North American Xyleborini north of Mexico: a review and key to genera and species (Coleoptera, Curculionidae, Scolytinae)

Abstract Bark and ambrosia beetles (Scolytinae) are the most successful group of invasive wood borers worldwide, and the most invasive among them are species in the tribe Xyleborini. This haplodiploid, highly inbred, fungus-farming group is represented by 30 non-native species in North America, of which at least five are serious pests. The few identification resources for Xyleborini that exist are becoming outdated due to new species arrivals and nomenclatural changes. Here we present a new comprehensive key to Xyleborini currently known from the continental United States. Compared to the previous key, the following species have been added to the North American fauna: Ambrosiodmus minor (Stebbing), Ambrosiophilus nodulosus (Eggers), Anisandrus maiche Kurentsov, Coptoborus pseudotenuis (Schedl), Cyclorhipidion fukiense (Eggers), Dryocoetoides reticulatus Atkinson, Dryoxylon onoharaense (Murayama), Euwallacea interjectus (Blandford), Xyleborinus andrewesi (Blandford), Xyleborinus artestriatus (Eichhoff), Xyleborinus octiesdentatus (Murayama), Xyleborus bispinatus Eichhoff, Xyleborus seriatus Blandford, Xyleborus spinulosus Blandford, and Xylosandrus amputatus (Blandford).


Introduction
Bark and ambrosia beetles (Curculionidae: Scolytinae) are considered one of the most injurious groups of insects in native and planted forests (Raffa et al. 2015). The vast majority breeds in dead or dying tissues and do not have economic impact. However, some species attack living trees, seedlings, or seeds of commercial importance causing severe damage (Raffa et al. 2015). Scolytines are among the most commonly intercepted taxa at United States ports of entry. True bark beetles (phloeophagous species) are intercepted more often than ambrosia-feeding species; however, ambrosia beetles of the tribe Xyleborini represent half of the 60 non-native scolytines established in the United States (Haack and Rabaglia 2013).
The Xyleborini, with 1177 recognized species, is the most species-rich tribe within Scolytinae (Smith and Hulcr 2015). This tribe of ambrosia beetles also includes some of the most abundant and widely distributed species (Rabaglia et al. 2006). The combination of fungus-farming, wide host range, and arrhenotokous inbreeding (haplodiploidy) makes the Xyleborini one of the most successful groups of colonizers in the world (Atkinson et al. 1990, Smith andHulcr 2015).
In the last decade, several exotic species of Xyleborini have successfully established in North America. The detection and control of both native and exotic species relies on a solid understanding of the systematics and identity of species. Since the last review of North American Xyleborini (Rabaglia et al. 2006), 15 additional non-native species have been recorded in North America and several nomenclatural changes have been made. The aim of this article is to review the species of Xyleborini occurring in continental North America, diagnose the new species for the region, and provide illustrated keys to genera and species.

Materials and methods
Specimens examined were from the cryo-preserved collection University of Florida Forest Entomology lab managed by JH (University of Florida, Gainesville, Florida, USA), the Florida State Collection of Arthropods (Gainesville, Florida, USA), and/or collected by the authors during various state, regional, and national surveys. Distribution records are as reported in Wood and Bright (1992), Atkinson (2017), recent publications, and unpublished data from the authors. Diagnostic characters used in the keys and notes are for the identification of genera and species occurring in North America and may not be useful for taxa occurring in other regions. Antennal club types are described as Hulcr et al. (2007). Interstria 1 is defined as the sutural interstria. Table 1 includes the complete list of species of Xyleborini occurring in continental North America.
Synonyms listed for each genus and species are cited from Alonso-Zarazaga and Lyal (2009), Alonso-Zarazaga et al. (2017), Beaver 2011, Bright (2014, and Wood and Bright (1992). References to original descriptions and synonymies are cited from Bright and Rabaglia (1999), Hulcr and Cognato (2009), Bright (1987, 1992), and Wood (1986). The type material collection information and repository correspond to Wood and Bright (1992). Abbreviations for location of type material are: Photographs were taken by JH and DG using an Olympus SZX16 stereomicroscope. Each image is a composite of up to 50 separate images taken with a Canon EOS Rebel T3i camera, and later stacked using the Helicon Focus software (v 6.0, Helicon Soft).

1
Body conspicuously long, 3.5 times as long as wide; protibiae narrow with five large teeth on outer margin; elytral declivity deeply concave and densely pubescent, declivital surface and lateral margins not armed ..........Dryoxylon -Body stout to slender, never 3.5 times as long as wide; protibiae broad and with more than 5 small denticles on the outer margin; elytral declivity usually not concave; if impressed, lateral margins armed with denticles .. Elytra narrowly rounded at apex, sutural apex strongly emarginate (Fig. 7) Notes. Ambrosiodmus lewisi was first reported in North America from southeastern Pennsylvania (Hoebeke 1991). This non-native species is the largest Ambrosiodmus in North America, and can be distinguished from A. minor by the tubercles on declivital interstriae 2, which are distinctly larger than those on other interstriae. Notes. The first collection in North America of A. minor was in Florida in 2011 (Rabaglia and Okins 2011). Similar to A. lewisi but with tubercles on declivital interstriae 2 not distinctly larger than those on other interstriae. Fig. 3 Pityophthorus obliquus LeConte, 1878. Xyleborus gilvipes Blandford, 1898. Synonymy Wood 1975. Ambrosiodmus linderae Hopkins, 1915. Synonymy Bright 1968. Xyleborus brasiliensis Eggers, 1928. Synonymy Wood 1975. Xyleborus mexicanus Eggers, 1931. Synonymy Wood 1972. Xyleborus pseudobrasiliensis Eggers, 1941. Synonymy Bright 1985. Xyleborus illepidus Schedl, 1941. Synonymy Wood 1975. Xyleborus melanarius Schedl, 1978. Synonymy Wood 1989.   Notes. This non-native species, first found in Maryland (Bright 1968), is now well-established and commonly found in the mid-Atlantic and southeastern states. This species is distinguished from other Ambrosiodmus by the combination of the red color, the small size, and the equally granulate declivital interstriae. Species of Ambrosiophilus differ from other members of the tribe by the black and robust body combined with the absence of asperities on a flat pronotal disc, and the rounded edge of elytral declivity. Notes. Ambrosiophilus atratus was first reported in eastern North America from Georgia, Maryland, Tennessee, Virginia and West Virginia (Atkinson et al. 1990). Differs from A. nodulosus by the absence of tubercles on the declivity. Species of Anisandrus differ from other members of the tribe by the combination of serrations on the frontal edge of pronotum, a tuft of setae at the base of the pronotum, the contiguous procoxae, and an obliquely truncate antennal club with the first segment of club covering the entire posterior side.

Notes.
Representing the first non-native scolytine reported in North America (Rabaglia et al. 2006), Anisandrus dispar was likely unintentionally introduced before 1817 (Wood 1977 Notes. Anisandrus maiche was first reported in the US from Pennsylvania, Ohio, and West Virginia (Rabaglia et al. 2009). Similar to A. dispar but smaller. This nonnative species was originally reported from western Pennsylvania and eastern Ohio, but is becoming increasingly common in northeastern states.  Notes. This is the most common species of Anisandrus in the northeastern U.S. Distinguished from other Anisandrus by the absence of significant sculpture on the elytral declivity. Wood (1957) synonymized A. sayi with X. obesus var. minor, but Swaine's name is available and should have priority.

Type species. Cnestus magnus Sampson
Species of Cnestus differ from other members of the tribe by the truncate elytra, which are shorter than the pronotum. Notes. Cnestus mutilatus was first collected in North America from Mississippi in 1999 (Schiefer and Bright 2004). This species is easily distinguished from other Xyleborini by the truncate and short elytra, with a circular declivity delimited by a distinct carina posteriorly and laterally.  Notes. Coptoborus pseudotenuis was first documented in the US based on a reared specimen from southern Florida in 2004 (Atkinson et al. 2010). Common in South America, either introduced or naturally spread to Florida. Distinguished from other Coptoborus by the slightly impressed interstria 2, 1 and 3 with 3-5 small denticles, and by the elevated apical margin of interstriae 1 and 2.

Cyclorhipidion Hagedorn, 1912
Terminalinus Hopkins, 1915. Synonymy Wood and Bright 1992. Kelantanius Nunberg, 1961. Synonymy Wood 1986 Type species. Cyclorhipidion pelliculosum Hagedorn Species of Cyclorhipidion differ from other members of the tribe by being overall pubescent and covered with minute, dense, confused punctures. Notes. This recently detected non-native species is very similar in general appearance to both C. bodoanum and C. pelliculosum except for body length, with an intermediate size (Hoebeke et al. 2018  Notes. Cyclorhipidion pelliculosum was first documented in the US from Pennsylvania in 1987 and from Maryland in 1989 (Atkinson et al. 1990). Distinguished from other Cyclorhipidion in North America by the larger size and the blackish brown color.
Species of Dryocoetoides differ from other members of the tribe by the stick-like protibia, the posterior face of which is rugose. Fig. 9 Type material. Holotype female; United States; NMNH.
Notes. Distinguished from other Dryocoetoides by the clearly indicated punctures in the declivital striae, the uniseriate tubercles in the interstriae, and the dull declivity. Only known from south Florida (Atkinson 2009).
Species of Dryoxylon differ from other members of the tribe by the long body, the not impressed submentum, the narrow protibia with a few large teeth on outer margin, and by the deeply concave elytral declivity.   Notes. This is the only species of the genus. Bright and Rabaglia (1999) placed it in the Dryocoetini based on tibial characters, but molecular analyses place it within the Xyleborini (Jordal et al. 2000, Jordal 2002. Distinguished by the obliquely truncate antennal club, the narrow protibiae with a few large teeth on outer margin, and by the distinctly concave, densely pubescent, and unarmed elytral declivity.
Species of Euwallacea differ from other members of the tribe by the costate and broad posterolateral edge of declivity. In most species the pronotum is subquadrate. Notes. This species is a complex of several distinct genotypes, the most common of which are known as the Tea shot hole borer, Polyphagous shot hole borer, and the Kuroshio shot hole borer (Stouthamer et al. 2017). The different lineages are supported by rapidly evolving mitochondrial genes and more conserved nuclear gene regions. Although these potential different species display morphological differences, reliable morphological diagnosis has not been established (Chen et al. 2016 Notes. The first American occurrence of this species was in Louisiana in 1984, originally confused with E. validus . Specimens from Asia can be larger in size, up to 3.8 mm long, overlapping with E. validus body size.   (Wood 1977) and later from Pennsylvania in 1980 (Wood 1982) and Louisiana in 1984 (Chapin and Oliver 1986). This species is distinguished from E. interjectus in North America by the larger size, the absence of tubercles from the apical half of the interstriae 2, and by uneven and tuberculate declivital costae.
Species of Theoborus differ from other members of the tribe by the light-brown color, the type 3 antennal club, the pointed elytral declivity apex in dorsal view, and the smooth posterior face of protibia.  Notes. It is unclear if this species was introduced from South America or is native to North America. Distinguished by the light-brown color, the short and steep elytral declivity with stout and short interstrial setae, and the smooth posterior face of protibia.
Notes. In the US, X. glabratus was first detected in a survey trap near Port Wentworth, Georgia in 2002 (Rabaglia et al. 2006). The ambrosia fungus vectored by this species is responsible for the death of 300 million bay trees (Persea spp.) and other Lauraceae in the southeastern United States (Hughes et al. 2017). This species is distinguished by the dark color and the glabrous elytral disc and declivity with small granules in all interstriae decreasing in size toward apex. Fig. 16 Xyleborus flohri Schedl, 1972. Synonymy Wood 1977 Type material. Lectotype female; Mexico. IRSNB.

Xyleborus intrusus Blandford, 1898
Distribution. Central America: El Salvador, Guatemala, Honduras; North America: Antilles, Canada: British Columbia, Mexico, United States: Arizona, California, Colorado, District of Columbia, Georgia, Idaho, Maine, Maryland, Mississippi, Montana, New Jersey, New Mexico, North Carolina, Oregon, Pennsylvania, South Carolina, South Dakota, Utah, Virginia, West Virginia. Notes. One of the few species of the genus restricted to conifers. Distinguished from other Xyleborus by the steep declivity which occupies the apical ¼ of the elytra, and broadly rounded posterolateral margin of the declivity. It is distinguished from X. pubescens by the larger declivital denticles and smaller, deeply impressed declivital strial punctures.   (Vandenberg et al. 2000) and in Oregon in 1997-98 (Mudge et al. 2001. Distinguished from X. volvulus by its larger size. Wood and Bright (1992) suggest that this species may be a synonym of X. volvulus.  (Hoebeke and Rabaglia 2008), X. seriatus is distinguished from other Xyleborus by the distinctly impressed area adjacent to the scutellum and the alternating series of longer and shorter setae on the elytra (Hoebeke and Rabaglia 2008). Both X. orientalis kalopanacis Kurenzov and X. orientalis aceris Kurenzov were listed as synonyms of X. orientalis by Wood and Bright (1992). Mandelshtam (2007)  Notes. Commonly known as the black twig borer, X. compactus was first collected in the US at Ft. Lauderdale, Florida in 1941 (Wood 1982). It attacks healthy twigs of living trees and shrubs in the southeastern United States. Distinguished by the small size, the black color, and the shining declivity. Fig. 19 Phloeotrogus crassiusculus Motschulsky, 1866. Xyleborus semiopacus Eichhoff, 1878. Synonymy Wood 1969. Xyleborus semigranosus Blandford, 1896. Synonymy Schedl 1959. Xyleborus ebriosus Niisima, 1909. Synonymy Choo 1983. Dryocoetes bengalensis Stebbing, 1908. Synonymy Beeson 1915. Xyleborus mascarenus Hagedorn, 1908. Synonymy Eggers 1923. Xyleborus okoumeensis Schedl, 1935. Synonymy Schedl 1959. Xyleborus declivigranulatus Schedl, 1936. Synonymy Schedl 1959. Notes. A widely introduced species around the globe, X. crassiusculus has spread in the US along the lower Piedmont region and coastal plain to North Carolina, Louisiana, Florida, and beyond (Atkinson et al. 2012). The first US record is based on a specimen collected in South Carolina in 1974 (Anderson 1974, as Xyleborus semiopacus). Distinguished by the confused declivital granules giving the declivity a dull appearance. Causes economic damage in nurseries and stored hardwood lumber (Smith and Hulcr 2015). Fig. 19 Xyleborus curtulus Eichhoff, 1869. Anisandrus zimmermanni Hopkins, 1915. Synonymy Bright 2014. Xyleborus curtuloides Eggers, 1941. Synonymy Wood 1982. Xyleborus biseriatus Schedl, 1963. Synonymy Wood 1973. Xyleborus strumosus Schedl, 1972. Synonymy Wood 1992 Type material. Holotype female: Brazil; IRSNB. Notes. This species is currently only known from central and southern Florida in the United States. Distinguished by the dark brown body, the small size, and the hairy and shagreened declivity. Notes. Originating from Asia, X. germanus has now spread across much of North America, including the Northeast, South and Southeast, and the Pacific Northwest (Weber and McPherson 1982;LaBonte et al. 2005); it was first thought to have been introduced into the US in a Long Island area greenhouse in 1932 (Felt 1932). Distinguished by the black color and the lack of strial setae on declivity.