We assessed the impact of the polyphagous shot hole borer (PSHB), Euwallacea whitfordiodendrus (Schedl), and Kuroshio shot hole borer (KSHB), E. kuroshio Gomez and Hulcr, on hardwood trees in southern California, southwestern China, and northwestern Vietnam. The highest levels of mortality were recorded from 10 of 39 tree species in the survey, and these were primarily native tree species.
Two invasive shot hole borers represent relatively recent introductions in southern California, USA, and continue to spread and cause injury and mortality to several native and ornamental tree species. They originate from Southeast Asia.
Knowledge of tree species susceptibility to these wood-boring beetles is essential to inform better pest management and to evaluate future risk for urban and wildland forests.
From 2012 to 2016, ground surveys were conducted in the invaded and native regions at PSHB/KSHB-infested and PSHB/KSHB-uninfested sites to record levels of tree injury and mortality on native and ornamental tree species.
In California, several native species of maple, Acer, willow, Salix, and sycamore, Platanus, were infested by either PSHB or KSHB at high rates (> 70%), and comparative rate of infestation by KSHB in all trees and in native trees surpased that by PSHB, whereas rate of infestation by PSHB in ornamental trees surpassed that by KSHB. Mortality of two maple species caused by PSHB exceeded 20%, whereas background mortality rate of hardwoods was 2% in uninfested areas.
These data should inform land managers about the tree species at most risk to injury and mortality, facilitate detection ground surveys, and direct prophylactic treatments for these invasive woodborers.
Invasive insects have caused widespread ecological and economic damage to North American forests (Wallner 1996; Mayfield et al. 2019). However, short-term ecological impacts, including intensity and speed of tree dieback and mortality, reduced populations of susceptible hosts, and loss of prominent canopy or keystone species, often highlight the impact of invasive species; gain the attention of the public; and demand and direct integrated pest management responses (Rizzo and Garbelotto 2003; Tisserat et al. 2009; Herms and McCullough 2014; Barnes et al. 2018). There has been a long history of establishment of invasive forest insects and diseases in the USA, primarily in the northeastern region of the country (Liebhold et al. 2013). Yet, the Pacific Coast region of the USA, specifically California, has also had a considerable number of introductions of invasive species that damage trees (Lee et al. 2007; Seybold et al. 2016, 2019a, b).
Two invasive ambrosia beetles, Euwallacea spp. Hopkins (Coleoptera: Scolytinae) (or (Coleoptera: Scolytidae) (Bright 2014; Bright 2019)), were first linked to tree injury and mortality in the early 2010s in southern California (Umeda et al. 2016). The polyphagous shot hole borer (PSHB), Euwallacea whitfordiodendrus (Schedl) (previously referred to as Euwallacea nr. fornicatus sp. No. 1 Eichhoff; O’Donnell et al. 2015), was first collected in 2003 in the region (Rabaglia et al. 2006; Seybold et al. 2016; Gomez et al. 2018b) but gained considerable attention when injury symptoms were first detected in 2012 on ornamental avocado trees, Persea americana Mill., in Los Angeles County (Eskalen et al. 2012). PSHB in California was identified initially as the tea shot hole borer (TSHB), Euwallacea fornicatus (Eichhoff) (previously referred to as Euwallacea fornicatus sp. No. 2; O’Donnell et al. 2015), because of their morphological similarity (Eskalen et al. 2013; Chen et al. 2017). However, DNA sequences from mitochondrial cytochrome oxidase c subunit 1 (COI) and cuticular hydrocarbon profiles support the status of PSHB and TSHB as separate taxa (O’Donnell et al. 2015; Chen et al. 2017; Stouthamer et al. 2017). Stouthamer et al. (2017) reported that the native range of PSHB may encompass Northern Thailand, Vietnam, China, Taiwan, and Okinawa.
Three symbiotic fungi, Fusarium euwallaceae S. Freeman, Z. Mendel, T. Aoki & O’Donnell; Graphium euwallaceae Lynch et al.; and Paracremonium pembeum Lynch et al. have been isolated from the mycangia of PSHB and from infected wood (Eskalen et al. 2013; Lynch et al. 2016). Among these fungal species, Fusarium euwallaceae was recovered at higher frequencies from the mycangia of PSHB and was the most prominent fungus found in the xylem of attacked trees (Cooperband et al. 2016; Lynch et al. 2016). Eskalen et al. (2012) referred to tree injury associated with PSHB and this fungus as “Fusarium dieback.”
Kuroshio shot hole borer (KSHB), E. kuroshio Gomez and Hulcr (previously referred to as Euwallacea nr. fornicatus sp. No. 5; O’Donnell et al. 2015, Gomez et al. 2018b), is a second exotic ambrosia beetle that was first detected in 2013 in urban forests of San Diego County (Chen et al. 2017; Stouthamer et al. 2017). KSHB is similar morphologically to PSHB and TSHB but differs in cuticular hydrocarbon phenotype (Chen et al. 2017) and in DNA sequence from the COI region (Stouthamer et al. 2017); it also carries novel Fusarium sp. and Graphium sp. symbionts (O’Donnell et al. 2015). KSHB populations in California are similar to populations in Taiwan and Okinawa, suggesting a possible origin for this species (Stouthamer et al. 2017).
Early collection records of TSHB originate from Southeast Asia where it has been associated with numerous economically important host species (Danthanarayana 1968; Wang and Yuan 2003; Kumar et al. 2011; Li et al. 2016; Gomez et al. 2019). However, there are limited host impact data associated with these, and other previous, host records. Tea shot hole borer has been introduced to several regions of the world, including Oceania, North and Central America, Africa, and Hawaii (Rabaglia et al. 2006; Mendel et al. 2012; CABI 2018; Paap et al. 2018). An Euwallacea sp. was recovered from an empty shipping container in Australia, further supporting the proclivity for spread of species in this genus (Stanaway et al. 2001). Danthanarayana (1968) provided an extensive list of 99 tree species in 36 families injured by TSHB in Southeast Asia, but TSHB is capable of reproducing in only 21 species.
Haack (2006) reported that in 2004 R.L. Penrose found E. fornicatus (i.e., PSHB) attacking species of maple, Acer L., alder, Alnus Mill., sycamore, Platanus L., and black locust Robinia L. in Los Angeles County. Since this initial survey, PSHB has been recorded in southern California from hundreds of tree species, and F. euwallaceae has been isolated from more than 100 tree species, but the beetle only reproduces in approximately 40 native, ornamental, and agriculturally important hardwood species (Eskalen et al. 2013; Boland 2016; Cooperband et al. 2016; UC Riverside 2018b). The discrepancy between the capacity to injure and the capacity to reproduce was also foretold with TSHB in Southeast Asia by Danthanarayana (1968). Host preference and susceptibility are still undefined and needed for developing integrated pest management options for these two invasive species.
PSHB and KSHB likely complete several generations a year in southern California (Cooperband et al. 2016; Chen et al. unpublished data). PSHB reproduce via arrhenotokous haplodiploidy (defined as the development of unfertilized haploid eggs into males and fertilized diploid eggs into females) and mate with siblings, which produces a collection of progeny that is female-biased and already mated by the time the new adult females emerge from a tree (Cooperband et al. 2016; Dodge et al. 2017). Newly emerged females have been observed to re-attack the same tree if the host is still a suitable substrate for the symbiotic fungi (TWC, unpublished data).
External injury symptoms associated with PSHB and KSHB entrance holes (attacks) can be observed primarily along the main stem and larger branches of trees and can also occur on exposed roots and from the root collar to the small diameter (< 2.5 cm) branches. Adult entrance holes are round and about 0.85 mm in diameter, and fine white boring dust emanates from the holes as tightly packed cylindrical columns, likely a result of the beetles usually attacking vigorous trees with moist xylem, or frass can be found at the base of trees (Coleman et al. 2013a). Depending on the tree species attacked, PSHB and KSHB injury symptoms can be identified either by wet discoloration, gumming, or sugary exudate near adult entrance holes on the outer bark of trees (Coleman et al. 2013a). High levels of PSHB/KSHB attacks on a tree can cause severe branch and crown dieback; epicormic growth along the stem and at the base of the tree; stem or branch failure; and eventual tree death (Coleman et al. 2013a).
PSHB and KSHB have caused injury and/or mortality to thousands of trees in southern California (CFPC 2015), mostly ornamental species in urban forests and native tree species in adjacent riparian forests located in the wildland-urban interface. However, the level of injury and risk to tree species from these invasive shot hole borers to ornamental and native tree species of southern California and elsewhere in the USA, are largely unquantified. Boland (2016) provided a thorough overview of KSHB attacks in one riparian corridor in San Diego County, but the tree injury and mortality data were not analyzed statistically and similar areas impacted by PSHB have not been assessed.
The absence of host preference, tree injury, and mortality data from invaded and native areas presents an obstacle to developing an integrated pest management program against these insect-disease complexes and assessing the risk of these complexes for other regions (Venette et al. 2010). The objective of this study was to assess the impact of PSHB and KSHB to ornamental and native tree species in southern California and in PSHB’s native region of China and Vietnam (Stouthamer et al. 2017; Smith et al. 2018). This information can assist with developing and focusing management actions on the most susceptible trees, reducing unwarranted treatments, and developing risk models.
Materials and methods
From May 2012 to April 2016, tree surveys were conducted to assess the impact (i.e., presence/absence and levels of infestation, tree injury, and tree mortality) from PSHB and KSHB in southern California forests. The impact of PSHB was assessed at 18 sites in urban and native forests in four infested counties (Los Angeles, Orange, Riverside, and San Bernardino). The impact of KSHB was assessed at three sites in urban and native forests in San Diego County. Each site included multiple survey plots (Fig. 1a). From 10 to 26 April 2015, surveys were also conducted to assess tree injury associated with PSHB in southwestern China and northwestern Vietnam to document impact of this beetle in its native region. Four infested sites were surveyed in southwestern China and five in northwestern Vietnam (Fig. 1b). Infested stands were identified from recorded distributional data (UC Riverside 2018a); through collection of Euwallacea spp. adults from infested trees; from trap captures on white elm bark beetle sticky panel traps (Synergy Semiochemicals, Delta, British Columbia, Canada, Product No. 4019); and through local knowledge by our coauthors.
Urban trees were surveyed along city streets, in neighborhoods, and in city and county parks, whereas trees in native forests were located mostly adjacent to or in riparian areas at the wildland-urban interface. These infested native stands were localized primarily at lower elevations and adjacent to infested urban areas. Native PSHB-infested forest sites were not only located principally on the Los Angeles Ranger District of the Angeles National Forest but also occurred in city, county, and wilderness parks and recreation areas. Across all sites, trees were chosen arbitrarily for assessments due to the diverse tree arrangements encountered (e.g., intensively managed parks, street trees, and dense forested areas immediately adjacent to creeks), but at least 50 trees were surveyed at a plot. Surveys encompassed all tree species in the area regardless of injury condition, and at least ten trees of a species were observed if available. Tree species could not be represented proportionately mostly due to the wide diversity of ornamental plantings found across the urban sites. Both ornamental and native tree species were found in the urban areas, whereas only a few ornamental or invasive plant species were found in the native areas. Latitude and longitude coordinates were recorded at all survey sites. Avocado groves maintained by California State Polytechnic University, Pomona were surveyed for PSHB injury in Los Angeles County as PSHB had spread to the university campus. Sites that were beyond the leading edge of spread of Euwallacea or had apparently escaped invasion (=uninfested sites) were surveyed to provide a baseline level of tree injury and mortality from other abiotic and biotic issues. These uninfested urban and native stands were located in Riverside, San Bernardino, and San Diego Counties. and on the San Gabriel Ranger District, Angeles National Forest and Front Country Ranger District, San Bernardino National Forest.
In southwestern China (Kunming, Yunnan Province), four urban sites were surveyed. They included the Southwestern Forestry University campus, Yunnan University, CuiHu Park, and Kunming city streets (Table 1). In northwestern Vietnam, six black wattle, Acacia mangium Willd., plantations at four sites with previously known PSHB-caused injury were assessed (Table 1). These plantations ranged from 3 to 7 years old; black wattle plantations are harvested in year seven. Although PSHB is likely native to these regions, mostly introduced ornamental and wood production species were surveyed in both countries, resulting in the documentation of novel host interactions for PSHB. At some of the urban sites, all trees were surveyed due to the limited number of trees available at a site.
We recorded data from all trees surveyed, including tree genus or species; diameter at breast height (DBH (in cm at 1.37 m)); tree status (living or dead); PSHB/KSHB infestation (yes or no); degree of crown thinning and dieback (ratings of 1: healthy, no apparent leaf or branch dieback; 2: minor twig dieback (10–25% leaf loss); 3: moderate branch dieback (26–50% leaf loss); 4: severe branch dieback (> 50% leaf loss); and 5: dead, no living crown); density of PSHB/KSHB injury along the main stem (0: no injury; 1: minor injury (1–10 attacks); 2: moderate injury (11–30 attacks); and 3: severe injury (> 30 attacks)); and other insect injury for infested and uninfested trees. The level of stem injury on moderately to severely injured and dead trees was quantified by recording the density of PSHB entrance holes in all three countries involved in the study. In California, entrance hole density was recorded within a 232-cm2 area at breast height (1.37 m) and at 0.3 m above the root collar. In southwestern China and northwestern Vietnam, entrance hole density measurements were only recorded at breast height because of time constraints. Measurements were taken on the north side of the tree to standardize our procedure, or were taken on the closest accessible area that was free of branches. Tree species, status, and DBH were noted for all trees with entrance hole density measurements. Crown ratings were not recorded for some tree species in the KSHB-infested sites in southern California because surveys were conducted during the winter season when leaves were absent, but all infested tree species were observed again during the growing season and rated for crown health. As a result, crown health ratings are available for each tree species surveyed. Variable radius prism plots (10 basal area factor) and fixed radius plots (0.04 ha) were established in black wattle plantations in northwestern Vietnam to characterize current forest stand conditions, including tree species present and tree status.
All statistical analyses were conducted in R (R Core Team 2016). A critical level of α = 0.05 was used for all analyses unless otherwise noted. The Kolmogorov-Smirnov test (R package “nortest”) and Levene’s test (R package “car”) were used to test normality and homogeneity of variances, respectively, where necessary. Proportion tests (R package “base”) were used for many comparisons, and the null hypothesis was equal percentages among groups (e.g., 50%:50% if comparisons were between two groups and 25%:25%:25%:25% if comparisons were among four groups). When analyzing proportion of infestation among tree species, only species with greater than five trees surveyed were included to meet the accuracy requirement of greater than 5 in each cell. Tree species only surveyed five times or greater were included in all analyses (see Table 2), but all data were presented to show potential trends.
For trees at infested sites in California, infestation rates between PSHB and KSHB and between ornamental and native trees were analyzed by proportion tests. Assessments between ornamental and native trees were analyzed to compare the potential impact in native and ornamental forested areas. Crown ratings between the PSHB- and KSHB-infested sites were compared by proportion tests, separately for each rating (from “1” to “5”). Stem injury ratings between the PSHB- and KSHB-infested sites were also compared by proportion tests, separately for each rating (from “0” to “3”). For tree species that occurred in both the PSHB- and KSHB-infested sites, comparison of infestation rates between PSHB and KSHB was conducted by a proportion test, separately for each species. No comparisons were made for tree species that occurred uniquely in either a PSHB- or KSHB-infested site.
For trees in the PSHB- and KSHB-infested sites, the following analyses were conducted separately for the PSHB- and KSHB-infested sites. Infestation rate was analyzed by a proportion test (i.e., if the rate deviated from 50%). Infestation status (i.e., infested or uninfested) and mortality by tree types (i.e., native or ornamental) were analyzed by proportion tests. DBH by infestation (i.e., infested or uninfested), DBH by tree status (i.e., live or dead), DBH by tree types (i.e., native or ornamental), DBH by tree species, and DBH by stem injury rating were either analyzed by Wilcoxon-Mann-Whitney tests if there were two groups or by Kruskal-Wallis rank sum tests if there were more than two groups. Differences in percentages of trees among various crown ratings or stem injury ratings were analyzed by proportion tests. Crown ratings or stem injury ratings among tree species were analyzed by Kruskal-Wallis rank sum tests. Entrance hole density (number of holes/232 cm2 on the bark surface at 1.37 and 0.3 m) between two heights and between tree types (i.e., ornamental or native) was analyzed by Wilcoxon-Mann-Whitney tests and among tree species was analyzed by Kruskal-Wallis rank sum tests. Density of entrance holes was not different between the height measurements for the southern California data, so data were pooled when analyzing effects of tree types and tree species on density.
For data collected in southwestern China, difference in DBH between tree species and differences in colonization density between tree species were analyzed by Kruskal-Wallis rank sum tests. Difference in DBH between infested and uninfested trees was analyzed by a Wilcoxon-Mann-Whitney test.
For data collected in northwestern Vietnam, difference of DBH between infested and uninfested trees was analyzed by a Wilcoxon-Mann-Whitney test. Difference in percentage of trees in various stem injury classes was analyzed by a proportion test.
A total of 5644 trees representing 39 tree species were surveyed in the PSHB/KSHB-infested and PSHB/KSHB-uninfested stands in southern California (Table 2). Of the 4535 trees from the PSHB sites, 2052 and 2483 were from the PSHB-uninfested and PSHB-infested sites, respectively. Of the 1109 trees from the KSHB sites, 519 and 590 were from the KSHB-uninfested and KSHB-infested sites, respectively. Mean DBH of all surveyed trees was 21.1 cm (± 0.28). All the following comparisons were made within the infested sites only unless otherwise noted.
Rate of infestation by KSHB was significantly higher than rate of infestation by PSHB across all species (Table 3 (Infestation)). Rate of infestation by PSHB in ornamental trees was significantly higher than KSHB in ornamental trees (Table 3 (Infestation)). Rate of infestation by KSHB in native trees was significantly higher than PSHB in native trees (Table 3 (Infestation)).
Most trees in the survey had healthy crowns (crown rating of “1”) (Fig. 2), a significantly lower proportion of trees in the KSHB sites had healthy crowns when compared with trees at the PSHB sites (Table 3 (Crown rating)). Crown dieback differed significantly between the PSHB and KSHB sites for all crown ratings except for a crown rating “2” (Table 3 (Crown rating)). Overall rate of tree mortality (crown rating of “5”) caused by both KSHB and PSHB was low, and not different between the two species (Table 3 (Crown rating)). An additional 3 (0.63%) and 32 (1.29%) trees were found dead in the KSHB and PSHB sites, respectively, but with no injury from either ambrosia beetle species. Stem injury was significantly different between the PSHB-infested and KSHB-infested sites for minor (rating of “1”) and severe stem injury (rating of “3”) (Table 3 (Stem injury rating)). Stems were injured more severely at the KSHB-infested sites.
PSHB infested 25.5% of American sweetgum, Liquidambar styraciflua L., and 23.0% of evergreen ash, Fraxinus uhdei (Wenz.) Lingl., whereas KSHB did not infest either of the two tree species (Tables 2 and 3 (Infestation by species)). The differences in infestation between the two beetle species for American sweetgum, evergreen ash, arroyo willow, Salix laevigata Benth., Fremont cottonwood, Populus fremontii S. Watson, Goodding’s black willow, Salix gooddingii C.R. Ball, southern magnolia, Magnolia grandifolia L., western sycamore, Platanus racemosa Nutt., and castorbean, Ricinus communis L., were not significant (Table 3 (Infestation by species)). Twenty tree species did not have KSHB injury but had varying levels of PSHB injury (Table 2). Golden medallion, Cassia leptophylla Vogel, was infested (95%, 19/20) by KSHB but was not surveyed in the PSHB-infested sites.
At the PSHB-infested sites, significantly more trees were infested than uninfested and the infestation rate on native trees did not differ from that on ornamental trees (Fig. 3a). Mortality of native trees was significantly greater than that of ornamental trees (Fig. 3a). DBH (mean (±s.e.)) of the PSHB-infested trees ranged from 0.25 to 122 cm but did not differ from that of the PSHB-uninfested trees (Fig. 3b). DBH of dead trees was smaller than that of living trees (Fig. 3b). DBH of the PSHB-infested ornamental trees was greater than that of the infested native trees (Fig. 3b). DBH of the infested trees differed among tree species (X262 = 586; P < 0.001) and among stem injury ratings (no injury, 34.3 cm (± 21.6); minor, 30.4 cm (± 0.72); moderate, 34.7 cm (± 1.48), and severe, 27.1 cm (± 0.94)) (X32 = 36.4; P < 0.001).
At the PSHB-infested sites, the percentages of crown ratings of all trees and PSHB-infested trees deviated from 20% (i.e., equal percentages for each crown category) (X42 = 2764; P < 0.001 and X42 = 878; P < 0.001, respectively). At these sites, the majority of all trees had healthy crowns (61.3%) followed by minor dieback (17.7%), moderate dieback (8.62%), severe dieback (5.44%), and dead trees (5.64%). Similarly, the majority of the PSHB-infested trees had healthy crowns, 47.7% (703/1473) followed by minor dieback, 23.8% (351/1473); moderate dieback, 11.6% (171/1473); severe dieback, 7.33% (108/1473); and dead trees, 9.50% (140/1473). Eleven tree species were killed by PSHB, including boxelder maple, A. negundo L., castorbean, bigleaf maple, A. macrophyllum Pursh, arroyo willow, red willow, Salix laevigata Bebb, Goodding’s black willow, Fremont cottonwood, London plane, Platanus x acerifolia (Alton) Willd., California bay laurel, Umbellaria californica (Hook. & Am.) Nutt., western sycamore, and white alder, Alnus rhombifolia Nutt., (Table 2). Mortality rates for boxelder maple, castorbean, and bigleaf maple exceeded 20% (Fig. 4a).
At the PSHB-infested sites, no stem injury (40.4%) was most the frequent survey outcome followed by minor injury (30.8%), severe injury (20.1%), and moderate injury (8.74%); these percentages deviated from 25% (X32 = 556; P < 0.001). Of the 1473 PSHB-infested trees, 51.5, 14.7, and 33.8% trees had a stem injury ratings of 1, 2, and 3, respectively; these percentages deviated from 33.3% (X22 = 880; P < 0.001).
At the PSHB-infested sites, stem injury differed among tree species (X1052 = 1617; P < 0.001). PSHB severely injured boxelder maple, castorbean, bigleaf maple, arroyo willow, red willow, Goodding’s black willow, Fremont cottonwood, London plane, California bay laurel, western sycamore, and white alder (Table 2). Branch and stem failure were observed on western sycamore and white alder following severe PSHB stem injury during the surveys (Fig. 4b). High levels (> 20%) of severe stem injury were recorded on boxelder maple, castorbean, bigleaf maple, red willow, and western sycamore by PSHB (Table 2).
At the KSHB-infested sites, significantly more trees were infested than uninfested, and the infestation rate on native trees was significantly greater than that on ornamental trees (Fig. 3a). The mortality rate of native trees did not differ from that of ornamental trees (Fig. 3a). DBH of KSHB-infested trees ranged from 2.79 to 53.6 cm, which was significantly greater than the DBH of KSHB-uninfested trees (Fig. 3b). DBH of trees killed by KSHB was smaller than that of living trees (Fig. 3b). DBH of infested trees differed among tree species (X102 = 81.2; P < 0.001) but not among stem injury ratings (no injury, 18.6 cm (± 2.86); minor, 21.4 cm (± 1.17); moderate, 23.2 cm (± 1.44); and severe injury, 20.6 cm (± 0.56)) (X32 = 2.02; P = 0.57).
Of the 473 trees with a recorded crown rating at the KSHB sites, the percentages of healthy crowns (53.3%); minor (17.1%), moderate (19.5%), severe dieback (5.44%), and dead trees (5.64%) deviated from 20% (X42 = 444; P < 0.001). Of the 274 KSHB-infested trees surveyed with crown ratings, 90 (32.8%), 58 (21.2%), 81 (29.6%), 8 (2.92%), and 37 (13.5%) had healthy crowns to dead trees, respectively, and the percentages deviated significantly from 20% (X42 = 128; P < 0.001). Fremont cottonwood, Goodding’s black willow, arroyo willow, London plane, and western sycamore were killed by KSHB (Table 2). Fremont cottonwood had the highest tree mortality associated with KSHB (9.62%) and the other four species ranged from 3.51 to 9.52% (Table 2).
At the KSHB-infested sites, 34.9% of trees had no stem injury, 13.2% had minor injury, 9.49% had moderate injury, and 41.9% had severe injury; these percentages deviated from 25% (X32 = 182; P < 0.001). Of the KSHB-infested trees, most had severe stem injury (1, 78 (20.3%); 2, 56 (14.6%); and 3, 247 (64.3%)); these percentages deviated from 33.3% (X22 = 347; P < 0.001).
At the KSHB-infested sites, stem injury differed among tree species (X1052 = 199; P < 0.001). No entrance holes were observed in ten of the tree species (Table 2). Over 20% of golden medallion, castorbean, arroyo willow, western sycamore, Goodding’s black willow, Fremont cottonwood, and London plane had severe stem injury (Table 2).
To gauge entrance hole densities, 49 trees from eight species (i.e., avocado, bigleaf maple, boxelder maple, castorbean, coast live oak, red willow, western sycamore, and white alder) were surveyed in southern California. Mean DBH of the trees surveyed was 19.2 cm (± 2.4). Mean entrance hole density (count/232 cm2) across all tree species was 17.3 (± 2.3) and 15.3 (± 2.4) holes at 1.37 and 0.3 m, respectively (X12 = 0.98; P = 0.32), so data were pooled for the two measurements (Table 4). Mean entrance hole densities (pooled over two heights) on native trees (15.2 (±2.59)) did not differ from those on ornamental trees (21.6 (± 4.27)) (X12 = 2.82; P = 0.09). Entrance hole densities differed among tree species (X72 = 21.2; P < 0.01); density was significantly higher on boxelder maple and lower on red willow (Table 4).
At sites that had no evidence of infestation by Euwallacea, tree mortality was low (2%) and healthy crown ratings dominated the individual tree conditions (PSHB, 98.3% (510/519); KSHB, 99.2% (2036/2052)). Common willow agrilus, Agrilus politus (Say), was the most prominent injury agent, other than PSHB/KSHB, found attacking arroyo willow (6×) and red willow (9×) in uninfested and infested stands (13×). Only two dead arroyo willows were found with common willow agrilus injury. American black bear, Ursus americana (Pallas), injury (i.e., claw marks) was the second dominant tree injury surveyed on white alder (7×), white mulberry (3×), and western sycamore (4×). Carpenterworm, Prionoxystus robiniae (Peck), injury was observed twice on coast live oak, Quercus agrifolia Née (one living and one dead tree) (Swiecki and Bernhardt 2006).
A total of 168 trees representing nine species were surveyed at four sites in Kunming. DBH (mean (± s.e.)) of all surveyed trees was 30.1 cm (± 1.36; n = 168), and DBH differed among tree species surveyed (X82 = 107; P < 0.001) (Table 2). Infestation rates were highest on trident maple, Acer buergerianum Miq., (55.8%) and oriental plane, Platanus orientalis L., (57.5%) (Table 2, Fig. 4c). One stem of wisteria, Wisteria, Nutt., stem (5.84 cm DBH) and two Chinese banyan, Ficus microcarpa L.f., (mean DBH 13.21 cm (± 1.27)) were infested by PSHB. One Chinese banyan had severe crown dieback. DBH (mean (±s.e.)) of infested trees was 37.2 cm (± 1.90; n = 56), which was significantly greater than that of uninfested trees (26.1 (± 1.76 cm) (n = 112)) (X12 = 17.0; P < 0.001). DBH of infested trees ranged from 5.8 to 86.4 cm. Crown thinning and dieback were only evident on trees with severe PSHB injury.
Branch dieback and partial death of the main stem from PSHB was evident on numerous trident maple and oriental plane trees (Table 2; Fig. 4c). The majority of trees surveyed had healthy crowns (Fig. 2). Moderate (14.8%, 7/47) and severe (4.26%, 2/47) dieback were observed on oriental plane during the surveys. New plantings of oriental plane along the street suggested previous tree mortality associated with PSHB, which was verified by Li. Moderate dieback of trident maple (13.3% (6/45)) was recorded during the surveys, whereas crowns of remaining tree species were all healthy (Fig. 3). Severe stem injury from PSHB was recorded on wisteria (100% (1/1)), oriental plane (34.0% (16/47)), and trident maple (31.1% (14/45)) (Table 2). Oriental plane and trident maple also had stem injury that could be classified as minor (26.7% (12/45); 19.1% (9/47), respectively) and moderate (2.22% (1/45); 4.26% (2/47), respectively). Entrance hole densities of PSHB (per 232 cm2) on the stem at 1.37 m across the three species was 18.5 (± 3.76) and did not differ among the species (i.e., trident maple, Chinese banyan, and oriental plane) (X22 = 4.98; P = 0.08).
A total of 116 black wattle trees were surveyed in six plantations at four sites in northwestern Vietnam and low levels of tree injury were associated with PSHB at these sites. Most of the black wattle plantations surveyed were four to 5 years old; one plantation was 7 years old (Fig. 4d). DBH of the PSHB-infested trees ranged from 4.57 to 42.9 cm. DBH (mean (±s.e.)) of the infested and uninfested black wattle (n = 116) was 13.6 cm (± 0.23), and DBH of the infested black wattle (n = 34) was 11.3 cm (± 0.98), which was significantly smaller than uninfested trees (14.6 cm (± 0.68)) (X12 = 8.44; P < 0.01) (Table 2). Mean total basal area of black wattle plantations surveyed was 11.2 m2 ha−1 (± 0.34). Mean basal area of trees injured by PSHB was 0.55 m2 ha−1 (± 0.13), representing 4.9% of the basal area in the plantations. Mean stem density in the plantations was 532 ha−1 (± 99.9) with 15.2 ha−1 (± 13.2) infested, representing a 2.9% infestation rate. Only 1% of the surveyed black wattle were killed by PSHB (Table 2).
Crowns of nearly all (98.3% = 114/116) trees in the survey were healthy, suggesting a low level of injury across the plantations. Of the 116 surveyed trees, 84 (72.4%), 19 (16.4%), 5 (4.31%), and 8 (6.89%) had PSHB stem injury ratings of 0, 1, 2, and 3, respectively (Table 2) (X32 = 143, P < 0.001). We observed two (1.72%) black wattle trees killed by PSHB (mean DBH 5.59 cm (± 1.02)) across all sites and several pruned black wattle stems resting on the forest floor were attacked by PSHB at one site. Castorbean was also observed with severe PSHB injury near Hanoi. Mean DBH (cm) and number of PSHB entrance holes (per 232 cm2) along the main stem of eight PSHB-infested black wattle was 43.2 (± 14.3) and 10.6 (± 2.65), respectively (Table 3).
Two invasive shot hole borers represent new threats to native and ornamental tree species in southern California, and potentially outside of this region in the USA and Mexico (García-Avila et al. 2016). Many land ownerships in southern California have already directed labor and funding to manage and remove dead and dying trees associated with PSHB/KSHB (California Legislature 2018). In our impact survey of southern California, each ambrosia beetle species showed high levels of infestation (> 59%), but KSHB caused more impact in its limited distribution in San Diego County. In its invaded range, KSHB has infested more native tree species than PSHB because the KSHB-infested areas have typically been riparian corridors in or near San Diego County parks. In contrast, PSHB has infested more species of ornamental trees than KSHB. This outcome may be a consequence of the spread of PSHB throughout the urban areas of Los Angeles, Orange, Riverside, and San Bernardino Counties.
Although the two shot hole borers are considered different species, the invasive populations of each in California share many biological and ecological similarities with respect to tree injury, tree mortality, and host size and host species preference. For both PSHB and KSHB, the highest infestation rates (> 40%) were recorded on arroyo willow, Fremont cottonwood, Goodding’s black willow, western sycamore, white alder, and castorbean (Table 2). Similar infestation rates (0 to 25%) for both beetle species were recorded on several other tree species, including American sweetgum, evergreen ash, and southern magnolia (Table 2).
Even though infestation levels by both beetles were exceptionally high for some tree species, tree mortality rates across all hardwood species were low (KSHB, 7.8%; PSHB, 5.6%) and just above background (2%). Within certain species of maples and willows, however, the mortality rates ranged from nearly 10% (KSHB) to over 25% (PSHB) (Tables 2 and 5). These levels of tree mortality from Euwallacea sp. are considerably lower when compared with other invasive species, including the goldspotted oak borer, Agrilus auroguttatus Schaeffer (13% of oaks; 48% on some survey plots); and the causal agent of sudden oak death, Phytophthora ramorum Werres et al. (3.1% for coast live oaks, 2.4% for black oaks, and 5.4% for tanoaks, per year over an 8-year survey interval); and native bark beetles in California (Rizzo and Garbelotto 2003; Rizzo et al. 2005; McPherson et al. 2010; Coleman et al. 2012; CFPC 2014, 2015, 2016, 2017). However, even the loss of a few trees in an urban setting can impact local esthetics considerably and lead to costly management, tree removal, and/or replacement.
Crown ratings have been used frequently in hardwood tree assessments to determine general health (Schomaker et al. 2007; Coleman et al. 2011; Hishinuma 2017), and many (> 53%) of the infested and uninfested trees in the PSHB- and KSHB-infested sites had ratings that suggested healthy crowns (Fig. 2). Minor, moderate, and severe crown dieback were evident in these sites but at lower percentages (< 20%). Moderate dieback was more prevalent in the KSHB-infested sites and likely a consequence of the high population pressure or the duration of infestation of this species in the Tijuana River Valley Regional Park (Boland 2016). Although Boland (2016) first reported instances of tree injury at this location, mortality quickly escalated to hundreds of thousands of trees within a year (CFPC 2017). The level of infestation and mortality from KSHB in this park was not observed elsewhere in the region or from PSHB. The extent of injury may be due to the dense stand conditions of susceptible hosts or other currently unknown contributing factors (e.g., high soil moisture) (Boland 2016).
Stem injury ratings also indicated a more pronounced impact by KSHB. Severe stem injury was prevalent in the KSHB-infested stands (41.9%), whereas stem injury classified as minor (40.4%) and severe (20.1%) occurred in the PSHB-infested stands. Severely injured trees likely will lead to patches of dead cambium, branch and stem failure, or complete tree mortality. Trees with this level of injury in developed sites will likely have to be removed because they cannot be saved with prophylactic or restorative treatments, and infested branches and trees have been shown to be attractive to PSHB (Byers et al. 2017). Stem injury ratings should be modified in the future to include very high densities of entrance holes (> 100), so injury level can be quantified with greater precision.
In southern California, trees do not appear to be succumbing to Fusarium dieback under low levels of injury from either beetle species. Symbiotic fungi carried by either species do not appear to be as pathogenic as the laurel wilt fungus associated with redbay ambrosia beetle, Xyleborus glabratus Eichh., on redbay, P. borbonia (L.) Spreng, in the southeastern USA (Evans et al. 2014). The combination of mechanical injury from gallery construction by the female parent and fungal inoculation at high densities along the main stem or branches leads to tree mortality. Infestation rate may have been overestimated because trees with low levels of attack may not have been suitable or preferred hosts for either PSHB or KSHB, i.e., these may have been unsuccessful attacks. The success of colonization attempts is difficult to ascertain during surveys without cutting into the xylem of a tree, which is often not an option in urban sites. Evidence of newly produced boring dust may be a second approach to gauge active infestations, but timing of surveys and weather may mask this symptom. Trees that produce a gumming response at the site of entry are often not hosts of either ambrosia beetle (Danthanarayana 1968; Eskalen et al. 2013).
In heavily infested sites, it appears that these ambrosia beetles may attack trees indiscriminately when populations are high, which may explain the elevated numbers of tree species reported previously to harbor entrance holes (Danthanarayana 1968; Eskalen et al. 2013), but relatively few of these have been confirmed as reproductive host species. This trend has been reported with bark beetle species during epidemics (Gibson et al. 2009; Hain et al. 2011), and may likely occur with other non-favored tree species when invasive shot hole borers have reached outbreak levels by attacking numerous favored host species in the vicinity.
PSHB killed more native trees than ornamental trees. Loss of hardwood canopy cover, basal area, and stem density from PSHB and KSHB may affect habitat for some threatened and endangered wildlife species, including arroyo toad, Anaxyrus californicus (Camp) and southwestern willow flycatcher, Empidonax traillii extimius (Audubon), in native riparian stands of southern California (Hatten and Paradzick 2003; Mitrovich et al. 2011). Thus, management options for PSHB and KSHB may be limited in these riparian corridors (e.g., because of the presence of endangered wildlife species or because of restrictions on insecticide applications near open water).
Both ambrosia beetles attacked trees in a wide range of diameter size classes; even the smallest stems (~ 2.0 cm DBH) were colonized across the three countries. Smaller trees were generally attacked and killed by both species, but the statistical significance of this small diameter difference may not transfer to biological significance. Because both beetle species attack trees in a wide range of diameter size classes, most ornamental and native host species are at risk to injury from the invasive shot hole borers.
Crown health ratings of infested trees detected in the southern California surveys suggested that additional trees will be killed by both species, i.e., the mortality rates may continue with time (McPherson et al. 2010). Eighteen and thirty-one percent of trees had moderate to severe dieback from PSHB and KSHB, respectively. Twelve tree species (PSHB, 12 species; KSHB, 5 species) were killed by at least one of these invasive beetles, and at least 29 individuals each of boxelder maple, castorbean, bigleaf maple, arroyo willow, red willow, Goodding’s black willow, Fremont cottonwood, London plane, California bay laurel, western sycamore, and white alder were surveyed in PSHB-infested sites (Table 2). Boxelder maple, castorbean, and bigleaf maple sustained the highest tree mortality (> 20%) from PSHB (Fig. 4a). Paap et al. (2018) reported an invasive populations of PSHB also attacking sentinel plantings of London plane in South Africa. At the KSHB-infested sites, mortality rates of Fremont cottonwood, Goodding’s black willow, arroyo willow, London plane, and western sycamore were < 10%, and each species was surveyed as at least 35 individuals (Table 2). Several willow species (i.e., arroyo, red, and Goodding’s black) were killed at rates of 8 to 16% by both invasive shot hole borers. Boxelder maple and castorbean have also been attacked by PSHB in Israel (Mendel et al. 2012). Euwallacea validus (Eichhoff), another invasive species, was found attacking tree of heaven, Ailanthus altissima (Mill.) Swingle and striped maple, Acer pensylvanicum L., in the eastern USA (Cognato et al. 2015), suggesting some uniformity in host range for the genus Euwallacea.
Severe stem injury was > 33 and > 64% among infested trees at the PSHB- and KSHB-infested sites, respectively. This underscores that tree mortality could continue after our surveys. Severe stem injury from PSHB was recorded on 16 tree species, whereas severe stem injury from KSHB was recorded on eight tree species. Species not killed by PSHB were American sweetgum, southern California black walnut, evergreen ash, and coast live oak. Golden medallion and castorbean had severe stem injury from KSHB, but neither of these species died in the KSHB-infested sites. Only one tree species, California bay laurel, attacked at low levels by PSHB, was killed, but in this isolated instance, contributing factors were likely. No other trees succumbed to PSHB or KSHB with low and moderate levels of stem injury and this same trend was reported in South Africa with PSHB (Paap et al. 2018).
Entrance hole densities recorded from two areas on the main stem of severely injured or dead trees across all tree species and all three regions suggested that a mean density threshold of 18.0 in a 232-cm2 area likely results in severe crown dieback or tree mortality. Because trees with this level of injury likely cannot be saved with insecticide and/or fungicide treatment, they should be removed and the wood should be handled properly to reduce the population pressure in an area (Jones and Paine 2015; Chen et al. unpublished data). High levels of attacks (6 to 19 per branch) were recorded from TSHB on branches of SOM in India, resulting in branch failure (Kumar et al. 2011). Thus, to facilitate management, a mean of > 18 attacks in a 232-cm2 sampling area can be used as a threshold to trigger removal of actively infested trees, particularly in southern California where the infestation is still spreading.
The urban settings surveyed in southwestern China were similar to those in southern California. Not surprisingly, PSHB infested a sycamore and a maple species, i.e., oriental plane and trident maple, respectively. Infested trees were generally larger in DBH than uninfested trees, which contradicted data collected in southern California. Previous surveys of PSHB injury in the same areas have recorded injury to smaller diameter trident maple (~ 10 cm DBH). This result may be linked more to population pressure and not to a diameter threshold with the trees (QL, unpublished data). Oriental plane and trident maple in southwestern China had high rates of infestation (> 55%) and severe stem injury. However, previous infestation rates from PSHB in this area were > 80% on trident maple (Li et al. 2015). The decrease in infestation rates may be explained by the loss of older trees to PSHB and the replanting of smaller trident maple. PSHB will likely continue to injure and kill trees in these sites because it is difficult to obtain permission to conduct active management (e.g., the removal of infested branches and trees) in a timely manner in Chinese urban forests.
In northwestern Vietnam, PSHB was not a major threat to black wattle plantations (1% infestation rate), but small diameter trees were observed with injury. High levels of attack densities appeared to be required to kill black wattle. It was difficult to determine why certain trees were getting attacked and if there were any contributing factors to the infestations and tree mortality in these plantations. A couple of the plantations in the survey were planted on old tea plantations or adjacent to current tea plantations, which was a potential association for future investigation. However, better sanitation of discarded cut stems on the forest floor could reduce localized PSHB populations and subsequent attacks on adjacent living trees. The short growing rotation of these plantations (approx. 7 years) may further limit the extent of tree injury and mortality and could serve potentially as a sanitation cut before new plantings.
Conclusions and future directions
These survey data represent a snap shot in time of the impacts associated with these two invasive beetles. Follow-up surveys and long-term plots should be established in urban and wildland forests to capture the impacts at newly infested sites. However, tree species observed with high levels of infestation, severe stem injury, and incidences of tree mortality will likely be the most susceptible to PSHB and KSHB as they spread in California (Table 5). The similarities of injury and mortality across several host species from PSHB/KSHB suggest that similar management recommendations and risk models can be developed for the two invasive species in the USA. These data should inform land managers about the tree species at most risk to injury and mortality, facilitate ground surveys, and direct prophylactic treatments.
Future damage by PSHB and KSHB could be forthcoming in California’s diverse agricultural crops. Many have raised concern about the potential threat of PSHB to avocado production worldwide, and branch dieback and mortality have been reported in Israel and California (Eskalen et al. 2012; Mendel et al. 2012; Freeman et al. 2013). However, we observed only low levels of injury from PSHB in an infested avocado grove in southern California. Our data suggest avocado is not a preferred host of PSHB, but additional surveys are needed to confirm potential impacts to production. Furthermore, TSHB did not cause damage to avocado plantations in southern Florida (Carrillo et al. 2016). Preliminary host range tests of English walnut, Juglans regia L., by our group suggest that multiple cultivars can serve as hosts for PSHB (Coleman et al. 2013b; Chen et al. 2014). Other fruit and nut tree crops grown in California’s Central Valley, e.g., almond, Prunus dulcis (Mill.) D. A. Webb, persimmon, Diospyros spp. L., pistachio, Pistacia vera L. pomegranate, Punica grantum L., and other Prunus, may also be vulnerable to PSHB and KSHB should their distributions expand. The use of sentinel tree plantings of dominant forest and agriculturally important tree species from the USA in the native range of these Euwallacea spp. may assist with host testing and future risk assessments (Vettraino et al. 2015).
Invasive shot hole borers (PSHB and KSHB) have spread to additional southern California counties since their initial detections in Los Angeles and San Diego Counties, respectively. Natural flight dispersal, movement of green waste from urban areas (TWC, personal observation), movement of firewood and nursery stock, and a diverse host range may be facilitating the spread of these species. TSHB is already present in the southern USA (i.e., Florida) (Carrillo et al. 2016). Euwallacea interjectus (Blandford), E. similis (Ferrari), and E. validus have been introduced into the USA to Florida, Georgia, Kentucky, South Carolina, Texas, and Virginia; Texas; and 17 states including nine primarily in the southeastern USA, respectively (Gomez et al. 2018a), suggesting that the distributions of PSHB and KSHB may spread to the coastal regions of the southern USA. Preliminary no-choice host testing for PSHB with tree species from Louisiana (black willow, Salix nigra Marshall, red maple, Acer rubrum L., and southern red oak, Quercus falcata Michx.) and New Mexico, USA (boxelder maple, quaking aspen, Populus tremuloides Michx., and narrowleaf cottonwood, Populus angustifolia James) revealed susceptible native hardwoods from these southern locations based on the presence of males, larvae, and pupae in a laboratory setting (Coleman et al. 2013b; Chen et al. 2014). This supports the potential for a USA range expansion outside of California. The California Legislature (2018) recently amended a bill (AB-2470) to address the management of the invasive shot hole borers within the state. This action may help limit the spread, address research gaps, and increase the pace of management for these exotic species in urban and native forests.
Barnes I, Fourie A, Wingfield MJ, Harrington TC (2018) New Ceratocystis species associated with rapid death of Metrosideros polymorpha in Hawaii. Persoonia-Molecular Phylogeny and Evolution of Fungi 40:154–181
Boland JM (2016) The impact of an invasive ambrosia beetle on the riparian habitats of the Tijuana River Valley, California. Peer J 4:e2141. https://doi.org/10.7717/peerj.2141
Bright DE (2014) A catalog of Scolytidae and Platypodidae (Coleoptera), supplement 3 (2000–2010), with notes on subfamily and tribal reclassifications. Insecta Mundi 356:1–336
Bright DE (2019) A taxonomic monograph of the bark and ambrosia beetles of the West Indies Coleoptera: Curculionoidea: Scolytidae and Platypodidae (Coleoptera). Studies on West Indian Scolytidae 7. In: Occasional papers of the Florida State Collection of Arthropods, Gainesville, Florida, 500 pp
Byers JA, Maoz Y, Levi–Zada A (2017) Attraction of Euwallacea sp. near fornicatus (Coleoptera: Curculionidae) to quercivorol and to infestations in avocado. J Econ Entomol 110:1515–1517
California Forest Pest Council (CFPC) (2014) California forest pest conditions. Sacramento, California. https://www.fs.usda.gov/detail/r5/forest-grasslandhealth/?cid=fsbdev3_046704. Accessed 26 Sept 2018
California Forest Pest Council (CFPC) (2015) California forest pest conditions. Sacramento, California. https://www.fs.usda.gov/detail/r5/forest-grasslandhealth/?cid=fsbdev3_046704. Accessed 26 Sept 2018
California Forest Pest Council (CFPC) (2016) California forest pest conditions. Sacramento, California. https://www.fs.usda.gov/detail/r5/forest-grasslandhealth/?cid=fsbdev3_046704. Accessed 26 September 2018
California Forest Pest Council (CFPC) (2017) California forest pest conditions. Sacramento, California. https://www.fs.usda.gov/detail/r5/forest-grasslandhealth/?cid=fsbdev3_046704. Accessed 26 Sept 2018
California Legislature (2018) AB-2470 Invasive Species Council of California. https://leginfo.legislature.ca.gov/faces/billTextClient.xhtml?bill_id=201720180AB2470. Accessed 26 Sept 2018
Carrillo D, Cruz LF, Kendra PE, Narvaez TI, Montgomery WS, Monterroso A, De Grave C, Cooperband MF (2016) Distribution, pest status and fungal associates of Euwallacea nr. fornicatus in Florida avocado groves. Insects 7:573–579
Centre for Agriculture and Biosciences International (CABI) (2018) Euwallacea fornicatus distribution map. [WWW document]. URL http://www.cabi.org/isc/datasheet/57163. Accessed 14 August 2018
Chen Y, Coleman, TW, Graves, AD, Meeker, JR, Seybold, SJ (2014) Host range of the invasive polyphagous shot hole borer. California Forest Pest Council Annual Meeting, 12–13 Nov 2014 (http://caforestpestcouncil.org/wp-content/uploads/2014/12/Chen.pdf). Accessed 17 September 2018
Chen Y, Dallara PL, Nelson LJ, Coleman TW, Hishinuma SM, Carrillo D, Seybold SJ (2017) Comparative morphometric and chemical analyses of phenotypes of two invasive ambrosia beetles (Euwallacea spp.) in the United States of America. Insect Sci 24:647–662
Chen Y, Coleman TW, Poloni AL, Nelson LJ, Seybold SJ (2019a). Reproduction and control of the invasive polyphagous shot hole borer, Euwallacea sp., in three species of hardwoods: effective sanitation through felling and chipping. Agricultural and Forest Entomology (in review)
Chen Y, Coleman TW, Poloni AL, Seybold SJ (2019b) Developing monitoring techniques for the invasive polyphagous shot hole borer, Euwallacea sp. (Coleoptera: Curculionidae: Scolytinae). Journal of Economic Entomology (in review)
Cognato AI, Hoekeke ER, Kajimura H, Smith SM (2015) History of the exotic ambrosia beetles Euwallacea interjectus and Euwallacea validus (Coleoptera: Curculionidae: Xyleborini) in the United States. J Econ Entomol 108:1129–1135
Coleman TW, Grulke NE, Daly M, Godinez C, Schilling S, Riggan PJ, Seybold SJ (2011) Coast live oak, Quercus agrifolia, susceptibility and response to goldspotted oak borer, Agrilus auroguttatus, injury in southern California. For Ecol Manag 261:1852–1865
Coleman TW, Graves AD, Hoddle M, Heath Z, Chen Y, Flint ML, Seybold SJ (2012) Forest stand composition and impacts associated with Agrilus auroguttatus Schaeffer (Coleoptera: Buprestidae) and Agrilus coxalis Waterhouse in oak woodlands. For Ecol Manag 276:104–117
Coleman TW, Eskalen A, Stouthamer R (2013a) New pest complex in California: the polyphagous shot hole borer, Euwallacea sp., and Fusarium Dieback, Fusarium euwallaceae. USDA Forest Service, Pest Alert, R5-PR-032, 4 November 2013, 5 pp. https://cisr.ucr.edu/pdf/pest_alert_pshb_and_fd.pdf. Accessed 24 Sept 2018
Coleman TW, Seybold SJ, Venette RC, Chen Y, Graves AD, Meeker JR (2013b) Host susceptibility and potential for range expansion of the invasive polyphagous shot hole borer (PSHB), Euwallacea sp., and Fusarium dieback, Fusarium euwallaceae. In: The U.S. Special Technology Development Project No. R5-2014-01, 2014–2016
Cooperband MF, Stouthamer R, Carillo D, Eskalen A, Thibault T, Cossé AA, Castrillo LA, Vandenberg JD, Rugman-Jones PF (2016) Biology of two members of the Euwallacea fornicatus species complex (Coleoptera: Curculionidae: Scolytinae), recently invasive in the U.S.A., reared on an ambrosia beetle artificial diet. Agric For Entomol 18:223–237. https://doi.org/10.1111/afe.12155
Danthanarayana W (1968) The distribution and host-range of the shot-hole borer (Xyleborus fornicatus Eichh.) of tea. Tea Quarterly 39:61–69
Dodge C, Coolidge J, Cooperband M, Cossé A, Carillo D, Stouthamer R (2017) Quercivorol as a lure for the polyphagous and Kuroshio shot hole borers, Euwallacea spp. nr. fornicatus (Coleoptera: Scolytinae), vectors of Fusarium dieback. Peer J 5:e3656. https://doi.org/10.7717/peerj.3656
Eskalen A, Gonzalez A, Wang DH, Twizeyimana M, Mayorquin JS, Lynch SC (2012) First report of a Fusarium sp. and its vector tea shot hole borer (Euwallacea fornicatus) causing Fusarium dieback on avocado in California. Plant Dis 96:1070. https://doi.org/10.1094/PDIS-03-12-0276-PDN
Eskalen A, Stouthamer R, Lynch SC, Rugman-Jones PF, Twizeyimana M, Gonzalez A, Thibault T (2013) Host range of Fusarium dieback and its ambrosia beetle (Coleoptera: Scolytinae) vector in southern California. Plant Dis 97:938–951
Evans JP, Scheffers BR, Hess M (2014) Effect of laurel wilt invasion on redbay populations in a martitime forest community. Biol Invasions 16:1581–1588
Freeman S, Sharon M, Mayman M, Mendel Z, Protasov A, Aoki T, Eskalen A, O’Donnell K (2013) Fusarium euawallaceae sp. nov.—a symibiotic fungus of Euwallacea sp., an invasive ambrosia beetle in Israel and California. Mycologia 105:1595–1606
García-Avila CDJ, Trujillo-Arriaga FJ, López-Buenfil JA, Gonzalez-Gomez R, Carrillo D, Cruz LF, Ruiz-Galvan I, Quezada-Salinas A, Acevedo-Reyes N (2016) First report of Euwallacea nr. fornicatus (Coleoptera: Curculionidae) in Mexico. Fla Entomol 99:55–56
Gibson K, Kegley S, Bentz B (2009) Mountain pine beetle. Forest insect and disease leaflet 2 (revised). USDA Forest Service, Portland, Oregon. FS-R6-RO-FIDL No. 2 2002-2009. 12pp
Gomez DF, Rabaglia RJ, Fairbanks KEO, Hulcr J (2018a) North American Xyleborini north of Mexico: a review and key to genera and species (Coleoptera, Curculionidae, Scolytinae). ZooKeys 768:19–68
Gomez DF, Skelton J, Sedonia Steininger M, Stouthamer R, Rugman-Jones P, Sittichaya W, Rabaglia RJ, Hulcr J (2018b) Species delineation within the Euwallacea fornicatus (Coleoptera: Curculionidae) complex revealed by morphometric and phylogenetic analyses. Insect Systematics and Diversity 2. https://doi.org/10.1093/isd/ixy018
Gomez DF, We L, Lei G, You L (2019) New host plant records for the Euwallacea fornicatus (Eichhoff) species (Coleoptera: Curculionidae: Scolytinae) across its natural and introduced distribution. J Asia Pac Entomol 22:338–340
Haack RA (2006) Exotic bark- and wood-boring Coleoptera in the United States: recent establishments and interceptions. Can J For Res 36:269–288
Hain FP, Duehl AJ, Gardner MJ, Payne TL (2011) Natural history of the southern pine beetle, pp 13–24. In: Coulson, RN, Klepzig KD (eds) Southern pine beetle II. USDA Forest Service, Southern Research Station General Technical Report SRS-140
Hatten JR, Paradzick CE (2003) A multiscaled model of southwestern willow flycatcher breeding habitat. J Wildl Manag 67:774–788
Herms DA, McCullough DG (2014) Emerald ash borer invasion of North America: history, biology, ecology, impacts, and management. Annu Rev Entomol 59:13–30
Hishinuma SM (2017) Interactions among the walnut twig beetle, Pityophthorus juglandis, the pathogenic fungus, Geosmithia morbida, and host species in thousand cankers disease in California. Dissertation, University of California, Davis
Jones ME, Paine TD (2015) Effect of chipping and solarization on emergence and boring activity of a recently introduced ambrosia beetle (Euwallacea sp., Coleoptera: Curculionidae: Scolytinae) in Southern California. J Econ Entomol 108:1852–1859
Kumar R, Rajkowa G, Sankar M, Rajan RK (2011) A new host for the shot-hole borer, Euwallacea fornicatus (Eichhoff) (Coleoptera: Scolytidae) from India. Acta Entomol Sin 54:734–738
Lee JC, Haack RA, Negrón JF, Witcosky JJ, Seybold SJ (2007) Invasive bark beetles. Forest insect and disease leaflet 176. USDA Forest Service, Pacific Northwest Region, Portland, Oregon. 12 pp.
Li Q, Guo H, Zhao Y, Zhang G, He G, Liu B (2015) Damage caused by Euwallacea fornicatus (Coleoptera: Scolytidae) and its control techniques in Kunming. China Acad J 41:193–196. https://doi.org/10.3969/j.issn.0529-1542.2015.03.038
Li Y, Gu XY, Kasson MT, Bateman CC, Guo J, Huang YT, Li Q, Rabaglia RJ, Hulcr J (2016) Distribution, host records, and symbiotic fungi of Euwallacea fornicatus (Coleoptera: Curculionidae: Scolytinae) in China. Florida Entomol 99:801–804
Liebhold AM, McCullough DG, Blackburn LM, Frankel SJ, Von Holle B, Aukema JE (2013) A highly aggregated geographical distribution of forest pest invasions in the USA. Divers Distrib 19:1208–1216
Lynch SC, Twizeyimana M, Mayorquin JS, Wang DH, Na F, Kayim M, Kasson MT, Thu PQ, Bateman C, Rugman-Jones PF, Hulcr J, Stouthamer R, Eskalen A (2016) Identification, pathogenicity and abundance of Paracremonium pembeum sp. nov. and Graphium euwallaceae sp. nov.—two newly discovered mycangial associates of the polyphagous shot hole borer (Euwallacea sp.) in California. Mycologia 108:313–329
Mayfield AE III, Seybold SJ, Haag WR, Johnson MT, Kerns BK, Kilgo JC, Larkin DJ, Lucardi RD, Moltzan BD, Pearson DE, Rothlisberger JD, Schardt JD, Schwartz MK, Young MK (2019) Impacts of invasive species in terrestrial and aquatic systems in the USA. In: Poland TM, Patel-Weynand T, Finch D, Ford Miniat C, Lopez V (eds) National assessment of invasive species. Springer Verlag, Berlin, pp 38–108
McPherson BA, Mori SR, Wood DL, Kelly M, Storer AJ, Švihra P, Standiford RB, Rizzo DM (2010) Responses of oaks and tanoaks to the sudden oak death pathogen after 8 y of monitoring in two coastal California forests. For Ecol Manag 259:2248–2255
Mendel Z, Protasov A, Sharon M, Zveibil A, Ben Yehuda S, O’Donnell K, Rabaglia R, Wysoki M, Freeman S (2012) An Asian ambrosia beetle Euwallacea fornicatus and its novel symbiotic fungus Fusarium sp. pose a serious threat to the Israeli avocado industry. Phytoparasitica 40:235–238
Mitrovich MJ, Gallegos EA, Lyren LM, Lovich RE, Fisher RN (2011) Habitat use and movement of the endangered arroyo toad (Anaxyrus californicus) in coastal southern California. J Herpetol 45:319–328
O’Donnell K, Sink S, Libeskind-Hadas R, Hulcr J, Kasson MT, Ploetz RC, Konkol JL, Ploetz JN, Carrillo D, Campbell A, Duncan RE, Liyanage PNH, Eskalen A, Na F, Geiser DM, Bateman C, Freeman S, Mendel Z, Sharon M, Aoki T, Cossé AA, Rooney AP (2015) Discordant phylogenies suggest repeated host shifts in the Fusarium–Euwallacea ambrosia beetle mutualism. Fungal Genet Biol 82:277–290
Paap T, de Beer ZW, Migliorini D, Nel WJ, Wingfield MJ (2018) The polyphagous shot hole borer (PSHB) and its fungal symbiont Fusarium euwallaceae: a new invasion in South Africa. Australas Plant Pathol 47:231–237
R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/
Rabaglia RJ, Dole SA, Cognato AI (2006) Review of American Xyleborina (Coleoptera: Curculionidae: Scolytinae) occurring north of Mexico, with an illustrated key. Ann Entomol Soc Am 99:1034–1056
Rizzo DM, Garbelotto M (2003) Sudden oak death: endangering California and Oregon forest ecosystems. Front Ecol Environ 1:197–204
Rizzo DM, Garbelotto M, Hansen EM (2005) Phytophthora ramorum: integrative research and management of an emerging pathogen in California and Oregon forests. Annu Rev Phytopathol 43:309–335
Schomaker ME, Zarnoch SJ, Bectold WA, Latelle DJ, Burkman WG, Cox SM (2007) Crown-condition classification: a guide to data collection and analysis. General Technical Report SRS-102. Asheville, North Carolina: US Department of Agriculture, Forest Service, Southern Research Station, 78 pp.
Seybold SJ, Penrose RL, Graves AD (2016) Invasive bark and ambrosia beetles in California Mediterranean forest ecosystems. In: Paine TD, Lieutier F (eds) Insects and diseases of Mediterranean forest systems. Springer International Publishing, Cham, Switzerland, pp 583–662. https://doi.org/10.1007/978-3-319-24744-1_21
Seybold SJ, Frankel SJ, Olson DH, Flitcroft R, Kerns BK, Lee JC, Ripley K, Munson AS (2019a) Northwest region summary. In: Poland TM, Patel-Weynand T, Finch D, Ford Miniat C, Lopez V (eds) National assessment of invasive species. Springer Verlag, pp 698–739
Seybold SJ, Graves AD, Frankel SJ, White A, Sutherland C, Munson AS (2019b) Southwest region summary. In: Poland TM, Patel-Weynand T, Finch D, Ford Miniat C, Lopez V (eds) National assessment of invasive species. Springer Verlag, pp 740–786
Smith SM, Rabaglia RJ, Beaver RA, Cognato AI, Thu PQ (2018) Attraction of ambrosia beetles, (Curculionidae: Scolytinae: Xyleborini) to semiochemicals in Vietnam with new records and a new species. Coleopt Bull 72:838–844
Stanaway MA, Zalucki MP, Gillespie PS, Rodriguez CM, Maynard GV (2001) Pest risk assessment of insects in sea cargo containers. Aust J Entomol 40:180–192
Stouthamer R, Rugman-Jones P, Thu PQ, Eskalen A, Thibault T, Hulcr J, Wang LJ, Jordal BH, Chen CY, Cooperband M, Lin CS, Kamata N, Lu S-S, Masuya H, Mendel Z, Rabaglia R, Sanguansub S, Shih H-H, Sittichaya W, Zong S (2017) Tracing the origin of a cryptic invader: Phylogeography of the Euwallacea fornicatus (Coleoptera: Curculionidae: Scolytinae) species complex. Agric For Entomol 19:366–375
Swiecki TJ, Bernhardt EA (2006) A field guide to insects and diseases of California oaks. USDA Forest Service Pacific Southwest Research Station. General Technical Report PSW-GTR-197, Albany, California, 151 pp.
Tisserat N, Cranshaw W, Leatherman D, Utley C, Alexander K (2009) Black walnut mortality in Colorado caused by the walnut twig beetle and thousand cankers disease. Online. Plant Health Progress. https://doi.org/10.1094/PHP-2009-0811-01-RS . http://entnemdept.ufl.edu/pestalert/thousand_cankers_disease_CO_0810.pdf. Accessed 22 Sept 2018.
Umeda C, Eskalen A, Paine TD (2016) Polyphagous shot hole borer and Fusarium dieback in California. In: Paine TD, Lieutier F (eds) Insects and diseases of Mediterranean forest systems. Springer International Publishing, Cham, Switzerland, pp 757–768. https://doi.org/10.1007/978-3-319-24744-1_26
University of California (UC) Riverside (2018a) http://eskalenlab.ucr.edu/distribution.html. Accessed 14 August 2018
University of California (UC) Riverside (2018b) http://eskalenlab.ucr.edu/shotholeborerhosts.html. Accessed 14 August 2018
Venette RC, Kriticos DJ, Magarey R, Koch FH, Baker RHA, Worner SP, Gomez Raboteaux NN, McKenney DW, Dobesberger EJ, Yemshanov D, De Barro PJ, Hutchinson WD, Fowler G, Kalaris TM, Pedlar J (2010) Pest risk maps for invasive alien species: a roadmap for improvement. BioScience 60:349–362
Vettraino A, Roques A, Yart A, Fan JT, Sun JH, Vannini A (2015) Sentinel trees as a tool to forecast invasions of alien plant pathogens. PLoS One 10(3):15. https://doi.org/10.1371/journal.pone.0120571
Wallner WE (1996) Invasive pests (‘biological pollutants’) and US forests: whose problem, who pays? Bull OEPP/EPPO 26:167–180
Wang WR, Yuan ZY (2003) A new pest of litchi, Xyleborus fornicatus and its control. South China Fruits 32:34–35
The authors thank Michael I. Jones, Department of Entomology and Nematology, University of California, Davis; Daniel Betancourt, Matthew Kellenberger, Kalee Koeslag, and Daniel Ryerson, USDA Forest Service, Forest Health Protection for their assistance with this study. We thank the many land managers and city foresters who facilitated this work, and especially the California State Polytechnic University for allowing access to their grounds.
This work was supported by grants from the United States Department of Agriculture, Forest Service; USDA, FS, Special Technology Development Program (R5-2014-01); USDA FS Pacific Southwest Region administered through cooperative agreements No. 14-CA-11272139-095 and 14-CA-11272139-096 between the USDA, FS, Pacific Southwest Research Station and the University of California, Davis, Department of Entomology and Nematology, Michael P. Parrella and Steven A. Nadler, PIs; and the Asia and the Pacific Forest Invasive Species Network. We are especially grateful to Sheri L. Smith for facilitating the funding from the USDA FS Pacific Southwest Region.
Statement on data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
Conflict of interest
The authors declare that they have no conflict of interest.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This article is part of the topical collection on Entomological issues during forest diebacks
Contributions of the co-authors: T. Coleman: designed and led the study, and collected, consolidated, and summarized the field data.
Y. Chen: contributed to field work and performed statistical analyses.
A. Poloni and S. Seybold: contributed to field work in California.
R. Rabaglia: provided insect taxonomic support.
R. Rabaglia, G. Man, J. Sun, Q. Li, and P. Q. Thu: contributed to field work in China and Vietnam.
R. Rabaglia, G. Man, J. Sun, and P. Q. Thu: coordinated work in China and Vietnam.
T. Coleman, A. Poloni, and S. Seybold: wrote the manuscript.
All authors contributed to writing or revising the manuscript approved for the publication.
Handling Editor: Aurélien Sallé
About this article
Cite this article
Coleman, T.W., Poloni, A.L., Chen, Y. et al. Hardwood injury and mortality associated with two shot hole borers, Euwallacea spp., in the invaded region of southern California, USA, and the native region of Southeast Asia. Annals of Forest Science 76, 61 (2019). https://doi.org/10.1007/s13595-019-0847-6
- Ambrosia beetles
- Hardwood tree mortality
- Impact assessment
- Invasive species