The recent increase in the number of non-native species
of insects being introduced into Europe and their spread,
caused by worldwide human travel and trade, has result-
ed in serious problems throughout Europe, including the
Czech Republic. The most well-known examples of in-
vasive species include Cameraria ohridella Deschka &
Dimic, 1986 (Lepidoptera: Gracillariidae) and Harmonia
axyridis (Pallas, 1773) (Coleoptera: Coccinellidae), which
have had a negative effect on horse chestnut trees and the
diversity of local ladybird beetle faunas in the countries in-
vaded, respectively (Percival et al., 2011; Vilcinskas et al.,
da (Takeuchi, 1939) was introduced into Europe, which re-
sulted in outbreaks of this species and extensive defoliation
of elms in some parts of South and Central Europe (Blank
et al., 2010; Zandigiacomo et al., 2011; Seljak, 2012). Here
ZH UHSRUW DQRWKHU QRQQDWLYH VSHFLHV RI VDZÀ\ WKDW KDV
Smith, 1974, which locally has become a pest of the orna-
mental azalea, Rhododendron molle, planted in parks and
gardens in certain locations in the Czech Republic.
Nematus lipovskyi is a member of the subfamily Nemati-
species worldwide, of which about 550 occur in Europe
(Taeger et al., 2010; Taeger & Blank, 2011). The mostly
free-feeding larvae are usually monophagous or oligopha-
gous on various trees, herbaceous plants and grasses.
Nematus lipovskyi was described by Smith (1974) from
females reared from swamp azalea (Rhododendron molle).
The type series consists of specimens from the following
US states: Massachusetts, New Jersey, Pennsylvania, Ala-
bama, Maryland, Maine, New Hampshire and Virginia. Ac-
cording to some references (Johnson & Lyon, 1991; Boggs
et al., 2000; Cranshaw, 2004) it is apparent that N. lipov skyi
is widely distributed in the eastern part of the USA, where
it is a familiar pest of ornamental deciduous species of Rho-
dodendron (Azalea), both native (such as R. calendulace-
um and R. viscosum) and introduced (R. molle from China
and Japan). In addition to Nematus lipovskyi, there are two
plants: Amauronematus azaleae Marlatt, 1896 (Tenthredi-
nidae, Nematinae) and Arge azaleae Smith, 1989. Outside
UKRGRGHQGURQVDZÀ\ EHORQJLQJ WRWKH IDPLO\ $UJLGDH LQ
Quanzhou City in China (Zheng & Chen, 2011), possibly
Arge similis (Snellen van Vollenhoven, 1860) (D. Smith,
pers. comm.). In the Czech Republic, Nematus lipov skyi
foliating Rhododendron molle in Charles University Bo-
tanic Garden in Prague. Due to a failure to rear the species,
collected directly from rhododendron shrubs. In spite of
the larvae being relatively well-known, they have not pre-
viously been described and the males are unknown. There-
fore, both larvae and males are described here. In addition,
the current status of this species’ occurrence in the Czech
Republic based on the preliminary results of a preliminary
monitoring project carried out by the Charles University
Faculty of Science and the State Phytosanitary Administra-
tion (hereafter abbreviated as SPA) (Kapitola & Pekárko-
vá, 2013), is also presented. Furthermore, an account of the
bionomics of the local population of N. lipovskyi in Charles
Eur. J. Entomol. 112 (1): 180–186, 2015
ISSN 1210-5759 (print), 1802-8829 (online)
JAN MACEK1 and PETR ŠÍPEK2
.H\ZRUGVHymenoptera, Tenthredinidae, Nematus lipovskyi, Czech Republic, Europe, Rhododendron molle, R. luteum, invasive
species, morphology, bionomics, dispersal, pest species, horticulture
$EVWUDFW$QHZQRQQDWLYHVSHFLHVRIVDZÀ\Nematus lipovskyi Smith, 1974, previously known only in the USA, has heavily infested
the ornamental azalea plant, Rhododendron molle, in the Czech Republic since at least 2010. The data on this species in the USA is
EULHÀ\VXPPDUL]HG7KHODUYDDQGKLWKHUWRXQNQRZQPDOH DUHQHZO\GHVFULEHG DQGLOOXVWUDWHG7KH OLIHF\FOHLVGHVFULEHGEDVHGRQ
LQFOXGHWKH¿UVWUHFRUGRID(XURSHDQVSHFLHVRID]DOHDRhododendron luteum). The current distribution of Nematus lipovskyi in the
Czech Republic based on the results of a preliminary monitoring project carried out by Charles University in Prague and the State
Phytosanitary Administration is presented. The pathways of its introduction and spread, potential phytosanitary measures and its effect
tion. Field observations on the occurrence, oviposition behaviour
and level of damage caused by N. lipovskyi in Charles University
Botanic Garden were carried out by P. Šípek, who also took pho-
tographs of living specimens and the damage to the host plants.
Voucher specimens of both larvae and adults are deposited in the
insect collection at the Department of Entomology, National Mu-
seum, Prague; photographs are kept in Charles University Fac-
ulty of Science photograph gallery archive. The distribution map
(Fig. 4) was prepared from a draft map produced by SPA and
vector maps were downloaded from http://www.vecteezy.com/.
For light microscopy of the collected material (Figs 1–2) a series
Samples of both adults and larvae (approx. 200 adults and 300
larvae) were collected from Charles University Botanic Garden
by one of the authors (PŠ), other samples of larvae were collected
at various locations throughout the Czech Republic by SPA in-
spectors (Kapitola & Pekárková, 2013). All material was submit-
tional Museum in Prague. Distribution records are supplemented
with the respective faunistic grid number of the grid mapping sys-
tem of Central Europe (Ehrendorfer & Hamann, 1965; Pruner &
Míka, 1996). Taxonomic analysis was carried out using standard
entomological procedures for morphological diagnostics. This
Fig. 1. Nematus lipovskyi Smith, 1974, adult: a – female; b – male; c – ovipositor (lateral view); d – female abdomen (apical part,
dorsal view); e – lancet; f – penis valva. Scales: a, b – 5 mm; c, e, f – 0.3 mm; d – 12 mm.
of digital photographs was taken with an OLYMPUS DP camera
attached to an OLYMPUS SZX microscope. Composite images
with an extended depth of focus were created using the software
CombineZP and subsequently processed using other graphic pro-
grammes. The other images were taken with various standard
cameras. Morphological terminology used in the descriptions fol-
lows that of Viitasaari (2002).
Nematus lipovskyi 6PLWK
'HVFULSWLRQ $GXOW. Female (Fig. 1) was described by
Smith (1974) who also provided illustrations of the ovi-
positor sheath and lancet.
Male (Fig. 1): Length: 4.5–5 mm. Yellow-orange with
DQWHQQDHODUJH VSRW RQIURQWDO ¿HOGH[WHQGLQJ DV IDUDV
frontal pit and antennal socket), mesonotum and metano-
tum, dorsal and ventral part of mesopleuron, metapleuron,
proximal half of metacoxa, all terga except narrow stripes
on posterior margins and laterotergites, black.
Head. Alutaceous, with short, dense, pale pubescence;
in dorsal view transverse with temples parallel and round-
ed posteriorly; postocellar area slightly convex, twice as
wide as long, lateral postocellar furrows short, slightly
depressed, parallel; OOL : OOC : POL = 1 : 1 : 0.9; fron-
WDO¿HOGÀDW ZLWK LQGLVWLQFWIURQWDOULGJHIURQWDOSLWGHHS
ginate anterior margin; malar space as long as diameter of
anterior ocellus; antenna distinctly longer than head and
WKRUD[ FRPELQHG UHODWLYH OHQJWKV RI ÀDJHOORPHUHV ±
about 0.95 : 1 : 1 : 0.75 : 0.70 : 0.63 : 0.63.
Thorax. Median mesoscutal lobe shiny in middle with
shallow scattered punctures, alutaceous anteriorly; median
mesoscutellar groove arc-shaped and narrow; lateral meso-
scutal lobes covered with dense shallow punctures with
alutaceous interspaces; mesoscutellum slightly convex,
¿QH SXQFWXUHV PHVRVFXWHOODU DSSHQGDJH ZLWK GLVWLQFW
deep punctures; metascutellum smooth, shiny; legs with
metatarsus a little shorter than metatibia, metabasitarsus as
long as three following tarsomeres combined; inner tibial
spur of metatibia a little shorter than half of metabasitarsus,
claws with small inner tooth.
Abdomen. Cylindrical with apex rounded posteriorly,
tion; genitalia as in Fig. 1.
9DULDELOLW\ 1R VLJQL¿FDQW YDULDWLRQ LQ WKH PDWHULDO
/DVWLQVWDU IHHGLQJ ODUYD (Figs 2, 3c). Body length
9–10 mm. Head greyish-green; entire head covered with
setae, labrum with four setae; mandibles with one seta,
stipes without setae, palpifer with three setae; second seg-
ment of maxillary palps with one small seta; prementum
with two very short setae, second segment of labial palp
with one short seta; body in upper part green, in lower part
paler; cuticle smooth and shiny, spiracles narrow; all tho-
racic segments with a pair of large dorsal lobes with long
setae, trochanter shorter than femur, with scattered long
hair-like setae, tibia longer than tarsus with ten hair-like se-
tae; abdominal segments with six annulets, annulets three,
SUHFHGLQJ DQQXOHW ¿UVW VHFRQG DQG IRXUWK DQQXOL ODUJH
convex dorsally; subspiracular, second postspiracular and
surpedal lobes prominent with ring-like spots surrounding
setal bases; second annulet with six, fourth annulet with
second postspiracular lobe with two long cylindrical setae,
ninth abdominal segment with two short conical protuber-
ances, suranal and subanal lobes with long hair-like setae,
basal parts of prolegs with black spots, covered with scat-
tered long hair-like setae.*
%LRQRPLFV This species is univoltine. Adults were
observed from the end of April to the beginning of May
2013, with a peak between 22–24 April. However the
be prolonged from mid-April to mid-May. The tempera-
WXUHVGXULQJ SHDNÀLJKW GD\V ZHUHDV IROORZVPLQLPXP
temperature 5°C, maximum day temperature 22°C, mean
KRVWSODQWV'XULQJ WKH ÀLJKW SHULRGPDVVVZDUPLQJZDV
low pitfall traps (on the ground) or yellow sticky plates in
but some 10 male individuals were collected attached to
the sticky covers of R. obtusum buds a few days later. Dur-
LQJWKH ÀLJKW SHULRGIHPDOHV ZHUH REVHUYHGOD\LQJHJJV
in the central vein of young leaves in bursting buds (Fig.
3). Oviposition was preceded by thorough inspection of
the bud. Young larvae hatched within 7–10 days of ovi-
from the preceding instars, which are characterized by the presen-
ce of prominent black setiferous pinnacles on the dorsal parts of
thorax and abdomen.
Fig. 2. Nematus lipovskyi Smith, 1974, last feeding larval in-
star preserved in alcohol (discolored): a – habitus (lateral view);
b – head + thorax (lateral view); c – head + thorax (dorsal view);
d – anal segment with caudal protuberances (dorsal view). Scales:
a – 5 mm; b, c – 4 mm; d – 1 mm.
position. The feeding tracks on the leaves have a charac-
teristic appearance. Larvae of the last feeding instar were
recorded from mid-May to the end of May. Larvae start
feeding on the leaf margin and subsequently completely
consume the whole leaf except for the thick central vein.
after oviposition and if there is a severe infestation the host
plants are completely defoliated within two to three weeks
instar (eonymph) descends and burrows into the soil where
LWKLEHUQDWHVDVDSUHSXSD LQVLGH D ¿UP FRFRRQ 3XSDWLRQ
occurs after hibernation and depending on the temperature
adults emerge between mid-April and mid-May.
In the USA, Smith (1974) listed Rhododendron viscosum
and R. molle as food plants; Johnson & Lyon (1991) added
R. calendulaceum. In the Czech Republic, in addition to R.
molle two other species of Rhododendron were recorded as
host plants for N. lipovskyi, the European R. luteum Sweet
and the R. obtusum hybrid “Ledikanense” from Japan.
Host plants, their origin and the parts consumed are listed
in Table 1. Larvae fed on both the leaves and blossoms of
R. molle and R. luteum. 2QO\WKH ÀRZHUV RIR. obtusum
were consumed, suggesting that R. obtusum may only be
an accidental host plant.
Massachusetts, USA, but it was not until 1974 that it was
formally described by Smith (1974). The USA is so far the
only country in which N. lipovskyi naturally occurs and is
distributed there in the eastern states from Maine in the
Wisconsin (Fig. 4) (D. Smith, pers. comm.). In Europe, it
ic Garden, Prague (Czech Republic) based on larvae feed-
ing on Rhododendron molle and R. luteum. Flying adults
were not recorded there until 2013. Additional data were
obtained either by inspectors of the SPA and other pub-
lic services during 2013 (Kapitola & Pekárková, 2013) or
came from various gardening enthusiasts (Fig. 4). Reports
from private gardening enthusiasts were only taken into
Fig. 3. Nematus lipovskyi Smith, 1974: a – ovipositing female; b – damage to R. luteum; c – alive larvae feeding on R. luteum (lateral
tograph), but did provide feedback on how long the spe-
cies had been causing visible damage in a particular local-
Central Bohemia (34) and Prague (18), but the species was
(2), Pardubice (1), Liberec (1), Ústí (1) and South Bohemia
(2). Except for the above mentioned records of adults in
the Botanic Garden, all records are based exclusively on
cies appears to disperse relatively slowly; with only two
records of N. lipovskyi in 2010, an additional two in 2011
and nine new localities in 2012. Currently the species is
recorded in at least 60 localities.
5HFRUGVVLQFH Bohemia centr., Praha, Botanic Garden
of the Faculty of Science, Charles University in Prague, Prague.
190 m a.s.l. Pavlata J., Macek P. & Šípek lgt. (5952); Bohemia
FHQWU.RĜHQLFH QHDU .ROtQ PDVO+REORYiSHUVFRPP
(6059); 5HFRUGV VLQFH Bohemia centr., Vrané nad Vlta-
vou, 196 m a.s.l., Tejnická, pers. com. (6052); Bohemia centr.,
Senohraby, 363 m a.s.l., Tóbiková, pers. com. (6164). 5HFRUGV
pers. com. (5852); Bohemia centr., Újezd nad Lesy, 255 m a.s.l.,
&DUYDQRYi SHUV FRP %RKHPLD FHQWU3UĤKRQLFH
m a.s.l., Gabrielová, pers. com. (5953, 6053); Bohemia centr.,
'REĜLFKRYLFHPDVO5XQGRYi SHUV FRP %RKH-
SHUV FRP %RKHPLD FHQWU 0QtãHN SRG %UG\ P
%RKHPLD ERUýHVNi /tSD PDVO.DSLWR-
OD 3HNiUNRYi %RKHPLD RU -LþtQ PDVO
.DSLWROD 3HNiUNRYi %RKHPLDFHQWU0ČOQtN
215 m a.s.l. (Kapitola & Pekárková, 2013) (5652, 5653); Bohe-
mia or., Kopidlno, 219 m a.s.l. (Kapitola & Pekárková, 2013)
(5657); Bohemia centr., Dolany u Prahy, 192 m a.s.l. (Kapitola
& Pekárková, 2013) (5752); Bohemia centr., Statenice, 258
m a.s.l. (Kapitola & Pekárková, 2013) (5851); Bohemia centr.,
%RKHPLD FHQWU 5R]WRN\ X 3UDK\ P DVO 9OþNRYi SHUV
com. (5852); Bohemia centr., Zdiby u Prahy, 295 m a.s.l., Seidl,
(Kapitola & Pekárková, 2013) (5852); Bohemia centr., Praha 7
±6WURPRYND P DVO 9RGYiĜNDSHUV FRP
%RKHPLD FHQWU3UDKD 9\VRþDQ\ P DVO .UiO
pers. com. (5853, 5952, 5953); Bohemia centr., Káraný, 173 m
a.s.l., Lohrová, pers. com. (5854); Bohemia centr., Velký Osek
Fig. 4. Distribution of N. lipovskyi in the United States and the Czech Republic. Asterisk – records since 2010; full circles – records
since 2011; open circles – records since 2012; grey circles – records since 2013; grey triangles – records since 2013 (SPA data).
TABLE 1. Host plants of N. lipovskyi.
Host plant species Country of origin of host plant /
observation of infestation Consumed parts Source
Rhododendron molle (Blume) G. Don
and hybrids China, Japan / USA, Czech Rep. /HDYHVÀRZHUV Smith, 1974; pers. observ.
Rhododendron calendulaceum (Michx.) Torr. USA / USA /HDYHVÀRZHUV" Johnson & Lyon (1991)
Rhododendron viscosum (L.) Torr. USA / USA /HDYHVÀRZHUV" Smith, 1974
Rhododendron luteum Sweet East and Central Europe,
West Asia / Czech Rep. /HDYHVÀRZHUV Pers. observ.
Rhododendron × obtusum “Ledikanense” Japan / Czech Rep. Flowers Pers. observ.
± 2VHþHN P DVO .RXERYi SHUV FRP %RKHPLD
centr., Praha 4, Bráník, 199 m a.s.l., Votýpka, pers. com. (5952);
%RKHPLDFHQWU3UDKD %ĜHYQRYPDVO 6YRERGD SHUV
FRP%RKHPLDFHQWU3UDKD 6WĜHãRYLFH P DVO
274 m a.s.l., Vinkler, pers. com. (5952); Bohemia centr., Praha 5,
Smíchov, 196 m a.s.l., Havová, pers. com. (5952); Bohemia cen-
$QGHUORYiSHUVFRP %RKHPLD FHQWU3UDKD.ĜHVOLFH
282 m a.s.l., Fiala, pers. com. (5953); Bohemia centr., Pacov u
&KRFHĖP DVO 3DYFR SHUV FRP GRXEWIXO
pers. com. (6053, 6054); Bohemia centr., Kamenice, 368 m a.s.l.,
Šefrna. pers. com. (6053, 6153); Bohemia centr., Jevany, 380
m a.s.l., (Kapitola & Pekárková, 2013) (6054); Bohemia centr.,
hemia centr., Samechov, 383 m a.s.l., Vávrová, pers. com. (6155);
%RKHPLD FHQWU /KRWND X 'REĜtãH P DVO
u Prahy, 360 m a.s.l., (Kapitola & Pekárková, 2013) (6254); Bo-
%RKHPLD FHQWU 5RåPLWiO SRG 7ĜHPãtQHP
m a.s.l., (Kapitola & Pekárková, 2013) (6349); Bohemia centr.,
.DPêNQDG 9OWDYRXPDVO 9HþHĜRYiSHUVFRP
Bohemia mer., Blatná, 440 m a.s.l., Šípek lgt. (6549); Bohemia
Based on the known distribution of N. lipovskyi it would
be easy to assume that the species was introduced into the
Czech Republic from the USA with ornamental azalea
plants used in horticulture. However this assumption may
QRW EH MXVWL¿HG DV WKH IDFW WKDW N. lipovskyi was origi-
nally detected in the USA may not mean that the species
originated from there. In fact, there are several species of
their native ranges. For example, Nematus tibialis New-
man, 1837 feeding on false acacia (Robinia pseudoacacia
Linnaeus, 1753), which is native to North America, was
described from Europe (Smith, 1979); another example
is Pristiphora angulata Lindqvist, 1974 described from
Scandinavia. The larvae of this species are known to de-
velop on a non-native Spiraea species, indicating that the
species must have originated elsewhere (Lindqvist, 1974).
Revealing the origin of N. lipovskyi would involve inten-
VLYH¿HOG UHVHDUFKLQ DOO DUHDVZKHUH VRIWOHDYHGD]DOHDV
occur, as well as revising all the known species of Nematus
to eliminate possible synonymies.
The newly established population of N. lipovskyi in the
Botanical Garden in Prague consumed not only R. molle,
but also caused considerable damage to R. luteum and in-
ÀRUHVFHQFHVRIR. obtusum. Rhododendron luteum, there-
fore, is a new food plant for Nematus lipovskyi. R. luteum
is native to southeast Europe and southwest Asia. In Eu-
rope it occurs in neighbouring countries such as Poland
and Austria south through the Balkans and east to southern
Russia (Anisko & Czekalski, 1993; Resner, 2005; Ren-
cová, 2013). In Britain, as an invasive plant species, it has
colonised many wet peatlands and bogs (Pilkington, 2011),
whereas the Austrian and Polish populations are protected
(Rencová, 2013). Whether N. lipovskyi presents a poten-
tial risk to the native population of soft-leaved deciduous
rhododendrons, or whether it can be used to control this
species is unknown and needs to be tested. However, our
observations suggest that a mass occurrence of azalea saw-
plant from reproducing. Moreover, after 3 successive years
of defoliation plants are visibly weaker and partial dieback
occurrs. In the USA, no large outbreaks followed by con-
tinuous defoliation of azalea plants are reported (D. Smith,
unpubl. data; Johnson & Lyon, 1991).
The present results based mostly on feeding tracks and
larval samples suggest Prague and its eastern outskirts to be
the very epicentre of this invasive species as the majority
of samples are recorded from this region. The most remote
Bohemia). N. lipovskyiLVXQLYROWLQH ZLWK D OLPLWHGÀLJKW
period, therefore we consider the dispersal potential of
adults to be rather low or local. It is presumed that the pri-
mary agents of spread of this species might be young plants
carrying eggs and soil containing cocoons. On the other
hand a congeneric willow-feeding species N. oligospilus
(Förster, 1854) dispersed remarkably quickly when intro-
duced into the southern hemisphere (Urban & Eardley,
1995; Koch & Smith, 2000; Caron et al., 2013), therefore
the dispersal and distribution of this species across Europe
should be monitored.
ACKNOWLEDGEMENTS. We are grateful to D. Smith (USA)
for providing general information on the distribution and biology
RIWKHD]DOHDVDZÀ\ LQ WKH 86$DQGIRUYDOXDEOH FRPPHQWV RQ
the manuscript. C. Carrington (Prague, Czech Republic) kindly
proofread the English. We would also like to thank L. Pavlata
(Charles University Botanic Garden in Prague) for his help with
WKLVLQYHVWLJDWLRQ 75ĤåLþNDDQG3.DSLWRODERWK PHPEHUV RI
the State Phytosanitary Administration (which is currently a sec-
tion of the Central Institute for Supervision and Testing in Agri-
culture), kindly provided the data on the distribution of N. lipo-
by Ministry of Culture of the Czech Republic (DKRVO 2014/12,
National Museum, 00023272).
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Received August 15, 2014; revised and accepted October 1, 2014
Prepublished online November 11, 2014