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Plant Health

Task 5.3. Preparing for pests and diseases

Task 5.3.2. Management of Agrilus planipennis, the emerald ash borer

Review of the Control and Management Strategies for Emerald Ash Borer (Agrilus planipennis)

Rachel Down and Neil Audsley

31st March 2017

Work Package 5 Control

Table of contents

Abstract……………………………………………………………………………………………………………………………… 3

Chapter 1: Introduction (biology, host range, disperal)………………………………………………………. 4

Chapter 2: Surveillance, detection and monitoring.……………………………………………………………. 9

Chapter 3: Chemical control options…………………………………………………………………………………. 21

Chapter 4: Biological control (parasitoids)…………………………………………………………………………. 31

Chapter 5: Microbial control agents………………………………………………………………………………….. 48

Chapter 6: Lure and kill decoys……………………………………………………………………………………….... 53

Chapter 7: Quarantine treatment of wood packaging material and logs…………………………… 55

Chapter 8: Slow Ash Mortality (SLAM) for emerald ash borer management……………………… 56

Chapter 9: Case study - Emerald ash borer in the U.S.A. and Canada....……………………………. 66

Chapter 10: Emerald ash borer in Europe and European Russia..……………………………………… 74

Chapter 11: UK contingency plans……………………………………………………………………………………. 77

Conclusions……………………………………………………………………………………………………………………… 81

Recommendations…………………………………………………………………………………………………………… 84

References………………………………………………………………………………………………………………………. 87

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Abstract

Emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), is a highly destructive insect that attacks and kills Fraxinus species of ash trees. In its native range in Asia emerald ash borer is only a sporadic pest, mainly attacking non native Fraxinus species, leaving the native species of ash unharmed unless already stressed by other factors. In 2002, the beetle was discovered in Michigan (U.S.A.) and Ontario (Canada), and has rapidly spread. In 2007 it was also discovered in Moscow (European Russia). In all instances the beetle was established, with increasing populations, upon discovery and was thought to have been present, but undetected, for several years. In these invaded areas, the native species of ash are highly susceptible to emerald ash borer, presumably because they have not co-evolved with the insect and built up resistance as a result.

When emerald ash borer was first discovered in North America there was very little information available about the pest. Regulatory agencies and scientists were fully aware that if the spread of the pest was to be contained and managed, research would be required to understand its biology, interactions with host plants and natural enemies, and control and management strategies would need to be evaluated.

This review details the research that has been conducted since 2002 in order to develop methods to help with detection, monitoring, management and control of the pest. Personnel in North America quickly realised that the beetle was too established and widespread to make eradication possible, and so in both the U.S.A. and Canada, management now focusses on slowing the rate of spread using a variety of methods determined according to factors specific to each outbreak site. These methods are continually being developed and improved. A range of methods for detection and monitoring of the beetle are available, all with their own advantages and disadvantages. Current methods for suppression of the pest include chemical control (considered appropriate for urban and sub-urban areas) and the use of non-native parasitoid wasps, originally found in China and the Russian Far East, and released into the U.S.A. as part of a classical biological control programme (considered more appropriate in rural and forested areas). In addition, new methods are continually coming onto the scene, for example, decoys capable of attracting beetles and then delivering an electric shock to kill them.

In European Russia the story is very different. There are no official control measures in place because emerald ash borer is not a regulated pest in Russia. This therefore poses a serious concern to the remainder of Europe, which has a continuous distribution of European ash (Fraxinus excelsior L.) throughout. European ash is known to be susceptible to the pest, and as such emerald ash borer is a very serious threat to ash trees throughout Europe. At its current rate of spread it is estimated that emerald ash borer will reach the Russian/Belarus border around 2020, although of course it could enter Europe via human-assisted dispersal at any location and point in time beforehand. It is therefore advised that European countries have robust strategies and contingency plans in place such that if an outbreak was detected, management strategies can be quickly implemented.

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Chapter 1: Introduction (biology, host range and dispersal)

The Emerald ash borer (EAB; Agrilus planipennis Fairmaire (Coleoptera: Buprestidae)) is a xylophagous woodboring insect that attacks and kills ash trees belonging to the Fraxinus species of the Oleaceae family (Poland et al., 2015). It is a native species of Asian countries, including northeastern China, Japan, Korea, Mongolia, Taiwan and Eastern Russia (Cappaert et al., 2005; Haack et al., 2002; Poland et al., 2015). Agrilus planipennis has several synonyms including A. marcopoli Obenberger (1930; type China), A. marcopoli ulmi Kurosawa (1956; type Japan) and A. feretrius Obenberger (1936; type Taiwan) (Haack et al., 2002). In its native range emerald ash borer is generally only considered to be a sporadic pest. However, in North America, Canada and European Russia, where the emerald ash borer is an invasive species, it is a devastating pest responsible for the destruction of tens of millions of ash trees resulting in hundreds of millions of dollars of economic losses in the U.S.A. (Kovacs et al., 2010; Emerald Ash Borer Information Network, 2017).

Biology of emerald ash borer

Adult emerald ash borer emerge in spring (late May – early June depending on location) by chewing D-shaped exit holes (2-4 mm; Straw et al., 2013; Herms and McCullough, 2014). It has been suggested that growing degree day accumulations of 450-550 days (McCullough et al., 2011a; Herms et al., 2014), based on a threshold of 10°C and starting date of 1st January, are required for emergence. Adults are most abundant after 1000 growing degree days (Herms et al., 2014). In contrast, Brown-Rytlewski and Wilson (2005) recorded the start of emergence between 348-584 growing degree days, with peak emergence between 572-1027 growing degree days (all based on a threshold of 10°C) in Michigan, U.S.A. depending on year and location. In 2004 they also noted a second wave of emergence later in the year (mid-August to early September). These data would suggest that other factors may influence the timing of emergence.

The adult beetles feed on the leaves causing crenulation to the edges, but do not cause significant damage to the canopy (Smitley et al., 2010a). The emerald ash borer lifecycle in Michigan, U.S.A. has been documented as follows. Adults live for three to six weeks, and are most active from late June to early July (Cappaert et al., 2005; Herms and McCullough, 2014; Poland et al., 2015, 2016). Reports on timing of mating and oviposition vary. Herms et al. (2014) and Herms and McCullough (2014) both report that they mate after five to seven days of feeding and females oviposit after feeding a further five to seven days, whereas McCullough et al. (2011a) suggests that they mate after seven days and start to oviposit 10-14 days later. Multiple matings can occur (Lyons et al., 2004). The eggs are laid individually in crevices on the bark and sometimes under bark flaps (Herms and McCullough, 2014); initially they are cream in colour but deepen to a reddish brown after a few days (Bauer et al., 2004a; Cappaert et al., 2005). In laboratory conditions the females typically lay 60-90 eggs, although up to 258 eggs during the course of a six week life span has been observed (Lyons et al. 2004; Cappaert et al., 2005). In the field, females typically lay 40-80 eggs (Herms and McCullough, 2014; Poland et al., 2015). Egg hatch occurs in late July/early August after about two weeks (Herms and McCullough, 2014). Larvae grow rapidly, passing through four larval stadia, tunnelling through the cambium layer under the bark, feeding on the phloem and scarring the xylem, resulting in tree girdling, and therefore inhibiting the flow of water and nutrients through the tree (Cappaert et al., 2005; Smitley et al., 2010a; Herms and McCullough, 2014; Poland et al., 2015). Tunnelling leads to

Control and management strategies for emerald ash borer ∣ March 2017 Page 4 the creation of characteristic serpentine galleries (Herms and McCullough, 2014; Poland et al., 2015). Around October/November the larvae stop feeding and excavate a 1 cm deep cell in the sapwood or outer bark and overwinter as prepupal larvae (Cappaert et al., 2005; Herms and McCullough, 2014; Poland et al., 2015). Pupation begins in mid-April and lasts for approximately 3 weeks after which the adults emerge (Cappaert et al., 2005; Herms and McCullough, 2014; Poland et al., 2015).

Usually emerald ash borer has a one year life cycle (univoltine) but in some instances two years are required for its development (bivoltine); understanding the factors that influence voltinism is important as it has implications on the dynamics of emerald ash borer populations and hence implications on survey protocols (Cappaert et al., 2005). Numerous suggestions as to the factors that influence voltinism are under investigation and hypotheses such as cooler climates, low attack densities, vigorous host trees, low nutrient levels or when oviposition occurs in the late summer, have all been suggested (Cappaert et al., 2005; Tluczek et al., 2011; Poland et al., 2015). Winter dissections of trees indicate that bivoltinism may be significant in vigorous, but lightly infested trees, at “outlier” sites with low population densities (Herms and McCullough, 2014), and could be a result of chemical or mechanical defences within the tree slowing down larval development (reported in Cappaert et al., 2005).

It is the larval feeding that is responsible for the decline in health of ash trees. Initially, when low numbers of larvae are present, symptoms of infestation are barely visible (McCullough et al., 2009a; Poland et al., 2011). As infestation levels and larval densities within the tree increase, symptoms become more visible progressing to pronounced thinning of the canopy followed by scattered branch dieback and then death of the above-ground stems and branches (Poland et al., 2011; Herms and McCullough, 2014).

Host range

Fraxinus species are widely distributed throughout much of Asia, Europe and North America. They can tolerate a variety of soil types and stressful conditions (McCullough et al., 2011a) and therefore can be found in rural and urban habitats. In its native range emerald ash borer is reported to attack native species such as Manchurian ash (F. mandshurica Rupr.), Chinese ash (F. chinensis Roxb. and F. rhynchophylla Hance) and Japanese ash (F. japonica Blume ex K. Koch and F. lanuginosa Koidz) (Cappaert et al. 2005). Although no non-ash hosts are reported in China, there are reports from Japan that emerald ash borer can colonise other species besides Fraxinus including Manchurian walnut (Juglans mandshurica Maxim.), wingnut (Peterocarya rhoifolia Sieb. & Zucc.) and Japanese elm (Ulmus davidiana var. japonica Planch) (Haack et al., 2002; Cappaert et al., 2005). In its native range emerald ash borer is only an occasional pest (Liu et al., 2003). However, the introduction and presence of, North American ash species in China has resulted in emerald ash borer outbreaks and increased its pest status (Liu et al., 2003; Liu et al., 2007). These North American ash species include velvet ash (F. velutina Torr.), green ash (F. pennsylvanica Marsh.) and white ash (F. americana L.). In some locations in China a high number (80%) of ash trees have been infested (Yang et al., 2014) resulting in 35% mortality (areas of Tianjin in 2002) (Yang et al., 2014).

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At least 16 North American ash species and several European ash species are thought to be vulnerable to emerald ash borer (McCullough and Mercader, 2012). Ash species native to the invaded areas that have been confirmed as suitable hosts for emerald ash borer include the North American green ash, white ash, black ash (F. nigra Marsh.), blue ash (F. quadrangulata Michx.), pumpkin ash (F. profunda [Bush] Bush), Oregon ash (F. latifolia Benth.) and velvet ash (Herms, 2015). In Europe, emerald ash borer has caused widespread mortality of European ash (F. excelsior L.) (Orlova-Bienkowskaja, 2014; Herms, 2015) and other indigenous European species, such as flowering ash (F. ornus L.) and Raywood ash (F. angustifolia subsp. oxycarpa [M. Bieb. Ex Willd.] Franco & Rocha Afonso) (Herms, 2015). Emerald ash borer preferentially attacks stressed ash trees (McCullough et al., 2009a,b; McCullough and Mercader, 2012), and in its native area the native ash tree species are only attacked when stressed (Rebek et al., 2008; Herms and McCullough, 2014; Poland et al., 2015). However, in invaded areas, such as North America, where the beetle encounters other species of ash tree, it will readily attack and kill healthy specimens of these ash trees (Cappaert et al., 2005; McCullough and Mercader 2012; Herms and McCullough, 2014 Poland et al., 2015). Of the North American species, black, green and white ash are highly susceptible (Cappaert et al., 2005; Herms and McCullough, 2014). Green ash seems to be consistently attacked before white ash, possibly because green ash has a rougher bark with many crevices therefore favouring oviposition, and white ash is attacked in preference to blue ash (Cappaert et al., 2005).

It is thought that the susceptibility of North American and European ash species to emerald ash borer is due to a combination of a lack of the natural defences present in Asian ash trees due to their co-evolution with the insect, and the lack of natural predators, parasites and pathogens outside of the insect’s natural range (Liu et al., 2003; Rebek et al., 2008; McKenzie et al., 2010; Herms and McCullough, 2014; Herms, 2015). Whilst the size of tree does not appear to influence colonisation, field evidence strongly indicates that emerald ash borer is significantly attracted to stressed trees (Cappaert et al. 2005; McCullough et al., 2009a,b). Other factors such as the use of volatiles by females to select oviposition hosts and larval conditioning may also influence attack (Cappaert et al., 2005).

The reports from Japan suggesting that emerald ash borer can develop on some non-ash species have prompted concerns in North America that it could shift to other species such as walnut, elm and hickory in the areas that it has invaded, especially as ash trees decline in numbers from attack. Cappaert et al. (2005) report that laboratory and field studies are ongoing in this respect, and whilst some have demonstrated that female beetles will oviposit in some other species, and that first instar larvae will attempt to feed, they fail to develop (Anulewicz et al., 2008). Laboratory studies have also demonstrated adult feeding and development to second instar larvae on privet (Oleaceae); consequently privet shrubs growing in areas with a high density of infested/dying ash have been monitored for emerald ash borer colonisation in the U.S.A. but no evidence of this has so far been found (Cappaert et al., 2005). More recently field evidence has been discovered suggesting that emerald ash borer can attack and complete its development in the white fringetree, Chionanthus virginicus L. (a native species of the Oleaceae family found in the southeastern U.S.A.) (Cipollini, 2015). A small number of ornamental white fringetree have been discovered that exhibit external symptoms of attack including canopy dieback, bark splitting and adult exit holes; actively feeding larvae were found when the bark was removed, along with evidence to suggest that the trees had already yielded at least three generations of emerald ash borer (Cipollini, 2015). Laboratory bioassays, performed over a 40 day period, have confirmed that white fringetree is an acceptable

Control and management strategies for emerald ash borer ∣ March 2017 Page 6 host, although larvae growing on the white fringetree appear to be smaller than those produced on green ash (Cipollini and Rigsby, 2015). It remains to be seen whether the emerald ash borer can complete its life cycle on the white fringetree only as it has not yet been determined whether the adults are able to mature sexually when feeding on this host species (Cipollini and Rigsby, 2015). The susceptibility of white fringetree to emerald ash borer raises the question of what the pest will do if it exhausts the ash tree resource: will it move to an alternate host? In addition, susceptibility to other tree species will have implications for horticulture and quarantine measures (Cipollini, 2015).

Dispersal

Spread occurs in two ways: long-range through human-assisted transport and short-range natural dispersal when the adult beetles fly to new hosts. Studies in North America have tried to estimate the spread of emerald ash borer in Michigan during the early years of the invasion using dendrochronological methods to establish the year of tree death (Siegert et al., 2014). These authors calculated that the rate of spread, based on ash tree mortality, averaged 3.84 km/year in the early years of infestation (1998-2001) but rose dramatically to nearly 13 km/year from 2001 when the outlier populations started to merge with the invasion front. They also estimated that on average 7.4 new satellite colonies were formed per year and that the average ‘jump’ distance of the colonies was 24.5 km. These dispersal rates are for the years prior to detection and implementation of quarantine measures and therefore will represent a combination of natural and human-assisted dispersal.

Natural dispersal can be affected by a number of factors such as the density and distribution of host trees, flight capability, wind direction, weather conditions and physical barriers; understanding the influences of these factors will lead to better predictions for the natural expansion of the core population and outlier infestations, which in turn will lead to better survey and management methods (Cappaert et al., 2005). Field studies in the U.S.A. so far indicate that natural dispersal from low density outlier sites is less than 1 km/year with the rate of spread increasing to 1.2-1.7 km/year as the infestation level rises (Mercader et al., 2016). As populations build at the outlier sites and dispersal rates start to increase, they eventually merge with each other and the main invasion front (McCullough and Mercader 2012; Siegert et al., 2014). Laboratory studies have shown that in some instances individual beetles are capable of flying for several kilometres (Bauer et al., 2004b; Taylor et al., 2004, 2010; Cappaert et al., 2005); one male beetle flew 5.2 km in 40 hours (Taylor et al., 2004). Taylor et al. (2004) also report that females flew further than males during a 24 hour period, and that mated females flew further (average of 1.7 km/ 24 hours) than unmated females, and suggest this may mean that females are programmed to make dispersal flights. Later laboratories studies by Taylor et al. (2010) demonstrated that the median corrected distance flown by females was more than 3km, with 20% of females flying > 10 km and 1% of females capable of flying > 20 km. However, the results of laboratory studies do not necessarily reflect what happens in the field.

Larval distribution patterns over a single generation at newly colonised sites indicate that the females lay a large proportion (90%) of their eggs within a 100m of the tree from which they emerged and > 97% within 300 m; a single larva was found on a tree 750 m away from the origin (Mercader et al., 2009). However, the authors of this study acknowledged that the particular distribution pattern of ash trees within the study sites (Michigan, U.S.A.) may have acted as a

Control and management strategies for emerald ash borer ∣ March 2017 Page 7 corridor to facilitate beetle dispersal, and that dispersal in areas where ash tree distribution is patchy may well be different. A similar study was performed by Siegert et al. (2010) at two outlier sites, also in Michigan, consisting of heterogeneous landscape (variety of wooded, agricultural, residential and urban). Their study looked at larval distribution patterns from emergence sites up to a distance of 800 m away. They found that 93% of larvae were located within 450 m of the origin, with the furthest infested tree 540 m from the origin at one site and 638 m from the origin at the second site. However, they did not investigate past 800m so it is possible that further infested trees past the 800m boundary were present but not identified. Whilst it is not known what triggers a proportion of females to undertake longer dispersal flights (McCullough and Mercader, 2012), in these studies dispersal was directed towards areas of abundant ash phloem. These authors also note that the health of the ash trees influenced dispersal; one of the study sites included a stressed (girdled) tree located 220 m from the origin, and this tree accounted for 62% of the larval galleries indicating that it was highly attractive to ovipositing beetles. Herms et al. (2014) report that a few female beetles will disperse up to 3 miles away. Satellite populations are more likely to become established when dispersal distances are low, making them harder to eradicate (Robinet and Liebhold, 2009).

It has been demonstrated that on average, infested trees can support the production of 89 emerald ash borer adults/m2 (McCullough and Siegert, 2007); Poland and McCullough (2010) extrapolated from this to suggest that a single 50cm diameter ash tree would be capable of producing 3600-4000 emerald ash borer adults before it dies.

In order to stand a chance of successfully containing a new infestation of emerald ash borer, not only does the infestation have to be rapidly detected, but human-assisted movement also needs to be prevented. In North America, it is thought likely that a high number of the outlier sites were established as a result of infested material being moved before quarantine procedures were in place (Cappaert et al., 2005), and lack of awareness by the general public can still result in unintentional movement (Cappaert et al., 2005). Such movement can be of infested nursery stock, logs and other related products (with or without bark), waste and scrap wood, and hardwood wood chips including wood fuel, wood packaging material, and by the adult beetles hitchhiking on vehicles (Cappaert et al., 2005; Poulsom, 2016). In North America movement of infested firewood has been a huge concern. Adult beetles can emerge from cut ash logs and firewood for up to a year (and occasionally longer) after the wood is cut (Petrice and Haack 2006, 2007; McCullough and Mercader 2012). Outlier sites are typically only discovered when trees start to show the syptoms of infestation i.e. three to four years after the emerald ash borer population (McCullough and Mercader, 2012).

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Chapter 2: Surveillance, detection and monitoring

Due to the aggressive and destructive nature of emerald ash borer, early and reliable detection is crucial. Detecting new infestations of emerald ash borer is very difficult because the early phase of infestation is asymptomatic. Reliable methods for monitoring emerald ash borer populations are also required to be able to accurately delimit infestations once found, and to monitor emerald ash borer dispersal and the effectiveness of any control measures implemented. As such a number of detection and monitoring methods have been developed, and have been reviewed by Ryall (2015). These methods are described below and the advantages and disadvantages of each method summarised in Table 1.

Visual surveying

During the early stages of attack, the D-shaped exit holes tend to be found only in the upper canopy, whilst the other more visible symptoms such as bark cracks, woodpecker attacks, canopy thinning and dieback, and epicormic branching do not become apparent until a tree is under heavy attack (Crook and Mastro, 2010; Herms and McCullough, 2014). Hence, whilst this method is easy to perform and relatively inexpensive compared with other methods, visual surveying is ineffective in the early stages of infestation, often failing to spot infested trees. In addition, symptoms of stress or disease in ash trees can be similar to those of emerald ash borer infestation so surveying for canopy condition alone is not sufficient to confirm the presence of emerald ash borer; adult exit holes, larvae or feeding galleries must also be found for positive confirmation (Ryall, 2015).

Sub-sampling

Sub-sampling methods focus on sampling only a portion of each individual tree for evidence of emerald ash borer infestation. In order for these methods to achieve good detection rates they must ensure that the data obtained from the sub-sampled portion of the tree will reliably detect the presence of emerald ash borer, and accurately predict the density of the infestation within the tree (Ryall, 2015). To this extent prior knowledge of how emerald ash borer are likely to be distributed within each individual tree, especially during the initial stages of infestation are important (Ryall, 2015), and have been investigated during protocol development (Ryall et al., 2011). Aiming for specific areas, which have been shown to correspond well with larval distribution patterns, potentially speeds up the rate of survey as inspectors can concentrate their efforts on these specific areas. If inspectors simply wish to confirm the presence of emerald ash borer they can move on to the next tree as soon as that evidence is found (Marshall et al., 2011; Ryall, 2015).

Sub-sampling by using trunk windows involves peeling back an area of bark from the main trunk of the ash tree at breast height (1.3 m) in order to look for evidence of emerald ash borer life stages and feeding galleries. For example, removing a 10 x 10 cm window of bark from the main trunk is a method that has been reported by Ryall et al. (2011) as having been operationally used. Marshall et al. (2011) report on a study to model the relationship between frequency of emerald ash borer larvae and stem diameter to create a predictive model for detecting emerald ash borer larvae in girdled ash. These authors state that at the time of their study, the most effective detection method available was to use girdled trap trees which are then felled after the end of the adult flight season,

Control and management strategies for emerald ash borer ∣ March 2017 Page 9 and all the bark is peeled down to a minimum stem diameter. Marshall et al. (2011) report that peeling the area of bark within the 8-12 cm diameter section of the trunk of girdled trap trees felled within a few months of the adult beetle flight season should result in finding more than 50% of the larvae infesting the tree whilst at the same time peeling less than 45% of the tree. Their study was conducted at a site with low infestation levels and signs and symptoms of infestation were minimal; tree diameter at breast height (dbh) ranged from 10-20 cm. Marshall et al. (2011) concluded that by concentrating detection efforts on this 8-12 cm diameter section of the tree increased the likelihood of detecting larvae in a reduced amount of time whilst still providing an accurate prediction of larval density within the tree. In comparison, Foelker et al. (2013) studied larval distribution patterns in larger trees (15-25 cm dbh) and found that the optimal part of the trunk to search for emerald ash borer larvae was around 17 cm dbh, corresponding to the part of the trunk that was 1-2 m above the tree base. It should be noted that both Marshall et al. (2011) and Foelker et al. (2013) worked with girdled trap trees, and as such their within-tree distribution patterns are for stressed trees that would have been highly attractive to ovipositing females. Within-tree larval distribution patterns may well differ in ungirdled trees. Others (Tluczek et al., 2011) suggest that debarking the trunk 2-5 m above the ground may be the most efficient way to find larvae as their studies (average tree dbh 10 cm) indicated that larval density was highest in this portion. However, the efficacy of using trunk sampling methods is unknown. Trunk sampling is also aesthetically damaging to the tree (Ryall et al., 2011).

Sub-sampling by branch sampling involves the removal of a specific number of branches from a tree and then peeling back the bark on section(s) of those branches. It is thought than in larger trees, emerald ash borer infestations start in the upper trunk and main branches of the tree before progressing down to the lower trunk (Haack et al., 2002; Cappaert et al., 2005; Ryall et al., 2011). Ryall et al. (2011) established a branch sampling method after developing a sample unit of sufficient size to detect infestation in 75% of asymptomatic trees. The sampling method that they developed was focussed on openly growing asymptomatic urban trees in known infestation areas in Ontario, Canada. Trees were 35-50 years old, 24-34 cm dbh and had large, live crowns. Initially they intensively sampled a total of 97 trees, 47 of which were known to be infested. This intensive sampling revealed that detectability of infestation within branches decreased with increasing distance from the base of the branch. Initially 2x 25cm branch sections were decided upon as potential samle units, one at 0-25 cm and the other at 100-125 cm from the base, but this required a branch of at least 125 cm (Ryall et al., 2011). This sample unit was compared with a 1x 50 cm sample unit at the base of the branch and found not to differ in reliability. The distribution of feeding galleries within a branch was more strongly associated with rough bark and the upper surface (rougher bark is more common on the upper surface), and on larger diameter pieces of branch (basal diameter > 6 cm). In addition, the authors did not observe any differences in detection levels between north and south facing branches in asymptomatic trees, but detectability was significantly higher in the middle crown compared with the upper or lower crown. Seventy five percent of the trees sampled were correctly assessed as infested when two middle crown branches were sampled using a 1x 50 cm sample unit at the base of each branch. When two lower crown branches were additionally included in the sampling a significant improvement in the detection rate was only observed at the lowest density category of infestation (< 8 galleries/m2). Ryall et al. (2011) then compared their branch sampling method with the trunk window method of sampling and found that on average their branch sampling method was 18 times more likely to detect a low density,

Control and management strategies for emerald ash borer ∣ March 2017 Page 10 asymptomatic, emerald ash borer infestation than the trunk window method. It should be noted however, that there were occasions when the branch sampling method failed to pick up an infestation that the trunk window method detected and vice versa.

To conclude, Ryall et al. (2011) demonstrated that sampling two mid-crown branches by removing the bark on a 50cm section at the base of each branch (diameter 5-8 cm) was able to correctly classify the infestation status of 75% of the trees samples when the infestation density was 8-16 galleries/m2. Even at lower densities, at least half of the trees were still correctly classified whereas the bark window method misclassified 84% of the trees as uninfested. Ryall et al. (2011) report that six municipalities in Ontario have now adopted this method of sampling to both detect for the presence of infested trees and to delineate a known infestation. The authors recommend sampling branches in open sunny locations because it is known that traps placed in such locations catch more beetles than those placed in shaded branches. This branch sampling method is more costly than the trunk window method taking approximately five times longer to perform. However, given the potential costs of false negatives the authors suggest that further validation of the cost effectiveness is required. In addition, they point out that the method can be performed at any time of the year (unlike using girdled trees) and can potentially be incorporated into tree maintenance programmes. However, it is important to note that the method was devised for 24-34 cm dbh trees and may need refining for smaller trees in which initial colonisation is more likely to occur on the main stem, and for larger trees that might require a greater number of branches to be sampled (Ryall et al., 2011).

Girdled trap trees

Emerald ash borer adults are highly attracted to stressed trees, and the method of girdling is far more efficient at eliciting the stress response than other stress-inducing treatments such as exposure to methyl jasmonate or herbicide (McCullough et al., 2009a,b; Tluczek et al., 2011;McCullough and Mercader, 2012; Ryall, 2015). Girdling involves deliberately removing a band of bark and phloem around the circumference of the ash tree trunk, in the spring, to attract gravid females, and is proven to be a highly effective method of detecting emerald ash borer, more so even than the currently available traps (Mercader et al., 2013; Ryall, 2015). Girdled trap trees have been used in North America both as detection tools and as part of emerald ash borer management programmes (such as Slow Ash Mortality; SLAM) (Rauscher, 2006; Hunt 2007; Poland and McCullough 2010). Details of such uses are provided in later sections of this review (chapters 8 and 9). Whilst girdled trap trees are highly effective at detecting emerald ash borer, it is a destructive method of sampling. They must be felled and removed in the autumn so that the population of larvae growing within them do not add to the overall population in the area, and this requires a high amount of labour (McCullough and Mercader, 2012). In addition it is not always possible to locate accessible trees suitable for girdling (McCullough and Mercader, 2012).

Biosurveillance

The hymenopteran, Cerceris fumipennis Say (Hymenoptera: Crabronidae), is a hunting wasp present in the eastern states of North America that preys on buprestid beetles. In recent years, research in

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North America has investigated the potential for monitoring the nest of this wasp for the presence of emerald ash borer prey as a means of detecting for the presence of emerald ash borer within the locality, and has shown some success (Ryall, 2015). However, this species of hunting wasp is not known to be present in the UK and as such the use of it as a means of detecting emerald ash borer is not discussed further in this review.

Remote sensing

Remote sensing has been touched upon briefly by Ryall (2015) and involves the collection of image data, often over a large scale and from a distance, for example by aeroplane or by making use of satellite data (Ryall, 2015). It can be used to identify areas of declining ash however, these would then need to be further investigated to confirm whether the decline is due to emerald ash borer infestation. As it is based around mapping declining ash trees, it has very limited use in detecting early infestations, and in addition it is an expensive method to use for detection and not readily available (Ryall, 2015).

Artificial traps and lures

The development of traps and lures for attracting and detecting emerald ash borer populations has been recently reviewed for a Future Proofing Plant Health Euphresco project (Down and Audsley, 2016a). The information in this section is taken from that review.

Progress towards the development of an effective trapping system for emerald ash borer has been reviewed (Crook and Mastro, 2010; Silk and Ryall, 2015). The apparent absence of a long-range sex pheromone means that a highly effective pheromone lure is not available for use in artificial traps; instead mate location is thought to rely on a combination of visual cues and host volatiles (Crook and Mastro, 2010). Lures containing host volatiles are not as effective as pheromones because the emitted lures have to compete with the volatiles that the surrounding ash trees emit (McCullough and Mercader, 2012). Many studies have been conducted to establish the most effective trap type, colour and lure for trapping emerald ash borer, however these studies do not yield consistent results (Crook and Mastro 2010) and the results can be difficult to compare.

Crook et al. (2009) indicated from their studies that green traps (540 - 550 nm wavelength), within the mid-canopy, would be the most effective trap for detecting emerald ash borer adults, perhaps using a lighter green (540 – 550 nm, 64% reflectance) earlier in the season. Likewise, Francese et al. (2010) also concluded that the optimal colour for trapping emerald ash borer was green (530-540 nm wavelength) in the mid-range (22-67%) of reflectance (brightness); 49% reflectance (i.e. a darker green) was more effective than 67% reflectance. However, purple traps (especially the new Sabic purple) have also been found to be attractive to the adults (Marshall et al., 2010; McCullough et al., 2011b; Poland et al., 2011; Francese et al., 2013a), especially the females (Crook et al., 2009; Francese et al., 2008), and especially in areas where population densities are low. Traps of both colours are reported to be more effective at catching emerald ash borer when deployed at a height of 13 m, within the tree canopy, than when deployed at 1.5 m (Crook et al., 2008, 2009).

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Emerald ash borer is attracted to bark and foliage volatiles from ash (reviewed by Crook and Mastro, 2010), including sesquiterpenes emitted from stressed trees. The active compounds within the ash tree bark volatile have been identified as α-cubebene, α-copaene, 7-epi-sequithujene, E- β- caryophyllene, α-humulene (also known as α-caryophyllene), and eremophilene (Crook et al., 2008; Cossé et al., 2008). An oil distillate (Phoebe oil) from the Brazilian walnut, Phoebe porosa Nees & Mart (Lauraceae) contains all six of these compounds. Five of the six compounds are also found in Manuka oil, the oil distillate from the New Zealand manuka tea tree, Leptospermum scoparium J.R. Forst & G. Forst (Myrtaceae) (Crook and Mastro, 2010). Both these oils attract emerald ash borer adults (both sexes) in field trapping studies, with Phoebe oil being the more effective, presumably because it contains 7-epi-sequithujene, which is lacking in Manuka oil (Crook et al., 2008). However, whilst Manuka oil is commercially available, Phoebe oil currently is not (Crook et al., 2014).

A number of components have been identified in ash leaf volatiles, emitted by plants damaged by feeding beetles, and these compounds have been shown to be attractive to emerald ash borer adults in laboratory studies (Rodriguez-Saona et al., 2006). Crook et al. (2014) report that subsequent investigations (Grant et al., 2010, 2011) suggest that one of these components, (3Z)- hexenol (also known as (Z)-3-hexen-1-ol), was able to increase trap catches, especially of male beetles. However, further work now suggests that (3Z)-hexenol only increases trap efficiencies in field studies when light green prism traps (wavelength 540 nm, 64% reflectance) are used; when the improved darker green (540 nm wavelength, 49% reflectance) Sabic prism traps are used, the addition of (3Z)-hexenol does not improve trap efficiency (Crook et al., 2012, 2014). In addition, Crook et al. (2012) indicated that bark volatiles (Manuka oil) may not be synergistic to (3Z)-hexenol when used on green traps. Combining some of the other green leaf volatiles to (3Z)-hexenol does not appear to further enhance trap catches of emerald ash borer (de Groot et al., 2008; Grant et al., 2010). Francese et al. (2013a) report on a large scale study of four trap designs (standard “Program used” purple prism traps, Sabic purple prism traps, Sabic green prism traps and green multifunnel traps (coated with Rain-X); all traps were baited with a blend of Manuka oil (50 mg/d) and (3Z)- hexenol (50 mg/d) to act as a lure. The Sabic purple prism trap had the highest detection rate (86%; detection rate defined as at least one catch on a trap over the course of the season), followed by the standard purple prism trap (73%), the Sabic green prism (66%) and lastly the green multifunnel trap (58%).

In addition to plant volatiles, some work has also been performed to identify possible emerald ash borer pheromones. In 2007, Bartelt et al. reported on the discovery of a macrocyclic lactone, (3Z)- dodecen-12-olide (also known as (3Z)-lactone), which was found to be approximately ten times more abundant in females. At the time of identification it was thought to be an aggregation pheromone rather than a typical sex pheromone because it was detected from both sexes, and because the highest amounts were detected in beetles two to four days after emergence when the beetles are still sexually immature (Bartelt et al., 2007). A synthetic (3Z)-lactone pheromone is now commercially available via Sylvar Technologies, Fredericton, NB, Canada (Ryall et al., 2013) and is capable of attracting male emerald ash borer (Silk et al., 2015). There is also some evidence to suggest that females may produce a cuticular hydrocarbon contact sex pheromone (Lelito et al., 2009) however, the components require further investigation (Silk and Ryall, 2015).

Crook et al. (2014) published the results of a study comparing multifunnel traps, prism traps and lure types at varying population densities as detection tools for emerald ash borer. They used two trap

Control and management strategies for emerald ash borer ∣ March 2017 Page 13 designs: Sabic purple prism traps (420 nm, 21.7% reflectance and 670 nm, 13.6 % reflectance; Great Lakes IPM, Vestaburg, MI) and green multifunnel (12 unit) traps (530 nm, 57% reflectance; Chemtica Internacional, San Jose, Costa Rica). Each of the two traps was baited with one of two lures; either Manuka oil (50 mg/d) and (3Z)-hexenol (50 mg/d) or (3Z)-hexenol (50 mg/d) and (3Z)-lactone (2 µg/d). The outer surfaces of the prism traps were coated with Tanglefoot glue (brushable formulation; Contech, Grand Rapids, MI) and green multifunnel traps were coated with fluon (Insect- A-Slip Insect barrier; Bioquip products, Rancho Dominguez, CA). Study sites were selected along or near the edges of the current emerald ash borer infestation across nine U.S. states. Traps were hung at a height of 5-8 m in the lower canopy. These authors found that there was a significant effect of trap type on catch, with the green multifunnel traps catching more beetles than the purple prism traps, however, the purple prism traps provided equal detection rates in areas of low beetle density compared with the green multifunnel traps. The type of lure had no significant effect on trap catch, with the two lure combinations providing similar rates of detection. Crook et al. (2014) therefore concluded that when large-scale surveys for emerald ash borer were required with traps hanging just below the canopy level in areas of low population density, green or purple fluon-coated traps would be equally effective irrespective of the lure combination used.

When combined with (3Z)-hexenol, (3Z)-lactone can significantly increase trap catches, particularly of male beetles (Silk et al., 2011; Ryall et al., 2012, 2013) but this may well be dependent on a number of factors including the dose of (3Z)-lactone, the type of trap used, the placement of traps (e.g. southern versus northern aspect; within versus below canopy) (Ryall, 2015; Ryall et al., 2015). Field experiments by Silk et al. (2011) concluded that combining the pheromone component with either green leaf volatiles or Phoebe oil did not affect the number of catches when sticky purple prism traps were used, however, when they deployed green prism traps in the canopy of ash trees a combination of the pheromone component and (3Z)-hexenol significantly increased the number of males caught in the traps. Indeed, after a study conducted in Canada, which included five different field trapping experiments, Ryall et al. (2015) were able to conclude that optimal set-up for emerald ash borer detection programmes was the deployment of dark green (540 nm wavelength, 49% reflectance; Synergy Semiochemicals Corp., Burnaby, BC) sticky prism traps baited with 3.0 mg (3Z)- lactone + (3Z)-hexenol hanging in the south aspect of the mid tree canopy.

Despite the number of studies investigating the efficacy of different trap types and lures for surveying emerald ash borer, very few have been performed at sites with very low population densities. However, optimal trap-lure combinations for very low population densities are essential for effective early detection of this species. Purple prism traps are reported to be more effective than their green counterparts at low beetle densities (Marshall et al., 2010; Francese et al., 2013a). In 2013 Ryall et al. report on field trials specifically designed to test the ability of green baited traps to reliably detect low levels of emerald ash borer infestation. These authors used sticky green prism traps (Synergy Semiochemicals, Burnaby, BC, Canada) suspended in the mid-crown of ash trees. During their first experiment, they baited the traps with the leaf volatile (3Z)-hexenol, to establish detection rates over a range of larval densities, and the relationship between mean trap capture with these traps and infestation density within the surrounding area. Results showed that these traps detected at least one adult in 55.3% of the plots categorised as ‘nil-low’ density and in 100% of plots within the moderate to high categories. Consistent results between trapping and branch sampling were observed in approximately 73% of the plots: 19.5% of the plots were deemed to be uninfested by both methods and 53.3% declared infested by both methods. The remaining 27% of

Control and management strategies for emerald ash borer ∣ March 2017 Page 14 the plots gave inconsistent results with traps failing to detect known infestations in 8% and branch sampling failing to detect infestations in 19% of plots where adults were successfully trapped (Ryall et al., 2013). In a second experiment performed by Ryall et al. (2013), the authors baited the traps with the (3Z)-lactone pheromone and/or (3Z)-hexenol in plots identified as nil-low population density as determined by branch sampling. Traps baited with both compounds had a detection rate of 88% compared with 60% for the traps baited with (3Z)-hexenol alone. Specifically, male catch was significantly increased with the addition of (3Z)-lactone to the bait, while the numbers of females caught by the two different lures was similar. These authors concluded by recommending the use of dark green sticky prism traps baited with both (3Z)-hexenol and (3Z)-lactone for early detection of emerald ash borer. They also suggest that further research is necessary, particularly with regard to identifying volatiles that are attractive to female beetles in order to maximise detection of virgin and/or mated females in new infestation areas (Ryall et al., 2013).

Some studies (McCullough et al., 2011b, Poland et al., 2011; Poland and McCullough, 2014) indicate that double-decker traps are more effective than canopy (prism) traps in areas of low emerald ash borer infestation. Field studies by Poland et al. (2011) at sites ranging from very low to heavy infestations concluded that 3 m tall double-decker traps with either purple or green prisms attached near the top, and baited with green leaf volatiles and Manuka oil, captured more adults than similar but taller (6m) tower traps, and both green and purple prism traps hung in the tree canopy. McCullough et al. (2011b) demonstrated that purple double decker traps, baited with a blend of ash leaf volatiles, Manuka oil and ethanol had a far higher detection rate compared with similarly baited green double decker traps or purple prism canopy traps baited with Manuka oil. More recently Poland and McCullough (2014) reported on field trials comparing different trap designs (canopy or double decker traps with two prisms attached to the pipe), colours (purple or green) and host volatile baits ((3Z)-hexenol combined with an 80:20 blend of Manuka and Phoebe oils or (3Z)- hexenol combined with Manuka oil). Infestation levels of emerald ash borer at their field sites ranged from low through to high. Their results confirmed that the effectiveness of the trap designs was influenced by the infestation level of the trapping area. Where heavy infestations were present, all trap design/colour/bait combinations attracted high numbers of beetles. However, at sites with low populations, the purple double decker traps were consistently more effective than the green canopy traps in terms of the number of adults caught, while overall, double-decker traps faired better than canopy traps and purple traps were more attractive than green traps (Poland et al., 2011; Poland and McCullough, 2014). This was also borne out with the detection rates: a 100% rate of detection was observed for both purple and green double decker traps compared with 82% for purple canopy traps and 64% for green canopy traps (Poland and McCullough, 2014).

Double decker traps are possibly more effective at low infestation levels because of their larger surface area, and because the free-standing design means they are very visible, can be positioned in full sun (taking advantage of the beetles preference for full sun), and provide a distinct point source of the lure without it being masked by volatiles emitted from host trees (McCullough et al., 2011b; Poland et al., 2011; Poland and McCullough, 2014; Herms and McCullough, 2014; Ryall, 2015). Whilst double decker traps are relatively simple to deploy, needing approximately the same time to set up as canopy traps, they are more costly because they require two panels as well as a PVC pipe and T- posts (Poland and McCullough, 2014; Ryall, 2015). However, these authors argue that the costs associated with “false negative trap data” can be substantial, as failing to detect the presence of emerald ash borer delays implementation of quarantine procedures and fails to protect the trees in

Control and management strategies for emerald ash borer ∣ March 2017 Page 15 the surrounding areas.The use of multifunnel traps has also been evaluated (Francese et al., 2011, 2013a, 2013b). Coating traps with a formulation that increases slipperiness also greatly enhances the numbers of beetles caught, as demonstrated by the use of Rain-X-coated traps (Francese et al., 2011), which caught significantly more beetles than untreated traps but did not catch any more than (Tangle-Trap) painted traps, and Fluon-coated traps (Francese et al., 2013b); Fluon appears to be the more effective coating.

Poland et al. (2011) and Ryall (2015) have discussed the advantages and disadvantages of the different types of traps and these can be seen summarised in Table 1. Poland et al. (2011) point out that canopy traps can sustain damage in storms and high winds and report that 20% of canopy traps were damaged in one incidence of bad weather compared with 3.8% of the double-decker traps. The placement of canopy traps can be difficult depending on the terrain and tree density. In addition, because they are placed within the tree canopy they may sometimes need to be cleaned and the stickiness (Pestick) re-applied as leaves and other debris from the trees can stick to the traps (Poland et al., 2011).

To summarise:

1. Numerous detection and survey methods for emerald ash borer have been developed. The pros and cons of these different detection/survey methods are described in Table 1. 2. The most effective detection method is the deployment of girdled trap trees. However, this is a destructive detection method (they must be felled). It is also labour intensive and suitable trees for girdling are not always available. 3. Extensive literature exits on trap designs, colours, placement, and lures used for detecting emerald ash borer, often with conflicting conclusions. 4. Based on current knowledge it is thought that the optimal trap for emerald ash borer detection programmes is the dark green sticky prism trap (540 nm wavelength, 49% reflectance; Synergy Semiochemicals Corp., Burnaby, BC) baited with 3.0 mg (3Z)-lactone + (3Z)-hexenol, hanging in the south aspect of the mid tree canopy (Ryall et al., 2015). 5. Purple prism traps baited with bark sequiterpenes may provide a suitable alternative (Ryall (2015). 6. There is evidence to suggest that at very low population densities, double decker traps (essentially two prism traps attached to a T-post at the top of a PVC pipe) may be more effective at trapping emerald ash borer. 7. Since the literature contains numerous conflicting comparisons of different trap designs, placements and lures, authors have concluded that survey protocols should perhaps include a mix of detection methods (Ryall, 2015). For instance, canopy traps may be more appropriate for systematic sampling across large areas whereas double-decker traps, used in conjunction with girdled detection trees and winter/early spring time visual surveys for trees with woodpecker damage, may be more appropriate for high risk sites (Poland et al., 2011; Poland and McCullough, 2014).

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Table 1. Summary of the various detection and surveying methods available for the management of emerald ash borer infestations. Taken from Poland et al. (2011) and Ryall (2015). 1. Whilst Cerceris fumipennis is widely distributed in the eastern States of North America, it is not known to be present in the U.K.

Survey method What does it involve? Advantages Disadvantages Visual Examining ash trees for signs Quick Not effective – fails to pick up low density infestations as and symptoms of emerald ash symptoms are generally not visible until three/four years borer infestation Easy – no extensive training needed after infestation

Relatively inexpensive Evidence of emerald ash borer larvae or adults is required to confirm that decline in tree health is due to emerald Can be performed all year round ash borer infestation as opposed to stress/disease (although canopy decline assessment should be done when the trees are in full leaf) Sub-sampling Trunk windows: Peeling If non-girdled trees are sampled they do Effectiveness of method not known - portions of bark (often at breast not need to be felled evidence suggests that in larger trees, infestation initially height) back to look for signs of occurs in the canopy rather than in the main trunk larvae and/or feeding galleries Quicker than using girdled trap trees Aesthetically damaging to the tree Easy – no extensive training needed

Sampling can be performed during autumn and winter when inspectors are less busy Branch sampling: Removing two Good detection rate – 75% if the density Method specifically developed for open growing, branches of at least 5-8 cm of larvae is > 8 galleries/m2 and detects asymptomatic urban trees of 24-34 cm dbh. Methodology basal diameter from the mid when trees are asymptomatic. Although likely to need refining for smaller trees (initial infestation canopy and then peeling back detection rates are lower when < 8 more likely to occur in the main stem) or larger trees bark from a 50 cm section from galleries/m2, the method is still more (sampling of more branches could be required to the basal area of each branch effective than visual surveying and maintain the detection efficiency) sampling by trunk windows. Can be time consuming and more expensive than some

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Trees do not need to be felled other methods

Removal of the branches can potentially Requires equipment such as pruners and saws, and also be incorporated into laboratory space for analysis pruning/maintenance programmes Requires removal of portions of tree from site Relatively easy to perform – some training required but not extensive

Can be performed year round although preferential to perform in the autumn or winter Girdled trap Trees are deliberately stressed The most effective method of sampling Trees must be felled in order to remove the larvae trees by removing a band of bark and with very good detection rates developing within them from the infestation area – must phloem in the spring to attract be performed in the autumn/winter before adults have adult beetles (known to Actually increases attack rate, especially chance to emerge preferentially attack stressed in low density infestation areas, therefore trees) may act as a population sink Tree felling leads to the reduction in ash trees over time

Can potentially be used in conjunction Large areas of bark may need to be peeled to confirm with insecticides e.g. attract the adult presence of emerald ash borer emerald ash borer into a sink area with girdled trees and then treat the Requires suitable trees to be available and easily surrounding trees with a systemic accessible insecticide Girdled trees become less attractive as the infestation rate in the surrounding area increases as they start to compete with other stressed trees

Use of girdled trees may result in attracting adults to the area, which then may oviposit on surrounding non-girdled trees.

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Labour intensive

Baited traps Sticky prism canopy traps: Non-destructive Require at least two site visits Baited with host volatiles, pheromones or a combination Easy to use, with minimal training Insect specimens must be cleaned of both Not re-useable

Possibly have a high false negative rate (although this is unknown)

Can sustain damage in bad weather

Trap placement can be difficult depending on the terrain and tree density

Sometimes need cleaning and stickiness re-applied as leaves and debris can stick to the traps

Can only be used during the short adult flight period

Lures are still being optimised Double decker traps: Two sticky Similar advantages to the sticky prism Similar disadvantages to the sticky prism traps (not all prism traps used at ground level traps with the addition that they may apply) and baited with host volatiles provide a higher detection rate In addition, more resources are required per trap e.g. T- post, PVC pipe

Require a ground location for deployment

Requires tall poles to set up the traps

Potentially prone to vandalism Reuseable multifunnel traps Non-destructive Difficult to set up

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Clean samples Need to be stored during the off-season

Re-useable The initial cost is more expensive than other trap types

Colour and lure combinations are still being optimised. Biosurveillance1 Nests of the buprestid-hunting Can be incorporated into citizen science There is only a short overlap between the flight periods of hymenopteran wasp Cerceris programmes the wasp and emerald ash borer fumipennis can be monitored for the presence emerald ash Can only be used where C. fumipennis nests are present borer taken as prey Time consuming Remote sensing Collecting images over a large Can cover large areas Does not detect low infestation levels when trees are scale from aeroplanes or asymptomatic so not appropriate for early detection satellites to map areas of ash Can identify areas of concern decline Does not confirm areas of decline are specifically due to emerald ash borer infestation

Expensive

Not readily available

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Chapter 3: Chemical control options

Due to adult female dispersal upon emergence, ash trees are considered at risk if they are 10-15 miles within a known infestation and insecticide treatment should be considered, beyond 10-15 miles and it is probably too early to start insecticide treatment (Herms et al., 2014). Two life stages are targeted for treatment: adult beetles and young larvae. A number of insecticide products, with different active ingredients, are currently registered for controlling emerald ash borer in the U.S.A. and Canada, and are documented in Table 2.

The active ingredients

Non-systemic pyrethroid insecticides, such as those containing the active ingredients bifenthrin and cyfluthrin, and carbaryl insecticides, have been shown to be toxic to adult emerald ash borer, and protect ash trees when used to spray the foliage and upper tree canopy (McCullough et al., 2004; Herms et al., 2014). However, they are not frequently used and are not a popular option because of spray drift, potential applicator exposure, environmental problems, effects on non-target organisms, difficulty in achieving good coverage of the upper canopy of large trees, and difficulties in reaching the location of trees with suitable spray equipment (Herms et al., 2014; McCullough, 2015).

Consequently, a number of systemic insecticides have been under investigation in North America for control of emerald ash borer. As the name suggests, systemic insecticides move systemically through the tree and can therefore be easily applied to trees either as a basal soil injection, basal soil drench or tree (trunk) injection. Drench treatments are less costly and quicker to administer however, tree injections, whilst more costly, are favoured over both broadcast foliar or bark sprays and soil treatments, especially in urban and environmentally sensitive areas where these methods of application can be publicly unacceptable or environmentally inappropriate (Cappaert et al., 2005). However, uptake and distribution of systemic compounds within a tree following injection is variable and dependent on the growing conditions, tree vigour and the extent of previous damage from emerald ash borer attack (Cappaert et al., 2005). In order for systemic compounds to be effective they have to be applied before infestations build up to such a level that they injure the tree’s vascular system thereby reducing the ability of the tree to translocate the insecticide throughout its trunk and canopy (Herms et al., 2014; McCullough 2015). Initially, most of the systemic insecticide products available contained imidacloprid as the active ingredient (McCullough, 2015), but the early field trials against emerald ash borer gave inconsistent levels of protection and are not reported here (Herms et al., 2014; Herms and McCullough, 2014; McCullough, 2015). Over time, a better understanding of systemic insecticide treatment, along with improved application technology, has resulted in new products, including some with alternative active ingredients (emamectin benzoate and azadirichtan) (Herms and McCullough, 2014; McCullough, 2015). Many different publications (e.g. Herms et al., 2014) suggest that treated trees should be maintained in good growing conditions to reduce stress and should be watered during dry weather conditions to help ensure the efficacy of systemic insecticides.

Neonicotinoids such as imidacloprid and dinotefuran act on the nicotinic acetylcholine receptors (nAChRs) in the insect nervous system (Schroeder and Flattum, 1984; Matsuda et al., 2001). Imidacloprid has been successfully used in the Asian longhorned beetle (Anaplophora glabripennis

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(Motchulsky) eradication programme in the U.S.A. (USDA-APHIS, 2016) and is also used to control the bronze birch borer (Agrilus anxius Gory) (Arborjet, 2014). Imidacloprid residues in the leaves of treated trees are thought to inhibit feeding in woodboring species such as the Asian longhorned beetle and the cottonwood borer (Plectodera scalator (F.) (Coleoptera: Cerambycidae), and cause intoxication or knockdown behaviour in adult beetles feeding on these leaves (Poland et al., 2006a). Larval weight gain data obtained during the Poland et al. (2016) laboratory efficacy study also suggests that imidacloprid has antifeedant effects towards emerald ash borer larvae. In contrast, dinotefuran residues in the leaves are toxic and can quickly kill the adults (Poland et al., 2016). However, imidacloprid, and indeed other neonicotinoids, have been implicated or perceived to have negative effects on beneficial soil dwelling arthropods and honey bees (Kreutzweiser et al., 2008a,b; McKenzie et al., 2010; Williams et al., 2015; Woodcock et al., 2016).

Emamectin benzoate is a macrocyclic lactone salt derivative avermectin compound and acts as a chlorine channel agonist (Lasota and Dybas, 1991). It is registered for pest control in fish farming in the U.K. (VMD, 2017), and for controlling insect and mite pests of trees in the U.S.A. (US-EPA, 2015). Early formulations applied as trunk injections have shown good efficacy against scolytinid and cerambycid beetles (Grossman and Upton 2006; Poland et al., 2006b; McCullough et al., 2011a), and a new formulation (Tree-Äge®; Arborjet, 2010) has since been developed and registered for control of emerald ash borer in ash trees in the United States. Emamectin benzoate is toxic to adult emerald ash borer (McCullough et al., 2011) and is also thought to be acutely toxic to the neonate larvae, killing them before they have excavated galleries (Poland et al., 2016).

Azadirachtin is a natural product describing a family of related tetranortriterpenoid compounds derived from seed kernel extracts of the neem tree, Azadirachta indica Juss. The active ingredients of the extract are thought to be Azadirachtin A and B (AZA-A and AZA-B), and because they are of plant origin their use is perceived as more acceptable in urban areas (McKenzie et al., 2010). Azadirachtin is known to have antifeedant effects, inhibiting larval feeding, and interferes with larval development by disrupting moulting hormones (Rembold et al., 1982; McCullough, 2015; Poland et al., 2016), which was corroborated for emerald ash borer by Poland et al. (2016). Azadirachtin also interferes with reproduction, reducing viable egg production of the mature female beetles, although it is likely that the younger females can recover to reproduce normally (McKenzie et al., 2010; Herms et al., 2014). It has insecticidal properties towards wood-boring pests (Naumann et al., 1994; Duthie- Holt et al., 1999; Naumann and Rankin 1999; Poland et al., 2006a; McKenzie et al., 2010) yet displays low toxicity towards birds and mammals, and low to moderate persistence in water, soil and foliage (reported in McKenzie et al., 2010). Azadirachtin has recently become available in the U.S.A and Canada for controlling emerald ash borer (McCullough, 2015).

Laboratory and field efficacy trials

The majority of efficacy studies have been conducted in the field following application of insecticide products to trees. However, one in vitro laboratory study has been performed to assess in detail the toxicity of insecticides, when incorporated into artificial diet, towards second and third instar emerald ash borer larvae. Poland et al. (2016) tested two neonicotinoid products, imidacloprid (Imicide; J. J Mauget Co., Arcadia, CA) and dinotefuran (Safari; Valent Professional Products, Walnut Creek, CA), an emamectin benzoate product (TREE-äge®; Arborjet, Inc., Woburn, MA), and two

Control and management strategies for emerald ash borer ∣ March 2017 Page 22 azadirachtin products, TreeAzin (BioForest Technologies, Inc., Sault Ste. Marie, Ontario) and Azasol (Arborjet, Inc., Woburn, MA). They tested these compounds over a range of doses encompassing the reported foliar residues levels, and reported that all were toxic to emerald ash borer larvae at concentrations representative of foliar residue levels.

Detailed analysis of the results indicated lethal concentrations, required to kill 50% of the larvae

(LC50), standardised by larval weight, of 0.015 ppm/g at day 63 for Imicide, 0.030 ppm/g at day 46 for Safari, 0.024 ppm/g at day 29 for TREE-äge®, 0.025 ppm/g at day 24 for TreeAzin and 0.027 ppm/g at day 27 for Azasol (Poland et al., 2016). Median lethal times to kill 50% of the treated larvae (LT50) were also estimated and ranged from 44-71 days for Imicide, 28-55 for Safari, 15-23 days for TREE- äge®, 10-52 days for TreeAzin and 10-64 days for Azasol, depending on the dose (Poland et al., 2016). Cumulative mortality was also measured: 100% and 83% mortality had occurred after 32 days of feeding on the 10 and 1 ppm doses of TREE-äge®. Larvae feeding on Imicide-containing diet showed 70-80% mortality by day 54 (0.1-10 ppm dose). After 45 days of feeding on Safari more than 80% of the larvae had died on all three doses tested (0.5 – 50 ppm). All larvae had died by day 18 on the three highest doses of TreeAzin tested (100, 10 and 1 ppm) with 83% mortality on the 0.1 ppm dose. After 27 days of feeding on the Azasol-containing diet, 95-100% of the larvae were dead on all doses (Poland et al., 2016). These results indicate that the emamectin benzoate and azadirachtin products are more toxic, and kill emerald ash borer larvae more quickly, than either of the neonicotinoid products (Poland et al., 2016).

A number of field tests have been performed to assess and compare efficacies of the different insecticide products available, and the relationship between efficacy, initial infestation level and tree size. Smitley et al. (2010a) conducted field trials at five sites in the U.S.A., applying the label rate of imidacloprid as a basal soil drench around the base of green and white ash, each spring, over the course of three years. The sites included small urban trees (5 -15 cm dbh), and medium to large trees (15-65 cm dbh), with variable conditions at the start of the trial (33 – 90% canopy thinning). Larval density and canopy thinning were used to evaluate efficacy as canopy thinning has previously been shown to be positively related to the level of infestation in terms of number of emergence holes (Smitley et al., 2008). This investigation determined that the efficacy of imidacloprid treatment was dependent on the tree size and the condition of the trees at the start of the investigation. The treatment afforded small, newly planted ash trees (5-6 cm dbh and 3-4 m tall) with a very high level of protection: following three years of treatment, all trees were healthy with < 20% canopy thinning whereas all the control trees were dead. Control trees exhibited 9.8 galleries/m2 (green ash) and 13.6 galleries/m2 (white ash) compared with 0.5 galleries/m2 and 0.0 galleries/m2, respectively, in the treated groups (Smitley et al., 2010a). Medium sized trees (23-37 cm dbh) were successfully protected (86% alive and healthy), with the trees gradually improving in condition over the three years, if they had less than 60% canopy thinning at the start of the trial (Smitley et al., 2010a). However, only 31% of trees that had more than 60% canopy thinning at the start of the trial were still alive. Larger trees (> 38 cm dbh) or medium sized trees with more than 60% canopy thinning at the start of the investigation continued to deteriorate during the treatment (Smitley et al., 2010a). These results led the authors to suggest that imidacloprid treatment rates could be increased for larger trees for better treatment (Smitley et al., 2010a).

In 2015, Smitley et al. published the results of their four to seven year study investigating the efficacy of basal soil drenches of three neonicotinoid insecticides to protect green ash. The study

Control and management strategies for emerald ash borer ∣ March 2017 Page 23 evaluated different timings of application as well as different application rates, and evaluated the results on the basis of canopy thinning. The products tested were Arena 50WDG (50% clothianidin); Bayer Advanced protect and feed II (liquid; 0.74% imidacloprid, 0.37% clothianidin), Bayer Advanced granules II (0.55% imidacloprid, 0.28% clothianidin), Merit 2F (25% imidacloprid), Xytect 75WSP (75% imidacloprid), Safari 20SG (20% dinotefuran) and Safari 2G (2% dinotefuran). At all study sites, trees ranged from 13 – 66 cm dbh and treatments were conducted at the first signs of canopy loss and branch dieback. The authors report good levels of protection (< 17% canopy loss with imidacloprid and clothianidn) with spring soil drenches of all products at application rates of ≥ 0.80g a.i./cm dbh per year proection was unreliable with an application rate < 0.80g a.i./cm dbh per year (Smitley et al., 2015). At one study site, the frequency of imidacloprid application was also investigated and demonstrated that trees treated every year or every other year benefitedfrom the treatment whereas those that were treated every third year declined in condition (Smitley et al., 2015). In addition, annual spring applications of imidacloprid gave effective and more consistent levels of protection against emerald ash borer than autumn applications to the extent that the authors do not recommend autumn application. They do however recommend that, provided treatment is initiated before the trees have been compromised, reliable control will be achieved with these products using the application methods that they describe.

McCullough et al. (2011a) evaluated the control provided by imidacloprid, dinotefuran and emamectin benzoate one and two seasons after treatment. Dinotefuran (Safari 20 SG; Valent USA Corp., Walnut Creek, CA) was administered by basal trunk spray; imidacloprid by basal trunk spray (Macho 2F; Albaugh Inc./Agri Star, Ankeny, IA) and trunk injection (Imicide (Hp 10%; JJ Mauget Co., Arcadia, CA) and emamectin benzoate (TREE-Äge 4% ME; Arborjet, Inc., Woburn, MA; Syngenta Crop Protection, Inc., Greensboro, NC) by trunk injection. Treatments were applied in the spring. Ash trees measured 11.5 – 48.1 cm dbh, and emerald ash borer was established in all experimental sites but tree canopies were relatively healthy and epicormics shoots were not present). The number of larval galleries found in the trees treated with emamectin benzoate was significantly lower (< 1%) than for untreated trees, both in the year of treatment and the following year, even if the treatment was not reapplied, demonstrating that trunk injections of emamectin benzoate can provide highly effective multi-year control of emerald ash borer( McCullough et al., 2011a). The neonicotinoid products were capable of reducing emerald ash borer larval density in the year of treatment but only continued to have this effect if the product was reapplied the following year, in other words annual treatment with the neonicotinoids appeared to be necessary to achieve control. However, the results observed during the two years were variable for the neonicotinoids; whilst imidacloprid was quite effective during the first year lower efficacy was observed the following year even after reapplication of treatment (McCullough et al., 2011a).

Excised leaf bioassays demonstrated that nearly 100% of adult beetles died within four days, typically after eating just one or two mouthfuls of leaves collected from trees injected with TREE- äge, even when leaves were collected and tested in the second year after treatment (McCullough et al., 2011a). The delay in the onset of oviposition (due to the maturation period required following adult emergence, and the speed at which emamectin benzoate kills adult emerald ash borer, provides an important window of opportunity to control the beetle before egg laying occurs (McCullough et al., 2011a; Herms et al., 2014). This result indicates that if an immature adult female were to feed on treated trees there is a very high chance that she will die before laying eggs (McCullough et al., 2011a).

Control and management strategies for emerald ash borer ∣ March 2017 Page 24

Excised leaf bioassays were also conducted by Mota-Sanchez et al. (2009) following tree injection with Imicide. When excised leaves were harvested 45 days after injection, the results indicated that the leaves were toxic to adult beetles feeding upon them with 70-81% of the beetles either dead or intoxicated after three days of feeding. However, a much lower mortality was observed (24%) when leaves collected a year after treatment were used for the bioassays, again indicating that imidacloprid will not provide more than one year of control (Mota-Sanchez et al., 2009).

Smitley et al. (2010b) also report upon the efficacy of emamectin benzoate trunk injections for controlling emerald ash borer. At one study site they gave some trees an annual treatment of an imidacloprid basal drench or a combination of an imidacloprid trunk injection and basal drench, for additional comparison. Tree size ranged from 35.6 – 43 cm dbh, and at the start of the study, all trees were healthy. For two to four years following treatment canopy thinning and dieback was used to measure tree health, and numbers of emerald ash borer larvae were determined. Results were very positive. When a single injection of emamectin benzoate was given in the spring, nearly 100% control of emerald ash borer larvae was achieved, even when the trees were under intense infestation pressure, and very little change in the tree canopy rating was observed in the following years; results were consistent (Smitley et al., 2010b). This level of control lasted for three years when a rate of 0.4 g a.i./2.54 cm dbh was applied to trees with a dbh of 41 cm, and for two years when a lower rate (0.1 or 0.2 g a.i./2.54 cm dbh) was applied to trees with a dbh of 38 cm (Smitley et al., 2010b). In comparison, the non-treated trees showed dramatic decline in their canopy ratings (from 15-19% canopy thinning to 54 - 87% over the duration of the follow up period). The imidacloprid applications resulted in healthy looking trees, as determined by canopy thinning ratings, but more larvae were found in the imidacloprid-treated trees (5.7 ± 5.6 per m2) compared with those treated with the emamectin benzoate (0.0 ± 0 per m2) (numbers of larvae found in the control trees were 23.6 ± 39.4 and 27.7 ± 28.9 per m2. Due to the large degree of variability in the control and imidacloprid-treated groups a significant difference in the numbers of larvae was only observed between the emamectin benzoate-treated and control group (Smitley et al., 2010b).

Flower et al. (2015) also report on a four year study investigating the effectiveness of biennial trunk injections of emamectin benzoate (TREE-ägeTM; 0.2 g a.i./2.5 cm dbh). The trees used in the study were between 7 - 27.6 cm dbh. These authors report that during the study, all untreated trees died. Treated trees that were initially healthy or showed only moderate symptoms maintained or improved their canopy condition. In contrast, 63% of trees that were already heavily impacted by infestation at the point of treatment declined or died whilst the remaining 37% of the heavily impacted treated trees were able to recover or stabilise (Flower et al., 2015). The results support the recommendation that trees should be treated before symptoms are evident for maximum effectiveness (Flower et al., 2015).

One thing to consider with current recommended usage patterns of emamectin benzoate for controlling emerald ash borer trees is that with long term application comes the possibility of the evolution of resistance to the active ingredient (Cappaert et al., 2005; Flower et al., 2015); reduced sensitivity to emamectin benzoate has already been observed in salmon lice (Espedal et al., 2013).

The efficacy of azadirachtin for the control of larval and adult emerald ash borer has also been field tested. McKenzie et al. (2010) trunk- injected TreeAzin to deliver known doses of azadirachtin A+B (ranging from 0 – 54.5 mg a.i./cm dbh) into uninfested green ash nursery trees (mean dbh of 2.2

Control and management strategies for emerald ash borer ∣ March 2017 Page 25 cm). The authors found no evidence that azadirachtin killed adult emerald ash borer when they were fed for three days on leaflets excised from trees injected with the highest dose; neither did they find any differences in the amounts of leaves consumed between control and treated groups. However, they do report significant inhibition of larval development, measured by the numbers of complete galleries. Doses ≥ 1.7 mg a.i./cm dbh resulted in fewer larvae completing their development. Development ceased (no complete galleries), and no larvae beyond the second instar were found, when the dose administered was ≥ 13.6 mg a.i./cm dbh (McKenzie et al., 2010). In an additional experiment, green ash trees (mean dbh 5 cm) were injected with an azadirachtin formulation on one of four injection dates to determine the effects of the timing of injection on larval development and adult emergence one year on from treatment. Injection timings were timed to coincide with the start of adult emergence (May), peak oviposition (June), July and August. The authors report significantly fewer exit holes were found the year following treatment on trees injected during May, June and July but not in August, and suggested that this may be because larger, more mature larvae could be less sensitive to azadirachtin (McKenzie et al., 2010). Once again a dose effect was observed; the lowest dose (20 mg a.i./cm dbh) did not reduce adult emergence. These authors concluded that treating trees at an early stage of infestation, with a dose of at least 40 a.i./cm dbh, during May – July should be sufficient to sustain the life of a tree for at least one year, but conceded that further work was needed to establish whether higher doses are needed for larger trees. Similar conclusions indicating that imidacloprid trunk injections were 70% more effective against emerald ash borer when applied in mid-May compared with mid-July have been reported within Herms et al. (2014).

Overall, studies demonstrate that it is best to start insecticide treatment while trees are still relatively healthy and therefore able to transport systemic insecticides through the trunk and into the branches and canopy. Once dieback and canopy thinning are noticeable, there is already extensive damage to the vascular system of the tree, limiting its ability to transport the insecticides (Herms et al., 2014). Under these conditions, treating with insecticide may stop additional emerald ash borer damage but will not reverse the damage already sustained; these trees need time to repair their vascular system and recover, hence will often show further deterioration before improvements are seen (Herms et al., 2014). Trees with less than half the expected amount of foliage or with more than 50% of the canopy dead are probably too extensively damaged to be able to save and therefore probably should not be treated (Herms et al., 2014). It is also imperative that the application of systemic insecticides is carefully timed so that it is present throughout the tree for adults and young larvae to encounter the toxin (Herms et al., 2014). Young larvae are generally more susceptible to insecticide treatments than older larvae so treatments applied earlier in the growing season are more effective than treatments applied later when the larvae are more mature; in addition larger larvae cause greater damage to the tree with their more extensive galleries (Herms et al., 2014).

Lethal trap trees

Lethal trap trees are not a new concept, and have been used or investigated for a number of insect pests, including bark beetles (Lister et al., 1976; Manville et al., 1988; McCullough et al., 2016). Lethal trap ash trees can be created by injecting a tree with emamectin benzoate and then girdling the tree a few weeks later, once the insecticide has had chance to translocate throughout the tree,

Control and management strategies for emerald ash borer ∣ March 2017 Page 26 meaning that the tree effectively lures emerald ash borer to their death. Using lethal trap trees has the potential to attract and kill the adult emerald ash borer when it feeds on the tree, reduce egg laying on the trap tree and potentially those around it too, and would prevent any larvae from developing on the trap tree (McCullough et al., 2016). In addition, the girdled tree would not need to be removed in the autumn/winter to destroy the larvae developing within it as the insecticide will kill any larvae developing within it, thus extending the life of the trap tree (although it will eventually die as a result of the girdling process) (McCullough et al., 2015). However, in order for lethal trap trees to be effective, the girdling process must not interfere with translocation of the insecticide, and this has been investigated by McCullough et al. (2016). Field trials were performed to compare emerald ash borer larval densities and adult beetle captures on girdled trees, emamectin benzoate- treated trees, trees treated with emamectin benzoate and girdled 18-21 days later, and untreated control trees. The trees, which were a mixture of green and white ash, ranged in size from 12.2 – 21.6 cm dbh, and had relatively healthy looking canopies. As expected more larval galleries were found on the girdled and untreated control trees than on the emamectin benzoate-treated trees and those treated with emamectin benzoate and then girdled. Sticky bands were placed around the treated trees in order to capture the adult beetles. Whilst relatively few were caught (only 88 in total), differences were observed between the different treatment groups. Thirty eight adults were captured on the girdled trees, 22 on the trees treated with emamectin benzoate and then girdled, 10 on the trees treated with emamectin benzoate and 18 on the untreated trees, indicating that adults were attracted to the girdled trees. It was thought that fewer adults were captured on the trees treated with emamectin benzoate and then girdled, compared with those that were only girdled because the adults that had fed on leaves containing the insecticide would have quickly died.

Analysis of leaf residues from leaves collected after emamectin benzoate treatment and girdling confirmed that the girdling did not interfere with the translocation of the insecticide (McCullough et al., 2016). This was further corroborated when the leaves from both the emamectin benzoate- treated trees and those treated with insecticide and then girdled, were shown to be highly toxic to the adults when used in excised leaf bioassays (McCullough et al., 2016). These authors hypothesised that lethal trap trees were most likely to be effective when used in relatively recent infestations.

Summary

1. Trees may be at risk if within 10-15 miles of an outbreak area.

2. Trees exhibiting more than 50% canopy decline are unlikely to recover even if treated with a highly effective insecticide (Herms et al., 2014).

3. Effectiveness varies according to injection methods and products (Cappaert et al., 2005). It is therefore imperative that products, application methods and rates are all individually tailored to the trees requiring treatment in order for effective treatment to be achieved. Factors such as tree size, health, ash borer density and location all need to be considered (Herms et al., 2014).

4. Emamectin benzoate and azadirachtin products are more effective at controlling emerald ash borer than neonicotinoid products. Emamectin benzoate performs consistently better than other

Control and management strategies for emerald ash borer ∣ March 2017 Page 27 products, providing at least two years of control with a single application, even in large trees under intense pest pressure (Smitley et al. 2010b; McCullough et al., 2011; McCullough and Mercader, 2012; Herms et al., 2014).

5. The speed at which emamectin benzoate kills adult emerald ash borer has implications for control. If treatment is applied before maturation of the females then it should significantly reduce the number of eggs laid providing a sufficient number of trees are treated (McCullough et al., 2011a).

6. Azadirachtin kills emerald ash borer larvae but not the adults (McKenzie et al., 2010). However, depending on the level of infestation, azadirachtin trunk injections should provide effective protection for one or two years (Herms et al., 2014).

7. Neonicotinoid products also have some toxicity towards adults and treatment can protect ash trees from declining (McCullough et al., 2011a; Herms and McCullough, 2014). However, efficacy varies according to the product formulation, application rate, method, timing, tree size and vigour, and ash borer density (McCullough et al., 2004; Smitley et al., 2010a,b; McCullough et al., 2011; Herms et al., 2014; Smitley et al.,2015). Field trials have sometimes given inconsistent results and treatments must be applied annually.

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Table 2. Summary of the insecticides currently registered for use against emerald ash borer in the United States and Canada with application methods and timings. Table and information taken directly from Herms et al. (2014), Flowers et al. (2015), PMRA (2017).

Active Product Application method Recommended timing ingredient Imidacloprid Merit® (75WP, 75 WSP, 2F) Soil injection/drench (4-6 week uptake and Early to mid-spring or mid-autumn (neonicotinoid) distribution) XytectTM (2F, 75WSP) Soil injection/drench (4-6 week uptake and Early to mid-spring or mid-autumn distribution) Imicide® Trunk injection Mid to late spring after trees have leafed out but before eggs have hatched IMA-jet®1 Trunk injection Spring to early summer IMA-jet 102 Trunk injection At least 30 days before egg hatch or adult flight Macho 2F Trunk spray Spring to early summer Bayer AdvancedTM Tree and Soil drench (4-6 week uptake and distribution) Early to mid-spring Shrub Insect Control OptrolTM Soil drench (4-6 week uptake and distribution) Early to mid-spring Confidor®2 Tree injection April - September Dinotefuran SafariTM (20 SG) Soil injection/drench (1-4 week uptake and Mid- to late spring (neonicotinoid) distribution) Systemic bark spray (quicker uptake and Mid- to late spring after trees have leafed distribution than soil treatment) out TransectTM Soil injection/drench (1-4 week uptake and Mid- to late spring distribution) Systemic bark spray (quicker uptake and Mid- to late spring after trees have leafed distribution than soil treatment) out Zylam® Liquid Systemic Soil injection/drench (1-4 week uptake and Mid- to late spring Insecticide distribution) Systemic bark spray (quicker uptake and Mid- to late spring after trees have leafed distribution than soil treatment) out

Control and management strategies for emerald ash borer ∣ March 2017 Page 29

Ortho Tree and Shrub Insect Granules Mid- to late spring Control Ready to Use Granules® Azadirachtin AzasolTM Trunk injection Mid- to late spring after trees have leafed out but before eggs have hatched TreeAzin®1 Trunk injection Mid- to late spring after trees have leafed out but before eggs have hatched Emamectin TREE-ägeTM Trunk injection Mid- to late spring after trees have leafed benzoate out but before eggs have hatched Carbaryl Sevin®SL Preventative trunk, branch and foliar cover sprays Two applications at four week intervals, Permethrin Astro® the first at 450-550 degree days (based on Bifenthrin OnyxTM 10°C threshold, 1st January start date) Cyfluthrin Tempo® Cyfluthrin Pointer Trunk injection Spring to Summer Acephate Orthene Trunk spray Spring to early summer Acecap 97 systemic insecticide Trunk implant Early April – early June (just prior to or at implants2 earliest indication of insect activity) Bidrin® Inject-A-Cide B® Trunk injection Spring to early summer

1. Registered in both the U.S.A. and Canada. 2. Registered in Canada only.

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Chapter 4: Biological control (parasitoids)

The use of natural enemies to suppress established populations of invasive pests can provide environmentally friendly biological control options in ecologically sensitive areas (Castrillo et al., 2010a). Biological control can either be classical or augmentative. Classical biological control, whereby exotic natural enemies are released to control exotic pests, has been used for more than 120 years resulting in the successful control of at least 165 insect pest species and utilising more than 2000 species of natural enemies (van Lenteren et al., 2006). Augmentative biological control involves the enhancement of indigenous natural enemies through direct manipulation of their populations by mass production and periodic colonisation (DeBach and Rosen, 1991). Extensive research has been conducted by scientists to identify candidate species of parasitoid wasps that would be suitable to use in biological control programmes for controlling emerald ash borer. This research includes surveys for parasitoid wasps that attack emerald ash borer both in its native and invaded ranges, elucidation of the biology of candidate species, host specificity testing, climatic matching, the development of mass rearing and release methods, and methods to survey their establishment in the environment once released. There is a wealth of literature on these topics, which are reviewed in the following sections. These topics have also been reviewed by the researchers responsible for the investigations and their reviews can be found in the USDA Forest Service technology transfer document FHTET-2014-09 (2015).

Classical biological control

Classical biological control, if successful, can be a very cost-effective, sustainable and environmentally friendly method of managing agricultural and forest pests (Duan et al., 2013a). With classical biological control in mind, USDA Forest Service and APHIS entomologists from the U.S.A. have worked in collaboration with the Chinese to search for natural enemies of emerald ash borer in China (Liu et al., 2003; Cappaert et al., 2005; Bauer et al., 2005, 2006; Yang et al., 2014; Bauer et al., 2015a).

In the autumn of 2003, an exploratory survey was conducted across six provinces in China for natural enemies of emerald ash borer (Liu et al., 2003); two species of parasitoids were found. The first was an undescribed gregarious ectoparasitic braconid species (Spathius sp.), found parasitizing 1-50% of emerald ash borer larvae in three trees, with on average 6.6 parasitoid larvae per emerald ash borer larvae (Liu et al., 2003), and has subsequently been described as Spathius agrili Yang sp. nov. (Hymenoptera: Braconidae) (Yang et al., 2005). The second, a gregarious endoparasitic eulophid species (Tetrastichus nov. sp.) was found parasitizing 3-50% of emerald ash borer larvae in three trees with an average of 9.4 parasitoid larvae per host (Liu et al. 2003), and has subsequently been described as Tetrastichus planipennisi Yang sp. nov. (Hymenoptera: Eulophidae) by Yang (reported in Gould et al., 2015). These two species were found again in 2006 during a subsequent survey (Fuester et al., 2007). Other subsequent surveys have found additional hymenopteran species parasitizing emerald ash borer and include the solitary egg parasitoid Oobius agrili Zhang et Huang sp. nov. (Hymenoptera: Encyrtidae) (Zhang et al., 2005), a gregarious ectoparasitoid of mature larvae/ pupae Sclerodermus pupariae Yang et Yao sp. nov. (Hymenoptera: Bethylidae), a solitary parasitoid of mature larvae Deuteroxorides orientalis Uchida (Hymenoptera: Ichneumonidae), and a Platygasteridae (Hymenoptera) species an egg parasitoid (reported in Yang et al., 2014).

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In addition surveys have been performed in two regions of the Russian Far East (Khabarovsk and Vladivostok) where emerald ash borer is a native species (Duan et al., 2012a). Surveys were conducted in both the spring and autumn in order to sample all immature life stages of emerald ash borer. Very little hymenopteran parasitism (< 1%) was observed in the Khabarovsk region however, 7-63% larval parasitism on green ash was observed in the Vladivostok region. Parasitism was predominantly due to a Spathius sp. (parasitism rate 76%), subsequently described as Spathius galinae Belokobylskij and Strazenac, Atanycolus nigriventris Vojnovskaja-Krieger (parasitism rate 23%) and T. planipennisi (parasitism rate 24%); in all cases third and fourth instar emerald ash borer larvae were attacked (Duan et al., 2012a; Gould et al., 2015). Parasitism was much lower (0-8%) on the native ash species. More recently, a new species of solitary egg parasitoid has been identified from the Vladivostok region of the Russian Far East and described as Oobius primorskyensis Yao & Duan (Yao et al., 2016).

Surveys for natural enemies of emerald ash borer have also been undertaken in South Korea, where two species of parasitoids were found, namely S. galinae and a larval endoparasitoid thought to be Tetrastichus telon (Graham) (Bauer et al., 2015a; Gould et al., 2015). However, surveys conducted in Japan and Mongolia did not yield any natural enemies, indeed, with the exception of one adult beetle, no emerald ash borer were found (Schaefer, 2003; Gould et al., 2015).

Tetrastichus planipennisi

Tetrastichus planipennisi is a gregarious endoparasitoid showing a clear preference for fourth instar emerald ash borer larvae in the wild (Liu et al., 2007; Ulyshen et al., 2010b). In rearing programmes, using artificially infested ash logs, the parasitoid is capable of parasitizing second to fourth instar larvae, preprepupae (J larvae) and prepupae but significantly more progeny are yielded from fourth instar larvae (Ulyshen et al., 2010a). It is koinobiont in nature (Ulyshen et al., 2010a), that is to say that the female parasitoid only temporarily paralyses the host larvae during oviposition, larvae then recover and do not die until the parasitoid larvae reach maturity. This parasitoid is found mainly in northeast China (Yang et al., 2014) and is thought to play an important role in suppressing emerald ash borer populations (Liu et al., 2007). In its native China T. planipennisi produces at least two generations per year (Yang et al., 2014) but is capable of producing four or more generations per year (Liu and Bauer, 2007) and levels of parasitism average approximately 22% (Liu et al., 2007) ranging from 0-65% (reported within Ulyshen et al., 2010a). It has good life cycle synchronicity with its host life cycle (Liu et al., 2007). Yang et al. (2014) report a 2.5 female : 1 male sex ratio whilst Liu and Bauer (2007) report a ratio of 3.5 : 1. Tetrastichus planipennisi has a high reproductive potential; brood sizes of 4 -172 have been reported (Ulyshen et al., 2010a), whilst Liu et al. (2007) report 5 - 122 larvae per host (average 35) and Yang et al. (2014) report 56 - 92 offspring per host. The high reproductive rate may enable this parasitoid to respond quickly to outbreaks of emerald ash borer (Liu et al., 2007).

Studies indicate that T. planipennisi has a narrow host range. Larvae of eight buprestid species (Agrilus anxius, Agrilus ruficollis, Agrilus bilineatus, Agrilus subcintus, Agrilus sp., Chrysobothris femorata, Chrysobothris floricola and Chrysobothris sexsignata), five cerambycid species (Neoclytus acuminatus, Megacyllene robiniae, Astylopsis sexguttata, Monochamus scutellus and an unknown species), two lepidopteran species (Galleria mellonella and Manduca sexta) and a tenebrionid

Control and management strategies for emerald ash borer ∣ March 2017 Page 32 species (Tenebrio molitor) were all rejected as hosts in no-choice experiments (Liu and Bauer, 2007). Tetrastichus planipennisi, known to be present in China between 41°N in the south and 44°N in the north is therefore climatically suited to northern States in the U.S.A such as Michigan (Liu et al., 2007).

All these characteristics mean that T. planipennisi has good potential to become an effective biological control agent of emerald ash borer (Duan et al., 2011a) and was approved for use in the U.S.A. in 2007 and Canada in 2013 (Gould et al., 2015). This parasitoid has a small ovipositor (2 – 2.5 mm in length) and as such may be better at parasitizing larvae in small ash trees (< 12 cm dbh) with thinner bark (Bauer et al., 2015b).

Spathius agrili

Spathius agrili is a gregarious ectoparasitoid (Yang et al., 2005) with a preference for late instar emerald ash borer larvae (Yang et al., 2010). During oviposition the female parasitoid envenomates the host larva resulting in permanent paralysis of the host (i.e. it is idiobiont in nature) (Yang et al., 2005). In the field up to 35 eggs per cluster on a host have been observed (Yang et al., 2005), and females can oviposit on multiple occasions (Yang et al., 2010). Generally, up to 18 offspring per cluster successfully develop to adulthood (average 8.4) and a 3:1 female to male sex ratio is observed (Yang et al., 2005). In comparison, rearing studies by Gould et al. (2011) indicated that female S. agrili were capable of producing an average of 51 eggs distributed between on average 9.5 clutches, with an average of 5.4 eggs per cluster; they also observed a 3 female : 1 male sex ratio. Spathius agrili has an ovipositor 3-4 mm in length (some suggest smaller (Watt et al., 2015)) but is apparently capable of parasitizing larvae through thick bark as found at 30cm dbh (Gould et al., 2011). In its native China this parasitoid is thought to complete up to four generations a year, and parasitism rates range from 10-90% (Yang et al., 2005, 2010). Its life cycle is well synchronised with emerald ash borer, with a large increase in parasitoid emergence timed for when the later instars of emerald ash borer larvae become available (Yang et al., 2010). It is reported to be quite scarce in northeast China (Gould et al., 2015) but to be the dominant parasitoid in northern China where it is thought to be an important factor in keeping emerald ash borer under control (Yang et al., 2008, 2014).

In China, emerald ash borer is the preferred host of S. agrili; no specimens have been observed to emerge from field-collected larvae of other species, including six other Agrilus species (Yang et al., 2008). No choice experiments have demonstrated that S. agrili is capable of attacking some other Agrilus species albeit with significantly lower rates of attack (Gould et al., 2015). However, these authors hypothesise that in the field S. agrili would be unlikely to attack these other species because they are not attracted to the host plants that these species are found on, and therefore would not naturally encounter them (Gould et al., 2015). Spathius agrili did however demonstrate attractancy to a species of willow (Salix babylonica L.), and in the U.S.A three Agrilus species use this species of willow as a host plant; it was suggested that as the larvae of these species are smaller than emerald ash borer larvae they would make less suitable hosts for the parasitoid and therefore should not be a cause for concern (Gould et al., 2015).

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Spathius agrili was approved for the biological control of emerald ash borer in the U.S.A. in 2007 (Bauer et al., 2015b).

Spathius galinae

Spathius galinae is a gregarious idiobiont ectoparasitoid with a preference for later instars of emerald ash borer larave (Bauer et al., 2015b) and is thought to be an important factor in controlling emerald ash borer in its native area (Duan et al., 2012a). Under laboratory rearing conditions, it can complete a generation in one month. One female parasitoid produces an average of 31 progeny if she is reared in groups or an average of 47 progeny if reared as a single pair (Duan et al., 2014). Spathius galinae has a longer ovipositor than both S. agrili and T. planipennisi (Duan et al., 2013a; Watt et al., 2015), and could therefore be used alongside S. agrili and T. planipennisi to parasitize emerald ash borer in larger trees with thicker bark (Abell et al., 2012; Yang et al., 2012). However, S. galinae also prefers larger instar larvae and therefore interspecific competition may occur between the parasitoid species. This species occurs several hundred kilometres further north than the S. agrili collected from China, making it a better climatic match to the north east American climate (Watt et al., 2015; Bauer et al., 2015b).

The host specificity of S. galinae has proved to be better than that of S. agrili (Gould et al., 2015). Fifteen alternative North American hosts have been tested comprising of 13 species of wood-boring beetles (five Agrilus species), a clearwing moth and a sawfly (Gould et al., 2015). Only one, the invasive gold spotted oak borer (Agrilus auroguttatus Schaeffer), was attacked by S. galinae and parasitism rates were lower (41%) compared with rates for emerald ash borer (71%) (Gould et al., 2015).

These attributes make S. galinae a good candidate biological control agent for emerald ash borer and as such a permit has recently been approved (2015) for its release in the U.S.A.

Oobius agrili

Oobius agrili Zhang and Huang (Hymenoptera: Encyrtidae) was discovered in the Jilin Province of China (43°N latitude) in 2004 and is found mainly in northeast China (Yang et al., 2014). It is a solitary parasitoid that attacks emerald ash borer eggs and is not known to have any other hosts in China (Liu et al., 2007). Oobius agrili is also thought to play an important role in suppressing emerald ash borer populations; together with T. planipennisi these parasitoids were thought to be responsible for 73.6% of emerald ash borer mortality in one surveyed site in Jilin Province in 2005; Bauer and Liu, 2007; Liu et al., 2007). This parasitoid is capable of at least two generations a year in its native range, with parasitism rates ranging from 0 to 61.5% (average 36.5%) (Bauer and Liu, 2007; Liu et al., 2007), and is reported to have a high female : male sex ratio (14.5:1; Bauer and Liu, 2007). Bauer and Liu (2007) report that under laboratory conditions, O. agrili females are capable of producing a maximum of 62 eggs in their lifetime, averaging 24 eggs, however Bauer et al. (2015b) report a higher average fecundity of 80 progeny per female wasp. A proportion of O. agrili populations enter an obligate diapause within host eggs to provide synchrony with the emerald ash borer life cycle (Bauer and Liu, 2007; Liu et al., 2007).

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No choice assays have been conducted to identify the potential host range of this parasitoid. Eggs of eight wood-boring insects (six Agrilus species and two cerambycid species (N. acuminatus and M. robiniae)) and four lepidopteran species (Choristoneura rosaceana, M. sexta, Bombyx mori and Pieris rapae) were offered (Bauer and Liu, 2007; Gould et al., 2015). These assays revealed that whilst O. agrili did not attack the eggs of the cerambycid and lepidopteran species, it did attack eggs of the bronze birch borer (A. anxius), two-lined chestnut borer (A. bilineatus) and red-necked cane borer (A. ruficollis), but not those of Agrilus cyanescens, Agrilus subcinctus and Agrilus egenus, leading researchers to conclude that this parasitoid could potentially attack, and develop, in Agrilus species with similar sized eggs to emerald ash borer (Bauer and Liu, (2007); Gould et al., 2015). Subsequent choice assays indicated that the parasitoid had a preference for emerald ash borer eggs over those of A. anxius, A. bilineatus and A. ruficollis (Bauer and Liu, 2007; Gould et al., 2015).

Oobius agrili was approved for use as a biological control agent for emerald ash borer in the U.S.A. in 2007 (Bauer et al., 2015b).

Oobius primorskyensis

Oobius primorskyensis Yao & Duan is a solitary egg parasitoid, and believed to reproduce entirely by thelytokous parthenogenesis (i.e. females are produced from unfertilised eggs), with no male specimens known (Yao et al., 2016). Whilst this species may not always be morphologically distinct from O. agrili, differences in diapause patterns and genetic differentiation suggest that they are two separate species (Yao et al., 2016). In addition, O. primorskyensis and O. agrili appear to inhabit distinct geographical ranges, which to date have not been found to overlap, with O. primoskyensis occurring further north than O. agrili (Yao et al., 2016).

Sclerodermus pupariae

Sclerodermus pupariae Yang et Yao is a gregarious idiobiont ectoparasitoid that attacks late stage emerald ash borer larvae (third and fourth instar larvae, pre-pupae and pupae (Yang et al., 2014). Females demonstrate considerable maternal care for their progeny to ensure successful development. Females will lay 26-58 eggs per host and a very highly biased female: male sex ratio (22:1) is reported with each brood typically only producing one or two males (Yang et al., 2014). Due to high host-searching and attacking capabilities, and the high female: male sex ratio, this parasitoid was considered by some to have good potential as a possible biological control agent (Yang et al., 2014). However, the parasitoid exhibits other characteristics, which North American researchers considered to be inappropriate for a biological control agent and therefore did not import specimens for further investigation (Gould et al., 2015). These less desirable characteristics are reported by Gould et al. (2015) to include a low ability to disperse because the females often lack wings, a broad host range, low parasitism levels in China, and finally that some Sclerodermus species are known to sting humans.

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Rearing of parasitoid species for release

An important component in a classical biological control programme is the ability to reliably rear large numbers of the control agent, for specific times of the year to correspond with release protocols, in as an efficient way as possible to maximise the numbers of good quality offspring (particularly females) (Duan and Oppel, 2012; Watt et al., 2015). Host plant, host-parasitoid group sizes (densities) and parasitoid : host ratios can all influence fitness parameters in breeding programmes (Duan and Oppel, 2012). In addition, a large and regular supply of emerald ash borer also need to be available (in other words, emerald ash borer also needs to be mass reared in the laboratory). Laboratory reared, rather than field collected, emerald ash borer are recommended to minimise disease and maximise emerald ash borer adult fecundity, and full details on how to do this are provided by Lelito et al. (2015). Duan et al. (2012b) present evidence that emerald ash borer larvae can complete their development in tropical ash, Fraxinus uhdei [Wenz.] Lingelsh, with Duan and Oppel (2012) suggesting that this has significant implications for an emerald ash borer breeding programme because tropical ash is more easily propagated, can be grown in a greenhouse, does not require a senescence period and grows faster than temperate Fraxinus species. However, Lelito et al. (2015) recommend that adult beetles are fed on field collected green ash foliage to maintain high fecundity, but during the winter foliage from tropical ash can be used instead. Rearing methods for emerald ash borer, along with those for T. planipennisi, S. agrili, S. galinae and O. agrili have also been extensively researched and documented (USDA-APHIS/ARS/FS, 2016) and are described in detail by Lelito et al. (2015).

Key points of the current rearing methods for O. agrili as described by Lelito et al. (2015), and based on the method originally described by Liu and Bauer (2007) with some modifications, are outlined as follows.

• Rearing conditions of 25 ± 1°C, 75-80% relative humidity are used. • A two generation system has been developed with long day (16h : 8h light : dark) and short day (8h: 16 h ligh : dark) conditions because a proportion of progeny will diapause. • Honey is provided to adults. • Females are provided with emerald ash borer eggs, laid on filter papers, from the day that they emerge. Batches of eggs are kept in the rearing chamber for one week. Females are kept in groups of up to twenty while exposed to the eggs (3-5 eggs per female wasp). • Groups of O. agrili females can be used for a further one week exposure. • O. agrili completes a generation in 20-25 days.

Current rearing methods for S. agrili are described (USDA-APHIS/ARS/FS, 2016) in detail by Lelito et al. (2015), and some key points are outlined as follows.

• Reared at 25-27°C, 75-80% relative humidity, 16h : 8h light : dark lighting regime. • Small diameter ash logs are used to rear emerald ash borer larvae to the right stage; ash logs are infested with emerald ash borer 24-26 days prior to S. agrili adult exposure. • Newly emerged females must be separated into groups of 20-25 to prevent overcrowding. • Groups of wasps are exposed to hosts for one week and can be re-used for three further exposures to hosts (groups consist of 10 females and 2-3 males). • Honey is provided, along with misting to provide water.

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• S. agrili completes a generation in one month. • Allowing diapause to occur is not recommended because emergence from diapause is staggered over several months and therefore cannot be timed to create synchronised groups.

Duan and Oppel (2012) investigated breeding parameters of T. planipennisi on emerald ash borer reared in tropical ash, and found that whilst no significant differences were observed in T. planipennisi parasitism rates of emerald ash borer larvae in green ash or tropical ash, significantly higher numbers of T. planipennisi offspring were produced on tropical ash compared with green ash, with broods being female-biased. In addition, these authors investigated the effects of host- parasitoid group sizes (whilst maintaining a 1:1 ratio) and the effects of increasing the parasitoid to host ratio. Larger host-parasitoid group sizes (3:3 – 12:12) were more favourable, producing significantly more offspring whilst still maintaining a strong female-biased ratio. However, increasing the parasitoid to host ratio had detrimental effects. Although more offspring were produced, the broods became male-biased (i.e. the numbers of female offspring did not change but numbers of male offspring increased) and female fitness was reduced even at a 2:1 ratio (Duan and Oppel, 2012). Watt et al. (2015) suggest that this could have been due to superparasitism (the parasitism of one host by more than one individual of the same species, and a phenomenom that they advise should be avoided becasue of the detrimental effects observed by Duan and Oppel (2012). As a result of their findings, Duan and Oppel (2012) recommended that T. planipennisi rearing programmes included the use of tropical ash rather than green ash, and maintenance of larger host- parasitoid group sizes (≥ 3:3) whilst keeping the parasitoid:host ratio at 1:1.

Briefly, current rearing methods for T. planipennisi, as described by Lelito et al. (2015) and USDA- APHIS/ARS/FS (2016) are very similar to those of S. agrili but with the following differences:

• Rearing conditions of 25°C, 75-80% relative humidity and a 16h :8 h light : dark lighting regime are used. • Rearing logs are from smaller trees (bark < 3 mm thick). • Ash logs are set up with emerald ash borer 22-24 days prior to T. planipennisi adult exposure because this parasitoid takes longer to find and parasitize the available hosts. • 12-15 parasitoids are used in each exposure cage. • Groups of T. planipennisi females are used twice. • Honey, streaked on the cage lids, is provided throughout. • T. planipennisi can be stored for long periods at 4 ± 1°C (> 75-80% relative humidity) in a state of torpor with low associated mortality (< 10% for up to six months). This allows for controlled and predictable adult wasp emergence.

A better understanding of fitness parameters has also been sought for S. galinae by Watt et al. (2015). They used third and fourth instar emerald ash borer larvae reared on tropical ash. Parasitoid: host ratio was investigated using four different ratios (1:1, 2:1, 4:1 and 8:1). The authors established that parasitism significantly increased with increasing parasitoid: host ratio, with ≥ 75% parasitism using the 8:1 ratio, while at the same time did not impact on brood size, sex ratio or female fitness parameters (Watt et al., 2015). Parasitoid and host group size (density) was also investigated; the parasitoid : host ratio was kept at 1:1 but the size of the groups was increased (groups of 1, 5, 10 and 20 parasitoids and hosts were used; Watt et al., 2015). Parasitism rates were significantly higher

Control and management strategies for emerald ash borer ∣ March 2017 Page 37 when groups of five or more parasitoids and hosts were used (>80 %) compared with 46% when groups consisted of a single pair. The number of progeny was also significantly altered according to the group sizes, with groups of ten and 20 parasitoids and hosts producing significantly more progeny than the smaller groups, and a group of ten significantly out performing a group of 20, whilst having no detrimental effect on the sex ratio of the emerging adults (Watt et al., 2015). Consequently, Watt et al. (2015) suggest that the mass rearing of S. galinae should expose groups of ten fourth instar emerald ash borer larvae to ten S. galinae.

Rearing methods for S. galinae are also described by Lelito et al. (2015) and USDA-APHIS/ARS/FS (2016). Some key points are outlined briefly below.

• Rearing conditions of 25 ± 1°C, 65 ± 10% relative humidity and a 16h :8 h light : dark lighting regime are used (temperatures < 15°C will induce obligatory diapause in mature S. galinae larvae). • Females are exposed to third and fourth instar emerald ash borer larvae reared on green or tropical ash logs however, non-emergence of S. galinae is much lower (only 2.1%) on tropical ash compared green ash (20%). • Results indicate that adult wasps can be exposed to emerald ash borer hosts for several weeks. • When reared as single pairs the wasps produce more progeny (average 47) than when reared in groups (average 31), contradicting the results of Watt et al. (2015). • Material can be stored for up to six months without any reduction in adult emergence but it is not yet known whether this is detrimental to adult fitness. • Generaion time is 29 days.

Risk assessments

Using biological control agents, such as parasitoid wasps, outside of their natural host range is not without risks of non-target effects, and as such step-wise environmental risk assessment schemes have been proposed to evaluate the risks associated with release (van Lenteren et al., 2003, 2006; van Lenteren and Loomans, 2006). Such risk assessment schemes have been discussed in a previous review for by Down and Audsley (2016b) and therefore are not included in this current review.

Methods for releasing parasitoids

Detailed guidance on site selection and methods of release for these four parasitoid species are provided by the USDA in their guidelines for the release and recovery of emerald ash borer (USDA- APHIS/ARS/FS, 2016), and are briefly discussed below.

Sites with good access, a high density of ash trees of varying sizes, and a low to moderate emerald ash borer density, as determined by the ash tree crown class condition 1 (healthy) and 2 (mostly healthy) (according to Smith (2006) and described in USDA-APHIS/ARS/FS, (2016)) are considered to be good release sites. Sites can include naturally forested areas, woodlots, wooded wetlands and riparian zones but areas that may be harvested or developed within five years should be avoided,

Control and management strategies for emerald ash borer ∣ March 2017 Page 38 along with areas with high amounts of human activity and transport (USDA-APHIS/ARS/FS, 2016). Sites should be at least 40 acres in size, with at least 25% (preferably more) of the trees being ash of varying sizes (seedlings through to mature trees); if smaller sites are used then they should have a higher density of ash and they should also be connected to other woodland areas via ash corridors (USDA-APHIS/ARS/FS, 2016).

Ideally, parasitoids should be released on a number of trees at the centre of each site, at least 100 m in from the edges if the edges are determined by roads and other non-wooded areas. At least the minimum number of recommended parasitoids should be released in the spring, and mid- to late summer, over a two year period, with releases of the larval parasitoids timed for the presence of third and preferably fourth instar larvae, and releases of O. agrili timed for when emerald ash borer eggs are present (USDA-APHIS/ARS/FS, 2016). Ideally the presence of the correct emerald ash borer life stage should be deterimined e.g. scraping ash bark to determine developmental life stages and trapping of adults at the release site. However, if this is not possible then spring releases of the larval parasitoids can be started when 300 growing degree days have been reached (based on 10°C), when a minimum of 200 adult females should be released every other week for five weeks (i.e. a minimum of 600 females); late summer/autumn releases of the larval parasitoids should commence from 1800 growing degree days, and again a minimum of 200 adult females should be released every other week for five weeks (USDA-APHIS/ARS/FS, 2016). More recently larval parasitoids have been released into the field at the pupal stage rather than as adults; small ash logs containing the parasitoid pupae are attached to trees and left in place for a minimum of six weeks to allow emergence of the adults (USDA-APHIS/ARS/FS, 2016).

Releases of O. agrili can begin once 800 growing degree days have accumulated (USDA- APHIS/ARS/FS, 2016), when a minimum of 100 adults should be released every week for four to six weeks (USDA-APHIS/ARS/FS, 2016). As O. agrili are not good flyers they should be released throughout the site to help ensure their establishment and dispersal (USDA-APHIS/ARS/FS, 2016). Oobius agrili parasitoids can also be released into the field as pupae within emerald ash borer eggs on filter paper in small plastic cups (oobinators), which should be left in place for at least six weeks to allow all adults to emerge (USDA-APHIS/ARS/FS, 2016).

Interspecific competition

Biological control programmes utilising multiple species will not necessarily be more successful than programmes that use just one species as has often been the case when used against insect pests; when the multiple species approach has appeared to be successful, the success is actually often due to only one of the released control agents (Denoth et al., 2002). Interspecific competition is common between parasitoid species and occurs both amongst the adults, searching out and ovipositing in shared host species, and between the larvae developing within/on the same host (Mackauer, 1990; Godfray, 1994; Quicke, 1997). Therefore programmes using multiple biological control agents must be designed with due understanding of such interspecific competition in order to predict the outcome (DeBach 1966; Ulyshen et al., 2010b; Yang et al., 2012).

Ulyshen et al. (2010b) published the results of laboratory and field studies investigating the possible interactions between S. agrili and T. planipennisi. In the field, and in the absence of the other

Control and management strategies for emerald ash borer ∣ March 2017 Page 39 parasitoid, both species showed similar rates of parasitism (Ulyshen et al., 2010b). However, whilst laboratory studies indicated that T. planipennisi did not parasitize (non parasitized) emerald ash borer larvae in the presence of S. agrili, in the field parasitism did occur (Ulyshen et al., 2010b). In contast, S. agrili would happily parasitize emerald ash borer larvae in the presence of T. planipennisi both in the laboratory and the field (Ulyshen et al., 2010b). The authors hypothesised that if these two species were released simultaneously then S. agrili would outcompete T. planipennisi because it is more efficient at locating and parasitizing hosts within the first 27 hours of exposure whereas T. planipennisi do not appear to be able to locate and parasitize hosts within that time period. When presented with hosts that were already parasitized by the other species, T. planipennisi would not parasitize on S. agrili-parasitized host wheras S. agrili would parasitize hosts already parasitized by T. planipennisi (although a preference for non-parasitized hosts was observed) (Ulyshen et al., 2010b). However S. agrili eggs laid on T. planipennisi-parasitized larvae failed to complete development before the T. planipennisi offspring emerged from the host (the T. planipennisi offspring being unaffected; Ulyshen et al., 2010a). Whilst these authors concede that the implications of their research are limited by difficulties in predicting how the two species will interact in the field, they recommend that they be released separately, in space and time, to limit negative interaction, until more is known as to whether the two species will be able to co-exist in North American forests (Ulyshen et al., 2010b).

Yang et al. (2013) conducted similar laboratory experiments to investigate the interactions between S. agrili and T. planipennisi. In contrast to the earlier Ulyshen et al. (2010b) study, these authors found that T. planipennisi would attack hosts previously parasitized by S. agrili for up to two days post parasitism by S. agrili, even when presented with a choice between these and healthy hosts; rates of parasitism were however significantly lower (22.7% and 68% respectively) and the number of progeny produced lower. In fact the T. planipennisi larvae were often found dead within the host whilst the S. agrili successfully developed to adulthood. Discrimination of parasitized and non- parasitized hosts was not immediate. No significant differences in rates of parasitism were observed in choice tests when T. planipennisi was exposed to hosts parasitized by S. agrili up to two hours beforehand (Yang et al., 2013). The authors suggest differences in methodology between their study and the Ulyshen et al. (2010b) study account for the contradictory observations. In contrast, the ability of S. agrili to parasitize and develop in hosts was unaffected by previous exposure of the host to T. planipennisi (Yang et al., 2013). Whilst these results would suggest that S. agrili might outcompete T. planipennisi, the authors suggest that in the field this is actually unlikely to happen. Their reasons being that T. planipennisi females have demonstrated that they can distinguish between healthy hosts and those already parasitized by S. agrili and that in the field hosts would be very abundant, providing the female parasitoids with plenty of choice (Yang et al., 2013).

Interspecific competition may also occur between S. agrili, T. planipennisi and S. galinae as they all have a preference for later instar emerald ash borer larvae (Yang et al., 2012). In both choice and no choice experiments, S. galinae have been observed to parasitize larvae already parasitized by T. planipennisi provided they were exposed to the larvae within four days of T. planipennisi parasitism. Rates of parasitism and numbers of progeny were however significantly lower in the T. planipennisi- parasitized hosts compared with the healthy non-parasitized hosts (Yang et al., 2012). The authors suggest this indicates that S. galinae is able to discriminate between healthy hosts, and those already parasitized, thus reducing the potential for negative effects when using these two parasitoids together. They go on to suggest that in the field, where healthy emerald ash borer larvae

Control and management strategies for emerald ash borer ∣ March 2017 Page 40 would be in abundance, little co-parasitism between S. galinae and T. planipennisi could be expected, and that these two species of parasitoid could be co-released in a biological control programme. It should be pointed out that Yang et al. (2012) did not conduct the converse set of experiments i.e. assessing the behaviour of T. planipennisi with hosts already parasitized by S. galinae.

Methods for monitoring the dispersal and establishment of released parasitoid wasps

In order to determine establishment of the parasitoids, recovery data should be obtained for at least one year following the final release (USDA-APHIS/ARS/FS, 2016). Methods for monitoring the dispersal, and establishment of, and impact of the biological control provided by the parasitoids following release are detailed by the USDA in their guidelines for the release and recovery of emerald ash borer (USDA-APHIS/ARS/FS, 2016) and by (Abell et al., 2015) and are briefly discussed below.

Adults of all species can be passively trapped using yellow pan traps and this is a relatively simple method of assessing establishment at a release site (Abell et al., 2015) but it does not provide any data on rates of parasitism (reported in Duan et al., 2012c). Yellow pan traps are not species specific which can be a further disadvantage as it means that personnel trained in taxonomy and identification are required to identify the species caught (Gould et al., 2015). A considerable amount of time might also be required to examine the trap contents, and separate out the species of interest from the remainder of the catch if incidental trap catches are high (Abell et al., 2015). That said, this non specificity can be an advantage if one or more parasitoids have been released and require monitoring (Abell et al., 2015). The greatest drawback perhaps is that the effectiveness of yellow pan traps is unknown and they may not be able to detect low density populations (Abell et al., 2015). The efficacy of yellow pan traps for catching S. agili and T. planipennisi can be improved by using recently identified pheromones as lures (Abell et al., 2015). However, these compounds are not commercially available and therefore must be synthesised. In the case of S. agrili, the identified pheromone is an aggregation pheromone and attracts both males and females (Cossé et al., 2012) whilst the pheromone identified from T. planipennisi is a female-produce sex pheromone that attracts males (Bauer et al., 2011a; Abell et al., 2015).

Monitoring for O. agrili parasitism is difficult and time consuming because the host eggs are small and hidden within bark crevices (Duan et al., 2012c). Methods that can be used include the use of sentinel eggs, and collecting and examining emerald ash borer eggs from the field for the presence of O. agrili parasitism (Abell et al., 2015).

Egg sentinel deployment can be conducted by placing laboratory reared eggs under small flaps of bark deliberately cut for this purpose or in protective enclosures that allow access for O. agrili but not to predators. However, the current preferred method of deploying egg sentinels involves the use of egg sentinel logsand was developed by Duan et al. (2012c). The former two egg sentinel methods are time consuming, and when eggs are placed under bark flaps they can be damaged during deployment, are prone to predation, and can be overlooked at the point of retrieval (Duan et al., 2011b; Abell et al., 2015). Egg sentinel logs have advantages over other methods of assessing O. agrili but are both time-consuming and it is expensive to produce the number of laboratory-reared

Control and management strategies for emerald ash borer ∣ March 2017 Page 41 eggs required (5-100 eggs are required per log), and eggs are still prone to predation even though a protective covering is used (Abell et al., 2015).

Egg sentinel logs are prepared in the laboratory by allowing emerald ash borer females to lay eggs in green ash logs (25 cm long, 5 cm diameter) (Duan et al., 2012c). Eggs can be counted and then protected by covering with curling ribbon before deployment. The method was tested at study sites previously used for O. agrili release (within the previous two years), and each site included a release and non-release control plot. Ten egg-sentinel logs were used at each site (five in the release plot and five in the control plot (Duan et al., 2012c) and attached to the trunks of ash trees. They were left at the field sites for two weeks to allow time for parasitism of the eggs. After this point the egg sentinel logs were returned to the laboratory and incubated before a second egg count was performed, and the eggs dissected to ascertain evidence of parasitism. Naturally occurring emerald ash borer eggs at these sites were also visually sampled for parasitism (plots visually searched for 30 minutes) in order to compare the efficacies of the two methods. These authors report that across the sites, 20-67% of the egg-sentinel logs contained one or more eggs parasitized by O. agrili, with 0.4 – 5.9% parasitism recorded (3.2% average across the sites). In comparison, visual surveying of naturally occurring eggs only detected parasitism in one of the three release plots on 30% of the sampled trees, resulting in 2.4% egg parasitism at that site. Interestingly this site was in fact, the same site that yielded the lowest percent egg parasitism using the egg-sentinel log method (0.4%). Overall, these authors conclude that the use of the egg-sentinel logs were successful at assessing establishment of O. agrili, and was more effective and less labour intensive than finding and visually inspecting naturally laid emerald ash borer eggs.

However, assessment of naturally occurring emerald ash borer eggs is the only method of detection that provides information on parasitism rates and the impact of released O. agrili on emerald ash borer populations (Abell et al., 2015). These assessments can be performed either by searching a tree for a fixed amount of time (e.g. 30 minutes) for the presence of eggs, and removing bark with eggs attached for subsequent inspection in the laboratory for signs of parasitism. Alternatively, a fixed amount of bark can be removed from each sampled tree, returned to the laboratory where it is sub-sampled by shaking a proportion of the bark above a nylon mesh to loosen and remove the eggs, which can then be inspected for signs of parasitism. Bark sifting is more time consuming than simply searching for eggs but is not hampered by factors such as light, weather conditions, difficulty of finding the eggs in the first place and variations in the ability of the assessor (Abell et al., 2014, 2015). Abell et al. (2014) recommend that the bark collection and sifting method is more reliable than the visual detection method, and should therefore be used when information on rates of parasitism, rather than simply detection of O. agrili following release, are required. Whichever sampling method is used, care needs to be taken that sampling bias is not inadvertently introduced into the process resulting in potential skewed data (Abell et al., 2015).

The above methods of monitoring can be adapted for monitoring the establishment of introduced larval parasitoids. Sentinel larvae can be used and in the simplest format, live larvae are inserted directly under the bark of live ash trees in the field (Abell et al., 2015). Alternatively, adult emerald ash borer can be caged around a tree trunk to oviposit or eggs fixed to the bark and the hatching larvae bore under the bark and develop (Abell et al., 2015). Larval sentinel logs can also be deployed, and provide a non-destructive and standardised method of monitoring for establishment of introduced parasitoids (Abell et al., 2015). Third and fourth instar larvae can be inserted into logs or

Control and management strategies for emerald ash borer ∣ March 2017 Page 42 eggs are fixed to the ash logs and the hatching larvae bore in naturally and are allowed to develop (Abell et al., 2015). The logs are then placed on ash trees in the field and left for one to two weeks before returning to the lab for analysis. It is more preferable to insert larvae rather than use eggs because a proportion of eggs will fail to hatch meaning an accurate starting number of host larvae cannot be attained (Abell et al., 2015). Larval sentinel logs, like their egg sentinel log counterparts are labour intensive to set up and require not only a supply of emerald ash borer larvae but also a supply of suitable ash logs both for the rearing of the larvae and for the production of the sentinel logs themselves (Abell et al., 2015). In addition, whilst predation of sentinel larvae is not normally an issue, fungal and bacterial contamination can be problematic and the sentinel larvae can be attacked and parasitized by native species of parasitoids rendering them unable to perform the function intended (Abell et al., 2015).

Again, the only method that allows for the direct monitoring of parasitism rates in the field, and impact on emerald ash borer populations, is to sample naturally occurring emerald ash borer larvae. Once larvae are found they can either be examined in the field or taken back to the laboratory for to look for signs of parasitism (Abell et al., 2015). This method does not require any of the extensive set up necessary for the production of sentinel logs however, it is a destructive method of sampling, and this needs to be taken into account if sampling is required over a number of years (Abell et al., 2015).

The release and establishment of the parasitoids used in classical biological control programmes for controlling emerald ash borer in the U.S.A. are reviewed in Chapter 9.

Associations in invaded areas between native parasitoid species and emerald ash borer

The search for indigenous natural parasitoids of North America with the potential to parasitize emerald ash borer began almost immediately in Michigan upon discovery of emerald ash borer. In 2002/2003 Bauer et al. (2004c) surveyed immature stages of emerald ash borer within a woodlot in Michigan, collecting specimens to rear in the lab for identification. Several native hymenopteran larval-pupal parasitoids, including braconids (Spathius simillimus Ashmend, Heterospilus sp., Atanycolus sp.), a chalcid (Phasgonophora sulcata Westwood), two eupelmid species (Balcha sp. and Eupelmus sp.), an eulophid egg parasitoid (Pediobius sp.), and three ichneumonid species (not identified) appeared to have already become associated with emerald ash borer in the field. Parasitism rates were low (0.05 – 0.3%; Bauer et al. (2005)), and the Balcha sp. was the most prevalent parasitoid found (Bauer et al., 2004c).

More recent surveys have been reported upon in other areas of the U.S.A. such as the one conducted in 2008 in Western Pennsylvania by Duan et al. (2009). Five species of hymenopteran parasitoids were found associated with emerald ash borer, including Balcha indica Mani & Kaul (Eupelmidae) (n = 32, accounting for 82% of the parasitoids recovered), Eupelmus pini Taylor (Eupelmidae)(n = 1), Dolichomitus vitticrus Townes (Ichneumonidae) (n = 2) and an unidentified Orthizema sp. Townes (n = 1) and Cubocephalus sp. Townes (n = 3) (both ichneumonids) (Duan et al., 2009); these five species accounted for an overall parasitism rate of 3.6% of the sampled emerald ash borer hosts (n = 1091). However, the authors were unable to confirm whether the three ichneumonid species were associated with emerald ash borer or to other insects infesting the ash

Control and management strategies for emerald ash borer ∣ March 2017 Page 43 bark. Laboratory studies confirmed that both B. indica and E. pini successfully attacked, and developed on, late instar larvae, pre-pupae and/or pupae of emerald ash borer (Duan et al., 2009).

A further study was conducted over a more extensive area of Pennsylvania a year later by Duan et al. (2013b). Once again B. indica was recovered from both survey sites together with the native braconid parasitoids Spathius laflammei Provancher (also known as Spathius benefactor Matthews) and Atanycolus nigropyga Shenefelt. In addition, at sites in western Pennsylvania, where rates of parasitism ranged from 0.5 to 4.6%, two further unidentified braconid species were found associated with emerald ash borer, a Spathius sp. and an Atanycolus sp. (possibly Atanycolus disputabilis (Cresson))(Duan et al., 2013b). At the central Pennsylvania sites, where rates of parasitism ranged from 0.5 to 1.5% parasitism) an ichneumonid Dolichomitus sp. was discovered (Duan et al., 2013b), along with A. nigropyga, S. laflammei and the unidentified Spathius sp., all associated with third and fourth instar larvae (Duan et al., 2013b). The Spathius spp. were gregarious in nature (3-9 parasitoid larvae per host larvae) whilst the Atanycolus spp. were solitary in nature (Duan et al., 2013b).

Perhaps the most promising indigeneous native parasitoid found attacking emerald ash borer larvae is the solitary Atanycolus sp. found in Michigan by Cappaert and McCullough (2008), subsequently described as Atanycolus cappaerti Marsh and Strazanac (Cappaert and McCullough, 2009), and associated with third and fourth instar emerald ash borer larvae. Upon discovery, average rates of parasitism at nine different locations ranged from 2 to 73%, and parasitism within individual trees reached 83%. The authors state the species was a well established parasitoid of emerald ash borer, over a large area (600 hectare site) amongst tens of thousands of trees distributed over the area, and hypothesise that it is either a rare native or nonindigenous species that has adopted emerald ash borer as its host (Cappaert and McCullough, 2008). Originally there was no evidence observed to suggest that it parasitized other common buprestid or cerambycid hosts (Cappaert and McCullough, 2008) although subsequent work has demonstrated that it will readily attack Agrilus liragus and A. bilineatus, and it is thought probably other Agrilus species too (Cappaert and McCullough, 2009).

Additional survey data include a report that the braconid Leluthia astigma (Ashmead) is associated with emerald ash borer in Ohio (Kula et al., 2010), and the association of both P. sulcata and B. indica in Ontario, Canada; P. sulcata was more abundant and thought to have a parasitism rate of approximately 40% (Lyons, 2008). In addition to B. indica, P. sulcata, Atanycolus sp., Spathius sp. and Eupelmus sp., Duan et al. (2012d) also report the presence of a Eurytomus sp. in Michigan during their surveys.

No native Tetrastichus species have yet been found attacking emerald ash borer in North America even though 21 species are known to be present (reported in Liu et al., 2007), one of which attacks bronze birch borer (Loerch and Cameron, 1983). Neither have any native egg parasitoids been discovered attacking emerald ash borer populations in North America. However, two new native Oobius species that parasitize eggs of other Agrilus species have been identified, namely Oobius minusculus Triapitsyn & Petrice, sp. n., which parasitizes both A. subcinctus Gory on ash and A. egenus Gory on black locust (Robinia pseudoacacia L.) trees, and Oobius whiteorum Triapitsyn sp. n., which parasitizes A. anxius Gory on European white birch (Betula pendula Roth) (Triapitsyn et al.,

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2015). In addition, other species of egg parasitoids have been reared from the native bronze birch borer (reported in Liu et al., 2007).

The most prevalent species found attacking emerald ash borer in North America are Atanycolus spp. and those that attack Agrilus spp. The parasitoids showing the highest rates of parasitism, and therefore the highest potential for natural suppression of emerald ash borer populations or use in augmentative biological control programmes, are the native P. sulcata and A. cappaerti, and the self- introduced exotic species B. indica (Bauer et al., 2015b). The biology of these three parasitoids has been investigated in some detail and can be found in the literature (Cappaert and McCullough, 2009; Duan et al., 2011c; Bauer et al., 2015b). It should be noted that the long life cycle of B. indica may be problematic when it comes to rearing the parasitoid and could limit its suitability as a biological control agent (Duan et al., 2011). Associations of native hymenopteran parasitoids with emerald ash borer are likely to continue to evolve and therefore surveying should continue (Duan et al., 2013b).

Very recently, a braconid parasitoid has been observed attacking emerald ash borer that have invaded European Russia (Orlova-Bienkowskaja and Belokobylskij, 2014; Orlova-Bienkowskaja, 2015). Spathius polonicus Niezabitowski (Hymenoptera: Braconidae) is described as a rare but widely distributed parasitoid of the western Palaearctic region, and has been recorded in many European countries (Belokobylskij, 2003; Orlova-Bienkowskaja and Belokobylskij, 2014) but has not previously been recorded in central European Russia (Orlova-Bienkowskaja and Belokobylskij, 2014). Orlova- Bienkowskaja (2015) suggest that the parasitoid could be a non-native species that came in naturally after the establishment of emerald ash borer or that it could have been introduced with emerald ash borer; the latter is thought unlikely. This species of parasitoid is a known ectoparasitoid of several buprestid species, including Agrilus suvorovi Obenberger and Agrilis viridis Linnaeus (Belokobylskij, 2003), and has now been found in late instar emerald ash borer larvae (Orlova- Bienkowskaja and Belokobylskij, 2014; Orlova-Bienkowskaja, 2015), with up to six offspring per host (Orlova-Bienkowskaja, 2015). These authors found evidence of high rates of parasitism (approximately 50%) across eight sites in the Moscow region, the furthest apart being 78 km (Orlova-Bienkowskaja, 2015). It has been suggested that this parasitoid could be augmented and released as a biological control agent for emerald ash borer, and could be well suited for this purpose as it is a native of temperate climates however, the potential for its use as a biological control agent would need to be further investigated (Orlova-Bienkowskaja and Belokobylskij, 2014; Orlova-Bienkowskaja, 2015).

The use of insecticides in conjunction with biological control agents

Potential exists for insecticides (particularly systemic insecticides) to be used in conjunction with biological control agents. Both additive and synergistic effects are possible because decreasing the pest density with a density-independent tactic (such as an insecticide) can enhance the effectiveness of a density-dependent tactic (such as biological control) (McCullough, 2015). McCullough and Mercader (2012) suggest that treating a proportion of trees with emamectin benzoate may allow introduced or native parasitoids to exert a demonstrable effect on emerald ash borer populations, which are currently thought to be so high that they overwhelm the parasitoid numbers. In addition, since parasitoids (and woodpeckers) do not prey upon dead larvae they are unlikely to come into contact with a systemic insecticide and therefore will not encounter harmful effects from the

Control and management strategies for emerald ash borer ∣ March 2017 Page 45 insecticide (McCullough, 2015). A recent study by Davidson and Rieske (2016) attempted to evaluate the compatibility if imidacloprid soil drenches with the release of T. planipennisi, S. agrili and O. agrili by comparing the efficacy and effects of full strength imidacloprid treatment, half strength imidacloprid treatment plus parasitoid release, parasitoid release, and no treatment on rates of larval parasitism and ash canopy decline. Spathius agrili was not recovered during the course of the investigation, probably due to failure to establish however, both T. planipennisi and O. agrili were recovered from emerald ash borer on trees that had also been treated with imidacloprid (Davidson and Rieske, 2016). No differences in rates of parasitism were observed between the insecticide- treated plots and no insecticide-treated plots, indicating that the two methods of control may be compatible (Davidson and Rieske, 2016). In this particular study, ash canopy decline continued in all plots but this was thought due to the large size of the trees, making the imidacloprid treatment less effective, however, lower densities of emerald ash borer larvae were seen in both the plots receiving the imidacloprid treatment, perhaps indicating that using a half strength dose of imidacloprid might be suitable for lowering the densities of larvae in treated trees whilst at the same time allowing development of parasitoid populations (Davidson and Rieske, 2016). Offspring of the egg parasitoid O. agrili should be able to develop on trees treated with insecticide as they will not encounter a systemic insecticide, resulting in the emergence of adult parasitoids that potentially will fly away and parasitize eggs on both treated and untreated trees (McCullough et al., 2015). However, depending on the efficacy of the insecticide used, there may not actually be any fourth instar larvae developing within an insecticide-treated tree.

Summary

1. Surveys conducted in the native ranges of emerald ash borer identified a number of parasitoid species with the potential to be introduced into North America as classical biological control agents.

2. After extensive laboratory testing, four suitable parasitoid species were decided upon and have been approved for release into the U.S.A. These are the egg parasitoid O. agrili, and the larval parasitoids T. planipennisi, S. agrili and S. galinae. Tetrastichus planipennisi was approved for release in Canada in 2013.

3. During the evaluation, process extensive research was performed and is detailed in the USDA Forest Service technology transfer document FHTET-2014-09 (2015). This research included investigations into the biology of the species, climatic matching, host specificity testing and mass- rearing methods. In addition methods for confirming the establishment of the parasitoids once released have been determined. Detailed rearing, release and recovery methods are also provided by the USDA APHIS Biological Control Production Facility (USDA-APHIS/ARS/FS, 2016).

4. Tetrastichus planipennisi has a relatively short ovipositor and can therefore only attack emerald ash borer in small trees (< 12 cm dbh) with thin bark.

5. Spathius galinae is suited to more northerly regions and has a long ovipositor meaning that it could nicely complement a biological control programme already utilising T. planipennisi and O. agrili.

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6. Decision makers should be aware of the potential for negative interactions between parasitoid species when multiple biological control agents are used.

7. A number of native hymenopteran parasitoids are known to attack emerald ash borer in North America (Table 3) but with the exception of A. cappaerti, B. indica and P. sulcata, parasitism rates are generally very low.

8. A braconid parasitoid, S. polonicus, has recently been discovered attacking emerald ash borer larvae in the invaded area of European Russia; parasitism rates appear to be high (ca. 50%) and the parasitoid widely distributed.

9. Potential exists for the combined use of insecticides and parasitoids, the aim being that the insecticide will suppress emerald ash borer populations sufficiently to allow the parasitoid populations to establish and take hold (subject to compatibility studies).

Table 3. Species of native hymenopteran parasitoids found attacking emerald ash borer in North America. Compiled from the literature reviewed and from the table presented by Bauer et al. (2015a,b). 1. Actually not native, thought to be self-introduced in the 1960s. 2. Association with emerald ash borer not confirmed.

Species Family Area where found in Stage of emerald ash North America borer attacked Balcha indica1 Eupelmidae Michigan Late immature stages Western Pennsylvania Canada Eupelmus pini Eupelmidae Michigan Late immature stages Western Pennsylvania Phasgonophora sulcata Chalcididae Michigan Immature stages Canada Atanycolus spp. Braconidae Michigan Late immature stages Atanycolus nigropyga Braconidae Western and Central Third and fourth instar Pennsylvania larvae Atanycolus cappaerti Braconidae Michigan Third and fourth instar larvae Atanycolus hicoriae Braconidae Northeastern USA Larval stages Atanycolus simplex Braconidae Northeastern USA Larval stages Heterospilus sp. Braconidae Michigan Immature stages Spathius floridanus = Braconidae Michigan Late immature stages Spathius simillimus Spathius sp. Braconidae Western Pennsylvania Third and fourth instar larvae Spathius laflammei = Braconidae Western and Central Third and fourth instar Spathius disputabilis Pennsylvania larvae Leluthia astigma Braconidae Ohio Late larval stages Dolichomitus vitticrus2 Ichneumonid Western Pennyslvania ae Orthizema sp.2 Ichneumonid Western Pennyslvania ae Cubocephalus sp.2 Ichneumonid Western Pennyslvania ae

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Chapter 5: Microbial control agents

Entomopathogenic fungi

Entomopathogenic fungi have a number of characteristics that make them good potential candidates for biological control. These include the ability to cause infection in all life stages of an insect, and the ability to provide an ongoing source of inoculum to spread the disease within a population by sporulating and multiplying within cadavers (Johny et al., 2012). As such they can be used to manage a number of agricultural pests (Copping, 2001; Gwynn, 2014) and are now also under investigation for the sustainable management of other invasive woodboring insects such as Japanese pine sawyer (Monochamus alternatus Hope) and Asian longhorned beetle (Anoplophora glabripennis (Motsch.) (Shimazu and Sato 1995; Dubois et al., 2004a,b; Hajek et al., 2006; Liu and Bauer, 2008b).

No entomopathogenic fungi were isolated from larvae collected during the initial surveys for natural enemies of emerald ash borer in China (Liu et al., 2003) although Beauveria bassiana (Balsamo) Vuillemin has subsuequently been found (Yang et al., 2014). Exploratory surveys in Michigan found that approximately 2% of emerald ash borer at the survey sites were infected with pathogenic fungi including isolates of B. bassiana, Metarhizium anisopliae (Metschnikoff) Sorokin, Paecilomyces farinosus (Holm ex SF Gray), Isaria farinosa (Holmsk.) Fries (formerly Paecilomyces fumosoroseus), and Lecanicillium lecanii (Zimmerman) Viegas (Bauer et al., 2004c). Laboratory studies have demonstrated that both M. anisopliae and B. bassiana (strain GHA) are highly virulent to emerald ash borer adults (Liu and Bauer, 2006). Some of the B. bassiana isolates found have been further characterised using morphological characteristics and seven microsatellite markers (Castrillo et al., 2010b). Analysis revealed that of 42 strains, which fell into four clonal groups, 32 of them had unique genotypes (Castrillo et al., 2010b). It is interesting to note however, that Johny et al., (2012) included five of these isolates in their characterisation study for comparison and identified three of them as B. bassiana, one as Beauveria pseudobassiana and one as Beauveria brongniartii) using their molecular criteria.

Castrillo et al. (2010b) chose representative strains from the different genetic clusters to compare virulence against emerald ash borer adults, both between each other and the commercial B. bassiana GHA, using dip tests. Mortality was high for all strains (73-92%), and not significantly different from each other or mortality induced by GHA (90%), with mean survival time ranging from 4 days (GHA) – 5.6 days (Castrillo et al., 2010b). The authors suggest that soil is the primary reservoir for inocula of these indigenous isolates, and that conidia move from the soil to the lower tree trunk by rain splash and air current, providing the means for emerald ash borer to become infected when they chew their way through the bark during emergence, during mating and when searching for oviposition sites (Liu and Bauer, 2008a; Castrillo et al., 2010b). In addition, neonate larvae need to chew through the bark to reach the phloem, and bark splits over feeding galleries provide opportunities for the fungal conidia to come into contact with other life stages (Liu and Bauer, 2008a; Castrillo et al., 2010b). To a certain extent a soil reservoir is also likely to constrain the levels of naturally occurring infection and limit epizootics, since emerald ash borer contact with the lower trunk is only likely to happen when a tree is heavily infested (Castrillo et al., 2010a). Infected emerald ash borer and indeed other infected insects infesting ash trees, are a potential additional

Control and management strategies for emerald ash borer ∣ March 2017 Page 48 source and dispersal mechanism of inocula, along with birds such as woodpeckers, which feed on the larvae (Castrillo et al., 2010b).

During 2008/2009 scientists in Canada surveyed five locations in southwestern Ontario where emerald ash borer had become well established (Johny et al., 2012). A range of samples were collected including dead adults, larvae and pupae, with and without visible fungal growth, and sporulating fungus from frass found in feeding galleries. Using morphological characteristics and molecular criteria, these investigators identified 78 isolates of Beauveria spp.; 17 of the isolates were identified as B. bassiana (grouped into three different sub-clades with five different genotypes within the sub-clades), whilst the remaining 62 were identified as B. pseudobassiana (two different genotypes). Representative isolates (23 in total) from the different identified clades were screened for virulence against emerald ash borer adults using the standard dip method at one concentration, along with the GHA commercial strain of B. bassiana for comparison. All isolates were pathogenic towards emerald ash borer adults with eight of them causing more than 90% mortality (Johny et al., 2012). These eight were further tested at multiple concentrations to determine differences in virulence. One strain in particular (B. bassiana L49-1AA) was both significantly more virulent (i.e. required lower concentrations for lethal effects), and produced significantly more conidia on emerald ash borer cadavers, than the other indigenous isolates and GHA (Johny et al., 2012). Whilst it also killed the adults significantly more quickly than the other indigenous isolates there was no difference in the mean survival times of adults treated with this isolate (6.16 days) compared with strain GHA (6.93 days) (Johny et al., 2012). The observed high virulence of isolate L49-1AA, coupled with its high in vivo conidia yield, led the authors to conclude that this indigenous strain should be investigated further as a potential microbial agent for controlling emerald ash borer.

The mycopesticide, Botanigard ES® (Emerald BioAgriculture, Lansing, MI), with the GHA strain of B. bassiana as the active ingredient, is already commercially available in some parts of North America, and has been evaluated for efficacy towards emerald ash borer. Adults are more susceptible than the larvae to this strain of B. bassiana when used as a pre-emergent spray (Bauer et al., 2004d). Studies by Liu and Bauer (2008a) investigated the lethal and sub-lethal effects of Botanigard ES® on emerald ash borer in both greenhouse and field trials using topical sprays compared with a fungal band treatment of GHA. Moderate effects against the adults were observed in the greenhouse studies when already infested logs were sprayed prior to adult emergence (mean fungal infection rates of 27.7 – 33.5% depending on the application rate). The longevity of the adults was also significantly reduced (approximately halved) compared with the control group; in the field, reduced longevity should translate to lower fecundity and therefore lower larval densities (Liu and Bauer, 2008b). In the field, the formulation was sprayed onto green ash tree trunks in the summer prior to adult emergence. Trees were approximately 20 years old, 9-14 cm dbh, height 8-10 m, and moderately infested with emerald ash borer. Adult infection rates ranged from 58.5 – 83% depending on the application rate used; however, the fungal band treatment was not so effective (32% adult mortality) (Liu and Bauer, 2008a). In comparison, fungal spray treatments applied in the autumn to the bark of white ash (7-10 cm dbh, 5-6 m height, with significant longitudinal bark splits) resulted in just 8% larval mortality but larval development appeared to be slower, as demonstrated by significantly fewer pre-pupae compared with the control group (Liu and Bauer, 2008a). These authors demonstrated that applying B. bassiana strain GHA to the bark prior to adult emergence could prove to be a viable means of managing emerald ash borer.

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Further data from field trials, investigating the application of Botanigard ES® as foliar and trunk sprays in areas of newly established and well established emerald ash borer, have been reported by Liu and Bauer (2008b). A reduction of 41% was seen in the emerald ash borer larval population in areas where emerald ash borer colonisation was new (predominantly white ash) following application, and 20% of larvae were infected with the fungus (Liu and Bauer, 2008b). Comparative results were observed when areas with well established emerald ash borer populations were treated (predominantly green ash; 47% reduction in larvae, 21% of larvae were infected; Liu and Bauer, 2008b). Some leaves were removed from trees following treatment in order to investigate the persistence of the fungal conidia. Collected leaves were used in adult leaf bioassays, and the results from these bioassays indicated that the conidia were able to persist in the environment for at least 11 days (78-100% adult death was observed after seven days of exposure to leaves that were collected from 2 hours to 264 hours after fungal application; Liu and Bauer, 2008b). In addition, during the following year, fewer emerald ash borer adults were present (63% less), and 42% less canopy dieback was observed, in the treated areas compared with the non-treated areas (Liu and Bauer, 2008b).

Deposition and persistence of B. bassiana strain GHA when applied as a trunk and foliar spray for controlling emerald ash borer has been further investigated in order to help develop effective and economic application strategies (Castrillo et al., 2010a). Viable conidia were still present 14 days after spraying, and could induce 11-40% mortality when presented to adult beetles however, a decline in virulence was observed within a week (50-83% mortality when presented one day after treatment (Castrillo et al., 2010a). These authors also state that unpublished work demonstrated the recovery of viable B. bassiana strain GHA from green ash tree bark more than a year after application. The cracks and crevices within the bark are likely to afford fungal conidia some protection when they get lodged in them during high pressure spray applications (Castrillo et al., 2010a). Decline in viability is more pronounced on leaf surfaces than on bark, but no differences in recovery of conidia were observed between the upper or lower leaf surfaces. This is promising because adults normally land and feed on the upper surface, and conidia on the upper surface are exposured to UV light (reduces viability of spores) and greater likelihood of being washed off from rainfall (Castrillo et al., 2010a). Canopy decline at the study sites was minimal due to infestation and such overlapping canopy may have protected conidia on the upper leaf surfaces (Castrillo et al., 2010a).

More recently the use of an autocontamination trap system has been investigated as a means of delivering two field-isolated strains of B. bassiana fungal conidia (L49-1AA and INRS-CFL, originally collected from the scolytinid beetle Tomicus piniperda L.) to emerald ash borer (Lyons et al., 2012). Autocontamination chambers containing the fungal isolates were attached to green multifunnel traps baited with (3Z)-hexenol, which were then placed in the field. Initially, viability of the fungal spores was tested by swabbing the pouches containing the spores at time intervals (up to 57 days) to analyse the spore counts and germination rates. Results indicated that whilst the INRS-CFL strain maintained good pathogenicity after 57 days of exposure in the field (> 69% conidia germination), in contrast pathogenicity of the L49-1AA strain was very low (< 5.3% germination), and indeed was low at all sample time points (Lyons et al., 2012). Autocontamination of adult beetles was tested out in the laboratory using fungal pouches that had been hung outdoors in the traps. Once again, strain INRS-CFL outperformed L49-1AA, with mean conidia loads on adult beetles following contact with the pouches calculated to be 579,200 and 2,400, respectively (after pouches had been exposed in

Control and management strategies for emerald ash borer ∣ March 2017 Page 50 the field for 29 days), although most beetles exposed to both strains of the pathogen died within 6 - 12 days of contamination (Lyons et al., 2012). The authors hypothesised that the poor viability and spore loads observed with the L49-1AA strain, which had previously shown good pathogenicity to emerald ash borer (Johny et al., 2012) was either due to suboptimal formulation within the pouches or adverse storage conditions prior to deployment. Autocontamination of emerald ash borer with strain L49-1AA was further tested out in the field. Non-sticky green multifunnel traps, baited with (3Z)-hexenol, and containing pouches loaded with fungal spores were hung in the field, and sticky bands placed around trees to recapture potentially autocontaminated beetles. Approximately 7% of the recaptured beetles exhibited signs of B. bassiana infection, and further analysis revealed that 1% of beetles were positive for the L49-1AA strain of B. bassiana placed in the traps (Lyons et al., 2012). The authors concluded successful demonstration that artificial traps can be easily adapted to include a fungal autocontamination chamber, and that emerald ash borer beetles will readily visit, and then disperse fungal conidia from these traps (Lyons et al., 2012).

However, more work is needed to optimise application rates, delivery methods, determine the efficacy of foliar and trunk applications and to assess any effects on non-target organisms (Liu and Bauer, 2008a). Fungal band treatments preserve fungal conidia, delivering persistent and prolonged efficacy in the field (Dubois et al., 2004b). They are effective at controlling some other woodboring species (Shimazu and Sato 1995; Dubois et al., 2004a,b) however, they seem less effective against emerald ash borer(Liu and Bauer, 2008a). These authors hypothesised that this was because emerald ash borer beetles were more likely to fly rather than walk across the fungal band.

A short piece of work has been reported on the evaluation of the susceptibility of adult T. planipennisi and S. agrili parasitoids, to the GHA strain of B. bassiana, in laboratory assays (Dean et al., 2012). These authors exposed adult parasitoids for three hours to twigs of ash that had been inoculated with B. bassiana spores or weak detergent only (untreated control group), before transferring the insects to clean chambers containing fresh untreated ash leaves for observation over the following 10 days. Survival of the T. planipennisi adults was not affected by exposure to B. bassiana (97% survival compared with 99% survival in the control group) although, those specimens that did die following exposure to the treated leaves did die as a result of fungal infection (Dean et al., 2012). In contrast, S. agrili were marginally (but significantly) affected, with 83% survival recorded for the insects in the treatment group compared with 97% in the control group; 77% of those that died in the treatment group died as a result of fungal infection (Dean et al., 2012). It is important to note however, that whilst this study might indicate that adult T. planipennisi are not susceptible, and S. agrili adults are marginally susceptible to B. bassiana infection, it does not investigate the fate of the parasitoid larvae developing within/on emerald ash borer larvae that are infected with B. bassiana.

Other forms of microbial control

In addition to studies with B. bassiana, Bauer et al. (2004d) also found that four registered Bacillus thuringienis (Bt)-based microbial insecticides had some toxicity to emerald ash borer adults, although relatively high concentrations of the products had to be used to demonstrate toxicity.

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A further microbial product, Spinosad (an aerobic fermentation of the soil microbial, Saccharopolyspora spinosa Mertz and Yao) has also been evaluated against emerald ash borer (Lewis and Smitley, 2011). These authors report the results of a field trial where they aerially sprayed twice a year for three years, with the applications made two weeks apart, and timed to target peak adult emergence. Yearly surveys indicated that the spinosad treatment did afford the ash trees some protection against emerald ash borer. Whilst a few dead trees were observed in the treated plots, the average percentage canopy dieback was approximately 23% compared with 53% in the control plots, which also had a higher proportion of dead trees (Lewis and Smitley, 2011). Ash foliage was also collected following treatment and used for residue testing, the results of which suggested that spinosad rapidly degraded after spraying (75% of the product remained on the foliage two days post- spraying but just 5% remained after a week; however basic laboratory studies did confirm mortality when adult emerald ash borer were allowed to feed on the collected foliage (Lewis and Smitley, 2011).

Bioinsecticides however, can often harm a wide range of other invertebrate species as they are often quite broad spectrum. In addition, they are often aerially applied and as such may not adequately cover the foliage or even reach emerald ash borer adults, which spend a considerable portion of their time on the tree trunk and branches (McCullough, 2015).

Summary

1. A field collected strain (L49-1AA) and a commercial strain (GHA) of the entomopathogenic fungus B. bassiana have been demonstrated to be highly virulent towards emerald ash borer.

2. Topical spray application to the tree trunk, in the summer prior to emergence of the emerald ash borer adults, appears to be the best method of delivering B. bassiana conidia.

3. Disadvantages of microbial control agents include lack of persistence in the field following application, inadequate coverage of spray applications, and lack of specificity towards the pest species thereby potentially resulting in harmful effects on non-target insects.

4. No forms of microbial control are currently reported to be in use to control emerald ash borer.

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Chapter 6: Lure and kill decoys

An exciting new technique is under development for attracting and killing emerald ash borer adults. This technique uses a visual decoy, representing a female emerald ash borer beetle, to elicit the mate-finding behaviour of the male beetles, luring them to fly to and alight upon the decoy, which in actual fact is an electroconductive trap capable of stunning and killing the males as they land (Domingue et al., 2014).

Previous work has shown that attaching a dead female emerald ash borer beetle placed to a sticky trap is a highly effective means of attracting and detecting male adults (Lelito et al., 2008; Domingue et al., 2013). The decoys make use of biomimicry, mimicking the visual cues that the male beetles use to find a mate. In the case of emerald ash borer, these cues relate to the positioning of the wing elytra of female beetles when at rest on an ash leaf in direct sunlight (Domingue et al., 2013) and the structural features on the cuticle of the elytra, specifically the iridescent green colouration (structural interference colouration created by multilayering of the epicuticle), and the fine spicules and spines on the elytra surface, which serve to scatter the light into intense strands. (Domingue et al., 2014).

The nano-bioreplication technique developed by Pulsifer et al. (2013) involves the stamping of a polymer quarter-wave Bragg stack reflector (peak reflectance at 540-550nm wavelength), incorporating a negative nickel dye and a positive epoxy dye, cast from the elytra of a dead female emerald ash borer in order to maintain the elytral fine structure, and has been proven to replicate the structural features of the female wing elytra. The decoys were first tested out in the field, in Hungary, to assess their visual effectiveness at attracting the two-spotted oak borer A. bigutattus. The decoys successfully elicited flight of the males from a distance of 0.5 -1 m; males flew towards the decoys and alighted upon them, remaining mounted on the decoys for up to 2 seconds before realising that the decoys were not real female beetles (Domingue et al., 2013; Domingue et al., 2014).

This nano-bioreplication technique, which has the advantage of being industrially scaleable (Pulsifer et al., 2013), was used to create effective decoys, which were then mounted on a green plastic surface at a 45°C angle above a trap opening; two steel pins (connected to a transformer) located at the centre of and just below the decoy were used to create a 4,000 volt electrical potential via two batteries, thus forming an electrocution trap (Domingue et al., 2014). Laboratory testing of the traps demonstrated that beetles were either killed, or stunned for up to 15 minutes, after coming into contact with the decoy. Traps were tested in the field in Pennsylvania. The inside of the trap cup contained a Kill strip (Vaportape II, Hercon Environmental) to prevent stunned beetles from exiting the trap when they regained consciousness. These preliminary field trials, whilst only catching relatively small numbers of emerald ash borer (14 beetles over an 11 day period by seven traps), demonstrated that the alighting beetles were predominantly male (13:3 male: female ratio), and trap catches increased in accordance with the flight season (Domingue et al., 2014). Traps were also tested out in Hungary where a number of Agrilus species were caught, as well as other non-target insects (the Hungarian traps were running continuously and therefore liable to trap dusk and night time flying insects whereas the traps used in Pennsylvania were only activated for a 12 hour period each day between 08:00 and 20:00) (Domingue et al., 2014). The Hungarian field trial demonstrated

Control and management strategies for emerald ash borer ∣ March 2017 Page 53 that the batteries needed to be replaced daily because the morning dew resulted in a continuous charge.

Whilst in its infancy, and requiring refinement, this work shows the potential for the development of new detection and trapping techniques. Domingue et al. (2014) suggest that the electrical events from a trap can be reported back to a manned base using wireless communication, for instance, thus alerting personnel to a detection.

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Chapter 7: Quarantine treatment of wood packaging material and logs

The International Standard for Phytosanitary Measures (ISPM-15, 2013), currently recommends one of two treatments for wood packaging material:

1. Heat treatment that ensures a minimum core temperature of 56 °C for 30 minutes.

2. Fumigation with methyl bromide.

However, a study by McCullough et al. (2007) suggests that a proportion of emerald ash borer prepupae might be able to survive the recommended heat treatment. Their study focussed on the processing of ash that was harvested in the winter, when most emerald ash borer would be at the prepupal stage, as the authors deemed that this would be the stage most likely to be able to survive any processing treatments; they would likely be less susceptible than other stages to desiccation of the wood and deterioration of the phloem (McCullough et al., 2007). If the prepupae were not physically injured or killed during the treatment process then it is likely that they would be able to successfully pupate and emerge as adults (McCullough et al., 2007). These authors tested a range of heat treatment temperatures, over a 20 minute or 2 hour time period, and their results demonstrated that no prepupae were able to survive a 60 °C heat treatment of 2 hours or longer. However, 50% of prepupae in wood chips were able to survive a 1 hour treatment of 60°C, and 50% of prepupae were capable of surviving a 20 minute treatment of 55 °C, with 17% of prepupae able to survive a 2 hour exposure to 55 °C, leading the authors to suggest that a proportion of emerald ash borer prepupae might be able to survive internationally recognised phytosanitary measures (McCullough et al., 2007).

The use of sulfuryl fluoride (SF) fumigation has been evaluated as an alternative to methyl bromide fumigation for treatment of emerald ash borer in ash logs (Barak et al., 2010). One hundred percent control of eggs (on filter paper within fumigant chambers) or larvae within logs was achieved, and was effective under commercial fumigation conditions using the following parameters (Barak et al., 2010):

15.6 °C by CxT dosage of 3,723 g-h/m3 of SF for 24 hours

15.6 °C by CxT dosage of 6,072 g-h/m3 of SF for 48 hours

21.1 °C by CxT dosage of 3,172 g-h/m3 of SF for 24 hours

21.1 °C by CxT dosage of 4,210 g-h/m3 of SF for 48 hours

Consequently these authors suggest that these treatment schedules could be proposed for a quarantine treatment of ash logs.

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Chapter 8: Slow Ash Mortality (SLAM) Management Programme

In 2008, a multi-agency pilot project known as Slow Ash Mortality (SLAM) was initiated in North America to develop, implement, and evaluate integrated strategies for managing recently established, localised outlier sites of emerald ash borer (Poland and McCullough, 2010; McCullough and Mercader, 2012). The project was tested cooperatively by scientists and partners from the Michigan State University, the USDA Forest Service, Michigan Technological University (MTU), the Michigan Department of Agriculture (MDA), Natural Resources and Environment (MDNRE) and the USDA Animal and Plant Health Inspection Service (APHIS) (Poland and McCullough, 2010). SLAM does not aim to eradicate emerald ash borer populations (Poland and McCullough, 2010). Instead, SLAM focuses on the ash trees themselves (i.e. the resource) within outbreak sites, and the aim of the project is to slow the onset and progression of ash mortality (Poland and McCullough, 2010; McCullough and Mercader, 2012). SLAM complements quarantine regulations which rather than focusing on local progression of mortality, are put in place to minimise long-range human-assisted movement of emerald ash borer (Poland and McCullough, 2010; McCullough and Mercader, 2012). Slowing the rate of ash mortality gives resource managers, council and private property owners the time to develop long-term plans to treat or replace vulnerable ash trees and hence results in proactive rather than reactive management (Poland and McCullough, 2010). The consensus is that SLAM is most likely to be successful when applied to relatively recent infestation sites, where ash mortality is minimal or concentrated to a small area, and at outlier sites that are geographically distinct from both the main invasion front and well established populations of emerald ash borer (Poland and McCullough, 2010). The five management tools incorporated into the SLAM programme are (Poland and McCullough, 2010):

1. Surveys to determine emerald ash borer distribution and density

2. Devising inventories to establish ash abundance and distribution

3. Suppression of emerald ash borer populations (by various methods)

4. Standard required regulatory measures

5. Public outreach campaigns.

The project was put into action immediately after infestations were found in 2007 at two sites near Moran and St Ignace in the Upper Peninsula area of Michigan. These are heterogenous landscapes that included small cities, rural areas, forests and swamps (McCullough and Mercader, 2012). The infestations were identified when a girdled ash tree used in a detection survey was found to be infested (Poland and McCullough, 2010; McCullough and Mercader, 2012). Initially, a quick visual survey was conducted in the autumn of 2007 in tandem with the destructive sampling of suspect trees. The survey revealed that both outbreaks were small and relatively recent: 13 infested trees were found at the Moran site, and one infested tree at St Ignace with a second found close by at Straits State Park (Poland and McCullough, 2010). The epicentres of the Moran and St Ignace infestations were thought to be approximately 25 km apart when they were discovered (Mercader et al., 2016). More extensive surveys were conducted in 2008 and 2009 using a combination of

Control and management strategies for emerald ash borer ∣ March 2017 Page 56 girdled ash trees that were debarked in the autumn and artificial traps, and are an important component of SLAM as, in particular, the girdled detection trees help to accurately determine the density and spatial distribution of all emerald ash borer life stages in the outbreak area (Poland and McCullough, 2010). This in turn helps to plan suppression activities by enabling informed decisions as to which trees should be used for trap trees and which should be used in the control programme (e.g. treated with insecticide, used as a sink tree or removed) (Poland and McCullough, 2010). Trees that were 10-15 cm dbh, and growing in open areas or along roadways, canopy gaps or the edge of woodlands were preferentially selected for girdling (Mercader et al., 2013). In order to create the girdle, a 15 -30 cm wide band of bark and phloem was removed around the circumference of the tree at a height of 1.1 - 1.3 m above ground level (Mercader et al., 2013). The artificial traps used consisted of purple prism traps, coated with Pestick, and baited with either Manuka oil or an 80:20 combination of Manuka oil: Phoebe oil, and were hung in the canopy of ash trees, at least 1.5 m above ground on the sunny side of the tree following the USDA-APHIS guidelines (Poland and McCullough, 2010; Mercader et al., 2013). For surveying purposes, the area surrounding the infestations was divided into three bands. The core area, within a 1.5 mile radius form the outermost known infested tree was divided into 40 acre grid cells (16 grid cells/square mile); the second band covered a 1.5 mile radius out from the core area (i.e. 1.5 -3 mile radius from the outermost known infested tree) and was divided into 160 acre grid cells (4 grid cells/square mile); the third band covered the 3 - 6 mile radius from the outermost known infested tree (1 grid cell = 1 square mile) (Poland and McCullough, 2010). Grid cells within the core area contained both a trap tree (when available) and an artificial trap, and grid cells in the remaining two bands contained one trap tree (when a suitable trap tree was unavailable an artificial trap was used instead) (Poland and McCullough, 2010). These surveys indicated that the emerald ash borer populations were building and starting to spread, with four outlier infestations found more than 800 m away from the core area at the Moran site (Poland and McCullough, 2010).

Four suppression treatments were implemented in 2009 and surveying continued as part of their follow up. The treatments used in the SLAM pilot project were removal of all infested trees (i.e. all trees known to be infested, trap trees and sink trees) in the autumn before developing larvae had chance to emerge as adults, insecticide application, sink trees, and harvesting of ash to remove available phloem (Poland and McCullough, 2010). Poland and McCullough (2010) and Mercader et al. (2011a) stress however, that the tactics used should be chosen on the basis of the factors (such as emerald ash borer population density and distribution, distribution and abundance of ash trees, accessibility of trees etc.) at each individual site. Insecticide treatment involved the application of the systemic insecticide TREE-age® (applied at a rate of 0.2g a.i./2.5 cm dbh, as a basal trunk injection in spring Mercader et al., 2015). In theory personnel had wanted to create a buffer zone, 400-800m around the outermost known infested tree in the core area, but in practice tree availability, accessibility and land ownership dictated which trees were treated. In total, 229 trees were treated in 2009 and 358 were treated in 2010 (Mercader et al., 2015). Clusters of sink trees were established by girdling 3-4 trees per cluster, situated within the core areas rather than on the boundaries, in order to establish powerful sources of attraction to contain the spread and limit dispersal out of the core area (Mercader et al., 2011a). In total, 2650 ash trees were girdled from 2008-2011 for either detection purposes or for use as sinks to supress population levels (Mercader et al., 2016). Tree harvesting, as a means of reducing but not eliminating ash phloem abundance was put into practice at the Moran site: 445 large ash tree (≥ 30 cm dbh) were harvested along with 100

Control and management strategies for emerald ash borer ∣ March 2017 Page 57 smaller trees. Reduction, not elimination, is the aim of harvesting in order to reduce the emerald ash borer population size. As emerald ash borer can develop in trees with a diameter as little as 2.5 cm and have the capacity to disperse, complete elimination of phloem abundance would not only require substantial effort, but may actually encourage the adult beetles to disperse further (Mercader et al., 2011a) and could result in inadvertent human-assisted dispersal caused by the movement of infested material for disposal (McCullough and Mercader, 2012). However, there are occasions when some felling may be necessary or useful, for example, to remove trees that are hazardous or have very low vigour in urban areas (McCullough and Mercader, 2012). These unwanted landscape ash in urban areas, which are designated for removal and replacement can serve as trap trees, by girdling in the spring and then removing in the autumn or winter, getting some value from the tree before removal (McCullough et al., 2015). In addition, some harvesting of saleable timber does provide forest owners with economic value from the trees, and may have a place in emerald ash borer management (McCullough et al., 2015). For example, in second growth forests the merchantable trees (e.g. > 25 cm dbh) may only represent a small portion of ash stems within a forest yet can collectively produce a vast number of emerald ash borer if left in place due to the phloem area that they represent (McCullough et al., 2005).

A model to simulate the spread of emerald ash borer has been developed (Mercader et al., 2011b) as part of the SLAM project and has been used to model the build-up of emerald ash borer populations and spread, and to evaluate the success of the measures implemented at the SLAM pilot sites (Poland and McCullough, 2010).

Larval count data from the girdled detection trees, and numbers of adults caught on the traps during the systemic grid surveys of the SLAM project were compared to assess the detection rates of these two detection methods. The results showed that across three years of surveying, the girdled detection trees were consistently more likely to detect emerald ash borer than the traps, even when the traps were hung in the canopy of a girdled tree (Mercader et al., 2013). A single detection tree had a > 50% probability of making a detection when larvae densities in the area were low (< 5 larvae per detection tree) and probability of detection increased to > 95% in areas of higher larval density (15 larvae per detection tree). In contrast, the probability of detection by an artificial trap was < 35% even when the local larval density was > 25 larvae per detection tree (Mercader et al., 2013). Similar results have been reported for other studies. For example McCullough et al. (2011b) demonstrated that all girdled trap trees in their low density study area were infested with emerald ash borer while 81% of the purple double decker traps captured one or more beetles; the green double decker traps and purple canopy traps were less effective with 56% and 25% respectively, catching one or more adult beetles. Variability in detection rates at low population densities remains high whether using girdled detection trees or artificial traps (Mercader et al., 2013). Increasing the numbers of traps used in the simulation model to five in the low density areas (< 5 larvae per detection tree) did not improve detection rates (40%) however, increasing the number of detection trees to three resulted in an increase in the probability of a single tree making a detection to 90%, and nearly 100% if five detection trees were used (Mercader et al., 2013). The probability of detection for traps did improve (62%) in areas of higher larvae density (15 larvae per detection tree) if five traps were used compared with 20% detection rate when one trap was used (Mercader et al., 2013). The authors thought that the artificial traps probably underestimated local population densities in this survey whilst the detection trees probably overestimated the local population density as probability is

Control and management strategies for emerald ash borer ∣ March 2017 Page 58 calculated on the basis of the number of larvae found in detection trees, which actively attract beetles to that particular tree.

In addition, the numbers of larvae retrieved from the girdled detection trees used at the two SLAM sites were entered into the simulation model, which then calculated that between 2008-2011, the rate of spread of the emerald ash borer population at the Moran site was 1.2 - 1.7 km/year whilst at the St Ignace site, which had a lower infestation level, rate of spread was calculated to be 0.4 - 0.7 km/year (Mercader et al., 2016). Results indicated that stratified dispersal was occurring, as spread was not evenly distributed across the areas and the rate of spread increased as population levels increased. By 2011 the populations at the two sites had begun to merge (Mercader et al., 2016). The higher rate of spread at the Moran site was thought to be due to a higher density of emerald ash borer in the epicentre, and the establishment of a number of satellite colonies ahead of the main invasion front (Mercader et al., 2016). Whilst human-assisted dispersal could not be ruled out for the formation of these outlier sites, it was thought unlikely because quarantine regulations were in place, public outreach and education was undertaken in earnest, and the satellite colonies were not found where expected if as a result of human-assisted dispersal (e.g. campsites, sawmills); hence it is likely that these satellite colonies were established as a result of female beetles undertaking long- range dispersal flights (Mercader et al., 2016). This hypothesis is backed up by the larval count data in the girdled detection trees, which indicated that every year a proportion of the females (perhaps up to 20%) were laying eggs on trees more than 2000 m from the infestation epicentres (Mercader et al., 2016).

Data obtained from the SLAM pilot project was used directly in the simulation model to evaluate the effectiveness of the treatments used, in particular the use of the insecticide Tree-äge®, or girdling ash trees, to suppress the density of emerald ash borer populations (Mercader et al., 2015) and the rate of spread (Mercader et al., 2016). The simulations revealed that both the insecticide treatment and girdling of ash trees had successfully, and significantly, reduced the local emerald ash borer populations in the two SLAM project areas (Mercader et al., 2015). With regard to the insecticide treatment, the number of trees treated was the more important component for controlling emerald ash borer density rather than the total phloem area treated with insecticide; as Mercader et al. (2015) point out, this would be expected as a gravid female is more likely to come into contact with the insecticide if a greater number of trees are treated. However, this was only the case at the Moran site, the converse was actually true at the St Ignace site, but it was thought that this was due to the St Ignace population being a distinct infestation over a very small area and most of the treated trees were concentrated in a few areas allowing strong control. The predicted outcome of this evaluation is very promising as it clearly indicated that the use of Tree-äge® treatment in the SLAM project sites resulted in detectable reductions in emerald ash borer, and slowed the progression of ash tree decline and mortality, despite the fact that < 1% of the total number of trees in the area (and < 1% of the total ash phloem available in the area) were treated with the insecticide (Mercader et al., 2015). The model also indicted that treating trees with the insecticide provided some protection to the neighbouring untreated trees (Mercader et al., 2015). During model simulation, the insecticide-treated trees appeared to have no effect on the rate of spread of the emerald ash borer population however, this is thought only to be the case because of the unforseen severe restrictions that were in place at the project sites with regard to insecticide treatment, leading to limited numbers and sub optimal distribution patterns of treated trees (Mercader et al., 2016).

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The use of the girdled detection and sink trees also resulted in a significant reduction in the emerald ash borer population in the SLAM project area (Mercader et al., 2015) and in the rate of spread of the population (Mercader et al., 2016). However, subtle nuances were detected in the model predictions, indicating that the outcomes following the use of girdled ash trees are complex (Mercader et al., 2015). For instance, when low levels of ash phloem were available, girdled trees would reduce the emerald ash borer density if they were placed in areas where the population density was low in the previous year but not when placed in areas where the population density was high in the previous year (Mercader et al., 2015). However, when levels of available ash phloem were high, girdled ash trees reduced the population density when placed in areas of high population density the previous year (Mercader et al., 2015). Whilst the girdled ash trees will take the larvae developing within them out of the emerald ash borer population, they can in some instances attract emerald ash borer females to oviposit on their neighbouring trees, creating a spillover effect and increasing larval densities within those trees (Mercader et al., 2015). However, this spillover effect can have its uses for instance girdled trees could be used to attract an emerald ash borer population away from high value trees, which could be treated with insecticide as an added precaution (Mercader et al., 2015). Alternatively, the spillover effect can be mitigated by using girdled trees in combination with an insecticide i.e. treat the trees surrounding the girdled trees so that beetles are lured to the area and then killed; these authors suggest that this strategy could reduce the overall number of trees requiring insecticide treatment within a management programme and therefore reduce costs but should be investigated further (Mercader et al., 2015).

From the SLAM pilot project data evaluations, these authors conclude that the model is a good tool to simulate potential treatment and management options but cannot be used to realistically forecast the formation of satellite populations or to make precise predictions about spread (Mercader et al., 2016).

The simulation model developed by Mercader et al. (2011b) has also been used to perform detailed modelling of the SLAM strategy in urban areas using field data from infestation areas within North America (McCullough and Mercader, 2012), and again demonstrated that treating ash with emamectin benzoate is the most effective option for slowing emerald ash borer population growth, spread and ash tree mortality (Mercader et al., 2011a; McCullough and Mercader, 2012). It is also an achievable and efficient method to deploy in urban areas because there are often up to date inventories of trees within public areas and the trees are generally accessible to those applying the treatment (McCullough and Mercader, 2012).

The simulation was used to help determine outcomes and costs of such a strategy. Their simulation ran over a ten year period covering a neighbourhood made up of 320 identical blocks arranged in a 20 x 16 grid, encompassing a total of 2314 ash trees. The model assumed that 400 adults emerged from a pile of ash firewood in the centre of the location and explored the following scenarios (McCullough and Mercader, 2012):

1. Baseline – no trees were treated with insecticide or removed.

2. Trees were removed – no trees were treated with insecticide, instead trees were removed once 60% of the phloem within the tree was consumed by emerald ash borer larvae, at which point canopy thinning and dieback would be visible.

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3. Trees were treated with insecticide (TREE-age®) a. Random treatment. Treatment of 10, 20, 30, 40 or 50% of all ash trees on a yearly basis. Trees were selected at random, from the trees that had not been treated for two or more years. Treatment was either initiated during the spring following the initial infestation (one year post-introduction) or four years after the initial introduction (representing what often happens because infestations are generally not detected for three to four years).

b. Targeted treatment. In these simulations, 10% of all ash trees were treated, on a yearly basis, but either targeted the trees growing in the block where the infestation originated, trees growing within a one block radius of the origin or trees growing within a two block radius of the origin. As in all cases less than 10% of the total number of ash trees occurred in the targeted areas, implementation of this strategy means that all ash trees in the targeted area are treated and then additional trees were randomly selected from the remainder of the surrounding environment in order to achieve 10%. The insecticide treatment remains effective for a two year period so in the years when a tree within the targeted area did not require treatment, 10% of trees (chosen from trees that had not been treated for two or more years) beyond the targeted area were treated. Targeted simulations were evaluated for treatment applications beginning one year or four years after infestation.

McCullough and Mercader (2012) acquired estimated costs for treatment, tree removal and replacement for six cities within the mideastern United States during 2010. Costs for removal and disposal included labour, equipment, fuel and administrative support (averaged $888 per tree); costs for replacement included procuring, planting and mulching of trees ≤ 6 cm diameter (similar cost to removal), and the cost of insecticide treatment included the cost of the insecticide applied at relatively low label rates, application equipment, labour, fuel and administrative support ($3.62/2.5 cm dbh). Annual and cumulative costs were calculated for treating 0, 10, 20, 30, 40 or 50% of ash trees when treatment started one or four years after infestation (McCullough and Mercader, 2012).

Removing ash trees as they declined and reached 60% phloem loss (scenario 2) only slightly reduced the overall number of trees that were lost in any given year when compared with the no treatment baseline (scenario 1). The first appearance of severely declining ash trees that required removal occurred in year three, and as the simulation progressed the rate at which ash trees were lost increased, such that by year seven, 58% had been removed and by year ten, 97% of the trees had gone (McCullough and Mercader, 2012); 100% of ash trees had died when no treatment whatsoever was used. The difference between these two scenarios is minimal because infested trees have a reduced ability to produce beetles as their phloem is consumed (McCullough and Mercader, 2012).

Randomly treating 20-50% of ash trees with the emamectin benzoate insecticide (scenario 3a), one year after infestation, resulted in ≥ 99.5% of ash trees still being present and alive after ten years compared with 75% when only 10% of the tree population was treated (McCullough and Mercader, 2012). Targeted insecticide treatments yielded different outcomes depending on whether treatment was initiated one year or four years after infestation. When treatment was started after one year, and 10% of ash trees were treated, randomly selecting the trees for treatment was least effective whereas targeting the treatment to within one or two blocks of the original infestation, rather than the trees within the block where the infestation originated, proved significantly more effective, with

Control and management strategies for emerald ash borer ∣ March 2017 Page 61 very little tree loss over the ten year period (McCullough and Mercader, 2012). However, results indicated that the effects of a ten year targeted strategy would start to decline, and this became apparent in years nine and ten when treatment was targeted to within a one block radius (McCullough and Mercader, 2012). This decline in effect would likely occur because whilst a relatively high proportion of emerald ash borer would be killed by the insecticide, each year a few would disperse out of the targeted area and into the areas not receiving any treatment (McCullough and Mercader, 2012). Interestingly, when treatment did not start until four years post-infestation the ten year outcome was very similar whether 10% of the trees were treated randomly (52% of trees still alive) or targeted at trees within the block where the infestation occurred (51% tree survival) because in actual fact only 0.3% of the total number of ash trees in the study site occurred within the infestation block, and therefore the remaining 9.7% of treated trees in this particular targeted approach were actually randomly selected from the wider environment (McCullough and Mercader, 2012). However, targeting treatment to within one or two blocks of the infestation resulted in 46% and 36% tree survival after ten years, because during the first four years, while no treatment was administered a proportion of individuals had dispersed and these new populations were already starting to build in areas that then did not receive much insecticide treatment (McCullough and Mercader, 2012).

Further scenarios applied to the McCullough and Mercader (2012) simulations suggested that access to all ash trees in the study environment was important. For example, when privately owned trees were excluded from insecticide treatment, 70% of ash trees remained alive after ten years when 10% of randomly selected trees were treated from one year post-infestation compared with 75% when random selection was able to be applied to the whole pool of trees within the treatment area (McCullough and Mercader, 2012).

The simulated costs of the various treatment options in the McCullough and Mercader (2012) study demonstrated that the cost of simply removing and replacing declining ash trees was substantially higher than the costs incurred by treating with emamectin benzoate (Table 4).

Table 4. Total cumulative costs of randomly treating a percentage of ash trees with emamectin benzoate insecticide every year, including the removal and replacing of declining ash trees when they reach a level of 60% phloem loss, as evaluated by McCullough and Mercader (2012). The actual costs associated with treating 10% of ash trees are not provided within the text of this publication, however, the authors state that the cumulative costs for treating 10% of the trees was more than double the cumulative costs associated with treating 20% of the trees.

Percentage of trees randomly Total cumulative cost over the ten year period treated with insecticide 0% (removal and replacement $1.9 million only) Treatment initiated one year Treatment initiated four years after infestation after infestation 20% $265,271 $364,554 30% $397,206 $304,524 40% $529,778 $381,369 50% $661,160 $468,168

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Simulations performed by Mercader et al. (2011a) comparing the effectiveness of ash tree removal, insecticide treatment and girdling of ash trees yielded similar results to those described above. The model predicted that after 15 years, treatment with an effective insecticide within a 300 m radius of the origin of infestation would reduce the population spread by 30%, and larval consumption of ash phloem beyond the treated area by 40% when compared with no treatment (Mercader et al., 2011a). The use of girdled ash trees also significantly decreased spread and larval consumption of ash phloem outside of the treated area (by 15% and 20%, respectively) but became less effective as larval densities increased (Mercader et al., 2011a). Both of these options were predicted to be effective when applied both one and four years after the initial infestation (Mercader et al., 2011a). In contrast, whilst removing ash trees to reduce ash phloem abundance lowered the emerald ash borer population within the treated area it did nothing to stop radial spread, population size or larval consumption of ash phloem beyond the treated area (Mercader et al., 2011a).

In summary, the McCullough and Mercader (2012) simulations indicate that in all scenarios slower onset and progression of ash tree mortality was achieved when insecticide treatment began one year, rather than four years after infestatation. This further demonstrates the need for effective detection tools in order that treatment can be applied as soon as possible. However, being able to establish when an infestation occurred is also important because the effectiveness of targeted insecticide treatment will differ depending on the interval between initial infestation and first application of treatment; targeted methods should therefore be decided upon accordingly. In some instances, such as when there is a four year delay between infestation and first treatment, treating randomly selected trees may be more effective than targeting trees within a specific radius of the initial infestation. Even when targeted treatments are applied one year after infestation in an area where the origin of the infestation can be located, the benefits of such a targeted approach started to decline over time, with random treatment ultimately protecting more trees. In fact, the authors actually suggest that using a targeted treatment approach is risky due to the difficulties in detecting low density emerald ash borer infestations, and the low likelihood of being able to ascertain the exact centre of the infestation (McCullough and Mercader, 2012). It is also important to have access to all trees within the area under a treatment strategy in order that all can be included in any treatment scenarios. The simulations showed that when treatment does not start until four years after the initial infestation, treating 20% of trees with emamectin benzoate was both economically efficient, and protected a high proportion of trees (McCullough and Mercader, 2012). Treatment will of course have to continue past ten years, however, 20% of ash can be treated for many years before the cost of this strategy would equal the cost of a no insecticide treatment strategy. The results observed in this study are consistent with the outcomes of other modelling exercises; economic analyses consistently indicate that treating ash trees, on alternate years with emamectin benzoate, is more beneficial than the pre-emptive tree removal or removing trees as they die (Kovacs et al., 2010; Mercader et al., 2011a; Vannatta et al., 2012); Poland et al., 2016). Managers need to take account of the fact that the most cost-effective strategy may not necessarily be the most effective solution for addressing emerald ash borer infestations, and the decisions should be made based on the needs/desires of individual affected communities (Vannatta et al., 2012).

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Summary

1. Girdled ash trees are consistently more likely to detect emerald ash borer than artificial traps during surveys, and provide valuable data on the density and spatial distribution of emerald ash borer in the outbreak area (Poland and McCullough, 2010).

2. Harvesting of ash trees can have its uses (e.g. allowing large trees to be harvested for timber for some economic gain). However, whilst it may reduce the population density of emerald ash borer within the treatment area, it does not slow the spread of the population or reduce population build- up in surrounding untreated areas. Indeed there are concerns that it could actually encourage the dispersal of gravid adult females (Mercader et al., 2011a; McCullough and Mercader, 2012).

3. To date, all predictive model simulations and evaluations of actual data indicate that the use of a highly effective insecticide, and girdled ash trees to act as a population sink, in management programmes are the options most likely to both reduce emerald ash borer population densities and slow the rate of spread (Mercader et al., 2011a, 2015, 2016; McCullough and Mercader, 2012).

4. The use of girdled trap trees does have some potential risk to a management strategy due to the complex set of outcomes predicted in simulations and evaluations. Therefore, whilst the use of girdled ash trees has been shown to effectively reduce emerald ash borer populations and rate of spread, resource and project managers should clearly understand the complex interactions and ensure that their use within a management programme is well thought out to take account of these interactions (Mercader et al., 2015).

5. Treatment with emamectin benzoate is not only highly effective for slowing population growth, spread and ash tree mortality, but is also the only option that keeps ash trees in the environment (Mercader et al., 2011a; McCullough and Mercader, 2012).

6. The earlier that emamectin benzoate treatment starts, the slower the onset and progression to ash tree mortality.

7. Each year up to 20% of females dispersed and laid eggs more than 2 km away from the epicentres of the SLAM pilot study sites (Mercader et al., 2016).

8. Decision makers should choose carefully between random selection and targeted selection of ash trees for emamectin benzoate treatment. Targeted selection is risky. In some instances (e.g. when there is a four year delay between infestation and initiation of treatment), better outcomes may be achieved when trees are randomly selected for treatment. Even when targeted treatment starts one year after infestation, a better outcome may ultimately be achieved with random selection (Mercader and McCullough, 2012).

9. When there is a four year delay between infestation and start of treatment (as is commonly the case because infestations are often not found for three to four years), treating 20% of the trees with emamectin benzoate was both economically efficient and protected a high proportion of trees (Mercader and McCullough, 2012).

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10. It is important to have access to all ash trees within a treatment area so that the treatment can be fully implemented in the manner dictated by the strategy, without any exclusions, to obtain maximum benefits of the strategy (Mercader and McCullough, 2012).

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Chapter 9: Case study - Emerald ash borer in the U.S.A. and Canada

Emerald ash borer was first discovered in the U.S.A on 25th June 2002, near Detroit, Michigan (Haack et al., 2002; Cappaert et al., 2005; Emerald Ash Borer Information Network, 2017) however, dendrochronological analyses suggest that it was actually introduced in the 1990s with the first tree deaths due to emerald ash borer attack occurring in 1997 (Siegert et al., 2014). Following the discovery, provincial officials in Ontario, Canada were informed, and consequently identified trees infested with emerald ash borer in nearby Windsor, Ontario on 7th August 2002 (Haack et al., 2002; Cappaert et al., 2005). The pest was probably transported into the U.S.A. in some form of solid wood packaging material originating from its native range (Cappaert et al., 2005). Emerald ash borer is now present in 29 U.S. States (as of January 2017; Emerald Ash Borer Information Network, 2017) and a second state (Quebec) in Canada.

Management of emerald ash borer infestations

Following the discovery in Michigan, the Michigan Department of Agriculture imposed state quarantine to regulate the movement of ash logs, nursery trees and other related products from known infested counties (Cappaert et al., 2005). A new Pest Advisory Group was established by USDA APHIS, along with a National Science Advisory Panel (Cappaert et al., 2005). Aerial and ground surveys were conducted by natural resource and regulatory officials to assess damage, leading to the discovery at the end of 2002, that at least 5-7 million ash trees were already dead, dying or declining as a result of emerald ash borer infestation across six counties of southeastern Michigan; by late 2004, this figure had risen to 15 million ash trees (Cappaert et al., 2005). Trace back and trace forward exercises were conducted to track nursery trees shipped from the infested area (McCullough, 2015). The long time interval between introduction and implementation of quarantine measures is thought to have resulted in a considerable number of distinct outlier sites created by human-assisted dispersal (Mercader et al., 2016). A clear-cut strategy involving an ash-free zone measuring 5-10 km around the infested area (similar to the firebreak strategies applied to large wildfires) was considered in the U.S.A. on the basis that if the advancing front of the infestation could be contained, or slowed to below the rate at which the core infestation expanded, then the emerald ash borer population would crash (McCullough, 2015). In the end it was never pursued in the U.S.A. due to the difficulties in accurately delineating the infested area, the insuperable costs and logistical impracticalities of such a task. Canadian officials however, did attempt this strategy in Ontario in 2004 but soon abandoned the idea when infested trees were found beyond the zone (McCullough, 2015).

It seems incredible that the damage could have become so widespread before the culprit was detected. However, there are a number of reasons, explained by Cappaert et al. (2005) as to why this was the case:

1. On a general note, invasive pests can experience a lag phase following introduction, when their population levels remain low and below detection thresholds. This phase can persist for several years until suitable weather conditions, host resources, inter and intraspecific interactions lead to an exponential increase in the population density (Crooks and Soulé, 2001).

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2. Urbanised areas and suburbs were not typically included in routine surveys by forest health specialists.

3. Symptoms of attack, such as epicormic shoots, canopy dieback, and bark cracks over the larval galleries are not usually apparent until a tree becomes heavily infested enabling low to moderate infestations to go undetected.

4. Ash trees within forested and urban areas were already in decline. Reports suggested that the insects associated with these declining trees were native redheaded ash borer (N. acuminatus and native clear wing borers e.g. banded ash clearwing borer (Podosesia aureocincta Purrington & Neilsen), ash borer (Podosesia syringae (Harris)) and peachtree borer (Synanthedon exitiosa (Say)) (actually secondary infestations).

5. Symptoms of emerald ash borer attack can be mistaken with the symptoms of ash yellows disease, caused by a mycoplasma-like organism.

Emerald ash borer has been responsible for the death of tens of millions of ash trees (Kovacs et al., 2010) and could kill more than 99% of trees in infested forested areas within six years of infestation occurring (Knight et al., 2013). The economic loss (of trees from forests, city and suburban landscapes forests) and environmental costs associated with emerald ash borer are huge. Ash is an important timber and pulp species in the U.S.A. with an estimated value of $25 billion and in addition is a popular landscape and street tree, valued at $231 million (within Cappaert et al. 2005). Hundreds of millions of dollars of economic losses in the U.S.A. are predicted (Kovacs et al., 2010; Emerald Ash Borer information Network, 2017). Back in 2005, Cappaert et al. estimated the cost of removing urban ash trees in the U.S.A. to be in the region of $20-60 billion (a necessity due to the risks to people and property if dead trees are left standing; Flower et al., 2015) even before the cost of replacing the trees was factored in. Losses of approximately $830 million on residential property values have also been predicted (Aukema et al., 2011). In terms of environmental impacts, ash species provide thermal cover and protection for wildlife and a variety of wildlife feed on the seeds (Cappaert et al., 2005).

The first delimitation surveys were performed by means of visual assessment of trees using a systematic pattern moving outwards from the edges of known infested core areas. However, it soon became clear that visual surveys were not an effective method for finding recent or low density infestations, especially on large trees, due in part to the lack of symptoms but also because early attack occurs at the canopy level, and the adult exit holes can be difficult to see on large trees with thick, rough bark (Cappaert et al., 2005; McCullough, 2015). Evidence was also gathering to suggest that some gravid females would travel long distances to lay their eggs even if there was an abundance of ash trees close to where they emerged (McCullough, 2015). In 2004, the regulatory agencies implemented the use of girdled trap trees in detection surveys using them at high density in high risk areas such as sawmills, areas recently planted with nursery ash trees, camp sites, and along roads, highways and state borders (Cappaert et al., 2005; Rauscher, 2006; Hunt, 2007; McCullough, 2015). This has proved to be an effective method of detection even in areas with low density emerald ash borer populations (Cappaert et al., 2005). The use of girdled trees positioned along such pathways served another purpose, namely to raise awareness with the general public, and their use resulted in the identification of several previously unknown infestations (McCullough, 2015). Visual surveys of these girdled trap trees, in conjunction with sticky bands, were used to

Control and management strategies for emerald ash borer ∣ March 2017 Page 67 monitor for adults and visible symptoms of attack, whilst felling and de-barking the trees in autumn and winter was conducted to find the larvae. Felling and debarking is important: a 2004 survey in Michigan, deploying more than 10,000 trap trees found that more than half the trap trees had larvae but no external symptoms were observed on them and no adults were found on the sticky traps (Cappaert et al., 2005). However, there are some disadvantages associated with the use of girdled trap trees (see Chapter 2). Trap trees are not used in Canada (Marchant, 2007).

The development of an effective and sensitive monitoring system that is able to detect low-density emerald ash borer populations, when no visible symptoms of attack are apparent, is one of the primary goals of the USDA-APHIS Plant Protection and Quarantine Emerald Ash Borer Cooperative Project. Hence, one major aspect of research in North America has focused on the development of effective traps (see Chapter 2). As a result (from 2008 onwards), current detection methods in the U.S.A. employ a combination of visual surveys at high-risk sites such as campsites, in conjunction with outreach activities to increase public awareness, and the deployment of thousands of traps baited with host volatiles (Crook and Mastro, 2010; McCullough and Mercader, 2012; USDA APHIS, 2017). In the U.S.A., purple prism traps baited with Manuka oil and (3Z)-hexenol are deployed (Crook and Mastro, 2010; Poland and McCullough, 2014; Emerald Ash Borer information Network, 2017; Herms and McCullough, 2014) whereas green sticky traps baited with (3Z)-hexenol are currently deployed in Canadian surveys (Ryall, 2015).

Complete eradication of emerald ash borer was never attempted in the U.S.A. because of the number and distribution of ash trees and the scale of the infestation upon discovery (McCullough, 2015) but it was initially attempted in Canada (Marchant, 2007). However, several eradication projects at localised outlier sites in Michigan, Ohio, Indiana and Maryland (U.S.A.) were attempted between 2003 and 2006 (Herms and McCullough, 2014; McCullough, 2015). Areas measuring an 800m radius beyond the furthest ash tree known to be infested were established; this distance was chosen as compromise between logistical and financial constraints and the need to eliminate infested but asymptomatic trees (McCullough, 2015), and took into consideration information available at the time suggesting that whilst some female beetles would disperse further most would lay their eggs within 100 m of their emergence point (Mercader et al., 2009; Siegert et al., 2010; McCullough, 2015). Within this area every ash tree with a diameter greater than 2.5 cm was felled, sectioned, and taken to a transport yard where it could be chipped (McCullough, 2015). Even these localised eradication attempts had to be abandoned. Mainly because outlier infestations continued to be found outside of the quarantine areas, but also because of decreasing funds for eradication, surveys, other associated activities, and difficulties enforcing the quarantine measures and educating the public (McCullough, 2015), and as such these attempts were neither economical or effective (Marchant, 2007). Attempts continued in an area in Maryland where eradication continued until 2009, resulting in the removal of 42,000 ash trees over an area of 70 km2 between 2003 and 2009 (McCullough, 2015). It has not been established whether any of these eradication attempts were successful but they would certainly have removed a large proportion of infested trees and emerald ash borer larvae within these areas (McCullough, 2015).

Due to the failure of eradication attempts, management of emerald ash borer in the U.S.A. and Canada now focuses on slowing the spread of the pest. Some have suggested that it may be too late to prevent the spread of the pest (Johny et al., 2012). Once eradication efforts were abandoned in the U.S.A. it became the responsibility of landowners and residents to either protect their trees from

Control and management strategies for emerald ash borer ∣ March 2017 Page 68 emerald ash borer infestation or deal with infested trees (McCullough, 2015). In 2008, a multi- agency pilot project (SLAM) was initiated in North America to develop, implement, and evaluate integrated strategies for managing recently established, localised outlier sites of emerald ash borer in urban areas (Poland and McCullough, 2010; McCullough and Mercader, 2012) (see chapter 8). Results of the pilot studies have been very promising and this style of management method is used in the U.S.A. Quarantine maps help professionals and landowners stay up to date with the locations of known infestations (Herms et al., 2014) allowing them to plan their strategies ahead of infestation. In addition, cumulative growing degree days are tracked and posted on the websites of many land grant universities, and the National Oceanic and Atmospheric Administration (NOAA) website, enabling people to calculate application timings and adult beetle emergence (Herms et al., 2014).

The management strategy in Canada is based around effective regulations and quarantine (restricting the movement of live ash trees and all firewood), visual and branch sampling detection surveys in high-risk areas including campsites (traps will only indicate that emerald ash borer is in the area, not which trees are infested), parks and nurseries, and communication strategies to educate the public; quarantine is viewed as the most important tool (Marchant, 2007; Liu and Bauer, 2008b; Johny et al., 2012; OMAFRA, 2017). Marchant (2007) reports that The Canadian Food Inspection Agency (CFIA) consider the lack of effective surveillance and early detection tools to been the main obstacle in a control strategy and hence reports that large scale control actions would not be considered to be viable strategies until such reliable tools are available.

Suppression of emerald ash borer populations

As of 2010, several systemic insecticide products have been registered for the control of emerald ash borer in the U.S.A.; the active ingredients include imidacloprid, dinotefuran, emamectin benzoate or azadirachtin (Table 2). Currently, products containing the active ingredient emamectin benzoate are considered to be the most effective against emerald ash borer as they provide highly effective control for two and possibly three years post-application (Smitley et al., 2010b; McCullough et al., 2011; McCullough and Mercader, 2012; Herms et al., 2014; Flowers et al., 2015). As such it is used by private landowners and municipalities to protect individual trees or as part of the SLAM programme because treating a proportion of trees within an area can slow the rate of emerald ash borer population growth and dispersal and ash mortality (Mercader et al., 2011a; McCullough and Mercader, 2012; McCullough et al., 2015; Mercader et al., 2015; Poland et al., 2016). Registration of insecticides in Canada lagged behind the U.S.A, with the first product (an organophosphate) registered in 2012, and the first systemic insecticide (containing imidacloprid registered in 2014) (PMRA, 2017). To date, four systemic insecticide products are registered for use against emerald ash borer in Canada, containing either imidacloprid or azadirachtin as the active ingredients, and are available for use on landscape trees, nursery trees, greenhouses and forests (OMAFRA, 2017); as yet no products with emeactin benzoate as the active ingredient are available in Canada (PMRA, 2017).

From the point when emerald ash borer was detected in North America, scientists conducted surveys in Michigan, and in the native ranges of emerald ash borer, in the hope of finding natural enemies. A number of native parasitoid species were found to parasitize emerald ash borer (see chapter 4), along with predatory beetles (Enoclerus sp. (Cleridae), a Catogenus sp. and a Tenebroides

Control and management strategies for emerald ash borer ∣ March 2017 Page 69 sp. (Trogossitidae) (Bauer et al., 2004c), and evidence of diseased emerald ash borer, but mortality caused by natural enemies in Michigan was generally low. Observations from later surveys, conducted in more extensive areas, have shown that in some localities parasitism by the native parasitoid wasp A. cappaerti can be quite high (Cappaert and McCullough, 2008,2009) (see chapter 4).

The largest (natural) cause of emerald ash borer mortality in North America is predation by woodpeckers, in particular the downy woodpecker (Picoides pubescens), the hairy woodpecker (Picoides villosus) and the red-bellied woodpecker (Melanerpes carolinus). Predation rates from woodpeckers can be as high as approximately 90% on some infested trees but are not consistently so, indeed there is a very high degree of variability (Lindell et al., 2008; Poland and McCullough, 2010; Flower et al., 2014; Jennings et al., 2016). Tree cover and suitable nesting conditions in the area, season, availability of food all year round, and condition of infested trees are all thought to play a part in woodpecker predation (Lindell et al., 2008; Flower et al., 2014, Jennings et al., 2013, 2016). Woodpeckers feed preferentially on the J-larvae, prepupae, pupae and sometimes the fourth instar larvae (Jennings et al., 2013). However, whilst predation rates can be very high, and have a significant effect on larval mortality, overall they are not thought to impact on emerald ash borer populations (Lindell et al., 2008; Poland and McCullough, 2010; Jennings et al., 2013, 2016; Flower et al., 2014). They preferentially attack ash trees that are heavily infested with emerald ash borer over ash trees with lighter infestations (i.e. they attack in a density dependent manner), and therefore tend to predate on trees that are in poor condition rather than those in relatively good condition; it is this preference that is thought to limit their ability to protect ash trees as the preferentially predated trees will likely die anyway as a result of their poor condition (Lindell et al., 2008; Jennings et al., 2013; Flower et al., 2014). Researchers have suggested that forest managers should consider maintaining environments that are attractive to woodpeckers by for example, maintaining snags which act as nesting, perching and territorial announcement sites (Lindell et al., 2008; Flowers et al., 2014) and even by providing them with suet in the summer, while they are raising their young, and emerald ash borer larvae are in the early stages of their development (Poland and McCullough, 2010).

The lack of suitable natural enemies to influence emerald ash borer populations in Michigan prompted scientists to concentrate their efforts on evaluating the suitability of parasitoids found in the native ranges of emerald ash borer (see chapter 4) for introduction into the U.S.A. (classical biological control). Following research on the biology, laboratory rearing and host specificity of three species from China, federal and state regulatory agencies approved their release for controlling emerald ash borer in Michigan, U.S.A. in 2007 (Gould et al., 2015) . Biological control is thought to be the most suitable method of managing emerald ash borer in forested areas because treating large numbers of trees distributed over a large (often inaccessible area) is likely to be impractical. Initially, numbers of released parasitoids were low. In 2007, a total of 1,406 O. agrili, 1,360 T. planipennisi and 311 S. agrili females (plus some males) were released at sites with a high ash density and increasing emerald ash borer populations, and during the winter of the following year O. agrili and S. agrili were found at some release sites indicating that they had been able to overwinter and reproduce in the field (Bauer et al., 2008, 2011b). Releases were expanded into other States in 2008 (Ohio and Indiana) such that, including further releases in Michigan, a total of 2,100 O. agrili, 600 T. planipennisi and 300 S. agrili females (plus some males) were released, with an approximate 1% parasitism rate for O. agrili and 10% parasitism rate for T. planipennisi observed in

Control and management strategies for emerald ash borer ∣ March 2017 Page 70 the year following release (Bauer et al., 2011b). Tetrastichus planipennisi was also recovered 800 m away from a release site indicating that it had started to disperse (Bauer et al., 2011b). By 2009, large numbers of parasitoids could be reared and releases (8,000 S. agrili, 20,000 T. planipennisi and 5,200 O. agrili females plus some males) occurred in Michigan, Ohio, Indiana and two additional States (Maryland and Illinois) (Bauer et al., 2011b).

These early results were encouraging and prompted the initiation of the USDA emerald ash borer control program, which included the building of the APHIS emerald ash borer biocontrol facility to mass rear the parasitoids and distribute them throughout the U.S.A. In addition, detailed guidelines on the site selection, release and recovery of the parasitoids have been published (USDA- APHIS/ARS/FS, 2016) and an online database (http://www.mapbiocontrol.org/) was set up to map the release and recovery of the parasitods (reported in Gould et al., 2015). Releases have continued over the years in a growing number of States: 2010 (West Virginia, Kentucky, New York, Wisconsin), 2011 (Minnesota, Pennsylvania, Virginia), 2012 (Missouri, Tennessee), 2013 (Massachusetts, North Carolina, Connecticut), and 2014 (Colorado, Georgia, New Jersey, New Hampshire) (Gould et al., 2015), and release sites now include both urban and natural ash stands (Duan et al., 2012b). Currently, it is a requirement of the USDA APHIS Biological Control Production Facility that persons receiving parasitoids from them must agree to submit data onto the database, detailing the release and recovery of these parasitoids at their release sites, so that the impact of their use as a biological control agent can be assessed centrally (USDA-APHIS/ARS/FS, 2016). Due to problems with establishment (either failure to overwinter or consistently very low rates of parasitism), S. agrili has not been released in northern States (above 40°N latitude) since 2012 (Bauer et al., 2015a,b; Gould et al., 2015); it is however reported to be able to successfully overwinter in the Midwestern U.S.A. (Gould et al., 2015) but it is too early to tell whether populations have become established (USDA- APHIS/ARS/FS, 2016).

Tetrastichus planipennisi was also approved for use in Canada in 2013 (Gould et al., 2015). Researchers received approval to release a fourth non-native parasitoid, S. galinae, in the U.S.A. in 2015, and this has now been released and establishment is being monitored.

Tetrastichus planipennisi is now confirmed as established, dispersing and increasing in population levels at numerous sites in the U.S.A. (Bauer et al., 2015a,b). Duan et al. (2013a) report on the release and recovery of T. planipennisi at six mixed, hardwood forest study sites, dominated by green ash but with other tree species, including white ash, black ash and non ash species, in southern Michigan. Each study site consisted of a parasitoid-release plot and a non-release control plot 1-6 km apart. Male and female parasitoids were put together in rearing cages for at least three days before release to allow mating to occur (Duan et al., 2013a). In 2007 and 2008, parasitoids were only released at one and three sites, respectively, and only small numbers of female parasitoids were available (671 in one site at 2007 and 111-203 females per site in 2008). In 2009, surveys at these three sites failed to recover any parasitoids, so an additional 3,200 females were released at each of these sites and in addition, large quantity releases (3,828 – 3,897 females per site) were made for the first time in the three other sites (Duan et al., 2013a). Releases were staggered in time, every one to three weeks from May to September. Parasitoid establishment and abundance was monitored by sampling larvae from two to six trees every year from both the release and control plots at each study site (Duan et al., 2013a). In the first year following the large scale releases, the proportion of sampled trees with one or more broods of the parasitoid was 33% and 4% in the

Control and management strategies for emerald ash borer ∣ March 2017 Page 71 parasitoid-release plots and control plots, respectively. By 2012, these figures had risen to 92% and 83% respectively (Duan et al., 2013a). Rates of emerald ash borer larvae parasitism also increased from 1.2% in the first year following release to 21.2% in 2012 in the plots where the parasitoid was released, and from 0.8% to 12.8% in the control plots (Duan et al., 2013a). The results demonstrate that T. planipennisi had become established and was quickly dispersing out into non-release areas, indicating that it is likely to become an important agent in suppressing emerald ash borer populations in this area (Duan et al., 2013a). These authors suggest that T. planipennisi was able to disperse by at least 1 km/year and probably more. Gould et al. (2015) report that T. planipennisi has also been recovered following release in Illinois, Indiana, Ohio, New York, Maryland, Wisconsin and Minnesota.

Oobius agrili has been recovered following release at a number of sites (Abell et al., 2011; Bauer et al., 2011b,2015a,b; Duan et al. 2011b, 2012c), initially in low numbers. Duan et al. (2012c) report 0.4-5.9% (average 3.2%) O. agrili parasitism across three study sites in the release plots two years after the release of the parasitoid but no evidence of parasitism at the non-release plots, indicating that O. agrili had become established but had not yet dispersed to the non-release plots.

Evaluations over a six year period at six sites in Michigan have confirmed that O. agrili populations are increasing, and are slowly dispersing into non-release areas (Abell et al., 2014). During this study two methods of locating emerald ash borer eggs in order to measure rates of O. agrili parasitism were compared: 30 minute timed visual searches by two people, and bark collection and sifting (performed during the last two years of monitoring only). Results showed that the bark sifting method was the more effective method of finding the eggs and hence measuring levels of parasitism and determining the percentage of trees that had O. agrili-parasitized eggs upon them (Abell et al., 2014). In terms of the percentage of trees with parasitized eggs upon them, the highest estimates obtained in 2013 were 27.9% for the release plots and 11.1% for the control plots. In the early years (2008-2012), rates of parasitism in the release plots were calculated to be just 0.7 – 4.2%, while rates of parasitism were estimated to be as high as 21.8% (2012) and 18.9% (2013) (Abell et al., 2014). Minimal parasitism (0-0.4%) was observed in the non-release plots between 2008-2012 but by 2013 parasitism rates as high as 8.6% were estimated in these plots (Abell et al., 2014). It was also obvious from the results that O. agrili distribution was patchy because whilst the majority of ash trees sampled had emerald ash borer eggs on them, at most (across all sites) only 35% of trees had parasitized eggs on them (Abell et al., 2014).

Oobius agrili has now been confirmed as established in a number of states in the U.S.A. (Michigan, Ohio, Indiana, Pennsylvania, Maryland and New York) following introduction.

Despite the fact that some of these parasitoid species are establishing themselves with increasing populations and distributions following release, the current levels of parasitism observed in the U.S.A. are still much lower than those observed in China (Duan et al., 2015). There is currently no evidence that emerald ash borer population growth, or the rate of ash tree mortality have slowed following introduction of these species, or indeed occurred as a result of any indigenous natural enemies (McCullough et al., 2015). However, initial releases of the introduced parasitoids were on a small scale, and only a short period of time has lapsed since release. Thus it is hoped that, with larger numbers released in the next few years, the parasitoids will become significantly more

Control and management strategies for emerald ash borer ∣ March 2017 Page 72 abundant and deliver rates of parasitism similar to those observed in their native range (Duan et al., 2015).

Summary

1. It was realised early on that eradication of emerald ash borer within North America would be impossible; large populations of the pest had become established in a number of localities before it had even been detected, assisted by both natural and human-assisted dispersal.

2. Both the U.S.A. and Canada concentrate their efforts on slowing the spread of emerald ash borer and rate of ash tree mortality, allowing resource managers to spread the cost of infestation and plan ahead. However, it is acknowledged that even this will be a difficult task.

3. Different tactics are used for detection and suppression of emerald ash borer.

A) Girdled detection trees are used in the U.S.A. where they are considered to be the most effective means of detecting and delineating emerald ash borer populations whereas branch sampling is used in Canada. B) Systemic insecticide treatments available in the U.S.A. for the control of emerald ash borer include the active ingredients imidacloprid, dinotefuran, emamectin benzoate and azadirachtin; the emamectin benzoate product is considered to be the most effective. However, in Canada only products containing imidacloprid and azadirachtin are currently available for use, with the azadirachtin product in use in Ontario municipalities (Bowman and Smith, 2012).

4. Four parasitoid wasps have been approved for release in the U.S.A. (see chapter 4). Of these T. planipennisi and O. agrili have been confirmed as established in some release sites, increasing in numbers and dispersing into non-release sites. Tetrastichus planipennisi has also been approved for release in Canada. A third parasitoid (S. agrili) is no longer released north of the 40° N latitude because it was failing to establish, however it is still available for release south of this latitude and indications are that it is establishing at some of the release sites in the more southerly States. A fourth parasitoid (S. galinae) was approved for release in 2015; it is currently too early to tell if it has become established at release sites.

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Chapter 10: Emerald ash borer in Europe and European Russia

The natural occurrence of emerald ash borer in the Russian Far East, together with the discovery of populations in, and around Moscow, raises major concerns that emerald ash borer could spread westward and invade Europe, where ash species are commonly planted as urban trees and are an important species of forest ecosystems (Baranchikov et al., 2008; Orlova-Bienkowskaja, 2014). Emerald ash borer is not a regulated pest in Russia and therefore no official control measures have been implemented; some infested trees have been felled but this has mainly been for safety reasons (Poulsom, 2016).

Emerald ash borer is thought to have been introduced to the Moscow area in the early 1990s although symptoms were not noticed, or at least not reported until 2004, and formal identification of the cause (emerald ash borer) did not occur until 2007 (Baranchikov et al., 2008; Izhevskiy and Mozolevskaya, 2010) by which point the pest was well established (Poulsom, 2016). The source of the infestation in Moscow is unknown but possibilities include introduction through infested planting stock or via wood packing material from China (Izhevskiy and Mozolevskaya, 2010). The most abundant species of ash in Moscow itself is the North American green ash but the European ash (F. excelsior) is present in small numbers (Straw et al., 2013). Emerald ash borer is already responsible for the death of 80% of the ash trees in Moscow (EPPO, 2007; Orlova-Bienkowskaja, 2015), equating to more than a million green ash trees (Straw et al., 2013; Poulsom, 2016).

Initially (up to 2005), the rate of spread of emerald ash borer across Moscow was thought to be around 4 km/year (within Straw et al., 2013; Poulsom, 2016). However, recent surveys conducted in 2009 and 2013 indicate that the distribution of emerald ash borer is expanding and the rate of spread is increasing (Table 5; Baranchikov et al., 2010; Straw et al., 2013; Orlova-Bienkowskaja, 2014). By 2009, severely damaged and dead green ash were found 95km west and 90 km south of Moscow city (Baranchikov et al., 2010), with an estimated rate of spread of 10-12 km per year (reported in Straw et al., 2013). Rates of spread during 2009-2013 have increased to 30 km/year southward and 31 km/year westward (Straw et al., 2013). However, it is thought possible that the rate of spread westwards could be 41-42 km/year, due to the known locations of infested trees a year earlier than the Straw et al. (2013) survey, and the fact that these authors were not able to delineate the infestation in this direction during their own survey. These high rates of spread are not thought to be due to natural dispersal alone but also include human-assisted dispersal, most likely the result of the beetle hitch-hiking on vehicles along the highways, with establishment aided by the planting of green ash along the highways (Straw et al., 2013; Orlova-Bienkowskaja, 2014).

The survey conducted by Straw et al. (2013) followed the main road routes, which are planted with green ash, out of Moscow, inspecting the ash trees along the way for signs of emerald ash borer infestation. The authors found that in Moscow city itself, green ash trees that were < 10 cm dbh were generally in very good health with little sign of infestation; infested trees that were < 10 cm dbh were stressed as a result of poor sites, or were recently planted and struggling to establish. This was in stark contrast to the larger trees (10-65 cm dbh) of which 98% were infested to varying degrees. With regard to the European ash trees within Moscow, 50% were in a poor state as a result of infestation whilst the other 50% showed no signs of infestation (Straw et al., 2013). However, European ash trees were scarce in Moscow and actually, only 14 specimens were found (Straw et al., 2013).

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Table 5. Distribution of emerald ash borer outwards from Moscow city centre.

Direction Distance (km) from Distance (km) from Distance (km) from Moscow in 20091 Moscow in 20132 Moscow in 20133 North 20 Not surveyed 230 Northwest - 155 - West 95 215 250 South west - 2354 - South 90 1105 460 East 30 Not surveyed 350 1,2,3. Information from Baranchikov et al. (2010), Straw et al. (2013) and Orlova-Bienkowskaja (2014), respectively. 4.Accurate delineation in this direction was not possible. After 235km there were no roadside plantings of ash as the motorway passed through an extensive area of natural forest in which ash appeared to be scarce (Straw et al., 2013); 5. After 110 km, roadside planting of ash was scarce, and the landscape changed from open countryside to a mixture of large fields and sites of broadleaved woodland with European ash being a major co-dominant species. From this point outwards the condition of the European ash ranged from poor (50-80% declining or dead between 160-190 km from Moscow, and variable condition 190-220 km from Moscow) to mostly healthy but with a small number of trees in a poor condition (showing evidence of adult feeding but no other signs of infestation up to 240 km from Moscow). This observation indicates that emerald ash borer is now established and prevalent in broadleaved woodland with an abundance of European ash, and has the potential to spread very effectively throughout this area (Straw et al., 2013).

There is no doubt that European ash is highly susceptible to emerald ash borer (Orlova- Bienkowskaja, 2014; Valenta et al., 2015; Straw et al., 2013; Forestry Commission, 2017) although some have suggested that emerald ash borer prefers the North American green ash to European ash (Baranchikov et al., 2010; Izhevskiy and Mozolevskaya, 2010; Straw et al., 2013). Straw et al. (2013) concluded from their survey that European ash is obviously susceptible to emerald ash borer attack but that when green ash is present the beetle appears to have a preference for the North American species, attacking the European species in this scenario when it is stressed or already in poor condition. However, Orlova-Bienkowskaja (2015) are in disagreement and state that whilst earlier reports indicated that European ash was less susceptible to emerald ash borer, this was not true, with many cases of severe damage and infestation of F. excelsior known within European Russia.

With the current rates of spread westward in European Russia, it is estimated that emerald ash borer will reach the Belarus border by approximately 2020 (Straw et al., 2013), a date also suggested by Orlova-Bienkowskaja (2014). However, it may well arrive at this point earlier as it cannot be ruled out that isolated populations of emerald ash borer already exist well in advance of the main invasion front (Straw et al., 2013). In fact the pest could arrive into any other part(s) of Europe at any point in time via infested wood products (Valenta et al., 2015). European ash, which is able to grow under a wide range of environmental conditions, is a widespread species in temperate regions of the northern hemisphere, and other European species, such as Fraxinus angustifolia and Fraxinus ornus occur in the south and southeast of Europe (EPPO, 2005). The North American green ash is also widely planted in some areas of Europe (EPPO, 2005). Given the continuous distribution of ash across the continent, there is no doubt that emerald ash borer will become a major forest pest once

Control and management strategies for emerald ash borer ∣ March 2017 Page 75 it arrives in Europe, and will be able to establish in the full range of F. excelsior (Valenta et al., 2015). In addition, European ash of all sizes are currently under attack from the fungal pathogen Chalara fraxinea across Europe, resulting in weakened and ultimately dead trees, leading Straw et al. (2013) to conclude that once the distribution of C. fraxinea and emerald ash borer overlap in Europe very few ash trees are likely to survive the combined onslaught.

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Chapter 11: UK contingency plans

Currently (as of March 2017), emerald ash borer is officially absent from the U.K. and the European Union (EU). Emerald ash borer features on the European and Mediterranean Plant Protection Organization (EPPO) A2 list (https://www.eppo.int/QUARANTINE/listA2.htm) i.e. it is recommended that member countries treat it as a quarantine pest. There is a high likelihood that emerald ash borer would establish, and cause significant damage if it were to enter the EU, and as such import restrictions are in place on ash wood and live ash from all regions where emerald ash borer is known to be present (native and invaded areas) (Poulsom, 2016). The pest is rapidly spreading westwards from Moscow and there is concern that if it reaches the Baltic States the risk of accidental introduction into the EU will significantly increase (Poulsom, 2016). In addition, emerald ash borer also has a very high mitigated risk rating (75/125) in the UK risk register due to the threat that it poses (https://secure.fera.defra.gov.uk/phiw/riskRegister/viewPestRisks.cfm?cslref=25310). A résumé, previously drawn up out lining some important features of emerald ash borer control and management options also concludes that it is highly likely that emerald ash borer will arrive in the EU, and that in order to manage an outbreak a cohesive strategy, which must include rigid quarantine measures, extensive surveying and probably all of the control options used in North America, will need to be implemented (Bell, 2015). Bell (2015) advises that contingency plans should be prepared such that immediate action can be taken if emerald ash borer were to be detected in the UK. Indeed, Bowman and Smith (2012) go as far as to say that there are a multitude of risks if a strategy is not in place, including risks to public safety, degradation of the ecosystem, negative public reaction and economic pressure.

The Forestry Commission cross-border Plant Health Service has drawn up a contingency plan to enable a rapid and effective response to an outbreak of emerald ash borer should it happen in the U.K. (Poulsom, 2016)1. The plan, which should be used in conjunction with the Defra Plant Health Contingency Plan, is designed to help government agencies anticipate, assess, prepare, respond and recover from such an outbreak (Poulsom, 2016).

The objectives of the contingency plan are as follows (Poulsom, 2016):

1. Raise awareness of the potential threat posed by emerald ash borer, ensuring correct identification of the adult beetles and symptoms of infestation.

2. Provide guidance.

3. Ensure all relevant personnel are familiar with the contingency plan to allow the implementation of effective and prompt management of infestations, with a view to eradication or if the population is established upon discovery, to slow the rate of spread.

4. Ensure good communications are in place.

The contingency plan recommends that a response should be triggered (and an outbreak declared on positive identification) if a live insect is found in a consignment of wood, wood packaging material

1 NB. Since writing this review the contingency plan for emerald ash borer has been updated. The updated version (Mainprize, 2017) can be found at https://planthealthportal.defra.gov.uk/pests-and- diseases/contingency-planning/.

Control and management strategies for emerald ash borer ∣ March 2017 Page 77 or dunnage, or if a live insect is found in the wider environment, or if the characteristic D-shaped exit hole is found in an ash tree (Poulsom, 2016). The discovery of dead specimens should be dealt with by conducting a trace backward/trace forward exercise and potentially surveying trees in the relevant apprioprate areas in order to ascertain whether an outbreak should be declared (Poulsom, 2016). All movement of consignments and site operations should be stopped while an incident is under investigation, and in addition a trace forward/trace backward exercise should be performed to identify other sites potentially at risk or already contaminated (Poulsom, 2016).

Expert identification will be required to determine the presence of emerald ash borer as the symptoms of infestation, such as canopy thinning, crown dieback and mortality can be confused with ash disease such as ash (Chalara) dieback (Poulsom, 2016). Once an outbreak has been positively identified further detailed inspections and information gathering needs to happen (Poulsom, 2016), including:

1. Likely origin of the pest and destination details of other parts of the same consignment.

2. Movement of ash plants/ash wood products, people, equipment and vehicles into and out of the site.

3. Details about geographic location, abiotic factors and ownership of the site.

4. Details of the infested host trees and any treatments that they may have had that could affect detection and diagnosis of the pest, and development of symptoms of infestation.

5. Details of the symptoms, how and when the pest was identified.

6. Life stages present, level of infestation, extent of damage.

7. Accessibility of the site in order to gain access for tree removal.

8. Potential biodiversity impacts of any control measures to be implemented.

The contingency plan suggests that the statutory regulated area around an outbreak centre should be a radius of at least 20 km around the infested trees. Delimiting surveys should include an intensive survey within at least a 1 km radius of the first trees found to be infested and where adults appear to have flown to in the wider environment, and line transects should be performed outwards to at least 10 km to determine the limits of the infested area and to demarcate the regulated area (Poulsom, 2016). Surveys will need to be extended accordingly if new infested trees are discovered during the survey procedure, and should be repeated annually (Poulsom, 2016). Poulsom (2016) advises that these survey methods should be reviewed according to available up to date guidance, and that it could be beneficial to have potential contractors in place and trained in survey methods.

The Forestry Commission contingency plan recommends that all ash trees within the known infested area should be surveyed as soon as possible, and then annually during mid to late summer (when the canopy should be at its fullest), in order to assess their health. Poulsom (2016) suggests that a canopy thinning and dieback scale, such as the series of photographs depicting 0-100% canopy thinning and dieback used by Smitley et al. (2008), can be used to do this. Ash tree canopy condition can also be graded using the revised scale of Smith (2006), adapted from Ball and Simmons (1980). Photographs depicting the different classes of canopy condition can be found in Smith (2006) or in

Control and management strategies for emerald ash borer ∣ March 2017 Page 78 the USDA release and recovery guidelines for emerald ash borer (USDA-APHIS/ARS/FS, 2016) and a written description of the scale is provided by Flower et al. (2014):

1. Healthy/full canopy – no defoliation. 2. Thinning canopy – slight reduction in leaf mass, all top branches exposed to sunlight have leaves. 3. Dieback – thinning canopy, some defoliation on the top branches exposed to sunlight (exclude lower branches from assessment). 4. More than 50% dieback – over half of the top branches are defoliated and the canopy has < 50% of the expected number of leaves. 5. Dead canopy – no leaves remain in the canopy (exclude epicormic shoots from assessment).

The plan recommends removal of the worst affected ash trees (e.g. those with more than 50% canopy thinning) to slow the rate of spread, particularly during the flight period of the adult. All material produced during this process should be chipped within the infested area to <1.5 cm in three dimensions and/or burned (Poulsom, 2016). However, the creation of clear-cut areas is not thought to be appropriate, unless perhaps in the very early stages of an outbreak under very restrictive circumstances. Poulsom (2016) give a number of reasons for this recommendation, including the fact that emerald ash borer is a strong flyer with some individuals being capable of making flights of several kilometres (Bauer et al., 2004b; Taylor et al., 2004; Cappaert et al., 2005; Herms et al., 2014). In addition, in the U.S.A., 800 m ash-free zones have been used in some eradication attempts but did not prevent spread (McCullough, 2015). It has been suggested that removing trees to create an ash- free zone could encourage adults to fly afield because it removes the phloem resource from their immediate locality (Mercader et al., 2011a; Poulsom, 2016). A further point suggested by Poulsom (2016) is that creating an ash-free zone could remove resistant genotypes that may have the potential to survive an outbreak. In addition to these actions, the contingency plan suggests the use of traps to detect for the presence of adults outside of the known infestation areas, and for consideration to be given for the prophylactic use of chemical insecticides, and the possibility of biological control options.

Public outreach and education, in the form of dissemination of well-timed and accurate information, has played an important part in the strategy used in the North American invasion because of the amount of firewood movement that ordinarily goes on in the region. The Forestry Commission contingency plan also recommends that public support and engagement will not only provide general surveillance but will also be important for the success of the management programme (Poulsom, 2016).

Any management programmes put in place will need to be reviewed regularly (at least once a year). In the meantime Poulsom (2016) recommends that the Forestry Commission contingency plan should be reviewed annually, and updated if necessary according to any new information that could affect its recommendations (such as new legislative measures, new or updated scientific research, changes to geographic distribution of the pest, identification of new pathways of introduction and endangered areas and lessons learned from outbreaks in other areas). Any management programme for such an outbreak will need to be viewed as a long term plan if it is to be successful; Cappaert et

Control and management strategies for emerald ash borer ∣ March 2017 Page 79 al. (2005) report that the U.S. emerald ash borer scientific advisory panel estimated a sustained effort over 12-15 years would be required for a successful management programme.

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Conclusions

There is no doubt that emerald ash borer is an extremely damaging pest of ash (Fraxinus spp.) trees outside of its native range, and therefore poses a serious threat should it invade the UK.

Initial detection of the pest is very difficult, as the invasion experiences in the U.S.A., Canada and European Russia testify, where in all cases the beetle was thought to be established, increasing in population size and spreading (both through natural and human-assisted dispersal) for a number of years before it was detected. There are a variety of reasons as to why this was the case, the predominant reason being due to the biology of the pest itself. At low densities of infestation, infested ash trees typically do not show any visible symptoms of attack. Whilst adult beetles feed on the leaves they cause little damage, and it is not until the number of larvae build up within a tree to such an extent that they effectively girdle the tree causing the canopy and branches above the damage to decline in health and eventually die. In addition, during the early stages of an infestation, the adults tend to stay, and lay their eggs, high up in the canopy rather than on the lower parts of the trunk, making it very difficult to spot the characteristic D-shaped exit holes that the adults create as they chew their way out through the bark. A further characteristic of early infestation is that the beetle often exhibits a bivoltine life cyle in healthy trees with low larvae densities, meaning that it can be two years before the first exit holes are even created.

Being able to detect infestation very early on is a necessity for successful eradication of the pest; failure to do so gives the pest time to disperse out from the original invasion area, possibly to quite a distance depending on the mode of dispersal, creating additional outlier sites. Experiences in North America and Canada show that in such circumstances eradication is impossible (indeed it was never even attempted in the U.S.A. because the pest was too established and dispersed to do so). Therefore the strategies for controlling emerald ash borer in these countries centre around slowing the rate of ash tree mortality, to maintain ash tree health for as long as possible, via the implementation of management strategies to suppress the population growth and dispersal of emerald ash borer. This allows resource managers/private landowners to plan for long term recovery measures and spread the costs associated with emerald ash borer infestation over time.

To date, a number of methods to detect emerald ash borer are in use, all with their own advantages and disadvantages, but none are effective at detecting very low populations i.e. new infestations. Some of the more popular methods for detecting and monitoring emerald ash borer include the use of artificial traps (used in both the U.S.A. and Canada) baited with bark volatiles (e.g. Manuka oil or a mixture of Manuka oil and Phoebe oil) or ash leaf volatiles ((3Z)-hexenol), deliberately girdled ash trap trees (thought to be the most effective method and in use in America), and branching sampling (also thought to be effective and in use in Canada).

Control with a chemical insecticide is a viable option for high-value trees and those in urban and sub- urban areas. There are three main active ingredients that form the basis of systemic insecticide treatments for emerald ash borer: neonicotinoids, the avermectin emamectin benzoate and azadirachtin. Systemic insecticides are favoured over foliar/trunk sprays for a variety of reasons (efficacy, operater safety, environmental concerns). Efficacy studies with the neonicotinoid-based products have sometimes yielded inconsistent results and have concluded that the treatment must be re-applied on an annual basis for continued protection. Azadirachtin and emamectin products have different modes of action but both have given good results in the field, although azadirachtin

Control and management strategies for emerald ash borer ∣ March 2017 Page 81 treatments may need to be given annually for continued protection. Emamectin benzoate products however, have been demonstrated to be consistently highly effective and longer lasting – up to two years and possibly longer. Azadirachtin is currently in use in Canada whilst emamectin benzoate products appear to be the current favoured chemical control option in the U.S.A. Whichever chemical control option is chosen, care needs to be taken over the deployment strategy e.g. what proportion of trees to treat, at what distance from the infestation epicentre, and factors such as tree health before treatment is initiated, and infestation density all need to be taken into consideration, and applications must be made in accordance with recommended instructions in order to gain maximum benefit.

Chemical control however, may not be an option in more rural or forested areas where there may be a large number of trees distributed over a large area, and which may be inaccessible with the necessary equipment for such forms of control. Some research has been reported on the use of microbial control agents but these have disadvantages. Often they do not persist for long in the environment after application, and many are not specific to the pest species therefore they can potentially harm non-target organisms. To date, there do not appear to be any microbial products in use to control emerald ash borer in North America.

A further possibility for suppressing emerald ash borer is the use of natural enemies, either those native to the invaded country or exotic natural enemies that are native in the natural range of emerald ash borer. The use of natural enemies in biological control programmes (either classical or augmentative) might be feasible for suppressing emerald ash borer populations in forested or rural areas, provided these areas are large enough or suitably linked together with ash corridors, and preferably contain a density of ash equivalent to 25% or more of the trees. These options were investigated as soon as emerald ash borer was confirmed in North America. The invaded areas have been surveyed for indigenous natural enemies that could be developing associations with emerald ash borer. Whilst a number of parasitoid wasp species were originally found, parasitism rates were very low. Surveys have continued over the years and in some instances locations have been found where indigenous parasitoids appear to have high rates of parasitism (e.g. the discovery of A. cappaerti in areas of Michigan). It is not inconceivable that given time non indigenous parasiotoids will continue to form associations with emerald ash borer, and that these associations might increase in efficacy with regard to controlling emerald ash borer populations. This has not been seen to date in North America, with the exception of predation by woodpeckers, which can be very high on heavily infested trees, and whilst it does not prevent a heavily infested tree from dying, it does reduce the number of adult beetles that emerge from a heavily predated tree.

Parasitoid wasps with good potential for biological control of emerald ash borer were found in China and imported into the U.S.A. for further investigation. This work has ultimately resulted in the use of three species of parasitoid (T. planipennisi, S. agrili and O. agrili) originally from China, and one species (S. galinae) originally from the Russian Far East, being approved for release in the U.S.A.; T. planipennisi has also been approved for use in Canada. Results following releases so far indicate that both T. planipennisi and O. agrili are establishing at the release sites, increasing in population density and dispersing into the surrounding areas but parasitism rates, whilst increasing, are not yet akin to those observed in the China. Time will tell whether higher parasitism rates will be achieved and hence whether these species will be able to suppress emerald ash borer in invaded areas. The data for S. agrili is less conclusive; it is no longer used in more northern areas of North America due

Control and management strategies for emerald ash borer ∣ March 2017 Page 82 to a failure to establish, but it is still being released in more southerly States, which are thought to have a better climatic match. It is too early to tell whether releases of S. galinae have been successful as it was only approved for release in 2015. More recently a parasitoid wasp (S. polonicus) has been discovered in European Russia attacking invasive emerald ash borer at several locations, with apparent high rates of parasitism. Very little is known about this species, which warrants further investigation for potential use in biological control programmes.

It is very clear that no one method for detection, monitoring or suppressing emerald ash borer populations is suitable for all infested sites, and the methods used at each particular outbreak site should be chosen on the basis of the individual site characteristics and needs of the landowner. The different tactics for management are not mutually exclusive and can be used together in integrated management strategies.

Quarantine regulations and public outreach have also both played an important part in the management of emerald ash borer in North America. Strict regulations must be in place, not only between quarantine and non-quarantine areas, but also within infested areas to limit the human- assisted spread of emerald ash borer. Public outreach and education also have an important part to play in management strategies. By gaining the support of the public, they are more likely to adhere to regulations (such as movement of firewood – a particular problem in North America), and to back any control and management strategies that need to be implemented e.g. by allowing access to ash trees on their land, and participating in citizen science, which may help to identify previously unknown infested sites.

The presence of emerald ash borer in European Russia, centred around Moscow but rapidly spreading outward, including in a westerly and southerly direction, is of great concern to other European countries. It is only a matter of time before emerald ash borer naturally arrives at the Russian border with other European countries. Given the distribution of susceptible species of ash throughout Europe, this insect has the potential to spread throughout Europe, causing untold economic and environmental damage, and thus it is imperative that countries within the EU have robust strategies in place, which can be implemented immediately upon the discovery of emerald ash borer in their country.

Finally, this literature review is not exhaustive, and does not cover all areas of research pertaining to the control and management of emerald ash borer. In particular, it does not cover details on host plant resistance, research that has been undertaken to breed ash trees with resistance to emerald ash borer, and neither does it cover long term plans for recovery following emerald ash borer infestation. These topics should be reviewed as they also form important components in strategies to manage emerald ash borer. As a result of the North American invasion, much has been learnt about emerald ash borer, thanks to the efforts of regulatory agencies and collaborating scientists across the world, and the ability to manage the pest and protect ash trees has evolved accordingly. However, research and management strategies evolve continually. Therefore, it is important to stay up to date with ongoing scientific research and the effectiveness of strategies already implemented in areas having to deal with outbreaks of this destructive pest.

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Recommendations

It must be noted that this document is a literature review, and as such the information contained within it is gathered from scientific publications, grey literature and information available on the internet rather than from any practical experience on the biology, control and management of emerald ash borer.

It should also be noted that the use of trade/product names in this review has been done merely for ease of reporting scientific progress in chemical control options of emerald ash borer; it does not mean that the authors endorse or recommend the effectiveness and/or use of these particular named products.

Following review of the literature, the authors would recommend consideration of the following actions.

1. Liaisons with the relevant national regulatory authorities within the United States (USDA) and Canada (CFIA), State regulatory authorities, and personnel within these countries responsible for the development and implementation of control and management strategies in order to gain their advice on the control and management of emerald ash borer infestations. Contact with all appropriate parties should be maintained at regular intervals in order to stay abreast of any updates and advances in their control and management strategies.

2. Lessons from North America would suggest that it is imperative to have a robust contingency plan and management strategy in place to deal with any potential outbreak as soon as the relevant authorities have been alerted to the possibility of such an outbreak. This should include ensuring that all field inspectors are confident at assessing for the signs of emerald ash borer infestation, and can recognise the different life stages of the beetle. It may also include having the required contractors in place for any such tasks that require contractors such that their tasks can begin immediately upon confirmation of an outbreak.

3. Lessons from North America would also suggest that it is highly likely that an infestation will be established before symptoms appear, and that detecting the presence of emerald ash borer in the early stages of infestation is notoriously difficult, making it realistically very hard to eradicate the pest. Careful consideration needs to be given to detection/surveillance strategies. Should you wait until a possible infestation has been reported, and positively identified, before implementing surveillance strategies or should additional surveillance strategies (in addition to routine visual inspections at the possible points of entry) be implemented prior to a positive detection? For example, should surveillance strategies such as baited artificial traps/girdled sentinel trees be in place for detecting flying adults at import points of entry, nurseries, wood storage yards and crate storage yards that are in receipt of ash wood/packaging material?

4. Evidence from North America suggests that infestations are only likely to be found after they have been established for several years, are likely to be larger than originally thought, and dispersal to outlier sites is also likely to have occurred between establishment and

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detection. This is likely to continue to be the case until reliable methods for the early detection of emerald ash borer infestations are established. Regulatory agencies/managers may need to accept that management rather than eradication is the only option.

5. All detection/sampling methods have disadvantages (Table 1). It is inevitable that no one method will be suitable for all situations therefore survey programmes should involve multiple approaches if necessary.

6. A range of methods are available for the suppression of emerald ash borer populations. Each has their own advantages and disadvantages and associated costs. No one suppression method will be suitable for all outbreak situations therefore management strategies should be flexible and take account of the circumstances at each particular infestation site. A management strategy can, and probably should, include a number of different suppression methods within it, as well as intensive surveying and public outreach campaigns.

7. Whilst still in its infancy, the introduction of non-native parasitoids (specifically T. planipennisi, S. agrili, S. galinae and O. agrili) into the U.S.A. as part of a classical biological control programme to suppress emerald ash borer populations in forested areas looks promising. Much of the necessary work required before release of these parasitoids has already been performed by North American scientists. However, if these species of parasitoids were to be considered for use in the U.K. then climatic matching should be performed, and it should be ascertained whether there are likely to be any alternative hosts available in the U.K. that these parasitoids could potentially attack.

8. A parasitoid (S. polonicus) that apparently is capable of attacking emerald ash borer larvae has recently been identified in European Russia and high rates of parasitism reported. However, very little is known about this species of parasitoid, which is rare but distributed widely across Europe. Further investigations into the suitability of this species for classical biological control (if absent from the U.K.) or augmentative biological control (if already present in the U.K.) are warranted.

9. Information on native parasitoid species (and indeed other natural enemies) that might be capable of attacking/predating upon emerald ash borer should be sought.

10. Lures currently used to bait artificial traps attract male and female emerald ash borer adults but preferentially tend to attract male beetles. Consideration should be given for further research into identifying host plant volatiles that are attractive to females in order to maximise the attraction of mated and virgin females to traps.

11. Detailed information on host plant resistance, ash tree breeding programmes, and strategies for recovery following an emerald ash borer infestation have not been discussed within this review. They are however, considered important components of the control and management strategies for emerald ash borer. Consideration should therefore be given for the current status of research for these topics to be reviewed.

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12. Whilst not included in this review, some researchers suggest that collecting ash seed now could help to ensure that a supply of ash exists for re-introduction at a later date following infestation, and could be useful in both assessing ash tree resistance and in breeding projects to create ash resistant to emerald ash borer.

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