First record of the mullein bug Campylomma miyamotoi Yasunaga, 2001 (Heteroptera: Miridae) in Europe

Abstract

Campylomma miyamotoi Yasunaga, 2001, an alien plant bug species (Hemiptera: Heteroptera: Miridae) associated to the Persian silk tree Albizia julibrissin Durazz, 1772 (Fabaceae), is recorded for the first time in the Iberian Peninsula. Described from Japan, it is also found in Korea. The species was recently reported for the first time from Turkey. This Iberian record is the first one in Europe and the second one out of its native distribution range, and spreads the presence of C. miyamotoi largely westwards within the Palaearctic area.

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Goula & Mateos (2021)
ARQUIVOS ENTOMOLÓXICOS, 24: 271-276
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ARTIGO / ARTÍCULO / ARTICLE
First record of the mullein bug Campylomma miyamotoi
Yasunaga, 2001 (Heteroptera: Miridae) in Europe
Marta Goula 1 & Eduardo Mateos 2
Department of Evolutionary Biology, Ecology and Environmental Sciences and Institute of Biodiversity Research (IRBIo), Faculty
of Biology, University of Barcelona. Av. Diagonal, 643. E-08028 Barcelona, Spain.
1 ORCID 0000-0001-6308-342X. e-mail: mgoula@ub.edu
2 ORCID 0000-0001-9741-5744. e-mail: emateos@ub.edu
Abstract: Campylomma miyamotoi Yasunaga, 2001, an alien plant bug species (Hemiptera: Heteroptera: Miridae)
associated to the Persian silk tree Albizia julibrissin Durazz, 1772 (Fabaceae), is recorded for the first time in the
Iberian Peninsula. Described from Japan, it is also found in Korea. The species was recently reported for the first time
from Turkey. This Iberian record is the first one in Europe and the second one out of its native distribution range, and
spreads the presence of C. miyamotoi largely westwards within the Palaearctic area.
Key words: Heteroptera, Miridae, Phylinae, Campylomma miyamotoi, allochthonous species, faunistics, new record,
Iberian Peninsula.
Resumen: Primer registro del mírido Campylomma miyamotoi Yasunaga, 2001 (Heteroptera: Miridae) en Europa.
Campylomma miyamotoi Yasunaga, 2001, una especie exótica de mírido (Hemiptera: Heteroptera: Miridae) asociada al
árbol de la seda Albizia julibrissin Durazz, 1772 (Fabaceae), se registra por primera vez en la Península Ibérica. Descrita
de Japón, también se encuentra en Corea. La especie fue señalada recientemente por primera vez de Turquía. Este
registro ibérico es el primero de Europa y el segundo fuera de su ámbito geográfico nativo, y extiende ampliamente la
presencia de C. miyamotoi hacia el extremo occidental del área paleártica.
Key words: Heteroptera, Miridae, Phylinae, Campylomma miyamotoi, especie alóctona, faunística, nueva cita, Península
Ibérica.
Recibido: 1 de octubre de 2021 Publicado on-line: 14 de octubre de 2021
Aceptado: 4 de octubre de 2021
Introduction
Human actions have increased the introduction of exotic species at a global scale (McNeely et al., 2001).
The increased mobility of people and their goods increases the probability of transporting species
worldwide, via trade of manufactured products or livestock, pets, or nursery stock, as well as
agriculture and forestry products (Hulme, 2009). Growing attention is paid to the arrival of
allochthonous species, which in certain circumstances may have significant impact, either environmental,
economic or on public health (Genovesi & Shine, 2004). Alien Heteroptera have been object of an
inventory available via the Internet, in the frame of the DAISIE Research Program. Rabitsch (2008)
thoroughly studies more than 40 species and analyzes the factors that contribute to their introduction
or expansion.
Phylinae is a large subfamily within the Miridae, presently organized in 9 tribes (Menard et al.,
2014). The characterization of the subfamily is supported by the inner genital structures (Schuh &

Goula & Mateos (2021): First record of the mullein bug Campylomma miyamotoi Yasunaga, 2001 (Het.: Miridae) in Europe
272
Weirauch, 2020), and the study of the male endosoma and parameres is often needed to reach a
reliable sorting to species. The subfamily, which includes five hundred genera (including Campylomma
Reuter, 1878), shows its greatest diversity in temperate regions (Cassis & Schuh, 2012).
Campylomma is a Palaeartic and Palaeotropical genus, extending to the Pacific Islands, which
includes more than 130 tiny or very tiny species (Schuh, 1995). In the Palaearctic region the genus
includes around fifty species (Kerzhner & Josifov, 1999; Aukema et al., 2013), and three of them, C.
annulicorne (Signoret, 1865), C. ribesi Goula, 1986 and C. verbasci (Meyer-Dür, 1843), already known
from the Iberian Peninsula, after C. nicolasi Reuter, 1883 was synonymized to C. verbasci by Carapezza
(1997). Yasunaga et al. (2015) diagnose the genus and here we summarize the most relevant external
features to quickly identify it in the context of the Iberian fauna: head large and very short, with big
eyes which extends down to the gula; a certain number of species show greenish or yellowish habitus,
including legs and antennae, and the species identification is very often only reliable on genitalic
characters of any of both sexes (Schuh, 1984; Yasunaga et al., 2015). Other Campylomma species are
darker, which are usually more easily identifiable. Tibiae are provided with dark spots, from which a
dark spine arises. In addition, first and second antennal segments may present dark spots or rings, or
are completely dark.
As for its biology, herbivorous or predatory species may be found within the genus. In case of
herbivory, oligophagy is the rule, while monophagy, although possible, is only the case for few
Campylomma species. Certain predator species are regarded as potential auxiliary fauna in orchards as
they prey on small insect pests (Schaefer & Panizzi, 2000). A zoophytophagous diet is estimated for C.
miyamotoi and C. fukagawai Yasunaga, Schuh & Dewal, 2015, which suck on their host plant Albizia
julibrissin, and prey on psyllids and aphids living on the same plant (Yasunaga et al., 2015).
The aim of this work is to record C. miyamotoi in Europe for the first time by means of samples
collected in the Iberian Peninsula, and provide useful comparative information to reliably identify the
Iberian Campylomma species.
Material and methods
Specimens of C. miyamotoi were collected by the second author in his home. Previously to capture, he
observed that specimens of a small insect were attracted to domestic light, which was also the capture
method in Izmir, in the Asian part of Turkey (Çerçi et al., 2019).
Samples were dry kept, glued to pinned cardboard labels.
The photographs of the habitus were taken with a Canon Eos 600D camera with a Canon 65 mm
macro lens. Each final habitus image is the result of stacking seven photographs using Adobe Photoshop
CS5 software.
Material studied:
Campylomma ribesi Goula, 1986
SPAIN: Barcelona: Liors (Montseny), 15.VII.198., Populus sp., 1♂, 1♀ (M. Goula leg., det. et coll.).
Campylomma annulicorne (Signoret, 1865)
BULGARIA: Mariza Bai, Harmanli, 17.VI.1962, 1♀ (M. Josifov leg. et det., M. Goula coll.); Rupite
bei Petrisch, 25.VI.1981, 1♂ (M. Josifov leg. et det., M. Goula coll.).
Campylomma verbasci (Meyer-Dür, 1843)
SPAIN: Barcelona: Santa Fe del Montseny, Can Lleonart, 16.VII.1984, Orobanche sp., 1♀ (M. Goula
leg., det. et coll.); Santa Fe del Montseny, Can Lleonart, 27.VII.1984, Verbascum sp., 1♂ (M. Goula
leg., det. et coll.).

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Campylomma miyamotoi Yasunaga, 2001
SPAIN: Barcelona: Cerdanyola del Vallès (urban area, position: N41° 29’ 01.5” E2° 08’ 57.6”),
22.VII.2021, Albizia julibrissin, 1♂, 1♀ (E. Mateos leg., M. Goula det. et coll.).
Results and discussion
After examining the material from Cerdanyola del Vallès, the specimens were identified as C. miyamotoi
Yasunaga, 2001.
Campylomma miyamotoi was described from samples swept from the Persian silk tree Albizia
julibrissin Durazz, 1772 in different Japanese localities, in August (Yasunaga, 2001). It is a tiny species
of ca. 2,5 mm long. Its general habitus (Figs. 1-3) and colour (greenish, fading to yellowish after death;
with dark rings or spots on legs and two first antennal segments), make it very close to the Iberian
species C. annulicorne (Figs. 4-5) and C. verbasci (Figs. 6-7). On the other hand, the Iberian endemism C.
ribesi is darker, and antennae are much thicker in males than in females (Figs. 8-9). However, male
vesica is clearly different between the four species (Figs. 10-13). Moreover, C. miyamotoi is much
smaller than the other Iberian species.
Another Japanese species, C. fukagawai, has been also found on the Persian silk tree.
Comparative description of endosoma in Yasunaga et al. (2015) is as follows: endosoma of C. fukagawai is
“weakly sigmoid, with bifurcate, short, broad apical appendages”, while in C. miyamotoi endosoma shows
“short, broad apical processes, and small”. According to figures in the original description of C.
miyamotoi (Yasunaga, 2001) and in the Korean revision for the genus (Duwal et al., 2013), and
descriptions already mentioned, we assume that in Yasunaga et al. (2015) Fig. 55 belongs in fact to C.
fukagawai, and Fig. 47 belongs to C. miyamotoi. We would like to point out that in C. fukagawai endosomal
processes are divergent, while in C. miyamotoi these processes run in parallel. Yasunaga et al. (2015)
sustain that both species possibly do not compete on their host plant, as adults of C. fukagawai were
collected earlier than those of C. miyamotoi.
Campylomma species usually exhibit a short range of host plants. Among the Iberian species,
Campylomma annulicorne is known to live on willow Salix spp. (Wagner, 1975), mainly S. babilonica
(Yasunaga et al., 2015), but also on Polygonum aviculare and Tripelurospermum sp. (Nau, 1979) and
Artemisia spp. (Duwal et al., 2013). According to present knowledge, C. miyamotoi is monophagous on
Albizia julibrissin. Campylomma ribesi is associated to Populus sp. (Goula, 1986a), including Populus nigra
(Gessé, 2011) and P. deltoides (Pagola-Carte, 2009), and to Salix alba (Pagola-Carte & Zabalegui, 2007).
Campylomma verbasci is mainly associated to Verbascum spp. (Goula, 1986b), but it is reputed to be
polyphagous (Wagner, 1975), with Cupressus sempervirens, Gossipium herbaceum, Heliotropium sp.,
Orobanche sp., Pirus communis, Prunus spinosa or Suaeda vera being recorded as host plants, among
others.
Concerning their geographic distribution, C. annulicorne is found in Europe, extending to central
Asia, and recently introduced in China (Kerzhner & Josifov, 1999; Aukema et al., 2013); C. miyamotoi has
been previously reported from Japan and Korea (Duwal et al., 2013) and Turkey (Çerçi et al., 2019), the
present Iberian citation being the westernmost location; C. ribesi is an Iberian endemism (Kerzhner &
Josifov, 1999); and C. verbasci is Palaeartic, present also in the Canary Islands, and accidentally
introduced in North America (Kerzhner & Josifov, 1999; Aukema et al., 2013).
Concluding remarks
The increasing use of exotic ornamental plants in urban environments may result in the facilitation of
the arrival of exotic species. It is worth to know that Persian silk tree, whose natural distribution area
extends form Far East to Central Asia, was introduced in Europe in 1745 (Salvador Palomo et al., 2002).

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Its pleasant appearance, together with its resistance to pests and to short periods of drought, make it
a good candidate as ornamental in urban green areas. Çerçi et al. (2019) suggest that C. miyamotoi may
have been recently introduced through travelling of people or trading of goods including plant seedlings,
or that it spread naturally following its host plant. Because of its small size, C. miyamotoi could be
present out of its native area much before than noticing it recently either in Turkey or in the Iberian
Peninsula. These two scattered reports, East and West of the Mediterranean Basin, will most probably
be followed by others elsewhere Persian silk trees are present.
The consequences of the arrival of this insect species to these new areas is difficult to predict,
as its biology is still poorly known. On the other hand, its monophagy related to Albizia julibrissin allows
to anticipate that, if any, the consequences of the presence of C. miyamotoi will be restricted to
ornamentals in urban areas.
Acknowledgments
To Álvaro Izuzquiza (Madrid, Biodiversidad Virtual), for providing information on Albizia julibrissin.
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10
11
12
13
Figs. 1-9.- Habitus of the Iberian
Campylomma species. 1-3.- C. miyamotoi
(lateral, dorsal, ventral). 4-5.- C. verbasci
(dorsal). 6-7.- C. annulicorne (dorsal). 8-9.- C.
ribesi (dorsal).
Figs. 10-13.- Endosoma of the Iberian
Campylomma species. 10.- C. miyamotoi. 11.- C.
verbasci. 12.- C. annulicorne. 13.- C. ribesi.
Figs. 1-9.- Habitus de las especies ibéricas de
Campylomma. 1-3.- C. miyamotoi (lateral,
dorsal, ventral). 4-5.- C. verbasci (dorsal). 6-
7.- C. annulicorne (dorsal). 8-9.- C. ribesi
(dorsal).
Figs. 10-13.- Endosoma de las especies
ibéricas de Campylomma. 10.- C. miyamotoi.
11.- C. verbasci. 12.- C. annulicorne. 13.- C.
ribesi.
2 mm
9
8
7
6
5
4
3
2
1
10
11, 12, 13
0,2 mm