Biology, Injury, and Management of Maple Tree Pests in Nurseries and Urban Landscapes S. D. Frank,1,2 W. E. Klingeman, III,3 S. A. White,4 and A. Fulcher3 1Corresponding author, e-mail: [email protected]. 2NC State University, Department of Entomology, 3318 Gardner Hall, Raleigh, NC 27965-7613. 3University of Tennessee Knoxville, Department of Plant Sciences. 4Clemson University, Department of Environmental Horticulture.

J. Integ. Pest Mngmt. 4(1): 2013; DOI: http://dx.doi.org/10.1603/IPM12007

ABSTRACT. Favored for their rapid growth and brilliant fall color, maple (Acer spp.) trees are among the most commonly grown deciduous shade trees in urban landscapes and commercial production nurseries. Many maple species used as ornamental plants share a suite of important arthropod pests that have the potential to reduce the trees’ economic and esthetic value. We review the biology, damage, and management for the most important pests of maples with emphasis on integrated pest management (IPM) tactics available for each pest. Unfortunately, the biology of some of these pests is not well studied. This knowledge gap, paired with the low esthetic threshold for damage on ornamental plants, has hindered development of IPM tactics for maple pests in nurseries and landscapes. Maples will likely remain a common landscape plant. Therefore, our challenge is to improve IPM of the diverse maple pest complex.

Key Words: Acer spp., arthropod, integrated pest management, key pest, ornamental plants

Maple (Acer) is the most common genus of deciduous street tree management (IPM) adoption by pest managers, including develop- planted in eastern North America (Raupp et al. 2006). Acer is also one ment of scouting and monitoring techniques or economic thresholds. of the most common tree genera planted in U.S. residential and Our objective was to review current knowledge on the biology and commercial landscapes, parks, and public spaces (S. F., unpublished management of the most common and economically important arthro- data). Maples have esthetic and horticultural qualities that make them pod pests of maple trees in commercial nurseries and urban land- popular among homeowners, landscape professionals, and landscape scapes. We organized the pests by taxonomic order. Thus, closely designers. Most maple species, such as red maple (Acer rubrum L.), related arthropods with similar morphology are presented together silver maple (Acer saccharinum L.), and Norway maple (Acer pla- with photographs to assist in identification. The sections are beetles tanoides L.) are large shade trees. These species are favored over other (Coleoptera), caterpillars (Lepidoptera), and sucking insects shade tree genera because they grow rapidly and produce a large (Hemiptera), such as leafhoppers, soft scale, and armored scale. A canopy with dense shade. The most desirable characteristic of maples final pest section covers gall forming insects and mites together because of the similar plant symptoms they produce. For each of the in urban landscapes is their brilliant fall color that includes bright pests in each section we review what is known about their life history, yellows and oranges to deep red depending on species and cultivar. diagnostic features, and the type of plant damage they inflict. Then we Maples of Japanese origin, such as Acer palmatum Thurber and Acer review management practices and IPM tools for each pest based on japonicum Thurber, are small statured and used as specimen trees. available research. Management is discussed in order of general IPM Hundreds of cultivars provide consumers with a variety of forms (e.g., implementation starting with scouting and monitoring, followed by weeping or upright), leaf shapes and sizes, bark color, and other decision making guidelines, and finally intervention that includes esthetic characteristics. cultural (host plant resistance, stress management), biological, and The great demand for maple trees makes them an important agri- chemical management practices. We end the paper with a synthesis of cultural crop. Trees in the genus Acer account for over 34% of trees IPM tactics that are available and research needed to improve IPM of grown in U.S. nurseries (USDA 2009). The most frequently grown maple trees growing in nurseries and landscapes. maple species include red maple, Norway maple, Japanese maple, A. palmatum, and Freeman maple (Acer ϫ freemanii E. Murray), which Biology and Management of Important Coleopteran Pests are hybrids of red and silver maples (USDA 1998). Maples can be Ambrosia Beetles. Exotic ambrosia beetles, primarily Xylosandrus grown in the ground or in containers. In-ground trees are dug from crassiusculus Motschulsky (Coleoptera: Curculionidae) and Xylosan- fields severing their root system, when trees are dormant, and the root drus germanus Blandford (Coleoptera: Curculionidae), attack over ball is wrapped in burlap for shipping. Container-grown trees are 200 tree species (Weber and McPherson 1983a, Oliver and Mannion 2001). They are among the most damaging pests of nursery-grown grown in plastic pots with pine bark or other soilless substrate. The trees present in southeast, northeast, and midwestern states (Adkins et root system of container-grown trees is not damaged by digging so al. 2010; C. M. Ranger, unpublished data). Female beetles are 3 mm they can be sold and planted any time of year. Nurseries are intensive or less and range in color from reddish-brown to black depending on production systems. Horticultural practices, such growing in monocul- species (Wood 1982; Figs. 1 and 2). Ambrosia beetles often become ture, fertilization, pruning, digging, and planting can make plants more active before leaf flush and are the first pests to attack nursery-grown susceptible to pests than plants grown in landscapes. maples (Oliver and Mannion 2001). Ambrosia beetles bore into host Maple trees are hosts for at least 81 potentially damaging arthropod tree trunks and excavate galleries in the heartwood where adult fe- pests (Johnson and Lyon 1988). The identity and severity of pests males deposit eggs, and larvae develop (Hoffmann 1941, Weber and varies by maple species, cultivar, and whether trees are growing in a McPherson 1983b). Female ambrosia beetles inoculate trees with nursery or landscape setting (Seagraves et al. 2012). Relatively little symbiotic ambrosia fungus on which the larvae feed (Baker and Norris research has been done on the biology and management of even the 1968). Estimates of development time range from 4 to 8 wk (Bu- most common and important maple pests. Particularly lacking for chanan 1941, Hoffmann 1941, Oliver and Mannion 2001). Adult most maple species is research that would help enhance integrated pest males are flightless and only disperse short distances if at all (Kirk- 2 JOURNAL OF INTEGRATED PEST MANAGEMENT VOL. 4, NO. 1

Fig. 1. Adult granulate ambrosia beetle, Xylosandrus crassisculus. Photo: J. R. Baker and S. B. Bambara, North Carolina State University, “Frass toothpick” formed when ambrosia beetles bore into Bugwood.org. Fig. 3. trees and push frass out behind them. Photo: S. D. Frank, North Carolina State University.

Fig. 2. Adult black stem borer, Xylosandrus germanus. Photo: J. R. Baker and S. B. Bambara, North Carolina State University, Bugwood.org.

Fig. 4. Baker style ambrosia beetle trap made from empty soda endall 1993). Thus, mature female beetles often mate with their brothers bottles. Photo: S. D. Frank, North Carolina State University. in the galleries then emerge to find new hosts. Xylosandrus crassiusculus and X. germanus can have three generations per year in the southern United States. However, injury to nursery stock is primarily inflicted by Ambrosia beetle traps should be deployed before the first warm days the first generation (Hudson and Mizell 1999; Oliver and Mannion 2001; in spring and monitored weekly to determine when adult flight begins S. D. Frank and C. M. Ranger, unpublished data). and ends (Hudson and Mizell 1999, Schultz and Whitaker 1999, Ambrosia beetle damage has been documented on many maple spe- Oliver and Mannion 2001). Optimal height for X. germanus traps cies, including A. rubrum and A. ϫ freemanii, (Hoffmann 1941, Frank appears to be 0.5 m (Reding et al. 2010). The most X. crassiusculus and Sadof 2011). Attacks occur most heavily within1mofthebase of were captured in traps 0.5 and 1.7 m from the ground compared with the trunk and are rare on smaller diameter branches above the first traps 3 m from the ground (Reding et al. 2010). scaffold branches (Oliver and Mannion 2001). Damage is characterized Plant health also plays an important role in ambrosia beetle manage- by “frass tooth picks” (Fig. 3) that are pushed out as beetles excavate their ment. Recent research has documented that stressed trees release volatile galleries. The diagnostic value of these is short lived as they are easily chemicals, including ethanol, that make them more attractive to ambrosia dislodged by wind, rain, and irrigation, exposing a 1-mm round entry beetles (Ranger et al. 2010; 2011; 2012; 2013). Although any kind of hole. Infested plants may die or become unmarketable from boring stress can make trees more susceptible to pests, flood stress in particular, damage, ambrosia fungus that disrupts vascular flow, or infection of makes trees more attractive to ambrosia beetles (Ranger et al. 2013). secondary pathogens (Buchanan 1941, Weber and McPherson 1984). When adult beetles are captured, growers can protect their trees by Management. Monitoring adult flight is an important part of am- spraying the trunks with residual contact insecticides, every 3–4 wk brosia beetle management (Hudson and Mizell 1999, Oliver and until beetle activity subsides Ϸ12 wk later to prevent beetles from Mannion 2001). Xylosandrus crassiusculus and X. germanus are at- boring into trees (Table 1) (Frank and Sadof 2011). It is recommended tracted to ethanol baits deployed within a Lindgren funnel tower or that growers avoid spraying tree canopies because this wastes insec- Baker soda-bottle trap (Reding et al. 2010, Ranger et al. 2011; Fig. 4). ticide, negatively affects natural enemies, and may result in secondary MARCH 2013 FRANK ET AL.: INTEGRATED PEST MANAGEMENT (IPM) FOR MAPLE TREE PESTS 3 ------

Fig. 5. Flatheaded appletree borer, Chrysobothris femorata, adult. Photo: David Cappaert, Michigan State University, Bugwood.org.

Fig. 6. Flatheaded appletree borer, Chrysobothris femorata, larvae

------in frass-filled gallery. Photo: Amy Fulcher, University of Tennessee, Knoxville.

outbreaks of maple spider mites, Oligonicus aceris Shimer (Frank and ------Sadof 2011). Once beetles are inside trees there is no effective control for either the larvae or the associated fungus. Flatheaded Appletree Borer. Flatheaded appletree borers, Chryso- bothris femorata Olivier (Coleoptera: Buprestidae), feed on a wide range of deciduous trees, including maples (Fenton and Maxwell 1937, Fenton 1942, Fisher 1942, Wellso and Manley 2007). These borers are distributed across the continental United States and extend into Canada (Fenton 1942, Fisher 1942, Wellso and Manley 2007). ------Adult C. femorata are bullet-shaped and 7.6–15.2 mm long. Their elytra have several irregular brassy spots (Fig. 5). Beneath the elytra, the abdomen is metallic purple with metallic bronze ventral surface (Hansen et al. 2009, Hansen 2010, Wellso and Manley 2007). Larvae are cream colored with bell-shaped abdominal segments and a flat-

January February March April May June Julytened, August sclerotized September October thoracic November December area (Fig. 6). At least eight other Chryso------bothris species occur in the southeastern United States (Manley and Wellso 1975, Wellso and Manley 2007). However, it is unclear which of these species, in addition to C. femorata, may damage nursery stock. Moreover, there is genetic evidence that species within this Chrysobothris complex may interbreed making identification difficult (Hansen 2010). Throughout its range, C. femorata emerge once per year, although some larvae require 2 yr to reach maturity (Burke 1919). Adult beetles emerge from trees in late spring and early summer corresponding to The activity of each pest may vary outside of Zone 7 and may differ depending upon exposure to cooler and warmer microclimates within Zone 7. Dashed lines indicate approximate phenology of the pest life Japanese maple scale Cottony maple leaf scale Calico scale Terrapin scale Ocellate gall midge Maple spider mite Cottony maple scale Eriophyid mites stage that is targeted with insecticides for optimal efficacy. Flatheaded appletree borer Maple shoot borer Green-striped mapleworm Bagworms Potato leafhopper Gloomy scale Ambrosia beetles Table 1. Seasonal timing(http://planthardiness.ars.usda.gov/PHZMWeb/) for management of key maple pests in landscapes and nurseries based on normal seasonal emergence in USDA Plant Hardiness Zone 7 Ϸ299 Celsius degree-days (DDC) at base 10°C (Fenton and Maxwell 4 JOURNAL OF INTEGRATED PEST MANAGEMENT VOL. 4, NO. 1

Fig. 8. Flagging of maple stem caused by maple shoot borer, Fig. 7. Red maple trunk 1 yr after damage by flatheaded appletree Proteoteras aesculana. Photo: Amy Fulcher, University of Tennessee, borer larvae. Photo: S. D. Frank, North Carolina State University. Knoxville.

1937, Potter et al. 1988). Adult females feed on the bark of new twigs maple trees under stress induced by root-pruning, transplanting, during a preoviposition period of 4–8 d after which, they lay an wounding, or defoliation were generally more attractive to C. femo- average of 66 eggs in bark cracks and wounds (Fenton and Maxwell rata and other buprestid borers than nonstressed trees. Even 1 yr after 1937), typically on the sunny side of trees (Oliver et al. 2010). Larvae stress treatments were implemented infestation by buprestid borers Ϸ hatch 7 d later. They chew through the egg directly into the host tree, was greater on plants that had undergone transplant stress (Potter et al. thereby avoiding desiccation, predation, and contact with surface- 1988). applied pesticides. Inside the tree, larvae feed on actively dividing Maple species and cultivars recently have been shown to differ in cambium tissues and sapwood. When fully developed, larvae bore into susceptibility to C. femorata attack (Seagraves et al. 2012). Overall, the heartwood and form pupal chambers with entrances that are tightly red maples were found to be more susceptible than sugar or Freeman plugged with frass. Pupation occurs in late spring to early summer and maples but with considerable variation within species. For example, lasts 1–2 wk. Adults emerge by cutting distinctive D-shaped exit holes over 37% of red maple ‘Burgundy Belle’ tree were attacked, but 0% in bark. of red maple ‘Autumn Flame’ were attacked (Seagraves et al. 2012). Chrysobothris femorata can attack healthy trees but prefer those Natural enemies of C. femorata include hymenopteran and dip- stressed by drought, plant disease, mechanical injury, and other en- teran parasitoids and clerid beetles (Krombein et al. 1979). These vironmental factors (Potter et al. 1988). The most serious injury is predators and parasitoids can reduce borer populations under natural caused by larval feeding beneath the bark that damages the cambium conditions (Fenton 1942) but their role in ornamental nurseries and layer and disrupts the flow of water and nutrients throughout the tree landscapes is unknown. (Potter et al. 1988, Coyle et al. 2005, Oliver et al. 2010; Fig. 7). A Chemical management of buprestid borers traditionally has relied single larva is capable of girdling a young tree within one season. In on broad-spectrum insecticides applied to tree bark when adults be- commercial production systems, unprotected red maples may sustain come active, to reduce oviposition and larval survival (Potter et al. almost 50% crop losses because of larval borer injury (Potter et al. 1988). Contact insecticides targeting adults and can be sprayed onto 1988, Oliver et al. 2010). Adults chew on woody tissues in branch tree trunks when borers are at peak emergence. Soil-applied systemic crotches, around bud scars, and at the base of leaf petioles, and insecticides can be applied in spring to help control larvae in tree consume foliage, but typically cause little economic damage. trunks (Table 1) (Oliver et al. 2010). A recent study showed that one Management. The abundance and seasonal activity of C. femorata application of certain soil applied systemic insecticides can protect and other buprestids can be monitored using purple panel traps cov- young nursery-ground maples from C. femorata for 1–3 yr (Oliver et ered with sticky material such as Tanglefoot (Tanglefoot Company, al. 2010). Grand Rapids, MI) (Oliver et al. 2004). These traps should be de- ployed in mid-April and are likely to catch a wide range of buprestids, Biology and Management of Important Lepidopteran Pests including many in the Chrysobothris complex (Hansen et al. 2009). If Maple Shoot Borer. Maple shoot borers, Proteoteras aesculana males are trapped, genitalia can be used to separate the six most Riley (Lepidoptera: Tortricidae), are distributed throughout the United common southeastern species (Hansen et al. 2009). Trees entering the States. Adults are mottled-gray and relatively nondescript, with wings second year of production can be scouted to determine presence of held in a wedge shape when at rest. They overwinter as adults that injury in late winter and flagged for monitoring in spring. Larval become active in early spring to lay eggs on new maple shoots feeding beneath the bark is indicated by raised, spiraling, or blistered (Seagraves et al. 2008). Larvae bore into new growing shoots, causing bark that may seep dark fluid. Removing frass, then regular monitor- them to die or “flag” (Fig. 8). Larvae develop within the shoot, ing for the D-shaped exit hole detects adult emergence, which allows expelling frass and silk from their tunnel. They pupate on the ground, more precisely scheduled preventive trunk applications. Another ap- then second generation adults emerge Ϸ12 wk after first generation proach is to cut the infested sections from several infested trees and adults (Seagraves et al. 2008). In addition to the immediate damage of keep them in a cage outside where they can be monitored for adult flagging branches on trees, death of the growing tip creates new forked emergence. growth that requires corrective pruning to remove all but a single main Proper plant management and maintenance are important, as borers stem, or leader, that may have to be trained to grow straight by using prefer to attack stressed trees. Potter et al. (1988) reported that red stakes. MARCH 2013 FRANK ET AL.: INTEGRATED PEST MANAGEMENT (IPM) FOR MAPLE TREE PESTS 5

Fig. 9. Late-instar green-striped mapleworms, Dryocampa rubicund, feeding on maple leaves. Photo: S. D. Frank, North Carolina State Fig. 10. Yellownecked caterpillar, Datana ministra, on the ground in University. a nursery surrounded by frass pellets diagnostic of caterpillar feeding. Photo: S. D. Frank, North Carolina State University.

Synthetic pheromone lures are available for P. aes- Management. Bags persisting on trees in fall contain the exoskeleton of the female culana that can be deployed in combination with sticky traps. Red and moth that may be filled with up to 1,000 eggs. Freeman maples are both more susceptible to P. aesculana than sugar Management. Free-living caterpillars and bagworms are suscepti- maples or exotic species but susceptibility of cultivars within species ble to a number of predators and parasitoids (Coffelt and Schultz 1992, is variable (Seagraves et al. 2012). Chemical control of P. aesculana 1993a; Sadof and Snyder 2005; Ellis et al. 2005). However, natural can be achieved with a single pyrethroid application from just before enemies may not keep abundance or damage below esthetic thresholds bud break until two pairs of leaves are present, which also coincides in nurseries or urban landscape settings (Coffelt and Schultz 1992, with peak trap catches (Table 1) (Seagraves et al. 2008). 1993a; Sadof and Snyder 2005; Ellis et al. 2005). Free-living cater- Green-striped mapleworm or rosy maple Leaf-Feeding Caterpillars. pillars can be monitored or scouted visually by counting egg masses moth, Dryocampa rubicunda (F.) (Lepidoptera: Saturniidae), is native or larvae (Coffelt and Schultz 1993b). Large caterpillars also leave to North America and distributed throughout the eastern half of the frass pellets on the ground beneath trees (Fig. 10). A positive linear United States from Canada south to Alabama and Mississippi (Wilson relationship exists between the number of A. senatoria egg masses and 1971, Baker 1972). Adult female D. rubicunda have wooly bodies the amount of defoliation that occurs on pin oak trees later in the with pink ventral sides and pink markings on the forewings. They season (Coffelt and Schultz 1993b). This can be used to determine emerge in midsummer and lay clusters of pale-green eggs on the which trees will be 25% defoliated, which is the established esthetic underside of maple leaves (Wilson 1971, Baker 1972). Young larvae injury level for A. senatoria on pin oaks, Quercus palustris Mu¨nch- are pale yellow with black heads and black spines. Larvae are fully hausen (Coffelt and Schultz 1990; 1993b). However, this method grown in Ϸ4 wk. They have bright red heads and pale yellow-green entails counting every egg mass on a tree rather than subsampling bodies with seven rows of dark green longitudinal stripes, two rows of branches, which makes the threshold difficult to use. A similar thresh- black spines, and two large horns on the second thoracic segment old has not been established for other caterpillar species or for maples. (Baker 1972; Fig. 9). There is one generation per year in the North and Thyridopteryx ephemeraeformis can be scouted in the winter or two in the South (Wilson 1971). Dryocampa rubicunda feed on most spring by looking for overwintering bags. Egg hatch corresponds to maple species. They consume entire leaves and can quickly defoliate around 512 DDC (base 7.2°C) and can be determined by cutting open large trees or stands of trees. bags or looking for young larvae (Mussey and Potter 1997). At low Other leaf-feeding caterpillars such as yellownecked caterpillar, population levels or over small areas, individual bags can be hand- Datana ministra (Drury), (Lepidoptera: Notodontidae; Fig. 10) and picked and destroyed before egg-hatch to reduce later infestations. orange-striped oakworms, Anisota senatoria (J.E. Smith) (Lepidop- Residual insecticides applied in late spring, when larvae are still small, tera: Saturniidae), also feed on maple trees in nurseries and land- provide effective control (Table 1) (Hale et al. 2001, Klingeman scapes, although they are less common on maples than D. rubicunda 2002). (Johnson and Lyon 1988). These caterpillar species, distributed throughout the eastern and midwestern United States (Baker 1972), Biology and Management of Important Hemipteran Pests can defoliate trees, causing esthetic damage and potentially reducing Potato Leafhopper. Adult potato leafhoppers, Empoasca fabae tree growth (Coffelt et al. 1993). Adults of both species are active in (Harris) (Hemiptera: Cicadellidae) migrate northward to other parts of midsummer and typically have one generation per year, although A. the United States from the Gulf of Mexico between late April and senatoria has been reported to have a second generation in some early June (Medler 1957). Female E. fabae oviposit along leaf veins warmer locations (Baker 1972). and at the base of leaves near the petiole (Potter and Spicer 1993, Bagworms, Thyridopteryx ephemeraeformis (Haworth) (Lepidop- Bentz and Townsend 1999). Development from egg to adult takes Ϸ3 tera: Psychidae), are a native insect distributed throughout the eastern wk depending on temperature resulting in five to six overlapping and midwestern United States that can be an occasional but severe pest generations (Hogg 1985). of maple trees (Kaufman 1968, Johnson and Lyon 1988). Larvae Adult E. fabae are 3–3.5 mm-long, wedge-shaped, and pale green emerge from eggs and are dispersed by the wind (Cox and Potter 1986, with a row of six white spots on their backs, between the wings and Hale et al. 2001). Caterpillars feed on foliage of Ͼ128 species of head (Fig. 11). They feed on the young leaves and buds of Ͼ200 plant native and ornamental trees, including maples (Kaufman 1968, John- species, including maples (DeLong 1971). Injury is caused by me- son and Lyon 1988, Neal and Santamour 1990, Klingeman 2002). chanical damage by the stylet and saliva injected into the plant during 6 JOURNAL OF INTEGRATED PEST MANAGEMENT VOL. 4, NO. 1

Fig. 11. Potato leafhopper, Empoasca fabae, adult. Photo: Steve L. Brown, University of Georgia, Bugwood.org.

Fig. 13. “Witches broom” or multiple leaders caused by potato leafhopper feeding on maple meristems and loss of apical dominance. Photo: Bill Klingeman, University of Tennessee.

Fig. 12. “Hopperburn” on maple leaves caused by potato leafhopper feeding. Photo: Amy Fulcher, University of Tennessee, Knoxville. feeding (Potter and Spicer 1993, Backus et al. 2005). Damaged leaves can have necrotic margins and severe cupping or stunting; these Fig. 14. Adult gloomy scale, Melanaspis tenebricosa, beneath it test symptoms are colloquially referred to as “hopperburn” (Fig. 12). which has been lifted off. Photo: S. D. Frank, North Carolina State University. Empoasca fabae feeding on buds and meristems causes loss of apical dominance resulting in a “witch’s broom” in which many stems grow from the damaged branch tip (Fig. 13; Potter and Spicer 1993; Bentz be more susceptible to E. fabae damage than Freeman maples, sugar and Townsend 1997, 1999). Empoasca fabae feeding injury in com- maples, or other species (Seagraves et al. 2012). mercial maple production reduces annual tree growth (Oliver et al. Management traditionally has relied on applications of pyrethroid, 2009), thus extending the time needed to produce a salable tree and organophosphate, or carbamate insecticides. Leafhopper-active con- increasing labor inputs because of extra pruning to improve esthetic tact insecticides can be used to reduce E. fabae abundance and damage appearance and train a central leader (Townsend 1989). (Potter and Spicer 1993). However, multiple applications per season Management. Arrival of potato leafhopper adults migrating from may be needed to keep E. fabae below damaging levels. Alternatively, the gulf coast can be monitored using yellow sticky cards above the recent research indicates that systemic neonicotinoid insecticides ap- canopy of maples (Potter and Spicer 1993). These traps should be plied as a drench can provide effective E. fabae control for 2 yr (Table deployed around 540–640 DDC (base 4.4°C) to detect arrival of 1) (Oliver et al. 2009). Systemic insecticide drenches need to be migratory E. fabae adults (Medler 1957, Mussey and Potter 1997, applied before E. fabae arrival. DeGooyer et al. 1998). Armored Scale (Hemiptera: Diaspidae). Scale insects are among the Host plant resistance can play an important role in managing E. most difficult pests to control in nurseries and landscapes (Adkins et fabae and their damage. One study found that, red and Freeman maple al. 2010). Armored scales can be differentiated from soft scales cultivars that break bud earliest in spring supported the lowest num- (Hemiptera: Coccidae) in two ways. Armored scale tests can be bers of E. fabae and sustained the least injury during the growing separated from the scale body beneath (Fig. 14) and armored scales do season (Townsend and Douglass 1998). Higher levels of foliar nutri- not produce honeydew, whereas soft scales do. In general, armored ent content, particularly nitrogen, may predispose maples to injury scales are sedentary, except for the first instar after eggs, called because of increased oviposition, nymphal survival, and development crawlers. Armored scales may settle on tree leaves or bark depending rate (Bentz and Townsend 2003). A recent study found red maples to on the species. They insert long thread-like mouth-parts into plant MARCH 2013 FRANK ET AL.: INTEGRATED PEST MANAGEMENT (IPM) FOR MAPLE TREE PESTS 7

Deleware, Georgia, Kentucky, Maryland, New Jersey, Pennsylvania, Rhode Island, Tennessee, Virginia, and Washington, DC. (Gill et al. 2011). Lopholeucaspis japonica has a wide host range that includes Japanese maples, red maples, paper bark maples [(Acer griseum (Franchet)], sugar maples, and many other tree species (Miller and Davidson 2005, Gill et al. 2011). Adult L. japonica tests are 1.0–1.8 mm long and oyster-shell shaped (Fig. 16). Tests are brown but appear white because of a white wax coating. Beneath the test, eggs, imma- tures, and adults are generally purple (Gill et al. 2011). Immature L. japonica overwinter on the trunks and branches of host plants and mature to adults in spring (Miller and Davidson 2005). Although the lifecycle of this pest has not been fully examined, it has two generations per year in Maryland, Virginia, and Kentucky (Miller and Davidson 2005). Starting in late March to early April, female scales begin laying up to 25 eggs. Eggs develop during April and May. Egg hatch and crawler emergence occur around mid-May for the first generation and in early August (Tennessee) for the second generation (Fulcher et al. 2011). Management of L. japonica is especially diffi- cult for two reasons. Two generations of crawlers emerge over 8–10 wk each so there are always multiple, overlapping generations and life Fig. 15. Dense population of gloomy scales on the bark of a red stages (Fulcher et al. 2011, Gill et al. 2011). In addition, first instars maple street tree. Photo: S. D. Frank, North Carolina State begin to form a waxy cover just 3 d after egg hatch, which protects University. them from insecticides. In Tennessee, crawler hatch has coincided with Syringa reticulata (Blume) H.Hara ‘Ivory Silk’ and Hydrangea quercifolia Bartram (oakleaf hydrangea) flowering (Fulcher et al. 2011). Management. Natural enemies are an important factor that help regulate armored scale abundance in urban landscapes, although the role of parasitoids in suppressing scales on maples in particular is less known (Luck and Dahlsten 1975, Tooker and Hanks 2000, Raupp et al. 2001). Likewise, very little research has investigated the role of parasitoids in commercial nurseries. Best management is achieved when natural enemies are protected from contact with insecticide spray or residue (McClure 1977, Raupp et al. 2001). Contact insec- ticides kill natural enemies but not mature armored scales, sometimes resulting in scale outbreaks (Luck and Dahlsten 1975, McClure 1977, Raupp et al. 2001). Armored scale control is most successful when insecticide appli- cations coincide with crawler emergence. This is particularly true when using contact insecticides. Plant trunks and branches can be inspected any time of year to scout for adult and immature scale covers. Crawler emergence may be predicted by growing degree-day models or observing plant phenology (Mussey and Potter 1997, Fig. 16. Lopholeucaspis japonica infestation. Photo: Brian Kunkel, Hodges and Braman 2004). Crawler activity can be confirmed by University of Delaware, Bugwood.org. flipping over scale tests to look for eggs and crawlers or by placing double-sided tape around branches to capture crawlers as they move. tissue to feed on parenchyma cells. Armored scale infestations reduce Very little research has been conducted on management of M. plant growth and can cause branch die-back and crown thinning. In tenebricosa, L. japonica, and other armored scales of maple produc- addition, scale tests are esthetically objectionable even if the insects tion or nurseries in general. However, research on other armored scale are dead. Maples are hosts for over 22 armored scale species (Miller species in landscapes and nurseries demonstrated the efficacy of and Davidson 2005). We have selected those most common and horticultural oil and reduced risk insecticides, such as insect growth damaging species in nurseries and landscapes to discuss here. regulators and some neonicotinoids, as alternatives to pyrethroid and Gloomy scale, Melanaspis tenebricosa (Comstock), occurs in organophosphate insecticides (Table 1) (Rebek and Sadof 2003, much of the eastern and midwestern United States (Miller and Da- Raupp et al. 2008, Frank 2012). vidson 2005) where it lives on the trunk and branches of maple trees. Soft Scale (Hemiptera: Coccidae). Soft scale insects feed on plant Gloomy scale tests are convex, gray, and occur in dense patches (Fig. phloem and excrete a carbohydrate-rich waste solution called honey- 15). Tests of females have a dark spot (shed exoskeleton) near the dew. Many soft scale species migrate from branches to leaves in the center whereas male tests have a spot near the edge. Under the test, spring and back again in the fall, although many others are sedentary scale bodies are yellow to orange (Fig. 14). except for the crawler stage. Soft scales damage trees by reducing the Melanaspis tenebricosa primarily overwinter as adults. In early amount of energy available for storage and growth. Twigs and summer, crawlers become active for 6–8 wk. They have one gener- branches will begin to die on trees with soft scale infestations, result- ation per year with crawlers active throughout June and July or later ing in a sparse and unshapely canopy. Large, long-term infestations depending on geographic location (Miller and Davidson 2005). can kill trees. Honeydew causes esthetic damage because it grows Lopholeucaspis japonica Cockerell (Fig. 16), probably was intro- sooty mold on the tree or plants below the tree. Honeydew also lands duced to the United States from Asia. Currently, L. japonica is found on cars and other surfaces below infested tress, which becomes a in several eastern U.S. states, including portions of Connecticut, nuisance to some homeowners. Soft scale products such as exoskel- 8 JOURNAL OF INTEGRATED PEST MANAGEMENT VOL. 4, NO. 1

Fig. 19. Nymphal and adult Pulvinaria spp. overwintering on red maple branches. Photo: A. G. Dale, North Carolina State University.

Fig. 17. Adult female Pulvinaria acericola with egg mass on red maple street tree. Photo: S. D. Frank, North Carolina State University.

Fig. 20. Adult calico scales, Eulecanium cerasorum, on a maple Fig. 18. Adult female Pulvinaria innumerabilis, with egg masses. trunk behind a support stake. Photo: Amy Fulcher, University of Photo: Eugene E. Nelson, Bugwood.org. Tennessee, Knoxville. etons and ovisacs can also reduce the esthetic value of nursery and Kentucky, nymphs molt into adults and begin producing eggs. Crawler landscape plants. Maple species are hosts for many soft scale species activity begins 4–6 wk later, corresponding to around 818 DDC (base (Johnson and Lyon 1988). We will focus on those particularly com- 4.4°C) (Hubbard and Potter 2005). Crawlers are active for 2–3 wk and mon or damaging in nursery production. settle on the undersides of leaves where they feed all summer. In fall, Pulvinaria acericola Walsh and Riley (Fig. 17), and cottony maple second instars migrate back to stems to overwinter. Hedge maples, scale, Pulvinaria innumerabilis Rathvon (Fig. 18), infest leaves and Acer campestre L., and sugar maple appear to support particularly branches of several maple species including A. rubrum, A. sacchari- large E. cerasorum infestations whereas susceptibility of red, Free- num, A. negundo, and A. saccharum (Putnam 1880; Johnson and Lyon man, and other maples varies by cultivar (Seagraves et al. 2012). 1988). Nymphs overwinter on maple twigs and develop to adults in Terrapin scale, Mesolecanium nigrofasciatum (Pergande), is a na- spring (Fig. 19). Female scales lay eggs in cottony masses that become tive scale species that occurs primarily in the eastern and midwestern oblong as the female crawls forward laying eggs behind (Fig. 17). United States. It attacks over 30 plant species but is most common on After oviposition, the female dies and her body remains attached to maple and Prunus spp. (Simanton 1916). Mesolecanium nigrofascia- one end of the cottony egg mass. Nymphs hatch after 15–19 d and tum are 3–4 mm and brown or reddish-brown and distinctively settle along leaf veins to feed. Nymphs molt into second instars after marked with radiating black bands (Fig. 21). Adult females produce a month or so and migrate to twigs in early fall. Pulvinaria acericola eggs in spring and crawlers emerge in early summer over Ϸ4wk egg hatch corresponds with 1044 DDC (base 4.4°C) (Mussey and (Simanton 1916). Crawlers feed on the undersides of leaves until late Potter 1997). Pulvinaria acericola is distributed throughout the east- summer, then third instars migrate back to twigs in fall. Mature and ern United States. Pulvinaria innumerabilis occurs in every state immature females overwinter (Simanton 1916). (Johnson and Lyon 1988). Management. Soft scale management is similar to that outlined for Calico scale, Eulecanium cerasorum Cockerell, attacks Acer spp. armored scale. An important difference is insecticide efficacy. Many and many other ornamental plant species in the eastern United States soft scale species can be controlled with systemic insecticides that do and some western states (Hubbard and Potter 2005). Adult E. cera- not kill armored scale (Sadof and Sclar 2000, Rebek and Sadof 2003). sorum are black or dark brown and white in a distinct geometric Mesolecanium nigrofasciatum, E. cerasorum, and other soft scales can pattern (Fig. 20). Eulecanium cerasorum has one generation per year be heavily parasitized in landscapes (Hubbard and Potter 2005; Vanek and overwinter as second instars. In early spring, about April in and Potter 2010), although the role of natural enemies in nurseries is MARCH 2013 FRANK ET AL.: INTEGRATED PEST MANAGEMENT (IPM) FOR MAPLE TREE PESTS 9

Fig. 21. Adult terrapin scale, Mesolecanium nigrofasciatum. Photo: Fig. 23. Red velvety leaf galls formed by gall mites, Aceria elongates. United States National Collection of Scale Insects Photographs Photo: Ronald S. Kelley, VT Department of Forests, Parks and Archive, USDA Agricultural Research Service, Bugwood.org. Recreation, Bugwood.org.

Eriophyid Mites. Across the United States, more than 30 eriophyid mite species use maples as host plants (Parrott 1908, Hodgkiss 1913, Hodgkiss 1930). These are primarily an esthetic concern on managed landscape trees (Johnson and Lyon 1988) and are not a concern in nurseries because of short tree production cycles. Plant injury from gall-forming eriophyid mites occurs in response to salivary fluids injected through mouthparts into plant cells. Most gall forming mites on maple overwinter beneath loose bark, in bark crevices, and beneath bud scales (Parrott 1908, Johnson and Lyon 1988, Patankar et al. 2012). The most frequently encountered and disfiguring eriophyid mites are discussed. Aceria elongatus Hodgkiss, gall mites, affect foliage near the trunk and larger branches. In early spring, leaves develop greenish to bright red, velvety galls (Keifer et al. 1982; Fig. 23). As mites mature, they move to new leaves and repeat the process but mite activity declines as in midsummer (Johnson and Lyon 1988). Although the galls are very noticeable, they generally do not reduce tree health (Johnson and Lyon 1988). Aceria negundo Hodgkiss mites occur throughout the Fig. 22. Galls on maple leaf caused by Acericecis ocellaris. Photo: United States. They cause blistered white patches on maple leaves (A. William M. Ciesla, Forest Health Management International, negundo; Keifer et al. 1982, Johnson and Lyon 1988). Many other Bugwood.org. erineum gall mites occur within different maple species and these are generally of minor economic and esthetic importance (Hodgkiss 1913, Johnson and Lyon 1988, Lindquist et al. 1996). not well understood. Outbreaks of soft scales can occur when contact Maple bladder gall mite, Vasates quadripedes Shimer, occurs insecticides or ants kill natural enemies (Merritt et al. 1983, Vanek and mostly on foliage of red and silver maple trees. The galls are solitary, Potter 2010). hollow, and have a small exit hole on the leaf underside (Fig. 24). Biology and Management of Important Gall-Forming Insect and Galls vary in size and color and may cause leaf surfaces to become Mite Pests. Acericecis ocellaris Osten Sacken (Diptera: Cecidomyii- distorted and senesce prematurely (Keifer et al. 1982). dae), larval feeding results in formation of an ocellate (single-spotted), Vasates aceriscrumena Riley, is most commonly a pest of sugar pale green to yellow, often bright red-margined gall (Fig. 22). Galls maple trees. Adult mites emerge from overwintering sites beneath are 5–6 mm in diameter and occur primarily on foliage of red maples bark and in leaf buds in late April to early May (Hodgkiss 1930, but also A. saccharinum, Acer spicatum Lamarck, and Acer pennsyl- Patankar et al. 2012) and begin feeding on new leaves. In southeastern vanicum L. (Osten Sacken 1862, Felt 1911, Gagne´1983). Gall mar- Ontario, solitary leaf galls are fully formed within Ϸ17 d (Patankar et gins become brown as they age (Johnson and Lyon 1988). Adult al. 2012). In the southeastern United States, galls appear about mid- midges emerge in early summer and lay eggs on abaxial leaf surfaces May. Eggs are laid shortly after galls become visible. Egg abundance (Johnson and Lyon 1988). Galls, which appear in late May and early peaks in late June to early July. Adults emerge from exit holes on leaf June in the eastern United States (Gagne´ 1983), contain a single, undersides in July and either disperse to new trees or move toward midge larva that attaches to the leaf surface at the center of the gall branches in search of overwintering sites (Parrott 1908, Keifer et al. (Osten Sacken 1862, Johnson and Lyon 1988). Larvae exit the gall and 1982, Patankar et al. 2012). By late July, galls may no longer contain drop to the ground to overwinter as pupae (Johnson and Lyon 1988). live mites (Johnson and Lyon 1988, Hale 2003, Patankar et al. 2012). Management. Occurrence of these galls may cause esthetic concern Spindles produced by V. aceriscrumena mites vary from pink to but generally do not harm trees. Thus, management is not usually crimson, yellowing later in the season (Fig. 25). They are Ϸ1 cm long, necessary but adult midges can be controlled by contact insecticides slender, and attach to the leaf surface often by a narrow stalk (Keifer applied in early May to coincide with emergence from pupae over- et al. 1982, Johnson and Lyon 1988, Hale 2003). In the landscape, the wintering beneath trees (Table 1). proportion of tree canopy foliage damaged from V. aceriscrumena 10 JOURNAL OF INTEGRATED PEST MANAGEMENT VOL. 4, NO. 1

different red maple cultivars, with Freeman maples sustaining the greatest levels of mite feeding injury, although resistance or tolerance mechanisms are not known (Seagraves et al. 2012). To our knowl- edge, efficacy provided by available miticides has not been tested.

Integration of Management Tools for Maple Pests in Nurseries and Landscapes Scouting and Monitoring. Many key pests of maple trees can be monitored or trapped using commercially available or easily made traps as discussed in individual pest sections above. The development or activity of many pests can be predicted using plant phenological indicators or degree-day accumulations, but this information is lacking for many pests such as ambrosia beetles, maple spider mites, and some scale species. In addition, most research and development of these predictive tools were conducted in the midwestern United States, such as Kentucky (Mussey and Potter 1997) and Ohio (Herms 2004) and thus may not be accurate in other parts of the country. Fig. 24. Bladder galls on the top of a maple leaf caused by maple Host Plant Resistance Effects on Pest Abundance and Damage. bladder gall mite, Vasates quadripedes. Photo: Cheryl Moorehead, Maple species and cultivars show different levels of resistance or individual, Bugwood.org. tolerance to arthropod pests (Seagraves et al. 2012). Host plant resis- tance has been studied most extensively for potato leafhoppers com- pared with other key maple pests. Research has found that Norway and sugar maples are less susceptible to E. fabae damage than red maples (Potter and Spicer 1993). Freeman maples are less susceptible to E. fabae damage than many red maple cultivars but the mechanisms for resistance or tolerance are not well understood (Potter and Spicer 1993, Townsend and Douglass 1998, Bentz and Townsend 1999). For example, a red maple clone with the second highest damage rating was among the least preferred for oviposition and a poor host for nymphal development (Bentz and Townsend 1999. These differences suggest that some maple species or cultivars may be able to tolerate E. fabae feeding via compensatory mechanisms whereas others may have chemical or physical defensive traits that disrupt E. fabae biology (i.e., development, fecundity, survivorship) and/or behavior (i.e., prefer- ence). Maple species and cultivars may be resistant to one pest but not others. Thus, when research is available, growers and landscapers need to select cultivars based on the most important pest in their area Fig. 25. Red maple leaves with extensive stippling damage from or growing conditions. maple spider mites. Photo: S. D. Frank, North Carolina State Klingeman (2002) demonstrated considerable variation in suscep- University. tibility of maple species and cultivars to feeding by T. ephemeraefor- mis. Red and Freeman maple cultivars also differ in susceptibility to increases as sugar maple trees age (Thomas et al. 2010). Infestations damage by O. aceris, Japanese beetles (Popillia japonica Newman), that result in 35% or more foliage with galls can reduce photosynthesis C. femorata, P. aesculana, and E. cerasorum, indicating resistance to and radial expansion (Patankar et al. 2011). one pest is not correlated with resistance to other pests (Seagraves et Management. Eriophyid mites are primarily an esthetic concern al. 2012). More research is needed to document the resistance of among maple trees established in the landscape and seldom require popular maple species to important pests so growers and landscapers management in commercial production systems. Dormant horticul- can make informed decisions when selecting maple species or tural oil can be applied to bark before leaf buds break in early spring. cultivars. After bud break, upper and lower leaf surfaces can be treated with Plant Culture Effects on Pest Abundance and Damage. Nutrient and insecticides to target actively feeding mites (Hale 2003). water stress influence plant health and susceptibility to pest attack Maple Spider Mite. Maple spider mite, Oligonychus aceris Shimer (Mattson and Haack 1987, Herms and Mattson 1992). Nutrient stress (Acari: Tetranychidae) is a frequent and damaging pest of maples in in maples can occur because of over- or underfertilization (Rose and nurseries and landscapes throughout much of the United States (John- Biernacka 1999) or, most typically, high soil or container substrate son and Lyon 1988). Oligonychus aceris overwinter as eggs on the pH, which influences nutrient availability (Altland 2006). Increasing bark of maple trees. Eggs hatch in spring and mites move from nitrogen fertilization can reduce plant defenses and increase the ni- branches to feed on the underside of leaves (Johnson and Lyon 1988). trogen content of plant tissues making them more attractive or nutri- Spider mites damage plants by piercing leaves and drawing out cell tious for arthropod pests (Herms and Mattson 1992). For example, contents resulting in brown stippling on leaves (Fig. 25). This piercing increasing nitrogen fertilization in two red maple clones increased E. process gives the plant a bronze cast in summer and reduces fall color fabae oviposition rate (Bentz and Townsend 2003). (Fig. 25). Mite feeding reduces photosynthesis and thus plant growth Water stress and physical plant damage can also increase tree in other plant species (Park and Lee 2002, 2005), although no research susceptibility to pests (Ranger et al. 2013). In a series of experiments, has been conducted specifically on O. aceris. maple trees were found to be more susceptible to C. femorata borer Management. Oligonychus aceris is a greater problem on trees that attack after stress caused by root pruning, trunk damage, and defoli- have been sprayed with pyrethroids targeting ambrosia beetles, potato ation (Potter et al. 1988). Appropriate planting depth is critical to leafhoppers, and other pests (Frank and Sadof 2011). In addition, there reduce tree stress and improve growth. In recent years, surveys of are considerable differences in the amount of damage incurred by various arboreta found that 75–93% of professionally planted trees MARCH 2013 FRANK ET AL.: INTEGRATED PEST MANAGEMENT (IPM) FOR MAPLE TREE PESTS 11 had root collars covered with either soil or mulch (Wells et al. 2006). exotic ants that collect their honeydew (Brightwell and Silverman In a study conducted by Wells and others (2006), ‘October Glory’ red 2010, Vanek and Potter 2010). Protection of scales by ants increases maples planted below grade by either 15 or 31 cm had 48 or 71% of scale abundance by reducing natural enemy abundance, predation, and their trunk circumference surrounded by girdling roots, which reduce parasitism. Increased scale abundance because of protection by ants water transport efficiency and increase plant stress. In contrast, trees can reduce maple growth and seed set (Brightwell and Silverman planted at grade, in accordance with current tree planting recommen- 2010). Because of the number of soft scale species on maple trees, ant dations, had only 14% of their trunk surrounded by girdling roots. management is an important aspect of IPM in nurseries and Leaf chlorophyll was lower in maples planted below grade in com- landscapes. parison with those planted at grade, which would reduce photosyn- Chemical Control Considerations in Maple Pest Management. Nurs- thesis. Deep planting not only results in poor growth but can also be ery growers and landscapers frequently use broad spectrum, contact a significant source of stress, which may increase plant susceptibility insecticides such as pyrethroids, organophosphates, and carbaryl to pests (Smiley and Booth 2000). (LeBude et al. 2012). Reliance on this short-list of pesticides persists Research is still needed to determine how irrigation and fertiliza- despite numerous reduced risk insecticides, such as IGRs and neoni- tion practices implemented by nursery growers affect the abundance cotinoids, that have become commercially available to both nursery and damage by key maple pests such as soft and armored scale insects. growers and landscape managers in recent decades. Many reduced risk Research is also needed to determine how irrigation and fertilizer insecticides, such as IGRs, have equal or better pest control efficacy affect host location and selection by coleopteran borers and other when compared with organophosphates and pyrethroids, and are less highly mobile pest species. This information would help growers and toxic to natural enemies (Frank 2012). Likewise, horticultural oil landscapers balance the potential costs and benefits of water and applications can control some pests as well as or better than pyre- fertilizer inputs. For example, fertilization levels that increase the throids, acephate (Sadof and Sclar 2000, Raupp et al. 2008) and abundance of a particular pest may still benefit plant growth or chlorpyrifos (Fondren and McCullough 2005) with less negative ef- flowering (Chow et al. 2009). Growers for whom that pest is common fects on natural enemy communities (Raupp et al. 2001). may choose to reduce fertilization, whereas growers outside the range Systemic insecticides can provide longer efficacy than contact of that pest or who don’t grow susceptible plants could increase insecticides. For example, management of E. fabae with pyrethroids fertilization. requires several applications per season. In contrast, drench applica- Decision Making. A major hindrance for implementation of IPM tions of imidacloprid or other neonicotinoids protect trees for up to 3 tactics in maple production and maintenance is the lack of economic yr (Oliver et al. 2009). Likewise, applications of systemic neonicoti- and esthetic thresholds to aid in IPM decision-making. Thresholds noids protected maple trees from C. femorata for up to 4 yr compared would help growers and landscape professionals determine when trees with applications of bifenthrin or chlorpyrifos trunk sprays, which may suffer reduced growth or permanent damage and when customers were less effective in the first year and provided no additional pro- may reject a plant or be dissatisfied with landscape treatments. In tection beyond the first year (Oliver et al. 2010). general, client tolerance for pest damage is very low. Consumers Current Use of IPM by Nursery and Landscape Professionals. Sur- prefer healthy-looking plants and are intolerant of even minimal veys by university extension faculty indicate that many nursery and damage at point-of-purchase (Sadof et al. 1987, Raupp et al. 1988, landscape professionals use reactionary, insecticide-based manage- Sadof and Alexander 1993, Townsley-Brascamp and Marr 1995, ment tactics rather than longer-term strategies at the other end of the Glasgow 1999, Klingeman et al. 2000). IPM continuum (Braman et al. 1997, Sellmer et al. 2004, LeBude et Biological Control Opportunities for Maple Pests. Augmentative al. 2012). Adoption of IPM in nurseries and landscapes is hindered by release of arthropod natural enemies for biological control in nurseries the high value of plants and customers’ low tolerance for pest damage. and landscapes has not been well studied. Biological control has been Nursery and landscape professionals also have trouble implementing effective in some nursery and landscape situations but not others IPM practices because they have to manage a diversity of pests on (Raupp et al. 1994, Shrewsbury and Smith-Fiola 2000, Shrewsbury dozens or hundreds of different plant species. In addition, very few and Hardin 2003). Many ecological factors may affect the efficacy of scouting protocols or thresholds have been developed to assist in IPM augmentative biological control in open environments, including em- decision making in nurseries and landscapes (but see Fulcher 2012). igration and intraguild predation (Collier and Van Steenwyk 2004). To Although maples are one of the most common deciduous shade tree our knowledge no research has tested the efficacy of microorganisms, genera grown in nurseries and urban landscapes, our review has such as bacteria (e.g., Bacillus thuringiensis) and fungus (e.g., Beau- identified many key pests that we know very little about. As maples veria bassiana) specifically on maple pests. Because of concerns are likely to remain a major part of urban forests and ornamental about cost, efficacy, and compatibility with insecticide applications, landscapes improving IPM of maple pests should remain an important growers have not adopted biological control as management option topic of research and extension efforts. (LeBude et al. 2012). Protecting natural enemies from the inimical effects of insecticides Acknowledgments is the most reliable way to benefit from biological control services. In We thank the many people who make their pictures available by nurseries, for example, Frank and Sadof (2011) demonstrated that submitting them to the Bugwood Network (www.bugwood.org/). We targeting permethrin applications to tree trunks below the first scaffold also thank Adam G. Dale for contributing his scale pictures to this branches, where ambrosia beetles attack, rather than spraying the publication. The authors thank members of the Southern Nursery IPM entire trunk and canopy increased natural enemy abundance in maple working group, Justin West, Adam Dale, Emily Meineke, and three nurseries and reduced O. aceris abundance later in the season. Con- anonymous reviewers for comments on previous versions of this siderable work in urban landscapes has documented that reducing manuscript. S.D.F. received support from the Horticultural Research natural enemy abundance with insecticide applications can result in Institute and North Carolina Nursery and Landscape Association. outbreaks of scales and other pests (Luck and Dahlsten 1975; DeBach and Rose 1977; McClure 1977; Merritt et al. 1983; Raupp et al. 2001, 2010). References Cited In other cases, ants tending honeydew-producing insects can dis- Adkins, C., G. Armel, M. Chappell, J. C. Chong, S. D. Frank, A. Fulcher, F. Hale, W. Klingeman, K. Ivors, A. Lebude, et al. 2010. Pest management rupt biological control by other natural enemies. In landscape maple strategic plan for container and field produced nursery crops. (http:// trees, research has found that soft scales, such as E. cerasorum and M. www.ipmcenters.org/pmsp/pdf/GA-KY-NC-SC-TNnurserycropsPMSP. nigrofasciatum, were protected from natural enemies while tended by pdf). 12 JOURNAL OF INTEGRATED PEST MANAGEMENT VOL. 4, NO. 1

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