3 Exotic Bark and Ambrosia in the USA: Potential and Current Invaders

Robert A. Haack1 and Robert J. Rabaglia2 1USDA Forest Service, Northern Research Station, 1407 S Harrison Road, East Lansing, Michigan 48823, USA; 2USDA Forest Service, Forest Health Protection, 1601 N Kent Street, RPC–7, Arlington, Virginia 22209, USA

3.1 Introduction Ambrosia ­ adults and larvae cultivate and feed on symbiotic ambrosia fungi that grow in Bark and ambrosia beetles (Coleoptera: the galleries (xylomycetophagous). Most scoly- : Scolytinae) are among the most tine in tropical regions exhibit the important affecting trees and forests ambrosial habit, while most scolytines in tem- worldwide. There are approximately 6000 scoly- perate forests are true bark beetles. There are tine species worldwide, with species found on all also a number of ­species that breed in seeds, continents except Antarctica (Table 3.1) (Wood cones, roots of woody plants, and stems and and Bright, 1992; Bright and Skidmore, 1997, roots of non-woody plants (Wood, 1982; 2002; Wood, 2007). The majority of species are Sauvard, 2004). found in the tropics, but many also occur in boreal Most species of bark and ambrosia beetles forests. Undoubtedly, there are hundreds of addi- live in injured, weakened or dying woody plants, tional species that have not yet been described. and are often among the first insects to colonize Many authorities now consider the bark and such host material (Haack and Slansky, 1987; ambrosia beetles a subfamily (Scolytinae) of Sauvard, 2004). A few species aggressively the weevil family (Curculionidae) (Alonso- attack healthy trees, and during outbreaks cause Zarazaga and Lyal, 2009), while others continue extensive mortality of their host trees. Efficient to treat them as a distinct family (Wood, 2007). host location is important, and is often medi- In this chapter, we will use the subfamily rank- ated by olfactory responses to host odors, tree ing Scolytinae, but recognize that most plant degradation products, or conspecific pherom- protection agencies worldwide continue to use ones (Byers, 2004). Pheromones are used to Scolytidae. attract potential mates, and in some scolytines Although adults of all scolytine species bore are also used to mass attack host trees to over- into their host to lay eggs, they exhibit many dif- come host resistance (Byers, 2004; Raffa et al., ferent habits and utilize many different host tis- 2008). sues. True bark beetles bore through the outer Mating systems and social organization vary bark to the phloem–cambial area where they among scolytines. Reproductive systems range construct characteristic galleries and lay eggs. from simple monogamy (one male with one Larval mines radiate out from the gallery as the female), to heterosanguineous polygyny (multi- larvae feed on the phloem (phloeophagous). ple members of one sex with one, unrelated Ambrosia beetle adults bore through the bark ­member of the opposite sex), to consanguineous and into the xylem (wood) where they lay eggs. polygyny (multiple members of one sex with one,

48 © CAB International 2013. Potential Invasive Pests of Agricultural Crops (ed. J. Peña) Exotic Bark and Ambrosia Beetles in the USA 49

Table 3.1. Approximate number of scolytine (Wermelinger, 2004). Other ­species vector species worldwide and the number of those ­pathogenic fungi that cause tree diseases, for classified as ambrosia beetles by geographic area. example the multistriatus Approximate number of (Marsham), which vectors the causal agents of scolytine speciesb Dutch elm disease (Evans and Finkral, 2010). Ambrosia beetles, and their associated fungi, Continent or Ambrosia often cause stain and degrade of valuable wood geographic areaa Total beetlesc products, and in some cases, the fungal associates may be highly pathogenic to new hosts (Fraedrich Africa 1140 260 Asia 1920 500 et al., 2008). In this chapter, we will: (i) summarize Australia 130 50 recent US interceptions of scolytines with a focus Europe 230 25 on those that were intercepted in association with North America 1700 400 wood; (ii) discuss the 58 scolytine species that South America 1250 450 were known to be established in the continental Pacific Islands 220 100 USA as of 2010; (iii) briefly discuss the biology Worldwide 6000 1800 and impact of the redbay ambrosia beetle, Xyleborus glabratus Eichhoff; and (iv) discuss cur- aGeographic regions follow Wood and Bright (1992), Europe and Asia are divided by Ural Mountains, Asia rent international efforts aimed at reducing the includes Indonesia and Philippines, Africa includes international movement of exotic plant pests. Madagascar, North America includes Antilles Islands and Central America to Panama, New Zealand is included with Australia. 3.2 Scolytine Interceptions on bTotals for each geographic area include all species in the region, not just the endemic species, therefore the sum of Wood from 1984 to 2008 all world regions is greater than the worldwide totals. cAmbrosia beetles are all genera in the tribes Corthylini, Since 1984, the United States Department of Hyorrhynchini, Premnobini, Scolytoplatypodini, Xyleborini, Agriculture (USDA), and Plant Health Xyloterini, and the genus Camptocerus. Inspection Service (APHIS) has maintained an electronic database for plant pests intercepted at related member of the opposite sex) (Wood, US ports of entry (Haack, 2001, 2006; McCullough 1982; Kirkendall, 1983). Social organization et al., 2006). At first, this database was known as ranges from parental care, to colonial breeding, the Port Information Network, or PIN, but is now and eusociality with division of labor and repro- called the Pest Interception Database, or PestID. duction (Crespi, 1994; Kirkendall et al., 1997). The internal policies of every country influence The cryptic nature of scolytines, along with how cargo is inspected and which interceptions their wide variety of mating systems, host finding are recorded. In the USA, not all interceptions are behaviors, and abilities to utilize different host entered into PestID, but rather there is a bias tissues, allow them to be very successful in their towards pests of live plants that are considered of native habitats as well as efficient invaders of new quarantine significance. This policy has affected habitats (Wood, 1977, 1982; Haack, 2001; Roques the number and types of scolytine interceptions et al., 2009; Sauvard et al., 2010). Ecologically and recorded over the years. For example, because economically, these beetles are a very important true bark beetles more often infest live trees than group. In North America, various members of do ambrosia beetles, it is more likely that inter- kill vast expanses of forests each ceptions of bark beetles will be entered into year. The current outbreak of the mountain pine PestID than will interceptions of ambrosia bee- beetle, Dendroctonus ponderosae Hopkins, has tles. In addition, given that Canada and the USA killed c. 18 million acres (7.3 million ha) of pine share many species, few interceptions from (Pinus) forests across the western USA, and a sim- Canada are ever considered of quarantine impor- ilar acreage in western Canada (Raffa et al., 2008; tance and entered into PestID. For example, of USDA Forest Service, 2010). In Europe, the spruce the 195 scolytine species recorded in Canada, bark beetle, Ips typographus (Linnaeus), histori- only five are unique to Canada, while 190 are also cally has been the major pest of spruce (Picea), present in the USA (Wood and Bright, 1992; resulting in extensive areas of tree mortality Bright and Skidmore, 1997, 2002). It is ­important 50 R.A. Haack and R.J. Rabaglia

to remember these policies when examining the (647 interceptions), then decreased during the interception data discussed below. 1990s (low of 161 in 1991), and increased again In our analysis, we used PestID interception in the 2000s (high of 517 in 2002; Fig. 3.1). Note records for scolytines associated with wood for that the number of interceptions shown for 1984 the 25-year period from 1984 through 2008. The is artificially low because the electronic PestID data set consisted of 8286 records. Note, that our database actually began midway through 1984. data set did not include all scolytines, such as The strong reduction in overall interceptions those found in food items like coffee and nuts ­during the late 1980s and 1990s was related to a (Haack, 2001), but rather focused on those asso- dramatic decline in interceptions from Europe ciated with wood in the form of wood packaging (Fig. 3.1). By contrast, the increase in intercep- material (e.g., crating, pallets and dunnage), lum- tions during the 2000s was primarily the result of ber and logs. Of the 8286 interceptions, 3446 more interceptions from Central America, espe- (42%) were identified to the species level; 2239 cially Mexico (Fig. 3.1). (27%) to only the genus level; and 2601 (31%) to There are many factors that influence only the family level (Table 3.2). In the discussion changes in interception rates (Haack, 2001). For below, these 8286 interception records are pre- example, exporters can change the type or quality sented as a means of suggesting which scolytines of packaging materials they use, or they can treat are most likely to invade the continental USA; the wood prior to export. Importing countries however, it is important to realize that the pool can also influence interception rates by changing of potential invaders will change in relation to their inspection policies, import regulations and changes in trading partners, types of imported major trading partners. For example, during the products and the tree species utilized to manu- 1990s, the USA implemented two regulations on facture wood packaging material. wood packaging material that likely affected interception rates. First, beginning in 1996, the USA required that all unmanufactured solid wood 3.3 Continent of Origin packaging be ‘totally free from bark and appar- ently free from live plant pests’ or else be certi- Scolytines from eight continents or world regions fied as treated for wood pests by the exporting were intercepted on wood in the USA from 1984 country (USDA APHIS, 1995). In addition, begin- to 2008 (Table 3.2). For each interception record, ning in 1999, the USA imposed stricter regula- we assigned the corresponding country of origin tions on wood articles exported from China to to a continent in a manner similar to that used in the USA (USDA APHIS, 1998). As for major Haack (2001, 2006), which is slightly different to changes in US trading partners, the most dra- the world regions used in Table 3.1 in this chap- matic change has been with China, given that the ter. For example, for the data that follow, we value of imports from China to the United States assigned all interceptions from Russia and Turkey increased from US$3.1 billion in 1984 when to Asia, Mexico to Central America, and Australia China was the 20th leading US trading partner, and New Zealand to the Pacific region. Most of to US$338 billion in 2008 when China was the the 8286 interceptions originated in Europe 2nd leading USA trading partner (US Census (48%), Central America (32%) and Asia (15%) Bureau, 2011). (Table 3.2). Overall, 46 genera and 107 species were identified among the intercepted scolytines (Table 3.2). The diversity of intercepted scoly- 3.4 Country of Origin tines was greatest for Asia and Europe (Table 3.2); however, keep in mind that USDA APHIS his- Scolytines were intercepted on wood at US ports torically identified more bark beetles than of entry from at least 85 distinct countries that ambrosia beetles. The five scolytine genera that exist today, plus two countries that no longer represented the most interceptions from each exist (USSR and Yugoslavia) and the US state of continent are given in Table 3.2. Hawai’i, for a total of 88 ‘countries’. Although Over the 25-year period from 1984 to Hawai’i is a US state, goods from Hawai’i are 2008, the annual number of wood-associated inspected when exported to the continental USA. scolytine interceptions was highest in 1985 Of the 85 countries that exist today, nine were in Exotic Bark and Ambrosia Beetles in the USA 51 , Orthotomicus , Ips , , Hylurgops , Pityogenes Hypothenemus , Dendroctonus Pseudopityophthorus , Cryptocarenus Pseudothysanoes Dryocoetes Crypturgus Pityophthorus Five most common genera in decreasing order most common genera Five , Ips OrthotomicusPityogenes , Hylurgops Scolytus , OrthotomicusHypothenemus , , Pityophthorus , Orthotomicus, Pityogenes Ips , Pityophthorus , , OrthotomicusPhloeosinus , Hypocryphalus, , Ips GnathotrichusPityophthorus , , Xyleborus, Pityophthorus Hypothenemus , , Pityogenes , Scolytus , Polygraphus , Dendroctonus , XyleborusHylurgus , Hylurgops Phloeosinus , , XyleborusHypothenemus , Hylurgus Coccotrypes, 3 1 5 4 16 43 28 72 11 107 Species 9 7 5 5 18 46 32 24 31 22 Number of identified Genera 1 8 5 38 19 38 356 483 3446 2498 Species level 8 3 3 18 34 619 324 117 2239 1113 Genus level Genus Number identified to only 0 8 3 27 17 54 243 2601 1094 1155 Family level Family 9 83 70 19 11 209 8286 1218 2690 3977 Number of interceptions Summary data by continent of origin for 8286 scolytine interceptions made in association with wood products or wood packaging materials at USA packaging products or wood 8286 scolytine interceptions made in association with wood Summary continent of origin for data by

a b America America America See text for details on how countries were assigned to continents as well as Haack (2001). as Haack countries assigned to continents as well details on how were for See text freely inside a container and not walking insect is found when a live example, This can happen, for some interceptions the country countryFor or likely of originnot listed. was associated closely with specific cargo. This is especially common when there is mixed cargo from multiple countries cargo from multiple within a single container. This is especially common when there mixed associated closely with specific cargo. Table 3.2. Table ports of entry from 1984 to 2008. Continent a b Africa Total Asia Central Central Caribbean Europe North Pacific South Unknown 52 R.A. Haack and R.J. Rabaglia

700

600

500 ar ye per 400

300 eptions eptions rc

200 No. inte No.

100

0 1988 1984 1986 1990 1992 1994 1996 1998 2000 2002 2004 2006 2008

Year

Total Asia Central America Europe

Fig. 3.1. Total number of annual wood-associated scolytine interception at US ports of entry and for selected continents of origin for the period 1984 through 2008.

Africa, 21 in Asia (which included Russia and ­maritime ports, 2572 at land borders with Canada Turkey), seven in Central America (including and Mexico, 415 at airports, 55 at other US Mexico), four in the Caribbean, 29 in Europe, five inspection stations, 6 at rail inspection centers, in the Pacific region (including Australia, Hawai’i 2 at foreign sites (preclearance inspections) and and New Zealand) and 11 in South America. There 1 in Hawai’i during pre-departure inspection to were 12 countries from which 100 or more inter- the US mainland. Of the 2572 interceptions at ceptions were made from 1984 to 2008: Mexico land borders, only 19 (0.7%) were actually of (2581 interceptions), Italy (1322), Germany Canadian origin, while 2534 (98.5%) were of (715), Spain (533), China (428), Belgium (316), Mexican origin, and the remainder (0.8%) were France (255), India (225), Turkey (180), Portugal from other countries for products shipped to the (178), United Kingdom (137) and Russia (113). USA through either Canada or Mexico. Additional details on scolytine interceptions by There were 100 or more wood-associated country can be viewed in Haack (2001) for the scolytine interceptions made in 15 US states and period 1985–2000. Puerto Rico from 1984 to 2008, including Texas (3065 interceptions), Florida (890), Georgia (615), California (576), Louisiana (399), Ohio 3.5 Intercepted Scolytines (340), South Carolina (339), Washington (272), by Receiving US State New York (238), Kentucky (233), Maryland (208), North Carolina (191), Puerto Rico (160), Scolytines were intercepted on wood at ports of New Jersey (131), Alabama (103) and Michigan entry in 38 US states as well as in Puerto Rico and (100). All of the states listed above have major the US Virgin Islands. Puerto Rico and the US maritime ports, international airports, or land Virgin Islands serve as official US ports of entry border crossings with Canada or Mexico. Overall, for many foreign goods that are later shipped to most interceptions made along the US west coast the US mainland. Of the 8286 wood-associated were on goods shipped from Asia. By contrast, scolytine interceptions, 5235 were made at most interceptions made along the US east coast Exotic Bark and Ambrosia Beetles in the USA 53

or at ports along the Great Lakes were of European 24 of the 25 years (Hylurgus, Orthotomicus and origin, and most interceptions made along the US ) (Table 3.3). border with Mexico, including California, were of Central American origin, remembering that Mexico was classified as part of Central America 3.7 Species of Intercepted in this analysis. Scolytines

Of the 8286 wood-associated scolytine intercept­ 3.6 Genera of Intercepted Scolytines ions, 3446 (42%) were identified to the species level and represented 107 species (Tables 3.2 and 3.4). As Of the 8286 wood-associated scolytine inter­ mentioned above for scolytine genera, many more ceptions, 5685 (69%) were identified to at least species would likely have been identified as well, if the genus level and represented 46 genera more interceptions had been ­identified to the spe- (Tables 3.2–3.3). Given that 31% of the intercep- cies level. Nevertheless, the species listed in tions were not identified beyond the family level it Table 3.4 are probably representative of those com- is likely that many more genera were intercepted. monly associated with wood packaging material There were 14 genera with 100 or more intercep- used in international trade, but of course lack tions from 1984 to 2008: Ips (917 interceptions), the scolytine species intercepted on US exports Pityophthorus (827), Pityogenes (618), Orthotomicus (Brockerhoff et al., 2006). The ten most commonly (591), Hylurgops (346), Hylurgus (291), Gnathot­ intercepted wood-associated­ scolytines were Ortho­ richus (216), Tomicus (194), Hypothenemus (182), tomicus erosus (Wollaston) (513 interceptions), Xyleborus (181), Dryocoetes (166), Phloeosinus Pityogenes chalcographus (Linnaeus) (512), Ips (160), Hylastes (135) and Hypocryphalus­ (115). typographus (292), Hylurgops palliatus (Gyllenhal) For each scolytine genus, the number of (282), Hylurgus ligniperda (Fabricius) (239), Ips originating continents (world regions), countries sexdentatus (Boerner) (189), and the top four originating countries are (Linnaeus) (159), Ips integer (Eichhoff) (82), ­presented in Table 3.3. Individuals identified as Hylastes ater (Paykull) (67) and Xyleborus Xyleborus were intercepted from seven conti- eurygraphus (Ratzeburg) (67) (Table 3.4). Of the nents, the most of any of the 46 identified ­genera, 107 identified scolytine ­species, there were 15 while two genera (Phloeosinus and Pityophthorus) ­species of Ips, 9 Xyleborus, 6 Pityogenes, 6 Hylastes, were each intercepted from six continents. Eight 5 Scolytus, and 4 each of Crypturgus, Hylurgops, Ortho­ genera were intercepted from 20 or more coun- t­ o m i c u s and P o l y g­ r a p h u s . We recognize that several tries, including Ips (38 countries), Pityogenes (35), taxonomic changes have occurred in recent years Hypothenemus (30), Orthotomicus (25), Xyleborus for some of the species listed in Table 3.4; however, (25), Hylurgops (23), Tomicus (22) and Dryocoetes for the sake of consistency, we are presenting the (21). A positive ­linear relationship was found species names as recorded by USDA APHIS. between the number of interceptions for a given As mentioned in Haack (2001), interception genus and the number of the originating coun- databases often include records that suggest tries (F[1, 44] = 57.7, P < 0.0001, R2 = 0.57). range expansion of a species. The PestID data- The number of receiving US states and the base suggests several cases of range expansion if number of years during the 25-year period from we consider the range data in Wood and Bright 1984 to 2008 that individuals of each scolytine (1992) and Wood (2007) complete, and that there genus were intercepted are provided in Table 3.3. were no errors in identification or data entry. For Ips beetles were intercepted in the most US states example, there were interception records in the (27) and specimens of five other genera were USA for several scolytine species originating from intercepted in 20 or more US states: Orthotomicus countries that were outside their published geo- (25 US states), Pityogenes (25), Dryocoetes (22), graphic ranges, including Dendroctonus frontalis Hylurgops (21) and Hylurgus (20) (Table 3.3). Five Zimmermann from Turkey (1 interception), genera were intercepted during each year of the Hylastes attenuatus Erichson from South Africa 25-year survey period (Hylurgops, Hypothenemus, (2), Hylurgops palliatus from Honduras (1) and Ips, Pityogenes and Pityophthorus), and ­individuals Venezuela (1), Hylurgus ligniperda from Venezuela of three other genera were intercepted during (1), Phloeosinus rudis Blandford from Belgium (1), 54 R.A. Haack and R.J. Rabaglia

2 3 2 1 5 1 3 4 16 11 16 18 11 10 23 15 22 13 25 24 18 25 25 24 1984 to 2008 intercepted from Number of years Number of years 2 3 2 6 1 9 5 3 7 7 1 2 2 13 11 14 22 18 21 20 16 13 27 25 receiving US states Number of a BR, PE BE IT, TR, ES, MX TT PE, VE, CR BR, IT, IN, PH CN, IT, TT DE, IT ES, PT, CN, KR, SG, HK TR MX, CA, CN, IT, DE, BE CN, IT, CN, IN MX, IT, FR, HN MX, IT, FR, DE IT, ES, UK, BE, UA, IT UK, BE, UA, MX MX, IT DE, IT, BE, MX DE, IT, IT, PT, ES, CL ES, PT, IT, IN, BR, TW, MY TW, IN, BR, VE, CN IN, BR, MX, IT, DE, ES MX, IT, MX, PE, BR IT, ES, CN, TR CN, ES, IT, Top four countries of four Top origin in decreasing order 2 8 1 2 6 1 6 3 2 8 6 1 2 3 13 15 21 15 23 16 10 30 38 25 countries Number of 1 3 1 2 5 4 1 5 1 3 4 1 2 5 3 1 2 5 5 4 5 5 2 3 continents Number of 0 3 0 0 7 0 6 1 2 4 2 0 18 36 10 32 47 80 11 122 301 240 808 552 Identified to species level 2 3 2 1 6 1 4 38 17 57 66 20 54 16 13 Number of interceptions 166 216 135 346 291 115 182 917 591 Total Summary data by genus for the 8286 wood-associated interception records of scolytines intercepted at US ports the 8286 wood-associated Summary for of entry genus data by from 1984 to 2008.

Araptus Chaetophloeus Cnemonyx Coccotrypes Cryphalus Cryptocarenus Crypturgus Cyrtogenius Dendroctonus Dryocoetes Euwallacea Gnathotrichus Hylastes Hylocurus Hylurgopinus Hylurgops Hylurgus Hypocryphalus Hypothenemus Ips Monarthrum Orthotomicus Table 3.3. Table Scolytine genus Exotic Bark and Ambrosia Beetles in the USA 55 2 4 2 1 1 2 1 2 8 6 20 25 10 25 20 10 22 17 24 17 20 10 25 25 2 4 7 1 1 0 1 2 1 2 7 6 17 25 19 17 19 17 19 10 19 10 33 38 BR, IN MX, CA CN, JP, IL ES, JO, BE ES, DE, IT, FR, GR, DE IT, MX, BR, ZA, IT DE, CN, RU IT, MX MX DO IT DE, BR ID CN, PT FR BE, CN, IT, TR BE, DE, FR, UK FR, ES, IT, TR, DE, FR IT, KR, GR CN, IT, TR, MX CN, IT, IN, IT NG CN, BE, IT, BE, CN, IT, FR BE, CN, IT, MX, IT, DE, ES MX, IT, 2 9 3 5 3 1 1 1 2 1 2 8 2 8 35 15 18 17 13 22 12 25 60 87 2 6 2 4 1 6 4 1 1 1 1 2 1 2 5 4 3 2 2 7 2 4 7 8 0 2 3 2 0 1 0 0 0 2 0 16 20 15 49 20 35 29 11 17 591 166 120 3446 2 4 3 1 1 2 1 3 18 66 99 98 64 38 17 12 17 160 618 827 194 181 2601 8286 b Country codes: AT Austria, AU Australia, AZ Azerbaijan, BE Belgium, BR Brazil, BZ Belize, CA Canada, CL Chile, CN China, CR Costa Rica, DE Germany, DO Dominican Republic, DO Dominican Republic, CN China, CR Costa Rica, DE Germany, CA Canada, CL Chile, BZ Belize, BE Belgium, BR Brazil, AZ Azerbaijan, Australia, AU Austria, AT Country codes: level. only identified to the family The interception records labeled Scolytidae were EC Ecuador, EE Estonia, ES Spain, FI Finland, FR France, GT Guatemala, GR Greece, GY Guyana, HK Hong Kong, HN Honduras, HR Croatia, ID Indonesia, IL Israel, IN India, HR Croatia, ID Indonesia, IL Israel, HN Honduras, HK Hong Kong, GY Guyana, GT Guatemala, GR Greece, EE Estonia, ES Spain, FI Finland, FR France, EC Ecuador, PT Portugal, PL Poland, PH Philippines, NG Nigeria, NL Netherlands, PE Peru, MY Malaysia, Latvia, MX Mexico, Lithuania, LV Vietnam, LT VN JO Jordan, KR South Korea, JP Japan, IT Italy, Venezuela, VE UK United Kingdom, Ukraine, UA Taiwan, TW Tobago, and Trinidad TT Turkey, TR SK Slovakia, SG Singapore, Russia, SE Sweden, Romania, RU RO ZA South Africa. a b Phloeosinus Pityogenes Pityokteines Pityophthorus Polygraphus Pseudopityophthorus Pseudothysanoes Pteleobius Scolytodes Scolytogenes Scolytoplatypus Scolytus Taphrorychus Tomicus Trypodendron Xyleborinus Xyleborus Xylosandrus Scolytidae Total 56 R.A. Haack and R.J. Rabaglia

Table 3.4. Summary data by species for the 3446 wood-associated interception records of scolytines that were intercepted at USA ports of entry from 1984 to 2008 and identified to the species level.

Top five originating No. No. No. No. countries in receiving Species interceptions continents countries decreasing ordera US states

Carphoborus bifurcus 1 1 1 MX 1 Eichhoff Carphoborus minimus 11 2 4 ES, TR, IT, BE 8 (Fabricius) Carphoborus pini 5 1 2 ES, IT 3 Eichhoff Carphoborus rossicus 1 1 1 DE 1 (Semenov) Chaetophloeus 3 1 1 MX 3 mexicanus Blackman Cryphalus abietis 2 1 2 DE, IT 1 (Ratzeburg) Cryphalus piceae 5 1 2 IT, FR 4 (Ratzeburg) Crypturgus cinereus 11 3 5 DE, ES, RU, BE, AU 6 (Herbst) Crypturgus 19 1 5 PT, ES, IT, FR, NL 8 mediterraneus Eichhoff Crypturgus 4 1 2 ES, GR 4 numidicus Ferrari Crypturgus pusillus 2 2 2 CN, LV 2 (Gyllenhal) Cyrtogenius luteus 10 1 4 CN, KR, SG, VN 6 (Blandford) Dendroctonus 2 2 2 MX, TR 2 frontalis Zimm. Dendroctonus 28 1 1 MX 3 mexicanus Hopkins Dendroctonus 2 1 1 CA 1 pseudotsugae Hopkins Dryocoetes 29 3 11 IT, BE, ES, BR, HR 14 autographus (Ratzeburg) Dryocoetes 1 1 1 IT 1 hectographus Reitter Dryocoetes villosus 17 1 5 BE, DE, UK, FR, IT 9 (Fabricius) Euwallacea 1 1 1 IN 1 andamanensis (Blandford) Euwallacea validus 5 1 1 CN 2 (Eichhoff) Gnathotrichus 3 1 1 MX 1 denticulatus Blackman Gnathotrichus 25 2 5 FR, IT, ES, DE, GT 6 materiarius (Fitch) Gnathotrichus 52 1 1 MX 3 sulcatus Leconte Continued Exotic Bark and Ambrosia Beetles in the USA 57

Table 3.4. Continued.

Top five originating No. No. No. No. countries in receiving Species interceptions continents countries decreasing ordera US states

Hylastes angustatus 4 1 2 BE, FR 3 (Herbst) Hylastes ater 67 2 10 ES, IT, FR, DE, UK 14 (Paykull) Hylastes attenuatus 23 2 7 ES, IT, PT, FR, ZA 8 Erichson Hylastes cunicularius 7 1 4 IT, DE, UK, BE 5 Erichson Hylastes linearis 10 1 3 ES, PT, IT 3 Erichson Hylastes opacus 1 1 1 PL 1 Erichson Hylesinus crenatus 1 1 1 UK 1 Fabricius Hylesinus varius 10 1 3 UK, BE, IT 5 (Fabricius) 2 2 2 MX, IT 2 (Eichhoff) Hylurgops glabratus 3 2 2 IT, RU 2 (Zetterstedt) Hylurgops incomptus 9 1 1 MX 1 (Blandford) Hylurgops palliatus 282 5 21 DE, IT, BE, UK, ES 21 (Gyllenhal) Hylurgops planirostris 7 1 1 MX 1 (Chapuis) Hylurgus ligniperda 239 4 15 IT, PT, ES, FR, CL 16 (Fabricius) Hylurgus micklitzi 1 1 1 IT 1 Wachtl Hypocryphalus 4 2 2 IN, BR 3 mangiferae (Stebbing) Hypothenemus 1 1 1 SG 1 birmanus (Eichhoff) Hypothenemus 1 1 1 PT 1 obscurus (Fabricius) Ips acuminatus 40 2 9 TR, IT, ES, FR, CN 11 (Gyllenhal) Ips amitinus (Eichhoff) 2 1 2 IT, FI 2 Ips apache Lanier 9 1 2 HN, MX 4 Ips bonanseai 27 1 1 MX 3 (Hopkins) Ips calligraphus 13 1 3 MX, HN, GT 4 (Germar) Ips cembrae (Heer) 9 2 4 IT, DE, TW, BE 5 Ips cribricollis 39 1 3 MX, HN, GT 4 (Eichhoff) Ips grandicollis 14 1 2 MX, GT 3 (Eichhoff) Ips integer (Eichhoff) 82 1 1 MX 3 Ips lecontei Swaine 43 1 2 MX, GT 4 Continued 58 R.A. Haack and R.J. Rabaglia

Table 3.4. Continued.

Top five originating No. No. No. No. countries in receiving Species interceptions continents countries decreasing ordera US states

Ips mannsfeldi (Wachtl) 7 2 2 ES, TR 4 Ips mexicanus 5 1 1 MX 1 (Hopkins) Ips pini (Say) 37 1 1 MX 2 Ips sexdentatus 189 2 12 IT, ES, FR, TR, PT 19 (Boerner) Ips typographus 292 2 25 IT, DE, BE, RO, RU 22 (Linnaeus) Orthotomicus erosus 513 3 20 IT, ES, TR, CN, PT 24 Wollaston Orthotomicus laricis 29 2 10 IT, FR, DE, ES, PL 12 (Fabricius) Orthotomicus proximus 2 1 2 IT, FI 2 (Eichhoff) Orthotomicus suturalis 8 1 3 UK, DE, EE 4 (Gyllenhal) Phloeosinus canadensis 2 1 1 CA 2 Swaine Phloeosinus rudis 14 2 2 JP, BE 7 Blandford Phloeotribus 2 2 2 ES, JO 2 scarabaeoides (Bernard) Pityogenes bidentatus 23 2 7 ES, FR, DE, IT, SE 9 (Herbst) Pityogenes bistridentatus 42 2 7 ES, TR, IT, FR, UK 9 (Eichhoff) Pityogenes calcaratus 4 1 3 ES, FR, IT 4 (Eichhoff) Pityogenes 512 3 31 DE, IT, BE, RU, ES 25 chalcographus (Linnaeus) Pityogenes quadridens 9 2 5 FI, TR, ES, LT, PT 7 (Hartig) Pityogenes trepanatus 1 1 1 LT 1 (Nordlinger) Pityokteines curvidens 3 1 3 FR, IT, GR 3 (Germar) Pityokteines spinidens 12 1 4 IT, FR, AT, DE 5 (Reitter) Pityophthorus 6 1 1 MX 1 mexicanus Blackman Pityophthorus 14 2 5 IT, DE, MX, NL, FR 8 pityographus (Ratzeburg) Polygraphus 44 2 10 IT, DE, CN, UK, BE 14 poligraphus (Linnaeus) Polygraphus proximus 1 1 1 IT 1 Blanchard Polygraphus rufipennis 2 1 1 CA 2 (Kirby) Continued Exotic Bark and Ambrosia Beetles in the USA 59

Table 3.4. Continued.

Top five originating No. No. No. No. countries in receiving Species interceptions continents countries decreasing ordera US states

Polygraphus 2 2 2 IT, AZ 1 subopacus Thomson Pseudohylesinus 3 1 1 MX 1 variegatus (Blandford) Pseudopityophthorus 1 1 1 MX 1 pruinosus (Eichhoff) Pseudopityophthorus 1 1 1 MX 1 yavapaii Blackman Pteleobius vittatus 1 1 1 IT 1 Fabricius Scolytus intricatus 12 1 4 BE, FR, IT, DE 8 (Ratzeburg) Scolytus multistriatus 2 2 2 IT, CA 2 (Marsham) Scolytus ratzeburgi 1 1 1 FI 1 Janson 4 2 2 CN, CA 4 Semenov Scolytus scolytus 1 1 1 UK 1 (Fabricius) Taphrorychus bicolor 21 1 5 BE, DE, FR, FI, NL 10 (Herbst) Taphrorychus villifrons 14 2 5 BE, DE, FR, LV, TR 9 (Dufour) Tomicus minor 7 2 3 TR, BR, IT 3 (Hartig) Tomicus piniperda 159 2 21 IT, FR, ES, UK, DE 19 (Linnaeus) Trypodendron 10 2 4 IT, TR, BE, FR 4 domesticum (Linnaeus) Trypodendron lineatum 12 2 7 IT, TR, CH, SK, IL 4 (Olivier) Trypodendron signatum 7 1 4 DE, FR, PO, BE 4 (Fabricius) Xyleborinus saxesenii 11 2 7 IT, CN, GR, TR, KR 6 (Ratzeburg) Xyleborus affinis 22 6 5 GY, MX, ID, HN, BR 8 Eichhoff Xyleborus apicalis 1 1 1 MY 1 Blandford Xyleborus dispar 2 1 1 IT 1 (Fabricius) Xyleborus eurygraphus 67 2 4 IT, TR, ES, GR 9 (Ratzeburg) Xyleborus ferrugineus 2 2 2 BR, BZ 2 (Fabricius) Xyleborus glabratus 1 1 1 CN 1 Eichhoff Xyleborus intrusus 9 1 3 HN, NI, MX 3 Blandford Continued 60 R.A. Haack and R.J. Rabaglia

Table 3.4. Continued.

Top five originating No. No. No. No. countries in receiving Species interceptions continents countries decreasing ordera US states

Xyleborus similis 1 1 1 VN 1 Ferrari Xyleborus volvulus 15 4 11 PE, GY, HN, VE, EC 7 (Fabricius) Xylechinus pilosus 2 1 1 IT 1 (Ratzeburg) Xylosandrus 10 3 4 CN, IT, NG, ID 8 ­crassiusculus (Motschulsky) Xylosandrus germanus 6 3 5 JP, PE, DE, BE, IT 5 (Blandford) Xylosandrus morigerus 1 1 1 BE 1 (Blandford) aCountry codes for Tables: AT Austria, AU Australia, AZ Azerbaijan, BE Belgium, BR Brazil, BZ Belize, CA Canada, CL Chile, CN China, CR Costa Rica, DE Germany, DO Dominican Republic, EC Ecuador, EE Estonia, ES Spain, FI Finland, FR France, GT Guatemala, GR Greece, GY Guyana, HK Hong Kong, HN Honduras, HR Croatia, ID Indonesia, IL Israel, IN India, IT Italy, JP Japan, JO Jordan, KR South Korea, LT Lithuania, LV Latvia, MX Mexico, MY Malaysia, NG Nigeria, NL Netherlands, PE Peru, PH Philippines, PL Poland, PT Portugal, RO Romania, RU Russia, SE Sweden, SG Singapore, SK Slovakia, TR Turkey, TT Trinidad and Tobago, TW Taiwan, UA Ukraine, UK United Kingdom, VE Venezuela, VN Vietnam, ZA South Africa.

Pityogenes chalcographus from Brazil (1) and where 25 or more species were identified among Tomicus minor (Hartig) from Brazil (1). Although the intercepted scolytines: Texas (67 species), the above interceptions should not be considered Florida (55), California (40), Louisiana (33), Georgia authoritative records that these species are estab- (30), South Carolina (30) and New York (25). lished in these countries, it is of interest to note that Kirkendall and Faccoli (2010) recently reported that Phloeosinus rudis is established in 3.8 Currently Established France and The Netherlands. Exotic Scolytines The number of originating continents and countries for each of the 107 identified scolytine As of 2010, we are aware of 58 scolytine species in species intercepted in the USA, as well as the 27 genera that are established in the continental top five originating countries, are presented in USA (Table 3.5). Many of the species listed in Table 3.4. There were six countries from which 20 Table 3.5, especially in the Xyleborini, had been or more wood-associated scolytine species were transferred to new genera since publication of the intercepted and identified: Italy (50 species), world catalog by Wood and Bright (1992), includ- France (29), Germany (28), Spain (28), Belgium ing Ambrosiophilus atratus (Eichhoff), Anisandrus (24) and Mexico (24). dispar (Fabricius), A. maiche Stark, Cnestus mutila­ The number of US states in which each of the tus (Blandford), Cyclorhipidion ­californicus (Wood), 107 identified scolytines were intercepted is pre- C. pelliculosum (Eichhoff), Dryoxylon onoharaen­ sented in Table 3.4. Overall, there was a significant sum (Murayama), Wallacellus similis (Ferrari), and positive linear relationship between the number Xyleborinus octiesdentatus (Murayama) and of interceptions for a given scolytine species and Xylosandrus amputatus (Blandford). In Wood and the number of the originating countries (F[1,105] = Bright (1992), all of the above species were for- 300.7, P < 0.0001, R2 = 0.74), and similarly between merly members of the genus Xyleborus except the number of interceptions and the number Cnestus mutilatus (formerly in Xylosandrus), and of receiving US states (F[1,105] = 212.5, P < 0.0001, X. amputatus (formerly in Amasa). The pine shoot R2 = 0.67) (Table 3.5). There were seven US states beetle, Tomicus piniperda, is the only scolytine of Exotic Bark and Ambrosia Beetles in the USA 61 d 5 3 6 7 14 23 37 29 20 11 13 10 36 36 36 16 36 16 38 17 37 18 record Continued first USA collection Reference of Reference c 3 1 2 2 1 2 2 4 2 1 1 1 1 1 29 18 17 20 18 10 48 48 as of 2010 where found where found No. US states No. Native Native range Eurasia Asia Asia Eurasia Europe Eurasia Europe Eurasia Eurasia Asia Africa Asia Africa Asia Asia Africa Asia Europe Asia Europe Europe Europe b PA CO LA State NY NY CA NY NY MI FL FL LA AZ, FL FL FL CA FL CA CA NY MA NY first collection Record or report of Year 2001 1994 1982 1987 1878 2004 1988 1994 1991 1956 1926 1934 1915 1939 1910 1992 1985 2009 1992 1868 1909 1877 a BB BB AB Feeding Feeding guild BB R BB BB BB BB ST ST ST ST ST ST ST ST ST BB BB BB BB fg e e Hylastes opacus Erichson Species Hylurgops palliatus (Gyllenhal) obscurusHylastinus (Marsham) Orthotomicus erosus (Wollaston) bidentatus (Herbst) Pityogenes Hylurgus ligniperda (Fabricius) piniperda (Linnaeus) Tomicus Coccotrypes Blandford advena Coccotrypes carpophagus (Hornung) Coccotrypes cyperi (Beeson) Coccotrypes dactyliperda (Fabricius) Coccotrypes distinctus (Motschulsky) Coccotrypes (Hopkins) rhizophorae Coccotrypes rutschuruensis Eggers Coccotrypes vulgaris (Eggers) Dactylotrypes longicollis (Wollaston) (Murayama) onoharaensum Dryoxylon Phloeosinus armatusPhloeosinus Reitter Scolytus mali (Bechstein) Scolytus multistriatus (Marsham) Scolytus rugulosus (Muller) Semenov Scolytus schevyrewi Summary data for the 58 exotic scolytines recognized as being established in the continental United States as of 2010. as being established scolytines recognized Summary the 58 exotic data for

Table 3.5. Table Hylastini Tribe Ipini Dryocoetini 62 R.A. Haack and R.J. Rabaglia d 2 8 1 9 4 4 2 30 34 31 36 26 21 25 28 16 26 32 15 36 18 22 12 25 27 record first USA collection Reference of Reference c 8 2 2 1 2 4 6 3 1 9 1 1 1 3 28 18 23 13 43 10 29 32 21 27 24 as of 2010 where found where found No. US states No. Native Native range Asia Asia Eurasia Asia Eurasia Eurasia Asia Asia Asia Asia Asia Asia Asia Asia Asia Asia Asia Eurasia Europe Africa Asia Asia Asia Europe Asia b FL NY WA FL CA MD FL SC NY MS CA PA TX LA GA MA FL State NY WA FL PA MD TN MA PA first collection Record or report of Year 2002 1976 1996 2009 1911 1992 1941 1974 1931 1999 1944 1987 2002 2008 2002 2005 2010 1868 2008 1939 1990 1942 1988 1817 2005 a AB AB AB AB AB AB AB AB AB AB AB AB AB AB AB AB AB Feeding Feeding guild BB AB AB AB AB AB AB AB e h e h h e e eh Cyclorhipidion californicus (Wood) Cyclorhipidion californicus Cyclorhipidion pelliculosum (Eichhoff) (Eichhoff) fornicatus Euwallacea (Eichhoff) validus Euwallacea similis (Ferrari) Wallacellus Xyleborinus alni (Niisima) (Blandford) Xyleborinus andrewesi Xyleborinus octiesdentatus (Murayama) (Ratzeburg) Xyleborinus saxesenii Xyleborus Eichhoff glabratus (Ratzeburg) Xyleborus pfeilii Xyleborus seriatus Blandford Xylosandrus amputatus (Blandford) Xylosandrus compactus (Eichhoff) Xylosandrus (Motschulsky) crassiusculus Xylosandrus germanus (Blandford) Species Crypturgus pusillus (Gyllenhal) Trypodendron domesticum (Linnaeus) Trypodendron Eichhoff Premnobius cavipennis (Blandford) lewisi Ambrosiodmus rubricollisAmbrosiodmus (Eichhoff) (Eichhoff) Ambrosiophilus atratus Anisandrus dispar (Fabricius) Anisandrus maiche Stark (Blandford) Cnestus mutilatus Continued.

Table 3.5. Table Tribe Crypturgini Xyloterini Premnobini Xyleborini Exotic Bark and Ambrosia Beetles in the USA 63 33 36 33 16 16 16 18 19 35 35 36 X. not X. saxesenii X. 1 1 1 3 6 1 1 1 1 14 20 Asia Asia Asia Africa Africa Africa Asia Africa Africa S America Africa FL FL FL TX CA SC GA, LA TX FL FL FL 1949 1960 1951 1904 1895 1881 1868 1876 1977 1977 1982 BB ST ST ST ST ST ST ST ST ST ST (Hulcr and Cognato, 2010). (Hulcr and Cognato, similis Xyleborus similis to Wallacellus (Stebbing) Hypocryphalus mangiferae Hypothenemus areccae (Hornung)Hypothenemus birmanusHypothenemus (Eichhoff) brunneusHypothenemus (Hopkins) Hopkins californicus Hypothenemus columbi Hopkins Hypothenemus crudiaeHypothenemus (Panzer) erectus LeConte Hypothenemus (Eggers) javanus Hypothenemus obscurusHypothenemus (Fabricius) setosus (Eichhoff) Hypothenemus . (1991), 4 = Bright (1968), 5 = Bright and Rabaglia (1999), 6 = Chapman (1910), 7 Chittenden (1898), (1990), 3 = Atkinson et al . 1= Anderson (1974), 2= Atkinson et al . References: Feeding guilds: AB = ambrosia beetles, feed primarily on fungus (xylomycetophagous), BB = bark beetles, feed primarily primarily BB = barkfeed on inner feed on fungus (xylomycetophagous), beetles, or phloem (phloeophagous), R = roots of AB = ambrosia beetles, guilds: Feeding FL = Florida,MD Maryland, GA = Georgia, LA Louisiana, MA Massachusetts, MI = Michigan, CO = Colorado, AZ = Arizona, CA California, US state abbreviations: Service Forest Early Detection & Rapid Response project. the USDA first detected in the USA by These species were ; onoharaensis not D. onoharaensum D. The current correct spellings are: commonly been misspelled in the scientific literature. These three species names have X yleborus californicus 2010); (Dole and Cognato, Xylosandrus to Cnestus mutilatus mutilatus the nomenclature of these species as follows: affected Recent taxonomic changes have Number of US states where reported in literature or found in the USDA Forest Service Early Detection & Rapid Response surveys as of 2010, exclusive of Hawai’i. Service Forest Earlyas of 2010, exclusive Detection & Rapid Response surveys Number of US states where reportedin the USDA or found in literature Bright and Rabaglia (1999) recorded this species from Delaware in 1977; the correct Delaware record is from 1997. the correct Delaware in 1977; Bright and Rabaglia (1999) recorded this species from Delaware . (2011), 9 = Felt (1932), 10 = Haack and Poland (2001), 11 = Hoebeke (1989), 12 = Hoebeke (1991), 13 = Hoebeke (2001), 14 = Hoebeke and Acciavatti (2006), 15 (2006), 15 and Acciavatti (2001), 14 = Hoebeke (1991), 13 = Hoebeke (1989), 12 = Hoebeke (2001), 11 = Hoebeke and Poland (1932), 10 = Haack (2011), 9 = Felt 8 = Cognato et al . (2001), (2005), 21 = Mudge et al . data), 18 = LeConte (1868), 19 (1876), 20 Lee et al . and Rabaglia (2008), 16 = Hopkins (1915), 17 LaBonte (unpublished = Hoebeke (2010), (2009), 28 = Rabaglia et al . (2006), 27 = Rabaglia et al . (1817), 26 = Rabaglia et al . Thomas (2010), 25 = Peck (2005), 24 = Okins and et al . 22 = NAPIS (2008), 23 Negrón (1982), Wood (1977), 36 = Wood (1975), 35 = Wood (1954), 34 = Wood (2000), 33 = et al . Vandenberg Thomas (2004), 32 = and Bright (2004), 31 = (1879), 30 = Schiefer 29 = Riley and Bright (1992). Wood (1992), 38 = Wood 37 = herbaceous plants, e.g. Trifolium, (herbiphagous), ST = most are seed and twig beetles, feeding in seeds (spermophagous), or the pith (myelophagous) or phloem of twigs. in seeds (spermophagous), or the pith (myelophagous) feeding (herbiphagous), ST = most are seed and twig beetles, Trifolium, e.g. herbaceous plants, Washington. = WA and Texas, TX = Tennessee, TN = SC = South Carolina, = Pennsylvania, PA York, MS = Mississippi, NY New pelliculosus to Cyclorhipidion ; and X. . not Xyleborus and Xyleboruspfeili pfeilii ; saxeseni a b c d e f g h 64 R.A. Haack and R.J. Rabaglia

the 58 exotics for which there is a USDA federal ­current worldwide geographic distribution quarantine that regulates movement of pine host (Wood and Bright, 1992). material to areas outside the known current US Kirkendall and Faccoli (2010) recently range of this bark beetle (Haack and Poland, reported that there are 18 species of exotic scoly- 2001). This US federal quarantine was enacted tines established in Europe, of which seven are soon after discovery of T. piniperda in 1992 and it also established in the USA: Ambrosiodmus rubri­ is still in effect as of 2010, even though this bark collis (Eichhoff), Ambrosiophilus atratus, Coccotrypes beetle has caused minimal damage in the cur- ­dactyliperda (Fabricius), Dactylotrypes longicollis, rently infested portions of the eastern USA. Xyleborus pfeilii (Ratzeburg), Xylosandrus crassiuscu­ Overall, 19 of the 107 intercepted scolytines lus and X. germanus. In addition, Kirkendall and listed in Table 3.4, and an additional two intercepted Faccoli (2010) list Cyclorhipidion bodoanum (Reitter) species listed in Haack (2001), which included US as established in Europe, and state that this species interceptions for scolytines on all products, are will be synonymized with C. californicus, which is among the 58 exotic scolytines now established in established in the USA (Table 3.5). Once this occurs the continental USA (Table 3.5). The 21 species, there will be eight exotic scolytines in common listed in the order they appear in Table 3.5, include: between Europe and the USA. Note that we listed Hylastes opacus Erichson, Hylurgops palliatus, Europe as the native range of D. longicollis in Hylurgus ligniperda, Tomicus piniperda, Scolytus multi­ Table 3.5 given that this species is native to the striatus, S. schevyrewi Semenov, Orthotomicus erosus, Canary Islands, which are an autonomous territory Pityogenes bidentatus (Herbst), Coccotrypes carpo­ of Spain. However, Kirkendall and Faccoli (2010) phagus (Hornung) (in Haack, 2001), Dactylotrypes treat this species as an exotic to continental Europe. longicollis (Wollaston) (in Haack, 2001), Crypturgus Of the 58 exotic scolytines in the USA, one pusillus (Gyllenhal), Trypodendron domesticum – Hylastinus obscurus (Marsham) – breeds in roots (Linnaeus), Euwallacea validus (Eichhoff), Xyle­ of herbaceous legumes, while the others breed borinus ­saxesenii (Ratzeburg), Xyleborus glabratus, primarily in woody plants and palms. We catego- Walla­cellus ­similis (Ferrari), Xylosandrus crassius­ rized 25 of the 58 scolytines as ambrosia beetles culus (Motschulsky), X. germanus (Blandford), (43%), 13 as bark beetles (22%), 19 as seed and Hypocryphalus mangiferae (Stebbing), Hypothenemus twig feeders (33%) and one as a root feeder of her- birmanus (Eichhoff) and H. obscurus (Fabricius). baceous plants (2%; Table 3.5). In general, consid- Undoubtedly, if more of the intercepted scolytines ering the 58 species listed in Table 3.5, the had been identified to the species level (Tables 3.2, ambrosia beetles in the tribes Premnobini and 3.4), then more of the scolytine species listed as Xyleborini are polyphagous, inbreeding species established in the USA (Table 3.5) would have been and breed primarily in broadleaf woody plants; found among the intercepted scolytines. This is bark beetles are outbreeding with the species especially true for species of Coccotrypes and of Hylastini, Ipini, Phloeosinini, and Tomicini Hypothenemus, which were seldom identified ­breeding in conifers while the Scolytini breed in beyond genus in the PestID database. For example, broadleaf woody plants; Coccotrypes species are only 3 of 502 Coccotrypes interceptions and 63 of inbreeders and reproduce mostly in the seeds 821 Hypothenemus interceptions were identified to of palms and broadleaf woody plants; and species during 1985–2000 (Haack, 2001). For those Hypothenemus species are inbreeders, generally scolytines considered true bark beetles, a significant polyphagous, and reproduce in seeds and twigs of positive relationship was found between intercep- broadleaf woody plants (Wood, 1982; Wood and tion frequency and likelihood of establishment Bright, 1992; Jordal et al., 2002). Considering the (Brockerhoff et al., 2006; Haack, 2006). feeding guilds of the 58 exotic scolytines and their The species Hypothenemus africanus (Hopkins) interception histories (Haack, 2001), it is likely was included by Haack (2001) in an earlier list of that some of the ambrosia beetles and most seed exotic scolytines that were considered to be estab- and twig feeders arrived in association with seeds, lished in the continental USA. However, even fruit, cuttings and live plants, whereas the though the type specimen of H. africanus was ­remaining ambrosia beetles and nearly all bark first described from South Africa (Hopkins, beetles arrived in association with wood packag- 1915), it is now considered more likely that this ing material, logs, lumber and perhaps fuel wood. species is native to the Americas given its In the case of fuel wood, for example, from Exotic Bark and Ambrosia Beetles in the USA 65

1996 to 2009 the USA imported fuel wood from Seven of the exotic scolytines first reported 34 countries in Africa, Asia, the Caribbean, Central since 2000 were discovered as part of the United America, Europe, North America (Canada) and States Department of Agriculture, Forest Service South America, with a total declared value on ‘Early Detection and Rapid Response’ (EDRR) arrival of >US$98 million for the 14-year period project (Table 3.5; Rabaglia et al., 2008). The EDRR (Haack et al., 2010b). Overall, the majority of exotic project was initiated as a pilot project in 2001 and scolytines in both the USA and Europe are inbreed- in 2007 the program was expanded to full imple- ing, polyphagous species, which are traits that mentation. Approximately 15 different US states favor invasiveness (Kirkendall and Faccoli, 2010). now participate in the survey each year, which uti- We attempted to locate in the scientific lit- lizes pheromone- and karimone-baited traps at 12 erature the earliest year of collection or the first sites per state (Rabaglia et al., 2008). The relatively year of reporting for each of the 58 exotic scoly- steep rate of new scolytine detections since 2000 tines. In addition, we tried to identify the US is in part a reflection of the increased survey state in which the first collection of each species efforts such as EDRR. Given the success of the was made. We recognize that nearly all exotic EDRR project in locating previously unknown insects are present for many years before they exotic scolytines, as well as increasing public are first collected, and similarly that the found- awareness and surveys by other groups, it is likely ing population of each exotic may enter the USA that more exotics will be found in the years ahead. at a location that is very distant from where it is Anisandrus dispar, formerly in the genus later first collected. For two species, Coccotrypes Xyleborus, was the earliest recorded exotic scoly- dactyliperda and Hypothenemus crudiae (Panzer), tine in the continental USA (Peck, 1817; we were not able to determine the US state in Table 3.5). Overall, about 16% (n = 9) of the 58 which the first collections were made. In both exotic scolytines were first collected or reported cases, the first reports listed two US states in during the 1800s, 24% (14) during 1900–1949, which each was collected but did not provide any 40% (23) during 1950–1999 and 21% (12) during dates of collection (LeConte, 1868; Hopkins, 2000–2010. Taken as a whole, the species accu- 1915). Nevertheless, we feel that such data can mulation curve for exotic scolytines in the USA be used to approximate the historical arrival rate has shown accelerated growth over the past two and the areas of the country where the founding centuries (Fig. 3.2), reflecting a similar steep population first became established. increase in US imports (Haack, 2001; US Census

60

50

40 . species . 30 e no

20 Cumulativ 10

0 1800 1850 1900 1950 2000 Year of first collection or first report

y = 4E-14e0.0174x R² = 0.9645

Fig. 3.2. Cumulative number of detections of new exotic scolytines in the continental USA by year of first collection or first published report. Data are from Table 3.5. Exponential equation fitted to the data. 66 R.A. Haack and R.J. Rabaglia

Bureau, 2011). Similarly, accelerating species and Pennsylvania (4). There were only two accumulation curves have been documented for ­interior US states where new exotics were first exotic phloem and wood borers in the USA reported: Ambrosiophilus atratus in Tennessee (Aukema et al., 2010) as well as for exotic scoly- and Scolytus schevyrewi in Colorado (Table 3.5); tines in Europe (Kirkendall and Faccoli, 2010). If however, it is likely that Colorado and Tennessee we consider the 57 exotic scolytines on palms and were not the initial states where these two spe- woody plants, and the three major feeding guilds cies first became established, given that each sco- they represent, a pattern emerged where most lytine was found in several states when first early invaders were seed and twig feeders while reported (Atkinson et al., 1990; Negrón et al., most recent invaders were ambrosia beetles 2005). When considering the US states in which (Table 3.5). the 58 exotic scolytines were first reported, along The 58 exotic scolytines were first reported with their assigned feeding guild, there was a ten- from 16 US states (Fig. 3.3; Table 3.5). As dency for ambrosia beetles to establish in the expected, 14 of these 16 states have major mari- south-eastern USA, bark beetles in the north- time or land-based ports of entry given that they east, and seed and twig beetles along the south- border oceans, the Great Lakes or neighboring ern tier of states from California to Florida countries. The five states where the most exotic (Fig. 3.3). Overall, Florida was the state in which scolytines were first found were Florida (17 spe- most exotic ambrosia beetles (5 of 25), as well as cies), New York (8), California (7), Louisiana (4) seed and twig beetles (11 of 19) were first found,

A. All exotic scolytines B. Exotic ambrosia beetles

WA MI 2

N 2 Y MA 2 PA 3 CO MD 2 CA TN 2 1 AZ M G SC 1 1 TX L S A 1 2 1 A F L 5

C. Exotic bark beetles D. Exotic seed and twig beetles

1 6 1 1 1 2 3 1 1 1 2 2 1 11

Fig. 3.3. Maps of the contiguous 48 US states indicating the states (shaded) where the established exotic scolytines were first reported in the continental USA by feeding guild. Map A indicates the 16 US states where one or more of the 58 exotic scolytines now established in the USA were first reported, and also provides the state abbreviations as given in Table 3.5. Similarly, maps are presented for the first US state of detection for the 25 exotic scolytines classified as ambrosia beetles (Map B), the 13 species of exotic bark beetles (Map C), and the 19 seed and twig feeders (Map D). Data are from Table 3.5. Numbers within each US state (Maps B–D) indicate the number of exotic scolytines that were first found in each state by feeding guild. For the two exotic seed and twig feeders (Coccotrypes dactyliperda and Hypothenemus crudiae) that were each initially reported from two US states (Table 3.5), we credited each state for each scolytine. No map is shown for Hylastinus obscurus, which is a root feeder of herbaceous legumes that was first found in New York. Exotic Bark and Ambrosia Beetles in the USA 67

whereas 6 of the 13 exotic bark beetles were first in Table 3.5 were established elsewhere in the found in New York (Fig. 3.3). These geographic world prior to their initial detection in the USA patterns may reflect historical trade routes for (Wood and Bright, 1992; Haack, 2001, Brockerhoff specific imports and their typical scolytine asso- et al., 2006; Kirkendall and Faccoli, 2010). ciates, or they may indicate strict biological (hosts) and environmental (temperature and humidity) conditions that some scolytines require for successful establishment. For example, it is 3.8.1 Redbay ambrosia beetle, logical that many of the exotic Coccotrypes species Xyleborus glabratus would be restricted to the relatively warm south- ern tier of states, given that they breed in seeds Very few of the 58 exotic scolytines currently of palm trees. established in the continental USA have been Spread is the third step in the invasion proc- reported to cause widespread ecological and eco- ess after arrival and establishment (Liebhold and nomic damage in recent decades. Three notable Tobin, 2008). Using the scientific literature and exceptions include one bark beetle (Scolytus mul­ trapping data from the US Forest Service EDRR tistriatus) and two ambrosia beetles (Xylosandrus project (Rabaglia et al., 2008), we calculated the crassiusculus and Xyleborus glabratus). S. multi­ number of states in the continental USA in which striatus is associated with widespread mortality each of the current 58 exotic scolytines was of elm (Ulmus) in North America, primarily as a reported as of 2010 (Table 3.5). We recognize result of vectoring fungi that are the causal agents that these numbers underestimate the true range of Dutch elm disease (Evans and Finkral, 2010). of these exotics, given that extensive sampling X. crassiusculus has caused extensive mortality of has not occurred in all US states. Moreover, broadleaf trees, especially small-diameter trees, because no exotic scolytines have been reported both in the USA and in other countries where it from Alaska as of 2010, the values given in has been introduced (Kirkendall and Ødegaard, Table 3.5 refer to only the 48 contiguous US 2007). Details on the discovery, biology and states. Of the 58 exotic scolytines listed in Table impact of X. glabratus are presented below. 3.5, 19 species were still only reported from a sin- The redbay ambrosia beetle, X. glabratus, gle state, whereas 39 were reported from two or was first reported in the USA in 2002. The initial more states each (Table 3.5). Scolytus multistria­ collection consisted of three adult specimens cap- tus and S. rugulosus (Muller) were the only two tured in traps near Port Wentworth, Georgia, exotics found in all 48 contiguous US states as of that were deployed as part of the USDA Forest 2010. As expected, there was a weak but signifi- Service EDRR project (Rabaglia et al., 2006, cant positive linear relation between the number 2008). Additional delimiting trapping in 2002 of years since initial discovery in the USA and the and 2003 around Port Wentworth and Savannah, number of states currently occupied by the exotic Georgia, found no additional beetles and there- scolytines as of 2010 (F[1, 56] = 8.3, P < 0.0055, fore it was thought that X. glabratus was not actu- R2 = 0.13). ally established. In 2003 significant redbay The native range of the 58 exotic scolytines (Persea borbonia) mortality was reported on currently established in the USA include the con- Hilton Head Island, South Carolina. Although tinents of Africa (10 species), Asia (30), Europe this mortality was first thought to be the result of (8), Eurasia (9) and South America (1) (Table 3.5). drought or fluctuations in the local water table, Note that we considered Eurasia separately from X. glabratus and an unidentified fungus were rec- Europe and Asia for those species whose native ognized as the cause of the redbay mortality by range extends widely over both continents. Most 2004. Since 2004, X. glabratus was reported in species of ambrosia beetles were of Asian origin Florida in 2005, Mississippi in 2009 and Alabama (76%), most bark beetles were native to Eurasia in 2010. Although natural spread has occurred (46%), and most seed and twig feeders were of through adult flight, human-assisted movement African origin (47%; Table 3.5). It is possible that of infested host material is suspected in cases of some exotic scolytines now established in the long-distance spread. There is no USDA federal USA arrived from locations outside their native quarantine that regulates movement of potential ranges, given that several of the 58 species listed host material of X. glabratus as of 2010. 68 R.A. Haack and R.J. Rabaglia

It was soon realized that the symbiotic the parental gallery. In the south-eastern USA ­fungal associate of X. glabratus was extremely there are overlapping generations throughout pathogenic to redbay (Fraedrich et al., 2008). the year with one generation requiring about Harrington et al. (2008) described the fungus as a 60 days (Hanula et al., 2008). As the female brood new species (Raffaelea lauricola) and also identi- adults feed in the gallery and become reproduc- fied it as the causal agent of the disease now tively mature, R. lauricola fungal spores become known as laurel wilt. packed in the mycangia near their mandibles. X. glabratus is native to Bangladesh, India, After mating, the female brood adults emerge Japan, Myanmar and Taiwan, and in Asia it is from the dead or dying host trees and either rein- reported to infest Leucaena glauca, Lindera latifo­ fest the same tree if there is suitable wood mois- lia, Lithocarpus edulis, Litsea elongata, Phoebe lan­ ture, or fly off to infest new host trees. ceolata and Shorea robusta (Rabaglia et al., 2006). For many native and exotic xyleborine X. glabratus carries spores of R. lauricola in its ambrosia beetles, ethanol is an effective attract- mandibular mycangia and inoculates a tree as it ant. The first specimens of X. glabratus in North bores through the bark and enters the xylem. America were collected in ethanol-baited funnel The fungus causes disruption of water flow in traps (Rabaglia et al., 2006). However, additional the xylem, which results in vascular wilt and a trapping using ethanol showed that it was only characteristic discolouration or ‘streaking’ of the weakly attractive to X. glabratus, whereas outer sapwood. In Asia, neither R. lauricola nor manuka oil and phoebe oil were shown to be X. glabratus has been reported to cause laurel wilt. highly attractive (Hanula and Sullivan, 2008). In North America, R. lauricola has been isolated Hanula et al. (2008) also showed that X. glabratus only from members of the family Lauraceae, i.e., was attracted to cut redbay bolts or injured red- redbay, avocado (Persea americana), swampbay bay trees. Current survey efforts for laurel wilt (P. palustris), camphor tree (Cinnamomum cam­ and X. glabratus focus on visual detection of wilted phora), pondberry (Lindera melissifolia), pondspice host trees or traps baited with manuka oil. (Litsea aestivalis) and sassafras (Sassafras albidum). Although X. glabratus has been found infest- Of the 22 exotic Xyleborini established in ing sassafras, Hanula et al. (2008) noted that the USA (Table 3.5), most species, with the excep- X. glabratus was not attracted to cut bolts of sas- tion of some Xylosandrus species, attack injured, safras. Even though this may slow the spread of weakened or dying trees. Xyleborus glabratus the disease in sassafras, observations in Georgia appears to be similar to these non-aggressive spe- indicate that laurel wilt is able to persist in coun- cies with the exception of its highly pathogenic, ties where sassafras is common but redbay is rare symbiotic fungus. Dispersing X. glabratus adult (Mayfield et al., 2009). females appear to be attracted to host odors, and Laurel wilt is well established from coastal after landing they initiate tunneling on the main South Carolina to Florida, as well as along the trunk and branches. If the tree is healthy, coloni- Gulf coast of Mississippi, and eradication is no zation may be unsuccessful, but in the process of longer feasible. Due to the extreme virulence of tunneling the beetle can inoculate the tree with R. lauricola, the ability of X. glabratus to initiate the fungus. The fungus grows quickly in the sap- populations from single unmated females and its wood, restricting water flow that leads to wilting efficiency in vectoring the fungus, continued foliage. In redbay, which seems to be the most sus- high levels of redbay mortality are expected. Man­ ceptible North American host, the entire crown agement of laurel wilt in forested areas where will wilt over a period of a few weeks to a few redbay is common will be difficult. Limiting long- months, resulting in eventual tree death (Fraedrich distance, human-assisted spread of the beetle et al., 2008). As a tree declines, X. glabratus adults could delay the impacts of the disease in currently are attracted to the tree and soon colonize and unaffected areas. Efforts such as germplasm con- produce brood in the sapwood. Adult females servation or screening for tree resistance may be bore into the xylem where they lay eggs and culti- the best long-term hope for redbay and other vate the symbiotic fungus on which the larvae affected species. For high-value landscape trees, feed. As is typical for xyleborine ambrosia bee- chemical treatments may be an option. Mayfield tles, female progeny greatly outnumber the et al. (2008a) demonstrated the ability of macro- flightless males, and mate with their siblings in infusion of the fungicide propiconazole to protect Exotic Bark and Ambrosia Beetles in the USA 69

redbay trees from laurel wilt. The movement of insects. By contrast, in three surveys conducted X. glabratus and laurel wilt into the commercial after implementation of ISPM No. 15, insect avocado-growing region of southern Florida infestation rates of imported wood packaging threatens the avocado industry, as well as in other material were reported as 0.1% in the USA (Haack US states, Mexico and elsewhere in the Americas and Petrice, 2009), 0.3% in the EU (IFQRG, 2006; (Mayfield et al., 2008b). Members of the Lauraceae Haack and Brockerhoff, 2011) and 0.5% in are primarily woody plants and number about Australia (Zahid et al., 2008). If these values are 3000 species worldwide, reaching their greatest representative of actual pre- and post-ISPM No. diversity in the tropical and subtropical latitudes 15 infestation rates, they suggest that implemen- of Asia and the Americas (Chanderbali et al., tation of ISPM No. 15 has lowered the occurrence 2001), and therefore there are hundreds of plant of live wood-infesting insects moving in wood species that are potentially at risk from this packaging material. Nevertheless, it is important insect–fungus disease complex. to note that in all three surveys, live bark- and wood-infesting insects were still present in some wood packaging items that had been stamped 3.9 Future Prospects with the ISPM No. 15 logo. The presence of live insects on wood marked with the ISPM No. 15 The world community has taken positive steps logo could indicate improper treatment, pest tol- to reduce the risk of pests being moved inadvert- erance to the treatment, infestation after treat- ently in international trade. For example, in ment or fraud. To reduce the possibilities that 2002, signatories to the International Plant Pro­ bark-infesting insects could survive or infest after tect­ion Convention (IPPC) adopted International treatment (Evans, 2007; Haack and Petrice, Standards for Phytosanitary Measures No. 15 2009), ISPM No. 15 was revised in 2009 to set (ISPM No. 15), which was entitled ‘Guidelines maximum size limits for individual pieces of for Regulating Wood Packaging Material in residual bark on wood packaging material (IPPC, International Trade’ (IPPC, 2002). ISPM No. 15 2009). The approved tolerance limits for residual was first revised in 2006 and most recently in bark allow for bark pieces of any length if they are 2009 (IPPC, 2009). The goal of ISPM No. 15 is to less than 3 cm in width (as may occur along the ‘reduce significantly the risk of introduction and edge of a board) or if a bark piece is wider than spread of most quarantine pests’ (IPPC, 2009). 3 cm, the total surface area must be less than The two currently approved phytosanitary treat- 50 cm2 (slightly larger than a typical credit card) ments for wood packaging material include heat (IPPC, 2009). Worldwide implementation of the treatment to a minimum temperature of 56°C recent revisions in ISPM No. 15 (IPPC, 2009) for 30 min throughout the profile of the wood should further reduce the phytosanitary risk of and including the core, and fumigation with wood packaging material. methyl bromide following prescribed schedules It should be noted that most, if not all, (IPPC, 2009). New methods are under develop- of the exotic scolytines (Table 3.5) and other ment and when approved they will be added to wood-infesting insects (Haack, 2006; Haack ISPM No. 15. et al., 2009, 2010a) discovered in the USA since After approval of ISPM No. 15 in 2002, indi- approval of ISPM No. 15 in 2002 very likely vidual countries or groups of countries began to became established prior to 2002. Therefore, require their trading partners to follow ISPM No. future discoveries of exotic bark- and wood- 15 protocols over the succeeding years. For exam- infesting insects should not be considered as evi- ple, Canada, Mexico and the USA began full dence that ISPM No. 15 has failed, unless the implementation of ISPM No. 15 in 2006. pest population can be dated accurately and Very few surveys were ever conducted for linked to wood packaging material. Here again, it insects of quarantine significance on wood pack- should be noted that the stated goal of ISPM No. aging material prior to initiation of ISPM No. 15. 15 is not zero risk but rather to significantly In the paper by Bulman (1992), based on a ran- reduce risk (IPPC, 2009). dom survey for pests in wood packaging material Scolytines can move internationally in many during 1989–1991 in New Zealand, 2.7% of the other products besides wood. Many scolytines consignments with wood were infested with are intercepted in food items such as fruits and 70 R.A. Haack and R.J. Rabaglia

nuts, cut plants, nursery stock (plants for plant- Platypodidae from the U.S. and Bahamas. ing) and wooden handicrafts (Haack, 2001, 2006; Coleopterists Bulletin 45, 152–164. Kirkendall and Faccoli, 2010; USDA APHIS, Aukema, J.E., McCullough, D.G., Von Holle, B., 2010). In recognition of the phytosanitary risk of Liebhold, A.M., Britton, K. and Frankel, S.J. (2010) Historical accumulation of nonindige- international trade of live plants, a draft ISPM nous forest pests in the continental US. was released in 2010 for country consultation BioScience 60, 886–897. entitled ‘Integrated Measures Approach for Bright, D.E. (1968) Review of the tribe Xyleborini in Plants for Planting in International Trade’ (IPPC, America north of Mexico (Coleoptera: 2010). This draft ISPM does not provide specific Scolytidae). The Canadian Entomologist 100, treatments, as does ISPM No. 15 for wood pack- 1288–1323. aging material, but rather provides guidelines for Bright, D.E. and Rabaglia, R.J. (1999) Dryoxylon, exporting countries to follow in the areas of pro- a new genus for Xyleborus onoharaensis duction practices, such as use of pest-free mother Murayama, recently established in the south- stock, isolation of introduced plant material, best eastern United States (Coleoptera: Scolytidae). Coleopterists Bulletin 53, 333–337. management practices and treatments, and qual- Bright, D.E. and Skidmore, R.E. (1997) A Catalog of ity control (standard operating procedures, record Scolytidae and Platypodidae (Coleoptera) keeping, training, internal audits and traceabil- Supplement 1 (1990–1994). National Research ity). If approved and implemented, an ISPM that Council Press, Ottawa. deals with plants for planting would certainly Bright, D.E. and Skidmore, R.E. (2002) A Catalog of help reduce the phytosanitary risk now associ- Scolytidae and Platypodidae (Coleoptera) ated with international trade in live plants. Supplement 2 (1995–1999). National Research Council Press, Ottawa. Brockerhoff, E.G., Bain, J., Kimberley, M.O. and Acknowledgements Knížek, M. (2006) Interception frequency of exotic bark and ambrosia beetles (Coleoptera: Scolytinae) and relationship with establish- We thank Thomas Atkinson, Lawrence Kirkendall ment in New Zealand and world-wide. and Milos Knížek for providing technical data on Canadian Journal of Forest Research 36, scolytines; James LaBonte for providing unpub- 289–298. lished data; Joseph Cavey for providing PestID Bulman, L.S. (1992) Forestry quarantine risk of data from USDA APHIS; and Toby Petrice and cargo imported into New Zealand. New Zealand Therese Poland for providing critical comments Journal of Forest Science 22, 32–38. on an earlier version of this chapter. Byers, J.A. (2004) Chemical ecology of bark bee- tles in a complex olfactory landscape. In: Lieutier, F., Day, K., Battisti, A., Grégoire, J.C. and Evans, H. (eds) Bark and Wood Boring References Insects in Living Trees in Europe, a Synthesis. Kluwer Academic Publishers, Dordrecht, The Alonso-Zarazaga, M.A. and Lyal, C.H.C. (2009) Netherlands, pp. 89–134. A catalogue of family and genus group names Chanderbali, A.S., van der Werff, H. and Renner, in Scolytinae and Platypodinae with nomen- S.S. (2001) Phylogeny and historical biogeog- clatural remarks (Coleoptera: Curculionidae). raphy of Lauraceae: evidence from the chloro- Zootaxa 2258, 1–134. plast and nuclear genomes. Annals of the Anderson, D.M. (1974) First record of Xyleborus Missouri Botanical Garden 88, 104–134. semiopacus in the continental United States Chapman, J.W. (1910) The introduction of a (Coleoptera: Scolytidae). US Department of European Scolytid (the smaller elm bark bee- Agriculture, Cooperative Economic Insect tle, Scolytus multistriatus Marsh.) into Report 24, 863–864. Massachusetts. Psyche 17, 63–68. Atkinson, T.H., Rabaglia, R.J. and Bright, D.E. (1990) Chittenden, F.H. (1898) Fruit-tree bark beetle Newly detected exotic species of Xyleborus (Scolytus rugulosus Ratz.). US Department of (Coleoptera: Scolytidae) with a revised key Agriculture, Division of Entomology, Series 2, to species in eastern North America. Canadian Circular 29, Washington, DC. Entomologist 122, 93–104. Cognato, A.I., O’Donnell, R. and Rabaglia, R.J. Atkinson, T.H., Rabaglia, R.J., Peck, S.B. and Foltz, (2011) An Asian ambrosia beetle, Xylosan­ J.L. (1991) New records of Scolytidae and drus amputatus (Blandford) (Curculionidae: Exotic Bark and Ambrosia Beetles in the USA 71

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