemlock woolly adelgid, p. 14. In: Fosbroke, S. L. C. and K. W. Gottschalk (eds.). Proceedings of the USDA Interagency Research Forum on Gypsy Moth and other Invasive Species 2002, January 15-18, 2002. Annapolis, Maryland, USA, USDA Forest Service General Technical Report NE-300.

Casagrande, R. A., M. DeSanto, J. Dacey, and A. Lambert. 2002. Pseudoscymnus tsugae for biological control of the hemlock woolly adelgid in suburban setting, pp. 170-180. In: B. Onken, R. Reardon, and J. Lashomb (eds.). Proceedings: Hemlock Woolly Adelgid in the Eastern United States Symposium, February 5-7, 2002, East Brunswick, New Jersey.  USDA Forest Service and New Jersey Agricultural Experiment Station Publication.

Cheah, C. A. and M. S. McClure.  1998.  Life history and development of Pseudoscymnus tsugae (Coleoptera: Coccinellidae), a new predator of the hemlock woolly adelgid (Homoptera: Adelgidae).  Environmental Entomology 27: 1531-1536.

Cheah, C. A. and M. S. McClure. 2002. Pseudoscymnus tsugae in Connecticut forests: the first five years, pp. 150-165. In: B. Onken, R. Reardon, and J. Lashomb (eds.). Proceedings: Hemlock Woolly Adelgid in the Eastern United States Symposium, February 5-7, 2002, East Brunswick, New Jersey.  USDA Forest Service and New Jersey Agricultural Experiment Station Publication.

Cheah, C.A.S.-J., M. A. Mayer, D. Palmer, T. Scudder, and R. Chianese. 2005. Assessments of biological control of hemlock woolly adelgid with Sasjiscymnus tsugae in Connecticut and New Jersey, pp. 116-130. In: Onken, B. and R. Reardon (Compilers). 3rd Symposium on Hemlock Woolly Adelgid in the Eastern United States. Asheville, NC. FHTET-2005-01.

Evans, R. A. 2002. An ecosystem unraveling? pp. 23-33. In: Onken, B., R. Reardon, and J. Lashomb (eds.). Proceedings: Hemlock Woolly Adelgid in the Eastern United States Symposium, February 5-7, 2002. East Brunswick, New Jersey, The State University of New Jersey, Rutgers, New Jersey.

Fender, K. M. 1945. A new Laricobius from Oregon (Coleoptera: Derodontidae) Pan-Pacific Entomologist 21: 152.

Havill, N. P., M. E. Montgomery, Guoyue Yu, S. Shiyake, and A. Caccone. 2006. Mitochondrial DNA from hemlock woolly adelgid (Hemiptera: Adelgidae) suggests cryptic speciation and pinpoints the source of the introduction to eastern North America. Annals of the Entomological Society of America 99: 195-203.

Lamb, A. B., S. M. Salom, and L. T. Kok. 2002. Field evaluation and improvement of rearing procedures for Laricobius nigrinus Fender (Coleoptera: Derodontidae), a predator of hemlock woolly adelgid, pp. 189-196. In: B. Onken, R. Reardon, and J. Lashomb (eds.). Proceedings: Hemlock Woolly Adelgid in the Eastern United States Symposium, February 5-7, 2002, East Brunswick, New Jersey.  USDA Forest Service and New Jersey Agricultural Experiment Station Publication.

Lamb, A. B., S. M. Salom, and L. T. Kok. 2005a. Guidelines for rearing Laricobius nigrinus Fender, pp. 309-318. In: Onken, B. and R. Reardon (Compilers). 3rd Symposium on Hemlock Woolly Adelgid in the Eastern United States. Asheville, NC. FHTET-2005-01.

Lamb, A. B., S. M. Salom, and L. T. Kok. 2005b. Survival and reproduction of Laricobius nirgrinus Fender (Coleoptera: Derodontidae), predator of hemlock woolly adelgid, Adelges tsugae Annand (Homoptera: Adelgidae) in field cages. Biological Control 32: 200-207.

Lu, W. and M. E. Montgomery. 2000. Comparative biology of three Scymnus lady beetles (Coleoptera: Coccinellidae): predators of Adelges tsugae (Homoptera: Adelgidae), pp. 188. In McManus, K. A., K. S. Shields, and D. R. Souto (eds.). Proceedings of a Symposium on Sustainable Management of Hemlock Ecosystems in Eastern North America, 22-24 June, 1999, Durham, New Hampshire. USDA Forest Service, Newtown Square, Pennsylvania, USA.

Lu, W. and M. E. Montgomery. 2001. Oviposition, development and feeding of Scymnus (Neopullus) sinuanodulus (Coleoptera: Coccinellidae): a predator of Adelges tsugae (Homoptera: Adelgidae).  Annals of the Entomological Society of America 94:  64-70.

Lu, W., P. Souphanya, and M. E. Montgomery. 2002. Descriptions of immature stages of Scymnus (Neopullus) sinuanodulus Yu and Yao (Coleoptera: Coccinellidae) with notes on life history. Coleopterists Bulletin 56: 127-141.

McAvoy, T., G. M. Zilahi-Balogh, S. M. Salom, and L. T. Kok. 2007. Development and feeding of Tetraphleps galchanoides Ghauri (Hemiptera: Anthocoridae), a predator of hemlock woolly adelgid. Biocontrol (In press).

McClure, M. S.  1987.  Biology and control of hemlock woolly adelgid.  Connecticut Agriculture Experiment Station Bulletin No. 851.

McClure, M.S. 1995. Using natural enemies from Japan to control hemlock woolly adelgid. Frontiers of Plant Science 47: 5-7.

McClure, M. S., C. A. S-J. Cheah, and T. C. Tigner. 2000. Is Pseudoscymnus tsugae the solution to the hemlock woolly adelgid problem? An early perspective, pp. 89-96. In: McManus, K. A., K. S. Shields, and D. R. Souto (eds.). Proceedings, Symposium on Sustainable Management of Hemlock Ecosystems in Eastern North America, 22-24 June 1999, Durham, NH.. USDA Forest Service General Technical Report NE-267.

Montgomery, M. E. and S. M. Lyon. 1996. Natural enemeis of adelgids in North America: their prospoect for biological control of Adelges tsugae (Homoptera: Adelgidae), pp. 89-102. In: Salom, S. M., T. C. Tigner, and R. C. Reardon (eds.). Proceedings, First Hemlock Woolly Adlegid Review, 1995. Charlottesville, Virgina, USDA Forest Service, FHTET 96-10.

Montgomery, M. E., S. M. Lyon, W. Lu, Y. Defu, and H. Wang. 1998. Developing biological control technology: evaluation of the feeding range of predaceous beetles, pp. 28-34. In Resource Technology 1997: Beijing International Symposium Proceedings. China Forestry Publishing House, Beijing.

Montgomery, M. E., D. Yao, and H. Wang. 2000. Chinese Coccinellidae for biological control of the hemlock woolly adelgid: description of native habitat, pp. 97-102. In: McManus, K. A., K. S. Shields, and D. R. Souto (eds.). Proceedings, Symposium on Sustainable Management of Hemlock Ecosystems in Eastern North America, 22-24 June 1999, Durham, NH. USDA Forest Service General Technical Report NE-267.

Montgomery, M. W., H. Wang, D. Yao, W. Lu, N. Havill, and G. Li. 2002. Biology of Scymnus ningshanensis (Coleoptera: Coccinellidae): a predator of Adelges tsugae (Homoptera: Adelgidae), pp. 181-188. In: B. Onken, R. Reardon, and J. Lashomb (eds.). Proceedings: Hemlock Woolly Adelgid in the Eastern United States Symposium, February 5-7, 2002, East Brunswick, New Jersey.  USDA Forest Service and New Jersey Agricultural Experiment Station Publication.

Montgomery, M. E., N. Havill, C. Cheah, M. McClure, G. Zilahi-Balogh, A. Lamb, and S. Salom. 2003. Hemlock woolly adelgid biological control research, p. 74. In: Fosbroke, S. L. C. and K. W. Gottschalk (eds.). Proceedings of the USDA Interagency Research Forum on Gypsy Moth and other Invasive Species 2002, January 15-18, 2002. Annapolis, Maryland, USA, USDA Forest Service General Technical Report NE-300.

Murphy, S. T. 1995. Insect natural enemy complexes of hemlock dwelling Adelges spp. in Asia and the identification of potential agents for the biological control of A. tsugae in the northeastern USA, pp. 34. International Institute of Biological Control (CABI), Silwood Park, Ascot, Berkshire, United Kingdom.

Palmer, D. J. and J. L. Sheppard. 2002. Mass rearing Pseudoscymnus tsugae at the New Jersey Department of Agriculture: challenges and lessons, pp. 214-220. In: B. Onken, R. Reardon, and J. Lashomb (eds.). Proceedings: Hemlock Woolly Adelgid in the Eastern United States Symposium, February 5-7, 2002, East Brunswick, New Jersey.  USDA Forest Service and New Jersey Agricultural Experiment Station Publication.

Sasaji, H. and M. S. McClure. 1997. Description and distribution of Pseudoscymnus tsugae sp. nov. (Coleoptera: Coccinellidae), an important predator of hemlock woolly adelgid in Japan. Annals of the Entomological Society of America 90: 563-568.

Vandenberg, N. J. 2004. Homonymy in the Coccinellidae (Coleoptera), or something fishy about Pseudoscymnus Chapin. Proceedings of the Entomological Society of Washington 106: 483-484.

Wallace, M.S. and F. P. Hain. 2000. Field surveys and evaluation of native and established predators of the hemlock woolly adelgid (Homoptera: Adelgidae) in the southeastern United States. Environmental Entomology 29: 638-644.

Wang, H., D. Yao, and G. Li. 1998. Investigation on hemlock woolly adelgid and its natural enemies in China, pp. 41-45. In: Resource Technology 1997: Beijing International Symposium sponsored by the Chinese Academy of Forestry and the USDA Forest Service, Resource Technology Institute. China Forestry Publishing House.

Yu, G. 2001. The coccinellids (Coleoptera) predacious on adelgids, with notes on the biocontrol of the hemlock woolly adelgid (Homoptera: Adelgidae). Special Publication of the Japanese Coleoptera Society, Osaka No. 1: 297-304.

Yu, G., M. E. Montgomery, and D. Yao. 2000. Lady beetles (Coleoptera: Coccinellidae) from Chinese hemlocks infested with the hemlock woolly adelgid, Adelges tsugae Annand (Homoptera: Adelgidae). Coleopterists’ Bulletin 54: 154-199.

Zhao, D., H. Guo, J. Zhou, X. Xu, Z. Wang, Y. Meng, and Y. Jiang. 1998. Food consumption of Scymnus camptodromus on hemlock woolly adelgid. Journal of Sichuan Forestry Science 19: 44-46.

Zilalahi-Balogh, G., L. T. Kok, and S. M. Salom. 2002a. A reveiw of world-wide biological control efforts for the family Adelgidae, pp. 129-140, In: Onken, B., R. Reardon, and J. Lashomb (eds.). Proceedings: Hemlock Woolly Adelgid in the Eastern United States Symposium, February 5-7, 2002. East Brunswick, New Jersey, The State University of New Jersey, Rutgers, New Jersey.

Zilahi-Balogh, G. M. G., L. T. Kok, and S. M. Salom. 2002b. Host specificity of Laricobius nigrinus (Coleoptera: Derodontidae), a potential biological control agent of the hemlock woolly adelgid, Adelges tsugae Annand (Homoptera: Adelgidae).  Biological Control 24: 192-198.

Zilahi-Balogh, G. M. G., L. M. Humble, A. B. Lamb, S. M. Salom, and L. T. Kok. 2003a. Seasonal abundance and synchrony between Laricobius nigrinus (Coleoptera: Derodontidae) and its prey, the hemlock woolly adelgid (Hemiptera: Adelgidae). The Canadian Entomologist 135: 103-115.

Zilahi-Balogh, G. M. G., S. M. Salom, and L. T. Kok.  2003b. Development and reproductive biology of Laricobius nigrinus, a potential biological control agent of Adelges tsugaeBiocontrol 48: 293-306.

Zilahi-Balogh, G. M., J. Jelinik, T. McAvoy, S. M. Salom, and L. T. Kok. 2007. Two new species of Laricobius (Coleoptera: Derodontidae) from China, and a key to Laricobius in the southeastern Palaearctic. Proc. Entomol. Soc. Washington (In press).