Aproceros leucopoda
(elm zigzag sawfly)

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.

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).

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.

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).

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'.

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),

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).

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).

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

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.

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.

25/01/19 Original text by: 

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