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Hemlock Woolly Adelgid in the Eastern United States: What Have We Learned?
Evan L. Preisser, Kelly L.F. Oten, and Fred P. Hain

Southeastern Naturalist, Volume 13, Special Issue 6 (2014): 1–15

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1 Hemlock Woolly Adelgid in the Eastern United States: What Have We Learned? Evan L. Preisser1,*, Kelly L.F. Oten2, and Fred P. Hain3 Abstract - Adelges tsugae (Hemlock Woolly Adelgid) is a small piercing-sucking insect that feeds on Tsuga spp. (hemlock ) trees. Native to Asia and the Pacific Northwest, the Hemlock Woolly Adelgid is invasive in the eastern United States where it attacks Tsuga canadensis (Eastern Hemlock) and T. caroliniana (Carolina Hemlock). It is currently found in 19 eastern states and has caused extensive mortality to hemlock forests. The ecological and economic impacts of this pest are significant, widespread, and often difficult to quantify. As the Hemlock Woolly Adelgid continues to disperse throughout the range of Eastern and Carolina Hemlocks, management techniques aimed at controlling it are being researched, implemented, and assessed. This introductory paper provides an overview of the biology, life cycle, ecology, and history of this pest in the eastern US as a foundation for this special issue. Introduction Adelges tsugae Annand (Hemlock Woolly Adelgid, [HWA]) is a small (≈3 mm adult) piercing-sucking insect that feeds on conifers in the genera Tsuga and Picea (Havill and Foottit 2007). The population invasive to the eastern US is native to Japan (Havill et al. 2006). Although HWA has minimal impact on its native host plants (McClure 1997), in the eastern US it has become a major pest of Tsuga canadensis (L.) Carrière (Eastern Hemlock) and T. caroliniana Engelmann (Carolina Hemlock), two species that have little or no defense against this insect (Montgomery et al. 2009). The resulting loss of hundreds of thousands of trees from forests ranging from Georgia to Massachusetts has profoundly affected both local communities and the associated ecosystems (Ellison et al. 2005). This special issue explores HWA impacts and the challenges posed by its invasion. It contains articles surveying the wide range of HWA-related questions researchers are addressing throughout the invaded range. In the following pages, we provide an overview of HWA biology, its interactions with and impacts on other species at the community and ecosystem level, and the current status of control efforts. Biogeography and History of the Invasion Hemlock Woolly Adelgid was first described as a species in the early 1920s from infestations on T. heterophylla Sargent (Western Hemlock) in the northwestern US (Annand 1924). HWA is genetically diverse throughout its native range, with 1Department of Biological Sciences, University of Rhode Island, 9 East Alumni Avenue, Kingston, RI 02881. 2North Carolina Forest Service, Goldsboro, NC 27530. 3Department of Entomology, North Carolina State University, Raleigh, NC 27695. *Corresponding author - Manuscript Editor: John Riggins Forest Impacts and Ecosystem Effects of the Hemlock Woolly Adelgid in the Eastern US 2014 Southeastern Naturalist 13(Special Issue 6):1–15 Southeastern Naturalist E.L. Preisser, K.L.F. Oten, and F.P. Hain 2014 2 Vol. 13, Special Issue 6 different lineages associated with particular regions and host plant species. The HWA population found in the northwestern US is genetically different from the population native to Asia and the invasive population in the eastern US, which originated from low-elevation populations infesting Tsuga sieboldii Carrière (Southern Japanese Hemlock) in central Japan (Havill et al. 2006). In the eastern US, HWA was first reported in the early 1950s near Richmond, VA (Souto et al.1996). Although it was initially thought to be mainly a pest of ornamentals, by the 1980s HWA had also begun to harm forest hemlocks. It is currently found in 19 eastern states, ranging from northern Georgia to southern Maine (USFS 2012). Life Cycle HWA has two generations per year in North America (Fig. 1). In the early spring, first-instar nymphs of the spring generation (progrediens, plural progredientes) emerge and seek out suitable feeding sites in the leaf cushion at the base of hemlock needles (McClure 1989, Oten et al. 2012). These first-instar nymphs are known as crawlers and either move actively on their natal host or are dispersed passively by wind, birds, deer, or humans (McClure 1990, Turner et al. 2011). Once the crawlers find an appropriate feeding site, they settle permanently and use their feeding styletbundle to probe and feed from xylem ray-parenchyma cells (Young et al. 1995). HWAs go through four larval instars before maturing into adults; because North American HWA reproduces asexually, each mature individual is theoretically capable of producing 20–30 summer-generation (sistens, plural sistentes) offspring in early summer (McClure 1989, Paradis 2011). After the summer-generation crawlers Figure 1. Hemlock Woolly Adelgid life cycle. In Japan, the adelgid alternates between Hemlock and Tigertail Spruce. Tigertail Spruce supports a sexual generation and gall formation. In the eastern United States there are only two generations on hemlock because winged migrants do not find suitable spruce species on which to complete the entire life cycle. The letters A and B refer to where the cycle begins again. Vince D’Amico and Nathan Havill created the artwork for this figure. Southeastern Naturalist 3 E.L. Preisser, K.L.F. Oten, and F.P. Hain 2014 Vol. 13, Special Issue 6 settle at the base of new-growth hemlock needles, they aestivate until late fall, when they begin to feed. They feed throughout the winter, and each adult is theoretically capable of producing 50–100 offspring the following spring (Paradis 2011). While the spring generation is the same in HWA’s native and invaded ranges, the summer generation differs substantially between the two areas. Summer-generation eggs hatch into either wingless asexual progrediens that feed on hemlock or winged sexually reproducing sexuparae that feed on Picea torano Carriere (Tigertail Spruce) in the native range (Sato 1999). In the invaded range, however, there are no suitable spruce hosts, and the sexuparae perish without reproducing. As a result, HWA in the eastern US is obligately asexual, and genetic variability is limited. Despite this lack of genetic recombination, however, there is evidence of adaptive genetic variation in cold tolerance in the invaded population (Butin et al. 2005). Population Ecology Although mature HWAs can produce a large number of offspring, both juvenile and adult adelgids also experience high mortality rates (McClure and Cheah 2002). The dispersing crawlers are wingless, passively dispersed, and have a high probability of dispersing to unsuitable habitat. Even under ideal conditions, early-instar mortality rates can approach 90% (Paradis 2011), and adults are susceptible to extreme heat in the summer and periods of intense cold in the winter (Trotter and Shields 2009). Because even low HWA densities substantively affect tree health, survival is highly density-dependent (McClure 1991); the previous generation’s density is the strongest predictor of HWA survival (Paradis 2011). In the invaded range, this density-dependent HWA mortality is compounded by the fact that sexuparae production increases in populations feeding on unhealthy or declining hosts. Both Eastern and Carolina Hemlocks are, however, higher-quality host plants for the invasive HWA population than many hemlock species that have co-evolved with other lineages of the adelgid (Montgomery et al. 2009). This may provide one explanation for why HWA is so abundant in its novel range. Community Ecology HWA has numerous predators in its native range (Cota Vieira et al. 2013, Hakeem et al. 2011, McClure and Cheah 1999), but no predators native to North America appear capable of reducing HWA densities sufficiently to consistently prevent hemlock decline and death (Havill et al., 2012). As a result, HWA’s most important intraspecific interactions likely involve those herbivores that co-occur on its host plant. Although Lambdina fiscellaria Guenee (Hemlock Looper) has historically been considered a major hemlock pest (Trial and Devine 1995), its densities appear to have declined in southern New England (E. Preisser, pers. observ.). In this region, the most commonly co-occurring hemlock herbivore is another invasive Hemipteran, Fiorinia externa Ferris (Elongate Hemlock Scale [EHS]; Preisser et al., 2008). This sessile armored scale feeds on the underside of hemlock needles, reproduces sexually, and has one generation per year in the northeastern US and two Southeastern Naturalist E.L. Preisser, K.L.F. Oten, and F.P. Hain 2014 4 Vol. 13, Special Issue 6 generations annually in the South (Abell and Van Driesche 2012, McClure 1978). Its dispersing crawler stage settles on hemlock foliage in late spring, approximately one month after HWA crawlers have begun feeding; because of this, the adelgid was predicted to competitively exclude the scale from hemlock (McClure 1997). In reality, however, both the range and population density of the scale have increased sharply in HWA-invaded areas of southern New England (Preisser et al. 2008). Because HWA and EHS are both sessile and feed on different plant structures, they interact via their impact on the shared host plant. This fact is important because the two species have very different impacts on plant health; both experimental research (Miller-Pierce and Preisser 2012, Miller-Pierce et al. 2010, Preisser and Elkinton 2008) and landscape surveys (Preisser et al. 2008, 2011) have found that while the EHS can reach higher densities than HWA, the latter species has a greater impact on plant health. Experimental work assessing their interactions on hemlock branches found that each species decreased the other species’ density by ≈30% relative to when the species occur by themselves (Preisser and Elkinton 2008); at the whole-tree level, however, intraspecific competition is only measurable when one species arrives several years earlier than the other (Miller-Pierce and Preisser 2012). In such a scenario, HWA densities are 40% lower when settling on trees previously infested with EHS; by contrast, the prior presence of HWA does not significantly reduce EHS densities (Miller-Pierce and Preisser 2012). Most recently, experimental work found that HWA crawlers avoided settling on EHS-infested branches, a finding supported by surveys showing that crawlers avoid settling at the base of EHS-infested needles (Gomez et al. 2014). These studies suggest that EHS, despite its apparent disadvantages, may actually be competitively dominant over HWA. Interaction with Hemlock While HWA is capable of quickly killing hemlock trees (McClure 1991, Orwig et al. 2002), the mechanism underlying such rapid HWA-mediated mortality has only recently begun to be addressed. Following initial infestation, the tree declines in health. This period is marked by needle drop, bud abortion, and inhibition of new growth (McClure 1991). A healthy hemlock can be killed in as little as four years, with many trees (especially in warmer climates) dying within ten years of infestation (McClure 1987, 1991; see the following larger-scale effects section, below, for a more detailed description of HWA-induced tree mortality). Some scientists hypothesized that hemlocks died from resource depletion (i.e., that large numbers of HWA essentially starved the tree of nutrients; McClure 1991). This explanation was challenged by work that used scanning electron microscopy to identify HWA’s precise feeding mode and cellular-level impact (Young et al. 1995). Because these researchers found that HWA feeding caused relatively little cellular damage, they proposed that the HWA’s impact on tree health was better explained by toxicity: fluids secreted by feeding adelgids, or the plant’s response to the feeding, had a disproportionately large impact on plant health. This explanation gained credence with the large increase in EHS densities in southern New England; similarly-sized to HWA but more Southeastern Naturalist 5 E.L. Preisser, K.L.F. Oten, and F.P. Hain 2014 Vol. 13, Special Issue 6 abundant (Preisser et al. 2008), these scales nonetheless had less impact on hemlock growth and survival (Miller-Pierce and Preisser 2012, Miller-Pierce et al. 2010, Preisser and Elkinton 2008, Preisser et al. 2008, 2011). The large amount of damage induced by HWA feeding appears linked to a hypersensitive response in hemlock. The presence of HWA at the base of a needle causes extensive damage (measured by the presence of hydrogen peroxidase) to the needle itself as well as to nearby new-growth foliage that had not been colonized by HWA crawlers (Radville et al. 2011). The hypersensitive response acts to isolate sessile herbivores by killing nearby tissue and starving the feeding insect (Fernandes 1990, Fernandes and Negreiros 2001). In the case of HWA, the hypersensitive response causes the induction of false growth rings in infested stems that interfere with solute transport and prevent the stems from obtaining the water necessary for photosynthesis (Domec et al. 2013, Gonda-King et al. 2012). As a result, the plant may experience chronic water stress and eventually be unable to carry out photosynthesis (Domec et al. 2013). Despite widespread cell death, induction of the hypersensitive response appears to cause relatively little harm to feeding HWA. On the contrary, HWA may biochemically manipulate the plant to induce this response. HWA possesses several enzymes similar to those used by related insects to feed upon and influence their host plants (Oten 2011). A detailed analysis of herbivore-mediated changes in hemlock amino acid concentrations found that HWA actually induced substantial increases in local nutrient levels (Gómez et al. 2012). This manipulation may be similar to that occurring in galling insects, where sessile herbivores manipulate plant physiology to build protective structures (i.e., galls) that serve as both food and protection (Havill and Foott it 2007). Larger-scale Effects HWA has killed so many hemlocks in the eastern US that the International Union for Conservation of Nature (IUCN) recently labeled Eastern Hemlock as near threatened and placed it on the Red List of Threatened Species (Farjon 2013). At the local level, HWA-induced hemlock mortality has substantially impacted many natural areas; Virginia’s Shenandoah National Park, for example, has lost ≈90% of its mature hemlocks (Townsend and Rieske-Kinney 2006). While noticeable hemlock mortality and decline continues, however, the initial predictions of complete mortality of Eastern and Carolina Hemlock have not been realized (Preisser et al. 2008). Especially in the northeastern US, a substantial number of infested trees continue to persist: a long-term study in Delaware Water Gap National Park (located on the NJ-PA border) found that 73% of Eastern Hemlocks survived for longer than ten years (Eschtruth et al. 2013). A recently published study of forest inventory analysis (FIA) data for 432 US counties made a similar point (Trotter et al. 2013). It found little evidence for large-scale decline and a slight increase in median live hemlock basal area between 1985 and 2005, a fact it attributed to the positive effects of reforestation and regeneration overwhelming the more recent negative impacts of HWA. Southeastern Naturalist E.L. Preisser, K.L.F. Oten, and F.P. Hain 2014 6 Vol. 13, Special Issue 6 Even if Eastern and Carolina Hemlock persist in eastern US ecosystems, the large losses caused by HWA infestation will substantially alter eastern forest ecosystems. Hemlocks are a shade-tolerant foundation species that shades and cools headwater streams that are home to trout and a wide variety of aquatic invertebrates (reviewed in Ellison et al. 2005, Orwig and Foster 2000). They also assist in soil stabilization and controlling hydrologic regimes (Ford and Vose 2007). Over a nineyear period, HWA-induced Eastern Hemlock decline in the Delaware Water Gap National Recreational Area (NJ) resulted in a doubling of understory light levels, a fourfold increase in vascular plant cover, and to the colonization of 35% surveyed plots by invasive plants (Eschtruth et al. 2006). Hemlock stands are critical habitat for a number of bird species (Rabenold et al. 1998), and the loss of hemlocks can substantially affect invertebrate community composition (Adkins and Rieske 2013, Dilling et al. 2007, Ingwell et al. 2012). There are 274 Eastern Hemlock cultivars, making it one of the most cultured and cultivated landscape tree species (Quimby 1996, Swartley 1984), which is often used as a hedge because of its response to shearing (Swartley 1984). It is also desired for its color, graceful habit, and, until recently, its freedom from disease and insects. According to 1995 nursery inventories in Tennessee and North Carolina, the value of Eastern Hemlock was approximately $34 million (J.R. Rhea, USDA Forest Service, Ashville, NC, pers. comm., cited in Bentz et al. 2002). HWA invasion has reduced the importance of native hemlocks for ornamental use and will likely also affect the more than 4 million cubic feet of timber produced in the region annually (Rhea 1995, Woodsen 2001). Land values also deteriorate as a result of HWA infestations. A study in residential New Jersey found that HWA-caused defoliation levels of 25-50% led nearby property values to decline by an average of more than $7,000.00 (Holmes et al. 2005). The future use of hemlocks as ornamentals relies in part on the ability to ef fectively manage HWA. Management Methods Chemical control HWA management is largely focused on biological control and chemical control (McClure 2001, McClure and Cheah 1999, Montgomery 1999, also see Onken and Reardon 2011). Chemical control is currently the most effective method and is widely used in ornamental and landscape settings, but it is generally impractical in forest settings due to prohibitive costs and the potential environmental impacts of wide-scale use (Cowles 2009, McClure 1992). Trees must be treated individually, often leading managers to target a series of high-value trees for treatment. Because chemicals degrade over time, they must be periodically re-applied to ensure continued control. In addition, the water-solubility of systemic insecticides allows for rapid uptake and internal transportation of the chemical throughout the tree, but also allows the insecticides to impact aquatic organisms in nearby water bodies. Imidacloprid, for example, has been detected in water at sites with low soil organic matter (US EPA 2003). The mode of chemical application may also affect hemlock-forest–associated fauna. Soil injections of imidacloprid, for example, can Southeastern Naturalist 7 E.L. Preisser, K.L.F. Oten, and F.P. Hain 2014 Vol. 13, Special Issue 6 cause significant declines in the abundance and richness of soil-dwelling springtails and other non-target organisms (Reynolds 2008). Forest applications may be limited due to geographical and logistical constraints such as difficulties in bringing equipment into a forest (Cowles et al. 2006). Furthermore, pesticides are not a fail-proof method. In Joyce Kilmer Memorial Forest (NC), pesticide applications appear largely ineffective in reducing HWA populations (Bompey 2010). However, research directed toward refining chemical treatment options has decreased their environmental impacts while increasing their efficacy (e.g., Cowles 2009). Chemicals are often the best option in ornamental settings, but they are generally impractical in forests as a stand-alone management tool. Sustainable adelgid management in forest settings will likely require the integration of chemical control methods with other management techniques (Bentz et al. 2002, Del Tredici and Kitajima 2004, McClure and Cheah 1999). Biological control There appear to be no predators native to the invaded range capable of consistently lowering adelgid densities sufficiently to prevent tree decline and death (Montgomery and Lyon 1996, Wallace and Hain 2000, Havill et al. 2012). Thus, researchers searching for effective HWA predators began to explore Asia and northwestern North America, the native range of the HWA, for organisms useful in a classical biological control program. Since the 1990s, this approach has been a major focus of HWA research and management (McClure and Cheah 2002, Onken and Reardon 2011), an effort that expanded considerably with the development of the Hemlock Woolly Adelgid Initiative in 2003. The current program includes 28 federal and state agencies, 24 universities, seven institutions in China and Japan, and numerous private industry groups (Onken and Reardon 2011). Several beetle species have been released in hopes of controlling HWA. In 1995, Sasajiscymnus tsugae Sasaji and McClure, a coccinellid beetle that is native to Japan, was the first to be released (Cheah 2008, 2011; Cheah and McClure 1998). Since then, there have been more than two million S. tsugae released on more than 400 sites in 16 states (Cheah 2011, Grant et al. 2010, Salom et al. 2008). It successfully reproduces and disperses following release, and is capable of surviving extreme climatic events (Cheah 2011). Between 2004 and 2011, more than 61,000 individuals of Scymnus sinuanodulus Yu and Yao, a coccinellid beetle native to China, have been released (Montgomery and Keena 2011). Because research suggests that this species is most climatically suited to the southern portion of the hemlock range in the eastern US (Salom et al. 2008), most of these releases have occurred in Georgia, North Carolina, and Tennessee. When released in these areas, the species does not seem to require additional efforts to assist in its establishment (Montgomery and Keena 2011). Other beetles in the same genus have also been (S. ningshanensis Yu and Yao) or are currently being (S. coniferarum Crotch and S. camptodromus Yu and Liu) evaluated as biological control agents. Native to western North America, the beetle S. coniferarum seems especially promising because its feeding habits temporally complement that Southeastern Naturalist E.L. Preisser, K.L.F. Oten, and F.P. Hain 2014 8 Vol. 13, Special Issue 6 of Laricobius nigrinus Fender (Tooth-necked Fungus Beetle, discussed in the next paragraph). Releases of S. coniferarum have begun, and research and efficacy trials continue (Montgomery et al. 2011). Initial problems in rearing S. camptodromus slowed this species’ evaluation, but it is still being pursued because it diapauses at the same time as HWA, has a broad geographic distribution, and is active during a critical period in the HWA life cycle (Montgomery and Keena 2011). Laricobius nigrinus (Coleoptera: Derodontidae), a specialist HWA predator native to Oregon and Washington (Kohler et al. 2008), shows particular promise as a biological control agent. Since its introduction in the eastern US in 2003, more than 380,000 beetles have been released throughout the region (Mausel et al. 2011, Salom et al. 2008). While its role as a biological control agent seems promising given its field-recovery success and ability to reduce HWA populations, it is hybridizing with a native beetle, L. rubidus LeConte (Klein et al. 2010), with unknown consequences (Havill et al. 2012). This native beetle, which feeds primarily on Pineus strobi Hartig (Pine Bark Adelgid), can be found feeding on HWA in areas where Pinus strobus L. (Eastern White Pine) and hemlock co-occur (Montgomery and Lyon 1996, Wallace and Hain 2000). The fact that L. nigrinus feeds exclusively on spring-generation eggs and nymphs (Kohler et al. 2008, Zilahi-Balogh et al. 2002) suggests that it will be most effective as part of a suite of predators. Another Laricobius beetle native to Japan, L. osakensis Montgomery and Shuyake, is also being researched and released (2000 of these beetles were set loose in eastern US hemlock forests in 2012) (K. Mooneyham, Virginia Tech, Blacksburg, VA, pers. comm.). This beetle is especially important because it is native to the region where the invasive lineage of the HWA also occurs (Havill et al. 2006, Lamb et al. 2011). A number of other organisms also have potential as biological control agents. Leucopis spp. flies (Diptera: Chamaemyiidae) prey on HWA in northwestern North America, but a lack of rearing methods and difficulty in species identification have slowed their development as control agents (Ross et al. 2010). A fungal agent, Lecanicillium muscarium Zare and Gams, is also under investigation (Salom et al. 2008). It is commercially available as Mycotal, a biopesticide. Some formulations of this fungal agent, which has been approved for use in the US and is already found in eastern US hemlock forests, can reduce HWA populations by up to 75%; ongoing research focuses on the challenges posed by harsh abiotic conditions and the need for mass deployment (Costa 2010, 2011). While biological control agents may help manage HWA populations, the high susceptibility of Eastern and Carolina Hemlock to HWA means that these agents must cause extremely high HWA mortality in order to be successful (McClure 1996). This level of HWA suppression will likely require a suite of predators (Cheah et al. 2004, Montgomery and Lyon 1996). Host-plant resistance When grown in the eastern US and experimentally infested with the HWA, hemlock species native to Asia and the Pacific Northwest are tolerant of and/or resistant to this pest (Bentz et al. 2002, 2007; Del Tredici and Kitajima 2004; Jetton et al. Southeastern Naturalist 9 E.L. Preisser, K.L.F. Oten, and F.P. Hain 2014 Vol. 13, Special Issue 6 2008; Oten 2011). These findings suggest that host-plant factors may play a role, perhaps in concert with natural enemies and the scattered distribution of hemlocks, in keeping HWA densities low in the native range (Montgomery and L yon 1996). Interspecific variation in hemlock resistance to HWA is well-documented and continues to be pursued as a key component in a long-term, integrated approach to HWA management. Hybrid crosses between HWA-resistant T. chinensis (Franch.) Pritzel ex Diels (Chinese Hemlock) and HWA-susceptible Carolina Hemlock produce progeny that are more HWA-resistant than Carolina Hemlocks (Montgomery et al. 2009). Similar hybridization attempts with Eastern Hemlock have been unsuccessful (Bentz et al. 2002, Pooler et al. 2002), but advances in hybridization methodology may assist in overcoming this obstacle. There have also been reports of a few Eastern Hemlocks growing in heavily HWA-damaged regions that appear to have remained healthy and vigorous. Their existence and continued vigor, despite coexisting with the HWA for more than 20 years, suggests the potential for some degree of HWA resistance/tolerance in Eastern and Carolina Hemlocks (Caswell et al. 2008). When cuttings from these putatively resistant trees were grown and evaluated in conjunction with cuttings from known HWA-susceptible trees, the putatively resistant cuttings had lower HWA settlement and higher HWA mortality than did control cuttings (Ingwell and Preisser 2011). While the development of resistant hemlocks suitable for forest restoration in the eastern US is a long process, initial investigations look somewhat promising. A long-term and sustainable approach to HWA management will likely incorporate chemical control, biological control, and host-plant resistance into an integrated management program. Conclusion The past decades have seen substantial progress towards a better understanding of HWA ecology and management. These accomplishments notwithstanding, we have yet to develop a long-term and cost-effective management strategy for the Hemlock Woolly Adelgid. It is our hope that the articles contained in this special issue move us closer to this goal, and to the preservation of our native hemlock trees. Acknowledgments This manuscript benefitted greatly from the comments of three an onymous reviewers. Literature Cited Abell, K., and R. Van Driesche. 2012. Impact of latitude on synchrony of a scale (Fiorinia externa) (Hemiptera: Diaspididae) and its parasitoid (Encarsia citrina) (Hymenoptera: Aphelinidae) in the Eastern United States. Biological Control 63:339–347. Adkins, J.K., and L.K. Rieske. 2013. Loss of a foundation forest species due to an exotic invader impacts terrestrial arthropod communities. Forest Ecology and Management 295:126–135. Southeastern Naturalist E.L. Preisser, K.L.F. Oten, and F.P. Hain 2014 10 Vol. 13, Special Issue 6 Annand, P. 1924. A new species of Adelges (Hemiptera: Phylloxeridae). Pan-Pacific Entomologist 1:79–82. Bentz, S.E., L. Riedel, M.R. Pooler, and A.M. Townsend. 2002. Hybridization and selfcompatibility in controlled pollinations of eastern North American and Asian hemlock (Tsuga) species. Journal of Arboriculture 28:200–205. Bentz, S.E., R.J. Griesbach, M.R. Pooler, and A.M. Townsend. 2007. Tsuga chinensis as a source of host resistance to the Hemlock Woolly Adelgid. Pp. 24–25, In K.W. Gottschalk (Ed.). Proceedings: 17th US Department of Agriculture Interagency Research Forum on Gypsy Moth and other Invasive Species. US Forest Service, Mor gantown WV. Bompey, N. 2010. US Forest Service increases efforts to save hemlocks in Asheville area. 11/08/2010 Edition, Page 2 Asheville Citizen Times, Asheville NC. Butin, E., A.M. Porter, and J.S. Elkinton. 2005. Adaptation during biological invasions and the case of Adelges tsugae. Evolutionary Ecology Research 87:887–900. Caswell, T., R. Casagrande, B. Maynard, and E.L. Preisser. 2008. Production and evaluation of Eastern Hemlocks potentially resistant to the Hemlock Woolly Adelgid. Pp. 124–134, In B. Onken and R.C. Reardon (Eds.). Fourth Symposium on Hemlock Woolly Adelgid in the Eastern United States. US Forest Service, Hartford, CT. Cheah, C. 2008. The case for Sasajiscymnus tsugae: Biological control has helped save Connecticut’s hemlocks. Pp. 279–280, In B. Onken and R.C. Reardon (Eds.). Fourth Symposium on Hemlock Woolly Adelgid in the Eastern United States. US Forest Service, Hartford, CT. Cheah, C. 2011. Sasajiscymnus (=Pseudoscymnus) tsugae, a ladybeetle from Japan. Pp. 43–52, In B. Onken and R.C. Reardon (Eds.). Implementation and Status of Biological Control of the Hemlock Woolly Adelgid. US Forest Service, Morgantown, WV. 230 pp. Cheah, C., and M. 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., M.E. Montgomery, S.M. Salom, B.L. Parker, S.D. Costa, and M. Skinner. 2004. Biological control of Hemlock Woolly Adelgid. R.C. Reardon and B. Onken (Technical Contributors). FHTET-2004-04. US Forest Service, Morgantown WV. 22 pp. Costa, S.D. 2010. Hemlock Woolly Adelgid suppression with aerial application of mycotal fungus in a microfactory formulation: Can it work? Pp. 36–42, In B. Onken and R.C. Reardon (Eds.). Fifth Symposium on Hemlock Woolly Adelgid in the Eastern United States. US Forest Service, Asheville NC. 230 pp. Costa, S.D. 2011. Insect-killing fungi for HWA management: Current status. Pp. 107–115, In B. Onken and R. Reardon (Eds.). Implementation and Status of Biological Control of the Hemlock Woolly Adelgid. US Forest Service, Morgantown, WV. Cota Vieira, L., A.S. Lamb, S. Shiyake, S.M. Salom, and L.T. Kok. 2013. Seasonal abundance and synchrony between Laricobius osakensis (Coleoptera: Derodontidae) and its prey, Adelges tsugae (Hemiptera: Adelgidae), in Japan. Annals of the Entomological Society of America 106:249–257. Cowles, R. 2009. Optimizing dosage and preventing leaching of imidacloprid for management of Hemlock Woolly Adelgid in forests. Forest Ecology and Management 257: 1026–1033. Cowles, R., M.E. Montgomery, and C. Cheah. 2006. Activity and residues of imidacloprid applied to soil and tree trunks to control Hemlock Woolly Adelgid (Hemiptera: Adelgidae) in forests. Journal of Economic Entomology 99:1258–1267. Southeastern Naturalist 11 E.L. Preisser, K.L.F. Oten, and F.P. Hain 2014 Vol. 13, Special Issue 6 Del Tredici, P., and A. Kitajima. 2004. Introduction and cultivation of Chinese Hemlock (Tsuga chinensis) and its resistance to Hemlock Woolly Adelgid (Adelges tsugae). Journal of Arboriculture 30:282–286. Dilling, C., P. Lambdin, J. Grant, and L. Buck. 2007. Insect guild structure associated with Eastern Hemlock in the southern Appalachians. Environmental Entomology 36:1408–1414. Domec, J.-C., L.N. Rivera, J.S. King, I. Peszlen, F.P. Hain, B. Smith, and J. Frampton. 2013. Hemlock Woolly Adelgid (Adelges tsugae) infestation affects water and carbon relations of Eastern Hemlock (Tsuga canadensis) and Carolina Hemlock (Tsuga caroliniana). New Phytologist 199:452–463. Ellison, A., M. Bank, B. Clinton, E. Colburn, K. Elliott, C. Ford, D. Foster, B. Kloeppel, J. Knoepp, G. Lovett, J. Mohan, D. Orwig, N. Rodenhouse, W. Sobczak, K. Stinson, J. Stone, C. Swan, J. Thompson, B. Von Holle, and J. Webster. 2005. Loss of foundation species: Consequences for the structure and dynamics of forested ecosystems. Frontiers in Ecology and the Environment 3:479–486. Eschtruth, A.K., N. Cleavitt, J.J. Battles, R.A. Evans, and T. Fahey. 2006. Vegetation dynamics in declining Eastern Hemlock stands: 9 years of forest response to Hemlock Woolly Adelgid infestation. Canadian Journal of Forest Research 36:1435–1450. Eschtruth, A.K., R.A. Evans, and J.J. Battles. 2013. Patterns and predictors of survival in Tsuga canadensis populations infested by the exotic pest Adelges tsugae: 20 years of monitoring. Forest Ecology and Management 305:195–203. Farjon, A. 2013. Tsuga canadensis. 2013. IUCN 2013. IUCN Red List of Threatened Species. Version 2013.1. Available online at Accessed 14 October 2013. Fernandes, G. 1990. Hypersensitivity: A neglected plant-resistance mechanism against insect herbivores. Environmental Entomology 19:1173–1182. Fernandes, G., and D. Negreiros. 2001. The occurrence and effectiveness of hypersensitive reaction against galling herbivores across host taxa. Ecologica l Entomology 26:46–55. Ford, C.R., and J.M. Vose. 2007. Tsuga canadensis (L.) Carr. mortality will impact hydrological processes in southern Appalachian forest ecosystems. Ecological Applications 17:1156–1167. Gómez, S., C.M. Orians, and E.L. Preisser. 2012. Exotic herbivores on a shared native host: Tissue quality after individual, simultaneous, and sequential attack. Oecologia 169:1015–1024. Gómez, S., L. Gonda-King, C.M. Orians, and E.L. Preisser. 2014. Competitor avoidance drives within-host feeding-site selection in a passively dispersed herbivore. Ecological Entomology 39:10–16. Gonda-King, L., L. Radville, and E.L. Preisser. 2012. False ring formation in Eastern Hemlock branches: Impacts of Hemlock Woolly Adelgid and Elongate Hemlock Scale. Environmental Entomology 41:523–531. Grant, J., A. Hakeem, J.R. Rhea, G. Wiggins, P. Lambdin, and G. Taylor. 2010. Recovery and establishment of introduced predators of Hemlock Woolly Adelgid in the southern Appalachians. Pp. 21–23, In B. Onken and R.C. Reardon (Eds.). Fifth Symposium on Hemlock Woolly Adelgid in the Eastern United States. US Forest Service, Asheville NC. Hakeem, A., J. Grant, G. Wiggins, P. Lambdin, and J.R. Rhea. 2011. Establishment and coexistence of two predators, Laricobius nigrinus and Sasajiscymnus tsugae, introduced against Hemlock Woolly Adelgid on Eastern Hemlock. Biocontrol Science and Technology 21:687–691. Southeastern Naturalist E.L. Preisser, K.L.F. Oten, and F.P. Hain 2014 12 Vol. 13, Special Issue 6 Havill, N., and R. Foottit. 2007. Biology and evolution of Adelgidae. Annual Review of Entomology 52:325–349. Havill, N., M.E. Montgomery, G. 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. Havill, N., G. Davis, D.L. Mausel, J. Klein, R. McDonald, C. Jones, M. Fischer, S.M. Salom, and A. Caccone. 2012. Hybridization between a native and introduced predator of Adelgidae: An unintended result of classical biological control. Biological Control 63:359–369. Holmes, T., E. Murphy, and D. Royle. 2005. The economic impacts of Hemlock Woolly Adelgid on residential landscape values: Sparta, New Jersey case study. Pp. 15–24, In B. Onken and R.C. Reardon (Eds.). Third Symposium on the Hemlock Woolly Adelgid in the Eastern United States. US Forest Service, Asheville, NC. Ingwell, L.L., and E.L. Preisser. 2011. Using citizen-science programs to identify host resistance in pest-invaded forests. Conservation Biology 25:182–188. Ingwell, L., M. Miller-Pierce, R.T. Trotter III, and E.L. Preisser. 2012. Vegetation and invertebrate community response to Eastern Hemlock decline in southern New England. Northeastern Naturalist 19:541–558. Jetton, R.M., F.P. Hain, W.S. Dvorak, and J. Frampton. 2008. Infestation rate of Hemlock Woolly Adelgid (Hemiptera: Adelgidae) among three North American hemlock (Tsuga) species following artificial inoculation. Journal of Entomologic al Science 43:438–442. Klein, J.L., A. Caccone, and N. Havill. 2010. Polymorphic microsatellite loci for Laricobius nigrinus and L. rubidus (Coleoptera: Derodontidae), predators of the Hemlock Woolly Adelgid. Molecular Ecology Resources 10:751–754. Kohler, G.R., V.L. Stiefel, K.F. Wallin, and D.W. Ross. 2008. Predators associated with the Hemlock Woolly Adelgid (Hemiptera: Adelgidae) in the Pacific Northwest. Environmental Entomology 37: 494–505. Lamb, A., M.E. Montgomery, L. Cota Vieira, S. Shiyake, and S.M. Salom. 2011. Laricobius osakensis, a Hemlock Woolly Adelgid predator from Japan. Pp. 90–96, In B. Onken and R.C. Reardon (Eds.). Implementation and Status of Biological Control of the Hemlock Woolly Adelgid. US Forest Service, Publication FHTET-2011-04, Morgantown, WV. 230 pp. Mausel, D.L., G.A. Davis, A.B. Lamb, G.M.G. Zilahi-Balogh, L.T. Kok, and S.M. Salom. 2011. Laricobius nigrinus Fender (Coleoptera: Derodontidae). Pp. 77–89, In B. Onken and R.C. Reardon (Eds.). Implementation and Status of Biological Control of the Hemlock Woolly Adelgid. US Forest Service, Publication FHTET-2011-04, Morgantown, WV. 230 pp. McClure, M.S. 1978. Seasonal development of Fiorinia externa, Tsugaspidiotus tsugae (Homoptera: Diaspididae), and their parasite, Aspidiotiphagus citrinus (Hymenoptera: Aphelinidae): Importance of parasite-host synchronism to the population dynamics of two scale pests of hemlock. Environmental Entomology 7:863–870. McClure, M.S. 1987. Biology and control of Hemlock Woolly Adelgid. Bulletin of the Connecticut Agricultural Experiment Station 851. McClure, M.S. 1989. Evidence of a polymorphic life cycle in the Hemlock Woolly Adelgid Adelges tsugae (Homoptera: Adelgidae). Annals of the Entomological Society of America 82:50–54. McClure, M.S. 1990. Role of wind, birds, deer, and humans in the dispersal of Hemlock Woolly Adelgid (Homoptera: Adelgidae). Environmental Entomology 19:36–43. Southeastern Naturalist 13 E.L. Preisser, K.L.F. Oten, and F.P. Hain 2014 Vol. 13, Special Issue 6 McClure, M.S. 1991. Density-dependent feedback and population cycles in Adelges tsugae (Homoptera: Adelgidae) on Tsuga canadensis. Environmental Entomology 20:258–264. McClure, M.S. 1992. Effect of implanted and injected pesticides and fertilizers on the survival of Adelges tsugae (Homoptera: Adelgidae) and on the growth of Tsuga canadensis. Journal of Economic Entomology 85:468–472. McClure, M.S. 1996. Biology of Adelges tsugae and its potential for spread in the northeastern United States. Pp. 16–25, In S.M. Salom, T. Tigner, and R.C. Reardon (Eds.). First Hemlock Woolly Adelgid Review. US Forest Service, Morgantown, WV. McClure, M.S. 1997. Biological control in native and introduced habitats: Lessons learned from the sap-feeding guilds on hemlock and pine. Pp 31–52, In D. Andow, D. Ragsdale, and R. Nyvall (Eds.). Ecological Interactions and Biological Control. Westview Press, Boulder, CO. McClure, M.S. 2001. Biological control of Hemlock Woolly Adelgid in the eastern United States. FHTET-2000-08. USDA Forest Service, Forest Health Technology Enterprise Team, Morgantown, WV. 10 pp. McClure, M.S., and C. Cheah. 1999. Reshaping the ecology of invading populations of Hemlock Woolly Adelgid, Adelges tsugae (Homoptera: Adelgidae), in Eastern North America. Biological Invasions 1:241–254. McClure, M.S., and C. Cheah. 2002. Important mortality factors in the life cycle of Hemlock Woolly Adelgid, Adelges tsugae, in the northeastern United States. Pp. 13–22, In R. Reardon, B. Onken, and J. Lashomb (Eds.). Symposium on the Hemlock Woolly Adelgid in Eastern North America. US Forest Service, New Brunswick, NJ. Miller-Pierce, M., and E.L. Preisser. 2012. Asymmetric priority effects influence the success of invasive forest insects. Ecological Entomology 37:350–358. Miller-Pierce, M., D.A. Orwig, and E.L. Preisser. 2010. Effects of Hemlock Woolly Adelgid and Elongate Hemlock Scale on Eastern Hemlock growth and foliar chemistry. Environmental Entomology 39:513–519. Montgomery, M.E. 1999. Woolly adelgids in the southern Appalachians: Why they are harmful and prospects for control. Pp. 47–57, In P. Gibson and C.R. Parker (Eds.). Proceedings of the Southern Appalachian Biological Control Initiative Workshop, 26–27 September 1996. FHTET-98-14. USDA Forest Service, Forest Health Technology Enterprise Team, Morgantown, WV. Montgomery, M.E., and M.A. Keena. 2011. Scymnus (Neopullus) lady beetles from China. Pp. 53–76, In B. Onken and R.C. Reardon (Eds.). Implementation and Status of Biological Control of the Hemlock Woolly Adelgid. US Forest Service, Publication FHTET-2011-04, Morgantown, WV. 230 pp. Montgomery, M.E., and S.M. Lyon. 1996. Natural enemies of adelgids in North America: Their prospect for biological control of Adelges tsugae (Homoptera: Adelgidae). Pp. 89–102, In S.M. Salom, T.C. Tigner, and R.C. Reardon (Eds.). Proceedings of the first Hemlock Woolly Adelgid review, 12 October 1995, Charlottesville, VA. FHTET 96-10. US Department of Agriculture, Forest Service, Forest Health Technology Enterprise Team, Morgantown, WV. Montgomery, M., S. Bentz, and R. Olsen. 2009. Evaluation of hemlock (Tsuga) species and hybrids for resistance to Adelges tsugae (Hemiptera: Adelgidae) using artificial infestation. Journal of Economic Entomology 102:1247–1254. Montgomery, M.E., T.J. McAvoy, and S.M. Salom. 2011. Other species considered. Pp. 116–122, In B. Onken and R.C. Reardon (Eds.). Implementation and Status of Biological Control of the Hemlock Woolly Adelgid. US Forest Service, Publication FHTET-2011-04, Morgantown, WV. 230 pp. Southeastern Naturalist E.L. Preisser, K.L.F. Oten, and F.P. Hain 2014 14 Vol. 13, Special Issue 6 Onken, B., and R.C. Reardon (Eds.). 2011. Implementation and Status of Biological Control of the Hemlock Woolly Adelgid. USDA FHTET-2011-04. 230 pp. Orwig, D.A., and D. Foster. 2000. Stand, landscape, and ecosystem analyses of Hemlock Woolly Adelgid outbreaks in southern New England: An overview. Pp. 123–125, In K. McManus, K. Shields, and D. Souto (Eds.). Symposium on Sustainable Management of Hemlock Ecosystems in Eastern North America. US Forest Service, Newtown Square, PA. Orwig, D.A., D. Foster, and D.L. Mausel. 2002. Landscape patterns of hemlock decline in New England due to the introduced Hemlock Woolly adelgid. Journal of Biogeography 29:1475–1487. Oten, K.L.F. 2011. Host-plant selection by the Hemlock Woolly Adelgid, Adelges tsugae Annand: Sensory systems and feeding behavior in relation to physical and chemical host-plant characteristics. Ph.D. Dissertation. North Carolina State University, Raleigh, NC. Oten, K.L.F., G.R. Bauchan, J. Frampton, and F.P. Hain. 2012. Biophysical characteristics of the stem and petiole surface of six hemlock (Tsuga) species and a hybrid: Implications for resistance to Adelges tsugae. Botany 90:1170–1178. Paradis, A. 2011. Population dynamics of the Hemlock Woolly Adelgid (Hemiptera: Adelgidae). Ph.D. Dissertation. University of Massachusetts, Amherst, MA. Pooler, M.R., L.G.H. Riedel, S.E. Bentz, and A.M. Townsend. 2002. Molecular markers used to verify interspecific hybridizations between hemlock (Tsuga) species. Journal of the American Society for Horticultural Science 127(4):623–627. Preisser, E.L., and J.S. Elkinton. 2008. Exploitative competition between invasive herbivores benefits a native host plant. Ecology 89:2671–2677. Preisser, E.L., A. Lodge, D.A. Orwig, and J.S. Elkinton. 2008. Range expansion and population dynamics of co-occurring invasive herbivores. Biological Invasions 10:201–213. Preisser, E.L., M. Miller-Pierce, J. Vansant, and D.A. Orwig. 2011. Eastern Hemlock (Tsuga canadensis) regeneration in the presence of Hemlock Woolly Adelgid (Adelges tsugae) and Elongate Hemlock Scale (Fiorinia externa). Canadian Journal of Forest Research 41:2433–2439. Quimby, J.W. 1996. Value and importance of hemlock ecosystems in the eastern United States. Pp. 1–8, In S.M. Salom, T. Tigner, and R.C. Reardon (Eds.). First Hemlock Woolly Adelgid Review. US Forest Service, Morgantown, WV. Rabenold, K.N., P.T. Fauth, B.W. Goodner, J.A. Sadowski, and P.G. Parker. 1998. Response of avian communities to disturbance by an exotic insect in spruce-fir forests of the southern Appalachians. Conservation Biology 12:177–189. Radville, L., A. Chaves, and E.L. Preisser. 2011. Variation in plant defense against invasive herbivores: Evidence for a hypersensitive response in Eastern Hemlocks (Tsuga canadensis). Journal of Chemical Ecology 37:592–597. Reynolds, W.N. 2008. Imidacloprid insecticide treatments for Hemlock Woolly Adelgid, Adelges tsugae Annand (Hemiptera: Adelgidae), affect a non-target soil arthropod community surrounding Eastern Hemlock, Tsuga canadensis Carriere. University of Tennessee, Knoxville, TN. Rhea, J.R. 1995. Economic and environmental impacts of the Hemlock Woolly Adelgid (Adelges tsugae) on the hemlock resources of Eastern North America., In Proceedings: International Union of Forest Research Organizations, XX World Congress, Tampare, Finland. Ross, D., S. Grubin, G. Kohler, and K.M. Wallin. 2010. Evaluation of Leucopis species (Diptera: Chamaemyiidae) from the PNW as potential biological control for the Hemlock Woolly Adelgid. Pp. 32, In B. Onken and R.C. Reardon (Eds.). Fifth Symposium on Hemlock Woolly Adelgid in the Eastern United States. US Forest Service, Asheville, NC. Southeastern Naturalist 15 E.L. Preisser, K.L.F. Oten, and F.P. Hain 2014 Vol. 13, Special Issue 6 Salom, S.M., L.T. Kok, A.B. Lamb, C. Jubb, and B. Onken. 2008. Biological control of Hemlock Woolly Adelgid: What is it going to take to make it work? Pp. 11–18, In B. Onken and R.C. Reardon (Eds.). Fourth Symposium on Hemlock Woolly Adelgid in the Eastern United States. US Forest Service, Hartford, CT. Sato, S. 1999. Galls on Tigertail Spruce made by Aphrastasia tsugae at Mt. Tsurugi. Gensei 73:1–26. Souto, D., T. Luther, and B. Chianese. 1996. Past and current status of Hemlock Woolly Adelgid in Eastern and Carolina Hemlock stands. Pp. 9–15, In S.M. Salom, T. Tigner, and R. Reardon (Eds.). First Hemlock Woolly Adelgid Review. US Forest Service, Morgantown, WV. Swartley, J.C. 1984. The Cultivated Hemlocks. Timber Press, Portland, OR. Townsend, L., and L. Rieske-Kinney. 2006. ENTFACT-452: Meeting the threat of the Hemlock Woolly Adelgid. Pp. 1–8. UK Cooperative Extension Service, Lexington, KY. Trial, H., and M. Devine. 1995. The impact of the Hemlock Loopers, Lambdina fiscellaria (Guenée) and L. Athasaria (Walker) on Eastern Hemlock and Balsam Fir in New England. Maine Forest Service, Department of Conservation, Augusta, ME. Trotter III, R.T., and K. Shields. 2009. Variation in winter survival of the invasive Hemlock Woolly Adelgid (Hemiptera: Adelgidae) across the Eastern United States. Environmental Entomology 38:577–587. Trotter III, R.T., R.S. Morin, S.N. Oswalt, and A.M. Liebhold. 2013. Changes in the regional abundance of hemlock associated with the invasion of Hemlock Woolly Adelgid (Adelges tsugae Annand). Biological Invasions 15:1–13. Turner, J., M. Fitzpatrick, and E.L. Preisser. 2011. Simulating the dispersal of Hemlock Woolly Adelgid in the temperate forest understory. Entomologia Experimentalis et Applicata 141:216–223. US Department of Agriculture Forest Service (USFS). 2012. Forest Health Protection: Hemlock Woolly Adelgid Distribution Map. Forest Health Protection Service, Newtown Square PA. US Environmental Protection Agency (USEPA). 2003. Imidacloprid: Pesticide tolerances. Fed eral Register 68, 35,303–35,315. Available online at EPA-PEST/2003/June/Day-13/p14880.htm. Accessed 15 July 2013. Wallace, M., 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. Woodsen, M.M. 2001. Forest invaders: Insects that invade hemlock trees. American Forests 4:12–13. Young, R., K. Shields, and G. Berlyn. 1995. Hemlock Woolly Adelgid (Homoptera: Adelgidae): Stylet bundle insertion and feeding sites. Annals of the Entomological Society of America 88:827–835. Zilahi-Balogh, G.M.G., L.T. Kok, and S.M. Salom. 2002. Host specificity of Laricobius nigrinus Fender (Coleoptera: Derodontidae), a potential biological control agent of the Hemlock Woolly Adelgid, Adelges tsugae Annand (Homoptera: Adelgidae). Biological Control 24:192–198.