Skip to main content Accessibility help
×
Home
Hostname: page-component-7f7b94f6bd-sqtrr Total loading time: 0.869 Render date: 2022-06-28T17:46:17.685Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "useRatesEcommerce": false, "useNewApi": true } hasContentIssue true

Elm zigzag sawfly, Aproceros leucopoda (Hymenoptera: Argidae), recorded for the first time in North America through community science

Published online by Cambridge University Press:  23 September 2021

Véronique Martel*
Affiliation:
Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Quebec City, Quebec, Canada
Olivier Morin
Affiliation:
Canadian Food Inspection Agency, Plant Health Science Directorate, Quebec City, Quebec, Canada
Spencer K. Monckton
Affiliation:
York University, Department of Biology, Toronto, Ontario, Canada
Charles S. Eiseman
Affiliation:
(unaffiliated) Northfield, Massachusetts, United States of America
Catherine Béliveau
Affiliation:
Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Quebec City, Quebec, Canada
Michel Cusson
Affiliation:
Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Quebec City, Quebec, Canada
Stephan M. Blank
Affiliation:
Senckenberg Deutsches Entomologisches Institut (German Entomological Institute), Müncheberg, Germany
*
*Corresponding author. Email: veronique.martel@nrcan-rncan.gc.ca
Rights & Permissions[Opens in a new window]

Abstract

The elm zigzag sawfly, Aproceros leucopoda Takeuchi (Hymenoptera: Argidae), was reported for the first time in North America during the summer of 2020. Characteristic zigzag defoliation was reported in the province of Québec, Canada, on the community science website, iNaturalist. Field trips conducted to the site resulted in the collection of live specimens (a few larvae and a cocoon from which an adult emerged) and onsite observation of diagnostic defoliation and empty cocoons, confirming the presence of this exotic species in Canada. Subsequent inspection of elm trees by naturalists and scientists in the south of the province led to the conclusion that the species is more widely distributed than first expected and that the invasion is not localised to a small area. Preliminary genetic data pointed to a possible European origin of the Canadian population, but conclusive assignment to source will require examination of more specimens and the collection of reference sequences from different European and Asian populations. This is a good example of the importance of community science in the detection of new invasive species.

Résumé

Résumé

La tenthrède en zigzag de l’orme, Aproceros leucopoda Takeuchi (Hymenoptera: Argidae), a été observée pour la première fois en Amérique du Nord durant l’été 2020. La défoliation en zigzag caractéristique de l’espèce a été rapportée dans la province de Québec, sur le site de science communautaire iNaturalist. Des sorties sur le terrain ont mené à la récolte de spécimens vivants (quelques larves et un cocon duquel un adulte a émergé) et à l’observation de défoliation typique et de cocons vides, confirmant la présence de cette espèce exotique au Canada. L’inspection subséquente d’ormes par des naturalistes et des scientifiques dans le sud de la province a mené à la conclusion que cette espèce est présente plus largement et que l’invasion n’est pas localisée à une petite superficie. Des analyses génétiques indiquent une possible origine européenne, mais l’identification formelle de la source nécessitera l’analyse de spécimens additionnels et la création d’une collection élargie de séquences de référence pour les populations européennes et asiatiques. Il s’agit d’un excellent exemple de l’importance de la science communautaire dans la détection de nouvelles espèces envahissantes.

Type
Research Paper
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.
Copyright
© The authors and Her Majesty, the Queen, in Right of Canada 2021. Published by Cambridge University Press on behalf of the Entomological Society of Canada

Introduction

Invasive alien species have been a major ecological concern for the last few decades, and most introductions of such species are anthropogenic (Lowry et al. Reference Lowry, Rollinson, Layboum, Scott, Aiello-Lammens and Gray2013). They can have an important impact on local biodiversity and also on ecosystem services and human well-being (McGeoch et al. Reference McGeoch, Butchart, Spear, Marais, Kleynhans and Symes2010; Shackleton et al. Reference Shackleton, Shackleton and Kull2018). Introduced species are often more disruptive in novel territories than in their native ranges through different mechanisms, including lower plant defense (Desurmont et al. Reference Desurmont, Donoghue, Clement and Agrawal2011) and lower susceptibility to natural enemies (enemy-release hypothesis; reviewed by Colautti et al. Reference Colautti, Ricciardi, Grigorovich and MacIsaac2004 and Heger and Jeschke Reference Heger and Jeschke2014), that remove checks to population growth and damage. The emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), is a recent example of an invasive insect having a higher impact in its introduced range both in Europe and in North America compared to in its native range in Asia (Poland and McCullough Reference Poland and McCullough2006; Orlova-Bienkowskaja Reference Orlova-Bienkowskaja2013). Two other examples of forest exotic pest species having higher impacts in their introduced ranges in North America are the pine shoot beetle, Tomicus piniperda (Linnaeus) (Coleoptera: Scolytidae) (reviewed in Poland and Haack Reference Poland and Haack2003), and the brown longhorn spruce beetle, Tetropium fuscum (Fabricius) (Coleoptera: Cerambycidae) (Smith and Hurley Reference Smith and Hurley2000).

In North America, elm trees are threatened by Dutch elm disease, which was accidentally introduced to Canada in 1945 (reviewed by Hubbes Reference Hubbes1999). This disease, caused by the fungus Ophiostoma ulmi (Buisman) Nannfeldt (Ophiostomataceae) and carried by two bark beetles, Hylurgopinus rufipes (Eichhoff) and Scolytus multistriatus (Marsham) (Coleoptera: Curculionidae), affects all three indigenous elm species in Canada – Ulmus americana Linnaeus, U. rubra Muhlenberg, and U. thomasii Sargent (Ulmaceae) – as well as exotic elm species. The disease causes rapid decline of elms and their eventual death. In the city of Toronto, Ontario, Canada, the elm population was reduced by 80% because of the disease (Huntley Reference Huntley1982, cited by Hubbes Reference Hubbes1999). However, some municipalities, including Québec City, Québec, Canada (which has American elm (U. americana) – also called white elm – as its emblem tree), have management programmes to rapidly eradicate new infestations, thus allowing elm to remain prominent in the urban landscape.

In addition to Dutch elm disease, Canadian elms are affected by several native insect pests and also alien insect species, including the recently introduced elm leafminers Orchestes steppensis Korotyaev (Coleoptera: Curculionidae), Stigmella multispicata Rocienė & Stonis (Lepidoptera: Nepticulidae), and Fenusa pusilla (Serville) (= F. ulmi Sundevall) (Hymenoptera: Tenthredinidae) (Sweeney et al. Reference Sweeney, Anderson, Webster and Neville2012; Miller and Ware Reference Miller and Ware2014; van Nieukerken et al. Reference van Nieukerken, Gilrein and Eiseman2018). The arrival of another invasive species attacking elms could thus have an important impact in North America. The elm zigzag sawfly, Aproceros leucopoda Takeuchi (Hymenoptera: Argidae), is indigenous to east Asia. It was reported for the first time in Central Europe in 2003 (Blank et al. Reference Blank, Hara, Mikulás, Csóka, Ciornei and Constantineanu2010), although an earlier, undetected presence seems plausible. The sawfly spread rapidly across a vast geographical area of western Eurasia and now ranges from England (Royal Botanic Garden Edinburgh 2018) in the west to central Russia (Sundukov Reference Sundukov2017) and Kazakhstan (Ashikbayev et al. Reference Ashikbayev, Mukhamadiyev, Mengdibayeva, Temirzhanov and Kuanyshbaev2018) in the east.

The life history of A. leucopoda favours successful establishment in new areas, whence it can spread rapidly (Blank et al. Reference Blank, Hara, Mikulás, Csóka, Ciornei and Constantineanu2010): it potentially can have four to six generations per year, leading to rapid population growth; it reproduces parthenogenetically without males – that is, it reproduces by thelytoky (all eggs are unfertilised and produce females) and no male has ever been observed; and it actively can disperse 45–90 km per year (Blank et al. Reference Blank, Hara, Mikulás, Csóka, Ciornei and Constantineanu2010, Reference Blank, Köhler, Pfannenstill, Neuenfeldt, Zimmer and Jansen2014). Its relatively low supercooling point, which varies between –12 °C and –24 °C in Europe (Vétek et al. Reference Vétek, Fekete, Ladányi, Cargnus, Zandigiacomo and Oláh2020), also suggests that it is able to survive Canadian winters.

Blank et al. (Reference Blank, Hara, Mikulás, Csóka, Ciornei and Constantineanu2010) examined the bionomics of this species. Elm zigzag sawfly females lay between 7 and 49 eggs individually on the edges of elm leaves. The young larvae hatch after four to eight days and start feeding from the edge of the leaf in a zigzag pattern between two veins towards the midrib. Later-instar larvae can eventually consume the entire leaf, leaving only the midrib. After 15–18 days, the last (sixth) instar larvae form loose cocoons, easily recognised, underneath the leaves. Adults emerge quickly (two to three days) after cocoon formation. Females can start laying eggs immediately without mating, which contributes to rapid population increase. Summer and winter cocoons are dimorphic: the former are as described above, whereas the latter have more solid walls that better protect larvae during winter on the ground. Such “winter” cocoons have been reported to be produced throughout the summer, which may indicate an adaptation that ensures some individuals will be ready for winter even if cold temperatures arrive unexpectedly. Adults from summer cocoons tend to be paler and have shorter genae than adults from winter cocoons.

Aproceros leucopoda attracted attention as a pest of elms in China and Japan, where the species is native (Wu Reference Wu2006; Blank et al. Reference Blank, Hara, Mikulás, Csóka, Ciornei and Constantineanu2010; Cao et al. Reference Cao, Lin, Wu, Zhang and Zhao2011). In Europe, serious damage has been reported, in particular in arid regions of Russia in the northwest Caucasus Range, where the introduced Siberian elm (U. pumila Linnaeus) has been planted in wind shelters along streets and arable areas (e.g., Martynov and Nikulina Reference Martynov and Nikulina2017; Belitskaya and Gribust Reference Belitskaya and Gribust2019). The elm zigzag sawfly can completely defoliate a tree (Zandigiacomo et al. Reference Zandigiacomo, Cargnus and Villani2011; Blank et al. Reference Blank, Köhler, Pfannenstill, Neuenfeldt, Zimmer and Jansen2014), and although attacked trees can produce a second batch of leaves and thus survive, their growth can be affected. No mortality has been reported at the time of writing (Zandigiacomo et al. Reference Zandigiacomo, Cargnus and Villani2011). However, the sawfly’s presence, like other pests, could exacerbate the impact of Dutch elm disease on trees affected by both (Büchel et al. Reference Büchel, Fenning, Gershenzon, Hilker and Meiners2015). Its presence in North America could thus have important impacts, especially for municipalities with programmes protecting against Dutch elm disease.

In summer 2020, the first observation of A. leucopoda in North America was reported on the community science website, iNaturalist (Hogue Reference Hogue2020). The objectives of the present study were: (1) to confirm species identification following onsite specimen collection; (2) to characterise the site of the first observation; (3) to solicit additional observations through social media and community science; and (4) to make a first assessment via molecular analysis of the likely geographic origin of this introduction.

Material and methods

Initial observation and field mission

The first signs of defoliation were observed on 30 July 2020 and published the next day on the community science website, iNaturalist (Hogue Reference Hogue2020). The photo published alongside the report was originally added to the “Leafminers of North America” project on iNaturalist, where it was recognised as depicting not a leaf mine but potential evidence of A. leucopoda. This observation was brought to the attention of entomologists in the province of Québec via email by the observer. The site was visited on 27 August 2020 for thorough investigation and specimen collection. Collected specimens were sent to the Canadian Food Inspection Agency Entomology Lab in Ottawa, Ontario, Canada for identification using the key from Blank et al. (Reference Blank, Hara, Mikulás, Csóka, Ciornei and Constantineanu2010). Three larvae and a single adult (emerged from a cocoon during transportation back to the lab) were deposited as voucher specimens in the entomological collection of the Canadian Food Inspection Agency Entomology Lab in Ottawa (CFIA#20-00981).

Characterisation of the first reported site

Site characteristics

The following protocol was adapted from Canada’s National Forest Inventory (Natural Resources Canada 2008). Six 0.01-ha plots (5.64-m radius) were established in Sainte-Martine, Québec, where the first observation was reported alongside a road, to characterise the site composition. These plots were set up in three pairs, each pair having one plot on each side of the road (Fig. 1). Within these plots, tree species, diameter at breast height, and crown class (dominant, codominant, intermediate, and suppressed) were noted for each tree that was larger than 9 cm in diameter at breast height. Starting from the centre of each plot, the same measurements were made on trees that were smaller than 9 cm in diameter at breast height within a radius of 2.82 m. Finally, within a 1-m radius from each plot’s centre, the understorey plants were identified.

Fig. 1. Map showing the six plots inventoried nearby the first observation of Aproceros leucopoda in Sainte-Martine, Québec, Canada. Plots were paired on both sides of the road, and a larger 200-m area was used to assess landscape use with satellite images.

The canopy coverage was measured using satellite images (Environmental Systems Research Institute 2021) in two zones for every plot: a small-scale zone covering exactly each of the six 5.64-m-radius plots and a larger-scale zone with a 200-m radius around each pair of plots that provided an idea of the surrounding landscape. The proportional coverage of three landscape types – forest, agricultural, and anthropogenic (i.e., roads and buildings) – was determined.

Elm zigzag sawfly damage

All elm trees within each 5.64-m-radius plot were examined for A. leucopoda damage. The entire canopy was examined, with the upper canopy being observed using binoculars. Damage was categorised depending on the degree of certainty that it was caused by A. leucopoda. Damage was characterised as A. leucopoda when zigzag defoliation was clearly visible. Indeed, early-instar larvae of some Sterictiphora species (Argidae, and also Sterictiphorinae such as Aproceros) are known to cause similar damage, but they all are restricted to Rosaceae for larval host plants (Eiseman Reference Eiseman2015; Eiseman and Smith Reference Eiseman and Smith2020). When defoliation was observed between veins but without any zigzag, this was considered consistent with damage by late-instar A. leucopoda and was recorded as probably A. leucopoda. Any other type of damage was ignored.

A Pearson correlation analysis was performed between the elm diameter at breast height and the total number of signs observed per tree using R software (R Core Team 2017).

Additional community science evidence

The Canadian Food Inspection Agency and the Canadian Forest Service posted requests on social media, asking communities to watch for any signs of this new insect (e.g., @MartelVronique3, 11 September 2020, https://twitter.com/MartelVronique3/status/1304526609731461120; @InspectionCan, 11 September 2020, https://twitter.com/InspectionCan/status/1304521361440886787). For any new report or observation, specimens were either collected by the observers and sent to the Canadian Food Inspection Agency, or Canadian Food Inspection Agency or Canadian Forest Service personnel visited the site to collect specimens for formal identification.

After the publication of a second observation on iNaturalist on 4 September 2020 (Drapeau-Picard Reference Drapeau-Picard2020), a search using iNaturalist’s custom URL feature was undertaken to find additional signs of the insect on elms. A custom search for elm observations centred on the midpoint of the two first feeding track records (45.6268, –73.4702), and the distance between them (108.84 km) was multiplied by 1.5 to define the search radius. Because it is possible that the species dispersed from one location to the other, we assumed that it could have done so equally in any direction and over the same distance. The search was restricted to verifiable observations recorded in the months of April–November (the probable active season), from April 2018 to May 2021. A total of 1281 elm observations were reviewed using iNaturalist’s identify function, at the following URL: https://inaturalist.ca/observations/identify?quality_grade=needs_id,research&lat=45.6268&lng=-73.4702&radius=163.26&year=2018,2019,2020&month=4,5,6,7,8,9,10,11&taxon_id=53549&place_id=any. Photos showing leaves in these observations were inspected for sign of A. leucopoda-feeding tracks.

A second custom search was performed to investigate the possibility of a separate introduction of A. leucopoda in Virginia, United States of America. This search was motivated by a June 2019 observation of an adult sawfly in Virginia (Seltzer Reference Seltzer2019), the resemblance to A. leucopoda of which was noted only after the species was first detected in Quebec in 2020. A custom URL search was used to review 1951 elm observations from within a 180-km radius of the Virginia observation, using the following URL: https://inaturalist.ca/observations/identify?quality_grade=needs_id,research&lat=39.037807&lng=-77.951755&radius=180&year=2018,2019,2020&month=4,5,6,7,8,9,10,11&taxon_id=53549&place_id=any.

Origin of the introduction

All specimens not sent for formal species identification by the Canadian Food Inspection Agency in Ottawa were stored in 70% ethanol for molecular-analysis comparisons with available European and Asian sequences. A total of 12 larvae were analysed: two larvae that were collected on 9 September 2020 in Saint-Pie, Québec (+45 178, –73 776) and 10 larvae that were collected on 11 September 2020 in Parc du Rocher, Saint-Amable, Québec (+45.645, –73.325).

DNA extraction

Samples of DNA were extracted from 12 individual larvae using the Qiagen DNeasy Blood and Tissue kit (cat. 69504; Qiagen, Hilden, Germany) following the “Purification of Total DNA from Animal Tissues” protocol provided with the kit. Larvae were crushed in a mix of 180 µL ATL buffer and 20 µL proteinase K, followed by an overnight incubation in a thermomixer (56 °C, 400 rpm 5 minutes/hour). The rest of the extraction followed the Qiagen protocol, including the facultative RNase step. The DNA was then eluted in 100 µL of water.

Mitochondrial cytochrome oxidase 1 barcode amplification and sequencing

Polymerase chain reaction amplification of each DNA sample was conducted using Platinum SuperFi DNA Polymerase (Invitrogen; Thermo-Fisher Scientific Inc., Waltham, Massachusetts, United States of America), following the manufacturer’s instructions for genomic DNA (5–50 ng of DNA/reaction) and a three-step amplification protocol for fragments shorter than 10 kilobases in length. Amplification was done using CO1 forward and reverse primers, with two different sets of primers to obtain overlapping amplicons (Table 1), and under the following conditions: 30 seconds at 98 °C, plus 35 cycles at 98 °C for 10 seconds, at 58 °C for 10 seconds, and at 72 °C for 15 seconds, and a final extension step of 72 °C for 5 minutes. Amplicons were sequenced from both ends using the same forward and reverse primers used for polymerase chain reaction amplification (SANGER Sequencing platform, Centre hospitalier universitaire de Québec–Université Laval Research Centre, Québec City, Québec, Canada).

Table 1. Primer sequences used for polymerase chain reaction amplification in the present study.

Phylogenetic analysis

The unique sequence obtained for the Saint-Pie and Saint-Amable specimens (GenBank accession number: MW887550) was compared to six European and Asian A. leucopoda CO1 sequences of sufficient length found in GenBank: KC974833 (Austria-1), KF936623 (Austria-2), KC973566 (Romania), KC976874 (China), KC976060 (Russia-1), KC975690 (Russia-2; Malm and Nyman Reference Malm and Nyman2015; Schmidt et al. Reference Schmidt, Taeger, Morinière, Liston, Blank and Kramp2017) and to that of Aprosthema austriacum, HQ563827 (Germany) as an outgroup. Aprosthema austriacum belongs to the same Argid subfamily, Sterictiphorinae, as Aproceros (Schmidt et al. Reference Schmidt, Taeger, Morinière, Liston, Blank and Kramp2017). Analyses were carried out using the maximum-likelihood method and the Tamura-3 model (Tamura Reference Tamura1992) with 1000 bootstrap replicates (MEGA X; Kumar et al. Reference Kumar, Stecher, Li, Knyaz and Tamura2018), based on a MUSCLE alignment (Edgar Reference Edgar2004a, Reference Edgar2004b) of 658 shared nucleotide positions from the CO1 barcode region, with no gap.

Results

Initial observation and field mission

Four larvae (three small ones and a larger one) and one cocoon were collected in Sainte-Martine, Québec on 27 August 2020. Several signs of typical zigzag defoliation, larvae, empty cocoons, and one unemerged summer cocoon were discovered (Fig. 2). The larvae and the adult that emerged from the cocoon were formally identified as Aproceros leucopoda at the Canadian Food Inspection Agency entomology laboratory in Ottawa (CFIA#20-00981).

Fig. 2. A, Typical zigzag defoliation with a close-up on the feeding Aproceros leucopoda larva, B, an empty summer cocoon on an elm leaf, and C, an elm leaf with late-instar larval defoliation and an unemerged cocoon (circled), all taken on the first visited site in Sainte-Martine, Québec, Canada.

Characterisation of the first reported site

Site characteristics

Analysis of satellite images showed that the landscape in the six sample plots consisted mainly of forests, although anthropogenic landscapes (roads and houses) and agricultural land were also present near four of the six paired plots (Fig. 3). Ulmus americana was the only elm species growing in the plots. A total of 37 elm trees were identified across all of the plots, accounting for up to 60% of the sites’ composition (Fig. 4), with an average diameter at breast height between 1.0 and 28.0 cm, depending on the plot (Table 2).

Fig. 3. Landscape usage in the 200-m radius around paired plots in Sainte-Martine, Québec, Canada obtained from the satellite image analysis.

Fig. 4. Tree species composition for each plot in Sainte-Martine, Québec, Canada.

Table 2. Average diameter at breast height (± standard deviation, in cm) for each tree species depending on the dominance (D, dominant; CD, codominant; I, intermediate; S, suppressed) for each plot in Sainte-Martine, Québec, Canada. No standard deviation is given when only one tree of that species was inventoried.

Elm zigzag sawfly damage

Damage was observed in every plot, on 27 of the 37 elm trees. For three of the six plots, as typical zigzag traces were not found, the damage was classified as probably from A. leucopoda (Fig. 5). A significant correlation occurred between the number of signs observed per tree and the tree’s diameter at breast height (r = 0.4656, t = 3.0681, df = 34, P = 0.004; Fig. 6).

Fig. 5. Total number of signs observed depending on the number of elm trees in each plot, depending on the certainty that it was caused by Aproceros leucopoda.

Fig. 6. Correlation between the number of signs observed on elm trees and their diameter at breast height (DBH) for all plots.

Additional community science evidence

As a result of social media efforts to encourage observations, 12 iNaturalist observations showing signs of elm zigzag sawfly were recorded between 4 September and 7 November 2020 from the Montréal area, bringing the total observations to 15 (Table 3). The elm zigzag sawfly was confirmed through formal Canadian Food Inspection Agency identification at seven sites in six Québec municipalities (Fig. 7).

Table 3. Research-grade iNaturalist observations of larvae or feeding tracks of Aproceros leucopoda, recorded in Canada in 2020. ON, Ontario; QC, Québec.

Fig. 7. Map showing the sites where the presence of Aproceros leucopoda was confirmed or suspected in Canada in 2020 and the area of the custom search on iNaturalist.

A search through 1281 iNaturalist elm observations yielded two that showed evidence of A. leucopoda. One previously overlooked observation was made on 6 July 2020, showing young larvae feeding along their characteristic zigzag tracks (Pharand Reference Pharand2020), and a visit to the site confirmed the presence of A. leucopoda through formal specimen identification. A second observation (made on 12 September 2020, but not posted to iNaturalist until May 2021) shows feeding tracks on an elm in Voyageur Provincial Park, Ontario (Clarkin Reference Clarkin2021), but the sawfly’s presence there had not been confirmed at the time of writing.

A secondary search of 1951 elm observations for the United States of America yielded a single observation from Virginia, made on 29 April 2019, that appears to show a zigzag feeding track with a larva present (McLean Reference McLean2019), although this could not be verified.

Origin of the introduction

The CO1 barcode that was sequenced was identical for all 12 A. leucopoda larvae tested (GenBank accession number: MW887550). Comparison of this sequence with existing GenBank entries confirmed the insect’s identity as A. leucopoda. The CO1-based maximum-likelihood phylogenetic analysis placed the Québec specimens nearest those from Austria and Romania, supported by a relative high bootstrap value (84%) and pointing to a possible European origin of the Québec population (Fig. 8).

Fig. 8. Maximum-likelihood phylogenetic tree of CO1 barcode sequences from populations of Aproceros leucopoda in Québec, Europe, and Asia, generated using MUSCLE and MEGA X. Branch-length scale represents 0.02 substitution per site. See the Material and methods section for the GenBank accession numbers.

Discussion

This is the first record of the exotic species Aproceros leucopoda in North America and, more specifically, in Canada, and its detection was greatly facilitated by the community science website iNaturalist. The species has been confirmed in six municipalities in southern Québec, with additional observed signs to be confirmed in a seventh municipality in Québec, in eastern Ontario (one putative sign), and in Virginia (also one putative sign), United States of America, suggesting that the species probably arrived before 2020 – possibly in 2018 or 2019, based on estimates of Blank et al. (Reference Blank, Köhler, Pfannenstill, Neuenfeldt, Zimmer and Jansen2014) regarding the speed of self-dispersal. In this instance, community science and the use of social media proved to be useful not only in the detection of a new invasive species but also in assessing its distribution in Canada to date.

The forest inventory performed at the site of the first observation shows that the area is mainly forested and has both agricultural and anthropogenic landscape elements. This suggests that A. leucopoda could be present in forested as well as in urban habitats. Indeed, the iNaturalist observations are from a wide range of habitats, including from within the city of Montréal, in botanical gardens, and in urban parks. In Europe, A. leucopoda has been found in a variety of habitats as well: along motorways, in parking areas, in cities, in botanical gardens and arboreta, in woods, and on mountains – everywhere elms grow – but it has been suggested that solitary elms in urban areas and recently planted trees may be more likely to be attacked (Zandigiacomo et al. Reference Zandigiacomo, Cargnus and Villani2011; Blank et al. Reference Blank, Köhler, Pfannenstill, Neuenfeldt, Zimmer and Jansen2014; Mol and Vonk Reference Mol and Vonk2015; Holuša et al. Reference Holuša, Stodůlková and Macek2017; Vétek et al. Reference Vétek, Bartha and Oláh2017). In the Netherlands, 71% of observations of A. leucopoda were within or near urban areas, and 32% were near roads and railways (Mol and Vonk Reference Mol and Vonk2015). This makes A. leucopoda an even better candidate for detection through community science.

In the present study, damage was observed on 73% of all elm trees in the sample plots and on trees of all sizes, although more signs were observed on larger-diameter trees. The damage was observed on U. americana, the only elm species found to be growing in the plots. However, A. leucopoda has been found to attack many native and introduced elm species in Europe, including cultivars resistant to Dutch elm disease (Zandigiacomo et al. Reference Zandigiacomo, Cargnus and Villani2011; Blank et al. Reference Blank, Köhler, Pfannenstill, Neuenfeldt, Zimmer and Jansen2014; Vétek et al. Reference Vétek, Bartha and Oláh2017), and at least some of the damaged elms observed in Québec via iNaturalist appear to be U. rubra. It should therefore be assumed that all elm species in North America are potential hosts for this exotic defoliator. Because the formal identification of the species occurred late in the season (early September), further studies covering the entire growing season will be undertaken to assess the species’ exact phenology in this new habitat, including the number of generations it can undergo under the local climate, the elm species it attacks or prefers, its potential impacts, and other basic life-history traits. In particular, its impact on elm varieties resistant to Dutch elm disease will need to be investigated to assess its risk to elm populations in Canada.

This study highlights the importance of community science in the detection of exotic species. Although community science is far from new, it has only grown in visibility and popularity, thanks in part to apps and websites like iNaturalist, which recorded its 50-millionth observation in September 2020 – approximately twice as many as had been recorded only a year earlier (iNaturalist 2020). Observations such as those reported on iNaturalist offer great potential for detecting new pest threats. For example, the platform Mosquito Alert allowed for the first detection of an exotic mosquito, Aedes japonicus (Theobald) (Diptera: Culicidae), in Spain (Eritja et al. Reference Eritja, Ruiz-Arrondo, Delacour-Estrella, Schaffner, Álvarez-Chachero and Bengoa2019), and iNaturalist facilitated the detection of the European firebug, Pyrrhocoris apterus Linnaeus (Hemiptera: Pyrrhocoridae), in Ontario (Oviedo Rojas and Jackson Reference Oviedo Rojas and Jackson2018). Similarly, the first detection of a North American fish, Cynoscion regalis (Bloch & Schneider) (Pisces: Sciaenidae), in Europe was made by fishermen in Portugal and reported in specialised magazines, personal blogs, and regional media (Morais and Teodósio Reference Morais and Teodósio2016). Although data collected through community science projects are sometimes criticised – for example, for their lack of true absence data, their quality, or their bias in geographic coverage – reported observations can often be validated, thereby making valuable contributions to science while also decreasing the costs of research and increasing community awareness (Crall et al. Reference Crall, Newmann, Jarnevich, Stohlgren, Waller and Graham2010; Bois et al. Reference Bois, Silander and Mehrhoff2011; Johnson et al. Reference Johnson, Mader, Dasgupta and Jumar2020; Larson et al. Reference Larson, Graham, Achury, Coon, Daniels and Gambrell2020; Encarnação et al. Reference Encarnação, Teodósio and Morais2021).

Community science apps may furthermore hold potential for monitoring for invasive species using methods similar to those outlined in the present study. This potential was in fact explored in the course of the present study: besides yielding the earliest observation of A. leucopoda in Québec, the iNaturalist custom URL search feature was also used to uncover the first suggested evidence of this species in Ontario and to investigate the possibility of a separate introduction in Virginia, United States of America. In the latter case, the putative observations from Virginia of an adult sawfly (Seltzer Reference Seltzer2019) and larva (McLean Reference McLean2019) – although not verified – have helped prompt on-the-ground monitoring in several other states.

The preliminary data on the genetic comparison of the DNA barcode sequences from Canadian specimens of A. leucopoda with the sequences of European and Asian specimens available from GenBank suggest the Canadian specimens derive from a European origin, with the sequences from Austria and Romania grouping with those from Québec. However, these results must be interpreted with caution, as only 12 specimens from Canada were sequenced and the number of European and Asian sequences available for comparison is also limited. Additional molecular investigations involving multiple markers will be conducted in 2021 with additional specimens and sequences from Canada, Europe, and Asia to more precisely identify the geographic origin of this introduction. Molecular analysis could eventually help to determine if one or more introductions occurred. The absence of variability among specimens of our small, geographically restricted sample might indicate that the Canadian population is based on the introduction and successful establishment of a single female of A. leucopoda, which reproduced parthenogenetically; this observation requires closer scrutiny.

The exact entrance pathway of this new invasive species to Canada remains unknown, even with the suggestion of a European origin. However, we speculate that it was introduced in the winter cocoon stage. Indeed, any other life stage would likely have died during transportation due to the combination of quick development and a lack of food (imported trees are transported in a dormant stage without foliage). Winter cocoons are formed on the ground and may have been transported within soil. Canadian import requirements prohibit entry of items with soil from off-continent, but fortuitous introductions of soil-borne pests are possible. The area where the Québec population was found may not be the point of introduction of the population; the insect may have dispersed from another locality instead.

Acknowledgements

The authors thank Karen McLachlan Hamilton and Graham Thurston from the Canadian Food Inspection Agency Entomology Lab for insect identification. They are also grateful to the individuals who reported defoliation or collected specimens: Alain Hogue, André-Philippe Drapeau Picard, Étienne Pharand, Morgan D. Jackson, Simon Amyot, Owen Clarkin, Carrie Seltzer, and Mary D. McLean. They appreciate the support of James Pagé from the Canadian Wildlife Federation for encouraging observations on iNaturalist. Finally, for their help in the field, in the lab, with analyses, and for comments on the manuscript, the authors thank Simon Trudeau, Sébastien Bélanger, Jessica Girona, Josée Laroche, Abdelmadjid Djoumad, and Erin Bullas.

This paper is dedicated to the memory of Dr. Gábor Vétek, who passed away too soon in December 2020.

Footnotes

Subject Editor: Therese Poland

References

Ashikbayev, N.Z., Mukhamadiyev, N.S., Mengdibayeva, G.Z., Temirzhanov, M.B., and Kuanyshbaev, N.K. 2018. Development of forest entomology in Kazakhstan. In The International Scientific and Practical Conference “Actual problems of sustainable development in forestry complex” dedicated to the 70th anniversary of higher forest education in Kazakhstan. Volume 2. Edited by T.I. Espolov, K.M. Tireuov, E.I. Islamov, S.B. Baizakov, K.T. Abayeva, E.Z. Kentbaev, and B.A. Kentbaeva. Aitumar Publishing, Almaty, Kazakhstan. Pp. 42–47.Google Scholar
Belitskaya, M.N. and Gribust, I.R. 2019. Dendrofagous in the forest reclamation complexes with the participation of introduced tree species in arid zone conditions. Environment and Human: Ecological Studies, 9: 343361. https://doi.org/10.31862/2500-2961-2019-9-3-343-361.Google Scholar
Blank, S.M., Hara, H., Mikulás, J., Csóka, G., Ciornei, C., Constantineanu, R., et al. 2010. Aproceros leucopoda (Hymenoptera: Argidae): an East Asian pest of elms (Ulmus spp.) invading Europe. European Journal of Entomology, 107: 357367. https://doi.org/10.14411/eje.2010.045.CrossRefGoogle Scholar
Blank, S.M., Köhler, T., Pfannenstill, T., Neuenfeldt, N., Zimmer, B., Jansen, E., et al. 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: 5774. https://doi.org/10.3897/JHR.41.8681.CrossRefGoogle Scholar
Bois, S.T., Silander, J.A., and Mehrhoff, L.J. 2011. Invasive plant atlas of New England: the role of citizens in the science of invasive alien species detection. Bioscience, 61: 763770. https://doi.org/10.1525/bio.2011.61.10.6.CrossRefGoogle Scholar
Büchel, K., Fenning, T., Gershenzon, J., Hilker, M., and Meiners, T. 2015. Elm defence against herbivores and pathogens: morphological, chemical and molecular regulation aspects. Phytochemistry Reviews, 15: 961983. https://doi.org/10.1007/s11101-015-9442-0.CrossRefGoogle Scholar
Cao, J.F., Lin, C.S., Wu, F.Y., Zhang, H.X., and Zhao, W.J. 2011. Bionomics and control of Aproceros leucopoda . Forest Pest and Disease, 6: 1820.Google Scholar
Clarkin, O. 2021. [Photograph submitted to iNaturalist]. Available from https://inaturalist.ca/observations/77748210 [accessed 7 May 2021].Google Scholar
Colautti, R.I., Ricciardi, A., Grigorovich, I.A., and MacIsaac, H.J. 2004. Is invasion success explained by the enemy release hypothesis? Ecology Letters, 7: 721733. https://doi.org/10.1111/j.1461-0248.2004.00616.x.CrossRefGoogle Scholar
Crall, A.W., Newmann, G.J., Jarnevich, C.S., Stohlgren, T.J., Waller, D.M., and Graham, J. 2010. Improving and integrating data on invasive species collected by citizen scientists. Biological Invasions, 12: 34193428. https://doi.org/10.1007/s10530-010-9740-9.CrossRefGoogle Scholar
Desurmont, G.A., Donoghue, M.J., Clement, W.L., and Agrawal, A.A. 2011. Evolutionary history predicts plant defense against an invasive pest. Proceedings of the National Academy of Science, 17: 70707074. https://doi.org/10.1073/pnas.1102891108.CrossRefGoogle Scholar
Drapeau-Picard, A.P. 2020. [Photograph submitted to iNaturalist]. Available from https://inaturalist.ca/observations/58949482 [accessed 9 March 2021].Google Scholar
Edgar, R.C. 2004a. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32: 17921797. https://doi.org/10.1093/nar/gkh340.CrossRefGoogle ScholarPubMed
Edgar, R.C. 2004b. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics, 5: 113. https://doi.org/10.1186/1471-2105-5-113.CrossRefGoogle ScholarPubMed
Eiseman, C.S. 2015. On the distinctive feeding pattern of Sterictiphora Billberg (Hymenoptera: Argidae) sawfly larvae. Proceedings of the Entomological Society of Washington, 117: 6567. https://doi.org/10.4289/0013-8797.117.1.65.CrossRefGoogle Scholar
Eiseman, C.S. and Smith, D.R. 2020. New sawfly (Hymenoptera: Argidae, Tenthredinidae) host records from northeastern North America. Proceedings of the Entomological Society of Washington, 122: 299307. https://doi.org/10.4289/0013-8797.122.2.299.CrossRefGoogle Scholar
Encarnação, J., Teodósio, M.A., and Morais, P. 2021. Citizen science and biological invasions: a review. Frontiers in Environmental Sciences, 8: 602980. https://doi.org/10.3389/fenvs.2020.602980.CrossRefGoogle Scholar
Environmental Systems Research Institute. 2021. ArcGIS Basemap Data 2009–2021. Environmental Systems Research Institute, Inc., Redlands, California, United States of America.Google Scholar
Eritja, R., Ruiz-Arrondo, I., Delacour-Estrella, S., Schaffner, F., Álvarez-Chachero, , Bengoa, M., et al. 2019. First detection of Aedes japonicus in Spain: an unexpected finding triggered by citizen science. Parasites and Vectors, 12: 53. https://doi.org/10.1186/s13071-019-3317-y.CrossRefGoogle ScholarPubMed
Hebert, P.D.N., Penton, E.H., Burns, J.M., Janzen, D.H., and Hallwachs, W. 2004. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator . Proceedings of the National Academy of Sciences, 101: 1481214817. https://doi.org/10.1073/pnas.0406166101.CrossRefGoogle ScholarPubMed
Heger, T. and Jeschke, J.M. 2014. The enemy release hypothesis as a hierarchy of hypotheses. Oikos, 123: 741750. https://doi.org/10.1111/j.1600-0706.2013.01263.x.CrossRefGoogle Scholar
Hogue, A. 2020. [Photograph submitted to iNaturalist]. Available from https://inaturalist.ca/observations/54944998 [accessed 9 March 2021].Google Scholar
Holuša, J., Stodůlková, P., and Macek, J. 2017. Observations on the occurrence and phenology of the invasive elm defoliator Aproceros leucopoda (Hymenoptera: Argidae) in the Czech Republic. Urban Forestry and Urban Greening, 21: 2933. https://doi.org/10.1016/j.ufug.2016.11.005.CrossRefGoogle Scholar
Hubbes, M. 1999. The American elm and Dutch elm disease. The Forestry Chronicle, 75: 265273. http://dx.doi.org/10.5558/tfc75265-2.CrossRefGoogle Scholar
Huntley, G.D. 1982. The elm: a resurgent resource or a persistent problem? In Proceedings of the Dutch elm disease symposium and workshop, Winnipeg, Manitoba, October 5–9, 1981. Edited by E.S. Kondo, Y. Hiratsuka, and W.B.G. Denyer. Manitoba Department of Natural Resources, Manitoba, Canada. Pp. 103–111.Google Scholar
iNaturalist. 2020. 50 million observations on iNaturalist! Available from https://www.inaturalist.org/blog/40699-50-million-observations-on-inaturalist [accessed 5 April 2021].Google Scholar
Johnson, B.A., Mader, A.D., Dasgupta, R., and Jumar, P. 2020. Citizen science and invasive alien species: an analysis of citizen science initiatives using information and communications technology (ICT) to collect invasive alien species observations. Global Ecology and Conservation, 21: e00812. https://doi.org/10.1016/j.gecco.2019.e00812.CrossRefGoogle Scholar
Kumar, S., Stecher, G., Li, M., Knyaz, C., and Tamura, K. 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35: 15471549. https://doi.org/10.1093/molbev/msy096.CrossRefGoogle ScholarPubMed
Larson, E.R., Graham, B.M., Achury, R., Coon, J.J., Daniels, M.K., Gambrell, D.K., et al. 2020. From eDNA to citizen science: emerging tools for the early detection of invasive species. Frontiers in Ecology and the Environment, 18: 194202. https://doi.org/10.1002/fee.2162.CrossRefGoogle Scholar
Lowry, E., Rollinson, E.J., Layboum, A.J., Scott, T.E., Aiello-Lammens, M.E., Gray, S.M., et al. 2013. Biological invasions: a field synopsis, systematic review and database of the literature. Ecology and Evolution, 3: 182196. https://doi.org/10.1002/ece3.431.CrossRefGoogle Scholar
Malm, T. and Nyman, T. 2015. Phylogeny of the symphytan grade of Hymenoptera: new pieces into the old jigsaw (fly) puzzle. Cladistics, 31: 117. https://doi.org/10.1111/cla.12069.CrossRefGoogle ScholarPubMed
Martynov, V.V. and Nikulina, T.V. 2017. Population surge of zigzag elm sawfly (Aproceros leucopoda (Takeuchi, 1939): Hymenoptera: Argidae) in northern Sea of Azov region. Russian Journal of Biological Invasions, 1: 2534. https://doi.org/10.1134/S2075111717020059.Google Scholar
McGeoch, M.A., Butchart, S.H., Spear, D., Marais, E., Kleynhans, E.J., Symes, A., et al. 2010. Global indicators of biological invasion: species numbers, biodiversity impact and policy responses. Diversity and Distributions, 16: 95108. https://doi.org/10.1111/j.1472-4642.2009.00633.x.CrossRefGoogle Scholar
McLean, M.D. 2019. [Photograph submitted to iNaturalist]. Available from https://www.inaturalist.org/observations/24028356 [accessed 9 March 2021].Google Scholar
Miller, F. and Ware, G. 2014. Seasonal activity, within-tree distribution, and ovipositional and feeding preference of the elm leafminer, Fenusa ulmi (Hymenoptera: Tenthredinidae). Journal of Environmental Horticulture, 32: 3948. https://doi.org/10.24266/0738-2898.32.1.39 CrossRefGoogle Scholar
Mol, A.W.M. and Vonk, D.H. 2015. De iepenzigzagbladwesp Aproceros leucopoda (Hymenoptera, Argidae), een invasieve exoot in Nederland. Entomologische Berichten, 75: 5063.Google Scholar
Morais, P. and Teodósio, M.A. 2016. The transatlantic introduction of weakfish Cynoscion regalis (Bloch & Schneider, 1801) (Sciaenidae, Pisces) into Europe. BioInvasions Records, 5: 259265. https://doi.org/10.3391/bir.2016.5.4.11.Google Scholar
Natural Resources Canada. 2008. Canada’s National Forest Inventory ground sampling guidelines: specifications for ongoing measurement. Canadian Forest Service, Natural Resources Canada, Ottawa, Ontario, Canada.Google Scholar
Orlova-Bienkowskaja, M.J. 2013. Ashes in Europe are in danger: the invasive range of Agrilus planipennis in European Russia is expanding. Biological Invasions, 16: 13451349. https://doi.org/10.1007/s10530-013-0579-8.CrossRefGoogle Scholar
Oviedo Rojas, P.J. and Jackson, M.D. 2018. Pyrrhocoris apterus L. (Hemiptera: Pyrrhocoridae), a newly introduced family, genus, and species to Ontario and Canada. Journal of the Entomological Society of Ontario, 149: 2732.Google Scholar
Pharand, É. 2020. [Photograph submitted to iNaturalist]. Available from https://inaturalist.ca/observations/59122142 [accessed 9 March 2021].Google Scholar
Poland, T.M. and Haack, R.A. 2003. Exotic forest insect pests and their impact on forest management. In Proceedings of the Society of American Foresters 2002 National Convention, Winston-Salem, North Carolina, October 5–9, 2002. Pp. 132–141. Society of American Foresters, Washington, D.C., United States of America.Google Scholar
Poland, T.M. and McCullough, D.G. 2006. Emerald ash borer: invasion of the urban forest and the threat to North America’s ash resource. Journal of Forestry, 104: 118124. https://doi.org/10.1093/jof/104.3.118.Google Scholar
R Core Team. 2017. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from https://www.Rproject.org/.Google Scholar
Royal Botanic Garden Edinburgh. 2018. Mark of Zorro: new pest coming soon to woodland near you? Available from https://www.rbge.org.uk/media-centre/press-releases/current/mark-of-zorro-new-pest-coming-soon-to-woodland-near-you [accessed 16 April 2021].Google Scholar
Schmidt, S., Taeger, A., Morinière, J., Liston, A., Blank, S.M., Kramp, K., et al. 2017. Identification of sawflies and horntails (Hymenoptera, ‘Symphyta’) through DNA barcodes: successes and caveats. Molecular Ecology Resources, 17: 670685. https://doi.org/10.1111/1755-0998.12614.CrossRefGoogle ScholarPubMed
Seltzer, C. 2019. [Photograph submitted to iNaturalist]. Available from https://inaturalist.ca/observations/27691429 [accessed 9 March 2021].Google Scholar
Shackleton, R.T., Shackleton, C.M., and Kull, C.A. 2018. The role of invasive alien species in shaping local livelihoods and human well-being: a review. Journal of Environmental Management, 229: 145157. https://doi.org/10.1016/j.jenvman.2018.05.007.CrossRefGoogle ScholarPubMed
Smith, G. and Hurley, J.E. 2000. First North American record of the Palaearctic species Tetropium fuscum (Fabr.) (Coleoptera: Cerambycidae). The Coleopterists Bulletin, 54: 540.CrossRefGoogle Scholar
Sundukov, Y.N. 2017. Suborder Symphyta: Sawflies and Wood Wasps. In Annotated Catalogue of the Hymenoptera of Russia. Volume 1. Symphyta and Apocrita: Aculeata. Edited by S.A. Belokobylskij and A.S. Lelej. Proceedings of the Zoological Institute of the Russian Academy of Sciences, Supplement Number 6. Pp. 20–117.Google Scholar
Sweeney, J., Anderson, R.S., Webster, R.P., and Neville, R. 2012. First records of Orchestes Fagi (L.) (Coleoptera: Curculionidae: Curculioninae) in North America, with a checklist of the North American Rhamphini. The Coleopterists Bulletin, 66: 297304.CrossRefGoogle Scholar
Tamura, K. 1992. Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G + C-content biases. Molecular Biology and Evolution, 9: 678687. https://doi.org/10.1093/oxfordjournals.molbev.a040752.Google ScholarPubMed
van Nieukerken, E.J., Gilrein, D.O., and Eiseman, C.S. 2018. Stigmella multispicata Rociene & Stonis, an Asian leafminer on Siberian elm, now widespread in eastern North America (Lepidoptera, Nepticulidae). ZooKeys, 784: 95125. https://doi.org/10.3897/zookeys.784.27296.CrossRefGoogle Scholar
Vétek, G., Bartha, D., and Oláh, R. 2017. Occurrence of the alien zigzag elm sawfly, Aproceros leucopoda (Hymenoptera: Argidae), in arboretums and botanical gardens of Hungary. Periodicum Biologorum, 119: 101106. https://doi.org/10.18054/pb.v119i2.4944.Google Scholar
Vétek, G., Fekete, V., Ladányi, M., Cargnus, E., Zandigiacomo, P., Oláh, R., et al. 2020. Cold tolerance strategy and cold hardiness of the invasive zigzag elm sawfly, Aproceros leucopoda (Hymenoptera: Argidae). Agricultural and Forest Entomology, 22: 231237. https://doi.org/10.1111/afe.12376.CrossRefGoogle Scholar
Wu, X. 2006. Studies on the biology and control of Aproceros leucopoda . Plant protection (Beijing), 32: 98100.Google Scholar
Zandigiacomo, P., Cargnus, E., and Villani, A. 2011. First record of the invasive sawfly Aproceros leucopoda infesting elms in Italy. Bulletin of Insectology, 64: 145149.Google Scholar
Figure 0

Fig. 1. Map showing the six plots inventoried nearby the first observation of Aproceros leucopoda in Sainte-Martine, Québec, Canada. Plots were paired on both sides of the road, and a larger 200-m area was used to assess landscape use with satellite images.

Figure 1

Table 1. Primer sequences used for polymerase chain reaction amplification in the present study.

Figure 2

Fig. 2. A, Typical zigzag defoliation with a close-up on the feeding Aproceros leucopoda larva, B, an empty summer cocoon on an elm leaf, and C, an elm leaf with late-instar larval defoliation and an unemerged cocoon (circled), all taken on the first visited site in Sainte-Martine, Québec, Canada.

Figure 3

Fig. 3. Landscape usage in the 200-m radius around paired plots in Sainte-Martine, Québec, Canada obtained from the satellite image analysis.

Figure 4

Fig. 4. Tree species composition for each plot in Sainte-Martine, Québec, Canada.

Figure 5

Table 2. Average diameter at breast height (± standard deviation, in cm) for each tree species depending on the dominance (D, dominant; CD, codominant; I, intermediate; S, suppressed) for each plot in Sainte-Martine, Québec, Canada. No standard deviation is given when only one tree of that species was inventoried.

Figure 6

Fig. 5. Total number of signs observed depending on the number of elm trees in each plot, depending on the certainty that it was caused by Aproceros leucopoda.

Figure 7

Fig. 6. Correlation between the number of signs observed on elm trees and their diameter at breast height (DBH) for all plots.

Figure 8

Table 3. Research-grade iNaturalist observations of larvae or feeding tracks of Aproceros leucopoda, recorded in Canada in 2020. ON, Ontario; QC, Québec.

Figure 9

Fig. 7. Map showing the sites where the presence of Aproceros leucopoda was confirmed or suspected in Canada in 2020 and the area of the custom search on iNaturalist.

Figure 10

Fig. 8. Maximum-likelihood phylogenetic tree of CO1 barcode sequences from populations of Aproceros leucopoda in Québec, Europe, and Asia, generated using MUSCLE and MEGA X. Branch-length scale represents 0.02 substitution per site. See the Material and methods section for the GenBank accession numbers.

You have Access Open access

Save article to Kindle

To save this article to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Elm zigzag sawfly, Aproceros leucopoda (Hymenoptera: Argidae), recorded for the first time in North America through community science
Available formats
×

Save article to Dropbox

To save this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about saving content to Dropbox.

Elm zigzag sawfly, Aproceros leucopoda (Hymenoptera: Argidae), recorded for the first time in North America through community science
Available formats
×

Save article to Google Drive

To save this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about saving content to Google Drive.

Elm zigzag sawfly, Aproceros leucopoda (Hymenoptera: Argidae), recorded for the first time in North America through community science
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *