Dispersal of emerald ash borer (Coleoptera: Buprestidae) parasitoids along an ash corridor in western New York

Accepted Manuscript Dispersal of emerald ash borer (Coleoptera: Buprestidae) parasitoids along an ash corridor in western New York Michael I. Jones, Juli R. Gould, Melissa L. Warden, Melissa K. Fierke PII: DOI: Reference:

S1049-9644(18)30641-8 https://doi.org/10.1016/j.biocontrol.2018.09.004 YBCON 3845

To appear in:

Biological Control

Received Date: Revised Date: Accepted Date:

20 January 2018 7 September 2018 9 September 2018

Please cite this article as: Jones, M.I., Gould, J.R., Warden, M.L., Fierke, M.K., Dispersal of emerald ash borer (Coleoptera: Buprestidae) parasitoids along an ash corridor in western New York, Biological Control (2018), doi: https://doi.org/10.1016/j.biocontrol.2018.09.004

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Dispersal of emerald ash borer (Coleoptera: Buprestidae) parasitoids along an ash corridor in western New York Michael I. Jonesa,*, Juli R. Gouldb,1, Melissa L. Wardenb,2 and Melissa K. Fierkea,3 a

State University of New York, College of Environmental Science and Forestry 1 Forestry Drive, Syracuse, NY 13210, United States *

e-mail: [email protected], corresponding author phone: (707) 338-7457 3

e-mail: [email protected] phone: (315) 470-6809 b

United States Department of Agriculture, Animal and Plant Health Inspection Service, Plant Protection and Quarantine, Science and Technology 1398 W. Truck Rd., Otis Air National Guard Base, Buzzards Bay, MA 02532, United States 1

e-mail: [email protected] phone: (508) 563-0923 2

e-mail: [email protected]

Jones 2 Abstract – Previous studies have documented that parasitoids introduced to North America for biological control of emerald ash borer (EAB), Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), are establishing and persisting. However, no study has explicitly assessed their dispersal capabilities. In 2013 and 2014, we released Spathius agrili Yang (Hymenoptera: Braconidae), Tetrastichus planipennisi Yang (Eulophidae), and Oobius agrili Zhang and Huang (Encyrtidae) at 5 km intervals along 20 km of an ash (Fraxinus spp.) corridor, along which EAB was spreading. From 2013 to 2017, we deployed yellow pan traps every 250 m to detect parasitoid dispersal along the corridor; traps were checked weekly throughout the summer. In 2014, 2015, and 2016, ash health data were collected at each trap location. In 2016, additional traps were established parallel to the study area to detect dispersal away from the corridor. EAB were recovered in traps each year of the study and severity of ash decline aligned with EAB trap detections to indicate build-up and movement of EAB populations. Tetrastichus planipennisi were first recovered in 2014 and trap recoveries increased each subsequent year of the study. The other parasitoid species were not recovered. In 2016, T. planipennisi were detected ~ 10 km from release points, established in areas with high EAB population densities, and were detected in traps ~ 3.9 km away from the corridor. By 2017, T. planipennisi recovered along the entire study area. This study quantifies dispersal of T. planipennisi and suggests it will be an important biological control agent of EAB in North America.

Key words: emerald ash borer; biological control; Tetrastichus planipennisi; parasitoid dispersal

Jones 3 1. Introduction Efforts to manage emerald ash borer (EAB), Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), an important invasive wood-boring beetle in North America, have focused on developing integrated pest management programs to control populations by reducing the rate of spread and thus slowing the loss of ash for as long as possible (McCullough et al., 2009). Examples of management tools include tree removal, systemic insecticides, trap trees, and classical biological control (Bauer et al., 2008; Fierke et al., 2013; McCullough et al., 2015). Classical biological control is the introduction of predators/pathogens/parasitoids from the native range of an invasive pest and offers an economically and environmentally sustainable long term management option for EAB (Bauer et al., 2015; Duan et al., 2013a, 2015, 2017). Early in the EAB biological control effort, three hymenopteran parasitoids collected from northeastern China were selected as candidate biological control agents for release in North America: two gregarious larval parasitoids, Tetrastichus planipennisi Yang (Hymenoptera: Eulophidae) and Spathius agrili Yang (Hymenoptera: Braconidae), and one egg parasitoid, Oobius agrili Zhang and Huang (Hymenoptera: Encyrtidae) (Liu et al., 2003; Yang et al., 2005; Zhang et al., 2005). To date, the three parasitoids have been released in 25 of the 34 states with known infestations (MapBioControl.org, 2018). Two of the species, T. planipennisi and O. agrili, appear to be establishing well in North America (Abell et al., 2014; Duan et al., 2013b, 2014), while the success of S. agrili in more northern areas is doubtful (USDA-APHIS/ARS/FS, 2015; Jones, 2018). There is abundant evidence of successful T. planipennisi establishment, yet information on spread and dispersal capabilities of the parasitoid in North America remain limited (Duan et al., 2013a) and only a few studies have detected evidence of dispersal away from release sites

Jones 4 into control sites. Duan et al. (2013a) destructively sampled trees in Michigan for several years and found T. planipennisi had dispersed at least 3 km into control sites where parasitoids had not been released. A similar study in Maryland determined T. planipennisi had dispersed into control sites > 5 km from well-established release sites several years after release (Jennings et al., 2016). Additionally, recoveries of T. planipennisi have been documented at sites throughout Michigan and New York not associated with releases (personal observation JRG). To estimate dispersal rates for some of these events, data were downloaded for 25 T. planipennisi recoveries from MapBioControl.org (online database of EAB parasitoid releases and recoveries). Examination of these data indicated T. planipennisi dispersed at least 0.3 km/year, with half of the dispersal rates ≥ 2 km/year, while one recovery was made 8.9 km from the nearest release site one year after release. These dispersal rates were considered minimum distances because T. planipennisi could have gone farther and/or faster, but samples were not always taken and trapping efforts did not necessarily detect T. planipennisi the first year it occupied a site. Thus, T. planipennisi appears capable of dispersing from release sites once established, yet data are anecdotal and the true dispersal capabilities of T. planipennisi, O. agrili, and S. agrili have not been explicitly studied. Dispersal capabilities are an important characteristic of a successful biological control agent (Heimpel and Asplen, 2011) and understanding how EAB parasitoids disperse can be helpful for determining their potential success in finding and controlling EAB populations. The objective of this study was to evaluate and quantify dispersal of the three introduced parasitoids away from release points along a corridor of ash, along which EAB populations were also spreading, to document how well they track the movement of EAB. To accomplish this, we released all three parasitoids along a linear corridor with abundant ash in western New York (Monroe Co.). When the study was initiated, the EAB infestation was concentrated to the

Jones 5 northern part of the study area. We conducted ash health assessment surveys to monitor the southerly progression of EAB populations along the corridor and deployed a series of yellow pan traps (YPTs) to detect parasitoid establishment and dispersal.

2. Methods 2.1. Study site This study was conducted along a 20 km segment of the Genesee Valley Greenway State Park (referred to hereafter as the “Greenway”), an open space corridor and multi-use trail located in western New York. The Greenway begins south of Rochester (Monroe Co.) and continues along an old canal and railroad route for 135 km to Cuba, New York (Cattaraugus Co.). Portions of the trail pass through woodlands, wetlands, and farmlands, with most of the trail consisting of an ~ 40 m wide corridor of early successional forest, containing a high density of ash, surrounded by agricultural land. In many areas, the canal was filled in and agricultural fields and development encroach on the trail. Where the canal was not filled in, the surrounding areas are often wet and flanked by generally small woodlots on one or both sides. The study area was established south of Rochester near Scottsville, NY (43.0765, 77.7088) and ran 20 km south (42.9160, -77.7852). It is dominated by early successional secondary growth northern deciduous forest containing high densities of green and white ash (Fraxinus pennsylvanica Marshall and F. americana L., respectively), and some black ash (F. nigra Marshall). Other commonly occurring trees include: cherry (Prunus spp.), maple (Acer spp.), black locust (Robinia pseudoacacia L.), hickory (Carya spp.), hawthorn (Crataegus spp.), oak (Quercus spp.), American basswood (Tilia americana L.), walnut and butternut (Juglans spp.).

Jones 6 Emerald ash borer was first detected in the Rochester area in 2010 and this study was initiated in 2013. Trees in the northern part of the study area north of Scottsville and adjacent to the Interstate-90 corridor (see Fig. 1A) showed signs of heavy to moderate EAB infestation, including canopy decline, woodpecker foraging, bark splits, exit holes, and moderate ash mortality. Trees adjacent to and just south of Scottsville exhibited some canopy decline, epicormic shoots, and evidence of woodpecker foraging, while trees towards the southern end of the study area showed no signs of infestation.

2.2. Parasitoid release Three parasitoid release points were established along the study area at 5 km intervals and were designated as R1 (= Release point 1) in the north, R2 in the center, and R3 in the south (Fig. 1A). Small ash bolts infested with EAB larvae parasitized by either T. plainpennisi or S. agrili and small vials containing O. agrili pupae inside EAB eggs were obtained from USDA APHIS EAB Biological Control Rearing Facility in Brighton, MI. Bolts and vials with eggs were hung at 1.3 m above the ground on several arbitrarily selected trees (5–10 trees) within 50 m of each release point. In 2013, ~ 10,000 T. planipennisi and ~ 1,800 S. agrili were released in the spring; ~ 1,800 O. agrili during the summer; and another ~ 2,500 T. planipennisi and ~ 1,800 S. agrili in the fall. In 2014, ~ 2,500 T. planipennisi were released in spring and ~ 1,500 O. agrili in summer. Equal numbers of each parasitoid species were released at the three release points. S. agrili was not released in the second year because other research indicated it was not establishing well in release sites north of the 40th parallel (Duan et al, 2014a; USDA-APHIS/ARS/FS, 2015).

2.3 Parasitoid sampling

Jones 7 Yellow pan traps (YPTs) (Abell et al., 2015) were deployed every ~ 250 m along the study area (n = 62) in May of each year and sampled through October for 2013–2017 to detect the introduced parasitoids. YPTs were used in this study because they are easy to maintain and have been effectively used to trap all three parasitoid species (Parisio et al., 2016). Traps consisted of a 0.35 L plastic yellow bowl (Sunshine Yellow – 09; Nationwide Party, Brooklyn, NY) nested within another yellow bowl attached to a shelf bracket, which was temporarily affixed to infested ash trees 1.3–1.5 m above the ground. Top bowls were filled with ~ 150 mL of 20% solution of clear propylene glycol (Solvents & Petroleum, Syracuse, NY) mixed with water and one drop of clear non-scented dish soap (to break the surface tension). Samples were collected weekly and the contents of each bowl were filtered through 190-micron mesh paint filters and stored in clear plastic bags at 10 ºC until sorted for T. planipennisi, S. agrili, O. agrili. Final identification of parasitoid species was confirmed by JRG. Any EAB caught in YPTs were also collected and counted. In 2016, the study area was moved 5 km south along the Greenway to avoid trapping in areas with high ash mortality in the north and to keep up with the southerly progress of EAB populations. An additional reference point (R04) was established 5 km south of R3 (see Fig. 1D). Thus, the adjusted study area consisted of R2 in the north, R3 in the middle, and the reference point R04 to the south. Additionally in 2016, to detect parasitoid dispersal across agricultural fields flanking the Greenway, 20 YPTs were established every 500 m along roads parallel to the Greenway on both the east and the west sides (n = 40 traps) of the northern 10 km of the study area (see Fig. 3). The distance of parallel traps from the Greenway ranged from 500 m to 3.9 km.

2.4. Ash health assessments

Jones 8 One 0.04 ha plot (10 x 40 m) was positioned perpendicular (east/west) and centered on the trail at each YPT location (n = 62). All tree species with ≥ 5 cm DBH (diameter at breast height, 1.3 m) were recorded into three size classes (< 10 cm, 10–20 cm, > 20 cm). Tree health was assessed by measuring canopy condition (adapted from Smith, 2006) and woodpecker foraging and given an infestation rating (Table 1). Woodpecker foraging was used as an infestation metric because it is easily quantifiable and can be an indication of relative EAB densities in a tree (Lindell et al., 2008). Total rating values ranged from 1–11 with 1 indicating a healthy tree, 2–4 = minor infestation, 5–7 = moderate, 8–10 = severe, and 11 indicating an EAB killed tree. Emerald ash borer associated decline and mortality was confirmed by the presence of D-shaped exit holes and bark splits with visible galleries. Ash health assessment plots were established in August 2014 and re-evaluated in 2015. In 2016, plots centered on R2 in and R3 were re-evaluated and new plots were established at the locations of YPTs in the south near R04.

2.5. Infestation maps Data from traps and ash health assessment plots were summarized by trap and plot and mapped into ArcGIS 10.1 (Environmental Systems Research Institute, Redlands, CA) to create visual references of the EAB infestation and movement of parasitoid populations. Infestation maps were created by conducting an inverse distance weighted spatial interpolation (default settings: power of 2 and search radius of 12 nearest points) of the mean infestation rating for each plot. Adult EAB caught in traps and traps positive for parasitoids are indicated on maps based on location of the YPT from which they were recovered.

2.6. Analysis

Jones 9 Ash health assessment data were summarized by plot (n = 62) and multiple recoveries of EAB and parasitoids from the same YPT were summarized by trap. To assess movement of the infestation and dispersal of parasitoids away from release points, the study area was divided into groups centered on each release point (including the R04 reference point). Each group included the release point and the 10 nearest traps and plots to the north and south of a release point (n = 21 plots/group), except for the group centered on R2, which had 20 plot and trap locations because there were no ash trees at one of the 250 m interval points. The statistical program R 3.1.3 (R Core Team, 2018) was used to analyze data. Mean distance of trap captures from each release point within a release group was tested for significance using ANOVA, followed by a post hoc Tukey HSD ( = 0.05). Normality of dispersal data was confirmed by using the Shapiro-Wilk Test and visual plots (density and qqnorm) due to small sample sizes. Ash health assessment plot data (n = 62) were tested for discrepancies in total density and total ash basal area between years using paired t-tests ( = 0.05). Differences in mean ash health rating by group within each year were tested for significance with an ANOVA followed by a Tukey HSD ( = 0.05). Dispersal distance for each year was estimated using the ArcGIS 10.1 Near tool (1 neighbor) to determine the distance of a parasitoid positive YPT from the nearest parasitoid positive YPT location in the previous year. To explore spatial relationships among locations of traps positive for EAB and parasitoids, we generated a spatial correlogram using the cross-correlation function in the R 3.1.3 package = ncf (Bjørnstad, 2016). The resulting correlograms estimate spatial dependence at discrete distance classes and the highest significant correlation represents distance over which parasitoid build-up lags behind that of the host (Bjørnstad and Bascompte, 2001). An

Jones 10 incremental distance band of 800 m (mean dispersal distance of EAB for the complete study period) was used to estimate significant correlations.

3. Results 3.1. EAB detections EAB were recovered from YPTs June through August each year of the study. In 2013, 42 EAB were recovered from 17 traps north of the middle release point (R2; Fig. 2). Most EAB (88.1%) were caught near R1 in the north ("near" refers to the 10 traps north and south of each release point), while 11.9% were caught in traps north of R2, and none were caught south of R2 (Fig. 1A). There were no traps that caught > 6 adults. In 2014, 66 EAB were recovered from 18 traps distributed along the study area (Fig. 1B & 2), with 95.5% recovered in the north and middle (45.5% and 50.0%, respectively) and 4.5% recovered in the south. The southernmost positive trap detection near R3 in 2014 was 4.8 km south of the southernmost positive trap detection in 2013. The trap at R1 caught 19 adults, while other positive traps caught ≤ 9 adults each. The following year, in 2015, 130 EAB were recovered from 30 traps along the study area (Fig. 1C & 2), with 8.4% of adults collected in the north and 91.6% collected in the middle and south (48.3% and 43.3%, respectively). Most traps caught ≤ 10 EAB, but two located south of R2 caught 15 and 35 adults. New trap detections in 2015 were ≤ 1 km from trap detections in 2014. With the study area moved south 5 km in 2016, traps near R2 were now in the north, while R3 was in the middle, and R04 furthest south. A total of 56 EAB were recovered from 23 traps along the study area (Fig. 1D & 2), with 23.3% and 62.5% collected near R2 and R3, respectively. The remaining 14.3% of EAB were collected from two YPTs located in heavily

Jones 11 infested woodlots at the most southern extent of the study area. No trap on the Greenway caught > 8 adults. Traps established parallel to the Greenway in 2016 caught 212 EAB. Most traps caught < 10 adults, but four caught 11, 19, 38, 74 adults. Distance of positive traps from the Greenway ranged from 500 m to 3.9 km (Fig. 3). In 2017, 101 EAB were collected from traps along the study area. Less than half were collected from traps in the north near R2 and middle near R3 (12.9% and 24.8%, respectively, while 62.4% were recovered in the south near R04 (Fig. 1E & 2). The majority of traps caught ≤ 6 adults, but two YPTs located in heavily infested woodlots south of R04 caught 22 adults each.

3.2. Parasitoid detections The only parasitoid consistently recovered in this study was T. planipennisi. No O. agrili were recovered and only one S. agrili was recovered. The S. agrili recovered was in the YPT on a tree at R1 and was caught < 1 week after a release, so was likely an adult emerging from a release bolt. The first detection of T. planipennisi was in July 2014. Since we only conducted spring releases until late May 2014, and this parasitoid has been documented in laboratory conditions to live ~ 6 wks (Duan et al., 2011b), the recovery most likely represented a new generation from a prior release; therefore, additional releases were not conducted in the fall. After initial detection of T. planipennisi in 2014, these parasitoids were caught from May to September each subsequent year of the study, with most adults caught in June. In 2014, 15 T. planipennisi were caught in 8 traps near R1 in the north and R2 in the middle, while none were recovered in the south near R3 (Fig. 1B & 2). Most T. planipennisi (80%) were recovered from traps ≤ 910 m from R1, while 3 adults were recovered ≤ 1.7 km from R2. The mean distance of

Jones 12 recovery from R1 was significantly less than the mean distance parasitoids were recovered from R2 (541 m and 1,600 m, respectively; F = 18.7, df = 1, 4, P < 0.01). In 2015, 60 T. planipennisi were collected from 22 traps distributed along the study area, with 30.0% collected in the north, 60.0% in the middle, and 10.0% in the south (Fig. 1C & 2). Two traps in the middle near R2 caught 12 and 13 adults, while the rest caught < 10 adults/trap. New trap detections were ≤ 2.1 km (median distance = 411 m) from 2014 detections, with the furthest detections in the south near R3. There were no significant differences in mean distance T. planipennisi were detected from R1 or R2 (1.0 km and 1.6 km, respectively; F = 2.2, df = 1, 18, P = 0.15). The estimated spatial correlogram indicated there was a significant relationship among locations of EAB and T. planipennisi positive traps, but the build-up of parasitoid populations lagged behind EAB populations by ~ 8 km. In 2016, 420 T. planipennisi were collected from 29 traps along the Greenway (Fig. 1D & 2). With the study area moved south by 5 km, most adults (80.9%) were caught in the northern part of the study area near R2, while 18.6% were collected in the middle near R3, and 0.5% in the south near R04. The maximum distance of new trap detections were ≤ 8.2 km (median distance = 314 m) from 2015 detections, with the furthest detection south of R04. Most traps caught < 10 adults, but five traps located in the north caught > 10 adults (11, 11, 16, 99, and 173), and one trap in the middle caught 30 adults. The estimated spatial correlogram indicated there was < 300 m lag between the build-up of T. planipennisi and EAB populations. A total of 51 T. planipennisi were recovered from 17 of the 40 traps established parallel to the Greenway in 2016 (Fig. 3), of which 16 caught < 10 adults and one caught 26 adults. The distance of positive traps from the Greenway ranged from 500 m to 3.9 km.

Jones 13 By 2017, 212 T. planipennisi were recovered from 38 traps distributed along the study area, with 8.5% collected in the north, 76.9% in the middle, and 14.6% in the south (Fig. 1E & 2). New trap detections were ≤ 1.0 km (median distance = 0 m) from 2016 detections. Traps generally caught < 10 adults, but 3 traps in the middle near R3 caught 14, 15, and 110, and one trap in the south near R04 caught 12.

3.3. Ash health assessments A total of 1,433 trees from 20 genera were surveyed in 62 plots during fall 2014. Ash represented 33.5% of trees surveyed and 33.0% of the basal area. Along the study area, 57.0% of ash trees (80% of the basal area) exhibited visual symptoms of infestation and 20.7% (30.0% of the basal area) were dead. Health assessment surveys identified the most heavily EAB infested area was in the north near R1 (Fig. 1B). These plots had a mean health rating of 5.0 (moderate decline), which was significantly higher (F = 6.42, df = 2, 59, P = 0.003) than plots in the middle near R2 and south near R3 (Fig. 4). Approximately 74% of trees in the north showed symptoms of infestation and 53.5% of all size classes were dead. In the middle, 62.9% of trees showed symptoms of infestation with a mean rating of 3.5 (minor EAB infestation), while 15.3% were dead. In the south, 43.7% of ash exhibited some symptoms of infestation, most appeared minor (rating = 1.9), with trees in several clusters exhibiting more moderate signs of decline. Only 3.2% of infested trees in the south were dead. In 2015, we attempted to reassess ash health at exact plot locations from 2014, but due to slight shifts in trap placement, stand measurements were slightly different. However, total ash density (/ha) and basal area (m2/ha) measured was not significantly different from 2014 (t = 0.49, df = 61, P = 0.65 and t = 0.37, df = 61, P = 0.71, respectively). Few newly infested trees were

Jones 14 observed, but the proportional number and basal area of dead trees across the study area increased from 20.7 % to 34.1% and from 30.0% to 41.0%, respectively (Fig. 4). Decline continued to be highest in the northern part of the study near R1 with 77.4% of trees across all size classes exhibiting symptoms of infestation, while mortality increased to 65.2%. The largest change in infestation severity occurred in the middle near R2, where the infestation increased from minor to moderate (infestation rating 3.5 to 5.7). The mean rating was not different from the north, but was significantly higher than the mean rating in the south near R3 (F = 8.59, df = 2, 59, P < 0.0001). More trees in the middle exhibited symptoms of infestation (67.9%) and mortality almost doubled to 27.2% from 15.3% in 2014. Symptoms of infestation in the south (41.4% of trees exhibited symptoms) changed very little and were slightly lower than in 2014 due to the slight shifts in health assessment plot locations. Ash mortality in the south only slightly increased to 5.0%. In 2016, health assessment plots near R2 and R3 were in approximately the same location as 2015 and there was no significant difference in ash density or ash basal area from 2015 (t = 0.61, df = 40, P = 0.55 and t = 0.17, df = 40, P = 0.86, respectively), while 21 new plots were surveyed in the south near R04. In 2016, ash represented 38% of the 1,659 trees surveyed and 39% of the basal area. After the study area was moved south 5 km, the number of trees exhibiting infestation symptoms in the north near R2 did not change much from previous years (~ 60%), but mortality almost doubled for a second year from 27.2% to 50.0%, with an increase in dead basal area from 42% to 82% (Fig. 4). The number of trees exhibiting symptoms of infestation in the middle near R3 slightly increased to 48.7%, while mortality increased from 5% to 23.4%. The mean infestation rating increased from minor (2.3) to moderate (4.8), which was not different from the mean health rating for the north, but was significantly higher than the

Jones 15 south (F = 9.9, df = 2, 59, P = 0.0002). Most trees in the south exhibited no symptoms of infestation and only a few had minor symptoms (mean infestation rating = 2.5). The trees with moderate to severe symptoms of infestation in the south were in two woodlots, one located at the R04 reference point and the other at the southern extent of the study area (Fig. 1D). In these woodlots, 33.0% of trees exhibited moderate symptoms of infestation, while 17.6% were dead.

4. Discussion This study demonstrated establishment and dispersal capabilities of T. planipennisi. The parasitoid was detected in YPTs ~ 1.5 km from release points in 2014 (one year after releases were first conducted) and ~ 4 km from release points by 2015. In 2016 (three years after release), T. planipennisi were detected ~ 10 km from release points, where it had established at the southern edge of the infestation in areas with high EAB population densities. Parasitoids were also detected across open, actively managed, agriculture fields and up to 3.9 km away from the Greenway. By 2017, four years following release, high numbers of T. planipennisi were detected along much of the 20 km study area and had likely dispersed beyond the southern extent. This is consistent with rates of dispersal detected in Michigan and Maryland (Duan et al., 2013a; Jennings et al., 2016) and from MapBioControl.org data. High numbers of EAB were consistently caught in YPTs during the study – which to our knowledge, has not been documented in other YPT studies. This was unexpected as early research by Francese et al. (2005) indicated yellow was not attractive to EAB. Therefore, recovery of EAB from YPTs could be due to the nature of the study area, e.g., a narrow corridor with high densities of ash, or more likely that traps were along the forest edge as several studies

Jones 16 exploring efficacy of EAB traps captured more EAB along forest edges (e.g., see Francese et al., 2008; McCullough et al., 2011). The locations of EAB positive traps corresponded to the southerly movement of EAB populations and were predictors of where substantial ash decline would occur the following year (Fig. 1B compared to 1C and then Fig. 1C to 1D). Additionally, the number of EAB caught in traps appeared to reflect EAB population densities in surrounding trees, which has been similarly observed in EAB trapping studies (Marshall et al., 2009; Poland and Mccullough, 2014, etc). For example, in 2013 EAB were only recovered from YPTs in the northern part of the study area where ash decline was obvious, but by 2014, they were recovered ~ 5 km south of 2013 detections and in high numbers in the middle where ash were in rapid decline, especially the larger size classes (> 20 cm DBH). Considerably fewer EAB were recovered from areas where they were detected in 2013, though those areas continued to exhibit substantial ash decline and mortality (Fig. 1B). Again in 2015, more EAB were recovered further south and fewer adults were caught in northern areas where ash health had declined (health rating > 7). The same pattern was observed in 2016 and 2017, with notable increases in trap recoveries in the south. Locations of traps recovering the most EAB each year indicated high population densities (i.e. the crest of the infestation wave, Burr and McCollough 2014) were moving south along the Greenway several kilometers per year. Siegert et al. (2014) found the spread of ash mortality occurred at a similar rate in the initial phase of an infestation in southeast Michigan. However, they suggested natural dispersal and anthropogenic movement of ash material contributed to the rate of spread, whereas movement of EAB populations along the Greenway would have been natural dispersal. While dispersal studies conducted in infestations with known origins found most EAB did not disperse far (~ 100 m) from their point of emergence, a small proportion of

Jones 17 adults did disperse ≥ 750 m to oviposit on suitable hosts (Mercader et al., 2009; Siegert et al., 2010). A flight mill study also showed that EAB are proficient fliers, with mated females capable of flying 1.3 km/day for several days (Taylor et al., 2010). Additionally, is it possible the linear and homogenous distribution of ash trees along the Greenway may have had a corridor effect on EAB spread, thereby facilitating population movement (Mercader et al., 2011). We expected to recover high numbers of EAB from YPTs in the south in 2016, but instead there was a reduction relative to 2015. The low number of EAB caught was likely due to high overwintering mortality during the winter of 2015–16, which was characterized by warm mid-winter temperatures (10–20 ºC) and an extreme freeze event (~ -31 ºC) that exceeded the cold tolerance of many overwintering EAB (Jones et al., 2017). Four of the YPTs parallel to the Greenway captured high numbers of EAB in 2016 (> 10 EAB/trap, Fig. 3), but those traps were on large open grown trees, which could have had different infestation dynamics compared to trees along the Greenway. We also did not have recovery data form YPTs parallel to the Greenway in previous years to compare relative population densities in those trees. In contrast to EAB, the number of T. planipennisi captured was much higher in 2016 than in previous years (Fig. 2) indicating their populations were less (if at all) affected by the 2016 freeze event. Tetrastichus planipennisi being cold tolerant is logical considering its establishment in northern areas (e.g., Minnesota, Ontario, CA) (MapBioControl.org), which have even colder winter temperatures than in New York (USDA, 2018). The parasitoid also appears more resilient to changes in winter temperatures and overwintering populations can reacclimate to cold temperatures even after they are exposed to periods of warm mid-winter temperatures (Jones, 2018), whereas EAB cannot (Sobek-Swant et al., 2012). However, Hanson et al. (2013) found overwintering mortality occurs if the parasitoid is exposed to long periods of cold temperatures.

Jones 18 Therefore, some overwintering mortality may have occurred, but T. planipennisi populations did not appear to be greatly impacted. EAB and T. planipennisi were frequently recovered from the same YPTs, which we attributed to the parasitoid establishing in areas with high EAB densities. This association was first observed in 2014, when the highest number of parasitoid detections were in the northern and middle parts of the study area where high numbers of EAB were also caught. By comparison, no parasitoids were detected in the southern part of the study area where no EAB were caught. The following year, as the infestation progressed south, more T. planipennisi were recovered further south where EAB population densities were highest based on YPT catches. Detection of the parasitoid in the southern part of the study area by 2015 suggest a numerical response to higher EAB populations by individuals originating from more northern release points rather than from the southern release point. Supporting evidence is that collection dates from the three positive YPTs near R3 indicated T. planipennisi were first recovered in the YPT closest to the middle release point (R2) in spring (May to mid-June), and were not detected in the two more southerly traps until summer and fall (late Jun to Aug). Since T. planipennisi can complete multiple generations each year in New York (Jones, 2018), it is likely that parasitoids recovered in spring/early summer represented emergence of an overwintering population, while parasitoids recovered in summer were more likely from a later generation. Based on this pattern of trap detections, populations that established north were moving south with EAB. Beginning in 2016, we moved the study south along the Greenway by 5 km as trap data indicated the infestation was approaching the southern extent of the original study area and we wanted to stay ahead of high EAB populations densities and parasitoid dispersal. The new 5 km portion of the study area in the south was lightly infested except for the two woodlots discovered

Jones 19 to the south, which were heavily infested and had likely been so for several years as ash decline and mortality was apparent in spring of 2016. It is likely that these infestations originated from the primary infestation to the north, as previous research by Siegert et al. (2014) documented EAB infestations are characterized by stratified dispersal and that satellite infestations commonly occur several kilometers ahead of the primary infestation. In 2016, high EAB population densities had again progressed south with obvious ash decline (mean health rating ≥ 5) in the north and middle parts of the study area, and most EAB and T. planipennisi were recovered from YPTs in the same areas. This indicated parasitoids had dispersed along much of the original study area by fall 2015 and so after three years their populations were moving with EAB populations. Parasitoids were only detected south of R04 later in the year during summer and fall, suggesting overwintering populations likely emerged from areas in the middle near R3 and dispersed ~ 5 km south across an area exhibiting few symptoms of EAB infestation. The ability for one generation of T. planipennisi to disperse such a distance is not surprising given laboratory flight mill tests have shown females are capable of flying 7 km (Fahrner et al., 2014). Once established in the woodlots, it seems the summer generation did not disperse far, as parasitoids from the fall generation were only collected ~ 750 m away. By 2017, parasitoid populations had dispersed across the 5 km gap of trees exhibiting minor symptoms of infestation and were well established near R04. As T. planipennisi dispersed along the study area from 2014 to 2016, the total number of YPT detections each year increased and the average distances of new YPT detections from the previous year’s detections decreased (median distance: 544 m from 2014 to 2015 and 314 m from 2015 to 2016). At the same time, the maximum distance of new detections increased (1.7 to 8.1 km, respectively). A plausible reason for this pattern may be host-dependent dispersal

Jones 20 (French and Travis, 2001), in which T. planipennisi dispersed and foraged across farther distances at lower EAB population densities in order to find hosts (i.e. in 2014, parasitoids were detected closer to R1 where more EAB were recovered, but were detected further from R2 where fewer EAB were recovered, Fig. 1B). As parasitoid populations established and built up in areas with high EAB densities, some individuals dispersed over longer distances – possibly to escape competition and find new foraging habitat. This was likely observed in 2016 as parasitoid populations established in the northern part of the study area (represented by an increase in the number of positive traps), while new trap detections were ~ 8 km to the south (Fig. 1D). This type of dispersal behavior indicates T. planipennisi is well suited and capable of dispersing over long distances, despite their relatively small size. Assuming most T. planipennisi detected in YPTs dispersed from northern release points, then detection of parasitoids at the southern extent of the study area in 2016 would represent ~ 10 km of dispersal in three years. Dispersal could have also been significant in 2017, but was likely not detected because parasitoid populations had already established at the southern extent of the study area. Recovery of parasitoids in YPTs parallel to the Greenway was another strong indication of dispersal and foraging capabilities of T. planipennisi (Fig. 3). Parasitoids were detected on both sides of the Greenway in traps 3.9 km away from the corridor, on trees that were open grown and along rights-of-ways, and in both agricultural and urban areas. For example, a YPT affixed to an open grown 7 cm DBH tree located ~ 1.5 km from the Greenway across agricultural fields caught 26 individuals. Recovery of parasitoids from such a diverse array of YPT placements is encouraging and suggests T. planipennisi not only established and dispersed well along the Greenway, but was also able to forage across large areas devoid of ash to find hosts.

Jones 21 One S. agrili adult was recovered, but location and timing of detection suggested it was likely associated with a release. We cannot be certain of O. agrili establishment since none were recovered during our study, but other studies in New York have detected the egg parasitoid using YPTs (Parisio et al., 2016). Furthermore, studies in the Midwest used a more detailed sampling technique of sorting through bark scrapings and determined the parasitoid had established (Duan et al., 2011a, 2011A; Abell et al., 2014), and an ongoing study in New York using the same methods also indicates establishment (MKF/JRG unpublished data). We stopped releasing S. agrili in the first year after evidence from concurrent studies suggested it was not establishing in northern climates (Duan et al., 2014a, 2015; USDA-APHIS/ARS/FS, 2015). Both native and introduced species of Spathius are commonly recovered in YPTs (Gould et al., 2009; Duan et al., 2013b, 2014a), therefore the lack of S. agrili detections in our study suggest it did indeed fail to establish.

5. Conclusions This study documented T. planipennisi is adept at following the movement of EAB populations and dispersed at least 10 km in four years. We also detected parasitoids in traps from May to September each year of the study, suggesting T. planipennisi is completing multiple generations each season and taking advantage of EAB undergoing one and two-year life cycles. We caught increasingly more T. planipennisi each year of the study, suggesting they are exhibiting a numerical response to higher EAB densities. The combination of highly successful establishment and dispersal capabilities of T. planipennisi in this study, as well as high host specificity, short development time, high reproductive potential, and female biased sex-ratio

Jones 22 (Duan et al., 2011), suggest this parasitoid species will be an important biological control agent of EAB in North America.

Jones 23 Acknowledgements We would like to thank SUNY ESF research technicians Mike Parisio, Emma Kubinski, and Hope Mahon, Ian Newcomb, Ben Kosalek, as well as Ethan Angell, David DeYoung, Catherine Catranis, and Zachary Corey with NYS Agriculture & Markets for their help releasing parasitoids and collecting samples. We are thankful to Meg Janis and Kristine Uribe from NYS County Parks for their partnership and enthusiasm in allowing us to conduct research along the Genesee Valley Greenway. We also thank the NYS Department of Environmental Conservation for supplying us with a research vehicle. This work was supported by the USDA National Institute of Food and Agriculture, McIntire Stennis project # 1000208 and the US Department of Agriculture, Animal and Plant Health Inspection Service.

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Jones 27 Gould, J.R., Fraser, I., Yang, Z., Wang, X.-Y., Mastro, V.C., Williams, D., 2009. Update on EAB biocontrol: release and recovery of Spathius agrili and discovery of new potential biocontrol agents in Asia. In. 20th USDA Interagency Research Forum on Invasive Species. Annapolis, MD, p. 29. Hanson, A.A., Venette, R.C., Lelito, J.P., 2013. Cold tolerance of Chinese emerald ash borer parasitoids: Spathius agrili Yang (Hymenoptera: Braconidae), Tetrastichus planipennisi Yang (Hymenoptera: Eulophidae), and Oobius agrili Zhang and Huang (Hymenoptera: Encyrtidae). Biol. Control 67, 516–529. https://doi.org/10.1016/j.biocontrol.2013.08.015 Heimpel, G.E., Asplen, M.K., 2011. A ‘Goldilocks’ hypothesis for dispersal of biological control agents. BioControl 56, 441–450. https://doi.org/10.1007/s10526-011-9381-7 Jennings, D.E., Duan, J.J., Bean, D., Gould, J.R., Rice, K.A., Shrewsbury, P.M., 2016. Monitoring the establishment and abundance of introduced parasitoids of emerald ash borer larvae in Maryland, U.S.A. Biol. Control 101, 138–144. https://doi.org/10.1016/j.biocontrol.2016.07.006 Jones, M.I., Gould, J.R., Fierke, M.K., 2017. Mortality of overwintering emerald ash borer (Coleoptera: Buprestidae) associated with an extreme cold event in New York, United States of America. Can. Entomol. 149, 482–486. https://doi.org/10.4039/tce.2017.17 Jones, M.I. 2018. Dispersal, phenology, and cold hardiness of emerald ash borer and it's introduced parasitoids (doctoral dissertation). State University of New York, College of Environmental Science and Forestry. Lindell, C.A., McCullough, D.G., Apostolou, N.M., Roth, M.B., 2008. Factors influencing woodpecker predation on emerald ash borer. Am. Midl. Nat. 159, 434–444.

Jones 28 Liu, H., Bauer, L.S., Gao, R., Zhao, T., Petrice, T.R., Haack, R.A., 2003. Exploratory survey for the emerald ash borer, Agrilus planipennis (Coleoptera: Buprestidae), and its natural enemies in China. Gt. Lakes Entomol. 36, 191–204. MapBioControl.org. 2018. Agent release tracking and data management for federal, state, and researchers releasing biocontrol agents for management of the emerald ash borer. Available online: http: //www.mapbiocontrol.org/ (accessed on 18 August 2018). Marshall, J.M., Storer, A.J., Fraser, I., Beachy, J.A., Mastro, V.C. 2009. Effectiveness of differing trap types for the detection of emerald ash borer (Coleoptera: Buprestidae). Environ. Entomol. 38, 1226–1234. https://doi.org/10.1603/022.038.0433 McCullough, D.G., Mercader, R.J., Siegert, N.W., 2015. Developing and integrating tactics to slow ash (Oleaceae) mortality caused by emerald ash borer (Coleoptera: Buprestidae). Can. Entomol. 147, 349–358. https://doi.org/10.4039/tce.2015.3 McCullough, D.G., Siegert, N.W., Bedford, J., 2009. Slowing ash mortality: a potential strategy to slam emerald ash borer in outlier sites. In. 20th USDA Interagency Research Forum on Invasive Species. Annapolis, MD, 44–46. McCullough, D.G., Siegert, N.W., Poland, T.M., Pierce, S.J., Ahn, S.Z., 2011. Effects of trap type, placement and ash distribution on emerald ash borer captures in a low density site. Environ. Entomol. 40, 1239–1252. https://doi.org/10.1603/EN11099 Mercader, R.J., Siegert, N.W., Liebhold, A.M., McCullough, D.G., 2009. Dispersal of the emerald ash borer, Agrilus planipennis , in newly-colonized sites. Agric. For. Entomol. 11, 421–424. https://doi.org/10.1111/j.1461-9563.2009.00451.x Mercader, R.J., Siegert, N.W., Liebhold, A.M., McCullough, D.G., 2011. Influence of foraging behavior and host spatial distribution on the localized spread of the emerald ash borer,

Jones 29 Agrilus planipennis. Popul. Ecol. 53, 271–285. https://doi.org/10.1007/s10144-010-02336 Parisio, M.S., Gould, J.R., Vandenberg, J.D., Bauer, L.S., Fierke, M.K., 2016. Evaluation of recovery and monitoring methods for parasitoids released against emerald ash borer. Biol. Control 106, 45–53. https://doi.org/10.1016/j.biocontrol.2016.12.009 Poland, T.M., McCullough, D.G., 2014. Comparison of trap types and colors for capturing emerald ash borer adults at different population densities. Environ. Entomol. 43, 157– 170. https://doi.org/10.1603/EN13137 R Core Team. 2018. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/ Siegert, N.W., McCullough, D.G., Liebhold, A.M., Telewski, F.W., 2014. Dendrochronological reconstruction of the epicentre and early spread of emerald ash borer in North America. Divers. Distrib. 20, 847–858. https://doi.org/10.1111/ddi.12212 Siegert, N.W., McCullough, D.G., Williams, D.W., Fraser, I., Poland, T.M., Pierce, S.J., 2010. Dispersal of Agrilus planipennis (Coleoptera: Buprestidae) from discrete epicenters in two outlier sites. Environ. Entomol. 39, 253–65. https://doi.org/10.1603/EN09029 Sobek-Swant, S., Crosthwaite, J.C., Lyons, D.B., Sinclair, B.J., 2012. Could phenotypic plasticity limit an invasive species? Incomplete reversibility of mid-winter deacclimation in emerald ash borer. Biol. Invasions 14, 115–125. https://doi.org/10.1007/s10530-0119988-8 Smith, A., 2006. Effects of community structure on forest susceptibility and response to the emerald ash borer invasion of the Huron River watershed in southeast Michigan (master’s thesis). The Ohio State University.

Jones 30 Taylor, R.J., Bauer, L.S., Poland, T.M., Windell, K.N., 2010. Flight performance of Agrilus planipennis (Coleoptera: Buprestidae) on a flight mill and in free flight. J. Insect Behav. 23, 128–148. USDA. 2018. Plant hardiness zone map. Available online: http://planthardiness.ars.usda.gov/PHZMWeb/Default.aspx (accessed 18 August 2018) USDA-APHIS/ARS/FS. 2015. Emerald ash borer biological control release and recovery guidelines. USDA-APHIS-ARS-FS, Riverdale, Maryland. Yang, Z., Strazanac, J.S., Marsh, P.M., Van Achterberg, C., Choi, W., 2005. First recorded parasitoid from China of Agrilus planipennis: a new species of Spathius (Hymenoptera: Braconidae: Doryctinae). Ann. Entomol. Soc. Am. 98, 636–642. https://doi.org/10.1603/0013-8746(2005)098[0636:FRPFCO]2.0.CO;2 Zhang, Y-Z., Huang, D-W., Zho, T-H., Liu, H-P., Bauer, L.S., 2005. Two new species of egg parasitoids (Hymenoptera: Encyrtidae) of wood-boring beetle pests from China. Phytoparasitica 33, 253–260.

Jones 31 Table 1. EAB infestation metric used to assess ash health. Canopy rating adapted from Smith, 2006.

Jones 32 Figure 1. Map of the study area along the Genesee Valley Greenway State Park depicting southerly progress of the EAB infestation (using ash health ratings and EAB caught in YPTs) and T. planipennisi caught in YPTs (n = 62 traps/year; deployed every 250 m). In 2016, the study area was shifted south 5 km and a reference point (R04) was established 5 km south of R3.

Figure 2. Mean (±SE) number of EAB and T. planipennisi collected from YPTs along the Greenway from 2013 to 2017, summarized by the groups of 21 traps centered on each release point, (n = 21 traps for R1, R3, & R04; n = 20 traps for R2; total = 62 traps/year). Numbers at top of each bar indicate total positive traps. In 2016 and 2017, the study area was moved south by 5 km and a new reference point (R04) was established 5 km south of R3. R04 is indicated in 2013, 2014, and 2015 to emphasize the shift in study area. No data were collected from traps near R1 in 2016 and 2017.

Figure 3. In 2016, 20 YPTs were established every 500 m on each side (n = 40) of the Greenway study area along a relatively parallel 10 km route. Both, EAB and T. planipennisi were detected in YPTs that were 500 m to 3.9 km from the Greenway.

Figure 4. Percent of uninfested, infested, and dead infested ash trees and mean (±SE) health rating summarized by year and group of plots centered on each release point (n = 21 plots for R1, R3, and R04 ; n = 20 plots for R2; total = 62 plots/year). R04 is indicated in 2014 and 2015 to emphasize the shift in study area. No data were collected from plots near R1 in 2016. Letters indicate significantly different means ( = 0.05).

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Jones 37 Highlights 

Monitored emerald ash borer parasitoid dispersal along an infested ash corridor using yellow pan traps



Both Tetrastichus planipennisi and emerald ash borer were recovered in traps



T. planipennisi established and dispersed to areas with high EAB population densities



T. planipennisi were recovered > 10 km from release points 5 years after release

Jones 38