First records of elm zigzag sawfly (Hymenoptera: Argidae) in the United States

Abstract

The elm zigzag sawfly (EZS), Aproceros leucopoda Takeuchi, was detected in the United States for the first time in Virginia in 2021. In 2022, it was confirmed in 4 additional states: Pennsylvania, North Carolina, Maryland, and New York. These are the first records of this species in the United States and demonstrate a rapid range expansion of an invasive defoliating pest. Native to Asia, EZS feeds exclusively on Ulmus spp. (elms; Ulmaceae). In the United States, feeding damage ranges in severity from minor to severe. Young instars create a zigzag-shaped pattern in leaves as they feed, while older larvae feed more completely on foliage, leaving only the midvein and sometimes thick lateral veins. This more complete feeding often obscures the signature zigzag defoliation of younger instars. Long-term health impacts to host trees are unknown, though aesthetic damage, growth loss, and branch dieback occur in Europe where it is also invasive. Little is known about management options for this pest, and continued expansion of this species’ range in the United States is expected.

elm, sawfly, defoliator, invasive species

The elm zigzag sawfly (Aproceros leucopoda Takeuchi (Hymenoptera: Argidae), EZS) is a sawfly native to East Asia that feeds exclusively on the foliage of Ulmus (elm; Ulmaceae) (Blank et al. 2014, Vétek et al. 2022). It was previously detected in central Europe in 2003 (Blank et al. 2010) and spread quickly, now ranging from England and France in the west, to Russia and Kazakhstan in the east (Ashikbayev et al. 2018, iNaturalist 2022). In Europe, it is considered a pest, sometimes severely defoliating its hosts (Blank et al. 2010, 2014, Martynoz and Nikulina 2017).

The first North American record of EZS occurred in Québec, Canada, in the summer of 2020 (Martel et al. 2021). This was recorded on iNaturalist, a social media network for biological observations, and later reported to Canadian officials (Martel et al. 2021). The following year, in 2021, EZS was confirmed in Virginia, representing the first detection in the United States and a significant range expansion. In 2022, it was detected in 4 additional states: Pennsylvania, North Carolina, Maryland, and New York. Adults are able to actively disperse 45–90 km per year (Blank et al. 2014), and their continued spread in the United States is anticipated.

In the United States, feeding damage ranges from minor to severe (Fig. 1). Young instars create a zigzag-shaped pattern in leaves as they feed from the leaf margin toward the midvein (Fig. 2). This distinct pattern is the basis of the common name used for this pest, EZS. Of note, Sterictiphora Billberg (Hymenoptera: Argidae) sawfly larvae also create this feeding pattern, but feed on Prunus spp. (cherry, plum, peach; Rosaceae) rather than elm (Eiseman 2015). Older EZS larvae feed more completely on foliage, leaving the midvein and thick lateral veins (Martynoz and Nikulina 2017) (Fig. 3). This feeding can remove significant amounts of foliage and often obscures the signature zigzag-shaped defoliation of younger instars. Elms are the exclusive host, though Vétek et al. (2022) recorded oviposition and larval feeding on Hemiptelea davidii (Hance) Plance (Ulmaceae), but all larvae died after a few days. As in Europe, EZS infestations in the United States occur on both native and cultivated elms (Blank et al. 2010) (Table 1).

Table 1.

Documented host species of EZS in the United States

Species	Common name	Location (state)
Ulmus americana	American elm	PA, NC, MD, NY
Ulmus alata	winged elm	NC
Ulmus parvifolia	Chinese elm	VA
Ulmus procera	English elm	VA
Ulmus pumila	Siberian elm	VA
Ulmus rubra	slippery elm	MD
Ulmus × ‘Cathedral’	Japanese × Siberian hybrid	VA

PA, Pennsylvania; NC, North Carolina; MD, Maryland; NY, New York; VA, Virginia.

Fig. 1.

Severe defoliation of Ulmus americana by EZS in Stokes County, NC. Photograph by K.L.F.O.

Fig. 2.

Young EZS larvae create distinct zigzag-patterned defoliation in leaves as they feed from the leaf margin toward the midvein. Photographs by M.A.B. (A) and E.D. (B).

Fig. 3.

As EZS larvae mature, leaves are consumed wholly, with the exception of the thick midvein and sometimes lateral veins (A). During high populations, this defoliation can lead to near-complete stripping of foliage on host trees (B). Photographs by K.L.F.O.

Generally, insect-caused defoliation events cause little harm to trees, but repeated severe defoliations can weaken or kill a host (Parry and McCullough 2004, Coyle et al. 2008). In Europe, trees severely defoliated by EZS produce a second flush of leaves later in the same season or the following year but often suffer branch dieback and reduced growth (Blank et al. 2010, Zandigiacomo et al. 2011). Pest status varies greatly between locations. Holuša et al. (2017) suggest it is a pest of solitary urban elms in the Czech Republic, but Artokhin et al. (2012) recorded damage across a 30,000 km² area in western Russia. Moreover, it is attacking an already-threatened tree genus, as beginning in the mid-1900s, Dutch elm disease (caused by scolytine-borne fungi of the genus Ophiostoma) caused widespread mortality of elms throughout North America and Europe (Santini and Faccoli 2015, Jernelöv 2017). In the United States, an estimated 77 million elms were killed between 1930 and 1980 (USDA 2006) and worldwide, potentially 400 million elms were killed over a period of 100 yr (Jernelöv 2017). Defoliation by EZS could further weaken Dutch elm disease-infected trees or, at the very least, present an additional threat to remaining elms (Blank et al. 2010). While EZS appears to primarily cause aesthetic issues, the potential for long-term tree health impacts in its newly expanded range is uncertain and should be investigated.

EZS larvae are small, reaching 10–11 mm long at maturity. Neonates are grayish-white and older larvae are light green with a black band on their head. T-shaped brown or black markings above the second and third pair of thoracic legs are diagnostic of the species (Fig. 4). Larvae feed for 10–18 days and progress through 6 instars (Blank et al. 2010, Martynoz and Nikulina 2017). Pupation occurs within seasonally-dimorphic cocoons, which are either loosely spun and net-like or solid-walled with silken strands on the surface. Loosely spun cocoons are most often attached to the undersides of leaves and occasionally on twigs or the ground (Fig. 5A and B). Pupation occurs within 2–3 days of cocoon formation and adult emergence occurs within 4–7 days of pupation (Blank et al. 2010). Solid-walled cocoons align with the overwintering stage and primarily occur in the leaf litter or the soil (Wu 2006, Blank et al. 2010). Overwintering solid-walled cocoons are produced throughout the season and not restricted to late-season generations, suggesting an adaptation for overwintering survival in the event of early onset winter (Blank et al. 2010, Martel et al. 2021). In heavy infestations in North Carolina, cocoons were also found attached to inanimate objects, such as fence posts (Fig. 5C), suggesting a possible mechanism of long-range dispersal should they become attached to vehicles or other objects transported long distances. Adults are small sawflies, reaching 7–8 mm in length; they are shiny black with pale legs and smoky-brown wings (Fig. 6). They reproduce by thelytoky, a type of parthenogenesis in which females lay unfertilized eggs that produce only females; no males have ever been recorded in this species (Blank et al. 2010). Females do not need to feed to lay eggs and can begin oviposition immediately following eclosion. Females lay 7–49 eggs singly along leaf margins; eggs eclose 4–8 days later (Blank et al. 2010, Martynoz and Nikulina 2017) (Fig. 6B).

Fig. 4.

Mature EZS larvae are light green with a black band on their head and T-shaped markings above the second and third pair of legs. Photograph by M.A.B.

Fig. 5.

EZS cocoons are primarily found on leaves (A, B) or within leaf litter or soil (overwintering pupae), but they may also be attached to man-made objects, like the fencepost shown here (C). Photographs by E.D. (A), M.A.B. (B), and K.L.F.O. (C).

Fig. 6.

Adult EZSs are shiny black with smoky wings (A, B). They reproduce by thelytoky, laying eggs (C) along leaf margins which leave an egg scar (circled) after eclosion (B). Photographs by M.A.B. (A, C) and E.D. (B).

Voltinism of this pest varies greatly. In Virginia, 2 generations were observed in 2021 and 1 generation in 2022. Lab-reared EZS have up to 7 generations per year, but field observations in Europe and Russia suggest that 2–4 generations per year are typical (Blank et al. 2010, Papp et al. 2018). Up to 6 generations per year have been documented in the Netherlands (Mol and Vonk 2015 in Martynoz and Nikulina 2017). Both parthenogenetic reproduction and multivoltine capacity favor rapid population growth. As EZS continues to spread into warmer climates, development time and voltinism are expected to increase, suggesting increased defoliation severity. Additional investigations should be conducted in areas with newly established populations to determine voltinism, population increase potential, and resulting defoliation.

There is little information in the literature that focuses on the successful management of this defoliating pest. In Hungary, control was achieved on the first generation of EZS by spraying 0.04% Decis 2.5 EC (deltamethrin) and 0.075% Nomolt (teflubenzurin) (Blank et al. 2010). In Romania, field applications of the entomopathogenic fungus, Beauvaria bassiana (Bals.) Vuill., resulted in dose-dependent reduction of EZS populations (Fătu et al. 2020). Bioassays by Del Pozo-Valdivia et al. (2022) in Virginia demonstrated 83% EZS mortality with foliar applications of dinotefuran. General-purpose insecticides labeled for use on trees and shrubs will likely work against EZS larvae, but remain untested. Management effective against other sawflies, such as the application of insecticidal soaps or horticultural oils when larvae are small, may also be effective. Lastly, physical removal through hand-picking or spraying a strong stream of water may dislodge larvae. Additional work investigating effective management tactics for EZS on landscape trees is warranted.

Several associated species have been documented during EZS infestations. In Pennsylvania, North Carolina, and Maryland, Monocesta coryli (Say) (larger elm leaf beetle; Coleoptera: Chrysomelidae) was observed on trees simultaneously infested with EZS. In Virginia, defoliation by Orchestes steppensis (Coleoptera: Curculionidae) commonly occurred alongside EZS. In Pennsylvania and North Carolina, species of Lochmaeus (Lepidoptera: Notodontidae) were also observed feeding on foliage of EZS-infested trees. In addition, several assassin bugs (Zelus sp.; Hemiptera: Reduviidae) were observed in North Carolina and also reported to be predatory on EZS in Canada (V. Martel, personal communication, 20 September 2022). Rhytisma sp. (Rhytismatales: Rhytismataceae), a plant pathogen causing tar spot, was observed on infested trees in Pennsylvania.

This article documents the initial detections of the invasive EZS in the United States in 2021 and 2022 (Fig. 7).

Fig. 7.

Confirmed and unconfirmed EZS in the United States, 2021–2022. Map created November 2022 by K.L.F.O.

First Record of EZS in Virginia (May 2021)

EZS was first detected in Virginia on 31 May 2021, near Winchester in Frederick County. A Virginia Department of Agriculture and Consumer Services (VDACS) inspector observed and photographed unusual defoliation damage to leaves of Ulmus pumila L. (Siberian elm) on 8 May 2020, but did not find the damaging insect. When notified to watch for EZS a year later, the VDACS inspector returned to the site and collected larvae from fresh damage. Larval specimens submitted to the Insect Identification Laboratory at Virginia Tech were confirmed as EZS by the US Department of Agriculture, Animal and Plant Health Inspection Services, Plant Protection and Quarantine (USDA APHIS PPQ). Also in 2021, EZS was found and confirmed in Clarke, Warren, Shenandoah, Rockingham, Page, Augusta, Albemarle, and Montgomery Counties. In 2022, it was detected and confirmed in Roanoke and Giles Counties. Larvae have been found feeding on Ulmus parvifolia Jacq. (Chinese elm), U. pumila, Ulmus ‘Cathedral’ (U. parvifolia × U. pumila hybrid), and Ulmus procera Salisb. (English elm). The most common host for detection was U. pumila upon which complete defoliation was observed in Frederick and Rockbridge Counties in July 2021.

First Record of EZS in Pennsylvania (June 2022)

An unconfirmed detection of EZS feeding damage on a private property in Lehigh County, PA, was reported by a private landowner in 2021. Investigation by Pennsylvania Department of Agriculture (PDA) staff documented the feeding damage, but the damaging insect was not found. Pupae were collected and more feeding damage was observed in August and September in the same area, though the specimens were too badly desiccated to confirm identification. The pupal cases that were collected matched later positive findings and supported its presence in Lehigh County. In 2022, larvae and pupae were collected June through August from 5 Pennsylvania counties: Bucks, Montgomery, Northampton, Schuylkill, and Berks. All collections, except the Montgomery County record, were taken from nursery stock; additional surveys have not been carried out to determine its establishment in the environment. All collections were from Ulmus americana L. (American elm), U. americana ‘Princeton’ variety, or unidentified Ulmus sp. Two collections were successfully reared, and adults were collected in the laboratory. Specimens were identified by PDA’s Entomology Program and confirmed by USDA APHIS PPQ.

First Record of EZS in North Carolina (August 2022)

The first report of EZS in North Carolina occurred in August 2022 near the Surry and Stokes County line. A homeowner observed severe defoliation of several large U. americana yard trees and reported it to the North Carolina Forest Service (NCFS) local county office. The Surry County assistant county ranger visited the site, observed the zigzag-shaped feeding damage, and identified the damage to be associated with EZS. Additional NCFS county staff, NCFS forest health staff, and a North Carolina State University (NCSU) Extension specialist visited the site on 16 August 2022. Larvae and pupae were collected and feeding damage observed; near-complete defoliation of U. americana was observed. Larval specimens were submitted to the NCSU Plant Disease and Insect Clinic where they were identified by M.A.B. and later submitted and confirmed by USDA APHIS PPQ. Additional detections by the NCFS occurred in the local area in the following weeks, all hosts being either U. americana or Ulmus alata Michx. (winged elm).

First Record of EZS in Maryland (August 2022)

A naturalist reported the presence of EZS in Garrett County, MD, at the Savage River Reservoir on 1 August 2022. A follow-up survey was completed on 24 August by the Forest Pest Management Section of the Maryland Department of Agriculture (MDA) where 6 larvae and 1 pupa were found as well as zigzag-shaped feeding damage and net-like cocoons. Of the 6 larvae, 5 were found on U. americana and 1 was found on Ulmus rubra Muhl. (slippery elm). Defoliation was more common in U. americana than in U. rubra, and defoliation at the site was minor, affecting less than 5% of the trees. Specimens were confirmed by the MDA Entomologist and USDA APHIS PPQ. Additional nonconfirmed reports of EZS have been recorded in Baltimore and Anne Arundel Counties where zigzag defoliation was found, but the damaging insect was not observed.

First Record of EZS in New York (August 2022)

Feeding damage associated with EZS was first observed at 3 State-owned forests in St. Lawrence County, NY, on 10 August 2022, by NYS Department of Environmental Conservation (DEC) staff. Observations were the result of targeted surveys in elm stands along the New York–Canada border near the provinces of Ontario and Québec, where EZS is established. A follow-up survey was conducted at Brasher State Forest in northwestern St. Lawrence County on 25 August 2022 to determine the extent of the damage and to collect a specimen for official confirmation. Multiple larvae and pupae were collected from a mixed stand dominated by U. americana and U. rubra. Specimens were identified by the DEC’s Forest Health Diagnostic Lab and confirmed by USDA APHIS PPQ on 8 September 2022. Less than 10% of trees surveyed showed signs of feeding damage, and visible defoliation was restricted to 1–3 leaves per tree. Initial observations indicated that EZS populations were at low levels and not yet causing significant defoliation. However, more extensive surveys are needed to assess the current distribution. The presence of EZS in northern New York poses an imminent threat to a region that contains the healthiest and most abundant elm in the state. U. americana, U. rubra, and U. thomasii exist in scattered, isolated stands that experience less frequent infection cycles of Dutch elm disease and often grow to considerable size.

Discussion

These records represent the first reports of EZS in the United States. While a relatively new invasion, the rapid succession of these detections across a broad geographic range along with EZS’s high reproductive capabilities suggest it will likely continue to spread rapidly. Furthermore, formal surveys have not been conducted in many states, and given the cryptic nature of this pest at low population densities, may mean that it has already invaded many areas undetected. While EZS damage is presumed to present mostly an aesthetic issue based on observations in Europe, it has already invaded areas in the United States at more southern latitudes than regions where those observations occurred. Generally, warmer climates present the opportunity of increased insect development rates and, in the case of multivoltine insects, the potential to rapidly build to damaging population levels in a single growing season. Investigations into the biology and management of EZS, specifically to assess its damaging potential in warmer climates and to identify effective treatment methods in its newly expanded range, are warranted.

Acknowledgments

In Virginia, we thank Heather Huntington for initial detection and Mark Sutphin for initial surveys. In Pennsylvania, we thank Suzanne Wainwright-Evans for her contributions. In North Carolina, we thank Elizabeth Edwards, Brian Heath, Chris Cooper, Jonathan Young, Robert Jefferson, and Janet Pearson (North Carolina Forest Service) for initial response and continued surveys. In Maryland, we thank Patrick Simons, Gaye Williams, and Joshua Emm for the initial find, surveys, and identification. In New York, we thank Jordan Stransky, Kelsey McLaughlin, and Erica Culbert for their field survey and lab assistance.

Author Contributions

Kelly Oten (Conceptualization-Lead, Data curation-Lead, Resources-Equal, Writing – original draft-Lead, Writing – review & editing-Lead), Eric Day (Data curation-Equal, Writing – original draft-Equal, Writing – review & editing-Equal), Theresa Dellinger (Data curation-Equal, Writing – original draft-Equal, Writing – review & editing-Equal), Heather Harmon Disque (Data curation-Equal, Writing – original draft-Equal, Writing – review & editing-Equal), Lawrence Barringer (Data curation-Equal, Writing – original draft-Equal, Writing – review & editing-Equal), Jessica Cancelliere (Data curation-Equal, Writing – original draft-Equal, Writing – review & editing-Equal), Liam Somers (Data curation-Equal, Writing – review & editing-Supporting), Matt Bertone (Visualization-Equal, Writing – original draft-Equal, Writing – review & editing-Equal)