Preferred name: Agrilus anxius
Authority: Gory
Taxonomic position: Animalia: Arthropoda: Hexapoda: Insecta: Coleoptera: Buprestidae
Other scientific names: Agrilus gravis LeConte, Agrilus torpidus LeConte
Common names in English: bronze birch borer
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Notes on taxonomy and nomenclature EPPO Categorization: A1 list
EU Categorization: A1 Quarantine pest (Annex II A)
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EPPO Code: AGRLAX

The larval host plants of A. anxius are trees in the genus Betula (birch). In North America, primary hosts are B. alleghaniensis, B. lenta, B. lutea, B. occidentalis, B. papyrifera, and B. populifolia (Balch & Prebble, 1940; Ball & Simmons, 1980; Santamour, 1999; Nielsen et al., 2011; Muilenburg & Herms, 2012). When planted in North America, several European and Asian birch species are readily infested and killed by A. anxius , including B. maximowicziana, B. pendula, B. platyphylla and B. pubescens, (Ball & Simmons, 1980; Miller et al., 1991; Nielsen et al., 2011; Muilenburg & Herms, 2012).

Host list: Betula albosinensis, Betula alleghaniensis, Betula dahurica, Betula ermanii, Betula lenta, Betula maximowicziana, Betula nigra, Betula occidentalis, Betula papyrifera, Betula pendula, Betula platyphylla var. japonica, Betula platyphylla var. szechuanica, Betula platyphylla, Betula populifolia, Betula pubescens, Betula pumila, Betula utilis subsp. jacquemontii, Betula

Agrilus anxius is native to much of the boreal and north temperate regions of North America where birch occurs (Bright, 1987; Muilenburg & Herms, 2012). Its current range has expanded into the Southern and Western United States as a result of widespread planting of birch species as ornamental trees (Duckles & Svihra, 1995; Muilenburg & Herms, 2012).

North America: Canada (Alberta, British Columbia, Manitoba, New Brunswick, Newfoundland, Nova Scotia, Ontario, Prince Edward Island, Québec, Saskatchewan), United States of America (Alaska, Arizona, Arkansas, California, Colorado, Connecticut, Delaware, District of Columbia, Georgia, Idaho, Illinois, Indiana, Iowa, Kansas, Kentucky, Maine, Maryland, Massachusetts, Michigan, Minnesota, Missouri, Montana, Nebraska, Nevada, New Hampshire, New Jersey, New Mexico, New York, North Carolina, North Dakota, Ohio, Oregon, Pennsylvania, Rhode Island, South Carolina, South Dakota, Utah, Vermont, Virginia, Washington, West Virginia, Wisconsin, Wyoming)

A. anxius usually completes its life cycle in one year but occasionally two years are required, depending on latitude, climatic conditions, and host condition (Balch & Prebble, 1940; Anderson, 1944; Nash et al., 1951). In Ohio and Michigan, adult emergence usually begins at about 278 cumulative degree days (DD), using a base temperature of 10°C and a starting date of January 1 (Muilenburg & Herms, 2012). Adult emergence generally occurs over 10–12 weeks, with peak emergence occurring about 2–4 weeks after first emergence (Barter, 1957; Akers & Nielsen, 1984; Loerch & Cameron, 1984). Adult emergence typically begins in May in Kentucky (Mussey & Potter, 1997), May to June in Ohio and Michigan (Akers & Nielsen, 1984; Muilenburg & Herms, 2012), and late June to early July in New Brunswick, Canada (Balch & Prebble, 1940; Barter, 1957). Individual adults live for 2–5 weeks (Akers & Nielsen, 1990), which is typical of many Agrilus species (Chamorro et al., 2015).

A. anxius adults consume foliage throughout their lifetime (Barter, 1957; Akers & Nielsen, 1990), which is common among Agrilus species (Chamorro et al., 2015). Adults typically feed for about one week to become sexually mature (Rutledge & Keena, 2019). Adults usually consume Betula and Populus foliage, but can survive and reproduce when fed foliage from other tree species under experimental conditions (Barter, 1957; Akers & Nielsen, 1990). Adults feed mostly along the leaf margin and cause negligible damage to trees (Barter, 1957; Muilenburg & Herms, 2012). No pheromone has yet been identified for A. anxius (Silk et al., 2020). Mate location is primarily visual (Rutledge & Keena, 2019), with mating occurring on the trunk, branches, and foliage of birch trees. Adults typically pair for 7-11 minutes (Barter, 1957; Rutledge & Keena, 2012). 

Females lay eggs singly or in clusters of up to 16 eggs, averaging 7 (Barter, 1957). Eggs are laid in bark crevices, cracks, and under loose layers of outer bark (Barter, 1957; Loerch & Cameron, 1984). Under laboratory conditions (approximately 25°C, 65% RH, and 16:8 L:D h photoperiod), females lived an average of 30 days and laid 55 eggs each (Rutledge & Keena, 2012). Eggs hatch in about 2 weeks (Barter, 1957). 

Newly hatched larvae tunnel directly through the outer bark into the underlying inner bark (phloem) tissue. There are 4 larval instars (Loerch & Cameron, 1983a). Larvae construct galleries in the cambial region at the phloem-xylem interface, with total average gallery length varying between 41-85 cm based on host condition and birch species (Anderson, 1944). Larvae tunnel in the outer sapwood for short distances to molt (Barter, 1957). Larvae use their terminal processes (urogomphi) to pack frass tightly within their galleries (Carlson & Knight, 1969). Larval galleries disrupt downward transport in phloem tissue and upward transport in the outer ring of xylem (sapwood), which at high densities and usually over multiple years can girdle and kill trees (Barter, 1957). All larval instars can overwinter (Barter, 1957). However, only pre-pupal larvae (4th instars that have completed feeding and constructed pupal cells by autumn) that overwinter and experience freezing temperatures will pupate the following spring (Barter, 1957). Upon completion of larval development, 4th instars construct pupal cells in the outer sapwood, generally during late summer or autumn (Barter, 1957; Loerch & Cameron, 1984). Larvae that do not become final instars by autumn will overwinter in the cambial region, complete larval development the following summer, and then overwinter a second time before pupating.

Larvae construct individual pupal cells that are about half their body length and pass the winter inside in a U- or J-shaped position (Carlson & Knight, 1969). Pupation occurs in May-June in Michigan (Carlson & Knight, 1969) and (Pennsylvania (Loerch & Cameron, 1984). 

Adults chew D-shaped exit holes as they emerge that are 3–5 mm wide (Muilenburg & Herms, 2012). Adult emergence usually occurs from May to the end of July (Barter, 1957; Akers & Nielsen, 1984). Newly emerged adults have nearly a 1:1 sex ratio (Barter, 1957).

A. anxius colonizes most Betula species and cultivars, although host resistance varies with B. nigra appearing to be nearly immune to colonization (Nielsen et al., 2011). A. anxius is typically a secondary invader of  North American birch species (e.g. B. allegheniensis, B. lutea, B. papyrifera, B. populifolia ) that have been stressed by drought, late spring frosts, old age, insect defoliation, soil compaction, and stem or root injury (Balch & Prebble, 1944; Anderson, 1944; Barter, 1957; Muilenburg & Herms, 2012; Haack & Petrice, 2019). European and Asian birch species that have been studied are much more susceptible than North American species to A. anxius (Miller et al., 1991; Nielsen et al., 2011). For example, in a 20-year common garden study in Ohio, USA, with a high number of replicates, bronze birch borer infestation caused complete mortality of Eurasian species (B. maximowicziana, B. pendula, B. platyphylla var. szechuanica, B. pubescens), but the majority of individuals (>75%) of North American species (B. nigra, B. papyrifera, B. populifolia) were still alive at the end of the study (Nielsen et al., 2011). European and Asian birch species are highly susceptible to A. anxius colonization even when not stressed (Muilenburg & Herms, 2012). A. anxius infests birch trees of all sizes, with larvae being found in branches as small as 1 cm in diameter (Muilenburg & Herms, 2012).

In North America, A. anxius populations generally exist at endemic levels (Balch & Prebble, 1940). However, periodic outbreaks have been reported during the past century, usually being associated with widespread drought and defoliation (Balch & Prebble, 1940; Nash et al., 1951; Houston, 1987; Muilenburg & Herms, 2012; Haack & Petrice, 2019).

Signs and symptoms

Trees that have been infested or currently are infested with A. anxius will have one or more of the following signs or symptoms: D-shaped holes on the bark surface created by emerging adults, meandering or zig-zag larval galleries filled with frass at the phloem–xylem interface, or serpentine swellings or ridges visible through the outer bark where wound periderm (callus tissue) has grown over larval galleries (Anderson, 1944; Barter, 1957). Trees infested with A. anxius exhibit branch dieback, especially after multiple years of infestation, usually beginning with the upper crown branches (Ball & Simmons, 1980). Branch dieback is usually preceded by yellowing and thinning of the foliage. 

Trapping

When developing survey protocols for A. anxius it is important to recall that A. anxius infests North American birch species when they are stressed, whereas it will infest both stressed and healthy Eurasian birch. Therefore, girdling individual North American birch trees usually increases the tree’s attractiveness to A. anxius adults (Rutledge, 2020; Silk et al., 2020). The specific host compounds, or combination of compounds, that A. anxius adults use to locate stressed trees is still unknown (Silk et al., 2020). A. anxius adults have been collected on both green and purple traps (Petrice et al., 2013; Rutledge, 2020; Silk et al., 2020). In addition, ground-nesting solitary wasps in the genus Cerceris, which specialize in capturing buprestid adults, can be used as biosurveillance tools for many buprestids, including A. anxius (Kurczewski & Miller, 1984; Swink et al., 2013).

Morphology

Eggs

The eggs of A. anxius are creamy white when first laid, becoming more yellow as they mature (Barter, 1957). Eggs appear oval in shape, but flattened, and are 1.3 to 1.5 mm long and 0.8 to 1.0 mm wide (Barter, 1957; Carlson & Knight. 1969). Females coat the eggs after deposition with a whitish substance that likely helps cement the eggs to the bark and prevent desiccation (Barter, 1957).

Larva

Larvae are creamy white with a brown head and urogomphi. The body is dorsoventrally flattened. The head is small and protracted into the enlarged prothorax. There are 10 abdominal segments, with the last terminating in two sclerotized tooth-like structures that are often called urogomphi, anal forceps, or terminal processes (Carlson & Knight, 1969; Loerch & Cameron, 1983a; Chamorro et al., 2015). Such terminal processes are characteristic of all known Agrilus larvae (Chamorro et al., 2015). A. anxius is recognized as having four larval instars (Loerch & Cameron, 1983a), although Barter (1957) reported five instars. Mature last-instar larvae measure 30-40 mm long (Barter, 1957; Carlson & Knight, 1969).

Pupa

Pupation takes place inside the cells that were constructed in the outer sapwood by the mature larvae prior to overwintering. The larva first contracts its body to about half its former length and then molts to the pupal stage (Barter, 1957). Pupae are creamy white at first, but as pupation progress the eyes darken first, then the mouthparts, and lastly the elytra, until the entire pupa becomes bronze to black (Barter, 1957; Carlson & Knight, 1969). These colour changes are very similar to those seen for A. planipennis as described in Haack et al. (2015). 

Adult

Adults are narrow, subcylindrical with coppery-bronze metallic colouration. They are usually 6-11 mm long (Barter, 1957), but can vary between 5–13 mm (Paiero et al., 2012). Males have a ventral groove on the first and second abdominal segments that is absent in females (Barter, 1957). Differences in aedeagus morphology are the most reliable characters to separate adult male A. anxius from the morphologically similar A. liragus (= A. granulatus liragus) (Barter & Brown, 1949; Carlson & Knight, 1969). Additionally, A. anxius has 22 chromosomes whereas A. liragus has 20 (Barter, 1957).

There is no information about natural dispersion of A. anxius adults by flight. However, under laboratory conditions, the emerald ash borer (Agrilus planipennis), which is similar in size   to A. anxius, can fly on average 1.3 km per day, with some individuals exceeding 7 km per day (Taylor et al., 2010). Most Agrilus species, like many other bark- and wood-infesting insects, can be transported in live host plants or wood products such as logs, firewood, solid wood packaging, lumber, bark, and wood chips (Meurisse et al., 2019). For example, during 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 from dunnage, 4 from crates, 5 from plants or plant parts, and 1 specimen was found loose in the ship hold (Haack et al., 2002; Haack, 2006).  Importation of wood chips from North America to Europe is a potential pathway for movement Agrilus species and other pests , especially when the chips are relatively large in size, untreated and stored outdoors in close proximity to susceptible host trees (McCullough et al., 2007; Kopinga et al., 2010; Flø et al., 2014).

Economic impact

In North America, A. anxius is considered the most serious pest of birch trees in both forest and amenity plantings (Barter, 1957; Ball & Simmons, 1980). In urban landscapes, A. anxius has caused widespread mortality of ornamental and street trees. In the northern hardwood and boreal forests of North America, periodic outbreaks of A. anxius have also led to widespread mortality of birch, causing negative impacts on forest tree composition and wildlife (Balch & Prebble, 1944; Nash et al., 1951; Millers et al., 1989; Haack & Petrice, 2019).

Betula species occur throughout most of Europe but are most common in the temperate and boreal forests of Northern Europe (Beck et al., 2016). Moreover, birch are the most important commercial broadleaved species in Northern Europe, being used for pulpwood, fuel wood, lumber, plywood, and as amenity trees (Hynynen et al., 2010; Beck et al., 2016).

Control

Control and detection of this type of wood-boring insect is difficult. There are several insecticides (e.g. azadiractin, bifenthrin, dicrotophos, dimethoate, dinotefuran, emamectin benzoate, imidacloprid, permethrin) that have been shown to control Agrilus species to varying degrees (Appleby et al., 1973; Petrice & Haack, 2006; McKenzie et al., 2010; Smitley et al., 2010; McCullough et al., 2011; Herms et al., 2019). They may be used in nurseries and on ornamental birch trees. Depending on the label, they can be applied as soil drenches, soil injections, trunk injections, lower trunk sprays, or cover sprays on the trunk, branches and foliage (Herms et al., 2019). The systemic insecticide emamectin benzoate, which is applied as a trunk injection, has demonstrated 2-year control against both A. planipennis larvae and leaf-feeding adults (McCullough et al., 2011; Herms et al., 2019).

Trees infested with buprestids can be cut down and then chipped or heat-treated to kill larvae and pupae within the host material (McCullough et al., 2007). However, there are uncertainties about the maximum allowable size of wood chips to guarantee complete mortality of any larvae or pupae present (McCullough et al., 2007; Kopinga et al., 2010; Økland et al., 2012). Additionally, the efficacy of heat-treatment in killing Agrilus larvae and pupae depends on the chamber temperature, the internal wood temperature, and duration of heat (Myers et al., 2009; Goebel et al., 2010; EPPO, 2020).

Several parasitoids of A. anxius  have been documented in North America, including egg parasitoids in the families Aphelinidae and Encyrtidae, and larval parasitoids in the families Braconidae, Chalcididae, Eulophidae, Eurytomidae, and Ichneumonidae (Nash et al., 1951; Barter, 1957; Loerch & Cameron, 1983b; Taylor et al., 2012; Triapitsyn et al., 2015). Although some natural enemies have caused more than 50%  mortality to A. anxius eggs or larvae (Nash et al., 1951; Barter, 1957; Loerch & Cameron, 1983b), there have been no studies on the role that these parasitoids play in the population dynamics of A. anxius in North America. With respect to entomopathogens, Kyei-Poku et al. (2011) reported a microsporidian infecting A. anxius in Ontario that varied greatly in incidence among populations. 

Phytosanitary risk

The wide geographic distribution of A. anxius in North America, from Alaska and Canada to parts of the Southern United States, indicates that A. anxius can tolerate a wide range of climatic conditions, and could probably establish throughout much of the EPPO region. Birch species exist throughout much of Europe and Asia, with some Betula species, such as B. pendula and B. pubescens, being very common in Northern Europe (Beck et al., 2016). For example, in Nordic and Baltic countries, birch species comprise from 11–16% and 17–28%, respectively, of the total volume of growing stock (Hynynen et al., 2010). Considering the high susceptibility of European Betula species to A. anxius, the introduction and establishment of this beetle would be likely to result in widespread mortality of Betula trees in forests, nurseries, and cities throughout Eurasia, with a similar effect to that of the introduction of the Asian buprestid A. planipennis  on ash (Fraxinus) trees in North America (Poland & McCullough, 2006). As evidence of the growing concern that A. anxius could be introduced to Europe there are several recent efforts in Europe to develop contingency plans and survey methods for A. anxius prior to its possible arrival (EFSA et al., 2020; Evans et al., 2020; Petter et al., 2020). 

Suggested phytosanitary measures are specified in the PRA performed by EPPO (EPPO, 2011); they are as follows. Plants for planting (except seeds) of Betula should originate from countries found free from the pest or be of small diameter (<2 cm for plants with stem, <1 cm for scions). Alternatively, they may be grown under insect-proof conditions. Wood chips should originate from countries found free from the pest or undergo heat treatment or fumigation. Betula wood with or without bark and furniture and other objects made of untreated birch wood should originate from countries found free from the pest, or undergo heat treatment or irradiation. Alternatively, outer sapwood should have been removed or wood commodities should be stored in the country of export for an appropriate period (1 year for wood chips, 2 years for wood). Importing during winter and processing some wood commodities (including woodchips) before the next flight period may be authorized under an import permit.

As a general approach, it has also been recommended that when importing plants for planting (except seeds) and wood commodities of Betula from countries where A. anxius occurs, precautions should have been taken to avoid any infestations while the consignments are transported through possibly infested areas (EPPO, 2017).

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Smitley DR, Doccola JJ & Cox DL (2010) Multiple-year protection of ash trees from emerald ash borer with a single trunk injection of emamectin benzoate, and single-year protection with an imidacloprid basal drench. Arboriculture & Urban Forestry 36, 206–211.

Swink WG, Paiero SM & Nalepa CA (2013) Buprestidae collected as prey by the solitary, ground nesting philanthine wasp Cerceris fumipennis (Hymenoptera: Crabronidae) in North Carolina. Annals of the Entomological Society of America 106, 111-116.

Taylor PB, Duan JJ, Fuester RW, Hoddle R & van Driesche R. (2012) Parasitoid guilds of Agrilus woodborers (Coleoptera: Buprestidae): their diversity and potential for use in biological control. Psyche doi:10.1155/2012/813929

Taylor RAJ, Bauer LS, Poland TM & Windell KN (2010) Flight performance of Agrilus planipennis (Coleoptera: Buprestidae) on a flight mill and in free flight. Journal of Insect Behavior 23, 128–148.

Triapitsyn SV, Petrice TR, Gates MW, Bauer LS (2015) Two new species of Oobius Trjapitzin (Hymenoptera, Encyrtidae) egg parasitoids of Agrilus spp. (Coleoptera, Buprestidae) from the USA, including a key and taxonomic notes on other congeneric Nearctic taxa. ZooKeys 498, 29–50. 

This datasheet was originally prepared in 2011 by VL Muilenburg and DA Herms, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH, USA.

The current datasheet was extensively revised and updated where needed in 2020 by Robert A. Haack, USDA Forest Service, Northern Research Station, Lansing, MI, USA (emeritus). His valuable contribution is gratefully acknowledged.

EPPO (2024) Agrilus anxius. EPPO datasheets on pests recommended for regulation. https://gd.eppo.int (accessed 2024-05-01)

This datasheet was first published in the EPPO Bulletin in 2011 and revised in 2020. 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 (2011) Agrilus anxius. Datasheets on pests recommended for regulation. EPPO Bulletin 41(3), 409-413. https://doi.org/10.1111/j.1365-2338.2011.02510.x