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Historical Population Increases and Related Inciting Factors of Agrilus anxius, , and Agrilus granulatus liragus (Coleoptera: ) in the Lake States (Michigan, Minnesota, and Wisconsin) Robert A. Haack and Toby R. Petrice USDA Forest Service, Northern Research Station, 3101 Technology Blvd., Suite F, Lansing, MI 48910 e-mail: [email protected] (emeritus) and [email protected]

Abstract Three native species of tree-infesting Agrilus (Coleoptera: Buprestidae) have regularly reached outbreak levels in the Lake States (Michigan, Minnesota, and Wisconsin), including A. anxius Gory (bronze borer), A. bilineatus (Weber) (twolined borer), and A. granulatus liragus Barter & Brown (bronze poplar borer). The main host trees for these Agrilus are species of Betula for A. anxius, Castanea and Quercus for A. bilineatus, and Populus for A. granulatus liragus. Based on 197 annual forest health reports for Michigan (1950–2017, 66 years), Minnesota (1950–2017, 64 years), and Wisconsin (1951–2017, 67 years), A. bilineatus was the most often reported Agrilus species in all three states (men- tioned in 90 annual reports), with A. anxius second (71 reports) and A. granulatus liragus third (21 reports). Drought was the most commonly reported inciting factor for outbreaks of all three Agrilus species, with defoliation events ranking second. The top two defoliators reported as inciting outbreaks of each species were, in decreasing order, pumila Leach (: ; birch leafminer) tied with Malacosoma disstria Hübner (: Lasiocampidae; forest tent caterpillar) for A. anxius; M. disstria and Alsophila pometaria (Harris) (Lepidoptera: Geometridae; fall cankerworm) for A. bilineatus; and M. disstria and Choristoneura conflictana (Walker) (Lepidoptera: ; large aspen tortrix) for A. granulatus liragus. Other environmental factors occasionally listed as inciting Agrilus outbreaks included late spring frosts, ice storms, and strong wind events. Keywords: Jewel , flatheaded borers, aspen, birch, , environmental stress, outbreak

The Agrilus (Coleoptera: Bu- with the most significant difference being prestidae) is considered the most speciose their larval host plants: A. anxius on Betula in the Kingdom with over 3200 (birch), A. bilineatus on Castanea (chestnut) recognized species worldwide as of April and Quercus (oak), and A. granulatus liragus 2019 (Jendek and Poláková 2014; E. Jendek, on Populus (aspen, cottonwood and poplar) pers. comm.). The continental United States (Solomon 1995). Each species is known to is known to have at least 194 recognized infest overmature trees as well as trees Agrilus species and subspecies, of which 13 stressed by drought, defoliation, and other species are exotic to the USA (Chamorro et factors (Dunbar and Stephens 1976, Dunn al. 2015; Hoebeke et al. 2017, DiGirolomo et al. 1986, Millers et al. 1989, Haack and et al. 2019). In the Lake States [a collective Acciavatti 1992, Solomon 1995, Muilenburg term for Michigan (MI), Minnesota (MN), and Herms 2012, Haack and Petrice 2020). and Wisconsin (WI)] there are at least 60 Several life-history studies have been known Agrilus species, of which 4 are exotic conducted on A. anxius, A. bilineatus, and A. (Wellso et al. 1976, Jendek 2013a, 2014). granulatus liragus in eastern North Amer- Among the native tree-infesting Agri- ica (Balch and Prebble 1940, Barter and lus, there are three species that regularly Brown 1949, Barter 1957, 1965, Carlson and reach outbreak levels in the Lake States: Knight 1969, Cote and Allen 1980, Haack Agrilus anxius Gory (), A. and Benjamin 1982, Loerch and Cameron bilineatus (Weber) (twolined chestnut borer), 1984, Muilenburg and Herms 2012). Their and A. granulatus liragus Barter & Brown life cycle is generally completed in one year, (bronze poplar borer) (Millers et al. 1989). but at times two years are needed, especially They are similar in size (adults are about when summers are cool or when eggs are 7–11 mm long) and have similar life histories laid on vigorous host trees or laid during

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late summer. In the Lake States, or other Since the discovery of the Asian species areas of similar latitude, adult emergence Agrilus planipennis Fairmaire (emerald of these three species usually starts in late ash borer) in North America in 2002 and in May or early June, peaks in late June, and European Russia in 2005 (Haack et al. 2002, then diminishes through July and August. 2015), there has been growing concern in Adults feed on host foliage for several days to Europe, as well as in other countries, that become sexually mature and then mate and various exotic species of Agrilus could enter oviposit in bark cracks and crevices along and greatly impact European urban and the major branches and trunks of host trees. forest trees (Flø et al. 2015). For example, as Eggs are laid singly or in small clusters. of April 2019, EPPO (European and Mediter- Upon eclosion, larvae tunnel through the ranean Plant Protection Organization) has bark and feed in the cambial region, con- conducted formal risk analyses (PRAs) structing zig-zag galleries that score both the for four Agrilus species, including A. anxius inner bark (phloem) and outermost sapwood in 2010 (EPPO 2011), A. planipennis in 2013 (xylem). There are four larval instars and (EPPO 2013), A. bilineatus in 2018 (EPPO larvae often enter the outer sapwood to molt. 2019a), and Agrilus fleischeri Obenberger in In late summer and autumn, mature last-in- 2018 (EPPO 2019b). We were team members star larvae construct individual pupal cells of the Expert Working Groups that conduct- in the outer sapwood on thin-barked trees, ed the above four Agrilus PRAs: RAH for A. which is common in Betula and Populus, or anxius and A. planipennis and TRP for A. in the outer bark on trees with thick bark, bilineatus and A. fleischeri. During the PRAs which is common in Castanea and Quercus. for A. anxius and A. bilineatus, we provided Pupation occurs in late spring and early the team members of the Expert Working summer. Newly formed adults exit through Groups with details on the outbreak history the bark by creating D-shaped exit holes that of these two species in the Lake States, and are characteristic for the genus. The sex ratio in turn the team members encouraged us to of emerging adults is about 1:1. summarize these data into a formal publica- tion. In addition, the recent discovery of A. Over the past several decades many bilineatus in Turkey (Hızal and Arslangün- changes have occurred in the taxonomic doğdu 2018), has further increased interest status of these three Agrilus species. Agri- in A. bilineatus and its potential threat lus anxius was initially described by Gory to European Castanea and Quercus trees (1841), and included what we now refer to as (EPPO 2019a, Haack and Petrice 2020). Giv- A. granulatus liragus. Over a century later, en the above, we reviewed several decades Barter and Brown (1949) named Agrilus of annual forest pest reports from the Lake liragus as a new species, separating it from States and recorded the number of times A. anxius based on color, male genitalia, and each native Agrilus species was mentioned larval host plants. Carlson and Knight (1969) as reaching pest status, as well as any biotic reevaluated the Agrilus anxius complex and and abiotic factors that could have incited reclassified A. liragus as a subspecies of A. the outbreaks. granulatus. Later, Bright (1987) recognized A. liragus as a distinct species, then Nel- Materials and Methods son et al. (2008) once again recognized the subspecies A. granulatus liragus. Although We reviewed all annual forest pest both combinations have appeared in recent reports that we could locate from Michigan scientific literature, we use A. granulatus (1950–2017, 66 reports, missing 1951 and liragus in the present paper. Agrilus bilin- 1973), Minnesota (1950–2017, 64 reports, eatus was first described in 1801 under the missing 1956, 1963, 1967, and 1973), and name Buprestis bilineata Weber (Fisher Wisconsin (1951–2017, 67 reports). Formal 1928). For many years, two subspecies of forest pest surveys, often involving aerial A. bilineatus were recognized based on surveys, ground surveys, and on-site visits in their larval hosts and subtle morphological response to calls from foresters and the pub- differences, with A. bilineatus bilineatus lic, have been conducted in Wisconsin since larvae feeding in Castanea and Quercus, and 1949, and in Michigan and Minnesota since larvae of A. bilineatus carpini Knull, feeding 1950 (WI CD 1953). Therefore, our dataset in Carpinus (hornbeam), Fagus (), and represents nearly all published forest pest Ostrya (hophornbeam) ( Knull 1923). This reports for these three US states. Moreover, latter subspecies was later elevated to spe- in 1951, forest health staff from the Lake cies status under the name Agrilus carpini States met in Madison, WI, to coordinate Knull (Nelson and Hespenheide 1998). Given their reporting and survey methods for for- the above history, it is understandable that est pests of mutual concern (WI CD 1953), there has been some confusion in the litera- therefore we feel comfortable comparing ture on the actual larval hosts of these three infestation records across the Lake States. Agrilus species. We located most reports in our USDA Forest

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Table 1. Number of reports (and percent of the total reports) by state where Agrilus anxi- us, A. bilineatus or A. granulatus liragus were mentioned as being pests in the annual forest health reports published by the Departments of Natural Resources in Michigan (MI; 1950–2017), Minnesota (MN; 1950–2017), and Wisconsin (WI; 1951–2017). State MI (66 reports) MN (64 reports) WI (67 reports) Agrilus anxius 11 (17 %) 33 (52 %) 27 (40 %) Agrilus bilineatus 16 (24 %) 34 (53 %) 40 (60 %) Agrilus granulatus liragus 7 (11 %) 11 (17 %) 3 (4 %)

Service library on the Michigan State Uni- Given that populations of many native versity campus, where our Insect Research Agrilus species increase when host trees are Unit has been located since 1956 (Haack weakened by various inciting factors such 2006). For any missing years, we contacted as drought and defoliation (Millers et al. the individual states, and in most cases they 1989, Solomon 1995), we also recorded any had copies available. Many of the reports mention in the reports of the possible inciting since the 1990s are now online for the Lake factors that could have triggered the Agrilus States as well as all other US states (FHP outbreaks. We recognize that changes in 2018). Although the structure of state gov- staffing, funding, and priorities have taken ernment has changed over time in the Lake place in each DNR Forest Health Unit in the States, these reports were typically prepared Lake States, but feel confident that the major by the Forest Health staff within each state’s forest pests were recorded each year and Department of Natural Resources (DNR). therefore the annual forest health reports The titles of these DNR reports changed over represent a good approximation of changes the decades, usually starting as Forest Pest in Agrilus populations over time. Reports in the 1950s and 1960s, changing to Forest Insect and Disease Reports in the Results 1970s and 1980s, and then to Forest Health Reports in the 1990s to the present. Agrilus anxius, A. bilineatus, and A. granulatus liragus were the only three na- When reviewing each report, we looked tive Agrilus species that were reported mul- for any mention of Agrilus beetles, either by tiple times as forest pests in the Lake States. scientific name or common name. We concen- Agrilus bilineatus was reported most often trated on native Agrilus species, but after in all three states, being mentioned in 90 of discovery of the exotic species A. planipennis the 197 annual reports (16 MI, 34 MN, and in each state (2002 in MI, 2008 in WI, 2009 in 40 WI reports; Table 1). Agrilus anxius was MN), A. planipennis was mentioned in every the next most frequently reported species, subsequent annual report. For each mention being mentioned in 71 reports (11 MI, 33 of a native Agrilus species, we recorded the MN, and 27 WI reports). Agrilus granulatus year of the report, where in the state the liragus was mentioned in 21 annual reports species reached pest status, and information (7 MI, 11 MN, and 3 WI reports). Based on all on the severity of the infestation. 197 reports, A. anxius was first reported in As a simple means to visualize the in- 1951 in Minnesota, and A. bilineatus and A. festation levels for each species over time, we granulatus liragus were both first reported assigned a value of 1 to infestations ranked in Wisconsin in 1966 and 1977, respectively. low and a value of 2 to infestations ranked Various weather-related phenomena moderate to severe by year and state. The and several defoliators were listed as sus- ranking of “low” was given when the descrip- pected inciting factors that could have weak- tion of the infestation was described in terms ened trees and thereby led to population of being local, scarce, light, spotty, scattered, increases of A. anxius, A. bilineatus, and A. etc. By contrast, a ranking of “moderate granulatus liragus in the Lake States (Table to severe” was given to infestations that 2). Inciting factors were presented for 72% of were described as abundant, widespread or the 182 listings of when these three Agrilus statewide, and usually causing severe tree species reached reportable levels (62% of the dieback or mortality. On a few occasions, 71 A. anxius listings, 74% of 90 A. bilineatus however, a ranking of low was given to situ- listings, and 95% of 21 A. granulatus liragus ations where infestations occurred statewide listings). Drought was the most commonly but were restricted to urban situations, such reported inciting factor for all three Agrilus as when A. anxius infested primarily orna- species combined (listed 119 times), as well mental birch trees. as individually for A. anxius (44 times), A.

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Table 2. Frequency (number of annual reports by state) of various inciting factors that were associated with population increases of Agrilus anxius, A. bilineatus and A. granulatus liragus in Michigan (MI; 66 reports during 1950–2017), Minnesota (MN; 64 reports during 1950–2017), and Wisconsin (WI; 67 reports during 1951–2017) based on each state’s pub- lished annual forest health reports. State Inciting factor by Agrilus species MI MN WI (including defoliator species, family, and common name) (66 yr) (64 Yr) (67 yr) Agrilus anxius, bronze birch borer Drought 10 18 16 Late spring frost 1 – – Hymenoptera Fenusa pumila Leach, Tenthredinidae, birch leafminer – 4 1 Lepidoptera Bucculatrix canadensisella Chambers, , birch skeletonizer – 1 – Malacosoma disstria Hübner, Lasiocampidae, forest tent caterpillar – 5 –

Agrilus bilineatus, twolined chestnut borer Drought 16 19 23 Hail or ice storm – – 2 Late spring frost – – 2 Strong wind event – 1 1 Dendrotettix quercus Packard, , post–oak locust – – 4 Lepidoptera Acleris semipurpurana (Kearfott), Tortricidae, oak leaftier – – 2 Alsophila pometaria (Harris), Geometridae, fall cankerworm – 3 9 argyrospila (Walker), Tortricidae, fruittree leafroller – – 1 (Walker), Tortricidae, oak leafroller 5 – – Bucculatrix ainsliella Murtfeldt, Bucculatricidae, oak skeletonizer – – 1 Erannis tiliaria (Harris), Geometridae, linden looper – 3 – Lochmaeus manteo Doubleday, , variable oakleaf caterpillar – – 2 Lymantria dispar (L), Erebidae, gypsy 1 – 1 Malacosoma disstria Hübner, Lasiocampidae, forest tent caterpillar 2 8 6 canicosta Franclemont, Notodontidae, redhumped oakworm – – 1 Franclemont, Notodontidae, orangehumped mapleworm – – 1 Phasmida Diapheromera femorata (Say), Diapheromeridae, northern walkingstick – – 3

Agrilus granulatus liragus, bronze poplar borer Drought 7 8 2 Lepidoptera Choristoneura conflictana (Walker), Tortricidae, large aspen tortrix 4 – 1 Malacosoma disstria Hübner, Lasiocampidae, forest tent caterpillar 4 7 1

bilineatus (58 times), and A. granulatus The greatest diversity of defoliators liragus (17 times; Table 2). Other weather listed as inciting factors for population events listed as inciting factors for popula- increases of the three Agrilus species was associated with A. bilineatus (13 defoliator tion increases of these Agrilus (mostly for A. species, representing 8 families in 3 orders), bilineatus) included late spring frosts, hail, followed by A. anxius (3 defoliators in 3 ice storms, and strong wind events (Table 2). families and 2 orders), and A. granulatus Several of the reports also mentioned tree liragus (2 defoliators in 2 families in 1 order; age (i.e., overmaturity) as well as sandy soils Table 2). The top two defoliators mentioned as inciting factors for each Agrilus species and shallow soils as predisposing factors that were, in decreasing order, Fenusa pumila increased tree vulnerability to Agrilus infes- Leach [formerly F. pusilla (Lepeletier)] and tation, especially during periods of drought. Malacosoma disstria Hübner (both tied) for

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Figure 1. Stacked bar graph (within years) showing the cumulative severity rank- ings (0–2 for each state by year) of Agrilus anxius, A. bilineatus, and A. granulatus liragus infestations in Michigan, Minnesota, and Wisconsin during 1968–2017 based on annual forest pest reports from each state. A value of 0 signifies that the insect was not reported as a pest, 1 represents an infestation ranked low, and 2 represents an infestation ranked moderate to severe within each state by year. See text for more details.

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A. anxius; Alsophila pometaria (Harris) and Discussion M. disstria for A. bilineatus; and M. disstria and Choristoneura conflictana (Walker) for It is not surprising that A. anxius, A. A. granulatus liragus. The insect order, bilineatus, and A. granulatus liragus were family and common name for each defoliator the most commonly reported Agrilus species in the Lake States, given that their respec- are listed in Table 2. Malacosoma disstria tive hosts, Betula, Populus and Quercus, are was the only defoliator listed as an inciting among the most common hardwood trees factor for all three Agrilus species (Table 2). (i.e., broadleaf trees, dicots) in the region The historic timeline of A. anxius, A. (MN DNR 2017, Pugh et al. 2017, WI DNR bilineatus, and A. granulatus liragus reach- 2018), and that these three Agrilus species ing pest status in the Lake States is depicted are the most damaging Agrilus species that for the 50-year period during 1968–2017 in infest these host trees in the Lake States Fig. 1. For the years not shown in Fig. 1 (Millers et al. 1989, Solomon 1995). As back- (1950–1967), there were no reports for any of ground, consider that the land areas of the Lake States are heavily forested (56% of MI, the three Agrilus species in Michigan, six re- 32% of MN, and 49% of WI), and that hard- ports for A. anxius in Minnesota (1951, 1955, wood forest types dominate the forestland in 1958–59, 1961, and 1964), and eight reports each state (73% in MI, 69% in MN, and 80% for A. anxius (1953, 1959–62, and 1965–67) in WI) (MN DNR 2017, Pugh et al. 2017, WI and two reports for A. bilineatus (1966–67) DNR 2018). The aspen-birch forest type is in Wisconsin. Agrilus anxius was reported the most common forest type in Minnesota, as a pest in all three states in the same it ranks second in Michigan and third in year only twice, in 1968 and 1970 (incited Wisconsin. By contrast, the oak-dominated by drought and late frost), and only once for forest types rank first in Wisconsin, second A. granulatus liragus in 2008 (incited by in Minnesota, and third in Michigan. The drought and C. conflictana and M. disstria most common forest type in Michigan is the defoliation; Fig. 1). By contrast, there were sugar /beech/yellow birch type (Pugh 12 years when A. bilineatus was reported as et al. 2017). a pest in all three states: 1978–80, 1988–91, There are also many conifers (e.g., 1993, 2004, 2007, 2009, and 2013; usually softwood trees, gymnosperms) in the Lake with drought and various combinations States, but none serve as larval hosts for of defoliators listed as the inciting agents any Agrilus species in this region (Jendek (Fig. 1). Moreover, during the 3-yr period and Poláková 2014). In fact, the only Agrilus 1988–1990, A. bilineatus infestations were species worldwide to be reared from a coni- reported as moderate to severe in all three fer host is A. schwerdtfegeri Schwerdtfeger, states, with drought and defoliation listed as which emerged from a dead branch of Pinus the main inciting factors (Fig. 1). maximinoi Moore (= P. tenuifolia Bentham) in Guatemala (Jendek 2013b). Four additional native Agrilus spe- The relationship of defoliation and cies were mentioned in the 197 reports we drought with population increases of A. reviewed and all in Wisconsin, including A. anxius, A. bilineatus, and A. granulatus li- otiosus Say, which was reared from dying ragus in the Lake States (Table 2), has been (Carya) trees that were also infested documented for many other Agrilus species with the bark Scolytus quadrispinosus worldwide (Ohgushi 1978, Vansteenkiste et Say (Curculionidae: Scolytinae) and the can- al. 2004, Sever et al. 2012, Sallé et al. 2014, ker fungus Ceratocystis smalleyii Johnson Chamorro et al. 2015). Tree responses to de- and Harrington (WI DNR 2005). The other foliation and drought can be highly variable, three Agrilus species were A. arcuatus (Say), depending on factors such as seasonality of A. cliftoni Knull, and A. transimpressus the stress event (early summer vs. late sum- Fall, all of which were reared in 2012 from mer), severity (mild vs. severe), and duration dead and dying branches of declining black (one year vs. multi-year) (Kulman 1971, walnut trees ( nigra L.) (WI DNR Kozlowski et al. 1991). Some typical early 2012; Andrea Diss-Torrance and Michael responses to defoliation include a reduction Hillstrom, pers. comm.). Two of these three in tree carbon balance, fine root growth, and water uptake, followed by mobilization walnut-infesting species (A. cliftoni and A. of stored reserves to develop and expand transimpressus) were recognized recently as replacement foliage, which often reduces new state records for Wisconsin (Hoftiezer subsequent stem growth and concentrations 2011). Collections of the above hickory- and of various defensive compounds present in walnut-infesting Agrilus species resulted stem tissues (Kulman 1971, Wright et al. from targeted surveys of declining hickory 1979, Ericsson et al. 1980, Heichel and Turn- and walnut stands in Wisconsin (WI DNR er 1983, Herms and Mattson 1992, Wargo 2005, 2012). 1996, Krokene 2015). Similarly, the response

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of phytophagous to drought-stressed attack (Haack and Benjamin 1982, Haack trees can vary widely by feeding guild, with et al. 1983, Petrice and Haack 2014). By borers usually being favored by drought contrast, the first appearance of wilting (Mattson et al. 1988, Larsson 1989, Huberty foliage and dieback on birch and aspen, and Denno 2004, Rouault et al. 2006, Haa- which have diffuse-porous xylem, usually vik et al. 2015, Showalter et al. 2018). For requires multiple years of infestation by example, severe drought can reduce a tree’s A. anxius and A. granulatus liragus before ability to develop callus tissue, which can enough annual rings of the outer conducting engulf and kill young wood-boring larvae xylem have been effectively girdled to reduce such as Agrilus larvae (Sallé et al. 2014). translocation and cause dieback (Barter The greater frequency of A. bilineatus 1957, 1965, Solomon 1995, Muilenburg and outbreaks in the Lake States as compared Herms 2012). Moreover, given that dieback with A. anxius and A. granulatus liragus is more gradual in birch and aspen, infesta- (Table 1, Fig. 1) may reflect differences in tion can occur throughout the entire tree as xylem structure of their host trees, with A. well as in the same area of a tree for several bilineatus infesting Quercus with ring-po- consecutive years until that portion of the rous xylem, while A. anxius infests Betula tree dies (Loerch and Cameron 1984). As and A. granulatus liragus infests Populus, an example of the difference in timing of which both have diffuse-porous xylem. This crown dieback in response to a stress event, is an important difference, given that water consider the widespread severe drought that moves primarily in the outermost annual occurred in 1988 throughout the Lake States ring of xylem in ring-porous trees, compared (Trenberth et al. 1988, Haack and Mattson with several annual rings in the outermost 1989, Jones et al. 1993), with widespread oak sapwood in diffuse-porous trees (Kozlowski mortality reported in all three Lake States 1961, Wiant and Walker 1961, Kozlowski in 1988 and continuing through to 1991 (Fig. and Winget 1963). This difference also helps 1), compared with fewer and more delayed explain why ring-porous trees are more infestations reported for A. anxius or A. vulnerable to girdling insects like Agrilus granulatus liragus (Fig. 1). larvae as well as pathogens that invade the In recent years, most aerial surveys outer xylem and cause wilt diseases such as for forest pests in the Lake States occur in chestnut blight, Dutch elm disease, and oak early summer, which enhances detection wilt (Zimmermann and McDonough 1978). of current-year, early-season defoliators. As an example consider the study in Wis- However, given that foliar wilting and dis- consin by Haack and Benjamin (1982) where coloration of Agrilus-infested trees usually the current-year annual ring of xylem along does not occur until late summer, this prac- the main trunk of mature red (Q. rubra L.) tice would usually lead to an undercount of and black (Q. velutina Lam.) measured the number of areas infested with species of 0.8–1.8 mm in width, whereas the average Agrilus, and therefore the outbreak history width (measured at the widest point between depicted in Fig. 1 should be considered as the dorsal and ventral surfaces of the en- an underestimate of the actual number of larged prothorax, Chamorro et al. 2015) of Agrilus infestations that took place in the third instar A. bilineatus larvae measured Lake States. Another difference between 0.9 mm and fourth (last) instars measured ring-porous and diffuse-porous trees that 1.3 mm, indicating that late-instar A. bilin- can influence the results of early-season eatus larvae could easily girdle the outermost aerial surveys is that ring-porous trees tend annual ring of xylem in many host trees. to leaf out later than diffuse-porous trees in Differences in xylem structure also any given area (Panchen et al. 2014). This influence the within-tree attack pattern occurs because in ring-porous trees, cur- of Agrilus species as well as the ease in rent-year earlywood xylem, which contains detecting infested trees. For example, in mostly large-diameter vessels that transport ring-porous trees, once the xylem tissue of a the bulk of the water, is produced before portion of a branch or the trunk is completely budburst, whereas in diffuse-porous trees, girdled, all foliage above the girdled area most current-year xylem is produced after usually wilts and dies that same year. For leaf elongation (Umebayashi et al. 2008, A. bilineatus, this usually happens in late Takahashi et al. 2013, Foster 2017). summer when most larvae are last instars Nonetheless, even in situations where and their feeding galleries are sufficiently late-summer aerial surveys are conducted, deep to girdle the outer annual-ring of xy- it would be easiest to detect first-season lem (Haack and Benjamin 1982, Haack and infestations of A. bilineatus because foliage Acciavatti 1992). Since A. bilineatus females will wilt and discolor during the first year apparently lay eggs only on live portions of of attack if the infested portion of the tree a host tree, the area of current-year infes- is completely girdled. By contrast, Agri- tation moves downward from the crown to lus-infested birch and aspen usually require the lower trunk in each subsequent year of multiple years of infestation before showing

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dieback and if infestations only occur for listed in Table 2, only two are exotic to North one or two years the trees may callus-over America (F. pumila and Lymantria dispar old galleries and recover (Balch and Prebble (Linnaeus)), and both are far less outbreak 1940, Anderson 1944, Barter 1957, 1965). prone today than in the past as a result of Given this situation, it is likely that Agrilus introduced natural enemies: mostly parasit- infestations of birch and aspen occur more oids for F. pumila (Kirichenko et al. 2019), often than depicted in Fig. 1. and a fungus and virus for L. dispar (Solter Many species of Agrilus, as well as and Hajek 2009). In addition, all of the defo- other borers, preferentially infest overma- liators listed in Table 2 initiate larval feeding ture trees, especially during periods of stress in early summer, with the exception of the (Balch and Prebble 1940, Kozlowski 1969, two Symmerista species, which are late-sea- Dunbar and Stephens 1976, Solomon 1995, son defoliators (Drooz 1985). Early-season Williams et al. 2013, Brown et al. 2015). defoliation typically reduces same-year tree Such a relationship, along with the forest growth more than late-season defoliation history of the Lake States, is important to because trees often use stored reserves to consider when viewing the pattern of Agrilus refoliate after early-season defoliation, but outbreaks depicted in Fig. 1. Consider that seldom refoliate after late-season defoliation most of the virgin forests in the Lake States (Kulman 1971, Ericsson et al. 1980). Howev- were logged during the late 1800s and early er, severe late-season defoliation can have a 1900s, with many large-scale forest fires greater impact on stem growth the following soon following (Stearns 1997, Dickmann year, compared with early season defoliation and Leefers 2003). Much of the cut-over land (Mattson et al. 1988). With respect to Agrilus was soon abandoned, or farmed for short adult activity, early-season defoliation would periods of time and then abandoned. Many usually occur prior to peak Agrilus oviposi- of these degraded lands were then colonized tion, whereas late-season defoliation would by “pioneer” tree species, such as aspen (P. usually occur after most Agrilus oviposition grandidentata Michx. and P. tremuloides had ended for the year. Outbreaks of many Michx.) and paper birch (B. papyrifera defoliators are also favored during periods of Marshall), which are short-lived trees that drought (Mattson and Haack 1987, Millers reach physiological maturity at 50-70 years et al. 1989), and drought plus defoliation (Burns and Honkala 1990). Although some would likely even more significantly weak- oaks in the Lake States are relatively short- en trees, which would further increase tree lived (Q. ellipsoidalis E.J. Hill), most oaks susceptibility to borer infestation (Thomas are moderate to long-lived species (Loehle et al. 2002). 1988, Burns and Honkala 1990, Barnes and Now that A. bilineatus has become Wagner 2004). Forest surveys conducted in established in Turkey (Hızal and Arslangün- the Lake States in the early 1990s indicated doğdu 2018, EPPO 2019a), it is difficult to a skewed distribution with a large “wave” predict how damaging this species will be to of forest stands then 55–75 years old (Stone European chestnut and oak trees. Drought 1997). More recent forest surveys in the Lake and widespread defoliation of hardwood States (2014 for MI, 2016 for MN, and 2015 trees are also common in Europe (Gibbs for WI) indicate sharp reductions in aspen and Greiggi 1997, Moraal and Hilszczanski and birch acreage, especially in older age 2000, Thomas et al. 2002, Sallé et al. 2014, classes, compared with increases in acreage Tiberi et al. 2016) and will likely make Eu- of oak-dominated forests, especially in older ropean host trees susceptible to A. bilineatus age classes (Pugh et al. 2017, MN DNR 2017, attack. However, throughout Europe there WI DNR 2018). Such shifts in the species are several native species of Agrilus that composition and age structure of forests in utilize chestnut and oak trees as larval hosts the Lake States may explain, in part, the (Jendek and Poláková 2014). Among these, decline in A. anxius outbreaks in recent A. biguttatus Fabricius is considered the years, the recent spike in the early 2000s of most destructive, especially on oaks, which A. granulatus liragus activity, and the near also commonly reaches outbreak levels in steady activity of A. bilineatus over the past response to defoliation and drought (Moraal several decades (Fig. 1). and Hilszczanski 2000, Sallé et al. 2014). The defoliators listed in Table 2 are Therefore, if European host trees are not common throughout the Lake States as well highly susceptible to A. bilineatus, then A. as in much of eastern North America, and a bilineatus will likely encounter high levels few also occur in the West (e.g., C. conflicta- of competition from native European Agrilus na, F. pumila, and M. disstria; Drooz 1985). for hosts and consequently A. bilineatus may At times, outbreaks of C. conflictanaand M. only become a minor pest in Europe. On disstria cover millions of hectares and can the other hand, if some European chestnut continue for multiple years before subsiding and oak species are highly susceptible to A. (Prentice 1955, Drooz 1985, Ciesla and Kruse bilineatus infestation, such as was the case 2009, Schowalter 2017). Of the defoliators when European L. trees were

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planted in Michigan (Haack 1986, Haack allied species (Coleoptera: Buprestidae). The and Petrice 2020), then A. bilineatus could Canadian Entomologist 81: 245–249. become a major pest in Europe. Nonetheless, Bright, D. E. 1987. The metallic wood-boring given that drought is predicted to increase beetles of Canada and Alaska: Coleoptera: in frequency and severity in the future, out- Buprestidae. The insects and arachnids of breaks of Agrilus species and many other Canada, Part 15. Publication 1810. Agricul- forest insects are expected to become more ture Canada, Ottawa. common in the United States and worldwide (Allen et al. 2010, Kolb et al. 2016). Brown, N., D. J. G. Inward, M. Jeger, and S. Denman. 2015. A review of Agrilus bigut- tatus in UK forests and its relationship with Acknowledgments acute oak decline. Forestry 88: 53–63. The authors thank the many forest Burns, R. M. and B. H. Honkala (eds.). 1990. health staff of the Departments of Natural Silvics of North America: Volume 2. Hard- Resources in Michigan, Minnesota, and woods. Agriculture Handbook 654. USDA Wisconsin for preparing the annual forest Forest Service, Washington, DC. pest reports for the past several decades; Carlson, R. W. and F. B. Knight. 1969. Biology, Val Cervenka for supplying many of the , and evolution of four sympatric early Minnesota forest pest reports; Andrea Agrilus beetles. Contributions of the Ameri- Diss-Torrance, Michael Hillstrom, Eduard can Entomological Institute 4(3): 1–105. Jendek, and Daniel Young for providing personal communications and unpublished Chamorro, M. L., E. Jendek, R. A. Haack, T. data, and Daniel Herms, Brian Schwingle, R. Petrice, N. E. Woodley, A. S. Konstan- Richard Westcott and two anonymous re- tinov, M. G. Volkovitsh, X. K. Yang, V. viewers for commenting on an earlier version V. Grebennikov, and S. W. Lingafelter. of this paper. 2015. Illustrated guide to the Agrilus planipennis Fairmaire and related species (Coleoptera, Buprestidae). Literature Cited Pensoft, Sofia, Bulgaria. Allen, C. D., A. K. Macalady, H. Chenchouni, Ciesla, W. M. and J. J. Kruse. 2009. Large aspen D. Bachelet, N. McDowell, M. Vennet- tortrix. Forest Insect & Disease Leaflet 139. ier, T. Kitzberger, A. Rigling, D. D. USDA Forest Service, Portland, OR. Breshears, E. H. Hogg, P. Gonzalez, R. Cote, W. A. and D. C. Allen. 1980. Biology of Fensham, Z. Zhang, J. Castro, N. Demi- two-lined chestnut borer, Agrilus bilineatus, dova, J.-H. Lim, G. Allard, S. W. Running, in . Annals of the Entomological A. Semerci, and N. Cobb. 2010. A global Society of America 73: 409–413. overview of drought and heat-induced tree mortality reveals emerging climate change Dickmann, D. I. and L. A. Leefers. 2003. The risks for forests. Forest Ecology and Man- forests of Michigan. University of Michigan agement 259: 660–684. Press, Ann Arbor, MI. Anderson, R. F. 1944. The relation between host DiGirolomo, M. F., E. Jendek, V. V. Greben- condition and attacks by the bronze birch nikov, and O. Nakládal. 2019. First North borer. Journal of Economic Entomology 37: American record of an unnamed West Pa- 588–596. laearctic Agrilus (Coleoptera: Buprestidae) infesting European beech () Balch, R. E. and J. S. Prebble. 1940. The bronze in City, USA. European Journal birch borer and its relation to the dying of of Entomology 116: 244–252. birch in New Brunswick forests. The Forestry Chronicle 16: 179–201. Dunbar, D. M. and G. R. Stephens. 1976. The bionomics of the two-lined chestnut borer, Barnes, B. V. and W. H. Wagner Jr. 2004. pp. 73–83. In J. F. Anderson and H. K. Kaya Michigan trees: a guide to the trees of the (eds.), Perspectives in forest entomology. Great Lakes region. University of Michigan Academic Press, New York. Press, Ann Arbor, MI. Dunn, J. P., T. W. Kimmerer, and G. L. Nor- Barter, G. W. 1957. Studies of the bronze birch din. 1986. The role of host tree condition in borer, Agrilus anxius Gory, in New Bruns- attack of white oaks by the twolined chestnut wick. The Canadian Entomologist 89: 12–36. borer, Agrilus bilineatus (Weber) (Coleoptera: Barter, G. W. 1965. Survival and development Buprestidae). Oecologia 70: 596–600. of the bronze poplar borer, Agrilus liragus Drooz, A. T. (ed.), 1985. Insects of eastern for- Barter and Brown (Coleoptera: Buprestidae). ests. Miscellaneous Publication 1426. USDA The Canadian Entomologist 97: 1063–1068. Forest Service, Washington, DC. Barter, G. W. and W. J. Brown. 1949. On the EPPO (European and Mediterranean Plant identity of Agrilus anxius Gory and some Protection Organization). 2011. Pest risk

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