Description of a new species of Aphanogmus Thomson (Hymenoptera: Ceraphronidae) that parasitizes acarivorous gall midges of Feltiella (Diptera: Cecidomyiidae) in Japan

Abstract

In 2008-2009, we reared small ceraphronids (about 0.5 mm in body length) from cocoons that had been made possibly by two acarivorous species, Feltiella acarisuga (Vallot) and F. acarivora (Zehntner) (Diptera: Cecidomyiidae) in Okinawa, Japan. Detailed morphological observation revealed that the ceraphronid was a new species of Aphanogmus Thomson (Hymenoptera: Ceraphronidae). We describe it as Aphanogmus flavigastris Matsuo, sp. n. Identification of the Aphanogmus species is essential to evaluate its possibly negative effects on the predatory activity of Feltiella species that have been used as control agents against tetranychid mites.

Full text

Description of a new species of Aphanogmus omson (Hymenoptera, Ceraphronidae)... 77
Description of a new species of Aphanogmus Thomson
(Hymenoptera, Ceraphronidae) that parasitizes
acarivorous gall midges of Feltiella
(Diptera, Cecidomyiidae) in Japan
Kazunori Matsuo1, Tomoko Ganaha-Kikumura2, Suguru Ohno2, Junichi Yukawa3
1 Biosystematics Laboratory, Faculty of Social and Cultural Studies, Kyushu University, Fukuoka 819–0395,
Japan 2 Okinawa Prefectural Agricultural Research Center, Okinawa 901–0336, Japan 3 Entomological
Laboratory, Faculty of Agriculture, Kyushu University, Fukuoka 812–8581, Japan
Corresponding author: Kazunori Matsuo (matsuosudachi@scs.kyushu-u.ac.jp)
Academic editor: N. Johnson  |  Received 14 March 2016  |  Accepted 31 May 2016  |  Published 8 June 2016
http://zoobank.org/5FE366FF-E882-4FB0-8D71-0B79E3FE3849
Citation: Matsuo K, Ganaha-Kikumura T, Ohno S, Yukawa J (2016) Description of a new species of Aphanogmus
omson (Hymenoptera, Ceraphronidae) that parasitizes acarivorous gall midges of Feltiella (Diptera, Cecidomyiidae)
in Japan. ZooKeys 596: 77–85. doi: 10.3897/zookeys.596.8472
Abstract
In 2008–2009, we reared small ceraphronids (about 0.5 mm in body length) from cocoons that had been
made possibly by two acarivorous species, Feltiella acarisuga (Vallot) and F. acarivora (Zehntner) (Diptera:
Cecidomyiidae) in Okinawa, Japan. Detailed morphological observation revealed that the ceraphronid
was a new species of Aphanogmus omson (Hymenoptera: Ceraphronidae). We describe it as Aphanog-
mus avigastris Matsuo, sp. n. Identication of the Aphanogmus species is essential to evaluate its possibly
negative eects on the predatory activity of Feltiella species that have been used as control agents against
tetranychid mites.
Keywords
Aphanogmus avigastris, Feltiella acarisuga, Feltiella acarivora, taxonomy
ZooKeys 596: 77–85 (2016)
doi: 10.3897/zookeys.596.8472
http://zookeys.pensoft.net
Copyright Kazunori Matsuo 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.
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Kazunori Matsuo et al. / ZooKeys 596: 77–85 (2016)
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Introduction
In 2008–2009, small (about 0.5 mm in body length) species of ceraphronids (Hyme-
noptera) were reared from cocoons that had been made possibly by two acarivorous
species, Feltiella acarisuga (Vallot) and F. acarivora (Zehntner) (Diptera: Cecidomyi-
idae) in Okinawa, Japan (Abe et al. 2011, Ganaha-Kikumura et al. 2012). Preliminary
identication revealed that the ceraphronid was a member of Aphanogmus omson
(Hymenoptera: Ceraphronidae), which contains at least 100 species worldwide (John-
son and Musetti 2004, Evans et al. 2005, Buhl et al. 2010). About 20% of them
have been known as parasitoids of various insects including Cecidomyiidae (Diptera),
Bethylidae, Ichneumonidae (Hymenoptera) and Cybocephalidae (Coleoptera) (Oat-
man 1985, Gilkeson et al. 1993, Polaszek and Dessart 1996, Evans et al. 2005). Host
information for the remaining 80% has not been provided. At present, two species,
Aphanogmus oridanus Ashmead and A. fulmeki Szelényi (=A. parvulus Roberti) have
been known to parasitize Feltiella species in the Holoarctic region. e former is an
endoparasitoid of Feltiella acarivora (Oatman 1985, Johnson and Musetti 2004) and
the latter attacks F. acarisuga, F. acarivora, Aphidoletes aphidimyza (Rondani), and My-
codiplosis sp. (Diptera: Cecidomyiidae) (Dessart 1992).
A few taxonomic studies have focused on Japanese species of Aphanogmus. Ash-
mead (1904) rst recorded Aphanogmus from Japan, describing A. hakonensis Ashmead
based on individuals collected from Hakone, Kanagawa. Polaszak and Dessart (1996)
detected several cryptic species of Aphanogmus hakonensis and proposed the species
complex of A. hakonensis. Ishii (1937) reported an unidentied species of Aphanog-
mus as a parasitoid of Cybocephalus species (Coleoptera: Cybocephalidae) that feed on
Unaspis yanonensis (Kuwana) (Hemiptera: Diaspididae) on citrus in Japan. Evans et
al. (2005) considered that Aphanogmus sp. reported in Ishii (1937) was identical to A.
inamicus Evans and Dessart. In total, two nominal species, Aphanogmus hakonensis and
A. inamicus have been known in Japan.
Larvae of all known Feltiella species feed on tetranychid mites (Acari: Tetranychi-
dae) (Gagné 1995, Gagné and Jaschhof 2014). In particular, Feltiella acarisuga is re-
garded as an important natural enemy against tetranychid mites that frequently de-
velop pesticide resistance and cause serious damage to various agricultural products
(Barnes 1933, Wardlow and Tobin 1990). erefore, the purpose of this study is to
identify the Aphanogmus found in Okinawa, as this is essential to evaluate its eect on
mortality of Feltiella species.
Material and methods
We collected more than one larva or cocoon of Feltiella from each collecting site in
Okinawa, Japan in 2008–2009. ey were kept in petri-dishes to rear Aphanogmus
and Feltiella species. Adults that emerged were preserved in 75% ethanol for morpho-
logical observation. If possible, host species of parasitoid wasp should be identied by

Description of a new species of Aphanogmus omson (Hymenoptera, Ceraphronidae)... 79
examining remnants of host insect but the male genitalia of host cecidomyiid, which
is important for species identication, would not be included in the remnants. Other-
wise, host species should be identied before the attack of parasitoid wasps. However,
this is not always applicable under natural conditions. erefore, we regarded host
cecidomyiid to be identical to either F. acarisuga or F. acarivora when A. avigastris
emerged from cocoons that coexisted on the same plant with either F. acarisuga or F.
acarivora, respectively because we have seldom seen F. acarisuga and F. acarivora on the
same plant.
For microscopic study, the ethanol-stored specimens were dried by the method de-
scribed in Matsuo and Yukawa (2009). Fore wings were mounted on slides in Canada
balsam using ethanol and xylene. Several specimens were gold-coated for micropho-
tography with a JEOL JSM-5600LV scanning electronic microscope. High resolution
image was taken with the methods described in Matsuo et al. (2012). Adult morpho-
logical terminology follows Mikó and Deans (2009), except for wing venation, which
follows Dessart (1963). e holotype and paratypes are deposited in the collection of
the Biosystematics Laboratory, Faculty of Social and Cultural Studies, Kyushu Uni-
versity, Japan.
Results and discussion
Aphanogmus avigastris Matsuo, sp. n.
http://zoobank.org/4725144C-E843-4706-8DE2-D58805F78F41
Ceraphronidae sp.: Abe et al. 2011: 277.
Ceraphronidae sp.: Ganaha-Kikumura et al. 2012: 323.
Etymology. e specic name, avigastris, is Latin meaning yellowish gaster, derived
from the color of the female metasoma.
Type material. See Table 1.
Description. FEMALE. Body length 0.5–0.6 mm (Figs 1, 2). Head dark brown.
Scape yellow; pedicel and all agellomeres yellowish brown. Mesosoma dark brown.
Fore wing with an infuscate area. Fore and mid coxae dark brown, sometimes yellow-
ish in apical half; fore and mid femora yellow, sometimes brownish; hind leg and all
tibiae yellow. Metasoma yellow, darker dorsally.
Head in dorsal view 1.5–1.7 times as wide as long, 1.2–1.4 times as wide as meso-
soma; POL: OOL: LOL = 1.8: 1.5: 1.0. Head in frontal view (Fig. 3) 1.0–1.1 times as
wide as high; malar space 0.3–0.5 times as long as eye height; lateral margin of torulus
distinctly raised; intertorular carina distinct; frontal depression transversely reticulate;
ocellar foveae absent; preocellar pit absent; facial pit absent; preoccipital furrow pre-
sent and extends from anterior ocellus to occipital foramen; preoccipital carina absent;
preoccipital lunula absent; occipital carina present; occipital depression absent; occiput
smooth. Antenna (Fig. 4) 10 segmented; scape about 0.6 times as long as height of

Kazunori Matsuo et al. / ZooKeys 596: 77–85 (2016)
80
Figure 1. A female of Aphanogmus avigastris. Scale bar: 100 μm.
Figures 2–5. Aphanogmus avigastris. 2 female body, lateral view 3 female head, frontal view; 4 female
antenna, lateral view 5 female mesosoma and metasoma, dorsal view. Scale bars: 2: 100 μm; 3–5: 50 μm.

Description of a new species of Aphanogmus omson (Hymenoptera, Ceraphronidae)... 81
Figures 6–9. Aphanogmus avigastris. 6 female scutellum, antero-dorsal view 7 female mesosoma, lateral
view 8 female fore wing, upper surface 9 male antenna, lateral view. Scale bars: 6: 20 μm; 7: 50 μm;
8, 9:100 μm.
head, as long as distance between inner orbits; pedicel 2.0–2.5 times as long as agel-
lomere 1; the following segments gradually widened; agellomere 7 about 2.0 times as
wide as agellomere 1; club 1 segmented.
Mesosoma 1.2–1.4 times as long as wide; 1.3–1.5 times as high as wide; ventral
pronotal pit distinct; mesoscutum reticulate, sparsely setose (Fig. 5); setal base slightly
pustulate; median mesoscutal sulcus complete; notaulus absent; parapsidal line absent;
interaxillar sulcus present; scutoscutellar sulcus angled medially, foveolate, continuous
with interaxillar sulcus; dorsal axillar area and mesoscutellum sculptured as mesoscu-
tum, with distinct lateral carina which connects posterior mesoscutellar sulcus (Fig.
6); mesoscutellum 1.4–1.6 times as long as wide; anterior mesopleural sulcus distinct
(Fig. 7); anterior mesopleural area nely reticulate with several setae; dorsal mesometa-
pleural carina straight; anterior mesopleural sulcus perpendicularly intersecting dorsal
mesometapleural carina; metapleural carina distinct, extends near dorsal mesometa-
pleural carina.
Fore wing about 3.0 times as long as wide, with a darkly pigmented band (Fig. 8);
radial vein 1.4–1.5 times as long as marginal vein. Metacoxa bare dorsally; longitudinal
metacoxal carina present at base.

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Table 1. A list of type specimens of Aphanogmus avigastris. All specimens are kept in the collection of the Biosystematics Laboratory, Faculty of Social and Cultural
Studies, Kyushu University, Japan.
Possible host Associated plant* Collecting site (collector**) Host collecting No. specimens Notes
F. acarisuga Pueraria montana Senbaru, Nishihara, Okinawa, Japan (SO) 22 vii 2008 1 female Holotype
F. acarisuga P. montana Senbaru, Nishihara, Okinawa, Japan (SO) 22 vii 2008 1 male Paratype
F. acarisuga Mallotus japonicus Uka, Kunigami, Okinawa, Japan (SO, TGK) 1 viii 2008 1 female Paratype
F. acarisuga Ma. japonicus Uehara, Ogimi, Okinawa, Japan (SO, TGK) 6 viii 2008 1 female Paratype
F. acarisuga Broussonetia papyrifera Gesashi, Higashi, Okinawa, Japan (SO) 21 ii 2009 1 female Paratype
F. acarivora Bauhinia variegata Senbaru, Nishihara, Okinawa, Japan (SO) 18 vii 2008 2 females Paratypes
F. acarivora Melanolepis multiglandulosa Hentona, Kunigami, Okinawa, Japan (SO) 31 vii 2008 2 males Paratypes
F. acarivora Mucuna macrocarpa Oku, Kunigami, Okinawa, Japan (SO, TGK) 1 viii 2008 2 females Paratypes
F. acarivora P. montana Iramina, Yomitan, Okinawa, Japan (SO) 2 x 2008 1 female Paratype
F. acarivora Morus australis Kijoka, Ogimi, Okinawa, Japan (SO) 16 x 2008 1 female Paratype
* e plant, from which Feltiella species were collected.
** Name of collectors. SO: Suguru Ohno, TGK: Tomoko Ganaha-Kikumura.

Description of a new species of Aphanogmus omson (Hymenoptera, Ceraphronidae)... 83
Syntergum with distinct transverse carina anteriorly, smooth, with 2–3 setae ante-
rolaterally, occupying more than half of total length of metasoma; longitudinal striae
of syntergum absent.
MALE. Diers from female as follows: Antenna (Fig. 9) 11 segmented; agellar
setae long, about 2.0 times width of agellomeres.
Distribution. Japan.
Host insects. Feltiella acarisuga and F. acarivora. Usually one, occasionally two or
three adults emerged from a single host cocoon.
Diagnosis
Evans et al. (2005) proposed the following three species groups based on characteristics
of the mesosoma and metasoma:
clavicornis group: mesoscutal median furrow and metasomal basal carina absent.
tenuicornis group: mesoscutal median furrow absent, metasomal basal carina present.
fumipennis group: mesoscutal median furrow and metasomal basal carina present.
According to the morphological features of these species groups, the new species
belongs to the fumipennis group, while Aphanogmus fulmeki and A. oridanus that
have been known as parasitoids of Feltiella species belong to the clavicornis group and
tenuicornis group, respectively. erefore, the new species can be distinguished from
Aphanogmus fulmeki and A. oridanus.
Among members of the fumipennis group, the new species shares the following
characteristics with species in the Aphanogmus hakonensis complex sensu Polaszak and
Dessart (1996): median mesoscutal sulcus present; dorsal axillar area and mesoscutel-
lum with distinct lateral carina; syntergum with distinct transverse carina anteriorly.
However, Aphanogmus avigastris does not belong to the A. hakonensis complex based
on the following characters: fore wing with a darkly pigmented band (hyaline in A. ha-
konensis complex); antenna of female with agellomere 2–7 not transverse (transverse
in A. hakonensis complex).
e new species is most similar to Aphanogmus inamicus as it shares the following
characters: median mesoscutal sulcus present; dorsal axillar area and mesoscutellum
with distinct lateral carina; syntergum with distinct transverse carina anteriorly; fore
wing with a darkly pigmented band; antenna of female with agellomere 2–7 not
transverse. However, Aphanogmus avigastris can be distinguished from A. inamicus by
the following characters: club of antenna 1 segmented (3 segmented in A. inamicus);
lateral carina on dorsal axillar area and mesoscutellum more raised than that of A.
inamicus; longitudinal striae of syntergum absent (present in A. inamicus); mesosoma
dark brown (reddish yellow in A. inamicus); infuscate area on fore wing smaller (from
marginal vein to posterior margin of fore wing in A. inamicus).
According to a key to the Palaearctic species of Aphanogmus (Szelényi 1940), the
new species runs to A. fasciolatus Förster based on the following characters: antenna
clavate; club 1 segmented and longer than the preceding two segments combined; ra-

Kazunori Matsuo et al. / ZooKeys 596: 77–85 (2016)
84
dial vein longer than marginal vein. However, the new species could be distinguished
from Aphanogmus fasciolatus by having longer pedicel that is distinctly longer than
agellomere 1 while A. fasciolatus has the pedicel that is shorter than agellomere 1.
We need to monitor the seasonal abundance of Aphanogmus avigastris for the suc-
cessful application of Feltiella species, because its congener A. oridanus that attacks F.
acarivora has been regarded to act as a negative force in controlling Tetranychus urticae
Koch (Acari: Tetranychidae) on strawberry in California (Oatman 1985). Shimoda
et al. (2016) recently developed a remarkable system for trapping Feltiella species and
other predators of spider mites using pots of Brassica rapa Linnaeus var. perviridis
L.H.Bailey (Brassicaceae), ‘komatsuna’ in Japanese, which bore Tetranychus urticae.
ey could rear an unidentied species of Aphanogmus from Feltiella acarisuga with the
trapping system. is method may be useful to collect plenty of individuals of Feltiella
and its parasitoids from ‘komatsuna’ in the elds. Further eld surveys are needed to
verify the ecacy of this method as a monitoring tool for Aphanogmus avigastris.
Acknowledgements
We thank Prof. Y. Abe and Dr. T. Ide for their support in taking SEM images. is
study was supported partly by Global COE Program (Center of excellence for Asian
conservation ecology as a basis of human-nature mutualism), MEXT, Japan to KM.
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