Journal of Integrated Pest Management, (2017) 9(1): 5; 1–16 doi: 10.1093/jipm/pmx029 Recommendations

Under Siege: Ash Management in the Wake of the Emerald Ash Borer

Houping Liu

Pennsylvania Department of Conservation and Natural Resources, Bureau of Forestry, 400 Market Street, RCSOB, 6th Floor, P.O. Box 8552, Harrisburg, PA 17105–8552 ([email protected])

Subject Editor: Dr. Eric Rebek

Received 24 April 2017; Editorial decision 27 October 2017

Abstract A conceptual framework designed to protect and preserve ash trees (Fraxinus spp.) from the emerald ash borer, Agrilus planipennis Fairemaire (Coleoptera: Buprestidae), at the community level was created in Pennsylvania in 2012. Advancements in the most recent Fraxinus systematics, taxonomy, distribution, and biogeography were reviewed. Description, biology, hosts, damage, invasion, spread, and potential impacts of A. planipennis were summarized. Ash resources at risk were identified, and pest status ofA. planipennis was evaluated. Current management strategies for A. planipennis (containment and eradication, host resistance, silviculture, chemical control, biological control, and slow ash mortality) were incorporated into the model plan. A template with step- by-step instructions was made available for communities to develop their own management plans by selecting from four management options (no action, selective management, preemptive management, and aggressive management) to fit their needs. Follow-up training and promotion of the model plan, coupled with technical support and financial assistance to participating communities resulted in 12 finished plans across the state, with more than 7,000 hazard trees removed, 5,000 trees treated, and 3,000 non-host trees planted. Case studies for three communities with implemented plans provided details to the plan development and execution process. The future of ash species and the direction of A. planipennis and ash management in North America are discussed.

Key words: ash management, Fraxinus, emerald ash borer, community

Ash trees (Fraxinus spp.) are commonly found in temperate and sub- northeastern China in the 1950s and 1960s (Zhang et al. 1995, Liu tropical regions from North America to Eurasia. Most of them are large et al. 2003). During the most recent outbreak in the late 1990s, thou- to medium-sized deciduous trees in their habitats, although there are a sands of velvet ash trees along streets and in urban parks were destroyed few evergreen shrubs and small trees adapted to arid environments (Wei in Tianjin City (Zhang et al. 1995). However, when EAB was acciden- and Green 1996). Ash are important timber species in many countries tally introduced to North America in 2002, it wreaked havoc in the where the wood is widely used for the manufacture of tool handles, Great Lakes region and Midwest and Northeast states. baseball bats, furniture, cabinetry, basketry, and solid wood packing This article examines management options for ash trees in the material (Stewart and Krajicek 1973). Cultivars of many ash species wake of EAB by 1) identifying ash resources at risk, 2) evaluating EAB are widely planted in urban communities for their aesthetic beauty and pest status, 3) introducing current management strategies, 4) sharing ability to thrive in those areas (MacFarlane and Meyer 2005). ash management plans from Pennsylvania, and 5) offering general The emerald ash borer (EAB), Agrilus planipennis Fairmaire conclusions and perspectives. Instead of managing EAB populations (Coleoptera: Buprestidae), is a woodboring beetle from northeast Asia over large areas, it is time to direct our limited resources to the pro- (China, Korea, Japan, and Russia’s Far East) (Yu 1992, Haack et al. tection of valuable individual trees and the conservation of the entire 2002, Xu 2003). Synonyms include Agrilus marcopoli Obenberger (in Fraxinus genus. This paradigm shift could have profound impact on China), A. marcopoli ulmi Korosawa (in Korea and Japan), and Agrilus the future directions of EAB/ash management programs nationwide. feretrius Obenberger (in Taiwan) (Jendek 1994). In the native range of EAB, it is generally considered a minor pest of ash species (Yu 1992; Liu Ash Species (Fraxinus spp.) et al. 2003, 2007; Wei et al. 2004; Baranchikov et al. 2008). Outbreaks are rare and only occurred when North American species such as white Systematics and Taxonomy (Fraxinus americana L.), green (Fraxinus pennsylvanica Marsh), and Ash is a group of flowering plants in the genus Fraxinus, one of velvet ash (Fraxinus velutina Torr.) were introduced into northern and the 24 extant genera in the olive family (Oleaceae). The genus was

© The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), 1 which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] Downloaded from https://academic.oup.com/jipm/article-abstract/9/1/5/4830135 by guest on 27 May 2018 2 Journal of Integrated Pest Management, 2017, Vol. 9, No. 1

described by Linnaeus in 1753. More than 450 described taxa Himalayan ash (Fraxinus griffithii C.B. Clarke) in east and southeast (mostly synonyms) have been described since then. Lingelsheim Asia, Chinese ash (Fraxinus chinensis Roxb.) in China, European ash (1920) included 64 species in his monograph, while Jeandroz (Fraxinus excelsior L.) in northern and central Europe to western et al. (1997) placed 34 species in five sections in their study based Russia, narrow-leaved ash (Fraxinus angustifolia Vahl) in southern on internal transcribed spacer sequences of nuclear ribosomal DNA. and central Europe to central Asia, and Manna ash (Fraxinus ornus In a systematic study on the genus, Wallander (2008) recognized 43 L.) in central and eastern Mediterranean. Those not mentioned are worldwide species in six sections (Dipetalae, Fraxinus, Melioides, more limited to certain areas with specific climatic and site condi- Ornus, Pauciflorae, and Sciadanthus) and one group of uncertain tions (Wallander 2008). placement (incertae sedis) (Table 1). This phylogeny of Fraxinus was Ash trees originated from North America in the Eocene (be- later adopted by Hinsinger et al. (2013) except for some differences tween 34 to 56 million years ago [mya]) (Call and Dilcher 1992, in the use of synonyms and the placement of Fraxinus platypoda Jeandroz et al. 1997, Besnard et al. 2009, Hinsinger et al. 2013). Oliv., Fraxinus cuspidata Torr., Fraxinus chiisanensis Nakai, and Dispersal between North America and Eurasia occurred during the Fraxinus spaethiana Lingelsh. Oligocene (between 23 to 34 mya) through a North Atlantic bridge Fraxinus is a monophyletic genus that is separated from others in (the Atlantic track) and the Beringia (the Pacific track) (Wallander the family by the large imparipinnate leaves and one-seeded samaras 2008, Hinsinger et al. 2013). Major events in the biogeographical (Wallander and Albert 2000). There is much variation in leaf morph- history of Fraxinus chronologically include: the appearance of the ology, including shape, size, texture, number of leaflets, and charac- genus in North America, early divergence of section Dipetalae, diver- teristics on leaf margin, petiolule, indumentums, epidermal papillae, sifications of sections Melioides and Pauciflorae, lineage migration rachis wings, etc. among different species. About one-third of the to Asia for the appearance of section Ornus and species F. platyp- ash species are entomophilous (insect pollinated) and two-thirds oda, expansion of section Sciadanthus in Eurasia and into Africa, are anemophilous (wind pollinated). Most anemophilous species divergence of Asian section Fraxinus, backward lineage migration are dioecious (having male and female flowers on separate plants) to North America for the appearance of F. nigra, differentiation of or polygamous (having male, female, and bisexual flowers on the F. mandshurica in Asia, and lineage expansion to Europe for the same plants). Most entomophilous species are androdioecious (both diversification of section Fraxinus though Eurasia (Jeandroz et al. bisexual and male flowers on the same plant), whereas a few are 1997, Wallander 2008, Hinsinger et al. 2013). hermaphrodites (both male and female flowers on the same plants). The ash flower is small with one pistil and two stamens. It may or may not contain a corolla and calyx. If present, the synsepalous EAB (A. planipennis Fairmarie) calyx is small, cup-shaped, and usually dentate, and the corolla is Description and Biology consisted of two or four white, linear and free petals. The petalifer- EAB adults (Fig. 1A) are metallic to coppery–green beetles in the ous flowers of the entomophilous species emerge with leaves from family Buprestidae. The body is slender and elongate, measuring 7 terminal buds in large showy panicles, while the apetalous flowers to 14 mm long. Eggs (Fig. 1B) are cream-colored initially, becom- of the anemophilous species occur before the leaves in lateral or ter- ing yellowish brown before hatching, oval, and measure 1.0 × minal inflorescences. There are four ovules in the syncarpous ovary, 0.6 mm (long axis × short axis). Larvae (Fig. 1 C–E) are white to although usually only one develops into a samara with one seed in- cream-colored and dorso-ventrally flattened with a mostly retracted side (Wallander 2008). brown head and a 10-segmented abdomen. The last abdominal segment has a pair of brown, pincer-like appendages (urogomphi). Distribution and Biogeography Pupae (Fig. 1F) are cream-colored and 7–14 mm long with visible Of the 43 recognized species of ash trees, 16 are found in the United appendages and a slightly curved abdomen (Yu 1992, Chamorro States, 4 in Mexico and Central America, 20 in eastern Asia, and 3 et al. 2012). Closely related species in the same family in North in Europe and western Asia (Table 1). White ash is a mesophytic America include the two-lined chestnut borer (A. bilineatus (Weber)) species ranging from Nova Scotia to Florida, and green ash is native and the bronze birch borer (A. anxius Gory). to the bottomlands from New Brunswick south to Oklahoma. As EAB has a 1- or 2-yr life cycle depending on geographical lo- a hydric species, black ash (Fraxinus nigra Marsh) occurs in bogs, cation and infestation stage. It overwinters as young larvae (2-yr swamps, and other sites with high water tables in eastern Canada generation) or mature larvae or prepupae (1-yr generation) in the and northeastern U.S. Pumpkin ash (Fraxinus profunda (Bush) outer sapwood or outer bark (Yu 1992). In southern Michigan, Bush) is found in floodplains, wet bottomlands, river valleys, and EAB adults begin to emerge in early May with the accumulation low areas in Atlantic coastal plains and interior lowland river val- of 400–500 growing degree days (GDD) based on 50°F and reach leys. Blue ash (Fraxinus quadrangulata Michx.) is an upland spe- peak emergence in early to mid-June at approximately 1,000 GDD cies native primarily to the Bluegrass region of Kentucky and the (Brown-Rytlewski and Wilson 2004). After emergence, adults feed Nashville Basin region in Tennessee. Other noticeable species in the on ash leaf margins for about 2 wk for supplemental nutrition be- United States include Carolina ash (Fraxinus caroliniana Mill.) in fore sexual maturity (Yu 1992). Adults mate 1 wk after emergence. the coastal plains from northeastern Virginia to Florida, Oregon Females lay eggs in bark crevices or between bark layers 2–3 wk ash (Fraxinus latifolia Benth.) along the west coast of Oregon to later. Each female produces 70–80 eggs (Yu 1992, Lyons et al. 2004). southern California, single-leaf ash (Fraxinus anomala Torr. ex. Newly hatched larvae bore directly into the bark until reaching the S. Wats.) and velvet ash (Fraxinus velutina Torr.) in arid areas in cambial region and phloem where they feed, often forming serpen- southwestern United States (Harlow et al. 1991). Worldwide, widely tine galleries under the bark. There are four instars in the larval distributed species include white and green ash in North America, stage. By mid-October, most larvae reach the last instar or become Fraxinus dubia (Willd. ex Schult & Schult. f.) P.S. Green & M. Nee prepupae. Pupation occurs in early April the following year. For in Mexico and Central America, Manchurian ash (Fraxinus mand- those overwintering as young larvae (1st to 3rd instar), pupation shurica Rupr.) in northeastern Asia, Fraxinus floribunda Wall. and may not take place for another year (Yu 1992, Tluczek et al. 2011).

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Table 1. Classification of Fraxinus (Oleaceae) with information on common names, distribution, synonyms, and morphological characteristics

Species Common name Distribution Synonyms Morphological characteristics

Section Dipetalae (Lingelsh.) E. Nikolaev 3 species F. anomala Torr ex. S. Wats. Single-leaf SW USA F. lowelli Sarg., F. potosina T.S. Shrub or small trees w/ simple leaves Brandeg. F. dipetala Hook. and Arn. California SW USA F. jonesii Lingelsh, F. parryi Shrub or small tree w/ two-petal flowers Moran, F. trifoliata (Torr.) Lewis and Epling F. quadrangulata Michx. Blue C & E USA, C Canada Medium-sized tree w/ quadrangular twigs Section Fraxinus 5 species F. angustifolia Vahl Narrow-leafed S & C Europe to F. oxycarpa Willd., F. oxyphylla Mediums-sized tree w/ narrow leaflets & C Asia M. Bieb, F. pallisiae A.J. simple racemes Willmont, F. potamophila Herder, F. sogdiana Bunge, F. syriaca Boiss. F. excelsior L. European N & C Europe to W F. coriariifolia Scheele Large tree w/ polygamous breeding Russia system F. mandshurica Rupr. Manchurian China, Japan, F. nigra ssp. mandshurica (Rupr.) Large tree w/ rudimentary stamens Korea, E Russia S.S. Sun F. nigra Marsh. Black E USA, E Canada Medium-sized tree w/ dark brown winter buds F. platypoda Oliv. China, Japan Medium-sized tree w/ swollen leaf petiole bases Section Melioides (Endl.) Lingelsh 10 species F. americana L. White E USA, E Canada F. biltmoreana Beadle Large tree w/ concave upper edge leaf scar F. berlandieriana DC. Mexican SW USA, Mexico Small tree w/ decurrent samara wings at the base F. caroliniana Mill. Carolina SE USA F. cubensis Griseb. Small tree w/ no terete seed cavity F. latifolia Benth. Oregon W USA F. oregona Nutt. Medium-sized tree w/ pubescent leaves and sessile leaflets F. papillosa Lingelsh. Chihuahuan SW USA, Mexico Small tree w/ papillose abaxial leaf surfaces F. pennsylvanica Marsh. Green C & E USA, Canada Large tree w/ flattened upper edge leaf scar F. profunda (Bush) Bush Pumpkin SE USA F. tomentosa Michx. f. Large tree w/ large leaves, twigs, and samaras F. texensis (Gray) Sarg. Texas SE USA (Texas) Small tree w/ few leaflets and small samaras F. uhdei (Wenzig) Lingelsh. Shamel C America F. cavekiana Standley and Small evergreen tree introduced to Steyerm, F. chiapensis Lundell, Hawaii & California F. hondurensis Standley F. velutina Torr. Velvet SW USA, Mexico F. attenuata M.E. Jones, F. pistaci- Small tree w/ pubescent leaves & aefolia Torr., F. toumeyi Britt petiolulate leaflets Section Ornus (Boehm.) DC. 15 species F. apertisquamifera Hara Japan Small tree w/ slender glabrous branchlets F. baroniana Diels. China Small tree w/ narrow leaflets, apetalous F. bungeana DC. China Shrubs or small tree w/ small leaves F. chinensis Roxb. Chinese E. Asia F. japonica Blume ex K. Koch, F. Medium-sized tree w/ glabrous rhynchophylla Hance branchlets, apetalous F. floribunda Wall. Himalaya, E Asia F. insularis Hemsl., F. retusa Medium-sized tree w/ dense brown to- Champ. ex Benth. mentose buds F. griffithii C.B. Clarke Himalayan SE Asia F. ferruginea Lingelsh, F. for- Small evergreen tree with large showy mosana Hayata, panicles F. philippinensis Merr. F. lanuginosa Koidz. Japanese Japan Medium-sized tree w/ distinctly serrate apetalous leaflets F. longicuspis Sieb. And Japan Medium-sized tree w/ gray-brown Zucc. branchlets F. malacophylla Hemsl. China, Thailand F. retusifoliolata Feng ex P.Y. Bai Small tree w/ brown tomentose leaflets F. micrantha Lingelsh. S flowered Himalaya Large tree w/ small inflorescences, Himalayan apetalous F. ornus L. Manna C & E Mediterranean Medium-sized tree w/ spectacular inflorescences

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Table 1. Continued

Species Common name Distribution Synonyms Morphological characteristics

F. paxiana Lingelsh. Himalaya, China F. sikkimensis (Lingelsh.) Medium-sized tree w/ near quadrangular Hand.-Mazz, F. suaveolens twigs W.W. Smith F. raibocarpa Regel C Asia Shrubs or small tree w/ falcate samaras F. sieboldiana Blume Chinese China, Japan, Korea Medium-sized tree w/ puberulent twigs flowering and leaf rachis F. trifoliolata W. W. Smith China Shrubs or small tree with three leaflets Section Pauciflorae (Lingelsh.) E. Wallander, stat. nov. 5 species F. dubia (Willd. ex Schult Mexico, Guatemala F. pretenensis Lundell, F. Small evergreen tree w/ leaflets & Schult. f.) P.S. Green & schiedeana Schlecht. and Cham containing entire margins M. Nee F. gooddingii Little Goodding’s SW USA, N Mexico Evergreen shrubs/small tree with coriaceous leaves F. greggii A. Gray Gregg’s SW USA, Mexico Evergreen shrubs/small tree with coriaceous leaves F. purpusii Brandegee Mexico, Guatemala F. bicolor Standley Small evergreen tree w/ coarsely serrate and Steyerm, F. vellerea leaflets Standley and Steyerm F. rufescens Lingelsh. Mexico Small evergreen tree w/ ferruginous- tomentose shoots Section Sciadanthus (Coss. et Dur.) Lingelsh. 2 species F. hubeiensis S.Z. Qu, C.B. China Medium-sized tree w/ calyx on apetalous Shang & P.L. Su flowers F. xanthoxyloides (G. Don) Afghan N Africa to China F. dimorpha Coss. and Dur. Shrub or small tree w/ calyx on female DC. apetalous flowers Incertae sedis 3 species F. cuspidata Torr. Fragrant SW USA, Mexico Shrub or small tree w/ flower corollas F. chiisanensis Nakai Korea Medium-sized tree w/ finely serrate leaflets F. spaethiana Lingelsh. Japan Large tree with stout glabrous branchlets

Based on Wallander (2008) with distribution information and morphological characteristics for Asian species from Ohwi, Meryer, and Walker (1965), and Wei and Green (1996). C-central, E-Eastern, W-West, N-North, SE-Southeast, SW-Southwest.

Hosts and Damage 2014). Initial diagnosis attributed this phenomenon to ash yellows, a In China, EAB hosts include F. chinensis Roxb., F. mandshurica Rupr., disease caused by a phytoplasma. However, further investigation in and Fraxinus rhynchophylla Hance (= F. chinensis Roxb.) (Yu 1992, 2002 revealed that A. planipennis was the real causal agent (Haack Xu 2003), as well as introduced Nearctic species such as white, green, et al. 2002). By 2003, at least 5–7 million ash trees were dead or and velvet ash (Zhang et al. 1995, Liu et al. 1996, Liu et al. 2003). In dying in the six-county area in southeastern Michigan (Cappaert Japan, EAB was recorded from F. mandshurica var. japonica Maxim., et al. 2005a, Poland and McCullough 2006). Attempts to contain Juglans mandshurica var. sieboldiana (Maxim.) CK Schneid, J. mand- this pest through regulation were not successful due to the size of shurica var. sachalinensis (Miyabe et Kudo) Kitamura, Pterocarya the infestation, the difficulties in early population detection, the lack rhoifolia Sied. et Zucc., and Ulmus davidiana var. japonica (Rehd.) of effective control methods, and the complexity in quarantine en- Nakai (Akiyama and Ohmomo 1997, Haack et al. 2002). In North forcement. As a result, infestation expanded to surrounding coun- America, EAB has been found on white, green, black, pumpkin, ties in Michigan as well as neighboring states. New detections were and blue ash (Cappaert et al. 2005a), although the white fringetree, reported in Ohio, Maryland, and Virginia in 2003; Indiana in 2004; Chionathus virginicus L. (Lamiales: Oleaceae) was recently added to Illinois in 2006; Pennsylvania and West Virginia in 2007; Missouri its host list (Cipollini 2015, Cipollini and Rigsby 2015, Peterson and and Wisconsin in 2008; Kentucky, Minnesota, and New York in Cipollini 2017). In Europe, EAB was recorded from green ash and 2009; Iowa and Tennessee in 2010; Connecticut, Massachusetts, European ash (Straw et al. 2013, Orlova-Bienkowskaja 2014). EAB and Kansas in 2012; New Hampshire, Georgia, North Carolina, and has the potential to infest all ash species across the globe based on its Colorado in 2013; New Jersey and Arkansas in 2014; Louisiana in invasion pattern observed in the infested areas. 2015; Alabama, Delaware, Nebraska, Oklahoma, and Texas in 2016; Signs and symptoms of EAB infestation include crown thinning and South Carolina in 2017 (http://www.emeraldashborer.info/). and dieback, epicormic shoots, woodpecker damage, bark splits, eggs In Canada, EAB was first confirmed in Windsor, Ontario in under bark, serpentine larval galleries, notched leaflets by adult feeding, August 2002, just a few weeks after its initial discovery in neighbor- D-shaped exit holes, and dead trees (Fig. 2). High larval density even- ing Detroit (Haack et al. 2002). It has since spread to multiple coun- tually leads to host tree mortality within 2–4 yr after canopy thinning ties within the province. EAB was also detected in Quebec in 2008 and branch dieback become evident (Herms and McCullough 2014). (NRC 2016). EAB also found its way to Europe with the first report on green ash in Moscow in 2007 (EPPO 2007, Baranchikov et al. Invasion and Spread 2008, Valenta et al. 2017). Almost all ash trees (green and European) Extensive decline and increasing mortality of native ash trees were in the city have since being killed or greatly damaged (Straw et al. first noticed in Detroit, Michigan in 2001 (Herms and McCullough 2013, Orlova-Bienkowskaja 2014).

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Fig. 1. Agrilus planipennis life stages. (A) adult (7–14 mm in length). (B) Eggs (1.0 × 0.6 mm). (C) 2nd instar larva (10–12 mm in length). (D) 4th instar larva (26–32 mm in length). (E) J-shaped 4th instar larva. (F) Pupa (7–14 mm in length).

EAB is currently found in 31 U.S. states, two Canadian provinces European and Manna ash are usually planted in the 1960s as street (http://www.emeraldashborer.info/) and one Russian city (Straw trees due to their tolerance to salt, drought, and soil compaction et al. 2013, Orlova-Bienkowskaja 2014) outside its native range. to replace American elm killed by Dutch elm disease a few decades Dendrochronological evidence indicated that the U.S. introduc- ago (MacFarlane and Meyer 2005). In Europe, European ash is a tion likely occurred in the 1990s from solid wood packing material high-quality timber species found across the continent (FRAXIGEN (Siegert et al. 2014). Since then, natural dispersal and human-assisted 2005, Dobrowolska et al. 2011). movement of infested logs, firewood, and nursery stocks have played Ash mortality in heavily infested areas could reach 99% within a pivotal role in the rapid spreading of this pest in North America. a few years (Knight et al. 2013). By 2007, an estimated 53 million ash trees in the early infested states of Michigan, Ohio, and Indiana Potential Impacts had been destroyed (Kovacs et al. 2010). Tens of millions more have EAB is the most destructive non-native forest pest to ever invade been killed in those and other infested states since then. The pro- the United States economically due to widespread tree mortality, jected economic cost of satellite populations in U.S. communities associated cost of quarantine regulations, and impact on related was $12.5 billion between 2005 and 2010 with no program to miti- industries, homeowners, and communities (Aukema et al. 2011), gate spread (Kovacs et al. 2011). The potential economic damage surpassing the chestnut blight (Cryphonectria parasitica (Murrill) for urban communities may reach $10.7 billion for the treatment, Barr (Diapothales: Cryphonectriaceae)) and Dutch elm disease removal, and replacement of the 17 million ash trees in 25 states (Ophiostoma ulmi (Buisman) Melin & Nannf and O. novo-ulmi expected to be affected between 2009 and 2019 (Kovacs et al. 2010). Brasier (Ophiostomatales: Ophiostomataceae)). An estimated In Canada, about 1.2 million ash trees are found in 641 communi- 8 billion ash trees are found in U.S. timberland, with a compen- ties. The estimated impact of EAB for the 30-yr time horizon ranged satory value of $282 billion (USDA FS 2008, Poland et al. 2015). from $265 million to $1.2 billion depending on the combination of Green, white, and black ash trees make up 7% of the hardwood spread, treatment, and discount rates (McKenney and Pedlar 2012, stand in northeastern Unites States and eastern Canada (Federal McKenney et al. 2012). These studies did not consider the ash trees Register 2003). Hundreds of millions more trees are estimated in growing in the forest, where white ash is a major component of at various urban communities as cultivars of green, velvet, and exotic least 26 forest cover types (Burns and Honkala 1990). In the Great

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Fig. 2. Signs and symptoms of Agrilus planipennis infestation on ash trees. (A) Crown thinning and dieback. (B) Epicormic shoots. (C) Woodpecker damage. (D) Bark splits. (E) Eggs under bark. (F–H) Serpentine larval gallery. (I) Notched leaflet by adult feeding. (J) D-shaped exit hole. (K) Dead tree.

Lakes states, EAB reversed the growing trend of ash trees in nat- red-bellied woodpecker (Melanerpes carolinus (L.)) and white- ural forests by decreasing ash volume from 12.7 to 3.2 m3/ha and breasted nuthatch (Sitta carolinensis Latham) have shown numer- increasing mortality from 0.1 to 1.4 m3/ha based on inventory data ical increases, while downy woodpecker (Picoides pubescens (L.)) between 2004 and 2009 (Pugh et al. 2011). and hairy woodpecker (Picoides villosus (L.)) declined initially but Profound ecological impact is also expected although it is diffi- exhibited at least temporary increases a few years later compared cult to quantify. Ash trees provide browse, thermal cover, nesting, to pre-infestation populations (Koenig et al. 2013). Canopy space and protection for a variety of wildlife species such as deer, moose, opened by the death of ash trees in many habitats will most likely and turkey. Ash seeds are consumed by ducks, song and game be occupied over time by invasive plants such as multiflora rose birds, small mammals, and insects. The existence of 21 species of (Rosa multiflora Thunb.), oriental bittersweet (Celastrus orbic- ash-feeding moths also depends on the survival of the ash trees ulatus Thunb.), honeysuckle (Lonicera spp.), and autumn olive (Wagner 2007, Wagner and Todd 2016). In addition, 43 native (Elaeagnus umbellata Thunb.) (Herms et al. 2009, Klooster et al. arthropod species associated exclusively with ash for feeding or 2014). This in turn will lead to habitat alteration and species dis- breeding purposes may face high risk of endangerment (Gandhi placement in the ecosystems, which most likely will result in land- and Herms 2010). On the flip side, insectivorous birds such as scape homogenization from the loss of species diversity.

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Ash trees also have cultural importance. Black ash is a valu- breeding program involving resistant non-Nearctic ash species and able cultural and spiritual resource to several Native American allopatric resistant ‘lingering’ green ash in North America has also and First Nation tribes in eastern North America in basket making been established (Mason et al. 2011, Koch et al. 2015). Successful (Reo 2009). Manna production in Sicily, Italy is mostly dependent selection, hybridization, and propagation of resistant genes may lead on manna ash (FRAXIGEN 2005). In China, F. hubeiensis S.Z. Qu, to EAB-resistant ash cultivars in the future. C.B. Shang & P.L. Su is generally used as an important tree species in Bonsai growing (Ming and Liao 1998). Silviculture Cutting and grinding infested ash trees to chips <2.5 cm in two dimen- Current EAB Management Strategies sions is 100% effective against EAB prepupae (McCullough et al. 2007). About 90% of EAB larvae were found on trees within 100 m Containment and Eradication of the adult emergence points at two outlier infestations in Michigan Containment efforts were attempted in Michigan and Ontario by (Mercader et al. 2009). In addition, large trees of marketable size (diam- federal and state (province) authorities in 2003. Quarantines to limit eter at breast height [dbh] ≥ 26 cm) contributed 55–65% of the total movement of ash trees, logs, and other ash-related materials out of EAB population although they accounted for only 6% of all ash trees the infested areas were enacted to prevent new EAB introductions. (McCullough and Siegert 2007). Therefore, tree removal can eliminate Ash-free zones of 5–10 km wide around known infestations were small satellite EAB populations or reduce the amount of food resources proposed to stop natural spread. In theory, EAB populations can available for potential EAB development in noninfested areas. be reduced via slowed expansion resulting from a lack of suitable EAB-infested logs can still be useful if properly debarked since hosts in the ash-free zones, coupled with high host mortality within larval galleries are constructed at the outer sapwood (ca. 4 cm the core infestation area. However, an ash-free zone was never initi- deep), and pupal chambers are usually found in the sapwood or in ated in the United States because of the difficulty in delineating the the bark depending on bark thickness. If enough bark and wood primary infestation. In Canada, an ash-free zone was established in are removed to eliminate EAB infestations, the logs can be trans- east Windsor by utilizing the natural barriers of Lake Erie, Lake St. ported safely to other areas and provide additional opportunities Clair, and the vast agricultural landscape of the region (CFIA 2004). for wood utilization. However, this effort failed as new EAB populations were soon found beyond the barriers (Herms and McCullough 2014). Chemical Control Eradications of localized satellite populations (outliers) were car- Chemical insecticides are effective against EAB adults and larvae ried out in Michigan, Ohio, Indiana, Maryland, and Virginia in the (Mota-Sanchez et al. 2009, Poland et al. 2016). Individual ash trees United States between 2003 and 2009 for small infestations with can be protected by various chemical insecticides through soil appli- known origins well beyond the quarantine. Infestation at each out- cations, trunk injections, basal sprays, or cover sprays (Herms et al. lier was first delineated through intensive visual surveys and field 2014). Treatment cost can vary from a few dollars to a couple of hun- sampling. All ash trees >2.5 cm in diameter within 800 m of an dred dollars for an average tree (e.g., 30 cm dbh) and is closely related infested tree were then felled, chipped, and burned. Ash stumps were to the type of insecticide, application method, treatment interval, site treated with herbicide to prevent natural sprouting. Overall, EAB conditions, and labor cost. Cover sprays target leaf-feeding adults was eradicated in 19 sites at the average cost of about $500,000/site with contact insecticides such as permethrin, bifenthrin, cyfluthrin, (Poland and McCullough 2006). This strategy was later abandoned or carbaryl (Herms et al. 2014), whereas soil application (injection as program funding became limited and more outliers popped up or drench) uses systemic insecticides (e.g., imidacloprid and dinote- across the country (Herms and McCullough 2014). furan) to target both leaf-feeding adults and phloem-feeding larvae after they are translocated to the entire tree through its vascular Host Resistance system (Mota-Sanchez et al. 2009, Smitley et al. 2010b). Systemic EAB infests only stressed or dying ash trees in its native range (Yu insecticides are also used through trunk injection (e.g., emamectin 1992; Liu et al. 2003, 2007; Wei et al. 2004; Baranchikov et al. benzoate, azadirachtin, imidacloprid, and dinotefuran) or basal spray 2008). However, it attacks apparently healthy trees of all species in (e.g., dinotefuran) for better efficiency (McKenzie et al. 2010, Smitley the introduced areas in North America and Europe. Black, green, et al. 2010a, Herms et al. 2014, Mercader et al. 2015). white, pumpkin, and European ashes are highly vulnerable to infest- Studies showed that trunk injection of emamectin benzoate con- ation (Klooster et al. 2014), while blue ash has showed some degree sistently provides at least 2 yr of EAB control (Smitley et al. 2010a, of resistance (Tanis and McCullough 2012). In Moscow, both the McCullough et al. 2011, Flower et al. 2015, Mercader et al. 2015), introduced green ash and native European ash were attacked (Straw whereas azadirachtin provides 1 or 2 yr of protection depending on et al. 2013, Orlova-Bienkowskaja 2014). pest pressure (McKenzie et al. 2010, Grimalt et al. 2011). Annual Introduced white, green, and velvet ash suffered heavy infesta- basal drenches with imidacloprid provided complete protection of tions in Asia (Zhang et al. 1995; Liu et al. 2003, 2007; Wei et al. small ash trees (dbh < 30 cm) for 3 yr while larger trees (dbh > 2004; Zhao et al. 2005; Duan et al. 2012a). On the other hand, com- 38 cm) continued to decline (Smitley et al. 2010a, b). Annual basal mon garden studies confirmed that Manchurian ash, a species native trunk sprays with dinotefuran protected ash trees up to 56 cm in to China, is more resistant to EAB than white, green, and black ash diameter (McCullough et al. 2011, Herms et al. 2014). Efficacy of (Rebek et al. 2008, Tanis and McCullough 2015). The difference in trunk injection of imidacloprid, soil application of dinotefuran, and EAB resistance between Asian and North America ash species has cover sprays of permethrin, bifenthrin, cyfluthrin, and cabaryl varied been attributed to targeted defenses selected from co-evolutionary among studies conducted at different locations (Herms et al. 2014). history (Liu et al. 2003, Rebek et al. 2008). It was suggested that phloem phenolics and proteomes, and pest physiological response Biological Control might play an important role in host resistance to EAB (Eyles et al. As expected in most invasions, native natural enemies were slow to 2007; Cipollini et al. 2011; Whitehill et al. 2011, 2012; Chakraborty respond to the invasive EAB populations in North America except et al. 2014; Rigsby et al. 2015; Villari et al. 2016). A traditional bark-foraging birds such as woodpeckers. Studies in Michigan

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and Ohio showed that larval predation rates by downy, hairy, with the accumulative costs of treatment substantially lower than and red-bellied woodpeckers achieved 85–95% on some heavily costs of removing dead or severely declining ash trees (McCullough infested trees (Cappaert et al. 2005b, Lindell et al. 2008, Flower and Siegert 2007, Mercader et al. 2009, McCullough and Mercader et al. 2014). Hymenopteran parasitoids such as Spathius flori- 2012, McCullough et al. 2015). danus Ashmead and Spathius laflammeri Provancher (Braconidae), Atanycolus hicoriae Shenefelt, Atanycolus disputabilis (Cresson), Atanycolus nigropopyga Shenefelt, and Antanycolus simplex Ash Management in Pennsylvania Cresson (Braconidae), Leluthia astigma (Ashmead) (Braconidae), Ash is an integral part of the forest in Pennsylvania, with four en- Phasgonophora sulcata Westwood (Chalcididae), and Balcha ind- demic species (green, white, black, and pumpkin) totaling more than ica Mani and Kaul (Eupelmidae) parasitized a small percentage of 300 million trees. A fifth species, blue ash, was recorded previously EAB larvae, whereas generalist predators including Enoclerus sp. but not confirmed. White ash ranked seventh on the top 10 species (Cleridae), Catogenus rufus (F.) (Passandridae), and Tenebroides list by statewide volume in 2011 (McCaskill et al. 2012). As in other sp. (Trogossitidae) were found attacking EAB larvae and pupae in communities across the country, there are millions more ash trees in the field (Liu et al. 2003, Bauer et al. 2004, Kula et al. 2010, Duan urban communities in Pennsylvania (Fig. 3). et al. 2012b). By 2007, a solitary larval-pupal parasitoid, Atanycolus In Pennsylvania, EAB was first discovered in Butler County cappaerti Marsh & Strazanac; (Hymenoptera: Braconidae) was in 2007. Two years later, it was found in eight more surrounding identified from southeast Michigan and has since been frequently counties, including Allegheny. The Pennsylvania Department of observed with relatively high parasitism rates across the region Conservation and Natural Resources (DCNR) initiated a pilot pro- compared to other indigenous parasitoid species (Cappaert and ject in North Park of Allegheny County near Pittsburgh in 2009 to McCullough 2009, 2010; Marsh et al. 2009; Duan et al. 2012b). figure out how ash resources in the Natodami Nature Center can be Additional parasitoids were also recovered from the field. However, effectively managed through a combination of tree removal, chem- the overall parasitism rates of all species are still considered low ical treatment, and biological control. The nature center is a popular (Duan et al. 2009, 2012b, 2013). environmental and educational destination in the county with more To the contrary, exploration surveys in the native range of EAB than 300 acres of forest and open lands. Ash makes up 10–20% of in China, Russian’s Far East, and South Korea resulted in five hyme- the tree species within the forest. EAB was first detected in the park nopteran parasitoids with much higher parasitism of EAB: Oobius in 2009. A total of 713 green ash trees (10.4–94.0 cm in diameter) agrili Zhang and Huang and Oobius primorskyensis Yao and Duan were identified in 15 plots at this site, with a crown dieback ratio (Encyrtidae)—solitary parasitoids of EAB eggs; Spathius agrili Yang ranging from 0.9–59.7%. A total of 17 large trees were removed and Spathius galinae Belokobylskij & Strazanac (Braconidae)—gre- to reduce safety hazard along a major road, whereas 249 trees garious ecto-parasitoids of EAB larvae; and Tetrastichus planipen- (7,279 cm total diameter) were treated with emamectin benzoate nisi Yang (Eulophidae)—gregarious endo-parasitoid of EAB larvae through trunk injection at 14 of the 15 plots in 2010. A total of (Liu et al. 2003, 2007; Yang et al. 2005, 2006; Zhang et al. 2005; 5,429 parasitoids (2,696 T. planipennisi, 1,758 S. agrili, and 975 Belokobylskij et al. 2012; Yao et al. 2016). Two parasitic beetles, O. agrili) were released between June and August at the plot with no Tenerus sp. (Coleoptera: Cleridae) and Xenoglena quadrisignata chemical treatment. Efficacy evaluation in 2011 and 2012 showed Mannerheim (Coleoptera: Trogossitidae) were also recovered from that crown dieback progressed slower on treated trees than that EAB in China (Wang et al. 2016). Oobius agrili, S. agrili, and T. of untreated controls in all but one plot, and six S. agrili cocoons planipennsisi have since been introduced, mass-reared, and released were recovered from a parasitized EAB larva from the release site. at various field sites in most infested states in the United States A second treatment was carried out in 2013. Now the only ash trees and provinces in Canada as part of the EAB biological control found alive in the center are those treated with chemical insecticide program after being evaluated in the laboratory for biology and (H.L., unpublished data). Lessons learned from this project were potential nontarget effects (Gould et al. 2011, USDA APHIS/ARS/ later applied to the development of the community ash management FS 2016). Spathius galinae was added to the release program in plan (Liu 2012). 2016. Field establishment of these parasitoids were confirmed (Duan et al. 2012b) and evaluation of their impact on EAB population are Community Ash Management Plan still ongoing. Other hymenopteran parasitoids recovered during the EAB infestation in the natural forests will certainly lead to lost foreign explorations include Scleroderma pupariae Yang and Yao timber revenues in a few years, whereas dead or dying ash trees in from China (Yang et al. 2012), Atanycolus nigriventris Vonovskaja- urban communities create safety hazards to the public. Removing Krieger from Russia (Belokobylskij et al. 2012), Tetrastichus telon ash from the ecosystem will permanently alter the natural habitats (Graham) from South Korea (Williams et al. 2010), and Spathus for related species, and sudden changes in canopy cover may result polonicus Niesabitowski from Europe (Orlova-Bienkowskaja and in negative impacts to local communities. Addressing these concerns Belokobylskij 2014). requires a well-conceived management plan with specific goals and implementable strategies. SLAM (Slow Ash Mortality) Many infested and threatened communities in the United States A management project, termed SLAM (Slow Ash Mortality), was ini- (e.g., Indiana, Michigan, Minnesota, Ohio, and Wisconsin) and tiated in 2008 with the goal to slow the onset and progression of ash Canada (e.g., Ontario) have developed EAB management plans for mortality in outlier infestations in northern Michigan (http://www. their ash trees based on management goals, pest conditions, avail- slameab.info). Management tools used in the project include girdling able resources, and public support. Pennsylvania benefited directly ash trees to delineate and monitor EAB populations, systemic in- from those plans in the development of its own community ash man- secticide injection to destroy EAB life stages before adult emergence, agement plan. In general, there are four options a community can and tree harvesting to reduce the amount of phloem available for choose from to manage its ash resources in response to EAB infesta- EAB development. Empirical model simulation showed that annual tion: no action, selective management, preemptive management, and treatment of 20% of ash trees protects 99% of the trees after 10 yr, aggressive management. Each option has its own pros and cons and

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Fig. 3. Ash resources in Pennsylvania. (A) Green ash. (B) Pumpkin ash. (C) White ash. (D) Male flowers from white ash. (E) Young seeds from white ash. (F) Blue ash with insets showing corky barks and mature seeds. (G) Narrow-leaved ash (subsp. oxycarpa) with insets showing slender leaflets and hairy midribs. (H) European ash (‘Diversiflora’) with inset showing single leaves.

every community needs to select an option that best fit its situation. community for the protection of its ash resources in the wake of EAB’ No action costs nothing up front but the community is most likely (Liu 2012). Major components of a typical community ash management to be burdened with the cost of hazard tree removal and replanting plan include the title, administration, executive summary, authority, tree afterwards. Selective management involves moderate costs for the inventory, EAB monitoring, management tools, wood utilization, mate- protection of some high-value ash trees in the community and is rial disposal, replanting, outreach, cost/benefit analysis, fiscal planning, complemented by limited tree removal and replacement. Preemptive time table, and data reporting (Table 3). Both urban and forest ash trees management costs the most up front by eliminating risk from can be considered within the plan. Communities large (state, county, EAB through complete tree removal before they become infested. city) and small (township, park, subdivision) throughout the state are Aggressive management costs more over time with the least negative encouraged to develop their own customized plans based on guidelines social and environmental impact from EAB infestation (Table 2). and a template provided in the document (PA DCNR 2012). A community ash management plan is defined as ‘a written Tree inventory is the crucial starting point for any management document specifically drafted to deal with current or anticipated plan. Trees on streets and day-use areas in the community should be EAB infestations in the forest. It contains clear objectives and via- inventoried completely, with key information such as location (lon- ble approaches in the management of ash trees at the commu- gitude and latitude), species, habitat, size (dbh), health conditions nity level. When adopted, it becomes the official action plan for the (crown dieback ratio), and other important information (e.g., tree

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Table 2. Comparison of different ash management options

Management EAB control Wood Canopy Expected results options utilization replacement Mechanical Chemical Biological Pros Cons

No action No No No No No • No upfront cost • Loss of 100% ash trees • Short time decision • Dead tree removal cost • Eliminated EAB problem • Permanent canopy gap • Major habitat disturbance • Lost timber value Selective Yes Yes Yes/No Yes Yes • Saved high-value trees • Loss of woodlot trees • Moderate cost over time • Long-term commitment • Short-term canopy gap • Persistent EAB problem • Minor habitat disturbance • Recouped timber value Preemptive Yes No No Yes Yes • Short-term canopy gap • Loss of 100% ash trees • Recouped timber value • High live tree removal • Short time decision cost • Eliminated EAB problem • Major habitat disturbance Aggressive Yes Yes Yes Yes Yes • Maximum tree protection • High cost over time • Short-term canopy gap • Long-term commitment • Minimum habitat • Persisted EAB problem disturbance • Recouped timber value

value) recorded for every tree; in contrast, trees in the forest should Service to establish a cost-effective process to complete street tree be estimated based on timber metrics (e.g., basal area) and volume inventories, to train communities to develop ash management plans, estimation (e.g., stocking) (USDA FS 2012). A cost/benefit analysis and to assist communities in completing their plans in 2014. All should follow to justify any management decisions to be adopted communities that expressed an interest and desire to respond to EAB by a community. This kind of analysis is relatively easy to carry out infestation proactively were considered. A total of 12 communities in urban communities as street and park trees have compensatory (Easton, Lancaster, Lewisburg, Newton, Philadelphia, Pottsville, values on shade, air quality, storm water discharge, heating/cooling Reading, State College, Wellsboro, Wester Chester, Greenwood costs, and aesthetic or property value (Dwyer et al. 1992, Nowak Furnace State Park, and the State Forest System) were selected after et al. 2002). However, cost/benefit analysis for ash trees in natural careful evaluation of their ash resources, EAB infestation levels, areas and in the forest may require further determination of their and local commitment (Table 4). All 12 communities had the fi- economic and ecological value as forest trees are vital parts of the nancial means and public support to complete the job by their own ecosystem that maintain biodiversity, produce timber, clean the air professional staff. Nine of the 12 communities have tree invento- and water, protect wildlife habitats, and provide recreation oppor- ries in place while three communities were still in need of ash tree tunities. Sadof et al. (2011) developed a web-based cost calculator inventories. EAB was only found in three communities (Lewisburg, using forest sizes and management scenarios to project management Pottsville, and State College). Each community except State College, costs and restoration. They found a combination of chemical treat- Greenwood Furnace, and State Forest was provided with $5,000 ment and tree removal is the most palatable option for the City of seed money to complete its ash management plan. Additional money Indianapolis, Indiana over a 25-yr period. Vannatta et al. (2012) was made available to the three communities without a tree inven- expanded the model by including the net value of the trees. Examples tory. The management plan is usually created by city (borough, state) of cost/benefit analyses for forest settings are found inLiu and Miller forester (arborist, public works director, shade tree commission, en- (2014). vironmental advisory council, entomologist) and administered by city (borough, state) council (committees). Training and Promotion Three i-Tree sessions (Slippery Rock University, Albright College, There are more than 2,500 municipalities (county, city, township, and Kutztown University) were held in 2014 to provide training and borough) in Pennsylvania, but very few have a designated ar- for college students to complete street tree inventory for three local borist and existing tree inventories to guide their tree management communities (Grove City, Reading, and Pottsville). The i-Tree Streets decisions. A lot has been done by DCNR to educate the commu- program is free software developed by USDA Forest Service for com- nities about EAB and its potential impact since its discovery in munities to catalogue and assess the benefit of street trees (https:// Pennsylvania in 2007, ranging from informational meetings to pro- www.itreetools.org/). The completed street tree inventory was used fessional training workshops, and media exposure to public cam- for the development of an ash management plan for each community. paigns. Focus has been shifted to the protection of high-value ash Four EAB sessions (West Chester, Greenwood Furnace, Pittsburg, trees since the creation of the community ash management plan in and Mansfield) were carried out in 2014 to raise public awareness of 2012 as more communities experienced EAB infestation across the the potential impact of EAB on ash resources in local communities. state. To promote the concept of ash management at the community A panel of leading experts and tree care professionals were invited to level within the state, DCNR’s Bureau of Forestry and Urban and speak on EAB biology, damage, survey, and management strategies. Community Forestry Council secured funding from USDA Forest Attendees learned the benefit of urban trees, ash resource inventory,

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Table 3. Major components of a typical community ash manage- including a state forest, a state park, five cities, and five boroughs. ment plan The state forest plan focuses on protecting ash genetic diversity in natural forests, whereas the state park plan emphasizes high-value Component Content tree protection and hazard mitigation for park users. Those two Title ✓ Identify ash management plan specifically for ash plans were completed by DCNR’s Bureau of Forestry staff with add- trees. itional financial support from USDA Forest Service. For cities and ✓ Incorporate ash management into community tree boroughs, the plan focuses on protecting urban trees and reducing care program. risk from dead and dying trees. More than 7,000 ash trees are being Administration ✓ List administrative agencies and removed mechanically, 5,000 trees treated chemically, and 3,000 persons-in-charge. non-host trees replanted in those communities (Table 4). ✓ Form technical teams to tackle each part of the The Borough of State College has been a certified ‘Tree City plan. USA’ since 1984. Complete inventory showed that 342 of its 7,000 Executive ✓ Outline management strategies and goals. summary ✓ Summarize proposed activities and expected street trees are ash trees, including 191 white, 146 green, and 5 un- results. known ash trees. Over half of the ash trees are smaller than 25 cm Authority ✓ Federal and state laws to declare nuisance. in diameter. Those 342 ash trees provide an estimated $81,046

✓ Local ordinances on jurisdiction, inspection, and annual benefit (energy saving, CO2 sequestration, air quality im- nuisance abatement. provement, storm water retention, and aesthetic value) to borough Tree Inventory ✓ Identify ash resources in the community. residents. EAB was first detected in the borough in 2012. The bor- ✓ Evaluate tree conditions and prioritize ash trees. ough completed a 10-yr (2015–2024) ash management plan in 2014 ✓ Create ash distribution maps. to protect its 160 high-value ash trees through chemical treatment, EAB monitoring ✓ By signs and symptoms of infestation (Fig. 2). and to remove and replace the remaining ash trees as they become ✓ By trapping with approved protocols. infested throughout the years. The total cost for this plan is between ✓ By reports from homeowners. Management tools ✓ Mechanical control (e.g., McCullough et al. 2007) $294,713 (low) and $396,715 (high) ($17,933 to $71,046/year) de- ✓ Chemical control (e.g., Herms et al. 2014) pending on chemical treatment options (Eveleth et al. 2015). ✓ Biological Control (e.g., USDA APHIS/ARS/FS Greenwood Furnace State Park is a 170-ha park near the historic 2016) iron-making center in central Pennsylvania. Ash is an integral part of Wood utilization ✓ Timber sale. the park with more than 200 trees in the day-use areas. EAB was first ✓ Salvage sale. detected in the park in 2011. A 10-yr (2012–2021) ash management Material disposal ✓ Quarantines and restrictions on the transporta- plan was developed in 2012 to protect its valuable ash resources and tion of ash materials to mitigate potential risk for park visitors. As of 2016, 15 high-value ✓ Rules and policies on material disposal at local ash trees in the picnic area were protected through chemical treat- marshalling yards. ment, 88 infested ash trees removed, and 127 non-host replacement Replanting ✓ Replacement ratio and time frame. ✓ Replacement species selection. trees planted. In addition, a total of 10,180 EAB parasitoids (3,313 Outreach ✓ Educate the public on EAB damage and ash tree O. agrili, 1,303 S. agrili, and 5,564 T. planipennisi) were released in health a nearby woodlot for potential biological control, with no confirm- ✓ Involve citizens in EAB monitoring, ash manage- ation of parasitoid establishment 2 yr later (H.L., unpublished data). ment, and replanting The total cost for this program is estimated at $115,277 over 10 yr, Cost/benefit ✓ Landscape tree value appraisal (e.g., Nowak et al. with an annual cost of $2,430 to $25,200 (Liu et al. 2012). analysis 2002). The nearly 1-million-ha State Forest system in Pennsylvania was Timber assessments, cruising, and appraisal (e.g., ✓ created to help ensure the long-term health, viability, and productiv- USDA FS 2012). ity of the state’s forests and to conserve native wild plants. A 10-yr ✓ EAB cost calculator (e.g., Sadof et al. 2011, Vannatta et al. 2012). (2014–2023) ash management plan was developed to combat EAB Fiscal planning ✓ Annual budget. infestation in 2014 with the following objectives: 1) manage ash as a Time table ✓ Annual activities component in the forest, 2) protect endangered ash species, 3) miti- Data Reporting ✓ Data collecting and storage. gate potential negative impacts, 4) conserve economic value through ✓ Data analysis. silviculture, 5) manage seed orchards and collecting seeds, and 6) ✓ Annual reports and final report. conduct training and public outreach. The total cost for this pro- ject is estimated at $1,756,100 over 10 yr, ranging from $31,500 to $307,600 annually. The estimated economic benefit for this project Pennsylvania’s changing forest, hazard tree risk management, impact is about $8,100,000, ranging from $560,000 to $1,060,000 annu- of invasive species, economics of EAB control, lingering ash, ash seed ally (Liu and Miller 2014). After 2 yr of implementation, ash still collection and gene conservation, current management tools, chemical count as desirable regeneration species in the forest. A total of 30 and biological control, Project S.L.A.M., ash wood utilization, species endangered pumpkin ash trees are chemically protected. Up to 1,000 selection for replanting, economic analysis of management options, hazard trees were removed from potential targets as part of the risk and management plans from local communities. A chemical treat- management. Harvesting of white ash increased from 2,044 million ment demonstration and field trip to local management areas were board feet (MBF) (4.8% of total harvest) in 2014 to 6,510 MBF also scheduled. A total of 262 people attended the training, including (14.8%) in 2015 and 15,405 MBF (24.5%) in 2016, which gen- resource managers of all levels, arborists, landowners, and educators. erated an extra $4 million timber revenue based on the weighted average price of $224/MBF. Over 200 white ash in a seed orchard Case Studies along with 1,700 white, green, and black ash trees in various forest Between 2014 and 2016, 12 communities in Pennsylvania had types were protected through chemical treatment. Seeds of all indig- developed their own ash management plans based on the template, enous ash species were collected from more than 250 trees and sent

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Table 4. Comparison of the 10-yr ash management plans from different communities in PA

Municipality County Ash resources Mechanic Chemical Biological Canopy Total budgeta Annual budget (no. trees) control control control replacement (1,000$) (low–high) (no. removed) (no. treated) (no. released) (no. replanted) (1,000$)

Easton Northampton 75 32 43 77 4–11 Lancaster Lancaster 390 178 112 356 250 16–50 Lewisburgb Union 249 249 249 175 35 249 108 27 249 61 75 Newton Delaware 261 171 71 242 275–308 4–208 Philadelphia Philadelphia 126,000 5,000 500 2,000 5,331 377–609 Pottsville Schuylkill 46 29 17 58 49 0–14 Reading Berks 502 270 232 270 632 29–141 State College Centre 342 182 160 182 295–397 18–71 Wellsboro Tioga 222 199 23 199 218 7–25 West Chester Chester 124 18 106 9,237 36 181 3–29 Greenwood Huntingdon 200 88 15 10,180 127 115 2–25 State Forest Statewide 300,000,000 1,000 3,650 41,611 0 1,756 32–308 Total 7,416 5,179 61,028 3,719

aBudget in range indicates different chemical treatment options. bScenarios under three management options of remove and replace, chemical treatment only, or remove only.

to USDA Forest Service storage facilities for long-term preservation. are required for the successful management of ash trees under siege Six coordinating meetings and eight field trainings were carried out from EAB. for resource managers and regional foresters for the implementation The question we need to ask ourselves regarding the fate of ash of this plan. In addition, a total of 41,611 EAB parasitoids (16,525 trees in North America right now is: do we want the outcome of Oobius agrili and 25,086 Tetrastichus planipennisi) were released American chestnut or that of American elm? Chestnut blight wiped at three sites for potential EAB biological control. No parasitoid out American chestnut in 50 yr (Griffin 2008). Only isolated trees species has established on those sites at the time of this publication at the edge of its native range escaped infection (Griffin et al. 1983). (H.L., unpublished data). Restoring this foundation tree species requires future scientific advancements (Jacobs et al. 2013). On the other hand, numerous Conclusions and Perspectives magnificent American elms are still around in its native range in The future of ash trees in North America is in peril in the wake of the the United States and Canada thanks to the aggressive preventative introduction of EAB. It is very likely that ash species that originated treatment of Dutch elm disease (Hubbes 1999, D’Arcy 2000). Our on this continent will be eliminated from forests and other major answer to this question will likely determine the action we will take landscapes under siege from this invasive forest pest. Host resistance in our communities. Ash seed does not bank well in the soil (Klooster from native ash species is virtually nonexistent. Chemical control is et al. 2014) and EAB can infest ash seedlings or sprouts as small as effective on individual trees although it can be very expensive and 2.5-cm in diameter (Rebek et al. 2008, Kashian 2016). On the other requires long-term commitment to be successful. Biological control side, despite active recruitments in all study sites, the likelihood of alone may not be enough to protect ash from EAB since even low these saplings and seedlings to become dominant or co-dominant pest densities can still result in high tree mortality. trees in forests appears to be low (Burr and McCullough 2014, It is imperative for communities with a high prevalence of ash Aubin et al. 2015, Kashian 2016). species to take proactive measures and develop ash management It’s common for the states (e.g., Wisconsin and Minnesota) to plans that will preserve ash in the natural forests, save high-value draft a response/preparedness/readiness plan based on the model ash trees in the neighborhoods and woodlots, and preserve the ben- developed by the state of Michigan (MDNR & MDA 2008). While efits of existing urban ash trees. As demonstrated in the case studies objectives and management recommendations are generally agreed above, a well-conceived ash management plan makes sense eco- upon by researchers and resource managers alike, the lack of details nomically, socially, and ecologically. Any community can have an and follow-up support makes implementation of most plans at the ash management plan as long as it values its ash resources. Affluent community level very unlikely. Our plan is unique as it focuses on pro- communities may be better positioned to adopt the management tecting high-value ash trees instead of suppressing EAB populations. plan as they have the resources to implement these strategies. A template with step-by-step instructions was provided to interested However, it is even more important for resource-strained communi- communities, followed by training on conducting tree inventories and ties to respond proactively as no action does not protect them from managing EAB populations. Economic benefits resulting from estab- future costs associated with the removal of dead trees following an lishment of a management plan were pivotal to garner support from EAB infestation. While creating a template with demonstration sites some communities. Established demonstration sites serve as continu- is the crucial starting point for natural resource management agen- ous training grounds for communities to see what to expect down the cies at the federal and state levels, training and promotion is key to road. In addition, Pennsylvania is one of the first states to treat ash successful adoption of the management plan by local communities. trees in natural forests across the state, which will have far-reaching Technical support and financial assistance by government agen- impact on species conservation in the future given the inherently nar- cies and research institutions will jump start the program and help row genetic base of urban trees (Raupp et al. 2006). Although it may guide the process. Community buy-in and long-term commitment be too late to save existing ash trees within the core of the initial EAB

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infestation, ash management plans will be crucial to newly invaded parasitoid of emerald ash borer, Agrilus planipennis (Coleoptera: communities or those yet to experience EAB. Buprestidae). Great Lakes Entomol. 41: 16–29. Cappaert, D., and D. G. McCullough. 2010. Phenology of Atanycolus cap- paerti (Hymenoptera: Braconidae), a native parasitoid of emerald Acknowledgments ash borer, Agrilus planipennis (Coleoptera: Buprestidae). Great Lakes Entomol. 41: 141–154. I thank Andrew Baechle (Allegheny County Parks) for assistance to the pilot Cappaert, D., D. G. McCullough, T. M. Poland, and N. W. Siegert. 2005a. project; Donald Eggen, Ellen Roane, Mark Faulkenberry, and Kendra McMillin Emerald ash borer in North America: a research and regulatory challenge. (DCNR Bureau of Forestry) for training and promotion of the ash community American Entomologist 51: 152–165. management plan; Alan Sam (State College Borough) for sharing their plan; Cappaert, D., D. G. McCullough, T. M. Poland, and N. W. Siegert. 2005b. The Don Coine (DCNR Bureau of State Parks) for assistance to the creation of the upside of the emerald ash borer catastrophe: a feast for woodpeckers, pp. Greenwood Furnace State Park EAB Plan; Scott Miller and Greg McPherson 69–70. In R. Mastro and R. Reardon (eds.), Emerald ash borer research (DCNR Bureau of Forestry) for the development and implementation of the and technology development meeting. FHTET-2004–15. USDA Forest state forest plan, and Robert Beleski (DCNR Bureau of Forestry) for white ash Service, Morgantown, WV. harvest data. Comments and suggestions by anonymous reviewers improved Chakraborty, S., J. G. Whitehill, A. L. Hill, S. O. Opiyo, D. Cipollini, D. this manuscript. Thanks also to the City of Easton, City of Lancaster, Borough A. Herms, and P. Bonello. 2014. Effects of water availability on emerald of Lewisburg, Borough of Newton, City of Philadelphia, City of Pottsville, ash borer larval performance and phloem phenolics of Manchurian and City of Reading, Borough of State College, Borough of Wellsboro, Borough black ash. Plant. Cell Environ. 37: 1009–1021. of West Chester, Greenwood Furnace State Park, and the State Forest System Chamorro, M. L., M. G. Volkovitsh, T. M. Poland, R. A. Haack, and S. for their support. Assistance and support to the state forest plan by foresters W. Lingafelter. 2012. Preimaginal stages of the emerald ash borer, Agrilus and resource managers in DCNR’s Bureau of Forestry are highly appreciated. planipennis Fairmaire (Coleoptera: Buprestidae): an invasive pest on ash Funding for these projects were provided by DCNR and USDA Forest Service trees (Fraxinus). PLoS ONE 7: e33185. grants 10-DG-11420004-337, 13-DG-11420004-100, 14-DG-11420004-191. Cipollini, D. 2015. 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