ore

JHR 41:57—74 (2014) JOURNAL OF *0erriewed opevaccersjoural
doi: 10.3897/JHR.41.868| (G-) Hymenoptera

http://jhr.pensoft.net The insertional Society of Hymenopterists. RESEARCH

Zig-zagging across Central Europe: recent range
extension, dispersal speed and larval hosts of Aproceros
leucopoda (Hymenoptera, Argidae) in Germany

Stephan M. Blank', Thomas Kohler’, Toralf Pfannenstill?, Nadine Neuenfeldt?,
Bianka Zimmer’, Ewald Jansen*, Andreas Taeger', Andrew D. Liston!

I Senckenberg Deutsches Entomologisches Institut, Eberswalder Str. 90, 15374 Miincheberg, Germany 2 Beuth
Hochschule fir Technik Berlin, Fachbereich V — Life Sciences and Technology, Luxemburger Str. 10, 13353
Berlin, Germany 3 Landesamt fir Lindliche Entwicklung, Landwirtschaft und Flurneuordnung (LELF),
Millroser Chaussee 54, 15236 Frankfurt/Oder, Germany 4 Alter Marktweg 8, 04319 Leipzig, Germany

Corresponding authors: Stephan M. Blank (sblank@senckenberg.de); Andrew D. Liston (aliston@senckenberg.de)

Academic editor: S. Schmidt| Received 1 October 2014 | Accepted 19 October 2014 | Published 22 December 2014
http://zoobank. org/E56A6898-OF FF-4750-8F 03-2 14B46E 1 CB27

Citation: Blank SM, Kohler T, Pfannenstill T, Neuenfeldt N, Zimmer B, Jansen E, Taeger A, Liston AD (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: 57-74. doi: 10.3897/JHR.41.8681

Abstract

Aproceros leucopoda, the zig-zag sawfly, an invasive pest of elms (U/mus spp.), was found in two separate
areas of Germany through July 2014, ie., a northern area including the states of Berlin, Brandenburg,
Mecklenburg-West Pomerania, Saxony and Saxony-Anhalt, and a southern area in Bavaria. A speed of
self-dispersal of 45-90 km/yr has been calculated from earlier and present records. Observations of A.
leucopoda in Belgium and the Netherlands during 2013, which are 360-610 km distant from records in
Germany of that year, are interpreted as resulting from human-mediated jump dispersal. Larvae, feeding
traces and cocoons were frequently found on the native elm species U. minor and U. glabra, whereas none
could be detected on U. /aevis. Other occurrences were often on Resista® elms, causing severe defoliation
in a recent planting. New host plant records for A. leucopoda are: U. minor ‘Webbiana, U. minor var.
suberosa , and the Resista® cultivars U. ‘New Horizon’, U. ‘Regal’ and U. ‘Rebona’. The future dispersal
of A. leucopoda throughout most of Germany is expected, because at least U. glabra and U. minor are

widespread in this country.

Keywords
Argidae, Aproceros leucopoda, zig-zag sawfly, invasive species, pest species, Ulmus laevis, Ulmus Resista®

hybrids, distribution in Germany, self-dispersal, human-mediated jump dispersal

Copyright Stephan M. Blank et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC
BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

58 Stephan M. Blank et al. / Journal of Hymenoptera Research 41: 57-74 (2014)

Introduction

The invasive zig-zag sawfly Aproceros leucopoda Takeuchi, 1939, is of East Asian origin
and was first found in Europe in 2003 (Blank et al. 2010). Its larvae feed on elms (UL
mus spp.) and sometimes severely defoliate their hosts. By 2009, the known European
distribution of A. /eucopoda extended from eastern Ukraine to Austria and from Po-
land to Romania. Since then, it has also been found in northern Italy (Zandigiacomo
et al. 2011), Slovenia (de Groot et al. 2012), Croatia (MatoSevi¢ 2012), Moldova
(Timus et al. 2008, misidentified as Arge sp.) and widely in European Russia from
Rostov-on-Don to Moscow (Artokhin et al. 2012, Anonymous 2013). In Germany,
it had been recorded only from the extreme southeast of Bavaria (Kraus et al. 2012)
but not from the eastern states close to the Polish border, although the records of A.
leucopoda from Poland made in 2003 are amongst the first from Europe. In 2013, A.
leucopoda was observed near northwestern Germany in Belgium (Boevé 2014) and in
the Netherlands (Mol and Vonk 2013).

Aproceros leucopoda is classified in the Argidae, which comprise roughly 70 species
in Europe and about 900 worldwide (Taeger et al. 2006, 2010). In Europe, a few spe-
cies of Arge have been reported to occur as pests of ornamental plants and forest trees
(e.g., Pschorn-Walcher 1982, Taeger et al. 1998). Outbreaks of Arge pullata (Zaddach,
1859) may occur on birch trees. When the trees grow in pastures, farm livestock can be
poisoned after ingestion of larvae (Brummerstedt et al. 1987, Thamsborg et al. 1987,
Kannan et al. 1988, Hara and Shinohara 2008). Similar to Aproceros leucopoda in its
association with elms as the larval hosts, is Arge captiva (F. Smith, 1874) (Shinohara
et al. 2009). It became an invasive pest after its accidental introduction to Kazakhstan,
where the larvae have severely damaged Dwarf Elm trees (U. pumila) planted in the
new capital Astana (Blank et al. 2011).

To effect an early warning, in 2011 A. leucopoda was placed on the EPPO Alert
List, which displays information on pest organisms that possibly represent a risk to the
European and Mediterranean EPPO member countries (EPPO 2014). The Federal
Research Centre for Cultivated Plants of Germany assessed the phytosanitary risk at-
tached to this invasive species as high (Schrader and Schroder 2013). As a result of the
monitoring of A. /eucopoda in Germany, we report here on the recent range extension
into large areas of Germany, map the current distribution in this country and provide
new information on host plant choice. The current distribution pattern is discussed
and the speed of the range extension is estimated.

Methods
Since 2009, A.D. Liston [ADL] and S.M. Blank [SMB] have paid special attention

to elms in eastern Brandenburg, in the expectation that Aproceros leucopoda would be-
come established in this region. Searches were made for feeding traces, larvae, cocoons
and imagines (Figs 1-2). These were described and illustrated in detail by Blank et al.

Aproceros leucopoda: recent range extension, dispersal speed, larval hosts ay

(2010). Following the first observations in eastern Brandenburg in May 2013, the
frequency of searches was increased and the area in Germany that was searched was
extended, covering initially Br [Berlin and Brandenburg], Ni [Lower Saxony, Nieder-
sachsen], Sn [Saxony], St [Saxony-Anhalt] (abbreviations of the German states as used
in the checklist of the sawflies of Germany, Blank et al. 2001). In early October 2013,
SMB checked the western distribution of A. /eucopoda while on a round-trip through
By [Bavaria], BW [Baden-Wurttemberg], He [Hesse], Ni, NW [North Rhine-Westphal-
ia] and SH [Schleswig-Holstein]. Observations of E. Jansen [EJ] during 2012-2013
primarily covered BW, Sn and St. T. Kohler [TK] contributed observations from Br
and MV [Mecklenburg-West Pomerania] in 2013-2014, T. Pfannenstill [TP] and B.
Zimmer [BZ] from southern Br in 2013-2014, and A. Taeger [AT] from St in 2014.
Usually, presence and absence of A. /eucopoda on a study site was noted by ADL, EJ,
SMB, TK, but only presence was recorded by AT, BZ and TP. To determine presence or
absence, elms on randomly chosen sites were screened for feeding traces, larvae, cocoons
or imagines from late May to early October. The time spent searching for A. leucopoda
depended on patch size of an individual elm stand, usually varying from 2—5 minutes
for small bushes to 5—10 minutes for large trees. Usually, the number of signs of A. leu-
copoda was noted for a patch, but sometimes the search was stopped as soon as a single
sign was detected. ADL, BZ, SMB and TK also determined the elm species or cultivar
on the study site. The nomenclature of U/mus taxa follows Mackenthun (2010). Un-
less attributed to other recorders, the observations were made by the authors. Voucher
specimens of larvae and imagines from some localities as well as extensive photographic
documentation of occurrences are held at the Senckenberg Deutsches Entomologisches
Institut. Statistical analysis of the observation data follows Zéfel (1988).

As a contribution towards encouragement of ‘citizen science’, an attempt was
made to mobilize additional potential observers by placing an illustrated description
of A. leucopoda and its distinctive feeding traces in the German popular press, with an
appeal that observations be reported to the Senckenberg Deutsches Entomologisches
Institut in Miincheberg (Bartel 2013). Records sent by citizen scientists as photos or
herbarium vouchers were collected and re-identified by ADL and SMB.

For the outbreak area in Schlieben, Brandenburg, N. Neuenfeldt and TP assessed
the density of specimens hibernating in cocoons in the ground. Samples of soil and
leaf litter were taken from below three elm trees in December 2013. Each sample was
from a 5—10 cm deep plot of ca 0.40 m? area. Cocoons of A. leucopoda were extracted
from a mixed sample of ca 1.8 kg soil and litter and stored outdoors in a tent until
imagines emerged.

The distribution map was prepared from a draft map produced by Carto Fauna-
Flora 1.2 (Barbier and Rasmont 1996), and subsequently enhanced with Adobe Pho-
toshop® and Corel Draw®. Countries outside Germany with records of A. leucopoda are
labelled with the international vehicle registration codes. German states are labelled
with the acronyms explained above. Distribution data for Ulmus glabra and U. mi-
nor were obtained from FLORKART (BfN and NetPhyD 2013). Free use of these

data for the purpose of scientific analyses is licensed under the provisions of Creative

60 Stephan M. Blank et al. / Journal of Hymenoptera Research 41: 57-74 (2014)

Commons BY-NC-SA 3.0 DE. Only data sets with unambiguous identifications and
observation dates later than 1979 were used to display the contemporary distribution
of these elms, which have disappeared in some regions of Germany since 1980.

To estimate the speed of annual range extension it seems prudent to compare
a number of estimates based on different hypothetical dispersal scenarios. Based on
the known records, we measured the distance, A, between the earliest records from
Hungary and Poland (Blank et al. 2010) and the most distant observation sites in
Germany; B, between the closest neighbouring sites, where A. leucopoda was recorded
within the period of a few years; C, the minimum and maximum distances between the
records in Belgium (Boevé 2014) and the Netherlands (Mol and Vonk 2013) and the
closest observation sites in Germany known in 2013. The annual dispersal speed was
calculated from these distances and the related years of observation.

Results

Distribution of A. leucopoda in Germany

Through mid-July 2014 Aproceros leucopoda was recorded from the easterly German
federal states of Berlin (recorded from 8 study sites), Brandenburg (39), Mecklenburg-
West Pomerania (1), Saxony (5) and Saxony-Anhalt (2) and also from southeast Ba-
varia (5). These numbers also include data published by Kraus et al. (2012) and Sob-
czyk and Nuss (2014). At most localities, the presence of A. leucopoda was revealed by
the conspicuous ‘zig-zag’ feeding traces (Fig. 1) made by the young larvae. However,
older larvae or cocoons also drew attention to its presence, particularly later in the year.
Only very few imagines were observed in the field, although several were reared from
cocoons collected from the undersides of elm leaves.

The data on the presence and absence of A. leucopoda throughout Germany and in
the neighbouring countries are mapped in Fig. 3. Aproceros leucopoda was not found
on 140 study sites, which are distributed in the above mentioned as well as in more
western federal states of Germany (Fig. 3, blue crosses). The record by Pimpl (2014)
for the Erzgebirge in Saxony is based on a misidentification of Cladius rufipes Serville,
1823 (Tenthredinidae, re-identification by SMB). Currently, the following additional
records for Germany exist (sorted by federal state and ‘Landkreis’, a subdivision of a
German federal state):

Bavaria: Landkreis Deggendorf: Niederalteich NW 3 km, rest area “Seebach’ on
highway A3, 48.788°N, 13.011°E, 315 m alt., 07.08.2013, 3 larvae and feeding traces,
Ulmus sp. Landkreis Freyung-Grafenau: Irlesberg S 700 m, along federal highway B12,
48.720°N, 13.531°E, 425 m alt., 07.08.2013, 1 larva and feeding traces, U. minor.
Landkreis Regensburg: Worth SE, rest area “Tiefenthal’ on highway A3, 48.993°N,
12.420°E, 335 m alt., 07.08.2013, 1 larva and 5 feeding traces, U. sp.

Berlin: Friedrichshagen, environs of S-train station, 52.456°N, 13.625°E,
20.05.2013, numerous, partly late instar larvae, U. glabra; Kreuzberg, Columbiadamm,

Aproceros leucopoda: recent range extension, dispersal speed, larval hosts 61

-

Figure |. Feeding traces, with young larvae of Aproceros leucopoda, on leaf of Ulmus minor, Forstbotanischer
Garten in Eberswalde (Brandenburg). Photo: SDEI/Liston.

52.483°N, 13.401°E, 29.8.2013, feeding traces, U. “New Horizon’ (planted in 2007—
2009); Lichterfelde, Botanic Garden, Arboretum, 52.453°N, 13.305°E, 24.07.2013,
feeding traces, U. davidiana var. japonica, U. minor ‘Webbiana’ and U. sp. (not U.
laevis); Lichterfelde, Botanic Garden, Balkan section, 52.453°N, 13.305°E, 24.07.2013,
feeding traces, U. minor ‘suberosa’; Pankow, Marchenweg, along FliefSgraben,
52.576°N, 13.475°E, 10.08.2013, 1 feeding trace, U. minor; Pankow, Treskowstrafe,
52.561°N, 13.429°E, 11.08.2013, 2 feeding traces, U. ‘Rebona’; Wedding, intersection
of Tegeler StrafSe and Lynarstrafie, 52.540°N, 13.358°E, 24.07.2013, feeding traces,
U. pumila var. arborea; Wedding, Utrechter StrafSe, 52.548°N, 13.355°E, 14.8.2013,
feeding traces, U. pumila var. arborea.

Brandenburg: Landkreis Barnim: Biesenthal ESE, Griintal, Feldgehdélz, 52.740°N,
13.728°E, 16.07.2013, feeding traces, U. minor; Eberswalde, Forstbotanischer Garten,
52.825°N, 13.791°E, 30 m alt., 23.06.2013, 30 larvae, U. minor. Landkreis Dahme-
Spreewald: Brusendorf NW, rest area ‘Am Fichtenplan’ on highway A10, 52.315°N,
13.497°E, 50 m alt., 07.08.2013, 3 feeding traces, U/mus cultivar with smooth leaves,
slender crown form. Landkreis Elbe-Elster: Kolochau, federal highway B87 in direction of
Herzberg, 51.716°N, 13.281°E, 27.08.2013, numerous larvae, feeding traces and cocoons,
massive infestation, U. ‘Resista’ cultivar; Schlieben in direction of Herzberg, bicycle path

from Kolochau for 3 km length, 51.727°N, 13.312°E, 29.07.2013, 3 reared 2, numerous

62 Stephan M. Blank et al. / Journal of Hymenoptera Research 41: 57-74 (2014)

larvae, feeding traces and cocoons, massive infestation, U. ‘New Horizon’. Stadtkreis
Frankfurt/Oder: Frankfurt/Oder, Leipziger Strafse, Stidring Center, 52.328°N, 14.521°E,
05.09.2013, 2 cocoons and feeding traces, 1-5% damage observed on 39 of ca 100 U.
‘Resista’ trees. Landkreis Havelland: Markisch Luch SW, 52.560°N, 12.602°E, 30 m alt.,
10.08.2013, 1 eonymph, U. cultivar planted as alley along street; Tremmen, 52.533°N,
12.8167°E, 06.09.2013, weak infestation on U. “New Horizon’ (planted 2010) and U.
‘Rebona’ (planted 2009). Landkreis Markisch-Oderland: Gabow N, 52.820°N, 14.071°E,
14.07.2013, 4 larvae, U. minor, Hoppegarten E, Berliner Chaussee, 52.496°N, 14.058°E,
20.05.2013, 15 leaves with feeding traces, 10 early instar larvae, U. glabra; Jahnsfelde,
52.507°N, 14.228°E, 19.05.2013, 6 leaves with feeding traces, 3 early instar larvae, U.
glabra; Miincheberg, car-park of Netto supermarket, 52.506°N, 14.133°E, 18.07.2013,
feeding traces, U. cultivar (‘Columella’?); Miincheberg, railway station, 52.524°N, 14.102°E,
04.07.2013, 3 feeding traces, U. glabra; Miincheberg, Waschbanksee, 52.502°N, 14.139°E,
14.07.2013, 5 feeding traces, cultivated U. cultivar (‘Sapporo Autumn Gold’, ‘New
Horizon’ or ‘Rebona’?); same site, 15.07.2013, 2 larvae, cultivated U. sp.; Miincheberg,
ZALF campus, 52.515°N, 14.115°E, 07.06.2013, 12 swept from U. glabra; same site,
04.07.2013, 2 larvae, U. glabra; same site, 20.06.2014, 4 larvae, U. glabra; Podelzig,
entrance of road to railway station, 52.482°N, 14.538°E, 30.07.2013, 10 feeding traces,
U. minor, Steinhéfel, alley, 52.400°N, 14.167°E, 30.08.2013, feeding traces, U. ‘Resista’
(planted ca 2008); Waldsieversdorf 2 km SW, road in direction of Rotes Luch, 52.523°N,
14.039°E, 14.08.2013, 1 feeding trace, U. glabra. Landkreis Oberhavel: Borgsdorf, S of
church, 52.704°N, 13.248°E, 25.06.2014, feeding traces, U. minor; Borgsdorf, W of quarry
pond, 52.704°N, 13.226°E, 25.06.2014, U. glabra; Liebenberg, Fichten, rest area of federal
highway B167, 52.890°N, 13.267°E, 14.07.2013, 1 feeding trace, U. glabra; Oranienburg,
Berliner StrafSe, 52.723°N, 13.250°E, 26.07.2013, feeding traces, U. glabra; Oranienburg,
Berliner StrafSe, in front of Poliklinik, 52.742°N, 13.239°E, 23.07.2013, feeding traces,
U. ‘New Horizon’; Oranienburg, HolbeinstrafSe, 52.725°N, 13.248°E, 20.07.2013, 3
leaves with feeding traces, U. minor (2 m high shoots growing from roots); Oranienburg,
IdenstrafSe, 52.771°N, 13.249°E, 23.07.2013, larva and several feeding traces, U. ‘Regal’;
Zehlendorf, W and S of clay pit, 52.799°N, 13.380°E, 20.07.2013, 1 cocoon, U. minor
(U. glabra and U. laevis growing nearby not infested). Landkreis Oberspreewald-Lausitz:
Calau SW 6 km, rest area on highway A13, 51.700°N, 13.899°E, 135 m alt., 01.08.2013,
feeding traces, two Ulmus cultivars (possibly sorts of Resista due to the narrowly cone-
shaped crown). Landkreis Oder-Spree: Beeskow, alley, 52.174°N, 14.247°E, 30.08.2013,
feeding traces, U. ‘Resista’ (planted 2007); Fangschleuse, S of railway station, 52.402°N,
13.825°E, 20.05.2013, 2 leaves with feeding traces, U. glabra; Kagel, along road L 323,
52.467°N, 13.917°E, 04.09.2013, 2 young larvae and feeding traces, U. ‘Resista’ (planted
2010). Landkreis Teltow-Flaming: Ahrensdorf near Ludwigsfelde, 52.317°N, 13.200°E,
01.10.2013, feeding traces, U. “Rebona’, observed by K. Langner; Ahrensdorf, alley along
street K 7220, 52.195°N, 13.172°E, 02.09.2013, heavy infestation, of 22 Ulmus trees
(planted ca 2008), late instar larvae still present on 01.10.; Blankenfelde SW 4 km, rest
area on highway A10, 52.308°N, 13.369°E, 30.06.2013, 4 feeding traces of early instar
larvae, U. glabra; Dahlewitz, Friedhofsweg, 52.319°N, 13.436°E, 7.9.2013, feeding traces

Aproceros leucopoda: recent range extension, dispersal speed, larval hosts 63

on 2 leaves, U. minor, Lowendorf, Martensmiihle, 52.204°N, 13.184°E, 27.08.2013,
larvae and feeding traces, U. sp.; Zossen-Neuhof, Cottbuser StrafSe, 52.144°N, 13.479°E,
29.08.2013, 2 feeding traces, U. sp. Landkreis Uckermark: Prenzlau, Seeliibber Weg,
53.299°N, 13.879°E, 11.08.2013, 3 feeding traces, U. glabra; Schénermark, railway
station, 53.106°N, 14.033°E, 11.08.2013, 2 feeding traces, U. glabra.

Mecklenburg-West Pomerania: Landkreis Mecklenburgische Seenplatte: Neustre-
litz, intersection of Strelitzer Strafe and BiirgerhorststrafSe, 53.357°N, 13.072°E,
27.08.2013, feeding traces, U. “New Horizon’.

Saxony: Landkreis Leipzig: Leipzig, Leipziger Auen, WeifSe Briicke, 51.303°N,
12.356°E, 125 m alt., 27.06.2014, 2 feeding traces, U. sp.; Leipzig-Riickmarsdorf,
Bienitz, 51.353°N, 12.252°E, 120 m alt., 22.06.2014, 3 feeding traces, U. sp. Land-
kreis MeifSen: Wildberg, 51.100°N, 13.588°E, 120 m alt., 01.08.2013, 2 larvae, U. sp.
(glabra or minor). Landkreis Nordsachsen: Kathewitz, nature reserve ‘Alte Elbe Kath-
ewitz, 51.516°N, 13.111°E, 85 m alt., 22.07.2014, more than 50 U/mus controlled,
but only 2 feeding traces of early instar larvae found; Schkeuditz, nature reserve “Lup-
peaue’, 51.381°N, 12.252°E, 100 m alt, 13.06.2014, 19 and 2 feeding traces, U. sp.

Saxony-Anhalt: Landkreis Aschersleben-Stafsfurt: Westeregeln, 51.960°N,
11.386°E, 06.07.2014, feeding traces, U. sp. Landkreis Saalkreis: Sietzsch E, rest area
‘Kapellenberg’ on highway A9, 51.492°N, 12.204°E, 110 m alt., 07.08.2013, 2 feed-
ing traces, U. minor.

The altitudinal range of the 66 study sites in Germany where A. leucopoda was
observed, varies from 20-425 m above sea level (elevation determined using Google
Earth where no original data were available). 51 observations were made below 100 m
altitude. These comprise most of the data from Berlin, Brandenburg, Mecklenburg-
West Pomerania and Saxony-Anhalt. All five records from Bavaria were at over 300 m
altitude. In Austria, A. /eucopoda was found between 160-580 m altitude (Blank et al.
2010; E. Altenhofer, unpublished data).

The press release by Senckenberg, requesting observations of A. leucopoda from citi-
zen scientists (Bartel 2013), was published in more than 300 print and online media
primarily in Germany, but also in neighbouring German-speaking countries. During
the following months, 23 persons responded by contacting ADL and SMB. Observa-
tions by three persons (among them TK and TP) were actually of A. leucopoda, whereas
those of 20 persons related to other insects, plant species other than elms, or were am-
biguous. As a result of the press release we were able to include 17 additional sites in this
study, including the report of the severe outbreak in Schlieben and the most northern
occurrence in Mecklenburg-West Pomerania, together with observations made on 13
elm species and cultivars, of which five were previously unrecorded as hosts.

Infestation of elm species and cultivars

At several localities all three Ulmus species which are autochthonous to Germany were
present. Where A. leucopoda was found at such places, it was more abundant on U. minor

64 Stephan M. Blank et al. / Journal of Hymenoptera Research 41: 57-74 (2014)

Table |. Infestation of elm species, varieties and cultivars by Aproceros leucopoda: Number of study sites
in Germany with [+] or without [-] larvae, larval feeding traces or cocoons attached to the tree. Observa-
tions from 2011-2014. Only unambiguously identified elm species, varieties and cultivars are listed. The

cultivars “New Horizon’, ‘Rebona’ and ‘Regal’ belong to the ‘Resista’ series.

Species or sort of elm
Ulmus crassifolia
Ulmus davidiana vat. japonica

N

Ulmus glabra 36
Ulmus glabra ‘Pendula
Ulmus x hollandica

Ulmus laevis

21
Ulmus lamellosa

Ulmus minor

Ulmus minor vat. suberosa

Ulmus minor ‘Webbiana
Ulmus minor ‘Wredev
Ulmus multinervis
Ulmus ‘New Horizon

Ulmus parvifolia

Ulmus pumila var. arborea
Ulmus ‘Rebona
Ulmus ‘Regal’

Ulmus ‘Resista’

—

than on U. glabra. Also the total number of observation sites with infestations on U. minor
is significantly higher than that on U. glabra (chi-squared test, n = 71 records including
varieties and cultivars [Table 1], y? = 7.79, p < 0,01). Despite careful searches of U. laevis,
no feeding traces or larvae were found. A very few feeding traces were seen on a single elm
labelled “U. /aevis” in Berlin Botanic Garden growing near other specimens under the
same name which bore no traces. However, the tree with the feeding traces possessed some
characters which are not typical for U. laevis, so there is doubt about its identity.

Aproceros leucopoda was found on several occasions feeding on Resista® elms. These
cultivars have not previously been recorded as hosts. No clear pattern of difference in
abundance of A. leucopoda was observed amongst these cultivars, of which three were
identified as U. “New Horizon’, U. ‘Regal’ and U. ‘Rebona’. U/mus minor ‘Webbiana’
and U. minor var. suberosa were recorded as new hosts for A. leucopoda, and U. davidiana
vat. japonica (previous records only from Japan) and U. pumila var. arborea (previous
records only from Hungary) were confirmed as hosts (Table 1). No signs of feeding were
found on U. crassifolia, U. glabra ‘Pendula’, U. lamellosa, U. x hollandica, U. multinervis
and U. parvifolia, nor on Zelkova species (Ulmaceae) partly growing close to Ulmus.

At most localities, comparatively low population levels were found, with insig-
nificant damage to the hosts. Elms at such localities were at the edges of woodland
or within areas of human settlement, i.e., in more or less sheltered positions. Serious

Aproceros leucopoda: recent range extension, dispersal speed, larval hosts 65

es
oa in
ed
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a ew 2 y

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ns

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i
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Figure 2. Feeding damage caused by Aproceros leucopoda on planted Ulmus ‘Resista’ during an outbreak
between Schlieben and Kolochau (Brandenburg). Photo: LELF/Pfannenstill.

defoliation has so far been recorded in Germany only at Schlieben (Brandenburg,
Landkreis Elbe-Elster). Surrounded by open agricultural areas, 235 trees of U. ‘New
Horizon’ were planted here as a three kilometre long avenue along a road and a bicycle
path in 2012. The trees originated from a nursery in the state of Schleswig-Holstein.
Aproceros leucopoda could neither be observed in this particular nursery (A. Frers, per-
sonal communication) nor at other sites in this state. This outbreak was first detected in
2013 but the infestation was much less severe in 2014. In 2013, damage was unevenly
distributed within the plantation. Many trees suffered severe damage, ranging from
partial defoliation of twigs to defoliation of most of the crown (Fig. 2). 35 solid-walled

66 Stephan M. Blank et al. / Journal of Hymenoptera Research 41: 57-74 (2014)

er ve :
2013 aye

NL °
2008 ©.
Warsaw

2003
Sandomierz
Basin

Aproceros leucopoda
® present
x absent
Ulmus glabra, U. minor
s:present after 1979

Figure 3. Distribution of Aproceros leucopoda in Germany, through 15.07.2014. Modified from Blank et
al. (2009), including additional data for Austria (own data, Kraus et al. 2011), Belgium (Boevé 2013), the
Czech Republic (own data, Juraskova et al. 2014), Germany (own data, Kraus et al. 2012, Pimpl 2014,
Sobczyk and Nuss 2014), Hungary (Haris 2010) and the Netherlands (Mol and Vonk 2013). Distribution
of Ulmus glabra and U. minor in Germany after BN and NetPhyD (2013). German states are labelled with
the abbreviations used in the checklist of the sawflies of Germany (Blank et al. 2001): Br — Brandenburg
and Berlin, By — Bavaria, BW — Baden-Wurttemberg, He — Hesse, MV — Mecklenburg-West Pomera-
nia, Ni — Lower Saxony (Niedersachsen), NW — North Rhine-Westphalia, RP — Rhineland-Palatinate,
SH — Schleswig-Holstein, SL — Saarland, Sn — Saxony, St — Saxony-Anhalt, Th — Thuringia. Countries
outside Germany where A. /eucopoda is recorded are labelled with the international vehicle registration

codes. Graphics: SDEI/Blank.

cocoons were separated from a mixed sample of soil and litter taken from below three
elm trees. A density of ca 29 cocoons/m? for overwintering specimens is calculated for
this outbreak site. In spring 2014, eight females emerged between April 8—25 under
outdoor conditions. A less severe outbreak occurred in Frankfurt/Oder (Brandenburg)
in 2013, where 1—5% defoliation was observed on 39 of ca 100 U. ‘Resista’ trees.

Dispersal distances and invasion speed of Aproceros leucopoda

In Europe A. leucopoda was first found in 2003 in the Sandomierz Basin of southeastern
Poland and in Dejtar, northern Hungary (Blank et al. 2010). The following estimates of
the invasion speed are based on the distances between presumed sources of subsequent

Aproceros leucopoda: recent range extension, dispersal speed, larval hosts 67

dispersal represented by the earliest recorded Hungarian and Polish localities and the
sites most distant from these where A. leucopoda has been observed in Germany:

e Sandomierz Basin (2003) to the most western recorded site, Westeregeln in Saxo-
ny-Anhalt (2014): distance 740 km, invasion speed ca 70 km/yr;

¢ Sandomierz Basin (2003) to the most northern recorded site, Neustrelitz in Meck-
lenburg-West Pomerania (2013): distance 660 km, invasion speed ca 65 km/yr;

e Dejtar (2003) to the most southeastern recorded site, Passau in Bavaria (2011)
(Kraus et al. 2012): distance 440 km, invasion speed ca 55 km/yr.

In the following cases the annual speed of invasion is calculated from the distance
between the closest neighbouring sites, where A. /eucopoda was recorded only a few
years later:

e Warsaw in Poland (2008) (Blank et al. 2010) to the closest recorded German site,
Podelzig in eastern Brandenburg (2013): distance 450 km, invasion speed ca 90 km/yr;
¢ St. Pdlten in Austria (2009) (Blank et al. 2010) to the most southeastern recorded
German site, Passau in Bavaria (2011): distance 170 km, invasion speed ca 85 km/yr;
¢ from the most southern recorded Bavarian site near Passau (2011) to the most
northern recorded Bavarian site, near Worth (2013): distance 90 km, invasion

speed ca 45 km/yr.

In 2013 A. leucopoda was observed for the first time in Belgium (Boevé 2014) and
the Netherlands (Mol and Vonk 2013). The following are the minimum and maxi-
mum distances between these sites and the closest German records known in 2013:

¢ Overijssel in the Netherlands to Sietzsch in Saxony-Anhalt, Germany: 360 km;
¢ Hoeilaart in Belgium to Worth in Bavaria, Germany: 610 km.

Discussion and conclusions

Among the native elm species of Germany, Aproceros leucopoda clearly prefers Ulmus
glabra and U. minor as larval hosts (Table 1), since no feeding has been observed on
U. laevis. On a mixed stand of all three elm species in Lower Austria (Traismauer),
U. laevis showed a very low infestation even during an outbreak of A. leucopoda (E.
Altenhofer, personal observation). A number of additional elm species and cultivars
must now be considered to be larval hosts. These were introduced to Germany as or-
namental trees in horticulture, for afforestation, or planted in botanical gardens for
scientific purposes. Feeding could not so far be observed on seven of the taxa listed
in Table 1. However, in these cases, it would be premature to conclude that they are
not potential hosts, because each of these species and cultivars was studied at only a
single site.

68 Stephan M. Blank et al. / Journal of Hymenoptera Research 41: 57-74 (2014)

Some of the Resista® hybrid elms now prove to be suitable hosts. These cultivars, of
complex hybrid parentage, were created to meet the demand for elms which are resist-
ant to the fungal diseases commonly referred to collectively as “Dutch elm disease”.
Ulmus ‘New Horizon’ and U. ‘Regal’ are at present respectively the most often and the
second most often planted elms of this sort in Germany (Mackenthun 2010). They
are usually planted in settings where they are highly visible to the public, such as along
roads and in city parks. Aside from possible effects on the health of the affected trees,
defoliation by A. /eucopoda will impair their aesthetic value. That “New Horizon’ and
‘Regal’ are acceptable hosts to A. leucopoda is not surprising, because U. pumila and
U. japonica figure prominently in the parentage of both (Mackenthun 2010). Ulmus
pumila is known to be highly susceptible to attack by A. leucopoda (e.g., Wu 2006,
Blank et al. 2010, Cao et al. 2011), whilst U. japonica is a known host in Japan (Blank
et al. 2010) and recorded here for the first time as a host in Europe.

The range of A. leucopoda in Germany currently comprises two separate areas
(Fig. 3). The northern one extends from southern Mecklenburg-West Pomerania in
the north to central Saxony in the south and from central Saxony-Anhalt in the west
to the Polish border in the east. The second, southern area covers part of southeast Ba-
varia. [hese two large areas of occurrence do not at present appear to be confluent. The
distribution of U. glabra, one of the two preferred native elm species, covers the low
mountain ranges of central Germany (Bf£N and NetPhyD 2013). Although autochtho-
nous U. glabra and U. minor have disappeared in several regions (BfN and NetPhyD
2013), their combined, largely continuous distribution throughout Germany (Fig. 3)
provides the opportunity for A. /eucopoda to spread further into more westerly parts
of the country.

The northern distribution area of A. leucopoda in Germany is mostly within the
North German Plain, which in the south is delimited by the low mountain ranges of
central Germany. Judging from available distribution data (Blank et al. 2010, Mol
and Vonk 2013, Boevé 2014, Sobczyk and Nuss 2014, Juraskova et al. 2014, present
data), A. leucopoda has been recorded only rarely above 400 m altitude in central Eu-
rope. From Austria into Bavaria, A. leucopoda has spread along the valley of the river
Danube, where A. leucopoda was found at a maximum altitude of 580 m near Zwettel,
Lower Austria (E. Altenhofer, personal communication). The Alps to the south and
the Bohemian Massif to the north of the valley possibly work as barriers. Future ob-
servations may reveal whether the low mountain ranges of central Germany will slow
down or restrict the dispersal of A. /eucopoda, despite the general presence there of at
least U. glabra.

Apart from range expansion through self-dispersal of imagines, it seems likely that
individuals can sometimes be accidentally transported by human agency over much
greater distances with road, rail, air and canal traffic (Blank et al. 2010). Trade by
nurseries of infested plants throughout a wide geographic area might also have a sig-
nificant impact, but we could not observe such an event involving A. leucopoda. The
occurrences in Belgium (Boevé 2014) and in the Netherlands (Mol and Vonk 2013)
seem likely to belong in the category of human-mediated jump dispersal (Suarez et al.

Aproceros leucopoda: recent range extension, dispersal speed, larval hosts 69

2001), because the gap of 360-610 km between these western records and the records
in eastern Germany was unsuccessfully searched by us for signs of A. leucopoda in 2012
and 2013 (Fig. 3). Contrarily, the two observed distribution areas in Bavaria and in
the northeastern German states should be explained by self-dispersal of A. leucopoda
originating from the neighbouring countries Austria, Poland and possibly the Czech
Republic, although human-mediated jump dispersal cannot be ruled out as a compo-
nent within self-dispersal. Records made during consecutive years in Austria indicate
a stepwise spread in a westerly direction (Fig. 3). Although comparable data from
western Poland are missing, we suppose that self-dispersal also took place here, because
the speeds of annual dispersal calculated from the distance between the Polish and the
eastern German records (65-90 km/yr) are similar to speeds calculated from Austrian,
Hungarian and Bavarian records (45—85 km/yr). The common distribution area of the
preferred native larval hosts, U. glabra and U. minor, is more or less continuous from
Germany to Hungary and to Poland (Meusel et al. 1965, BfN and NetPhyD 2013),
which has facilitated the self-dispersal of A. leucopoda in a westerly direction.

The 2013 observations from southeastern Bavaria indicate an apparently limited
speed of range extension (45 km/yr) in that area since A. leucopoda was first recorded
near Passau in 2011 (Kraus et al. 2012), although the total of study sites in Bavaria is
comparatively low. Contrastingly, range expansion into northeastern Germany seems
to have been both more rapid and extensive. At the majority of German localities, a
low number of feeding traces made by young larvae were often the only signs that the
species was present, perhaps indicating that colonisation had recently taken place. The
inconspicuous damage may also have been a reason for the low number of replies by
citizen scientists in response to our press release in 2013 (Bartel 2013). If the spread of
A. leucopoda into eastern Germany is nevertheless assumed to have depended purely
on natural dispersal of imagines, the distance (ca 220 km) between the most westerly
recorded locality (Westeregeln) and the Polish border (Podelzig) indicates that the first
female may already have arrived in northeastern Germany two to five years before 2013.

Very little is known about the dispersal ability of sawflies and horntails (Hyme-
noptera ‘Symphyta’) in general, or the time scales and distances associated with the
spread of individual species undergoing range expansion. The speed of annual range
expansion resulting from self-dispersal of 45-90 km/yr estimated here for A. leucopoda
lies within the range known for a few sawflies and for other insects. Nematus oligospilus
Forster, 1854 (Tenthredinidae), a sawfly species invasive to New Zealand with larvae
feeding on willow, extended its range through the North Island at 300 km/yr (Charles
and Allan 2000; ca 165 km/yr measured as a straight line). In South America Ovruski
and Fidalgo (1991) observed a range expansion of 300 km/yr also for NV. desantisi D.R.
Smith, 1983, which might be conspecific with NV. oligospilus from New Zealand (Koch
and Smith 2000). Ovruski and Fidalgo (1991) supposed passive transport to be a pos-
sible component of the dispersal. Gilpinia hercyniae (Hartig, 1837) (Diprionidae) is
invasive to the Nearctic, where its larvae damage spruce trees (Picea spp.). The speed of
range expansion in Canada is given as 50 km/yr (CABI 2014). The average speed for
Sirex noctilio Fabricius, 1793 (Siricidae), a woodwasp invasive in South America, has

70 Stephan M. Blank et al. / Journal of Hymenoptera Research 41: 57-74 (2014)

been estimated as 30-50 km/yr (Yemshanov et al. 2009). Smith (1996) summarized
distribution data for the invasive Asian woodwasp Eriotremex formosanus (Matsumura,
1912), which in the United States was first observed in southern Georgia and in north-
ern Florida in 1974. E. formosana was found 15 years later in southeastern Virginia,
about 740 km distant from these earliest sites (ca 50 km/yr) and 16 years later in east-
ern Texas, 990 km distant (ca 60 km/yr). However, S. noctilio and E. formosanus differ
greatly from the Aproceros, Gilpinia and Nematus species in several ways, e.g., in the
large body and the larval feeding habit inside solid wood. Sirex noctilio reproduces sex-
ually and usually produces at most one generation per year (Eichhorn 1982), whereas
E. formosanus is apparently parthenogenetic in the US and supposedly has two genera-
tions per year, based on phenological data (Smith 1996). Compared to the range ex-
pansion of 30-60 km/yr resulting from self-dispersal of these woodwasps, not even the
highest estimated speed of 90 km/yr for A. leucopoda seems excessive, because several
life traits of A. leucopoda promote rapid dispersal: it reproduces parthenogenetically,
has up to four generations per year, and the larvae are external feeders on leaves (Blank
et al. 2010), which appear more nutritious than wood infested by fungi. Among insects
other than Hymenoptera, Brown et al. (2008) calculated an invasion speed of 58-145
km/yr for Harmonia axyridis (Pallas, 1771) (Coleoptera, Coccinellidae) in Europe.
The considerably higher speed of 500 km/yr estimated for this species in South Africa
(Stals 2010) probably includes jump-dispersal events. The speed of range expansion in
Cameraria ohridella Deschka & Dimié, 1986 (Lepidoptera, Gracilariidae) in central
and western Europe was estimated to be 60-70 km/yr based on the dates of first ob-
servations in European countries (Serfova and Lagtivka 2001), although these authors
also cite much lower speeds for other moths. For C. ohridella both active dispersal and
passive transport by wind and man were considered to play a role.

The rapid range expansion of A. /eucopoda throughout Europe predicted by Blank
et al. (2010) is evidently taking place, and likely to progress. Although occurrences in
Germany have so far seldom resulted in severe defoliation, this may only be because
population levels still have not peaked. The considerable differences in climate between
the European territories which it has already colonised, together with the altitudinal
range inhabited by the species, suggest that it should easily be able to spread through
most of Europe where elms grow (Meusel et al. 1965). Whether it is possible in the
long-term to exclude it from territories such as the British Isles or Scandinavia, which
may be adequately protected by the sea from self-dispersal events, remains to be seen.

Acknowledgements

For the communication of additional observations we are grateful to Ewald Altenhofer
(Etzen), Antje Frers (Ellerhoop), and Katrin Langner (Ludwigsfelde). Marko Prous
(Miincheberg) assisted ADL and SMB with fieldwork. David R. Smith (Washington)
quickly supplied the missing copy of Ovruski and Fidalgo (1991). Gordon Mackenthun
(Leipzig) kindly helped with the identification of some elm specimens. The volunteers

Aproceros leucopoda: recent range extension, dispersal speed, larval hosts 71

contributing to the Flora of Germany as well as the Bundesamt fiir Naturschutz and
the Netzwerk Phytodiversitaet Deutschland are acknowledged for freely providing
distribution data of the elms in Germany. Thomas Schmitt (Miincheberg), Marko
Prous, David R. Smith, and an anonymous referee checked earlier versions of the
manuscript and helped to improve it.

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