Thiabendazole as a Therapeutic Root Flare Injection for Beech Leaf Disease Management

Introduction

Beech leaf disease (BLD) is an emerging threat to American beech (Fagus grandifolia) in Eastern forests, as well as for landscape European (F. sylvatica) and American beech in North America (Ewing et al. 2019). Since the initial detection of the disease in Lake County, OH, in 2012, the disease has spread to 14 additional states in the USA and to Ontario, Canada (Volk and Martin 2023). The disease is caused by the foliar feeding nematode Litylenchus crenatae mccannii (Lcm)(Carta et al. 2020). Symptoms of the disease include conspicuous, foliar interveinal dark green or chlorotic banding; crinkled, epinastic leaves; bud abortion; and eventual tree decline (Fearer et al. 2022). Foliar symptoms associated with the disease are the result of damage that occurs in buds prior to leaf emergence (Carta et al. 2020; Vieira et al. 2023; Fletcher et al. 2024). These symptoms can significantly reduce the photosynthetic potential of the canopy (McIntire 2023; Fletcher et al. 2024), resulting in a progressive depletion of carbohydrate reserves following successive years of infection (Skomarkova et al. 2006).

American beech is an important late-successional hardwood species in eastern North America ranging from as far north as Canada and south into Florida (Tubbs and Houston 1990). Beech are a masting species that produce large quantities of nuts on a cyclical basis that provide a source of nutrition for wildlife such as birds, rodents, deer, and bear (Tubbs and Houston 1990; McCullough et al. 2005). In addition, the epithet of American beech ‘grandifolia’ means large leaf and is in reference to the shade that beech provide as overstory. This shade can be critical for understory habitat for a variety of plant species and wildlife (Stephanson and Ribarik Coe 2017). In addition to the ecological importance of beech, American and European beech are important ornamental shade trees in North America due to their iconic smooth bark, fall color characteristics, and historical use. Beech are also planted in landscapes, parks, and collections. Unabated, BLD is likely to have lasting impacts in natural and planted forest settings, as well as in ornamental and horticultural applications.

The development of management solutions for BLD is paramount, and utilizing pesticides in a management program is likely to be economically feasible for individual trees. Previously, fluopyram, a nematicidal and fungicidal active ingredient in the SDHI (succinate dehydrogenase inhibitor) family of chemistry in the ornamental labeled product Broadform (Envu, Cary, NC, USA) was found to be effective in suppressing numbers of Lcm and reducing symptoms of BLD (Loyd et al. 2024). This product must be applied as a complete foliar cover spray to provide efficacy, which can be challenging for large shade trees. For large trees where sprays are not an option, a systemic treatment applied as a drench or root flare injection is needed. Emamectin benzoate and abamectin are 2 avermectin class pesticides with nematicidal properties that are active ingredients in products labeled for root flare injections of trees. However, neither are effective in reducing Lcm populations or reducing BLD symptoms (Loyd et al. 2024).

Thiabendazole is in the benzimidazole class, FRAC group 1, and is the active ingredient in Arbotect 20-S (Syngenta, Basel, Switzerland). It is a broad-spectrum fungicide containing 26.6% active ingredient thiabendazole hypophosphite (TBZ). This product is routinely used to treat and prevent Dutch elm disease and anthracnose of sycamores when applied as a root flare injection in trees (Stipes 1973; Stennes and French 1987; Himelick and Neely 1988). Although routinely used in the arboriculture industry for these fungal diseases, thiabendazole was originally discovered and classified as a potent anthelmintic for use in treatments against livestock parasites (Brown et al. 1961) and only later found to have antifungal properties (Staron and Allard 1964). In fact, a single dose of 50-mg TBZ/kg body weight eliminated more than 95% of gastrointestinal parasitic nematodes representing 10 different genera in sheep (Brown et al. 1961). Since its discovery, TBZ has been used in veterinary medicine (Kelly et al. 1981; Njanja et al. 1987; Williams and Broussard 1995), agriculture (Vitti et al. 2014), and commercial mushroom production (Mcleod 1973) in suppressing parasitic nematodes. It was approved by the United States Federal Drug Administration in 1967 as a human medication (Mintezol; MERCK & CO., Inc., Rahway, NJ, USA) for treatment of strongyloidiasis (threadworm) and several other parasitic infections (NCATS 2024) until eventual replacement with newer medications. The objective of this study was to determine if thiabendazole applied as a root flare injection to beech trees could suppress the population of Lcm and provide therapy to trees suffering from BLD.

Materials and Methods

Results

Initially, all trees at each location had on average 64 ± 7 (Aurora, OH); 65 ± 4 (Chardon, OH); and 42 ± 4 (Hillsborough, NJ) percent canopy with BLD symptoms and 10 ± 3 (Aurora, OH); 20 ± 2 (Chardon, OH); and 25 ± 2 (Hillsborough, NJ) percent canopy with fine twig dieback. The following growing season post-treatment, there was a significant (P < 0.05) reduction in the percent canopy with BLD symptoms in trees treated with TBZ at the Aurora and Chardon, OH, sites where disease (percent canopy with BLD) was on average reduced by 70% (Aurora, OH) and 85% (Chardon, OH). After 2 growing seasons posttreatment, TBZ-treated trees at the Aurora, OH, site again had significantly lower percent canopy with BLD symptoms than pretreatment ratings, with no increase in disease severity compared to one year posttreatment. At both the Aurora and Chardon, OH, sites, the percent of the canopy with fine twig dieback did not significantly (P > 0.05) change over time posttreatment for nontreated control or TBZ-treated trees.

At the Hillsborough, NJ, site, percent canopy with BLD symptoms significantly increased (P < 0.05) in trees treated with TBZ, where treated trees had on average a 66% increase of the canopy with BLD symptoms. However, the percent canopy with fine twig dieback significantly improved (P < 0.05) in the TBZ-treated trees by 71%, while the percent canopy with fine twig dieback significantly increased by 95% in the nontreated control trees.

At all sites and for both pre- and post-treatment years, nontreated control trees had either similar percent canopy BLD symptoms (P > 0.05)(Aurora and Chardon, OH) or significantly increased in percent canopy BLD symptoms (P < 0.05)(Hillsborough, NJ) (Table 1).

On average, there were significantly (P < 0.05) lower numbers of Lcm in dormant bud tissues in TBZ-treated trees compared to the nontreated control trees at the Chardon, OH, and Hillsborough, NJ, sites, and although not significant, a trend of lower quantities of Lcm in dormant buds from the Aurora, OH, site (Table 2). There was significant variation in the Lcm/g of bud tissue. Overall, there was an 86% (Aurora, OH); 99% (Chardon, OH); and 70% (Hillsborough, NJ) reduction in Lcm across TBZ-injected trees compared to nontreated controls.

While there was some damage associated with the injection sites, the frequency of cracked and fluxing sites was generally low across all study locations (Table 3). The average percentage of cracked injection sites per tree across all locations 11 mpt was 19%. The average percentage of injection sites per tree showing evidence of fluxing across all locations 11 mpt was 12%, although no active fluxing was observed. The average wound closure visual rating per tree was 1.4 ± 0.1 at the Chardon, OH, and Hillsborough, NJ, sites 11 mpt. At the Aurora, OH, site, wound closure was measured again after 22 mpt, and the average percentage of cracked injection sites per tree was 20%, the average number of fluxing sites per tree was 0.7%, and the average wound closure rating per tree was 2.7 ± 0.1.

Discussion

This research demonstrates that root flare injections with TBZ can provide beneficial therapy to beech trees suffering from BLD. There was significant visual improvement of the beech trees treated with TBZ at all 3 sites. Trees treated with TBZ root flare injections on 2022 August 7 and 2023 July 11 in Aurora and Chardon, OH, respectively, had a significant reduction in the percent canopy showing BLD symptoms in 2023 and/or 2024, suggesting that one treatment, even at the “low rate” (Aurora, OH), can substantially reduce symptoms (Figure 1A-B). At the Aurora, OH, site, this was further supported by observing no change in fine twig dieback progression in the TBZ-treated trees, while there was a trend of increased canopy fine twig dieback in nontreated control trees. While the disease severity (percent canopy with BLD) of all trees increased at the Hills-borough, NJ, site, trees injected with the “low rate” of TBZ had canopy density that was significantly greater than nontreated control trees (Figure 1C-E). This was due to a significant reduction in fine twig dieback in TBZ-treated trees and a significant increase in fine twig dieback in nontreated controls. Fine twig dieback symptom expression is presumed to be associated with bud abortion caused by Lcm (Vieira et al. 2023).

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Figure 1.

An illustrative representation of treatment effect of root flare injections with TBZ showing symptom reduction in beech trees compared to nontreated control trees. (A-B) Close up of leaf banding symptom in a nontreated control tree (A) and disease free canopy of a TBZ injected tree (B) 11 months post-treatment at the Chardon, OH, site where injections were applied at the “high rate”; (C-D) photograph taken up into the canopy illustrating differences in canopy density of a nontreated control tree (C) and TBZ injected tree (D) 11 months post-treatment at the Hillsborough, NJ, site where injections were applied at the “low rate”; (E) side-by-side photograph of a nontreated control tree (left) and TBZ injected tree (right) at the Hillsborough, NJ, site where injections were applied at the “low rate”; (F-G) close up of leaf banding symptom in a nontreated control tree (F) and disease free canopy of an TBZ injected tree (G) 22 months post-treatment at the Aurora, OH, site where injections were applied at the “low rate”.

We suspect the disparities in the data across the study locations may be due to the variable treatment timing. Reed et al. (2020) showed that Lcm disperses from symptomatic leaves to maturing buds as early as late July, peaking with the highest population of mobile nematodes being extracted from leaves in September. Lcm begin to interact and cause damage within developing buds as soon as they enter the bud sheaths in the late summer/early fall (Vieira et al. 2023). It is unknown if thiabendazole can move into beech bud tissue prior to dormancy, but these data suggest that it does not move in significant concentrations where the nematodes are developing.

Significant reductions in the percentage of canopies with BLD at the Aurora and Chardon, OH, sites may be due to treatment application occurring prior to the peak of Lcm dispersion, where treatments were applied on 2022 August 7 and 2023 July 11. Contrary to this, the percentage of canopy with BLD symptoms increased at the Hillsborough, NJ, site, where treatments were applied on 2023 August 30, possibly well into the peak dispersal period. This late treatment in NJ could have resulted in successful establishment of Lcm in the maturing buds prior to treatment deployment. This theory is supported by our dormant bud nematode counts at the site, where nematodes in buds from TBZ-treated trees (although significantly fewer than in the nontreated control buds) were still likely abundant enough to result in BLD symptoms. Despite this, the significant difference between treated and nontreated control trees at this site suggests that the treatment may have been successful in reducing the overall dispersing population of Lcm. This is supported by the significant reduction of fine twig dieback, or bud abortion, in the TBZ-treated trees compared to a significant increase in fine twig dieback in nontreated controls (Figure 1E and Table 1).

Beech leaf disease severity in the second growing season after root flare injections with TBZ was only evaluated at the Aurora, OH, site. Here, treated trees continued to show a significant reduction in percent canopy with BLD symptoms when compared to the nontreated control trees (Figure 1F-G). It is difficult to determine based on these data whether this is due to TBZ residues being translocated to new leaves and buds or just a reduction in local inoculum sources within the individual trees and surrounding forest. Stennes and French (1987) showed that American elms injected with the equivalent of 1.86-g TBZ/cm DBH did not have significant distribution into new growth tissues one full growing season following injections. At the Aurora, OH, site, we applied 1.03-g TBZ/cm DBH, which would suggest that this sustained reduction in BLD was due to inoculum dynamics and not pesticide residues. However, Stennes and French (1987) also found that TBZ was distributed into twigs of American elms 2 seasons post-treatment when injected at a rate of 5.59 g/cm DBH. At the Chardon, OH, site, TBZ was applied at 4.10 g/cm DBH; therefore, it is plausible that some residues may redistribute into new flushes the following season similarly in beech. As we continue to study these trees, it will be important to determine at what point BLD symptoms return to damaging levels at both the “low” and “high” rates of thiabendazole used in this study. This will help determine retreatment intervals and expectations. Further, although we did not quantify these specifically, there were differences in uptake time between the “high” and “low” rates of TBZ used here due to the total volume being 4× in the “high rate”. We anecdotally observed an estimated uptake time of 10 to 15 minutes for the “low rate” solution to move into the tree, while the “high rate” solution moved into the tree in 30 to 45 minutes.

While there was some damage associated with the injection sites (Figure 2), the frequency was quite low across all study locations. It is difficult to determine what negative physiological effects occur from external, visual observations, but no acute or chronic phytotoxicity in the canopy was observed at any of the study locations. Cracking and fluxing, indicative of wound damage, occurred at a rate of 19% and 12%, respectively, across all locations 11 mpt. Following 22 mpt, at the Aurora, OH, site, we observed similar levels of cracking at a frequency of 20%, but fluxing was trending lower. Furthermore, the injection sites were closing rapidly after 22 mpt with a consensus visual rating of 2.7, indicating that most injection sites were actively closing, with most fully closed. Given the low-pressure injection system and large dilution of material (1:20 to 1:40), this treatment can provide significant reduction in BLD symptoms and cause minimal long-term damage to the root flares. Given that the TBZ injections yielded more than one season worth of protection (i.e., Aurora, OH, site), we speculate that injections will not need to be made more often than 3 or more years or when damaging levels of BLD return.

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Figure 2.

An illustrative representation of wound closure symptoms and visual consensus rating. (A) An example of a cracked injection site 11 months post-treatment where the visual wound closure rating was scored a 1 (not closing); (B) an example of a fluxing injection site 11 months post-treatment where the visual wound closure rating was scored a 1 (not closing); (C) an example of a cracked injection site 22 months post-treatment where the visual wound closure rating was scored a 2 (actively closing); (D) an example of a fully closed injection site 22 months post-treatment where the visual wound closure rating was scored a 3 (fully closed).

Conclusions

This study demonstrates a novel and effective treatment of root flare injections with thiabendazole as found in Arbotect 20-S for suppression of beech leaf disease, caused by the foliar nematode Litylenchus crenatae mccannii. As the disease continues to spread throughout North America, management strategies like the one developed here are critical to keeping beech trees healthy. While this treatment can be deployed and effective in natural landscapes, injecting trees can be costly, and strategizing treatments on select individuals may be warranted, but treatments of whole forests will not likely be feasible. Continued work investigating the combination of silviculture practices such as reduction in stand density in conjunction with pesticide application, similar to what is recommended for management of hemlock woolly adelgid (Vose et al. 2013; Mayfield et al. 2023), may be a potential strategy in slowing the spread of this disease in a forest setting. TBZ injection represents an effective treatment option for large beech (> 25-cm DBH) where full coverage sprays with fluopyram are difficult, where trees are growing near bodies of water, or where pesticide drift may be of concern. This root flare injection recommendation should be implemented into a BLD integrated pest management program for beech in the United States where the use of thiabendazole for treatment of BLD is legal.

Conflicts of Interest

Cory McCurry and Mark Ware report being employed by Rainbow Ecoscience, a company that directly sells Thiabendazole (Arbotect 20-S) and provides education to tree care professionals on best practices for tree injection. The remaining authors reported no conflicts of interest.