Tom W. Coleman

Previously unrecorded damage to oak, Quercus spp., in southern California by the goldspotted oak borer, Agrilus coxalis Waterhouse (Coleoptera: Buprestidae)

Abstract A new and potentially devastating pest of oaks, Quercus spp., has been discovered in southern California. The goldspotted oak borer, Agrilus coxalis Waterhouse (Coleoptera: Buprestidae), colonizes the sapwood surface and phloem of the main stem and larger branches of at least three species of Quercus in San Diego Co., California. Larval feeding kills patches and strips of the phloem and cambium resulting in crown die back followed by mortality. In a survey of forest stand conditions at three sites in this area, 67% of the Quercus trees were found with external or internal evidence of A. coxalis attack. The literature and known distribution of A. coxalis are reviewed, and similarities in the behavior and impact of this species with other tree-killing Agrilus spp. are discussed.

Collection History and Comparison of the Interactions of the Goldspotted Oak Borer, Agrilus auroguttatus Schaeffer (Coleoptera: Buprestidae), with Host Oaks in Southern California and Southeastern Arizona, U.S.A.

ABSTRACT An invasive population of the goldspotted oak borer, Agrilus auroguttatus Schaeffer (Coleoptera: Buprestidae), is colonizing and killing three species of oaks in San Diego Co., California. However, the interactions of A. auroguttatus with oaks in its native range in southeastern Arizona have not been recorded. We present a complete inventory of the North and Central American collection records of A. auroguttatus and Agrilus coxalis Waterhouse from the literature and from a survey of the holdings of 27 museum and personal collections. We also discuss the relationship between this collection history and the behavior of A. auroguttatus as an intracontinental invasive species. Surveys of native populations of A. auroguttatus in oak forest stands from four mountain ranges in southeastern Arizona revealed injury patterns on Emory oak, Quercus emoryi Torrey, and silverleaf oak, Quercus hypoleucoides A. Camus, similar to those observed on other “red” oaks in California. No damage was observed on “white” oaks in Arizona, and observed only rarely on a white oak, Quercus engelmannii Greene, in California. In Arizona, adult emergence was confirmed from bark removed from Q. emoryi, representing the first developmental record of A. auroguttatus from a native host. Late instars of Agrilus sp. were also recovered from Q. hypoleucoides, but they were not reared to the adult stage for species identification. Nonetheless, our observations of damage and the presence of larvae in the same configuration and location in the outer bark as we would expect for A. auroguttatus suggest that Q. hypoleucoides is also likely a host. Two hymenopteran parasitoids, Calosota elongata Gibson (Eupelmidae) and Atanycolus simplex Cresson (Braconidae), and two likely coleopteran predators (Trogossitidae and Elateridae) emerged from, or were collected in southeastern Arizona from, Q. emoryi bark infested with A. auroguttatus. Based on the museum survey results, the morphological similarity of individuals from the California and Arizona populations, the spatial dynamics of the pattern of infestation in California, the geographic isolation of hosts in California from native populations of the beetle, and the proximity of San Diego Co. to southeastern Arizona, we hypothesize that A. auroguttatus was introduced to California from Arizona or less likely from the Mexican states of Baja California, Chihuahua, or Sonora, and that the introduction most likely occurred on oak firewood. Further, we hypothesize that the oak mortality in southern California is occurring from this intracontinental invasive species because the beetle is filling a vacant niche by colonizing and developing in non-coevolved trees with low host resistance in the absence of a diverse and coevolved insect natural enemy complex.

Can the destruction of California's oak woodlands be prevented? Potential for biological control of the goldspotted oak borer, Agrilus auroguttatus.

The goldspotted oak borer (GSOB), Agrilus auroguttatus Schaeffer (Coleoptera: Buprestidae), is an introduced and aggressive phloem/wood borer infesting native oaks in southern California. Elevated levels of oak mortality have occurred continually for the last nine years on three oak species in San Diego Co., California, USA. Biological control is being assessed as an option for long-term and widespread management of the invasive population of GSOB. Foreign exploration in the native ranges of GSOB and a related sibling species (Agrilus coxalis Waterhouse) was conducted to determine life history information, to assess the natural enemy complex, and to collect specimens for molecular analyses that could help to identify the area of origin of California’s introduced population. Two species of parasitoids, Calosota elongata Gibson (Eupelmidae) and Atanycolus simplex Cresson (Braconidae), were discovered with GSOB populations in Arizona and California. No insect natural enemies were found with populations of A. coxalis in southern Mexico. However, Quercus conzatti Trel. and Quercus peduncularis Nee in Oaxaca and Chiapas, respectively, were recorded as the first known hosts of A. coxalis. A comparative analysis of our understanding of the natural enemy complexes for other pestiferous Agrilus with that of GSOB suggests that more effort should be directed at uncovering potential egg parasitoids and microbial pathogens of GSOB. Analyses of mitochondrial and nuclear ribosomal DNA (rDNA) revealed that the California population of GSOB was more similar to the Arizona population. Specimens of A. coxalis from southern Mexico were confirmed as a separate species. Additional surveys and sampling are needed across the complete native range of the GSOB species complex to develop a comprehensive inventory of parasitoid species that could be considered for use in a classical biological control program in California and to delineate the area of origin of California’s population.

Sanitation Options for Managing Oak Wood Infested with the Invasive Goldspotted Oak Borer (Coleoptera: Buprestidae) in Southern California

ABSTRACT Movement of invasive wood-boring insects in wood products presents a threat to forest health and a management challenge for public and private land managers. The goldspotted oak borer, Agrilus auroguttatus Schaeffer (Coleoptera: Buprestidae), is a new pest in San Diego and Riverside Cos., CA, believed to have been introduced on firewood. This beetle has caused elevated levels of oak mortality since 2002. From 2009–2011, we tested several sanitation methods, applicable to large and small land parcels, to reduce or prevent goldspotted oak borer emergence from infested oak wood. In most experiments, emergence of goldspotted oak borer adults from the positive controls demonstrated that the beetle could complete development in firewood-sized pieces of cut oak wood. In 2009, adult emergence from sun-exposed oak wood began and peaked 2- to 4-wks earlier at a low elevation site than at a high elevation site (late May to late June). However, there were no significant effects of elevation or host species on the emergence response of goldspotted oak borer by solarization treatment in this study. Solarization of infested wood with thick (6 mil) and thin (1 mil) plastic tarpaulins (tarps) did not significantly reduce emergence of adults despite recordings of greater mean and maximum daily temperatures in both tarped treatments and greater relative humidity in the thick-tarped treatment (all compared with nontarped controls). Grinding wood with a 3″-minus screen (≤7.6 cm) significantly reduced goldspotted oak borer emergence compared with control treatments, and this was the best method for reducing adult emergence among those tested. In a separate grinding study, no adults emerged when wood was ground to 9″-minus (22.9 cm), 2″-minus (5.1 cm), or 1″-minus (2.5 cm) screen sizes, but a low level of adult emergence from the positive controls limited any inferences from this experiment. Debarking cut wood pieces eliminated goldspotted oak borer emergence from the wood fraction, but adults emerged from the shaved bark and phloem.

Developing Monitoring Techniques for the Invasive Goldspotted Oak Borer (Coleoptera: Buprestidae) in California

ABSTRACT The goldspotted oak borer, Agrilus auroguttatus Schaeffer (Coleoptera: Buprestidae), is an invasive species that has colonized oak woodlands in southern California. To better define its seasonal flight activity, assist with forest and integrated pest management activities, and define the current distribution in California, an effective monitoring technique for A. auroguttatus is necessary. We assessed the efficacy of two colors of flight-intercept prism traps, the placement of these traps at three heights, and several commercially available lures [Manuka oil, Phoebe oil, and a green leaf volatile, (3Z)-hexenol] for monitoring the flight of adult A. auroguttatus. Landing rates and the densities of D-shaped emergence holes of A. auroguttatus adults were assessed on the lower stems of coast live oak, Quercus agrifolia Née, of varying size and crown health classes. Purple flight-intercept prism traps placed at heights of 3 m and 4.5 m caught significantly more female A. auroguttatus than green prism traps. In one experiment, males also responded at a significantly higher level to purple than to green prism traps placed at 3 m height. The addition of commercially available lures significantly enhanced male, but not female, A. auroguttatus trap catch when compared with unbaited control traps. There were no differences among male flight responses to the three lures. A. auroguttatus landing rates and emergence hole densities were significantly greater on the largest-diameter trees (>76.2 cm diameter at breast height) and on trees with severe crown thinning or complete crown collapse. The annual increment in emergence hole densities was also significantly greater on trees with severe crown thinning or complete crown collapse. In three trapping studies over multiple years in southern California, the adult flight period began as early as mid-May, peaked in mid-June to early July, and ended in early- to mid-September. To demonstrate the efficacy of the detection method for A. auroguttatus (unbaited purple traps at 3 m height), a delimitation survey conducted from 2009 to 2012 confirmed that the species was only present in San Diego Co., but that the distribution was expanding northward.

Population genetics of goldspotted oak borer, Agrilus auroguttatus Schaeffer (Coleoptera: Buprestidae): investigating the origin of an invasive pest of native oaks in California

The goldspotted oak borer, Agrilus auroguttatus Schaeffer, is an invasive woodborer in California USA that is native to oak woodlands across southern Arizona USA. Developing a classical biological control program for this pest in southern California is a high priority due to the continuing ecological and economic damage caused by this insect since its recent introduction into the area. In an attempt to determine the area of origin for this invasive beetle, analyses of the mitochondrial cytochrome oxidase and ribosomal nuclear D2 domain of the 28S gene regions were undertaken and provided insight into the phylogeographic relationship between and within populations of A. auroguttatus in Arizona and California. The area of origin for the invasive population of goldspotted oak borer in California was not determined conclusively, although our molecular data suggests the Dragoon Mountains in Cochise Co., Arizona as a possible source for the California population of A. auroguttatus. Results also confirmed that individuals collected from populations across southern Arizona and California are all A. auroguttatus, and are not part of a cryptic species complex comprised of the morphologically similar A. coxalis. Future surveys for natural enemies of A. auroguttatus will focus on the Dragoon Mountains as a potential source for co-evolved enemies for use in a classical biological control program against this invasive woodborer in southern California.

Agrilus auroguttatus (Coleoptera: Buprestidae) Seasonal Development within Quercus agrifolia (Fagales: Fagaceae) in Southern California

ABSTRACT We investigated seasonal development of the goldspotted oak borer, Agrilus auroguttatus Schaeffer (Coleoptera: Buprestidae), and physical conditions of the phloem within a preferred host species, coast live oak, Quercus agrifolia Née. We sampled infested trees on a monthly basis at two sites in southern California throughout 2011. Measurements of an exposed portion of the head capsule, the peristoma, indicated that there were four larval instars. Pupae and teneral or mature adults were found within trees from April through August. Adults were captured in flight between May and mid-October, with peak flight from July through August. Within-tree A. auroguttatus prepupal mortality did not differ between sites and increased significantly from 3 ± 3% in January to 36 ± 9% in March (mean ± SE). Prepupae were present in trees throughout most of the year, which made it difficult to determine generation time; it was likely 1 yr for the majority of individuals, and possibly longer or shorter than 1 yr for others. Seasonal A. auroguttatus development, according to within-tree development and adult trap catch, was apparently 2 mo ahead at one site, which had a greater past and current level of A. auroguttatus infestation compared with the other. There was also evidence at the more severely infested site that within-tree A. auroguttatus population densities were positively related to proportion of dying phloem tissue. This suggested that the level of current infestation affected host tree condition, or that dying tissue was more suitable for larval development.

Impact of the goldspotted oak borer, Agrilus auroguttatus, on the health of coast live oak before and after treatment with two systemic insecticides.

BACKGROUND The invasive goldspotted oak borer, Agrilus auroguttatus, is threatening the health and survival of oak trees in San Diego County, California. From two sites in the core area of the infestation, we report a 2.5 year investigation of the impact of A. auroguttatus on coast live oak, Quercus agrifolia, before and after treatment with two systemic insecticides, emamectin benzoate (EB) and imidacloprid (IC). RESULTS None of the 446 survey trees died during the study. The crown dieback rating of most trees at both study sites remained unchanged, regardless of insecticide treatment. A higher cumulative increase in the number of A. auroguttatus emergence holes was observed on trees that were previously infested and on trees with larger diameters. Over the 2.5 year period, the new infestation rates of initially uninfested trees across the untreated and treated groups were 50% (EB) and 32% (IC), and neither EB nor IC treatment affected cumulative increases in the number of emergence holes. EB-injected trees did not have significant annual increases in the number of A. auroguttatus emergence holes at either 1.5 or 2.5 years compared with that at 0.5 years, whereas untreated trees had significant annual increases. Although IC-injected trees had a significantly greater annual increment in the number of emergence holes than untreated trees during the last year of the study, treated trees had significant reductions in annual increases in emergence holes at both 1.5 and 2.5 years compared with that at 0.5 years. Untreated trees had no significant reduction in the annual increase in emergence holes at 1.5 and 2.5 years. CONCLUSIONS A. auroguttatus preferentially attacked previously infested and larger (diameter at breast height > 15-30 cm) oak trees, but the attacks led to very gradual changes in the health of the trees. Both EB and IC provided minor suppressive effects on A. auroguttatus emergence. Published 2014. This article is a U.S. Government work and is in the public domain in the USA.

Goldspotted oak borer effects on tree health and colonization patterns at six newly-established sites

Newly‐established populations of invasive wood‐inhabiting insects provide an opportunity for the study of invasion dynamics and for collecting information to improve management options for these cryptic species. From 2011 to 2013, we studied the dynamics of the goldspotted oak borer Agrilus auroguttatus Schaeffer (Coleoptera: Buprestidae), a new pest of oaks in southern California, at six sites that had been colonized recently. At all sites, the percentage of coast live oaks Quercus agrifolia Née, colonized by A. auroguttatus increased between 2011 (6–33%) and 2013 (23–40%), although beetle densities did not grow rapidly at most sites. From 2011 to 2013, there were minor changes in signs and symptoms of A. auroguttatus infestation (adult emergence holes, bark staining, and evidence of woodpecker foraging), except at one site where an outbreak occurred. At some sites, noticeable negative changes in oak crown health occurred 1 year prior to positive A. auroguttatus population growth. Among sites, most of the A. auroguttatus population density (66–93%) was produced by a small number of heavily‐infested trees (= brood trees). Early identification and removal of brood trees in newly‐invaded areas could slow the growth of A. auroguttatus populations.

Foliar nutrients explain goldspotted oak borer, Agrilus auroguttatus, adult feeding preference among four California oak species.

Adults of the invasive goldspotted oak borer, Agrilus auroguttatus Schaeffer (Coleoptera: Buprestidae), consumed foliar weight in no‐choice feeding tests of, in descending order, California black oak Quercus kelloggii Newb., Engelmann oak, Quercus engelmannii Greene, coast live oak, Quercus agrifolia Née, and canyon live oak, Quercus chrysolepis Liebm. (Fagaceae). Furthermore, significantly more foliar area was consumed of Q. kelloggii than of Q. chrysolepis. In dual‐choice feeding tests with isolated leaf disks, A. auroguttatus consumed significantly more foliar weight and area of Q. kelloggii relative to the other three oak species, and more foliar weight of Q. agrifolia than of Q. chrysolepis. In dual‐choice feeding tests with leaves on small branches, A. auroguttatus consumed more foliar weight of Q. kelloggii than of Q. engelmannii and Q. agrifolia. Thus, multiple experiments suggested that adults of A. auroguttatus preferred the foliage of Q. kelloggii over that of the other three oak species, and among the other three species they did not appear to have a strong feeding preference. Factor analysis reduced the quantities of 13 foliar nutrients into two new variables (factor 1 and factor 2). Factor 1 was weighted heavily on the quantities of nitrogen, sulfur, phosphorus, potassium, zinc, and copper, whereas factor 2 was weighted heavily on the quantities of zinc, iron, and aluminum. Factor 1 varied by oak species, with Q. kelloggii having a higher factor 1 nutrient content than the other three species. Factor 2 response was higher in Q. kelloggii, Q. agrifolia, and Q. engelmannii than in Q. chrysolepis. The collective effects of four macronutrients (nitrogen, sulfur, phosphorus, and potassium) and two micronutrients (zinc and copper) suggest that these might be the nutrients directing preferential feeding of A. auroguttatus adults on the foliage of Q. kelloggii. Leaf toughness might also play an important role in feeding preference. Female A. auroguttatus did not show an ovipositional preference among the four oak species.