Aproceros leucopoda
(elm zigzag sawfly)

Pictures

Picture	Title	Caption	Copyright
Title Larval damage Caption Aproceros leucopoda (zigzag sawfly); advanced stage of larval damage to an elm leaf (Ulmus spp), with larva present. Copyright ©Gyorgy Csoka/Hungary Forest Research Institute/Bugwood.org - CC BY 3.0 US	Larval damage	Aproceros leucopoda (zigzag sawfly); advanced stage of larval damage to an elm leaf (Ulmus spp), with larva present.	©Gyorgy Csoka/Hungary Forest Research Institute/Bugwood.org - CC BY 3.0 US
Title Larva feeding Caption Aproceros leucopoda (zigzag sawfly); larva feeding on an elm leaf (Ulmus spp). Copyright ©Gyorgy Csoka/Hungary Forest Research Institute/Bugwood.org - CC BY 3.0 US	Larva feeding	Aproceros leucopoda (zigzag sawfly); larva feeding on an elm leaf (Ulmus spp).	©Gyorgy Csoka/Hungary Forest Research Institute/Bugwood.org - CC BY 3.0 US
Title Larval damage Caption Aproceros leucopoda (zigzag sawfly); characteristic 'serpentine' larval damage on elm leaf (Ulmus spp). Copyright ©Gyorgy Csoka/Hungary Forest Research Institute/Bugwood.org - CC BY 3.0 US	Larval damage	Aproceros leucopoda (zigzag sawfly); characteristic 'serpentine' larval damage on elm leaf (Ulmus spp).	©Gyorgy Csoka/Hungary Forest Research Institute/Bugwood.org - CC BY 3.0 US
Title Adult sawfly Caption Aproceros leucopoda (zigzag sawfly); adult sawfly, at rest on an elm leaf (Ulmus spp). Copyright ©Gyorgy Csoka/Hungary Forest Research Institute/Bugwood.org - CC BY 3.0 US	Adult sawfly	Aproceros leucopoda (zigzag sawfly); adult sawfly, at rest on an elm leaf (Ulmus spp).	©Gyorgy Csoka/Hungary Forest Research Institute/Bugwood.org - CC BY 3.0 US
Title Adult sawfly Caption Aproceros leucopoda (zigzag sawfly); adult sawfly, at rest on an elm leaf (Ulmus spp). Copyright ©Gyorgy Csoka/Hungary Forest Research Institute/Bugwood.org - CC BY 3.0 US	Adult sawfly	Aproceros leucopoda (zigzag sawfly); adult sawfly, at rest on an elm leaf (Ulmus spp).	©Gyorgy Csoka/Hungary Forest Research Institute/Bugwood.org - CC BY 3.0 US
Title Pupal case Caption Aproceros leucopoda (zigzag sawfly); pupal case. Reticulate cocoon of the summer generation, attached to the underside of a leaf. Southern Hungary. May 2012. Copyright ©Siga/via wikipedia - CC BY-SA 3.0	Pupal case	Aproceros leucopoda (zigzag sawfly); pupal case. Reticulate cocoon of the summer generation, attached to the underside of a leaf. Southern Hungary. May 2012.	©Siga/via wikipedia - CC BY-SA 3.0

Identity

Preferred Scientific Name

• Aproceros leucopoda Takeuchi

Preferred Common Name

• elm zigzag sawfly

International Common Names

• English: East Asian sawfly; elm sawfly; zigzag sawfly
• Russian: восточноазиатского ильмового пилильщика

Local Common Names

• Croatia: Brijestova osa listarica
• Germany: Japanische Ulmenblattwespe; Zickzack-Blattwespe
• Hungary: Kanyargós szillevéldarázs
• Netherlands: Iepenzigzagbladwesp
• Romania: Viespea neagra a ulmului

Summary of Invasiveness

Elm zigzag sawfly is considered a minor pest within its native range in East Asia, but since first arriving in Hungary and Poland in 2003 the sawfly has spread rapidly through Europe and is continuing to expand its range. Severe localized defoliation has been recorded by the species throughout Europe on elms in a variety of situations. Most elm species are utilised as host plants, which combined with it being both parthenogenic and multivoltine means populations can build up rapidly in suitable areas. No specific predators are known, and whilst parasitoids have been described on the species in Europe no studies have investigated their efficacy at controlling elm zigzag sawfly. This species was removed from the EPPO Alert List in 2015 following no international action on the species being requested by the EPPO member countries.

Taxonomic Tree

• Domain: Eukaryota
•     Kingdom: Metazoa
•         Phylum: Arthropoda
•             Subphylum: Uniramia
•                 Class: Insecta
•                     Order: Hymenoptera
•                         Family: Argidae
•                             Genus: Aproceros
•                                 Species: Aproceros leucopoda

Notes on Taxonomy and Nomenclature

No taxonomic changes to Aproceros leucopoda have been made since it was first described by Takeuchi in 1939 (Taeger and Blank, 2011).

Description

Adults are small sawflies, almost entirely dark brown other than pale, yellow to white legs and palps. The summer and winter generations may be distinguished by the length of the genae (Blank et al., 2010).

Larvae are typical sawflies with prolegs and a globular head capsule (Blank et al., 2010), but can be distinguished from other sawflies by the possession of a pair of appendages on the supra-anal lobe, T-shaped brown marks on thoracic legs 2 and 3, and a transversal lateral dark stripe between the stemmata. Young larvae usually produce the ‘zigzag’ feeding damage which aids identification, though older larvae often feed over the traces and obscure them.

Pupae are usually found on the underside of leaves within a thin-walled lattice structure, which is replaced by a solid-walled structure to protect the overwintering generation in the final generation before winter. 

Distribution

Though the native distribution of elm zigzag sawfly is believed to include Japan (from where the species was first described), far eastern Russia, eastern China and the Korean peninsula (Wu and Xin, 2006; Sundukov, 2009), the true original distribution of the species is likely never to be known thanks to more recent population spreads in both China and Russia (Zhelokhovtsev and Zinoviev, 1995; Jiangfeng, 2011; Yu et al., 2011). In addition, there appear to be no primary references to the Korean population other than Sundukov (2009) and questions have been raised about the accuracy of the record from far eastern Russia (Blank et al., 2010). Significant defoliation caused by the species was not described until 1995 in Japan (Blank et al., 2010) and field observations indicate that the species can be difficult to find at very low densities, even given the distinctive larval feeding trace (Blake pers. obvs.). As such the known distribution of the species is likely to be an underestimate of its true distribution; adults are strong fliers (Wu and Xin, 2006), which enables the front of an invading population to spread at 45-90 km a year (Blank et al., 2014).

Distribution Table

The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

History of Introduction and Spread

Elm zigzag sawfly was first recorded in Europe in 2003 in both Hungary and Poland. Since then it has spread rapidly to new countries, most recently Switzerland and the UK (EPPO, 2018; Forest Research, 2018). It is unknown how the species arrived from eastern Asia into Europe, though elm plants transported for horticulture or forestry have been implicated (Blank et al., 2010). Associations between large roads and the spread of A. leucopoda have been noted, potentially both aiding movements within country (Schrader and Schröder, 2013) and allowing it to become established in new countries (Zandigiacomo et al., 2011; Blank et al., 2014). How the species spread into the British Isles is unknown (Forest Research, 2018); A. leucopoda was thought to be unable to cross the Channel (minimum 30 km width) by self-dispersal (Blank et al., 2014), so there remains the possibility that it acted as a hitchhiker (Blank et al., 2014). As such, finding the species in Scandinavia may be somewhat more likely than originally considered by Blank et al. (2014).

Risk of Introduction

A. leucopoda is highly likely to continue to spread in all directions via self-dispersal from its current distribution in Europe (Blank et al., 2010; Tuffen, 2016), as well as continuing to spread through China and eastern Russia (Wu and Xin, 2006; Sundukov, 2009). Though human-assisted movements from plants for planting have been hypothesised (Schrader and Schröder, 2013), this has not yet been observed, and the distinctive damage to the leaves of young plants may lead to them being rejected for sale (Tuffen, 2016). However, eggs laid in the leaves are cryptic, and could easily be missed; though as eggs only take 4-8 days to hatch the turnaround for nursery plants would have to be extremely fast (Blank et al., 2010). The wintering cocoons are similarly cryptic, and may be easily missed if attached to leaf litter transported alongside the tree. As elms (Ulmus) are usually moved whilst dormant (Tuffen, 2016) this may be a more likely pathway for areas which import elm trees. Given the parthenogenic nature of the species it would take very few individuals being transported to a suitable location for establishment to begin. A. leucopoda was placed on the EPPO alert list in 2011, but was removed in 2015 following no international action on the species being requested by the EPPO member countries.

Habitat

A. leucopoda appears to feed on elms (Ulmus spp.) in a variety of habitats, including arboretums and botanical gardens, roadside trees, urban plantings, and in natural woodlands (Blank et al., 2014; Vétek et al., 2017; Zúbrik et al., 2017; Forest Research, 2018). The species may decline in abundance with increasing altitude (Zúbrik et al., 2017), and it may show a preference for solitary, open grown elms rather than those in forest situations (Holuša et al., 2017), causing higher levels of defoliation on trees in such situations (Blank et al., 2010; Zandigiacomo et al., 2011; Mol and Vonk, 2015).

Habitat List

Hosts/Species Affected

Reviews of elms (Ulmus spp.) in botanical gardens have revealed a number of species attacked by A. leucopoda which are only rarely planted through Europe, plus others which have not been attacked (Blank et al., 2014; Vétek et al., 2017). However, some of these records are hampered by small sample sizes (n=1 in some cases); subsequent work may find that such species are eventually attacked by A. leucopoda. Nevertheless, localized host preferences have been detected, such as an apparent aversion to Ulmus laevis in Germany (Blank et al., 2014) and in Poland (Borowski, 2018), despite this being a host tree elsewhere. Zúbrik et al. (2017) found U. laevis to be fed upon by A. leucopoda but recorded no evidence of the species on U. glabra. This may be due to climatic differences between the regions in which U. glabra grows within Slovakia, as U. glabra is an important host elsewhere (Blank et al., 2010; Csóka et al., 2012; Vétek et al., 2017). Elms can often be hard to identify to species level, which along with the genus’s complicated taxonomic history means that there may be occasional issues with host identification and differences in the names reported.

Successful development by A. leucopoda on non-Ulmus species has not been reported. Papp (2018) showed that whilst females will lay eggs on Zelkova serrata and Hemiptelea davidii (both Ulmaceae) larvae appeared not to complete development. There is thus no evidence that either species is a true host for A. leucopoda.

Significant wild hosts include Ulmus 'Lobel', Ulmus 'New Horizon', Ulmus 'Rebona', Ulmus 'Regal' and Ulmus 'Resista'.

Host Plants and Other Plants Affected

Growth Stages

Symptoms

Looking for the 'zigzag' feeding pattern of young A. leucopoda larvae on elm trees is the most used method for detecting the species. If found, larvae can then be keyed through using Blank et al. (2010). Older larvae often eat over the original feeding trace, obscuring it (Vétek et al., 2017). The lattice-like pupal cocoons are also distinctive, usually being found on the underside of leaves. Heavy infestations may lead to extreme defoliation, but the 'zigzags' should still be visible, along with pupal cocoons.

List of Symptoms/Signs

Biology and Ecology

Genetics

As a species which practices thelytokous parthenogenesis, A. leucopoda isn’t known to hybridize with other species. No widespread work on the genetic variation of the species has been published.

Reproductive biology

A. leucopoda is an extremely fast developer, with full generations taking 24-29 days to complete (Blank et al., 2010) though this is variable with respect to temperature (Papp et al., 2018). Adults lay approximately 10-40 eggs, though occasionally they may lay up to 60 (Blank et al., 2010; Papp, 2018).

Physiology and phenology

Few studies on A. leucopoda in its native range have been completed, as such most of the data on its survival strategy have only been collected for the non-native population in Europe. Even when reared at stable temperatures the life-cycle speed of A. leucopoda remains variable, though the thermal minimum for development appears to be just above 7°C (Papp et al., 2018). As temperatures begin to fall in autumn, larvae build a strong-walled lattice cocoon in which they overwinter in the leaf litter under the host tree. The species completes four generations in a year in Japan (Blank et al., 2010) but completes between four and six generations a year in Europe (Zandigiacomo et al., 2011; Mol and Vonk, 2015; Papp, 2018). However, the species exhibits polymodality, and thus individual larvae may be difficult to assign to a particular generation (Holuša et al., 2017).

Longevity

Adult lifespan varies between 3 and 11 days (Papp, 2018). Four to 8 days are spent as an egg, 15-18 days are spent as a larva, and the adult emerges from the cocoon 4 to 7 days after this has first been spun (Blank et al., 2010).

Activity patterns

No daily rhythms are known. Active adults have been observed in the day time (Blake, pers. obvs.). Larvae construct overwintering cocoons in autumn, presumably as a response to declining light levels or temperature. There is a possibility that these cocoons may be used to undergo extended diapause for a number of years as utilized by other related sawflies (Holuša et al., 2017).

Nutrition

A. leucopoda is only known to feed on the leaves of elm (Ulmus spp.) trees.

Environmental requirements

A. leucopoda has been recorded from a wide variety of altitudes, generally <400 m a.s.l., though records exists up to and just over 700 m a.s.l. (Holuša et al., 2017; Zúbrik et al., 2017). Research indicates that heavy infestations are observed only at lower altitudes in Slovenia, below 150 m a.s.l. (Zúbrik et al., 2017). Little data on other environmental factors are known. There may be a preference for solitary, open grown elms rather than those in forest situations (Holuša et al., 2017),

Climate

Latitude/Altitude Ranges

Air Temperature

Natural enemies

Means of Movement and Dispersal

Accidental introduction: Blank et al. (2014) estimated a spread of 45-90 km/yr for this species through a combination of human-mediated jump dispersal and natural self-dispersal, and estimated that a gap of 360-610 km had been crossed by the species due to human-mediated jump dispersal. Additional accidental associations with rail, air and canal traffic have been posited (Blank et al., 2010).

Natural dispersal: no data on true natural (self-propelled, wind, etc.) dispersal has been collected for A. leucopoda. 

Pathway Causes

Pathway Vectors

Plant Trade

Wood Packaging

Impact Summary

Economic Impact

No significant impacts are known, though dense populations of A. leucopoda have caused enough damage to the leaf area of very small elm trees to be a factor affecting growth. Heavy defoliation has led to branch dieback in rare circumstances (Blank et al., 2010). Long-term, repeated defoliations which eventually kill the tree have not been recorded.

Environmental Impact

As a fecund, mobile, defoliating species tolerant of a wide range of environments where its host plant grows, A. leucopoda represents a highly competitive elm (Ulmus spp.) specialist. Though no studies have analysed the effect of Aproceros browsing on elm growth and competition with other elm browsers, it is possible that larvae can have negative, if usually minor, effects on tree health and the growth of native elm browsers. As only branch dieback, and not tree death, has been reported as the most extreme impact of A. leucopoda on elm, impacts on habitats and biodiversity are only likely to be minor. No studies have yet been conducted looking into the impact of A. leucopoda competition on elm herbivores of conservation concern.

Threatened Species

Social Impact

Reduction of aesthetic value could occur in instances of heavy defoliation on trees planted for amenity value (Tuffen, 2016).

Risk and Impact Factors

• Proved invasive outside its native range
• Tolerant of shade
• Highly mobile locally
• Benefits from human association (i.e. it is a human commensal)
• Fast growing
• Has high reproductive potential
• Has propagules that can remain viable for more than one year
• Reproduces asexually

• Host damage
• Reduced amenity values

• Herbivory/grazing/browsing

• Highly likely to be transported internationally accidentally

Detection and Inspection

A. leucopoda is best detected as a feeding larva on leaves, the ‘zigzag’ browsing traces being easily recognisable as this is the only species known to produce such feeding damage on elm. Leaf-miners on elm feed within the leaf and may be mistaken for A. leucopoda, particularly the species producing more chaotic mines (e.g. Stigmella spp.), though these do not chew through the entire leaf. Once found, mature larvae can be swiftly identified by looking for T-shaped marks on thoracic legs 2 and 3 and a transversal lateral dark stripe between the stemmata. Adults are harder to find, though if captured they can be keyed out through Blank et al. (2010). The lattice-like pupal cocoons are also distinctive and can usually be found on the underside of leaves. Eggs and overwintering cocoons, particularly if the latter have fallen to the ground, are more difficult to detect. Adults are known to fly to yellow sticky panel traps often used for monitoring other sawflies, which should be a suitable method for detecting adults (Vétek et al., 2016).

Similarities to Other Species/Conditions

Blank et al. (2010) provide a key to separate adults of A. leucopoda from other West Palaearctic Hymenoptera, noting distinct differences between the wings of A. leucopoda and other Argidae, including an absent anal cell on the hind wings and a distally opened radial cell on both wings. The black to dark-brown body and head help distinguish it from Pseudoprosthema. Sawfly larvae feeding on elm (Ulmus) may be identified as A. leucopoda by the T-shaped brown marks above thoracic legs 2 and 3; such larvae are usually found feeding within a zigzag-shaped feeding trace (though sometimes this may be obscured). Other sawflies on elm (such as Arge captiva) do not feed in a zigzag manner, nor do they possess the distinctive markings (Blank et al., 2014).

The zigzag feeding habit has only been described for A. leucopoda and some Sterictiphora spp. (Sterictiphorinae) (Vétek et al., 2017), though these latter species have only been recorded on Prunus and Amelanchier (Eiseman, 2015). Aproceros and Sterictiphora can be distinguished as larvae based on the host plant and possession of the T-shaped markings in Aproceros (Blank et al., 2014). Aproceros also cycles through multiple generations a year and builds non-overwintering cocoons on foliage rather than on the ground (Eiseman, 2015).

Prevention and Control

Prevention

SPS measures (quarantine, certification, prohibition)

Preventing A. leucopoda from becoming established in additional suitable areas of Europe, China and eastern Russia is near impossible (Wu and Xin, 2006; Sundukov, 2009; Blank et al., 2010; Tuffen, 2016), though phytosanitary measures on movements of Ulmus, in particular moving plants in the dormant period and without leaf litter, should help slow human-assisted movements. The species is no longer on the EPPO alert list as of 2015. Preventing the species establishing itself in other suitable areas, such as the USA, will necessitate phytosanitary measures being placed on Ulmus exported from regions where A. leucopoda is present.

Early warning systems

These are not known to have been trialled for monitoring A. leucopoda.

Rapid response

No attempt has been made to eradicate A. leucopoda after establishment. Though pesticides are effective against the larvae (Blank et al., 2010), the adults can disperse effectively across large distances and are difficult to find at low density (Forest Research, 2018). Eradication with pesticides may struggle to effectively control the overwintering population thanks to a layer of leaf litter protecting the pupal cocoons.

Public awareness

Public outreach attempts have proven extremely successful in rapidly determining the extent of a recently established population of A. leucopoda (Forest Research, 2018).

Eradication

Never attempted and unlikely to be successful due to the dispersal ability of the adults as well as the cryptic nature of the larvae at low densities. Follow-up monitoring to recent establishments has revealed populations can be across a much larger range than initially expected (Forest Research, 2018).

Containment/zoning

Unlikely to be effective due to adult dispersal ability.

Control

Cultural control and sanitary measures

Only likely to be effective in preventing the establishment of A. leucopoda across a major sea barrier. Imports of Ulmus to uninhabited areas should be subject to robust phytosanitary measures.

Physical/mechanical control

Physical removal of larvae on small trees/shrubs could be effective at reducing feeding pressure in garden situations, but would not contribute to the control of the species at even a local level if there are untreated hosts nearby.

Movement control

Only likely to be effective in preventing the establishment of A. leucopoda across a major sea barrier. Imports of Ulmus to uninhabited areas should be subject to robust phytosanitary measures. Reducing human-assisted movement across land should be effective at slowing the spread of the sawfly across the Palearctic.

Biological control

Though predators and parasitoids of A. leucopoda are known, they have not yet been demonstrated to cause a significant drop in the sawfly’s population density. Viral diseases of pest sawflies are well understood and cause significant population crashes in nature (Bird, 1953), though these are not known from A. leucopoda.

Chemical control

Effective against larvae in discrete populations (Blank et al., 2010), but unlikely to be effective on larger populations.

Host resistance (incl. vaccination)

Little host resistance against A. leucopoda is known in Ulmus. Multi-species studies have found little difference in the susceptibility of different Ulmus spp. to A. leucopoda (Véteket al., 2017). Though Ulmus laevis isn’t utilised as a host in Germany (Blank et al., 2014) and Poland (Borowski, 2018), even when A. leucopoda is present in the local environment, it is a suitable host elsewhere in Europe.

IPM

Currently unstudied.

Monitoring and surveillance (incl. remote sensing)

Extremely effective when combined with a public awareness campaign at establishing the population extent of A. leucopoda in new establishments (Forest Research, 2018), but this is unlikely to be effective at detecting the initial stages of establishment when the species could be locally eradicated. Within-country surveillance has been effective at not only discovering new localities for A. leucopoda (Schrader and Schröder, 2013; Blank et al., 2014), but has also revealed new host records and offered insights into host preferences (Véteket al., 2017; Zúbrik et al., 2017).

Mitigation

Likely to only be effective where the large amount of repeated physical removal of larvae on individual trees is worth the substantial effort, such as on a small number of small amenity trees in a garden or park. Completely unsuitable for the control of A. leucopoda once established in the wider environment.

Gaps in Knowledge/Research Needs

More research on A. leucopoda would be welcome in the following areas:

• New records of predators and parasitoids of the species, which could eventually be followed up with studies on their effectiveness at managing A. leucopoda populations.
• More information on the susceptibility of different Ulmus species is needed, particularly why U. laevis is apparently not utilised as a host in some areas, and yet is suitable elsewhere.
• Impacts of competition from A. leucopoda on other Ulmus-browsing herbivores, especially those of conservation concern.
• Long term datasets on herbivory pressure from A. leucopoda and the impact on elm growth and dieback.

References

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Blank, S. M., Köhler, T., Pfannenstill, T., Neuenfeldt, N., Zimmer, B., Jansen, E., Taeger, A., Liston, A. D., 2014. Zig-zagging across Central Europe: recent range extension, dispersal speed and larval hosts of Aproceros leucopoda (Hymenoptera, Argidae) in Germany. Journal of Hymenoptera Research, 41, 57.

Borowski, J., 2018. Two new localities of the zigzag elm sawfly Aproceros leucopoda Takeuchi, 1939 (Hymenoptera, Symphyta: Argidae) in Poland. World Scientific News, 92(2), 367-371.

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Eiseman, C. S., 2015. On the distinctive feeding pattern of Sterictiphora Billberg (Hymenoptera: Argidae) sawfly larvae. Proceedings of the Entomological Society of Washington, 117(1), 65-67. http://www.bioone.org/doi/full/10.4289/0013-8797.117.1.65

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Holuša, J., Stodulková, P., Macek, J., 2017. Observations on the occurrence and phenology of the invasive elm defoliator Aproceros leucopoda (Hymenoptera: Argidae) in the Czech Republic. Urban Forestry & Urban Greening, 21, 29-33.

Höelling, D., 2018. Aproceros leucopoda Takeuchi, 1939 – Erstbeobachtung der Zickzack-Ulmenblattwespe in der Schweiz (Hymenoptera: Argidae). Entomo Helvetica 11:149-152. https://sciencesnaturelles.ch/uuid/b15a3097-c732-5f1c-8c5a-77d040c31171?r=20180524162801_1529355682_032ebc4b-2580-5580-9269-9d20f99287eb

Jiangfeng, C., 2011. Bionomics and control of Aproceros leucopoda. Forest Pest and Disease, 6, 004.

JNCC, 2010. Cosmia diffinis priority terrestrial invertebrate list – Biodiversity Action Plan version 2. Peterborough, UK: Joint Nature Conservation Committee.http://jncc.defra.gov.uk/_speciespages/241.pdf

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Links to Websites

Principal Source

Draft datasheet under review

Contributors

25/01/19 Original text by: 

Max Blake, Forest Research, Alice Holt Lodge, Wrecclesham, Surrey, UK.

Distribution Maps