SYSTEMATICS
Discovery of Cynipidae (Hymenoptera: Cynipoidea) From the
Indochina Region, With Description of Three New Species
YOSHIHISA ABE,1,2 TATSUYA IDE,1,3 KAZUHIKO KONISHI,4
AND
TAKATOSHI UENO5
Ann. Entomol. Soc. Am. 107(2): 399Ð406 (2014); DOI: http://dx.doi.org/10.1603/AN13180
ABSTRACT Plagiotrochus indochinensis Abe, Ide, Konishi, & Ueno sp. nov., Dryocosmus okajimai
Abe, Ide, Konishi, & Ueno sp. nov., and Synophrus vietnamensis Abe, Ide, Konishi, & Ueno sp. nov. are
described from Vietnam. This is the Þrst record of Cynipidae (Hymenoptera: Cynipoidea) from the
Indochina region; the former two species belong to tribe Cynipini and the latter to the inquiline tribe
Synergini. Based on the observation of a female P. indochinensis inserting its ovipositor into a young
sprout of Quercus (Cyclobalanopsis) helferiana A. de Candolle in the Þeld, this wasp species is
considered to induce galls on this evergreen oak species. This article conÞrms that members of
Cynipini that induce galls on Cyclobalanopsis (the ring cup oaks) are widely distributed in Asia, as
predicted previously. Although D. okajimai was collected by sweeping an evergreen Fagaceae tree,
its host remains to be clariÞed. Because the adults of S. vietnamensis were collected by sweeping an
evergreen Fagaceae tree in June and dissecting a bud gall on Castanopsis sp. in September, it is
considered that this wasp species has more than one generation a year. The gall-inducing ability and
host plant speciÞcity of S. vietnamensis should be examined carefully in future. The high species
richness of Quercus L. and related genera in the Indochina region increases the likelihood of the
existence of little-known, but potentially diverse, cynipid fauna in this region.
KEY WORDS gall wasp, Plagiotrochus, Dryocosmus, Synophrus, Cyclobalanopsis
A review of tribes within the Cynipidae in the Oriental and Eastern Palearctic regions revealed that the
cynipid fauna in these regions is likely to be extremely
rich (Abe et al. 2007). Among the eight tribes in this
family, the Cynipini, which is comprised of ⬇1,000
species worldwide, is the most speciose (Liljeblad et
al. 2011). Almost all of the species in this tribe are
known to induce galls on the subgenus Quercus of the
genus Quercus L. (Fagaceae) (Liljeblad et al. 2008).
The majority of Cynipini species have been recorded
from the Nearctic and Western Palearctic regions, but
the cynipid fauna in the Oriental and Eastern Palearctic regions is considered to be diverse because of
the richness of potential host plants, such as the genera
Lithocarpus Blume and Castanopsis (D. Don) Spach,
and the strictly Asian subgenus Cyclobalanopsis (the
ring cup oaks) of the genus Quercus (Fagaceae) and
the subgenus Quercus (Abe et al. 2007, Liu et al. 2012).
After initially proposing that the Cynipini were associated with the subgenus Cyclobalanopsis in the Oriental and Eastern Palearctic regions (Abe et al. 2007),
the association between these cynipids and ring cup
1 Biosystematics Laboratory, Faculty of Social and Cultural Studies,
Kyushu University, Motooka, Fukuoka, Japan.
2 Corresponding author, e-mail: [email protected].
3 Japan Society for the Promotion of Science, Chiyoda-ku, Tokyo,
Japan.
4 NARO Hokkaido Agricultural Research Center, Sapporo, Japan.
5 Institute of Biological Control, Faculty of Agriculture, Kyushu
University, Hakozaki, Fukuoka, Japan.
oaks was Þrst conÞrmed by the description of Plagiotrochus masudai Ide, Wachi & Abe, 2010, which
induces galls on Q. (C.) glauca Thunb. in Japan (Ide
et al. 2010). To date, two species of Plagiotrochus Mayr,
1881, including P. masudai, two species of Dryocosmus
Giraud, 1859, seven species of Cycloneuroterus Melika
& Tang, 2011, and two species of Cyclocynips Melika,
Tang, & Sinclair, 2013 have been described as gallinducing Cynipini on Cyclobalanopsis (Ide et al. 2010,
2012, 2013; Tang et al. 2011a,b,; Melika et al. 2013). In
addition, even a species of the tribe Synergini, which
had previously been considered to be composed of
inquiline gall wasps that depended mainly on other
cynipid taxa for galls, was observed to induce galls on
Cyclobalanopsis (Abe et al. 2011). All of the wasps,
inducing galls on Cyclobalanopsis, have been described from Japan and Taiwan in the northeastern
limit of the distribution range of this plant subgenus.
It has not yet been clariÞed whether this limit in the
geographic range of gall wasps is because of the limited distribution of the wasps or merely because of the
lack of sampling in regions of Asia outside Japan and
Taiwan.
Recently, we obtained specimens of Cynipidae
from Vietnam. This family has not been recorded
from the Indochina region. Here, we describe three
new species of Cynipidae and discuss the biogeographic signiÞcance of their occurrence in this region.
0013-8746/14/0399Ð0406$04.00/0 䉷 2014 Entomological Society of America
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ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA
Vol. 107, no. 2
Ronquist and Nordlander (1989), Ronquist (1994),
and Liljeblad et al. (2008). Descriptions of surface
sculpture are according to Harris (1979).
Examination of External Morphology. The external
structure of the dry-mounted wasp specimens was
examined under a binocular stereomicroscope (MZ12,
Leica, Solms, Germany; Þtted with a DS-L1 camera,
Nikon, Tokyo, Japan), and the lengths of the hind tibia
of the holotypes were measured using an ocular micrometer. The type specimens were examined under
a scanning electron microscope at 3.0 KV (JSM5600LV, JEOL, Tokyo, Japan).
Specimens Examined. All the specimens were collected in Da Lat, Lam Dong. Province, Vietnam, and
are deposited at the Biosystematics Laboratory, Faculty of Social and Cultural Studies, Kyushu University
(BLKU) and the Laboratory of Entomology, Tokyo
University of Agriculture (TUA).
Fig. 1. Holotype female habitus of P. indochinensis, lateral view (scale bar ⫽ 1 mm).
Materials and Methods
Abbreviations and Terminology. The following
morphological abbreviations are used: OOL, ocularocellar line (distance from the outer edge of a lateral
ocellus to the compound eye); POL, postocellar line
(distance between the inner edges of the two lateral
ocelli); and LOL, lateral-ocellar line (distance between the front and lateral ocelli). Morphological
terminology are in accordance with Richards (1977),
Results
Plagiotrochus indochinensis Abe, Ide,
Konishi et Ueno, sp. nov.
(Figs. 1Ð3)
Holotype Female. Head brown except for dark
brown vertex, occiput, and area between antennal
sockets and ocelii; mesosoma brown except for dark
brown pronotum, mesopleuron, mesoscutellum, metascutellum, metanotal trough, metapleuron, and propodeum; metasoma brown, but partly dark brown.
Head as broad as mesosoma in dorsal view, imbricate. POL:OOL:LOL ⫽ 10:7:5. Distance between an-
Fig. 2. Holotype female of P. indochinensis. (a) Head, anterior view; (b) head and mesosoma, lateral view; (c) mesosoma,
dorsal view; (d) mesosoma, posterodorsal view; and (e) hypopygial spine (scale bars ⫽ 100 ␮m).
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401
Fig. 3. Holotype female of P. indochinensis inserting its ovipositor into young sprout of Q. (C.) helferiana under Þeld
conditions.
tennal rims 0.5 times as long as distance between
antennal rim and inner margin of the compound eye.
Lower face and occiput pubescent. Facial strigae radiating from lateral clypeus reaching eye margin. Antenna 14-segmented; relative lengths of ßagellomeres:
9, 8, 7, 7, 7, 7, 7, 6, 6, 5, 5, and 8.
Pronotum areolate, dorsally rugose, pubescent. Anterior part of mesoscutum transversely carinate-rugose, mid and posterior parts strongly imbricate;
notaulus percurrent, distinct; anteroadmedian, and
parapsidal signa present. Mesoscutellum reticulaterugose with two fovae at base; fovea closed on posterior margin; foveal septum broad. Metanotal trough
almost smooth. Lateral propodeal carina distinct,
strongly curved outward; median propodeal area with
irregular carinae; lateral propodeal area pubescent.
Mesopleuron medially areolate.
Marginal cell of forewing open on anterior margin,
4.9 times as long as broad, wing surface closely ciliated.
Apex of metatarsal claw slightly bent, base not expanded.
Metasoma shiny, smooth; metasomal terga II and VII
sparsely pubescent; metasomal terga III-VII with small
punctures. Hypopygial spine sparsely pubescent; projecting part 4.5 times as long as broad in ventral view.
Length of hind tibia 0.76 mm.
Male. Unknown.
Holotype. Tuyen Lam Lake, Da Lat, Lam Dong
Province, Vietnam, 1,419 m altitude, 15ÐIIIÐ2013, T.
Ueno and K. Konishi leg., BLKU.
Etymology. Named for its occurrence in the Indochina region.
Geographic Distribution. Vietnam.
Host Plant. Quercus (Cyclobalanopsis) helferiana.
This plant species is considered to be the host plant
because the holotype female was observed to insert its
ovipositor into a young sprout of this evergreen oak
(Fig. 3). The host plant was identiÞed based on description by Menitsky (2005).
Remarks. According to a key of Palearctic genera of
Cynipini (Melika et al. 2010), this new species was
classiÞed as a member of Plagiotrochus because the
adult female has the following diagnostic character-
Fig. 4. Holotype female habitus of D. okajimai, lateral
view (scale bar ⫽ 1 mm).
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ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA
istics of this genus: 1) subocular impression absent, 2)
facial strigae radiating from lateral clypeus reaching
eye margin, 3) mesoscutum transversely rugose, 4)
lateral propodeal carina bent outward, 5) median part
of mesopleuron not smooth, and 6) hypopygial spine
slender, short, with sparse setae not forming a hair tuft.
P. indochinensis is readily distinguishable from other
members of this genus by having irregular carinae on the
median propodeal area (Fig. 2d). In some specimens of
the sexual generation of P. masudai, several irregular
carinae are present between lateral propodeal carinae
(Þgs. 12 and 20 in Ide et al. 2010), and the situation of the
median propodeal area in P. masudai is often similar to
that in P. indochinensis. In P. masudai, the vertex and
upper face are rugose and the projecting part of the
hypopygial spine has long subapical setae extending beyond the apex of the spine (Þgs. 10 and 15 in Ide et al.
2010). However, in P. indochinensis, the vertex and upper
face are imbricate and the projecting part of the hypopygial spine has sparse short setae (Fig. 2a and e).
Dryocosmus okajimai Abe, Ide,
Konishi et Ueno, sp. nov.
(Figs. 4 and 5)
Holotype Female. Body black except for brownish
ocelli, antenna, mandible, palpi, tegula, and legs.
Head as broad as mesosoma in dorsal view. POL:
OOL:LOL ⫽ 9:9:4. Distance between antennal rims 0.5
times as long as the distance between antennal rim and
inner margin of compound eye. Vertex and upper face
smooth. Carinae connecting antennal sockets present.
Vol. 107, no. 2
Slight vertical carina present between antennal socket
and anterior tentorial pit; area between vertical carinae smooth, but area between vertical carina and eye
margin rugulose. Facial strigae radiating from lateral
clypeus reaching eye margin. Lower face and occiput
pubescent. Gena and occiput imbricate. Antenna 14segmented; relative lengths of ßagellomeres: 9, 9, 8, 8,
7, 7, 6, 6, 5, 5, 5, 7.
Pronotum dorsolaterally rugose, dorsally pubescent.
Mesoscutum smooth; notaulus percurrent, distinct; anteroadmedian signum absent; parapsidal signum weak;
median mesoscutal impression present only as a slight
impression. Mesoscutellum smooth dorsally, reticulaterugose laterally and posteriorly, sparsely pubescent with
two fovae at base; fovea open on posterior margin; foveal
septum broad with two pits. Metanotal trough with some
vertical carinae. Lateral propodeal carina distinct,
strongly curved outward; carina along dorsal propodeal
margin, connecting lateral propodeal carinae present;
median propodeal area with some carinae radiating from
ventral margin; lateral propodeal area sparsely pubescent. Mesopleuron smooth.
Marginal cell of forewing open on anterior margin,
4.1 times as long as broad, wing surface closely ciliated.
Apex of metatarsal claw slightly bent, base not expanded.
Metasoma shiny, smooth; metasomal terga II and
VII sparsely pubescent; metasomal terga IIÐVII with
small punctures. Hypopygial spine sparsely pubescent; projecting part 1.5 times as long as broad in
ventral view; apical seta beyond apex of spine.
Length of hind tibia 0.68 mm.
Fig. 5. Holotype female of D. okajimai. (a) Head, anterior view; (b) head and mesosoma, lateral view; (c) mesosoma,
dorsal view; (d) mesosoma, posterodorsal view; and (e) hypopygial spine (scale bars ⫽ 100 ␮m).
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ABE ET AL.: DISCOVERY OF CYNIPIDAE FROM INDOCHINA
403
but it is uncertain whether this wasp induces galls on
this tree or not.
Remarks. This new species falls into Dryocosmus in
a key to the Palearctic genera of Cynipini (Melika et
al. 2010). Among Eastern Asian species of Dryocosmus,
only D. okajimai has the following two morphological
features: 1) two weak vertical carinae between antennal sockets and anterior tentorial pits and 2) broad
(one-third the length of fovea) foveal septum with
two pits.
Synophrus vietnamensis Abe, Ide,
Konishi et Ueno, sp. nov.
(Figs. 6 Ð 8)
Fig. 6. Holotype female habitus of S. vietnamensis, lateral
view (scale bar ⫽ 1 mm).
Male. Unknown.
Holotype. Tuyen Lam Lake, Da Lat, Lam Dong
Province, Vietnam, 1,419 m altitude, 1ÐVIIÐ2013, T.
Ueno leg., BLKU.
Etymology. Named in honor of Prof. S. Okajima, the
principal investigator of the Þeld survey in Vietnam.
Geographic Distribution. Vietnam.
Host Plant. Unknown. The holotype female was
collected by sweeping an evergreen Fagaceae tree,
Holotype Female. Head and mesosoma black;
ocelli, antenna, mandible, palpi, tegula, and legs
brownish, but most part of coxae and femora blackish.
Metasoma blackish brown.
Head as broad as mesosoma in dorsal view. POL:
OOL:LOL ⫽ 10:8:5. Distance between antennal rims
0.5 times as long as the distance between antennal rim
and inner margin of compound eye. Vertex and gena
imbricate; upper face costulate; median frontal carina
present; lateral frontal carina absent; lower face pubescent, facial strigae radiating from clypeus reaching
eye margin and antennal socket. Antenna 13-segmented; relative lengths of ßagellomeres: 8, 5, 5, 6, 6, 7, 7,
7, 6, 5, 10.
Pronotum reticulate-rugose; lateral pronotal carina
almost absent. Mesoscutum transversely carinate-ru-
Fig. 7. Holotype female of S. vietnamensis. (a) Head, anterior view; (b) head and mesosoma, lateral view; (c) head and
mesosoma, dorsal view; (d) mesosoma, posterolateral view; and (e) hypopygial spine (scale bars ⫽ 100 ␮m).
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ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA
Vol. 107, no. 2
Fig. 8. Host gall of S. vietnamensis on Castanopsis sp.
gose; notaulus percurrent, distinct; anteroadmedian
signum indistinct and parapsidal signum distinct. Median mesoscutal impression only as a slight impression.
Mesoscutellum reticulate-rugose with two fovae at
base; fovea with some vertical carinae, closed on posterior margin; foveal septum broad. Metanotal trough
with some vertical carinae. Propodeum pubescent;
lateral propodeal carina distinct, straight. Mesopleuron strigate, coriarious anteriorly.
Marginal cell of forewing open on anterior margin,
2.6 times as long as broad, wing surface closely ciliated.
Metasomal terga II and III fused without Þssure
between these two terga, shiny, with a few setae basolaterally. These two fused terga and lateral ßap with
dense small punctures. Hypopygial spine sparsely pubescent; projecting part 1.1 times as long as broad in
ventral view.
Length of hind tibia 0.80 mm.
Male. Differs from the female as follows. Antenna
15-segmented; relative lengths of ßagellomeres: 11, 5,
5, 5.5, 6, 7, 7, 7, 6, 6, 5, 5, 5; Þrst ßagellomere incised on
outer margin, weakly swollen distally. Frons densely
pubescent. Metasomal terga II and III fused with Þssure between these two terga dorsally.
Type Material. HOLOTYPE. Tuyen Lam Lake, Da
Lat, Lam Dong Province, Vietnam, 1419 m altitude,
30 ÐVIÐ2013 (sweeping), T. Ueno leg., BLKU. PARATYPES. One female and one male (BLKU) and two
females (TUA), same locality and collector, early IXÐ
2013, host: a bud gall on Castanopsis sp.
Etymology. Named for its occurrence in Vietnam.
Geographic Distribution. Vietnam.
Host Gall. Bud gall on Castanopsis sp. (Fig. 8).
When one gall was dissected in early September, four
wasps (three females and one male) of S. vietnamensis
emerged from it.
Remarks. Based on the current deÞnition of Synophrus Hartig, 1843 (Pénzes et al. 2009), this new
species is considered a member of this genus. S. vietnamensis can be easily separated from other species of
the genus by having median frontal carina. Seven
species of this genus have been known, all of which are
distributed in the Western Palearctic (Pénzes et al.
2009). Synophrus olivieri Kieffer, 1898 was also recorded from the Indian Himalaya (Weidner 1961), but
this record “requires further study before the identiÞcation is conÞrmed” (Abe et al. 2007, page 178).
Therefore, this is convincing evidence for the occurrence of Synophrus in Asia. Because the adult wasps
were obtained at the same locality by sweeping an
evergreen Fagaceae tree in June and by dissecting a
bud gall on Castanopsis sp. in September, this species
has more than one generation a year.
Discussion
P. indochinensis Abe, Ide, Konishi et Ueno, sp. nov.,
D. okajimai Abe, Ide, Konishi et Ueno, sp. nov., and S.
vietnamensis Abe, Ide, Konishi et Ueno, sp. nov. are
described from Vietnam in the present article. This is
the Þrst record of Cynipidae from the Indochina region, corroborating the prediction of Abe et al. (2007)
regarding the potential diversity of cynipid fauna in
this region. The high species richness of potential gall
wasp hosts, that is, Quercus and related genera in the
Indochina region (Abe et al. 2007, Liu et al. 2012),
implies that this region could potentially support a rich
variety of Cynipidae (mainly Cynipini and Synergini).
Consequently, further surveys need to be conducted
in the warm, humid, highland forests of the Indochina
region to discover little-known but potentially rich
cynipid fauna. Moreover, in the Palearctic region,
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ABE ET AL.: DISCOVERY OF CYNIPIDAE FROM INDOCHINA
most members of the speciose tribe Cynipini exhibit
alternation of generations within the same year (Abe
et al. 2007). Therefore, further studies need to be
conducted to clarify whether the life cycles of Cynipini from the Indochina region differ from those in the
Palearctic region.
In total, 19 species have been assigned to the genus
Plagiotrochus worldwide, of which two induce galls on
Cyclobalanopsis (Ide et al. 2010, Tang et al. 2011a).
Based on the occurrence of these two species, it seems
likely that, in a similar way that P. indochinensis was
predicted to induce galls on Cyclobalanopsis, other
Plagiotrochus species inducing galls on this plant subgenus will be discovered in the Oriental and eastern
Palearctic regions (Ide et al. 2010).
Generally, members of Cynipini exhibit alternation
of generations within a year, that is, the adults of the
sexual generation emerge in spring and their offspring
emerge as the asexual generation late in the fall of the
same year (Yukawa and Masuda 1996, Stone et al.
2002). However, in P. masudai, which depends on
Cyclobalanopsis in Japan, completion of the life cycle
requires 3 yr, and the adults of both the asexual and
sexual generations emerge in spring (Ide et al. 2010).
To clarify the relationships between host plants and
the life cycle of Cynipini, the life cycle of P. indochinensis on Cyclobalanopsis needs to be investigated.
The genus Dryocosmus currently contains 31 species worldwide (Ide et al. 2013). While seven species
occur in Asia, only two are associated with Cyclobalanopsis (Ide et al. 2013). Among Cynipini, this genus
has an exceptionally wide host range, which includes
the genera Castanea Miller, Castanopsis, Chrysolepis
Hjelmqvist, and Lithocarpus, and sections Cerris, Lobatae, and Protobalanus of the genus Quercus (Ide et
al. 2013). Further study is thus necessary to clarify the
host plant and life cycle of D. okajimai. Because Dryocosmus appears to be a polyphyletic group (Ács et al.
2007, Stone et al. 2009, Melika et al. 2011), further
phylogenetic analyses using molecular markers or
morphology of known Holarctic species in this genus
need to be undertaken to clarify the systematic status
of this genus.
The genus Synophrus was originally described as a
gall inducer (Hartig 1843) and later transferred to the
Synergini based on the adult morphology (Ronquist
1994). The modiÞcation of the host gall by Synophrus
is remarkable among cynipid inquilines, but the inquilinism of this genus is supported by indirect evidence (Pénzes et al. 2009). Because a rearing experiment demonstrated gall induction by a species of
Synergini, Synergus itoensis Abe, Ide, & Wachi, 2011,
further investigations of the biology of this tribe could
conceivably Þnd more gall inducers (Abe et al. 2011).
Synophrus appears to be closely related to Saphonecrus
Dalla Torre & Kieffer, 1910 (Pénzes et al. 2009). Because it is currently not clear whether Saphonecrus
hupingshanensis Liu, Yang, & Zhu, 2012 is an inquiline
or a gall inducer on the chinquapin genus Castanopsis
(Liu et al. 2012), the gall-inducing ability and host
plant speciÞcity of S. vietnamensis warrant further
studies.
405
Acknowledgments
This study was partly supported by Grants-in-Aid for ScientiÞc Research (24405028) and for JSPS Fellows (24-5764)
from the Japan Society for the Promotion of Science, and by
Global COE Program (Center of Excellence for Asian Conservation Ecology as a Basis of Human-Nature Mutualism),
Ministry of Education, Culture, Sports, Science and Technology, Japan. We thank T. Mita and H. T. Pham for their help
in the Þeld survey. We also thank Prof. S. Okajima for his
support in various ways.
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Received 19 November 2013; accepted 15 January 2014.