Abstract
Background The European elm scale (EES), Gossyparia spuria (Modeer)(Hemiptera: Eriococcidae), has been a marked pest on American elm (Ulmus americana) in western states since its invasion. Tactics to control this insect pest have been largely based on chemical controls; first insecticidal sprays and then systemic applications, but in recent years insecticide resistant scales have become an apparent problem.
Methods This paper (1) outlines how insecticide resistance was likely established in Colorado, (2) documents neonicotinoid resistance in this plant parasite by showing scale insects feeding on trees with high levels of imidacloprid insecticides, and (3) explores alternative control options that will be integral to maintaining American elms as part of the urban landscape in western states: i.e., acephate, e.g., ACE-jet (Arborjet, Woburn, MA, USA) and Lepitect (Rainbow Ecoscience, Minnetonka, MN, USA); azadirachtin, e.g., AzaGuard® (BioSafe Systems, LLC, East Hartford, CT, USA) and AzaSol (Arborjet, Woburn, MA, USA); buprofezin with and without horticultural oil, e.g., Talus (SePRO Corporation, Carmel, IN, USA); and pyriproxyfen with and without horticultural oil, e.g., Distance® (Valent Professional Products, Walnut Creek, CA, USA).
Results Based on our findings, the current recommendation for control of neonicotinoid resistant EES is using the insect growth regulator pyriproxyfen (e.g., Distance), which is applied as a spray. In addition to pesticides, we found several natural insect enemies that attacked the EES in Colorado. We captured 11 species of wasps that parasitize the EES from emergence cages. Through cultivar resistance experiments, we have also identified several elm varieties that show promise in reducing EES damage, suggesting their suitability for planting in urban landscapes.
Conclusion This study investigated alternative chemical control treatments, documented biological control agents present in the area, and screened for cultivars with scale resistance, all of which need to be considered to maintain American elms with longstanding EES infestations successfully.
Introduction
In Western North America, including Colorado, American elm (Ulmus americana L.) remains a common and highly valued shade tree. Dutch elm disease and the associated bark beetle vectors remain a concern in this region, but rigorous sanitation efforts have greatly limited tree losses from this source. A second threat that can affect American elm is the European elm scale (EES), Gossyparia spuria (Modeer).
The EES was unintentionally introduced into North America from Europe, and this insect was first reported from Westchester, NY (Howard 1889). It subsequently spread throughout North America (Hartzell 1919; Miller and Miller 1993; García Morales et al. 2016), but significant problems have long been reported in Western North America, where American elm is not native (Herbert 1924). There, high populations of EES are a chronic condition on most American elm, with EES often heavily encrusting limbs, contributing to branch dieback and retarding tree growth (List 1920). Newly transplanted trees with thinner bark are particularly susceptible and may sustain high populations packed within bark furrows of the trunk, sometimes sufficient to kill trees. European elm scale is also a prodigious producer of honeydew, capable of causing serious nuisance problems, which greatly diminish the host’s value as a street tree (Kosztarab and Kozár 1988).
Historically, EES was managed by a variety of insecticide sprays, applied during the dormant season or targeting the crawler stages (Cleveland 1931; Deay and Ulman 1948; Thompson 1962; Thompson 1967; Cranshaw et al. 1989). Initial trials using systemic insecticides were not effective (Weaver and Dorsey 1966). However, in the early 1990s, tests of the systemic insecticide imidacloprid were found to be extremely effective against EES when applied as a soil treatment (Sclar and Cranshaw 1996). As a result of the outstanding control provided and ease of use, this new application method was rapidly adopted as the standard for control; subsequently, almost every American elm within the Front Range communities of Eastern Colorado received a soil application of imidacloprid, usually on an annual or biannual schedule. As additional soil-applied insecticides became available for EES control (chlothianidan, dinotefuran), they were sometimes substituted. However, all of the soil-applied systemic insecticides (imidacloprid, chlothianidan, dinotefuran) used during this period were in the neonicotinoid class of insecticides with the same mode of action, nicotinic acetylcholine receptor (NACHR) competitive modulators, according to the Insecticide Resistance Action Committee (IRAC 2024). In most urban areas of Colorado, this has resulted in the continuous use of one or more neonicotinoid insecticides on essentially every American elm for almost 2 decades.
Development of a Problem—Neonicotinoid Resistance in European Elm Scale
In the early 2000s, some arborists first observed cases where imidacloprid appeared to diminish in effective EES control. The number of such reports has steadily increased and occurred over a progressively wide area in following years. Although there are many possible reasons for unexpectedly poor performance following a soil application of an insecticide, the reported situations suggested resistance to the insecticide was a plausible cause.
To investigate whether evidence supported neonicotinoid resistance in some Colorado EES populations, a total of 22 mature imidacloprid-treated trees that ranged from approximately 30 to 50 in at DBH, located in Fort Collins and Greeley, were selected in 2014. These trees were chosen based on information from industry professionals who noticed a range in EES control, some with a notable lack of control where scale populations were high and damaging, on imidacloprid-treated trees. These trees were managed by the City of Fort Collins, City of Greely, Colorado State University arborists, and private property owners. All trees were located in irrigated turf areas. Between 2014 August 15 and August 23, 12 leaves were collected toward the bottom of the canopy in 4 cardinal directions using a pole pruner.
A plot comparing the concentration of imidacloprid to the average number of nymphs on leaves confirmed leaves from 10 trees treated by imidacloprid supported high numbers of EES (ranging from 16 to 177 average nymphs/leaf), suggesting poor control; 10 imidacloprid-treated trees had only low numbers of nymphs (ranging from 0 to 9 nymphs/leaf), suggesting good-excellent control (Figure 1). Two trees had lower levels of imidacloprid (ranging from 0.3 to 0.5 ng/mL in leaf tissue) and low infestation (ranging from 0 to 4 nymphs/leaf).
The concentration of imidacloprid residue in leaves (ng/mL) and the number of European elm scale (EES)( Gossyparia spuria) nymphs on leaves collected from 22 American elm trees in 2014 August. All trees had been treated with imidacloprid and were located in either Fort Collins or Greeley, CO. Trees were selected to show a range in perceived EES control, from good-excellent to poor.
At the same time, additional leaves were collected to analyze levels of imidacloprid residue present in foliage. After collection, leaves were kept on ice and immediately stored in a –80 °C freezer until preparation and analysis. Residue analysis was subsequently performed on 0.1-g samples of macerated leaf tissue diluted 1:10 in water. Samples were centrifuged at 9,000 rpm for 2 minutes which prepared the supernatant for use in an Enzyme-Linked Immunosorbent Assay (ELISA)(Abraxis LLC, Westminster, PA, USA). Samples were processed as described by the kit, and the ELISA absorbance readings were plotted as a logistic 4 parameter curve to determine the concentration of imidacloprid in the leaf tissues.
Residue levels in leaf tissues ranged threefold among the samples, from approximately 0.3 to 0.9 ng/mL as shown in the nonlinear pattern depicted in the bivariate plot (Figure 1). Indeed, all of the trees that experienced high numbers of EES nymphs (> 16 nymphs/leaf) also had high concentrations of imidacloprid (> 0.75 ng/mL)(Figure 1). This finding provided the first strongly supportive evidence that resistance to imidacloprid had developed within some EES populations in Colorado. Further evidence emerged from subsequent insecticide evaluations, one of which is described below. These found not only imidacloprid but also other neonicotinoid insecticides (e.g., dinotefuran, chlothianidan) to fail consistently in providing EES control, indicating scales cross-resistant to all insecticides in the neonicotinoid class. To our knowledge, this is the first recorded instance of insecticide resistance in a shade tree system.
Search for an Alternative Control for Neonicotinoid-Resistant European Elm Scale
A large-scale experiment was begun in 2014 to evaluate alternatives to imidacloprid for the control of EES. The trial was conducted on a stand of mature American elms located on the Colorado State University Fort Collins campus. The seedling American elms used in the experiment were planted in 1881, 1922, and 1925 and have received supplemental irrigation since planting (Alexander 1998). American elms were spaced approximately 35 ft (10.67 m) away from neighboring elms and ranged from 30 to 57 in (76.2 to 144.78 cm) at DBH for an average of 41 in (104.14 cm) at DBH. During the experiment, the elms receive supplemental water from March to November. During the peak growing season of June, July, and August, irrigation occurs approximately 3 times per week and results in 1.5 in (3.81 cm) of water. These trees had previously received regular soil applications of imidacloprid on an annual or biannual basis for at least 16 years, but prior to the trial, there were indications of decreasing EES control at the site.
The trial was arranged in a randomized complete block design with 5 replications. Individual trees were considered the plot units, with each tree within a replication receiving a different insecticide treatment. Four treatments involved foliar sprays made 2014 May 28: Distance® (pyriproxyfen; Valent Professional Products, Walnut Creek, CA, USA) 8 fl oz/100 gal; Distance® 8 fl oz/100 gal + 1% horticultural oil; Talus 70DF (buprofezin; SePRO Corporation, Carmel, IN, USA) 14 oz/100 gal; and Talus 70DF 14 oz/100 gal + 1% horticultural oil. Trunk injections (Arborjet microinjection system, Woburn, MA, USA) were made as a series every 6 in (15.24 cm) around the base of the trees on 2014 June 18. AzaSol (azadirachtin; Arborjet, Woburn, MA, USA) was applied at the rate of 4 mL/in DBH; ACE-jet (acephate; Arborjet, Woburn, MA, USA) was applied at a rate of 9 mL/injection. A soil injection of Zenith (imidacloprid; Bayer Corporation, Whippany, NJ, USA) at 0.2 fl oz/in DBH was made 2014 July 5.
Some additional treatments were included in late June of 2015, applied to trees that were not treated with any insecticides the previous year. This included trunk injection of new trees with both AzaSol and ACE-jet. AzaGuard® (a second azadirachtin formulation)(Bio-Safe Systems, LLC, East Hartford, CT, USA) was injected (0.6 fl oz/in DBH) using the Rainbow Tree Care macro-infusion equipment (Rainbow Ecoscience, Minnetonka, MN, USA). In addition, a soil injection application of Lepitect (acephate; Rainbow Ecoscience, Minnetonka, MN, USA) at a rate of 0.4 oz/in DBH was included.
Following the 2014 applications, an initial evaluation was made by collecting branch sections from each tree in the trial on 2014 August 21 and 22. Branches were collected using a pole pruner; when the canopy was too high, a bucket truck was used. Four small branches were collected from different areas of the canopy of each tree, and the number of scales present 30 cm beyond the current-year growth were counted to obtain data on the current-year infestation. During the August collection, many of the scales had begun to move back to twigs, so counts were made of scales on both leaves (12 leaves/tree) and twigs (3 twigs/tree). A second evaluation was made of these trees the following spring (2015 May 18–22), when all scales were on small branches and females had begun to swell with maturing eggs. A similar evaluation was made in 2015, collecting sample branches on May 24 and 27 from trees involved in both 2014 and 2015 applications. Data from each sampling date were analyzed separately using an ANOVA followed by a Tukey HSD on log-transformed data to satisfy model assumptions. Significant differences were based on P ≤ 0.05, analyzed using JMP software (11.1.0v; SAS Institute, Cary, NC, USA). All data were backtransformed in the presentation of figures and descriptive statistics.
During the initial 2014 August sampling, some significant suppression of EES remaining on leaves was noted with ACE-jet (74.1% compared to check, P = 0.0066) and Distance® (53.5%, P = 0.0367) treatments (Table 1). There was a reduction in the number of nymphs on twigs at this time following the Talus + horticultural oil treatment (64.9%, P = 0.0238). Importantly, there were no differences in EES between the control and imidacloprid treatments on leaves or twigs (P = 1 and P = 0.9995, respectively).
Number of European elm scale (EES)(Gossyparia spuria) nymphs on leaves or twigs collected from mature American elm included in an insecticide evaluation trial conducted during 2014 to 2016. Five trees were used in each treatment. In 2014, the different insecticide treatments were applied between May 28 and July 5; all 2015 treatments occurred in June. Data from each sampling date were analyzed separately using an ANOVA followed by a Tukey HSD on log-transformed data. Data are presented on the original scale (mean ± standard error). Numbers not followed by the same letter are significantly different (P ≤ 0.05).
Some of the results shifted when the trial was re-evaluated the following spring (2015 May). At that time, superior control was observed on twigs from trees treated with Distance® (97%, P = 0.0009); Distance® combined with horticultural oil also looked promising (91%, P = 0.0037). Though not significantly different, AzaSol also looked better at this time (69.2%, P = 0.8421) than during the previous August evaluation. Effectiveness appeared to decline with the ACE-jet and Talus treatments, as they were no different than the control (P = 1 and P = 0.9998, respectively).
In the following year’s evaluation (2016 May), trees treated in 2014 with Distance® continued to provide the best control of EES (Distance® alone 63%, P = 0.2391; and Distance® + horticultural oil 77%, P = 0.0148). Trees treated in 2015 with the azadirachtin formulations AzaGuard® and AzaSol provided 65% and 43% control, respectively (P = 0.0448 and P = 0.9974). The sole non-neonicotinoid soil injection, Leptitect, provided 59% control (P = 0.8182). Trees treated in 2014 with a neonicotinoid Zenith (imidacloprid) tended to have the highest number of scales in the spring 2015 and 2016 surveys of twigs, 168% and 148% compared to the control, and continued to show no difference from the control in 2015 (P = 0.9818) or 2016 (P = 0.9959).
Leaves from trees treated with imidacloprid in 2014 were collected in 2014 and 2015 August to sample for residues of imidacloprid, using the methods described above. This indicated average concentrations of 0.88 ng/mL and 0.38 ng/mL from collections made in the 2 consecutive years. This indicated that residue levels decreased approximately half the year following application but remained high. These high levels of imidacloprid found in leaves, combined with poor (negative) control of EES, are further indications of resistance to imidacloprid among scales at this site.
Based on these results, the current recommendation for control of neonicotinoid resistant EES is the use of the insect growth regulator pyriproxyfen (Distance®) applied as a spray. Where sprays are not possible, alternatives that can provide some control include trunk injections with either azadirachtin (AzaGuard®, Azasol) or acephate (ACE-jet) or soil injections with acephate (Lepitect). Though not included in the study, new generation products targeted towards piercing/sucking insects should be tested for efficacy against EES in search of less toxic alternatives.
Potential Roles of Biological Control Organisms
Because of the more limited ability to control EES with insecticides, there has been renewed interest in the potential of other management methods. This includes developing information on biological controls of EES (e.g., predators, parasitoids of EES). These have received little previous attention in Colorado, but their potential significance was alluded to in the first discussion of EES management in the state:
Practically all insects, after they have been established in a section a great length of time, have many natural enemies in the form of parasitic and predaceous insects, bacterial and fungus diseases, birds and other animals that tend to keep them in check. But when the insect is transported to another country, it escapes its enemies and develops unhindered. (List 1920)
Seeing that EES has been established in Colorado for over 100 years, a survey of biological control agents was timely.
Better information on existing natural controls can be used in a few ways. For one, it can be used to help integrate existing natural enemies with other controls (e.g., insecticides) by identifying periods when natural enemies are most active and likely to be exposed to insecticides. Surveys can also identify what natural enemy species are present—and absent. This can suggest biological control species that may be good candidates for future introductions where they do not already exist.
To identify predator species associated with EES, sampling was conducted on heavily infested American elms on the Colorado State University campus during 2014 and 2016. Twenty ‘Valley Forge’ cultivars were planted in 2011, ranging in DBH from 3 to 13 in (7.62 to 33.02 cm) and averaging 6 in (15.24 cm) at DBH in 2017. These were used to evaluate the presence of predatory arthropods. Tree spacing and irrigation schedules were the same as other experiments using Colorado State University trees. Sampling was done monthly from June to August by rapidly beating scale-infested branches 10 times over a collecting tray to dislodge insects (Figure 2). Two beat sheet samples were taken from each tree and arthropods were collected for subsequent identification (Table 2).
Pictures illustrating the damage caused by European elm scale (EES) and various predators found while sampling heavily infested American elm. (a) Picture of an American elm infested with EES. Black coloration is caused by the growth of sooty mold on honeydew excreted by EES. (b) Green lacewing larvae (Chrysoperla rufilabris) eating EES. (c) Parasitoid wasp ovipositing in/on EES. (d) Predatory mirid (Chlamydatus associatus) found on American elm. (e) Convergent lady beetle (Hippodamia convergens) eating EES. (f) Seven-spot lady beetle (Coccinella septempunctata) eating EES. (g) An arrow pointing to a parasitized and mummified EES.
The number of predatory species found on 20 ‘Valley Forge’ cultivars of American elm infested with European elm scale (EES)(Gossyparia spuria). Predators were dislodged from the tree and collected for identification using beat sheet sampling techniques once per month in June, July, and August of 2014 and 2016. Count data is presented to show the diversity in predatory arthropods.
To assess the activity of parasitoid wasps, field collections were made in 2016 and 2017. Between April and September of each year, 5 branch samples, 30 cm beyond the current-year growth of EES-infested American elm, were collected from each of 3 different sites around Fort Collins, CO, at biweekly intervals.Sites included mature American elms at Colorado State University’s Oval Drive and the City of Fort Collins’ City Park, as well as unirrigated mature American elms in a shelter belt at the Colorado State Forest Service nursery. Additional samples were obtained at one time point from an irrigated mature elm at the University of Colorado Boulder main campus; from a mature, sporadically irrigated street tree in North Boulder, CO; and a nonirrigated mature elm at the Agricultural Research, Development and Education Center, Colorado State University. The branches were then placed into emergence cages and maintained for parasitoid collection.
As many as 11 species of parasitoid wasps were collected from emergence cages containing EES-infested branches in 2016 and 2017 (Table 3 and Figure 3). However, it has not been possible to get positive identifications for any of these, and some may be different forms/sexes of the same species or hyperparasitoids. Emergence of parasitoids occurred on collections made throughout the study period (April through September) but were greatest from mid-May through mid-July. The most encountered was a Coccophagus species (Hymenoptera: Aphelinidae), which was recovered from samples collected throughout the study period and at incidence exceeding 7% on some collection dates. Related species, C. gossypariae, C. insidiator, and C. lycimnia, have been documented as predominant parasitoids of the EES (Kosztarab and Kozár 1988; Kosztarab 1996; García Morales et al. 2016). The known parasitoid C. insidiator was introduced and established in California (Flanders 1952; Dreistadt and Hagen 1994), and other species of Trichomasthus and Metaphycus have been documented parasitizing EES (Dreistadt and Hagen 1994).
Pictures of 11 parasitoid wasp species found to emerge from EES-infested branches. However, it has not been possible to get positive identifications for any of these, and some may be different forms/sexes of the same species or hyperparasitoids. (a) Species A, (b) Species B, (c) Species C, (d) Species D, (e) Species E, (f) Species F, (g) Species G, (h) Species H, (i) Species I, (j) Species J, (k) Species K. Species identifications of the parasitoids have not been completed.
Total parasitoid wasps collected from emergence cages containing 30-cm long branches taken from mature American elms on Colorado State University’s campus infested with European elm scale (EES)(Gossyparia spuria). The count data are presented to show the diversity of parasitoid wasps.
The greatest activity of both the insect predators and parasitoids was found to occur during a 2-month period running from mid-May to mid-July. It is, therefore, suggested that any use of insecticides that might adversely affect these natural enemies of EES be applied at times outside this period. Quesada and Sadof (2020) show that applications of reduced risk insecticides like pyriproxyfen during the period of crawler activity had minimal impact on natural enemies compared to broad spectrum products.
These results show that some insect natural enemies present attack EES in Colorado. Furthermore, there exists a large number of parasitoid species, so there is likely limited value in attempts to introduce additional species present elsewhere in North America. However, despite the presence of a natural enemy component attacking EES in Colorado, they clearly are not sufficiently effective to provide adequate EES control. European elm scale presenting less of a problem in Eastern North America compared to Western areas (Herbert 1924) may be due to the reduced efficiency of natural enemies. Studies on another soft scale insect, Parthenolecanium corni, suggest that temperature plays a role in decreasing parasitism levels when the environment is hot and scale densities are high (Dawadi and Sadof 2023). Effectiveness of EES parasitoids could perhaps also be related to regional differences affecting insect ecology on American elm.
Is Host Plant Resistance the Future for Control?
A considerable range in susceptibility to EES exists among different elm species and cultivars. This is well indicated when comparing the 2 most commonly grown elm species in Colorado: American elm (U. americana) and Siberian elm ( U. pumila L.). American elm is consistently infested by EES at high, damaging levels; ESS is rarely found on Siberian elm and never in high population.
Observations of the elms grown in Colorado for the National Elm Trial (Griffin et al. 2017) provided an excellent opportunity to make comparisons of EES among several cultivars in a replicated planting (Table 4). National elm trial cultivars were planted in 2005 within a common garden plot. There were 5 replications of 17 cultivars ( n = 85) spaced 18 to 20 ft from neighboring elms. Throughout the growing season, they received 1 hour of supplemental water every 3 days using a drip irrigation system. Water levels were adjusted to allow trees to go into dormancy in the fall before the first freeze. Each tree was evaluated to determine the presence of EES on 2013 September 23 and 2014 May 20. In 2012, cultivars ranged from 0.2-in (0.5-cm) DBH to 5.6-in (14.2-cm) DBH with an average DBH of 2.2 in (5.6 cm).
Infestation of elm cultivars with European elm scale (EES)(Gossyparia spuria) observed in replicated plantings at Colorado State University in association with the National Elm Trial. Trees were evaluated for percent of branch/leaves infested and percent of the tree crown affected in 2013 and 2014, then ratings were used to determine placement on a 3-point scale: 1–No Scale Observed; 2–Scale Present, Low Level (up to 30% of canopy affected or branches infested); and 3–Scale Present, High Level (30% or more of leaves or branches infested and canopy).
Three of the four U. americana cultivars included in this study were extremely heavily infested by EES (‘Lewis and Clark’, ‘Valley Forge’, ‘Princeton’). At the trial site in Fort Collins, CO, EES infestation led to the complete loss of ‘Lewis and Clark’ and a 40% loss of ‘Princeton’. Concurrently grown plantings of ‘Valley Forge’ on the campus of Colorado State University have been so heavily damaged by EES that many have been removed, and the remainder have required insecticide (pyriproxyfen) treatment. The U. americana cultivar ‘New Harmony’ showed less susceptibility to EES. Also found to be seriously damaged by EES were the hybrids ‘Patriot’, ‘New Horizon’, and ‘Pioneer’.
Griffin et al. (2017) reported that scale insects—a mixture of EES and European fruit lecanium, Parthenolecanium corni (Bouché)—were a minor issue in most trial locations, which were located almost exclusively in the Eastern half of the United States. They found that across all locations, scale insects were reported most damaging on ‘New Harmony’, ‘Morton’, ‘New Horizon’, and ‘Morton Glossy’, all of which had infestation that led to affected crowns from EES in Colorado. The fourth cultivar, ‘Morton’ (Accolade™), was not observed to be infested with EES in Colorado, along with ‘Morton Stalwart’ (Commendation™) and ‘Morton Plainsman’ (Vanguard™). All of these cultivars, except ‘New Harmony’, are elms of Asian parentage, and most all were hybrids. Even with supplemental irrigation, some cultivar differences in EES density and susceptibility to EES could be regional differences associated with adaptation. Establishment and performance varied among the National Elm Trial cultivars and could be attributed to climatic differences (Griffin et al. 2017). In other systems, precipitation and urban heat islands have not only impacted tree growth but also the capacity to withstand scale populations (Frank and Just 2020; Dale and Frank 2022).
The difficulty in controlling EES in sites where populations have developed resistance to neonicotinoid insecticides precludes the consideration of most, if not all, American elm cultivars presently being developed. If American elm is to be considered a viable species for future planting in Western North America, then resistance to EES will have to be a critical feature. This will require exploring genotypes that show resistance to this insect and introducing these into nursery production. Fortunately, there are indications that this can be, with some effort, a real possibility.
Resistance to EES in an American elm was first recognized almost 25 years ago. At that time, City Forester Tim Buchanan noticed that one elm in Fort Collins (CO) City Park did not show the extensive blackening on the bark produced by sooty mold that grows on EES-excreted honeydew. Following up, he arranged with a local nursery in 1996 to propagate a couple dozen trees from cuttings. When large enough (2001), these trees were planted at several locations within the city as street trees. Examination of these trees was similar to the National Elm Trial evaluations and included an annual site visit in 2016 and 2017 to determine the level of scale present on branches/leaves and whether the canopy was affected. A few scales were present but in very low and non-damaging numbers, which confirms some level of resistance. Additional cuttings from these EES-resistant elms have since been collected and are presently being propagated using the trade name ‘Scalebuster’.
The need to discover additional EES-resistant American elms is now a regular message being regionally promoted among arborist groups. Recently, a few additional trees have been found that appear to be EES-resistant, and it is reasonable to expect that more will be found in the near future. EES-resistant elms that are developed as a result could become as important a feature to the future of American elm in Western North America as Dutch elm disease resistance is in the east.
Conclusion
In an attempt to establish diverse and resilient urban forests, finding ways to maintain plantings of iconic tree species is imperative. Currently, EES is the most significant pest affecting American elms in Western North American communities and, therefore, an essential problem to study. After years of successful EES treatment using neonicotinoid insecticides, in some instances, these products are not providing ample control. We documented this phenomenon in Colorado by showing that EES fed on the plant tissues of neonicotinoid-treated trees that contained significant amounts of insecticide residues. As is typical in cases of insecticide resistance, scales were documented more frequently on imidacloprid-treated trees when compared to untreated check trees. As a result, American elms are experiencing severe damage by EES, and management tactics are needed. This study investigated alternative chemical control treatments, documented biological control agents present in the area, and screened for cultivars with scale resistance, all of which need to be considered in order to successfully maintain American elms with longstanding EES infestations.
Acknowledgements
The authors thank Barbra Rose at the Colorado State University Veterinary Teaching Hospital for providing insight and equipment for the ELISA tests. Mike Baars, Austin Broberg, Matt Camper, Kellie Due, Peter Forrence, Alison Hall, Matt Hudson, Jorge Ibarra-Caballero, Emily Luna, and Allison Serafin provided field or laboratory assistance. Arborists at Colorado State University Facilities, Davey Tree Company, SavATree, the University of Colorado Boulder, and Rainbow Treecare Scientific Advancements, including Vince Aquino, Steve Geist, Rodney Gillespie, Don Grosman, Fred Haberecht, David Hansen, Mark Hiatt, Steve McCarthy, Scott Simonds, Toni Smith, Sye Vasquez, and Gery Whiteman, helped collect samples, provide management information on the elms, and/or assisted with treatment applications. Dr. William Jacobi established and maintained the National Elm Trial plots in Fort Collins. He also graciously shared management information and data. City Foresters and arborists in Greeley, Fort Collins, Denver, and Boulder helped locate and allowed use of their American elms, including Shiloh Hatcher, Tim Buchanan, Ralph Zentz, Rob Davis, Rich Wilson, Vince Aquino, Pat Bohin, and Kathleen Alexander. Funding for this project was provided by Colorado State University, Agricultural Experiment Station.
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