EPPO Datasheet: Agrilus planipennis
Taxonomic position: Animalia: Arthropoda: Hexapoda: Insecta: Coleoptera: Buprestidae
Other scientific names: Agrilus marcopoli ulmi Kurosawa, Agrilus marcopoli Obenberger
Common names in English: emerald ash borer
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Notes on taxonomy and nomenclature
Jendek (1994) synonymized three Agrilus species under the name Agrilus planipennis Fairmaire (1888; type China), including A. feretrius Obenberger (1936; type Taiwan), A. marcopoli Obenberger (1930; type China), and A. marcopoli ulmi Kurosawa (1956; type Japan). Much of the early literature on A. planipennis refers to A. marcopoli in China and to A. marcopoli ulmi in Japan. More recently, Chamorro et al. (2015) reclassified the A. feretrius specimens from Taiwan as Agrilus tomentipennis along with specimens from Laos.
EU Categorization: Emergency measures (formerly), A1 Quarantine pest (Annex II A)
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EPPO Code: AGRLPL
Native hosts of A. planipennis include almost exclusively species of ash (Fraxinus). The known Asian species include Fraxinus chinensis, F. chinensis subsp. rhynchophylla, Fraxinus mandshurica and Fraxinus platypoda (= F. spaethiana) (Liu et al., 2003; Wei et al., 2004; Zhao et al., 2005; Mori, 2012). In North America, A. planipennis has infested all species of native ash so far encountered, including Fraxinus americana, Fraxinus latifolia. Fraxinus nigra, Fraxinus pennsylvanica, Fraxinus profunda, and Fraxinus quadrangulata (Haack et al., 2002; Poland and McCullough, 2006; Herms, 2015), as well as Chionanthus virginicus (Peterson & Cipollini, 2017). In European Russia, A. planipennis has infested and completed development in Fraxinus angustifolia subsp. oxycarpa, Fraxinus excelsior, and Fraxinus ornus (Baranchikov et al., 2014; Orlova-Bienkowskaja et al., 2020). The North American species Fraxinus velutina has been attacked in China (Liu et al., 2003). In laboratory studies, A. planipennis has successfully completed development in cut trunk sections of Fraxinus uhdei (Herms, 2015) and Olea europaea (Cipollini et al., 2017). Reports from Japan (Akiyama & Ohmomo, 1997; Sugiura, 2008) that A. planipennis can complete development in Juglans ailanthifolia, Juglans mandshurica, Pterocarya rhoifolia, and Ulmus davidiana are now considered incorrect larval host records (referring to personal communications in section 7, p. 12 - EPPO, 2013a; Sigiura N, pers. comm.). Although Fraxinus japonica and Fraxinus lanuginosa have been reported as larval hosts for A. planipennis by various authors, no published rearing records have been found.Host list: Chionanthus virginicus, Fraxinus americana, Fraxinus angustifolia subsp. oxycarpa, Fraxinus chinensis subsp. rhynchophylla, Fraxinus chinensis, Fraxinus excelsior, Fraxinus latifolia, Fraxinus mandshurica, Fraxinus nigra, Fraxinus ornus, Fraxinus pennsylvanica, Fraxinus platypoda, Fraxinus quadrangulata, Fraxinus velutina
GEOGRAPHICAL DISTRIBUTION 2021-01-08
A. planipennis is native to several Asian countries (China, Japan, North Korea, South Korea, and the Russian Far East). Early reports of A. planipennis occurring in Mongolia (Yu, 1992; Jendek, 1994) have been questioned in recent publications (Orlova-Bienkowskaja & Volkovitsh, 2018, EFSA et al., 2020). In addition, Schaefer (2005) reported that ash (Fraxinus) trees are absent in Mongolia and that no A. planipennis specimens were present in Mongolia’s National University insect collection in Ulaanbaatar. Similarly, reports of A. planipennis being native to Taiwan (Jendek, 1994) and Laos (Jendek & Grebennikov, 2011), are now uncertain given that these specimens were recently reassigned to the species Agrilus tomentipennis Jendek & Chamorro (Jendek & Chamorro, 2012; Chamorro et al., 2015), which is highly similar in appearance to A. planipennis. Clearly, more research is needed to define the true native range of A. planipennis in South-Eastern Asia.
In recent decades, A. planipennis has spread to new parts of China as well as to North America and Europe. In China, A. planipennis was recently reported in the western province of Xinjiang, where it is considered non-native (Orlova-Bienkowskaja & Volkovitsh, 2018). In North America, A. planipennis was first reported in 2002 near Detroit, Michigan, US and in neighboring Windsor, Ontario, CA (Haack et al., 2002). As of December 2020, A. planipennis was found in 35 US states and the District of Columbia and in five Canadian provinces (EABinfo, 2020). In Europe, A. planipennis adults were first collected in European Russia near Moscow in 2003 but not positively identified until 2005 (Baranchikov et al., 2008; Haack et al., 2015). As of 2020, A. planipennis has spread to several regions of European Russia and into Western Ukraine (Orlova-Bienkowskaja et al., 2020; Volkovitsh & Suslov, 2020). The exact pathways by which A. planipennis first reached North America and European Russia are unknown. However, wood packaging is considered the likely original source in North America, and either nursery stock or wood packaging in Russia (Haack et al., 2015).EPPO Region: Russia (Central Russia, Far East, Southern Russia), Ukraine
Asia: China (Beijing, Hebei, Heilongjiang, Jilin, Liaoning, Shandong, Tianjin, Xinjiang), Japan (Hokkaido, Honshu, Kyushu, Shikoku), Korea Dem. People's Republic, Korea, Republic
North America: Canada (Manitoba, New Brunswick, Nova Scotia, Ontario, Québec), United States of America (Alabama, Arkansas, Colorado, Connecticut, Delaware, District of Columbia, Georgia, Illinois, Indiana, Iowa, Kansas, Kentucky, Louisiana, Maine, Maryland, Massachusetts, Michigan, Minnesota, Missouri, Nebraska, New Hampshire, New Jersey, New York, North Carolina, Ohio, Oklahoma, Oregon, Pennsylvania, Rhode Island, South Carolina, South Dakota, Tennessee, Texas, Vermont, Virginia, West Virginia, Wisconsin)
Agrilus is the largest genus of animals worldwide, with over 3200 recognized species (Kelnarova et al., 2019). Agrilus are native to Africa, Asia, Australia, Europe and the Americas, but not New Zealand (Chamorro et al., 2015). Agrilus larvae typically feed and develop in the cambial region of woody plants (vines, shrubs, and trees) as well as internally in the lower stems and roots of some herbaceous perennials (Chamorro et al., 2015). Adults often have striking metallic colours and members of the family Buprestidae are often referred to as jewel beetles. Several Agrilus species are of economic importance in forestry, arboriculture, and agriculture. No native European or North American species of Agrilus are known to infest and kill ash trees, although some infest branches which are dying or recently dead, e.g., A. convexicollis Redtenbacher in Europe (Orlova-Bienkowskaja & Volkovitsh, 2015) and A. subcinctus Gory in North America (Petrice et al., 2009).
Several studies and reviews have been published on the life-history of A. planipennis in China, Europe, and North America. Below is a summary based largely on Yu (1992), Haack et al. (2002), Cappaert et al. (2005), Wei et al. (2007), Wang et al. (2010), Chamorro et al. (2015), Herms & McCullough (2014), Haack et al. (2015), Poland et al. (2015), Orlova-Bienkowskaja & Bieńkowski (2016), Valenta et al. (2017) and EFSA et al. (2020). A. planipennis typically has one generation per year although some individuals may require two years when developing in vigorous hosts, when developing from eggs laid in late summer, or where summer temperatures are cool. Depending on latitude and local temperatures, adult emergence usually begins in May or June, peaks in late May to early July, and adult activity can persist into September. After emergence, adults feed on host foliage for 1-2 weeks to become sexually mature. Adults are most active on sunny days. Adult males orient visually towards females when seeking mates. Adult females produce at least one short-range pheromone and two contact pheromones. Mating occurs on foliage and the bark surface of host trees. Adults feed throughout their lifespan and will mate multiple times. Eggs are laid singly or in small groups on the bark surface, usually in bark cracks and crevices. Adults usually live 3-9 weeks and females lay an average of 40 to 90 eggs in their lifetime. Eggs hatch in 1-2 weeks. Newly hatched larvae tunnel through the outer bark to the cambial region where they tunnel and feed in the inner bark (phloem) and outermost sapwood, creating meandering frass-packed galleries. There are four larval instars. Fourth-instar larvae construct pupal cells in the outer bark if the bark is sufficiently thick or in the outer sapwood. Most individuals overwinter as fourth-instar larvae, in a doubled-over position and referred to as J-shaped larvae or prepupae. Crosthwaite et al. (2011) reported a supercooling point of about -30 °C for A. planipennis prepupae. However, Orlova-Bienkowskaja & Bieńkowski (2020) noted that A. planipennis populations have survived in areas experiencing -30 °C but so far not in areas experiencing -34 °C or below. If larvae do not become fourth instars by autumn, they overwinter in the cambial region and complete larval development the next summer, and then overwinter a second time before becoming adults. Pupation usually begins in April or May and takes about 3-4 weeks. Newly formed adults take about 1 week to harden their exoskeleton before chewing their way out of the tree through D-shaped exit holes that are about 3–4 mm wide.
DETECTION AND IDENTIFICATION 2021-01-08
Signs and symptoms
Signs are physical damage to the plant usually made by the insect pest, whereas symptoms are a tree’s response to the infestation. In the case of A. planipennis, the two most commonly observed signs include frass-filled larval galleries in the cambial region and adult exit holes on the bark surface (DeGroot et al., 2006; EFSA et al., 2020). Another sign, although less often seen, are notches along the leaf margins where adults have fed. Some vertebrates produce signs that can be used to locate infested trees such as woodpeckers that produce holes in the bark when feeding on A. planipennis or squirrels that feed on larvae and leave behind strips of ragged bark (DeGroot et al., 2006). Typical symptoms include yellowing and thinning of foliage, crown dieback and eventual tree mortality. On some ash trees, epicormic shoots develop along the lower trunk of heavily infested trees, and at times the bark produces vertical splits or cracks, 5-15 cm long, usually over larval galleries where the sapwood has produced callus tissue in response to larval feeding. As no European species of Agrilus are known to infest the trunks of ash, the occurrence of galleries and exit holes typical of Agrilus in ash tree trunks and larger branches should automatically be suspect.
Development of traps and lures for A. planipennis has been the focus of many studies (Herms & McCullough, 2014; Poland et al. 2015; EFSA et al., 2020). Various shades of green and purple are highly attractive to A. planipennis adults. Both funnel traps and sticky prism traps have been used in regional surveys. Traps can be placed in the canopy, beneath the canopy, or near ground level. Traps baited with certain green leaf volatiles [e.g., (3Z)-hexenol] or pheromones [e.g., (3Z)-lactone] capture more A. planipennis adults than unbaited traps (Silk et al., 2020). Girdled ash trees are more attractive to A. planipennis than non-girdled trees and therefore can be used as a detection tool. For example, individual ash trees could be girdled in late spring or early summer to attract ovipositing A. planipennis and then debarked in autumn or winter to look for A. planipennis larvae and their galleries (Herms & McCullough, 2014). Survey methods and strategies for eradication of A. planipennis populations discovered in Europe have been published (EPPO, 2013b; EFSA et al., 2020; Evans et al., 2020).
Several papers provide detailed photos of A. planipennis adults, including Chamorro et al. (2015) and Volkovitsh et al. (2020). Photos of all A. planipennis immature stages are presented in Chamorro et al. (2012), Haack et al. (2015), and EFSA et al. (2020), among others. Additional photos of A. planipennis larvae can be found in Petrice et al. (2009) and Volkovitsh et al. (2020).
Eggs are creamy yellow when first laid, turning reddish brown before hatching (DeGroot et al., 2006; Chamorro et al., 2012). Eggs are oval in cross section and somewhat flattened, measuring about-1.0–1.2 mm long; 0.6 mm wide, and 0.3 mm high. A glue-like substance on the bottom of the egg helps fasten it to the bark surface (Chamorro et al., 2012).
Mature fourth-instar larvae of A. planipennis are 26–36 mm long and creamy white (Yu, 1992; Chamorro et al., 2012). The body is elongate, and dorsoventrally flattened. The head is small, brown, and retracted into the prothorax, exposing only the mouthparts. The prothorax is enlarged, and the meso and metathorax are slightly narrower. Spiracles are found on the mesothorax and abdominal segments 1-8. The abdomen is 10-segmented terminates in a pair of brownish, sclerotized tooth-like structures that are often called urogomphi, anal forceps, or terminal processes (Petrice et al., 2009; Chamorro et al., 2012). Such terminal processes are characteristic of all known Agrilus larvae (Chamorro et al., 2015). The prothoracic plate is pigmented with a bifurcated pronotal groove and abdominal segments 2–7 are trapezoidal or bell-shaped in appearance (Petrice et al., 2009; Chamorro et al., 2012).
Pupation occurs in the cells that were constructed in the outer sapwood or outer bark by the mature larvae prior to overwintering. The larva contracts its body and then molts to the pupal stage. Pupae are 10-18 mm long, 4-6 mm wide, and creamy white at first. As pupation progresses the eyes darken first, then the mouthparts, and lastly the elytra, until the entire pupa darkens (Haack et al., 2015). The antennae stretch back to the base of the elytra and the last few segments of the abdomen bend slightly ventrad (Yu, 1992).
Adults of A. planipennis are 8.5–15.0 mm long and 3.0–3.5 mm wide (Yu, 1992; DeGroot et al., 2006; Chamorro et al., 2015). The body is narrow, elongate, cuneiform, and a beautiful metallic blue-green colour. The elytra are glabrous. The head is flat and the vertex is shield-shaped. The compound eyes are kidney-shaped and somewhat bronze-coloured. The prothorax is transversely rectangular and slightly wider than the head, but the same width as the anterior margin of the elytra. The anterior margin of the elytra is raised, forming a transverse ridge.
PATHWAYS FOR MOVEMENT 2021-01-08
Under laboratory conditions, A. planipennis adults can fly on average 1.3 km per day, with some individuals exceeding 7 km per day (Taylor et al., 2010). However, long-distance movement that involves 10s or 100s of kilometers likely results from human assistance. Although there have been no reports of A. planipennis being intercepted in wood packaging material, several Agrilus individuals that were identified only to the genus level have been intercepted. For example, between 1985-2000 there were 38 distinct interceptions of Agrilus species made at US ports of entry that originated from 11 countries, and of these 28 were recovered from dunnage, 4 from crating, 5 from live plants or plant parts, and 1 specimen was found loose in the ship (Haack et al., 2002; Haack, 2006). In North America, A. planipennis has been moved in ash nursery stock, ash logs, ash firewood, and also been found hitch-hiking on the outside and inside of vehicles (Buck and Marshall, 2008; Haack et al., 2015). In addition, Short et al. (2020) suggested that A. planipennis adults could hitch-hike on trains. Petrice & Haack (2006) reported that a small percentage of A. planipennis can emerge from firewood for two seasons after the wood was cut from infested trees.
PEST SIGNIFICANCE 2021-01-08
A. planipennis has infested and killed ash trees in Asia where the pest is native as well as in Europe and North America where it has been introduced. A. planipennis readily kills stressed ash trees, but in addition it can kill healthy ash trees especially if the trees are non-coevolved ash species such as those native to Europe and North America. A. planipennis can infest and kill large mature ash trees as well as trees and branches as small as 1 cm in diameter (EPPO, 2013b). Hundreds of millions of ash trees have been killed in North America, resulting in billions of dollars spent on tree protection, removal, and replacement (Herms & McCullough, 2014). A. planipennis is considered the most costly non-native forest insect to have invaded the United States (Aukema et al., 2011). In European Russia, A. planipennis has so far killed mostly plantations of the North American ash species F. pennsylvanica (Orlova-Bienkowskaja et al., 2020), but as the pest spreads in Europe major economic impacts are expected given that several ash species are common throughout Europe and many are already known to be susceptible to A. planipennis (Baranchikov et al., 2014; EFSA et al., 2020).
The only non-ash larval host of A. planipennis so far documented in North America has been the white fringetree Chionanthus virginicus (Peterson & Cipollini, 2017). Chionanthus and Fraxinus are both genera in the Oleaceae family. A. planipennis has infested C. virginicus at multiple sites in at least four US states; however, compared to ash trees, mortality rates of C. virginicus are much lower (Peterson & Cipollini 2017).
Several ecological impacts have been documented in North America following the introduction of A. planipennis. For example, Klooster et al. (2016) documented over 99% ash tree mortality in several forest stands in Michigan, an ending of ash seed production, increased openings in the forest canopy, an accumulation of coarse woody debris resulting from the dying ash trees, an increase in alien invasive plants, and changes to arthropod and bird communities. In addition, Wagner & Todd (2016) documented 98 arthropods in the United States that are ash specialists as larvae or adults, including 32 species of Lepidoptera, 25 Hemiptera, 24 Coleoptera, 9 Diptera, 5 Acari, and 3 Hymenoptera. In European Russia, populations of various ash-associated xylophagous beetles and their natural enemies are increasing as the geographic range of A. planipennis expands (Orlova-Bienkowskaja, 2015; Orlova-Bienkowskaja & Volkovitsh, 2015).
Several insecticides have been tested in North America to protect ash trees from A. planipennis (Herms et al., 2019). Depending on the product label, these insecticides can be applied as soil drenches, soil injections, trunk injections, or cover sprays on the trunk, branches and foliage. The systemic insecticide emamectin benzoate gives 2 to 3 years of control against both A. planipennis larvae and leaf-feeding adults (McCullough et al., 2011; 2019; Herms et al., 2019). Due to the expense of treatment, insecticides are typically used on high-value landscape ash trees.
Trees infested with A. planipennis can be cut down and chipped to kill larvae and pupae within the host material (McCullough et al., 2007). To ensure high pest mortality when chipping, the openings in the chipper screen should be 2.5 cm in size or smaller.
The current heat treatment standard in ISPM 15 for wood packaging materials requires that a minimum core temperature of 56°C be maintained for 30 continuous minutes. Haack and Petrice (unpublished data) recorded 100% A. planipennis mortality in small ash logs subjected to a core temperature of 56 °C for 30 minutes while holding the heating chamber temperature constant at 60°, 65°, 70° or 75°C. In other studies, summarized by Haack et al. (2014), a few A. planipennis have survived various heat treatment schedules but in none of these tests did the researchers follow ISPM-15 guidelines exactly.
Several parasitoids of A. planipennis have been reported in the literature from Asia, Europe, and North America (Taylor et al., 2012; Orlova-Bienkowskaja & Belokobylskij, 2014; Bauer et al., 2015; Duan et al., 2019). The egg parasitoids include species of Oobius (Encyrtidae) and Ooencyrtus (Encyrtidae). The larval parasitoids include species of Atanycolus (Braconidae), Balcha (Eupelmidae), Cubocephalus (Ichneumonidae) Dolichomitus (Ichneumonidae), Eupelmus (Eupelmidae), Orthizema (Ichneumonidae), Phasgonophora (Chalcididae), Spathius (Braconidae) Sclerodermus (Bethylidae), and Tetrastichus (Eulophidae). In North America, three biocontrol agents from China and one from the Russian Far East have been released to help control A. planipennis (Bauer et al., 2015; Duan et al., 2019). The parasitoids from China include the encyrtid egg parasitoid Oobius agrili and two larval parasitoids, the braconid Spathius agrili and the eulophid Tetrastichus planipennisi and from Russia, the braconid Spathius galinae was introduced. Of the three Chinese parasitoids, O. agrili and T. planipennisi appear to be well established and spreading naturally in North America, whereas it is too early to assess the Russian parasitoid, which was first released in 2016 (Duan et al., 2019a, 2019b). As for predators of A. planipennis, woodpeckers (Picidae) are the most important group (Jennings et al., 2016). Some of the insect predators associated with A. planipennis include species of Cleridae, Passandridae, and Trogossitidae (Liu et al., 2003).
Fraxinus spp. are widespread components of mixed deciduous forests in Europe as far as the Caucasus, throughout (F. excelsior), in the south (F. angustifolia) and in the centre and southeast (F. ornus) (EFSA et al., 2020). They are commonly grown for amenity purposes and are known to be susceptible to A. planipennis. The North American species F. pennsylvanica is planted for timber and shelter in Central and South-Eastern Europe and is highly susceptible to A. planipennis. The introduction of A. planipennis into North America and European Russia shows that there are pathways to disseminate this pest outside its area of origin, especially in wood packaging material. Ash mortality has been reported in both North America and European Russia. Control and detection of this type of wood-boring insect is difficult. In view of its area of origin and the areas where it has been introduced, it is highly probable that A. planipennis could become established in most of Europe where Fraxinus spp. are common.
PHYTOSANITARY MEASURES 2021-01-08
The Asian buprestid A. planipennis was first detected in North America (USA and Canada) in 2002 and then in the European part of Russia (Moscow region) in 2005. A. planipennis was added to EPPO A1 List of pests recommended for regulation in 2004 based on a PRA performed by the EPPO Panel on Quarantine Pests for Forestry in 2003. Later, in 2009, A. planipennis was transferred to the A2 List given its establishment in European Russia (EPPO, 2013a). EPPO member countries are thus recommended to regulate A. planipennis as a quarantine pest. Suggested phytosanitary measures are specified in the PRA performed by EPPO (EPPO, 2013a) and they are as follows. Plants for planting (except seeds) of Fraxinus (and currently a few other tree genera that were listed as potential hosts in Japan) should originate from countries found free from the pest. Alternatively, they may be grown under insect-proof conditions. Wood chips, wood waste, firewood, bark, and cut branches should originate from countries found free from the pest. If bark is present on firewood, lumber, logs or furniture made from untreated wood then the bark should be removed as well as the outer 2.5 cm of sapwood. Wood packaging should be treated to ISPM-15 standards. As a general approach, it has also been recommended that when importing plants for planting (except seeds) and wood commodities of Fraxinus from countries where A. planipennis occurs, precautions should have been taken to avoid any infestations while the consignments are transported through possibly infested areas (EPPO, 2020).
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This datasheet was extensively revised and updated in 2021 by Robert A. Haack, USDA Forest Service, Northern Research Station, Lansing, MI, USA (emeritus). His valuable contribution is gratefully acknowledged.
How to cite this datasheet?
Datasheet history 2021-01-08
This datasheet was first published in the EPPO Bulletin in 2005 and revised in 2021. It is now maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.
EPPO (2005) Agrilus planipennis. Datasheets on pests recommended for regulation. EPPO Bulletin 35(3), 436-438. https://doi.org/10.1111/j.1365-2338.2005.00844.x