TISCIA monograph series

Oak associated inquilines

(Hymenoptera, Cynipidae, Synergini)

Zsolt Pénzes, Chang-Ti Tang, Péter Bihari,

Miklós Bozsó, Szabina Schwéger and George Melika

Szeged
2012

Two countries, one goal, joint success!

 Oak associated inquilines
(Hymenoptera, Cynipidae, Synergini)
TISCIA monograph series
1. J. Hamar and A. Sárkány-Kiss (eds.): The Maros/Mureş River Valley.
A Study of the Geography, Hydrobiology and Ecology of the River
and its Environment, 1995.
2. A. Sárkány-Kiss and J. Hamar (eds.): The Criş/Körös Rivers’ Valleys.
A Study of the Geography, Hydrobiology and Ecology of the River
and its Environment, 1997.
3. A. Sárkány-Kiss and J. Hamar (eds.): The Someş/Szamos River
Valleys. A Study of the Geography, Hydrobiology and Ecology of the
River and its Environment, 1999.
4. J. Hamar and A. Sárkány-Kiss (eds.): The Upper Tisa Valley.
Preparatory Proposal for Ramsar Site Designation and an Ecological
Background, 1999.
5. L. Gallé and L. Körmöczi (eds.): Ecology of River Valleys, 2000.
6. Sárkány-Kiss and J. Hamar (eds.): Ecological Aspects of the Tisa
River Basin, 2002.
7. L. Gallé (ed.): Vegetation and Fauna of Tisza River Basin, I. 2005.
8. L. Gallé (ed.): Vegetation and Fauna of Tisza River Basin, II. 2008.
9. L. Körmöczi (ed.): Ecological and socio-economic relations in the
valleys of river Körös/Criş and river Maros/Mureş, 2011.
10. L. Körmöczi (ed.): Landscape-scale connections between the land use,
habitat quality and ecosystem goods and services in the Mureş/Maros
valley, 2012.
11. Zsolt Pénzes, Chang-Ti Tang, Péter Bihari, Miklós Bozsó, Szabina
Schwéger and George Melika: Oak associated inquilines
(Hymenoptera, Cynipidae, Synergini), 2012.
 TISCIA monograph series
Volume 11

Oak associated inquilines

(Hymenoptera, Cynipidae, Synergini)

Zsolt Pénzes, Chang-Ti Tang, Péter Bihari,

Miklós Bozsó, Szabina Schwéger and George Melika

This volume was prepared in the framework of “Landscape-scale

connections between the land use, habitat quality and ecosystem goods and
services in the Mures/Maros valley” (HURO0901/205/2.2.2) project that is
implemented under the Hungary-Romania Cross-Border Co-operation
Programme, and is part-financed by the European Union through the
European Regional Development Fund, and the Republic of Hungary and
Romania.

Szeged
2012

The content of this volume does not necessarily represent the official position of
the European Union.
Zsolt Pénzes, Chang-Ti Tang, Péter Bihari, Miklós Bozsó, Szabina Schwéger and
George Melika: Oak associated inquilines (Hymenoptera, Cynipidae, Synergini).
Tiscia Monograph Series 11, Szeged, 2012.

Series editor: László Körmöczi

Published by the Depatment of Ecology, University of Szeged, H-6226 Szeged,

Közép fasor 52., Hungary

ISSN 1418 - 0448

Contributors of the volume

Péter Bihari, University of Szeged, Department of Ecology, Szeged, 6726

Hungary; Biological Research Center of Hungarian Academy of
Sciences, Institute of Genetics, 6726, Szeged
Miklós Bozsó, University of Szeged, Department of Ecology, Szeged, 6726
Hungary
George Melika, Budapest Plant Pest Diagnostic Laboratory, National Food Chain
Safety Office, Directorate of Plant Protection, Soil Conservation and
Agri-environment, Budapest, 1118 Hungary
Zsolt Pénzes, University of Szeged, Department of Ecology, Szeged, 6726
Hungary; Biological Research Center of Hungarian Academy of
Sciences, Institute of Genetics, 6726, Szeged
Szabina Schwéger, University of Szeged, Department of Ecology, Szeged, 6726
Hungary
Chang-Ti Tang, Department of Entomology, National Chung Hsing University,
Taichung, 40227 Taiwan
 Contents

Introduction ............................................................................................................ 1
Main characteristics of the tribe Synergini ............................................................. 2
Taxonomy, diversity and distribution of inquiline cynipids: Tribe
Synergini Ashmead, 1896 ....................................................................... 4
Synergus complex of genera ................................................................................ 15
Plant hosts of oak cynipid inquilines .................................................................... 35
Phylogeny of Synergini ........................................................................................ 39
Host gall associations of oak cynipid inquilines................................................... 53
Plant host associations of oak cynipid inquilines ................................................. 59
Conclusions and future directions ........................................................................ 65
Acknowledgements .............................................................................................. 66
References ............................................................................................................ 66
Introduction

Cynipidae lies within the superfamily Cynipoidea of the Hymenoptera, which

includes approximately 3000 described species (Fergusson 1995, Ronquist 1999).
With the exception of the Cynipidae and a group of gall-inhabiting inquiline
genera in Figitidae, the cynipoids are all parasitoids, and probably cynipid
gallwasps have evolved from parasitoid ancestors (Ronquist 1995, 1999). Cynipid
gallwasps (Hymenoptera: Cynipidae) induce some of the world's most visually
striking, and structurally complex plant galls. Approximately 1400 cynipid
gallwasp species are currently recognized (Liljeblad and Ronquist 1998, Ronquist
1999, Ronquist and Liljeblad 2001, Nieves-Aldrey 2001, Melika 2006), although
Nordlander (1984) has estimated that the actual number is between 3000 and
6000.
For historical reasons, all extant gallwasps belong to the subfamily Cynipinae
and are divided into two main trophic groups: the gall inducers and the gall-
associated inquilines, which together make up eight tribes (Csóka et al. 2005,
Liljeblad et al. 2011). These are mainly characterized using biology and host plant
data in combination with some morphological features. The Cynipini,
Diplolepidini, Pediaspidini and Eschatocerini comprise the typical gall wasps
found on oaks and roses as well as on some other woody plants of the eudicot
subclass Rosidae (collectively called the woody rosid gallers). All gall inducers
on herbaceous plants (+ some Rubus), from a wide variety of plant families,
belong to the paraphyletic assemblage ‘‘Aylacini’’ (Melika 2006, Liljeblad et al.
2011). Recently, a unique South African tribe Qwaqwaiini was described, with
only one known genus and species, Qwaqwaia scolopiae Liljeblad, Nieves-
Aldrey and Melika which induces galls on Scolopia mundii (Salicaceae)
(Liljeblad et al. 2011). The seventh tribe known from South America, the
Paraulacini, originally were thought to be inquilines, like Synergini, however,
judging from larval biology and by the fact that they are lethal to the gall inducing
Aditrochus (Chalcidoidea: Pteromalidae: Ormocerinae) host species on
Nothofagus (Nothofagaceae), it is entirely possible that they are parasitoids
(Nieves-Aldrey et al. 2009).
Another lineage, distinct from the woody rosid gallers and other mentioned
gall inducing tribes, gave rise to the tribe Synergini (ca. 185 species), whose
members are all inquiline inhabitants of the galls of other cynipid gall wasps
(Nylander 2004a, Liljeblad et al. 2008, Liljeblad et al. 2011). Although
phytophagous, and able to induce the development of nutritive tissues within galls
of other cynipids, they are apparently unable to induce their own galls de novo.
The differences between gall-inducing cynipid wasps and cynipid inquilines are

1
thus not only morphological, but also represent an important and obvious
biological division within the subfamily.
A number of review-like papers were published on the tribe Synergini in the
last decade, however, all of them were fragmentary, either dealing with the
morpho-taxonomy of the tribe, emphasized on a particular zoogeographical
region/particular genus or only phylogenetic approach was given (Nieves-Aldrey
2001, Pujade-Villar et al. 2003, Csóka et al. 2005, Sadeghi et al. 2006, Pénzes et
al. 2009, Ács et al. 2010, Melika et al. 2012). Since many new data were
published on Synergini, especially with the description of new genera and species
from the Eastern Palaearctic, Oriental and Neotropical Regions, which nobody yet
generalized. In this paper we try to review our current knowledge of the Synergini
tribe, focusing on the morhologically, systematically and phylogenetically most
contraversial Synergus-complex of genera, together with analysing the most
recent unpublished phylogenetic result.

Main characteristics of the tribe Synergini

Inquilinism. The term inquiline is derived from the Latin “inquilineus”

meaning tenant or guest. Inquilinism is usually considered to represent a
unilaterally beneficial relationship that benefits only the inquiline (Askew 1984).
It is a form of cleptoparasitism (termed agastoparasitism by Ronquist (1994)).
However, the real (obligate) inquilinism in cynipids is much more than a simple
unilateral interaction (Askew 1984, Ronquist 1994, Csóka et al. 2005). As strictly
defined, it is an obligatory relationship between two species in which the benefits
are entirely unilateral but without detrimental effects on the partner. There are
many examples of inquilinism in Hymenoptera, especially in the social
hymenopteran groups of bees, wasps and ants (Askew 1984). In cynipid galls this
definition applies to a taxonomically diverse group that includes inquiline
gallwasps and their close cynipoid relatives, moths, beetles and gall midges. This
paper focuses on the inquiline cynipids that feed obligately on plant tissues within
developing galls and to some extent, stimulate the development of tissues
characteristic to galls. The hymenopteran inquilines in cynipid galls are all
cynipoids, and are either members of the cynipid tribe Synergini (Cynipidae), or
figitids (Figitidae) in the subfamilies Parnipinae, Thrasorinae and Euceroptrinae
(Ronquist and Nieves-Aldrey 2001, Ross-Farré and Pujade-Villar 2007,
Buffington and Liljeblad 2008).
Gall-inducing ability in inquilines. The inquiline cynipids have lost the
ability to induce their own galls de novo. Nevertheless, they have retained the
ability to modify the gall tissue directly surrounding them into the characteristic
nutritive tissue also found in the larval chambers of the gall inducer, and all are
wholly phytophagous. Some inquiline cynipids can substantially modify gall

2
structures outside the nutritive tissues, and the entire gall can be either enlarged
(Shorthouse 1973, 1980) or stunted (Washburn and Cornell 1981; Wiebes-Rijks
1982) depending on the number of larvae in the gall. For example, when the
unilocular galls of the rose cynipid gallwasp Diplolepis nodulosa (Beutenmüller)
are attacked by the inquiline Periclistus pirata (Osten Sacken), the result is a gall
three times the size of one inhabited only by the gall inducer, and contains 17
inquiline larval chambers (Brooks and Shorthouse 1998). The most dramatic
modification of host gall structure by an inquiline cynipid in oak galls is that
caused by members of the genus Synophrus. S. politus Hartig attacks, at a very
early stage, tiny sexual generation cynipid galls induced by species in the
“Andricus burgundus” complex (Pujade-Villar et al. 2003). Whilst most other
cynipid inquilines induce differentiation of nutritive tissues in a developing host
gall exclusively, the Synophrus larva appears to control differentiation of the
whole gall and only lacks the ability to initiate gall induction. Feeding activity of
the larvae on the chamber walls is thought to induce the growth and
differentiation of the gall tissues, as is the case for cynipid gall inducers. The gall
of S. politus is unilocular, and the larva moves freely within a large cavity.
However, the apperance of “Synophrus galls” is unstructured comparing to the
variety of galls of true inducers (Cynipini), so the nature of interaction with the
host plant and their share in gall development remain to be explored. More
striking even is the recently described new inquiline species, Synergus itoensis
Abe, Ide and Wachi from Japan, for which rearing experiments demonstrated gall
induction in the seed coat of the acorn of Quercus glauca Thunb. (Abe et al.
2011). All of these changes, caused by inquilines, have the potential to
significantly modify parasitoid attack rates and so to influence mortality rates in
inquilines and gall inducers. The inquiline influences may be more generally
important than is currently known (Sanver and Hawkins 2000).
Effects on the host gall larvae: lethal and non lethal inquilines. Some cynipid
inquilines kill the host larva early in the development of the gall. However, this is
not a trophic relationship since they do not feed on the host larva. It appears that
where inquiline eggs are placed in close proximity to the gall-inducer's larval
chambers, the more rapid development of the inquiline larvae and their chambers
crushes the gall inducer (Weld 1952, Evans 1965, Shorthouse 1973, 1980,
Wiebes-Rijks 1979). An inquiline can be lethal in one type of gall, but develop in
the peripheral tissues of another host gall with no apparent harm to the original
gall-inducer (Mayr 1872, Nieves-Aldrey 2001). A subset of inquiline cynipids
(termed lethal inquilines, Duffet 1968) inflicts substantial mortality on gall
inducers. In oak cynipid galls, inquilines can be divided into those whose larval
chambers occupy the host larval chamber, and those whose chambers develop in
outer gall tissues. Closely related inquilines may have quite different impacts on
their host: For example, in the asexual generation galls of the oak cynipid gall
wasp Andricus kollari (Hartig), Synergus reinhardi Mayr is a lethal inquiline in

3
the larval chamber, while Synergus umbraculus (Olivier) develops in the outer
wall of the gall and has no obvious negative effect on the gall inducer
(Schönrogge et al. 1996, 2000). When attacked by non-lethal inquilines, both
inquilines and the gall inducer may emerge from a single gall. The total numbers
emerging are the highest when non-lethal inquilines (such as S. umbraculus, S.
facialis Hartig and S. pallicornis Hartig) infest the outer gall parenchyma of large
host galls, as in case of Andricus quercuscalicis (Burgsdorf) (Schönrogge et al.
1996).
The biology of inquiline immature stages. The morphology of the immature
stages of cynipid inquilines are already discussed in some papers (Vårdal et al.
2003, Nieves-Aldrey et al. 2005) as well as their biology. The most detailed
studies were made on Periclistus pirata (Osten Sacken) inquilines in galls
induced by the rose gallwasps Diplolepis polita (Ashmead) and D. nodulosa (see
for example, Shorthouse 1973, Brooks and Shorthouse 1998).
Inquiline life cycles and phenology. Most species have similar life cycles,
with a single generation per year synchronised with their hosts. Adults usually
emerge from the galls after the gall inducers and lay eggs in freshly initiated galls.
Part of the species, especially in the Synergus genus, produce two generations per
year and some of them show generational dimorphism (for example, Synergus
facialis) (Wiebes-Rijks 1979, Melika 2006).

Taxonomy, diversity and distribution of inquiline cynipids: Tribe

Synergini Ashmead, 1896

The adult cynipid inquilines are insects of small to moderate size, from 0.8 to 7 mm
in body length, and share the following morphological characters: genae not or weakly
expanded behind eyes; lower face usually with radiating striae from clypeus reaching
antennal rims; clypeus indistinct and ventral clypeal margin straight; subocular sulcus
absent; distance between occipital and oral foramina longer than height of occipital
foramen; long postgenal sulci and postgenal ridges united well before reaching
hypostomata; maxillary palp 5–segmented; labial palp with three segments. Antenna of
female with 12–14 segments; antenna of male with 14–15 segments, with first
flagellomere usually more or less expanded apically. Mesosoma sculptured. Pronotum
relatively long, measuring medially 1/5 to 1/3 of the shortest distance across lateral
margin; pronotal pits (admedian depressions) usually conspicuous and separated medially,
sometimes associated with a weak pronotal plate; lateral pronotal carinae present or not;
lateral longitudinal carinae of propodeum subparallel. Fully winged except for some males
of Synergus thaumacerus; tarsal claws with an acute basal lobe or tooth. Metasoma with
the second tergum reduced or ring shaped and dorsally with longitudinal ridges (sulcate);
third and fourth abdominal terga free or usually fused and covering almost all the
metasoma; prominent part of the ventral spine of hypopygium short.

4
 The taxonomic position and classification of the cynipid inquilines has long
been controversial, but has recently been clarified somewhat (Pujade-Villar et al.
2003, Pénzes et al. 2009), nevertheless some genera are still problematic,
especially on the species level (Ács et al. 2010). Hartig (1840) was the first to
recognise the biological differences between the inquiline and gall forming
Cynipidae. He described the genera Ceroptres, Synergus and Synophrus as
inquilines from oak galls, although he regarded Synophrus as a gall inducing
genus (Hartig 1840, 1843). At different times the cynipid inquilines have either
been placed in a separate subfamily within the Cynipidae (Hartig 1840, Ashmead
1896a, 1903), included in the herb gall wasp tribe Aylacini (Roskam 1992), or
lumped with the gall inducers into a large group without subdivisions (Weld
1952, Eady and Quinlan 1963). However, more recently they have been classified
as belonging to the tribe Synergini within the Cynipidae (Burks 1979, Ronquist
1999, Melika 2006).
The entire world fauna of the tribe Synergini includes 186 species of
inquilines in nine genera (Table 1): six genera, Agastoroxenia Nieves-Aldrey &
Medianero, 2010, Ceroptres Hartig, 1840, Saphonecrus Dalla Torre & Kieffer,
1910, Synergus Hartig, 1840, Synophrus Hartig, 1843 and Ufo Melika & Pujade-
Villar, 2005, form the Synergus-complex of genera and all are inquilines in
cynipid galls on oak and oak-relative genera within Fagaceae (Csóka et al. 2005,
Melika et al. 2005, van Noort et al. 2007, Ács et al. 2010, Nieves-Aldrey and
Medianero 2010). Inquiline cynipids associate with cynipid galls on roses
(Diplolepidini) are represented with only one genus Periclistus Förster, 1869.
Synophromorpha Ashmead, 1903 are inquilines in Diastrophus galls on Rubus
(Rosaceae) (Ritchie 1984). The mentioned 8 genera are distributed mainly in the
temperate zone of the northern hemisphaere, in the Holarctic region, however,
Agastoroxenia is known only from the Neotropics, as well as 14 Synergus species
known from Panama and Guatemala (Nieves-Aldrey and Medianero 2011 and
Table 1). Few oak gall associated inquiline species are known also from the
Oriental region: two Saphonecrus species from the Philippines (Weld 1926),
some newly described Saphonecrus species from the Oriental Region of China
(Wang et al. 2010, Liu et al. 2012) and 1 species of Ufo from Taiwan (Melika et
al. 2012).
The genus Rhoophilus Mayr, 1881 raises an interesting biogeographic
problem. This genus is known only from a single species, R. loewi Mayr, 1881
and is the only cynipid genus restricted to the Ethiopian region in South Africa
(Mayr 1881, van Noort et al. 2007). No inquiline cynipids are known from
Eschatocerine cynipid galls, very few attack aylacine cynipid galls - the
exceptions are Synophromorpha species that develop in Diastrophus cynipid galls
on bramble, Rubus (Ritchie and Shorthouse 1987b). A marked feature of cynipid
inquilines is that they are generally more specific to a particular plant taxon than
they are to a given host gall inducer.

5
Table 1. The world distribution and species richness of Synergini genera (WP, Western
Palaearctic, EP, Eastern Palaearctic, OR, Oriental Region, NA, Nearctic, NT, Neotropical
Region, ET, Ethiopian Region).

Genera Hosts WP EP OR NA NT ET World

Agastoroxenia Oak cynipid – – – – 1 – 1
Nieves-Aldrey et galls
Medianero, 2010
Ceroptres Oak cynipid 2 4 – 17 – – 23
Hartig, 1840 galls
Synergus Oak cynipid 30 10 – 55 14 – 109
Hartig, 1840 galls
Saphonecrus Dalla Oak cynipid 6 9 2 4 – – 21
Torre & Kieffer, galls
1910
Synophrus Oak 7 – – – – – 7
Hartig, 1843 cynipids
Ufo Melika & Oak cynipid – 3 1 – – – 4
Pujade, 2005 galls
Periclistus Rosa 3 4 – 7 – – 14
Förster, 1869 cynipid galls
Synophromorpha Rubus galls – 2 – 4 – – 6
Ashmead, 1903
Rhoophilus Rhus galls – – – – – 1 1
Mayr, 1881
Total: 48 32 3 87 15 1 186

The number of known Synergini species (Table 1) is unevenly distributed

between the zoogeographical regions. Pujade-Villar et al. (2003) revised the
Synergini of the Western Palaearctic and synonymised 29 doubtful species,
Sadeghi et al. (2006) described 5 new species from Iran and, thus bringing the
number of recognised species in the Western Palaearctic to 48 species. No doubt,
the most studied region is the Western Palaearctic and the number of described
species probably will not change essentially with further research. The number of
Eastern Palaearctic species increased essentially during the last decade and the
growing tendency will stay because of the activity of some cynipid research
groups in China and Taiwan. The same growing tendency characterizes the
Neotropics, where a considerable number of new species was described during the
last years (Nieves-Aldrey and Medianero 2010, 2011). The high number of
inquilines described from the USA and Canada is unadequate to the number of
species known from Mexico. Research in Mexico will definitely recon the hidden
diversity of Synergini in the large and very peculiar faunistic and floristic zones
of the country.

6
 Despite the shared characters given above, the Synergini represents a
polyphyletic assemblage of inquiline lineages, which we shall discuss in details
later. Below we give a brief taxonomic overview of all known Synergini genera,
with short morphology, taxonomic assignment and diversity. The non-oak host
related genera (Periclistus, Synophromorpha and Rhoophilus) are briefly
discussed below while the oak and near oak-related host genera, Ceroptres and
the Synergus complex of genera (Agastoroxenia, Saphonecrus, Synergus,
Synophrus and Ufo), are given in details.

Periclistus Förster, 1869

Type species: Aylax caninae Hartig, 1840.
Periclistus is very similar to Ceroptres in the shape of the first metasomal tergite but
females have the 2nd metasomal tergite completely fused with the 3rd (a suture present
between them in males). Head and mesosoma black, metasoma chestnut brown, with
darker posterior tergites. Antenna and legs yellow to partially chestnut brown; coxae dark
brown to black. Head delicately coriaceous to alutaceous, nearly as high as broad in front
view; gena not broadened behind eye; malar space very short, much shorter than height of
eye; malar space and lower face with strong striae, radiating from clypeus and reaching
eye and antennal sockets. Clypeus small, quadrangular, slightly higher than broad, with
distinct anterior tentorial pits, clypeo-pleurostomal line and epistomal sulcus; ventrally
rounded, not projecting over mandibles. Frons, vertex, occiput, postocciput and postgena
delicately coriaceous to alutaceous. POL slightly longer than OOL; transfacial distance
slightly shorter than height of eye. Antenna filiform, 12–13-segmented in female and 14–
segmented in male. Scutum uniformly delicately coriaceous; notauli complete, although
sometimes weakly impressed; median mesoscutal line usually extending at least to half of
scutum length. Scutellum rugose, with more delicate sculpture towards center of scutellar
disk and in between scutellar foveae. Scutelar foveae transversely ovate, only slightly
broader than high, well-delimited around, separated by central carina. Mesopleuron
transversely striate. Lateral propodeal carinae subparallel; central propodeal area
coriaceous, without setae; lateral propodeal area delicately uniformly coriaceous, with
relatively dense white setae. Forewing margin with long cilia; radial cell closed, at least
3.0 times as long as broad, areolet distinct, Rs+M nearly reaching basalis. Metasomal
tergites 2 and 3 fused in female, free in male, punctate in dorso-posterior part, sometimes
punctures indistinct; prominent part of ventral spine of hypopygium very short (Fig. 1).

Periclistus has an Holarctic distribution with 14 known species (Table 2),

which from seven species are known from America north of Mexico (Burks
1979); three species are known from the Western Palaearctic, P. brandtii, P.
caninae and P. idoneus known from Israel only (Belizin 1973). Four species of
Periclistus were described from the Eastern Palaearctic: P. mongolicus from
Mongolia (Belizin 1973), P. capillatus from Primorskij Kraj of Russia (Belizin
1968), and two species, P. natalis and P. quinlani from Japan, from Diplolepis
japonica (Walker) galls (Abe et al. 2007). P. capillatus and P. natalis were reared
by one of the co-authors (GM) also from galls of Liebelia fukudae (Shinji) in the
Far East of Russia and Hokkaido, Japan. Except L. fukudae, the genus Liebelia

7
Kieffer which associates with wild roses, is represented by other 7 species
described from Kyrgyzstan, Kazakhstan, Uzbekistan and Siberia and no doubts,
they support a number of undescribed Periclistus species (Belizin 1957,
Vyrzhikovskaja 1963).

Figure 1. Periclistus brandtii: a–h, female: a, head, anterior view, b, head, dorsal view, c,
mesosoma, anterodorsal view, d, mesosoma and propleura, anterior view, e, mesosoma,
dorsal view, f, mesosoma, lateral view, g, forewing, part with radial cell, h, metasoma,
lateral view. i, metasoma, lateral view, male.

8
Table 2. Known species of Periclistus: distribution and host associations.

Species Distribution Host plants/galls

P. arefactus McCracken & NA: USA, California Diplolepis sp. on wild roses
Egbert, 1922
P. brandtii (Ratzeburg, WP: entire Diplolepis sp. on wild roses
1831)
P. californicus Ashmead, NA: USA, California Diplolepis sp. on wild roses
1896
P. caninae (Hartig, 1840) WP: entire Diplolepis sp. on wild roses
P. capillatus Belizin, 1968 EP: Russia, Diplolepis sp. and Liebelia
Primorskij Kraj sp. on wild roses
P. idoneus Belizin, 1973 WP: Israel Unknown
P. mongolicus Belizin, 1973 EP: Mongolia Unknown
P. natalis Taketani & EP: Japan Diplolepis sp. and Liebelia
Jasumatzu, 1973 sp. on wild roses
P. obliquus Provancher, NA: USA, California Diplolepis sp. on wild roses
1888
P. piceus Fullaway, 1911 NA: USA, California Diplolepis sp. on wild roses
P. pirata (Osten Sacken, NA: Eastern USA Diplolepis sp. on wild roses
1863) and Canada
P. quinlani Taketani & EP: Japan Diplolepis sp. on wild roses
Jasumatzu, 1973
P. semipiceus (Harris, 1841) NA: USA, Diplolepis sp. on wild roses
Massachusetts
P. smilacis Ashmead, 1896 NA: USA, Florida Diastrophus smilacis on
Smilax
Total: 14 species

The biology and hosts of Periclistus idoneus described from Israel are
unknown yet (Belizin 1973). It is closely related to P. brandtii and must be
revised in order to confirm its validity (Pujade-Villar et al. 2003). Another
species, P. spinosissimae Dettmer, reared from Diplolepis spinosissimae (Giraud)
and known from the Netherlands (Dettmer 1924) and Great Britain (Eady and
Quinlan 1963) is closely related to P. caninae and must be revised in order to
confirm its validity (Pujade-Villar et al. 2003).
Periclistus species are associated with Diplolepis and Liebelia rose galls,
except one nearctic species, P. smilacis known from Florida and reared from galls
of Diastrophus smilacis (Ashmead 1896a). This host association was doubted for
a long time, however, one of the co-authors (GM, unpublished data) also reared P.
smilacis adults from galls of D. smilacis on Smilax sp. (a monocot vine). All
known gall wasps are associated with eudicots that is why this host shift is very
unusual (Ronquist and Liljeblad 2001). The biology of Periclistus species has
been studied in details in some holarctic species (e.g. Brooks and Shorthouse

9
1998, Shorthouse 1973, 1980). Larvae of some species can strongly modify the
gall structure of the host (Shorthouse 1973, 1980). Two common Western
Palaearctic species: P. brandtii usually attacks multilocular galls of Diplolepis
mayri (Schlechtendal) and D. rosae (L.), while P. caninae usually attacks
monolocular galls of D. nervosa (Curtis) and D. eglanteriae (Hartig). All
Periclistus species are monovoltine and known from the sexual generations
(Melika 2006).

Synophromorpha Ashmead, 1903

Type species: Synophrus sylvestris Osten Sacken, 1861 (desig. In Ritchie and
Shorthouse 1987b).
Originally Synophromorpha salicis Ashmead, 1903 was designated as the type-
species. Unfortunately the type-species of this genus is from unknown locality and its host
was supposed to be a dipterous gall-inducer on Salix. The type species has not been
located and probably was lost (Weld 1952, Burks 1979). Details on the taxonomy,
systematics, morphology, biology, host associations and phylogeny of Synophromorpha
are given in Ritchie and Shorthouse (1987b). The genus is most similar to Periclistus and
differs as follows: the mesoscutum is smooth to granulate, with strong setigerous
punctures anteriorly; notauli are very strong, complete, in a form of distinct deep grooves;
the ventral margin of the subalar triangle smooth, without rows of setigerous punctures;
the maxillary palp with five segments; T1 smooth and crescent shaped, T2+3 fused in
females but separate in males; the radial cell of the forewing is opened (Ritchie and
Shorthouse 1987b).

Only 6 species of Synophromorpha are known: 4 from the Nearctic and 2

from the Eastern Palaearctic (Table 3).

Table 3. Known species of Synophromorpha: distribution and host associations.

Species Distribution Host plants/galls

S. kaulbarsi Ritchie & NA: Mexico, Puebla, Unknown
Shorthouse, 1987 Naupan
S. rubi Weld, 1952 NA: USA, Illinois Diastrophus sp. on Rubus
S. sylvestris (Osten Sacken, NA: USA, Eastern Diastrophus sp. on Rubus
1861) Coast
S. taketanii Abe, 1998 Stem gall on Rubus
S. terricola Weld, 1952 NA: USA, DC and Diastrophus sp. on Rubus
Virginia
S. tobiasi Belizin, 1973 EP: Tajikistan, Unknown
Kyrgyzstan
Total: 6 species

Synophromorpha kaulbarsi described from Mexico is the most plesiomorphic

species in the genus and host associations are still unknown, probably some gall-
inducers on Rubus (Ritchie and Shorthouse 1987b). Synophromorpha tobiasi is

10
known from Tajikistan and Kyrgyzstan (Belizin 1973). The taxonomic status of
this species is uncertain and the type must be revised (Abe et al. 2007). The
second Eastern Palaearctic species, S. taketanii, was reared from stem swelling-
like galls on Rubus palmatus in Japan, however, whether it is a Diastrophus gall
or not must be clarified (Abe 1998, Abe et al. 2007).

Rhoophilus Mayr, 1881

Type species: Rhoophilus loewi Mayr, 1881
Rhoophilus is morphologically related to the holarctic inquiline genera Synergus,
Saphonecrus, and Synophrus, all of which typically attack oak cynipid galls. A sister
group relationship between Rhoophilus and the oak inquiline genera Synergus +
Synophrus + Saphonecrus was hypothesized by Ronquist (1994) and Liljeblad and
Ronquist (1998). Shared diagnostic characters include the following: the ventral margin of
the clypeau is straight not projecting over mandibles; radiating striae on the lower face
reaching or almost reaching the compound eye; the distance between occipital and oral
foramina is longer than the height of the occipital foramen; the position of the anterior end
of the metapleural sulcus is high; the mesoscutum with strong transverse ridges, the
mesopleuron also with longitudinal ridges; tarsal claws with a blunt small basal lobe.

The biology of Rhoophilus loewi has been controversial. Despite the fact that
the species had always been classified with the inquiline cynipids, its host was
unknown and the species was sometimes considered as the true gall inducer wasp
on Rhus species (Anacardiaceae) (Dalla Torre and Kieffer 1910, Ronquist 1999).
Recently it was demonstrated that R. loewi is an inquiline in galls induced by a
cecidosid moth genus Scyrotis on Rhus species (Anacardiaceae) and thus,
represents one of the few known cases where the host for a cynipid wasp is not
itself a cynipid. Rhoophilus is a lethal inquiline; its larval cells expand into the
hollow interior of the host gall resulting in death of the gall inducer (van Noort et
al. 2007).
Rhoophilus loewi and the recently described south african cynipid gall-
inducer Qwaqwaia scolopiae Liljeblad, Nieves-Aldrey & Melika on Scolopia
mundii (Salicaceae) represent the only cynipid taxa with an Afrotropical
distribution (Liljeblad et al. 2011). Ronquist and Liljeblad (2001) hypothesized
that the gall wasps (Cynipidae) arose in Europe, around the Black Sea, and that
the genera Eschatocerus (gall inducers on Acacia and Prosopis) and Rhoophilus
apparently spread later to South America and South Africa, respectively.
However, recent results may contradict this hypothesis. Eschatocerus and
Rhoophilus may represent older primitive lineages of cynipids and as such the
biogeographical history of the basal Cynipidae is still not clear (Nylander 2004a).
The presence of Rhoophilus, Qwaqwaia and Phanacis neserorum Melika &
Prinsloo in southern Africa, far from other centres of cynipid diversity, suggests
that other african groups may await discovery (Melika and Prinsloo 2007,
Liljeblad et al. 2011).

11
Ceroptres Hartig, 1840
Type species: Ceroptres clavicornis Hartig, 1840.
Body predominantly black, rarely chestnut brown or even orange; antenna and legs
light brown to yellow chestnut brown, except darker to black scape and coxae. Head
alutaceous to delicately coriaceous, broader than high in front view, with sparse white
short setae. Gena not broadened behind eye; malar space much shorter than height of eye,
with striae radiating from clypeus and reaching eye. Transfacial distance shorter than
height of eye; diameter of antennal torulus 3.0 times as large as distance between them
and slightly longer than distance between torulus and eye margin. Inner margins of eyes
slightly converging ventrally. Clypeus small, quadrangular, anterior tentorial pits, clypeo-
pleurostomal line and epistomal suclus distinct, ventral margin rounded, not projecting
over mandibles. Lower face with striae radiating from clypeus and reaching inner margin
of eye and antennal sockets, with two vertical more or less distinct raised carina running
from antennal sockets and reaching or not clypeus. Frons, vertex and occiput uniformly
alutaceous. Distance between occipital and oral foramens larger than height of occipital
foramen; gular sulci united well above hypostoma. Antenna of female slightly clavate, 12-
13-segmented, in male – 14-15-segmented; F2 slightly shorter or equal F1. Pronotum
dorso-medially 1/3-1/2 times shorter than measuring along lateral outer margin;
submedian pronotal pits narrow, transverse, separated by a median carina. Scutum
delicately coriaceous to alutaceous; notauli complete, well-impressed along entire length
or indistinct only in anterior 1/3; median mesoscutal line short, extending to 1/3 of scutum
length or in a form of short triangle. Scutellum coriaceous to rugose, rounded, scutellar
foveae transverse, more or less well-delimited posteriorly, separated by a distinct central
carina. Mesopleuron smooth, shining, with some very delicate transverse striae, especially
in antero-dorsal part; metapleural sulcus reaching mesopleuron in the upper 1/3 of its
height. Lateral propodeal carina subparallel. Forewing with short cilia on margin, radial
cell closed along wing margin. Tarsal claws with basal lobe. Metasoma nearly as high as
long in lateral view; metasomal tergite 2 small, with dense setae antero-laterally and free,
not fused with metasomal tergite 3, which occupying 2/3 or more of metasoma length.
Prominent part of ventral spine of hypopygium very short (Fig. 2).

Ceroptres, at least the palaearctic species, has two main diagnostic

morphological characters (autapomorphies): two raised vertical carinae on the
lower face and the metasomal tergite 2 is free (not fused with metasomal tergite 3)
and small (ratio of median length of metasomal tergite 2 to median length of
tergite 3 <1.0). Ceroptres is also the only Synergini in cynipid galls on oaks with
a smooth and shining metasomal tergite 1, reduced to a dorsal crescent-shaped
scale, without sulci. While the European species of Ceroptres are distinct from
other inquiline genera and particularly from Synergus, the situation for the
nearctic species is less clear. Weld (unpublished data) found specimens that are
intermediate between Ceroptres and Synergus. For example, the vertical carinae
extending from the ventral margin of the antennal sockets (which are well-
developed in European species) are incomplete or absent in the nearctic Ceroptres
specimens. Ritchie (1984) believed similarities between Synergus and Ceroptres
to support a close relationship between the two genera. This opinion has been
supported by Liljeblad and Ronquist (1998), who stated that the North American

12
species of Ceroptres resemble other inquiline genera more than they do European
species in the same nominal genus. However, close relationships between
Ceroptres and Synergus are not supported by recent sequence-based molecular
phylogenetic analyses, which find Ceroptres to represent a separate case for
evolution of inquilinism of oak cynipid galls. Molecular phylogenies suggest that
it is derived from a different gall-inducing ancestor which about we shall talk in
details later (Nylander 2004a, Ács et al. 2010).

Figure 2. Ceroptres cerri, female: a, head, anterior view, b, head, dorsal view, c,
mesosoma, anterodorsal view, c, mesosoma, anterodorsal view, d, mesosoma and
propleura, anterior view, e, mesosoma, dorsal view, f, mesosoma, lateral view, g,
forewing, part with radial cell, h, metasoma, lateral view.

13
 Ceroptres is distributed throughout the Holarctic Region and 23 valid species
are known (Table 4): six species from the Palaearctic and 17 from the Nearctic
(Ritchie 1984, Burks 1979, Melika and Buss 2002, Melika 2006, Abe et al. 2007,
Wang et al. 2012).

Table 4. Known species of Ceroptres: distribution and host associations.

Species Distribution Host plants

C. catesbaei Ashmead, 1885 NA: USA, Florida Quercus sect. Lobatae
C. cerri Mayr, 1872 WP: entire Quercus sect. Cerris
C. clavicornis Hartig, 1840 WP: entire Quercus sect. Quercus
C. confertus (McCracken & NA: USA, California Quercus sect. Quercus
Egbert, 1922)
C. cornigera Melika & Buss, NA: Eastern USA Quercus sect. Lobatae
2002
C. distinctus Wang, Liu & Chen, EP: China (Zhejiang) Unknown
2012
C. frondosae Ashmead, 1896 NA, USA, Missouri Unknown
C. inermis (Walsh, 1864) NA: USA, Illinois Gall-midges on Lobatae
oaks
C. kovalevi Belizin, 1973 EP: Russia, Quercus sect. Quercus
Primorskij Kraj
C. lanigerae Ashmead, 1885 NA: USA, Florida Quercus sect. Quercus
C. masudai Abe, 1997 EP: Japan, Korea, Quercus sect. Quercus
Russia, China
C. minutissimi Ashmead, 1885 NA: USA, Florida Quercus sect. Quercus
C. montensis Weld,1957 NA: USA, California Quercus sect.
Protobalanus
C. niger Fullaway, 1911 NA: USA, California Unknown
C. petiolicola (Osten Sacken, NA: Eastern USA Quercus sect. Quercus
1861)
C. politus Ashmead, 1896 NA, USA, Virginia Unknown
C. quercusarbos (Fitch, 1859) NA: USA, New York Quercus sect. Quercus
C. quercusficus (Fitch, 1859) NA: USA, New York Quercus sect. Quercus
C. quercusobtusilobae (Karsch, NA: USA, Texas Quercus sect. Quercus
1880)
C. quercuspisum (Fitch, 1859) NA: USA, New York Quercus sect. Quercus
C. quercustuber (Fitch, 1859) NA: USA, New York Quercus sect. Quercus
C. rufiventris Ashmead, 1896 NA, USA: Missouri Quercus sect. Lobatae
C. setosus Wang, Liu & Chen, EP: China (Zhejiang) Unknown
2012
Total: 23 species

14
 Four Eastern Palaearctic species, C. distinctus, C. kovalevi, C. masudai and
C. setosus are known. Ceroptres kovalevi and C. masudai associate with galls on
white oaks and are known from the Far East of Russia and Japan, Korea, Russia,
China, respectively (Belizin 1973, Abe 1997, Abe et al. 2007, Wang et al. 2012).
Host gall and host plant associations of two species from China, C. distinctus and
C. setosus, are unknown (Wang et al. 2012).
The nearctic species have never been revised and it is very difficult to
identify any of them, 16 species were listed in Burks (1979), and the only one
species, C. cornigera, known to associate with stem galls on red oaks, was
described later (Melika and Buss 2002).

Synergus complex of genera

Inquilines of the tribe Synergini attack the galls in the gallwasp tribes
Cynipini (oak gallwasps, hosts to the inquiline genera Agastoroxenia, Ceroptres,
Saphonecrus, Synergus, Synophrus and Ufo), Diplolepidini (rose gallwasps, hosts
to the inquiline genus Periclistus), Aylacini (herb gallwasps, hosts to the inquiline
genus Synophromorpha) and galls induced by Cecidosid moths on Rhus (hosts to
the inquiline genus Rhoophilus) (Ronquist 1994, 1999, Csóka et al. 2005, van
Noort et al. 2007). The morphological taxonomy of the inquilines which attack
hosts in the gallwasp tribes Cynipini has been studied in details (Mayr 1872;
Wiebes-Rijks, 1979; Nieves-Aldrey and Pujade-Villar 1985, 1986; Pujade-Villar
and Nieves-Aldrey 1990, 1993; Liljeblad and Ronquist 1998; Liljebald et al.
2008; Pujade-Villar et al. 2003, Melika 2006) and showed that five genera,
Agastoroxenia, Saphonecrus, Synergus, Synophrus and Ufo morphologically
differ from Ceroptres and form a distinct monophyletic lineage, which we call the
Synergus complex of genera.

Agastoroxenia Nieves-Aldrey & Medianero, 2010

Type species: Agastoroxenia panamensis Nieves-Aldrey & Medianero, 2010.
The genus is readily differentiated from other genera of Synergini by 13–segmented
antenna in both females and males; pedicel relatively long, 2.5 times longer than broad
and longer than scape and F2; F1 of male antenna strongly curved dorsally, excavated
medially, and expanded apically and basally. Metatarsal claws with small basal tooth, less
than one third as long as the apical tooth. Gena expanded behind compound eye; frontal
carinae present, branched near ocellar plate and vertex; irradiating lower face striae
strong, broad and blunt; ventral margin of clypeus slightly projected over mandibles;
lower face with irregular longitudinal rugae medially; distance between occipital foramen
and oral foramen shorter than height of occipital foramen; postgenal sulci meet at middle
part of postgenal bridge. Lateral pronotal carina indistinct; notauli complete but faint in
anterior one third of mesoscutum; mesoscutum with transverse interrupted and spaced
rugae; mesopleuron longitudinally striate with coriaceous sculpture between striae;

15
scutellar foveae large, inner margins widely diverge and opened posteriorly; lateral
propodeal carina broad, subparallel; radial cell obsoletely closed on wing margin by
depigmented R1, T2–3 covering 95% of metasoma; ventral projection of hypopygium as
long as high.

Morphologically, Agastoroxenia is related to Saphonecrus and Synophrus by

the 13-segmented antenna in females, however, in males the antenna is also 13-
segmented which is a unique autapomorphic feature among all the known genera
of Synergini. With slightly expanded genae, weakly sulcated dorsal part of 1st
metasomal tergite and the general sculpture of the mesoscutum and mesopleuron,
this genus resembles Synophrus, but it has strong frontal carinae, a character state
that is shared by the majority of the Synergus species.
This genus, with one known species, Agastoroxenia panamensis Nieves-
Aldrey & Medianero, is distributed in Panama, an inquiline reared from an
unidentified Andricus stem gall on Q. lancifolia (Quercus section, Lobatae)
(Nieves-Aldrey and Medianero 2010).

Saphonecrus Dalla Torre et Kieffer, 1910

Type species: Synergus connatus Hartig, 1840.
Body from entirely black to yellowish or light brown. Head delicately coriaceous to
alutaceous, nearly as high as broad in front view; gena not brodened behind eye; malar
space nearly 2.0 times shorter than height of eye, with striae radiating from clypeus and
reaching eye margin; lower face coriaceous, with striae radiating from clypeus and
reaching eye and antennal sockets and often extending into area betwen antennal socket
and inner margin of eye; median elevated area coriaceous. Clypeus small, with indistinct
tentorial pits, clypeo-pleurostomal line and epistomal sulcus indistinct; ventrally
projecting over mandibles, widely emarginated, incised or not medially, rounded or
straight. POL much longer than OOL; OOL always longer than diameter of lateral ocellus.
Transfacial distance shorter than height of eye. Inner margins of eyes parallel or slightly
converging ventrally. Frons delicately coriaceous, lateral frontal carina absent or very
indistinct; vertex and occiput delicately coriaceous. Antennae 13–14-segmented in female,
14–15-segmented in males; F1 in males curved in middle and slightly expanded apically.
Mesosoma flatenned dorso-ventrally, longer than high in lateral view. Pronotum
uniformly delicately coriaceous; lateral pronotal carina absent or present, corners of
pronotum dorsally rounded or strongly angled. Scutum with delicate interrupted
transverse striae. Notauli incomplete or complete; median scutal line absent or in a form of
a short triangle. Scutellum slightly elongated or rounded, uniformly rugose; slightly
overhanging metanotum. Scutelar foveae small, transverse, separated by central carina.
Mesopleuron striate, metapleural sulcus reaching mesopleuron in upper 1/3 of its height,
Lateral propodeal carinae uniformly broad, straight, subparallel or slightly converging
inwards ventrally; central propodeal area coriaceous, with white setae in anterior half;
lateral propodeal area delicately uniformly coriaceous, with relatively dense white setae.
Forewing longer than body, margin with short cilia; radial cell opened along wing margin.
Metasoma equal or slightly longer than head+mesosoma; metasomal tergites 2 and 3 fused,
without punctures, with few white setae antero-laterally; hypopygium with dense punctures,
prominent part of ventral spine of hypopygium very short, with few short white setae
(Figs 3–5).

16
Figure 3. Saphonecrus undulatus (“undulatus” group): a–i, female: a, head, anterior view,
b, head, dorsal view, c, antenna, d, mesosoma and propleura, anterior view, e, mesosoma,
anterodorsal view, f, mesosoma, lateral view, g, forewing, part with radial cell, h,
mesosoma, dorsal view, i, metasoma, lateral view. j, antenna, male.

17
Figure 4. Saphonecrus gallaepomiformis (“barbotini” group), female: a, head, anterior
view, b, head, dorsal view, c, antenna, d, mesosoma and propleura, anterior view, e,
mesosoma, lateral view, f, mesosoma, dorsal view, g, forewing, part with radial cell, h,
metasoma, lateral view.

18
Figure 5. Saphonecrus “sp.50-51” (“connatus” group): a–h, female: a, head, anterior view,
b, head, dorsal view, c, antenna, d, mesosoma and propleura, anterior view, e, mesosoma,
dorsal view, f, mesosoma, lateral view, g, forewing, part with radial cell, h, metasoma,
lateral view. i, antenna, male.

The genus Saphonecrus was established by Dalla Torre and Kieffer (1910)
for the oak inquiline species with an open radial cell (in contrast to Synergus,
where this cell is closed, except in Synergus plagiotrochi). Although the
separation of this genus from Synergus has subsequently been widely questioned
(Eady and Quinlan 1963, Ritchie 1984, Pujade-Villar and Nieves-Aldrey 1990),
the two genera have never been formally synonymised. Ritchie (1984) regarded
the characters distinguishing Saphonecrus from Synergus as apomorphic, and saw
19
Saphonecrus as a specialised monophyletic lineage within Synergus. Pujade-
Villar and Nieves-Aldrey (1990) revised the European species and maintained the
genus, but also questioned its validity. We consider Saphonecrus to be
polyphyletic and closely allied to Synergus. The two genera can be separated by a
combination of characters: Saphonecrus species have an open radial cell, female
antennae have 13 segments, and the lateral frontal carinae usually are absent. In
contrast, most Synergus species have a closed radial cell; female antennae are 14
segmented and lateral frontal carinae are usually present. The presence/absence of
the lateral frontal carinae and lateral pronotal carina in Saphonecrus (Synergus)
are inconsistent character states which about we shall talk in details later.
The Western Palaearctic species are associated mainly with galls on section
Cerris oaks, including Mediterranean evergreen species (Q. ilex, Q. suber, Q.
coccifera) and Q. cerris in Central Europe, while some are associated with galls
develop on white oaks (e.g. Q. petraea, Q. robur). Species associated with Cerris
and Quercus section oaks have a single generation per year and emerge after one
winter in the gall, while those on evergreen oaks have at least the potential for two
generations in a year (Pujade-Villar and Nieves-Aldrey 1990). It was showed that
the biology of the European Saphonecrus species can be divided into three
groups: (i) includes species with one annual generation, and associated with galls
on section Quercus oaks (S. connatus); (ii) also includes monovoltine species,
associated with galls on section Cerris oaks (S. undulatus and S. haimi; also S.
irani belongs to this group); (iii) some Mediterranean species, with bivoltine life
cycles, associated with galls on evergreen oaks (S. barbotini and S.
gallaepomiformis) (Pujade-Villar and Nieves-Aldrey 1990). Pujade-Villar (2004)
showed that the widely reported Synergus gallaepomiformis is a Saphonecrus, the
senior synonym of S. lusitanicus, valid name of which must be Saphonecrus
gallaepomiformis (Boyer de Fonscolombe, 1832). We follow this nomenclatorial
change in our review.
Saphonecrus is distributed mainly in the Holarctic: six valid species are
known for the Western Palaearctic, with a few uncertain status species (Pujade-
Villar et al. 2003); 7 species were listed for the Eastern Palaearctic (Abe et al.
2007); 4 species for the Nearctic (Burks 1979), and only two species were known
from the Oriental region (Weld 1926). Recently new species were described from
Japan (Wachi et al. 2011a) and eastern palaearctic/oriental China (Wang et al.
2010). The first inquiline, Saphonecrus hupingshanensis, which associate with
non-oak plant, Castanopsis carlesii, reared from a multi-chambered, midrib leaf
gall, was described (Liu et al. 2012). Recently two Andricus Hartig species were
transferred to Ufo, U. shirakashii (Shinji) and U. shirokashicola (Shinji) (Wachi
et al. 2011b), however, genetic distances and morphological analyses showed that
they are Saphonecrus, S. shirakashii and S. shirokashicola (Melika et al. 2012). A
large number of new Saphonecrus and near Saphonecrus (new genera) species are
under description. One species, S. connatus, thought to be a trans-palaearctic

20
species and was mentioned for Japan and Korea, reared from leaf galls on Q.
dentata (Sakagami 1949, Abe et al. 2007). However, this record might be well S.
chaodongzhui Melika, Ács & Bechtold known from China, which closely
resembles S. connatus (Melika et al. 2004). Thus, the total number of known valid
species of Saphonecrus is 23 (Table 5).
Two Saphonecrus species, S. serratus and S. areolatus, were described from
Philippines (Weld 1926). The analyses of the types showed that both species have
an unusually short pronotum dorsally, like in Cynipini. The head is transverse
from above; the frons with strong parallel striae radiating from toruli and reaching
ocelli and vertex; the radial cell of the forewing is opened, the forewing margin
with long dense cilia; lateral propodeal carinae are curved outwards, not parallel;
the last visible metasomal tergite with micropunctures, the prominent part the
ventral spine of the hypopygium much longer than usually in Saphonecrus. At the
same time, in S. serratus the female antenna with 13 flagellomeres and the 2nd
metasomal tergite dorsally is not incised, straight; the metanotal trough without
setae, glabrous, while in S. areolatus the female antenna with 12 flagellomeres
and the 2nd metasomal tergite dorsally is strongly incised; the metanotal trough
with dense white setae. These two species, definitely form a distinct unit, away
from the typical Saphonecrus [detailed morphoanalysis and nomenclatorial
changes concerning these two species will be done elsewhere].
Four Nearctic Saphonecrus species are known (Table 5), however, some of
them possess some non-typical character states for Saphonecrus and produce a
mixture of character states for Saphonecrus-Synergus and thus their assignment to
Saphonecrus genus must be examined in details.
Saphonecrus brevis is known from New Mexico and Arizona, reared from
stem swelling-like galls of Andricus ruginosus Bassett associated with white oaks.
This species is similar to the European Synergus plagiotrochi with its opened
radial cell in the forewing. Female antenna with 12 flagellomeres; lateral frontal
carinae are absent; the mesoscutum with strong transverse shiny rugae, space
between rugae shiny; notauli complete, reaching pronotum; lateral pronotal
carinae are absent, thus the pronotum laterodorsally is rounded; the mesopleural
sulcus nearly straight, do not bented towards the mesopleuron as in typical
Saphonecrus; tarsal claws are simple. The last visible tergite dorsally
microreticulate, not punctured as in other species of Saphonecrus and Synergus;
the metasomal petiole with very weak, delicate striae laterally, no striae dorsally
and the striae are not longitudinally orientated. So, S. brevis is not a “typical”
Saphonecrus and might well represent a distinct genus.
Saphonecrus brevicornis based on the original description might be a good
Saphonecrus (Ashmead 1896b).

21
Table 5. Known species of Saphonecrus: distribution and host associations.

Species Distribution Host plants

S. areolatus Weld, 1926 O: Philippines, Luzon Unknown
S. barbotini Pujade-Villar & WP: Iberia Quercus sect. Cerris
Nieves-Aldrey, 1985
S. brevicornis (Ashmead, NA: California Unknown
1896)
S. brevis Weld, 1926 NA: USA, Arizona, New Quercus sect. Quercus
Mexico
S. chaodongzhui Melika, Ács EP: China, Yunnan Unknown
& Bechtold, 2004
S. connatus (Hartig, 1840) WP: Europe Quercus sect. Quercus
S. diversus Belizin, 1968 EP: Russia, Primorskij Unknown
Kraj
S. excisus (Kieffer, 1904) EP: Bengal, Kurseong Lithocarpus elegans
S. favanus Weld, 1944 NA: DC and Missouri Quercus sect. Lobatae
S. flavitibilis Wang & Chen, EP: China, Zhejiang Unknown
2010
S. gemmariae Ashmead, 1885 NA: USA, Florida Quercus sect. Lobatae
S. haimi (Mayr, 1872) WP: Europe, N.Africa Quercus sect. Cerris
S. hupingshanensis Liu, Yang EP/O: China, Hunan Castanopsis carlesii
& Zhu, 2012
S. irani Melika & Pujade- WP: Iran Quercus sect. Cerris
Villar, 2006
S. gallaepomiformis (Boyer WP: Iberia Quercus sect. Cerris
de Fonscolombe, 1832)*
S. naiquanlini Melika, Ács & EP: China, Zhejiang Unknown
Bechtold, 2004
S. serratus Weld, 1926 O: Philippines, Luzon Unknown
S. shirakashii (Shinji, 1940) EP: Japan Quercus subgenus
Cyclobalanopsis
S. shirokashicola (Shinji, EP: Japan Quercus subgenus
1941) Cyclobalanopsis
S. sinicus Belizin, 1968 EP: China, Sichuan Unknown
S. tianmushanus Wang & EP: China, Zhejiang Unknown
Chen, 2010
S. undulatus (Mayr, 1872) WP: Europe Quercus sect. Cerris
S. yukawai Wachi, Ide & EP: Japan Quercus sect. Cerris
Abe, 2011
Total: 23 species
* earlier, in all relevant literature, this species was referred to Saphonecrus
lusitanicus (Tavares, 1902). After examination of types, Pujade-Villar (2004) made
the adequate nomenclatorial changes and proposed the new name, Saphonecrus
gallaepomiformis, which we follow herein.

22
 Saphonecrus gemmariae was described from Florida, on the basis of one
male which emerged from Callirhytis quercusgemmariae (Ashmead) gall on red
oaks (Ashmead 1885). The type supposed to be deposited at the Smithsonian
Institution, USNM, however, was not located in the collection by the curator, M.
Buffington and also by GM. The description of the male is very brief, not enough
to make a definite decision whether S. gemmariae is really a Saphonecrus and
thus must be treated as a species with uncertain status.
Saphonecrus favanus is known from the United States (DC and Missouri),
reared from a root gall of Dryocosmus favus Beutenmüller on red oaks (Weld
1944). Morphologically a non-typical Saphonecrus species: the frons, vertex and
mesoscutum with deep numerous punctures (somehow resembles Synergus
subterraneus); the head quadrangular in front view, the clypeus impressed, the
lower face delicately coriaceous, without radiating striae; female antenna with 11
flagellomeres; lateral frontal and lateral pronotal carinae are absent; the forewing
without cilia; the metapleural sulcus reaches metapleuron in the upper 1/3 of its
height; the petiole with parallel sulci all around; the last metasomal tergite
posterodorsally with micropunctures posterodorsally. So, S. favanus is not a
“typical” Saphonecrus and might well represent a distinct genus.
An ongoing research on Taiwan (T.C-T, GM) reveals a large number of new
Saphonecrus and near Saphonecrus species, reared from different galls, what
suggests that Saphonecrus is definitely a polyphyletic group and evolutionary
relationships within this group are much more complicated that were thought
earlier (Pénzes et al. 2009, Ács et al. 2010). Description of new species and new
genera are under preparation, a preliminary demonstration of diversity is
illustrated below.

Synergus Hartig, 1840

Type species: Synergus vulgaris Hartig, 1840.
Body length 0.8-4.5 mm, with sparse white setae. Predominantly black, chestnut
brown or orange brown, antenna and legs always much lighter than body. Wing veins dark
to pale brown. Head alutaceous to dull rugose, transverse in front view, with sparse white
setae, nearly 2.0 times as broad as long from above and always broader than high in front
view, slightly broader than mesosoma. Gena coriaceous, not broadened behind eye,
invisible in front view behind eye, converging ventrally. Malar space nearly 2.0 times
shorter than height of eye, with striae radiating from clypeus and reaching eye. POL
around 2.0 times as long as OOL. Transfacial distance longer than height of eye. Lower
face with more or less strong striae radiating from ventral margin of clypeus and usually
reaching eye and antennal sockets. Clypeus with radiating striae, delimited from lower
face by distinct anterior tentorial pits, epistomal sulcus and clypeo-pleurostomal line;
ventrally usually straight. Frons coriaceous to dull rugose, with or without punctures;
lateral frontal carinae strong or delicate, indistinct. Vertex and occiput dull rugose to
delicately coriaceous, with or without punctures. Antennae 14–segmented in female and
15–segmented in male; F1 in male straight or modified, excavated and curved medially,
broadened apically and/or basally. Mesosoma flattened dorso-ventrally, slightly longer

23
than high in lateral view, with white setae. Pronotum coriaceous to rugose, with white
setae, lateral pronotal carina strong or absent, lateral corners of pronotum strongly angled
or rounded. Scutum with or without transverse rugae, but always distinctly with
tarnsversely orientated sculpture. Notauli complete, deeply impressed or indistinct,
incomplete, shallowly impressed; median mesoscutal line extending to half or more length
of scutum or present in a form of short triangle only. Scutellum rounded, dull rugose to
delicately coriaceous, slightly overhanging metanotum. Scutellar foveae present,
separated by a more or less broad central carina. Mesopleuron striate. Metapleural sulcus
reaching mesopleuron in upper one-third of its height. Lateral propodeal carinae nearly
straight, subparallel or slightly converging inwards in the most posterior part. Forewing
margin with cilia; radial cell closed, except partially closed in S. plagiotrochi. Metasomal
tergites 2+3 fused, with more or less broad band of punctures posteriorly; prominent part
of ventral spine of hypopygium very short (Fig. 6).

Mayr (1872) subdivided Synergus into two sections: Section I contains those
species in which fused metasomal tergites 2+3 are with a more or less broad band
of punctures posteriorly and Section II contains species in which fused metasomal
tergites 2+3 have only a small dorso-posterior patch of punctures. This division is
artificial and does not reflect the phylogenetic relationships (Ács et al. 2010),
however, it was useful for the separation and classification of the species. Though
initially proposed on the basis of morphology, these sections are also associated
with apparent biological differences. Section I species predominantly have a
single generation per year (univoltine), and their development in a host gall is
rarely lethal to the gall-inducer. In contrast, Section II species predominantly have
two generations per year (bivoltine), and their attack frequently causes death of
the gall inducer (Csóka et al. 2005). Section II species are also characterised by
high between-generation variation in some adult morphological attributes,
particularly size and colour (Nieves-Aldrey and Pujade-Villar 1986, Pujade-Villar
1992, Wiebes-Rijks 1979), which can make morphology-based identification
difficult. As a result, morphology-based identification is often only possible to
complexes of morphologically similar species (Ács et al. 2010).
Many nearctic Synergus species differs from Palaearctic species by a simple
tarsal claw and partially smooth, incompletely sulcated first tergite while in all
Palaearctic species the tarsal claws posses a basal lobe and the first metasomal
tergite is completely sulcate. It was already showed for S. mexicanus and S.
castanopsidis (Pujade-Villar and Melika 2005). Preliminary morphological
analyses showed that there are at least three distinct morphological groups within
the nearctic Synergus, one of them does agree with the Palaearctic Synergus while
two others are distinct. Further research will definitely split the current Synergus
into a number of lineages as it was already found in Saphonecrus.

24
 Figure 6. Synergus facialis, female: a, head, anterior view, b, head, dorsal view, c,
mesosoma, anterodorsal view, e, mesosoma, dorsal view, d, mesosoma, lateral view, e,
mesosoma, dorsal view, f, mesosoma and propodeum, anterodorsal view, g, metasoma,
lateral view.

Pujade-Villar (2004) showed that the widely reported Synergus

gallaepomiformis should be named Synergus facialis Hartig, 1840, and Synergus
gallaepomiformis is a senior synonym of Saphonecrus lusitanicus and thus the
valid name for the later must be Saphonecrus gallaepomiformis (Boyer de
Fonscolombe, 1832). Synergus facialis (earlier widely referred as S.
gallaepomiformis) has been reared from galls of Andricus symbioticus Kovalev
and A. attractus Kovalev collected from Q. mongolicus, near Lake Khasan
(Primorskij Kraj, Russia) (Kovalev 1965) which, however, we strongly doubt and

25
probably it is S. chinensis or an undescribed species, morphologically very similar
to S. facialis (Abe et al. 2007).
Synergus is the most species-rich oak gall inquiline cynipid genus, with 109
known species (Table 6), with a long and complex history of taxonomic revision
(see Pujade-Villar et al. 2003, Melika 2006). Synergus has mainly a Holarctic
distribution, however, some species are known from the Oriental China and also
from the Neotropical region. Currently 40 valid species are known from the
Palaearctic: 30 from the Western Palaearctic (Pujade-Villar et al. 2003, Sadeghi et
al. 2006); 10 from the Eastern Palaearctic (Table 6). Status of some Eastern
Palaearctic species, described in the first half of 20th century, S. atamiensis, S.
hakonensis, S. iwatensis, S. jezoensis, S. mizunarae, is still uncertain and must be
solved (Abe et al. 2007).
Fifty five Synergus species are known from the Nearctic, 54 from America
north of Mexico (USA and Canada) (Table 6). The fauna of Mexico is thought to
be rich in inquiline species, though only two species have been actually recorded:
Synergus dugesi and S. filicornis (syn. S. furnessana), known from the neotropical
part of Mexico only and from Guatemala (Asmead 1899, Ritchie 1984, Ritchie
and Shorthouse 1987a).
The inquiline oak gallwasp fauna of the Neotropics have been poorly studied
and only representatives of Synergus genus are known for this region (Weld 1952,
Ritchie and Shorthouse 1987a, Nieves-Aldrey 2005, Pujade-Villar and Hanson
2006). However, the distribution range of the host plant, Quercus and particularly
section Lobatae, extends as far south as Colombia (Correa et al. 2004). Synergus
filicornis described from Guatemala was for a long time the only Synergus
recorded from Central and South America (Cameron 1883). Later, five species
were added: Synergus cultratus, S. mesoamericanus, and S. kinseyi (Ritchie and
Shorthouse 1987a) from Guatemala and Synergus nicaraguensis from Nicaragua
(Díaz and Gallardo 1998). The southernmost American record for an oak cynipid
inquiline was the recently described Synergus colombianus from Colombia
(Nieves-Aldrey 2005). Other 8 species were recently described from Panama
(Nieves-Aldrey and Medianero 2011). One species, S. filicornis, described from
Guatemala, is known also from Mexico and originally was described by Weld
(1913) as S. furnessana, however, later was synonymized to S. filicornis (Weld
1930). Thus, currently 14 Synergus species are known from the Neotropics (Table
6).

26
Table 6. Known species of Synergus: distribution and host associations.

Species Distribution Host plants

S. acsi Melika & Pujade-Villar, 2006 WP: Iran Quercus sect. Cerris
S. agrifoliae Ashmead, 1896 NA: USA, Quercus sect. Quercus
California
S. apicalis Hartig, 1841 WP: throughout Quercus sect. Quercus
S. atamiensis Ashmead, 1904 EP: Japan Unknown
S. atra Gillette, 1896 NA: USA, Quercus sect. Quercus
Colorado
S. atripennis Ashmead, 1896 NA: USA, Quercus sect. Quercus
Florida
S. atripes Gillette, 1896 NA: USA, Quercus sect. Quercus
Colorado
S. baruensis Nieves-Aldrey & NT: Panama Quercus sect. Lobatae
Medianero, 2011
S. batatoides Ashmead, 1885 NA: USA, Quercus sect. Quercus
Florida
S. bechtoldae Melika & Pujade-Villar, WP: Iran Quercus sect. Quercus
2006
S. bellus McCracken & Egbert, 1922 NA: USA, Unknown
California
S. bicolor Ashmead, 1885 NA: USA, Quercus sect. Quercus
Florida
S. campanula Osten Sacken, 1865 NA: Eastern Quercus sect. Quercus
USA
S. castanopsidis (Beutenmüller, 1918) NA: USA, Chrysolepis spp.
California
S. chinensis Melika, Ács & Bechtold, EP: China, Quercus sect. Quercus
2004 Korea
S. chiricanus Nieves-Aldrey & NT: Panama Quercus sect. Quercus
Medianero, 2011
S. citriformis (Ashmead, 1885) NA: USA, Quercus sect. Lobatae
Florida
S. clandestinus Eady, 1952 WP: throughout Quercus sect. Quercus
S. colombianus Nieves-Aldrey, 2005 NT: Colombia Quercus sect. Lobatae
S. confertus McCracken & Egbert, NA: USA, Quercus sect. Quercus
1922 California
S. coniferae Ashmead, 1885 NA: USA, Quercus sect. Lobatae
Florida
S. consobrinus Giraud in Houard, 1911 WP: Austria, Quercus sect. Cerris
Hungary
S. crassicornis (Curtis, 1838) WP: throughout Quercus sect. Quercus
S. cultratus Ritchie & Shorthouse, NT: Guatemala Quercus sect. Quercus
1987

27
S. dacianus Kierych, 1985 WP: Europe Quercus sect. Cerris
S. davisi (Beutenmüller, 1907) NA: USA, New Quercus sect. Lobatae
Jersey
S. diaphanus Houard, 1911 WP: Austria, Quercus sect. Quercus
Hungary
S. digressus McCracken & Egbert, NA: USA, Unknown
1922 California
S. dimorphus Osten Sacken, 1865 NA: USA, DC Unknown
S. distinctus McCracken & Egbert, NA: USA, Quercus sect. Quercus
1922 California
S. dorsalis (Provancher, 1888) NA: USA, Unknown
California
S. dugesi Ashmead, 1899 NA: Mexico Quercus sect. Quercus
S. duricoria Gillette, 1896 NA: USA, Quercus sect. Quercus
Delaware
S. elegans Nieves-Aldrey & NT: Panama Quercus sect. Quercus
Medianero, 2011 and Lobatae
S. erinacei Gillette, 1896 NA: USA, NY, Unknown
Iowa
S. facialis Hartig, 1840* WP: throughout Quercus sect. Quercus
S. ficigerae Ashmead, 1885 NA: USA, Quercus sect. Quercus
Florida
S. filicornis Cameron, 1883 NT: Guatemala Quercus sect. Quercus
S. flavens McCracken & Egbert, 1922 NA: USA, Quercus sect.
California Protobalanus
S. flavipes Hartig, 1843 WP: Austria, Quercus sect. Cerris
Hungary
S. flavus Kieffer, 1904 NA: USA, Quercus sect. Lobatae
California
S. gabrieli Nieves-Aldrey & NT: Panama Quercus sect. Lobatae
Medianero, 2011
S. garryana Gillette, 1893 NA: USA, Quercus sect. Quercus
Wash., Oregon
S. gifuensis Ashmead, 1904 EP: Japan Quercus sect. Quercus
S. hakonensis Ashmead, 1904 EP: Japan Unknown
S. hayneanus (Ratzeburg, 1833) WP: throughout Quercus sect. Quercus
S. ibericus Tavares, 1920 WP: Iberian Quercus sect. Quercus
Peninsula
S. ilicinus (Barbotin, 1972) WP: Spain, Quercus sect. Cerris
France
S. incisus Gillette, 1896 NA: USA, Quercus sect. Quercus
Colorado
S. incrassatus Hartig, 1840 WP: throughout Quercus sect. Quercus
S. itoensis Abe, Ide & Wachi, 2011 EP: Japan Quercus subgenus
Cyclobalanopsis

28
S. iwatensis Shinji, 1941 EP: Japan Unknown
S. japonicus Walker, 1874 EP: Japan, Korea Quercus sect. Quercus
S. jezoensis Uchida & Sakagami, 1948 EP: Japan Unknown
S. kinseyi Ritchie & Shorthouse, 1987 NT: Guatemala Quercus sect. Quercus
S. laeviventris (Osten Sacken, 1861) NA: USA, DC Quercus sect. Lobatae
S. laticephalus Nieves-Aldrey & NT: Panama Quercus sect. Lobatae
Medianero, 2011
S. lignicola (Osten Sacken, 1862) NA: Eastern Quercus sect. Lobatae
USA
S. luteus Nieves-Aldrey & Medianero, NT: Panama Quercus sect. Quercus
2011
S. magnificus Weld, 1957 NA: USA, Quercus sect.
California Protobalanus
S. magnus Gillette, 1891 NA: USA, Quercus sect. Lobatae
Michigan
S. medullae Ashmead, 1885 NA: USA, Quercus sect. Lobatae
Florida
S. mendax Walsh, 1864 NA: USA, Quercus sect. Lobatae
Illinois
S. mesoamericanus Ritchie & NT: Guatemala, Quercus sect. Quercus
Shorthouse, 1987 Panama
S. mexicanus Gillette, 1896 NA: USA, New Unknown
Mexico
S. mikoi Melika & Pujade-Villar, 2006 WP: Iran Quercus sect. Quercus
S. mizunarae Shinji, 1940 EP: Japan Unknown
S. multiplicatus Fullaway, 1911 NA: USA, Quercus sect. Quercus
California
S. nicaraguensis Díaz & Gallardo, NT: Nicaragua, Quercus sect. Quercus
1998 Panama and Lobatae
S. niger Fullaway, 1911 NA: USA, Unknown
California
S. nigroornatus McCracken & Egbert, NA: USA, Quercus sect.
1922 California Protobalanus
S. obtusilobae (Ashmead, 1885) NA: USA, Unknown
Florida
S. ochreus Fullaway, 1911 NA: USA, Quercus sect. Lobatae
California
S. oneratus oneratus (Harris, 1841) NA: Eastern Quercus sect. Quercus
USA
S. oneratus coloradensis Gillette, 1896 NA: USA, Quercus sect. Quercus
Colorado
S. pacificus McCracken & Egbert, NA: USA, Quercus sect.
1922 California Protobalanus
S. pallicornis Hartig, 1841 WP: throughout Quercus sect. Quercus
S. pallidipennis Mayr, 1872 WP: throughout Quercus sect. Quercus

29
S. pallipes Hartig, 1840 WP: throughout Quercus sect. Quercus
S. palmirae Melika & Pujade-Villar, WP: Iran Quercus sect. Cerris
2006
S. physocerus Hartig, 1843 WP: throughout Quercus sect. Quercus
and Cerris
S. plagiotrochi Nieves-Aldrey & Pujade- WP: Spain, Quercus sect. Cerris
Villar, 1986 France
S. pomiformis (Ashmead, 1885) NA: USA, Quercus sect. Lobatae
California
S. profusus McCracken & Egbert, NA: USA, Quercus sect. Quercus
1922 California
S. punctatus Gillette, 1896 NA: USA, Quercus sect. Quercus
Colorado
S. quercuslana (Fitch, 1859) NA: USA, NY, Quercus sect. Quercus
Iowa
S. radiatus Mayr, 1872 WP: throughout Quercus sect. Quercus
S. ramoni Nieves-Aldrey & NT: Panama Quercus sect. Lobatae
Medianero, 2011
S. reinhardi Mayr, 1872 WP: throughout Quercus sect. Quercus
S. reniformis McCracken & Egbert, NA: USA, Quercus sect.
1922 California Protobalanus
S. ruficornis Hartig, 1840 WP: throughout Quercus sect. Quercus
S. rufinotaulis Nieves-Aldrey & NT: Panama Quercus sect. Quercus
Medianero, 2011
S. rutulus McCracken & Egbert, 1922 NA: USA, Quercus sect. Quercus
California
S. similis Gillette, 1896 NA: USA, Quercus sect. Quercus
Colorado
S. splendidus Fullaway, 1911 NA: USA, Quercus sect. Lobatae
California
S. stelluli Burnett, 1976 NA: USA, Quercus sect. Quercus
California
S. subterraneus Giraud (in Houard, WP: Austria, Quercus sect. Quercus
1911) Spain
S. succinipedis (Ashmead, 1885) NA: USA, Quercus sect. Quercus
Florida
S. synophri Kieffer, 1901 WP: North Quercus sect. Cerris
Africa
S. thaumacerus (Dalman, 1823) WP: throughout Quercus sect. Cerris
and Quercus
S. tibialis Hartig, 1840 WP: throughout Quercus sect. Quercus
S. umbraculus (Olivier, 1791) WP: throughout Quercus sect. Quercus
S. variabilis Mayr, 1872 WP: Europe Quercus sect. Cerris
S. varicolor Fullaway, 1911 NA: USA, Quercus sect. Lobatae
California

30
 S. variegatus McCracken & Egbert, NA: USA, Quercus sect.
1922 California Protobalanus
S. villosus Gillette, 1891 NA: USA, Quercus sect. Quercus
Michigan
S. virentis (Ashmead, 1885) NA: USA, Quercus sect. Quercus
Florida
S. walshii Gillette, 1896 NA: USA, Unknown
Illinois
S. xialongmeni Melika, Ács & EP: China Quercus sect. Quercus
Bechtold, 2004
Total: 109 species
* earlier known as S. gallaepomifomis (Boyer de Fonscolombe, 1832), after the
examination of types, the valid name is Synergus facialis (Pujade-Villar 2004).

Synophrus Hartig, 1843

Type species: Synophrus politus Hartig, 1843.
Morphologically, Synophrus appears most closely related to Saphonecrus (Melika
2006, Pénzes et al. 2009). Two morphological characters have been suggested to separate
Synophrus from Saphonecrus: in Synophrus the metapleural sulcus reaches the anterior
margin of the metapleuron at half or slightly higher of its height and the 2nd metasomal
tergite has longitudinal sulci only laterally, being smooth dorsally, while in Saphonecrus
the metapleural sulcus reaches the anterior margin of the metapleuron in the upper 1/3 of
its height, and the entire 2nd metasomal tergite has longitudinal sulci (Pujade-Villar et al.
2003). In Synophrus lateral frontal carinae are absent; male antennae has 13 flagellomeres;
lateral propodeal carinae are absent, the pronotum is rounded in dorsal view; the radial cell
in the forewing is opened (Fig. 7) (Pénzes et al. 2009).

Currently 7 Synophrus species are known from the Western Palaearctic only
(Table 7), all of which are able to impose their own gall phenotypes on those of
their hosts (Pénzes et al. 2009).
One species, Synophrus mexicanus (Gillette, 1896) was listed for the nearctic
fauna (Burks 1979). Originally it was described as a Synergus (Gillette 1896),
later Weld (1952) transferred it to Synophrus and Ritchie (1984) affirmed that.
Examination of the type verified that it is a Synergus species and thus its original
status, Synergus mexicanus, was restored (Pujade-Villar and Melika 2005).
Weidner (1961) recorded Synophrus olivieri from the Indian Himalaya, but
this identification is almost certainly incorrect.
Originally described as a gall inducer (Hartig 1843), Synophrus was later
transferred to the Synergini on the basis of adult morphology (Ronquist 1994). An
inquiline life history is supported by indirect evidence. It was observed that S.
politus emerged from irregularly spherical and highly lignified stem swelling
galls that developed over the summer in the exact location in which spring bud
galls of a known gall inducing wasp, Andricus burgundus Giraud were initiated
(Pujade-Villar et al. 2003). This modification of the host gall is extreme among
cynipid inquilines, and attack by Synophrus is always lethal to the host gallwasp.

31
 Figure 7. Synophrus hungaricus, female: a, head, anterior view, b, head, dorsal view,
c, mesosoma, lateral view, e, mesosoma, dorsal view, d, mesosoma, dorsal view, e,
mesosoma and propodeum, anterodorsal view, f, forewing, part with radial cell, g,
metasoma, lateral view.

Ufo Melika & Pujade-Villar, 2005

Type species: Ufo abei Melika et Pujade-Villar, 2005.
Ufo is characterized by the next morphological characters: head trapezoid (in
females) or ovate (in males) in anterior view; strongly transverse, 2.5–2.8 times broader
than high in dorsal view; frons and vertex alutaceous or smooth; interocellar triangle very
narrow, posterior edge of frontal ocellus lies on line between anterior edges of lateral
ocelli; occiput and postgena smooth; anterior part of pronotum rectangular in dorsal view,
anterior and lateral sides form a right angle; pronotum descending vertically to propleura;
lateral part of pronotum going down from dorsal part also nearly at a right angle; strong
pronotal carina divides lateral part from frontal, both of which also oriented almost at
right angle to each other; tarsal claws with distinct acute basal lobe (Fig. 8).

32
Table 7. Known species of Synophrus: distribution and host associations.

Species Distribution Host plants/galls

S. hungaricus Melika & Mikó, WP: Hungary Quercus sect. Cerris
2009
S. libani Melika & Pujade-Villar, WP: Lebanon Quercus sect. Cerris
2009
S. olivieri Kieffer, 1898 WP: N.Africa, Iran, Quercus sect. Cerris
Caucasus
S. pilulae Houard, 1911 WP: Austria, Hungary Quercus sect. Cerris
S. politus Hartig, 1843 WP: Europe, Turkey, Quercus sect. Cerris
Jordan
S. syriacus Melika, 2009 WP: Iran, Syria Quercus sect. Cerris
S. hispanicus Pujade-Villar, WP: Iberia Quercus sect. Cerris
2009
Total: 7 species

In the allied genera, Synergus and Saphonecrus, the head is usually rounded,
quadrangular or slightly ovate in anterior view; less transverse in dorsal view,
only 1.6–2.1 times as broad as high; the frons and vertex always clearly
sculptured, at least delicately coriaceous; interocellar triangle much broader; the
occiput is sculptured; the lateral pronotal carina, when present, never with a
rectangular aspect in dorsal view, the pronotum more rounded in dorsal view; the
base of the tarsal claw is broadened, and the basal lobe present, however, not in a
form of an acute lobe. Also the host plant associations for all Ufo species is
typical – they always attack galls developing on Quercus section Cerris only
(Melika et al. 2012).
Four species of Ufo are known, three from the Eastern Palaearctic and one
from the Oriental Region (Table 8).

Table 8. Known species of Ufo: distribution and host associations.

Species Distribution Host plants/galls

U. abei Melika & Pujade-Villar, 2005 EP: Japan Quercus sect. Cerris
U. cerroneuroteri Tang & Melika, OR: Taiwan Quercus sect. Cerris
2012
U. koreanus Melika, Pujade-Villar & EP: Korea Quercus sect. Cerris
Choi, 2007
U. nipponicus Melika, 2012 EP: Japan Quercus sect. Cerris
Total: 4 species

33
 Figure 8. Ufo cerroneuroteri: a–g, female: a, head, anterior view, b, head, dorsal
view, c, antenna, d, mesosoma, lateral view, e, mesosoma and propleura, anterior view, f,
pronotum and mesoscutum, dorsal view, g, metasoma, lateral view. h, metasoma, lateral
view, male.

Based on the morphology and DNA sequences, Ufo belongs to the Synergus
complex of genera (Melika et al. 2005, 2007, 2012). Within the Synergus
complex, Ufo possesses with a few synapomorphies: the head is trapezoid in

34
anterior view and very narrow in dorsal view, rectangular aspect of the pronotum
has distinct rectangular aspect in dorsal view, the tarsal claw with a very acute
basal lobe, host cynipid galls associated exclusively with oaks of subgenus
Quercus, section Cerris. Ufo forms a distinct group within the Synergus complex
as detailed below.

Plant hosts of oak cynipid inquilines

Cynipid inquilines associate with gallwasps which are intimate parasites of

oak trees, and in order to understand their evolution the knowledge of their host
plant associations is important. Recent analyses primarily of Western Palaearctic
oak gallwasps have revealed a deep phylogenetic divide between gallwasp taxa
galling different oak sections (Cook et al. 2002, Ács et al. 2007, Liljeblad et al.
2008, Stone et al. 2009). A deep evolutionary split might be in host plant
associations of inquilines, particularly those of the Synergus complex (Ács et al.
2010). The aim of this chapter is to provide an outline of taxonomy, diversity and
distribution of oaks and oak related genera, to introduce briefly the phylogenetic
and phylogeographic patterns in oaks and oak relatives and how they influence
the phylogeny of cynipid inquilines.
Nine genera are recognised within the angiosperm family Fagaceae, which
contains two highly diverse morphological groups that dominate a variety of
habitats throughout the Northern Hemisphere. Fagaceae is divided into two
subfamilies: Fagoidea, with Fagus and Quercus genera [the latter is a host plant
for almost all known Cynipini] and Castaneoidea, with insect-pollinated
Castanea, Castanopsis, Chrysolepis, Lithocarpus and Notholithocarpus, all five
of which serve as hosts for Cynipini (Govaerts and Frodin 1998, Manos et al.
2008; Fig 9). The number of known species within Fagaceae is contraversial;
from 900 to ca. 1050 species are mentioned (Govaerts and Frodin 1998, Oh and
Manos 2008). Several tropical close relatives of oaks have in the past been
included in the genus Quercus, including the genus Trigonobalanus from
Malaysia and Borneo, Colombobalanus from Colombia, and Formanodendron
from China and southeastern Asia. These three genera have now been combined
in the genus Trigonobalanus (Nixon and Crepet 1989, Govaerts and Frodin 1998),
and though undoubtedly closely related to oaks, no gallwasps are known yet to
gall Trigonobalanus species. The family Fagaceae also includes the southern
beeches of the genus Nothofagus, with 36 known species distributed in South
America (Chile and Argentina) and Australasia (Li et al. 2007). Though no
Cynipini attack Nothofagus, they have been colonised by the gallwasp genera
Paraulax Kieffer and Cecinothofagus Nieves-Aldrey & Liljeblad (tribe
Paraulacini) documented in Chile and Argentina, however no Cynipidae are

35
known on this genus from Australasia (Nieves-Aldrey et al. 2009). Gallwasps
have thus colonised the plant family Fagaceae at least twice.

Figure 9. Phylogeny of Fagaceae (modified from Oh and Manos 2008)

Castanea (chestnuts) genus is represented by 8–10 species, native to

temperate regions of the Northern Hemisphere, with only one known gallwasp,
Dryocosmus kuriphilus. However, cynipid inquilines were not reared yet from
these galls.
Castanopsis (chinquapin oaks) is a genus of evergreen trees which contains
about 120 species, which are today restricted to tropical and subtropical eastern
Asia (Oh and Manos 2008). Total of 58 species are native to China, with 30
endemic; the other species occur further south in Indochina to Indonesia, and also
few species are known from Japan (http://www.efloras.org/). Recently a number
of new gallwasp and cynipid inquiline species were described from Castanopsis.
Chrysolepis (golden chinquapin oaks) is a small genus, endemic to the
western United States (from western Washington south to the Transverse Ranges
in Southern California, and east into Nevada), with two species. Ch. chrysophylla
and Ch. sempervirens. Some morphological features of the genus resemble those
of Castanopsis but differ in the nuts being triangular and fully enclosed in a
sectioned cupule, and in having bisexual catkins. The fruits somehow resemble
nuts of Castanea (chestnuts), but in Chrysolepis nuts develop 14–16 months
while in Castanea only 3–5 months and have evergreen leaves. Some inquilines
associate with few cynipid gallwasps develop on Chrysolepis species.
Manos et al. (2001) mentioned 334 species worldwide for Lithocarpus sensu
stricto (stone oaks), others listed only 100 species or even less (Flora of Taiwan
1996). Earlier about 100 species were treated in Pasania genus (e.g. Flora of

36
Taiwan 1996) which was synonymized to Lithocarpus and currently all are
treated together in Lithocarpus genus (Govaerts and Frodin 1998). All are native
to east and southeast Asia. They are evergreen trees with leathery, alternate
leaves, the seed is a nut very similar to an oak acorn, but with a very hard, woody
nut shell. Saphonecrus inquilines associate with cynipid gallwasps develop on
Lithocarpus species.
Notholithocarpus (tanbark oaks or tanoaks) with only one known North
American species, N. densiflorus, only recently was established (Manos et al.
2008, Oh and Manos 2008). It is an evergreen tree, native to the western United
States, California. It is most closely related to the north temperate oaks, Quercus,
but not to the Asian Lithocarpus. Few cynipids are known to associate with this
host.
Majority of Cynipini induce galls on members of a large, systematically well-
studied, wind-pollinated genus Quercus which is divided into two long-
established subgenera – the strictly Asian subgenus Cyclobalanopsis (the cycle
cup or ring cup oaks), and the more widespread subgenus Quercus (Camus 1936-
54, Nixon 1985, 1993, Govaerts and Frodin 1998, Manos et al. 1999).
The subgenus Quercus is divided into several discrete sections (Govaerts and
Frodin 1998), including Lobatae (the red oaks), Protobalanus (the golden cup or
intermediate oaks), Quercus sensu stricto (the white oaks), and Cerris. This
classification is based on molecular phylogenies (Manos et al. 1999, Manos and
Stanford 2001) and differs slightly from the alternatives based on morphological
or biochemical traits (e.g. Nixon 1993, Zhou et al. 1995). The section Cerris has
sometimes been divided into two subsections: Ilex species groups (with evergreen
leaves) and Cerris species groups (with semi-deciduous leaves) (Nixon 1993). Of
the 4 oak sections in the subgenus Quercus, Quercus sensu stricto is holarctic,
Lobatae and Protobalanus are restricted to North America, and Cerris is restricted
to the Palaearctic.
Worldwide, there are 531 recognised oak species (Govaerts and Frodin
1998). This total is divided between the Southeast Asian subgenus
Cyclobalanopsis (76 species), and the more widespread subgenus Quercus, with
455 species. The subgenus Quercus is most abundant in temperate regions of the
Northern Hemisphere. In the Neotropics oaks extend southwards as far as the
Colombian Andes (Nieves-Aldrey 2005). In the Eastern Palaearctic, oaks,
particularly Cyclobalanopsis species are a major component of climax forests in
highland areas from the eastern Himalayas southwards through the Philippines
and Malaysia into Java (Docters van Leuwen-Reijnvaan and Docters van Leuwen
1926).
Oak species richness is highest in the Nearctic (ca. 300 species) and the
epicentre of modern oak richness is in the Sierra Madre Occidental of Mexico (ca
135-200 species) (Nixon 1993, Manos et al. 1999). The Palaearctic supports ca.
170 species, with ca. 130 species in the Eastern Palaearctic and only 29 species in

37
the Western Palaearctic (Govaerts and Frodin 1998), with 13 in section Cerris and
16 in Quercus sensu stricto. The oak flora of the Western Palaearctic is clearly
defined, and only one oak species from the Western Palaearctic, Q. cerris, is also
recorded from western Afghanistan (Govaerts and Frodin 1998). The oak sections
Cerris and Quercus sensu stricto are widespread in the Eastern Palaearctic, and
the regional richness of oaks – with 32 species in China (Linkuo and Tao 1998),
at least 17 in Himalayan India, Nepal and Bhutan (Negi and Naithani 1995), and 6
in Japan (Ohwi 1961) – exceeds the Western Palaearctic’s 29 species.
The monophyly of two Fagaceae subfamilies, Castaneoideae and Fagoideae,
were suggested by their remarkably similar flowers. However, recent
phylogenetic reconstructions based on molecular data provide a strong evidence
to reject the monophyly of the subfamily Castaneoideae and showed two distinct
lineages within it (Manos et al. 2008, Oh and Manos 2008). Within this
paraphyletic subfamily there are several well supported lineages. Chrysolepis is
strongly supported as sister group to Asian species of Lithocarpus; while the
North American Notholithocarpus densiflorus is placed within the Quercus and
Castanea + Castanopsis clade, several nodes away from Lithocarpus (Fig. 9).
Phylogenies of castaneoid genera also strongly supports Castanea and the strictly
southeast Asian genus Castanopsis as sister taxa which agree with some
molecular studies and taxonomic treatments (Camus 1936-54, Manos et al. 2001,
Oh and Manos 2008).
Recent combined analysis resolved two clades of Quercus and Quercus
subgenus Quercus was shown to be non-monophyletic. Oh and Manos (2008)
recovered a mostly New World clade of species classified within subgenus
Quercus representing the sections Quercus s.str. (white oaks), Protobalanus, and
Lobatae. However, the Old World species classified within subgenus Quercus
section Cerris are more closely related to Quercus subgenus Cyclobalanopsis than
they are to other sections of subg. Quercus. The strictly Old World groups are
united into one clade, and because the monophyly of the oaks remains likely, this
novel pairing of temperate (sect. Cerris) and tropical (subg. Cyclobalanopsis)
lineages suggests that previous classifications of the oaks was problematic (Oh
and Manos 2008). More data are needed to resolve the placement of the two
groups of Quercus relative to N. densiflorus and Castanea + Castanopsis.
Oaks and their close relatives probably first diversified in Southeast Asia,
either during the Palaeocene (65–56 mya) or the Eocene (56–35 mya) (Zhou
1992, 1993, Cannon and Manos 2003, Manos et al. 1999), with an ancient divide
into two monophyletic lineages: (i) the subgenus Cyclobalanopsis and the section
Cerris of the subgenus Quercus and (ii) sections Lobatae, Quercus sensu stricto
and Protobalanus of the subgenus Quercus (Manos and Stanford 2001). The
Asian distribution of Cyclobalanopsis, the eurasian distribution of section Cerris,
and the absence of fossils of these two groups from the Nearctic suggest that oaks
originated and differentiated into these two basal lineages in Asia, but this

38
conclusion remains tentative (Zhou 1992, 1993, Manos and Stanford 2001). A
striking feature of phylogenetic analyses of the oak gallwasps (Ács et al. 2007,
Stone et al. 2009) is that (with the exception of host alternator species) they show
the same deep divide between genera associated with section Cerris on one hand,
and those associated with sections Quercus sensu stricto and the nearctic red oak
section Lobatae on the other. If the divergence between the oak sections occurred
in Eastern Asia, then it is plausible that this same region was the cradle for the
origin and initial diversification of oak gallwasps and their inquilines.
After the initial diversification of oaks and oak relatives in Asia, one lineage
dispersed into North America via the Bering Land bridge, which existed for long
periods through the Eocene and Oligocene (38–25 mya) into the early Miocene
(25–5 mya). Warmer global climates through the Eocene and early Oligocene
allowed oak forests to develop across northeastern Siberia and across the Bering
Land bridge into Alaska, Canada and Greenland (Thorne 1993, White et al. 1997,
Zhou 1992, 1993). Oaks were present in North America from the Eocene (56–35
mya), and there gave rise to the oak sections Lobatae, Protobalanus and Quercus
sensu stricto. Palaearctic white oaks were probably derived from ancestors that
spread westwards from North America back across the Bering land bridge in the
Oligocene (White et al. 1997, Manos and Stanford 2001), and the white oak floras
of these two major regions have had separate evolutionary histories for ca. 17
mya (Manos and Stanford 2001). From early Asian centres of diversity, oaks in
the sections Cerris and Quercus sensu stricto reached the Western Palaearctic by
spreading westwards along the foothills of the Himalaya and the temperate
highlands of Central Asia, and the western palaearctic radiations in both oak
sections are thought to be relatively recent, dating from around the Pliocene (ca.
5mya) (Manos and Stanford 2001).

Phylogeny of Synergini

Cynipoid wasps (Cynipoidea) are fall into two groups: macrocynipoids and
microcynipoids (Ronquist 1995, 1999). The phytophagous gallwasps (gall
inducers and inquilines, Cynipidae) are microcynipoids. During the last decade
the Cynipoidea and particularly Cynipidae have been subject to intense
phylogenetic research based on morphological characters of adults, gene
sequences and gall structures (Cook et al. 2002, Liljeblad 2002, Liljeblad and
Ronquist 1998, Liljeblad et al. 2008; Rokas et al. 2003, Ronquist and Liljeblad
2001, Ronquist and Nieves-Aldrey 2001, Stone and Cook 1998). The
macrocynipoids form a basal paraphyletic grade falling into three lineages, the
Austrocynipidae, Ibaliidae, and Liopteridae. The microcynipoids (Cynipidae and
Figitidae) are monophyletic and form two monophyletic sister lineages, the
phytophagous Cynipidae and the parasitic Figitidae (s. lato) (Fig. 10).

39
 Figure 10. Relationships among Synergini (in bold) and other gall-inducing Cynipidae
taxa (modified from Nylander 2004a)

The higher phylogeny of the Cynipidae was treated in several recent papers
(Ronquist 1994, 1999, Liljeblad and Ronquist 1998, Liljeblad et al. 2008,
Ronquist and Liljeblad 2001, Nylander 2004a). The phytophagous cynipid gall
inducers and inquilines are forming a natural group. In addition to their unique
phytophagous habit, a number of synapomorphies in their morphology is known
(Liljeblad and Ronquist 1998). Liljeblad and Ronquist (1998), Ronquist (1994,
1999), Ronquist and Liljeblad (2001) divided Cynipidae into three groups: (i)
inquilines (the tribe Synergini), (ii) the herb gallers (tribe Aylacini), and (iii) the
woody rosid gallers (tribes Diplolepidini, Eschatocerini, Pediaspidini and
Cynipini). A recent molecular phylogenetic analysis arised a conflict concerns the
monophyly of the woody-rosid gallers, which all induce galls on woody members
of the rosid clade of eudicots (Nylander 2004a). Based on DNA sequences, the
woody-rosid gallers that are not associated with oaks (Diplolepidini,
Eschatocerini and Pediaspidini) do not form a monophyletic group and are
distantly related to Cynipini.
The Cynipidae comprise of 7 gall-inducing tribes and one inquilines tribe,
Synergini. Early taxonomists (Hartig 1840, Ashmead 1903), based on
morphological similarities, grouped all inquilines together. Others have suggested
that the inquilines are polyphyletic, with each inquiline being more closely related
to its particular gallwasp host (Askew 1984). Shorthouse (1980) thought that
inquilines represent forms that never evolved the gall inducing capability on their

40
own. Morphological evidence has long supported the view that the Synergini are a
monophyletic group that diverged from within a paraphyletic tribe (Aylacini) of
herb gallwasps, with ancestry closest to the herb-galling genera Diastrophus and
Xestophanes (Ronquist 1994, Ronquist and Liljeblad 2001, Liljeblad 2002,
Liljeblad et al. 2008). Liljeblad (2002) hypothesized that cynipid inquilines in oak
galls are derived from gall inducing cynipids close to Diastrophus, via an
intermediate evolution of inquilinism in rose cynipid galls. This hypothesis placed
the oak cynipid inquilines close to the rose cynipid inquilines, represented by
species of Periclistus and Synophromorpha genera.
The inquilines are now believed to represent polyphyletic (or paraphyletic)
assemblage, in which species associated with rose cynipids are distinct from those
associated with oaks. Molecular phylogenetic evidence suggests that the
inquilines are not a monophyletic group, and instead comprise up to 3 distinct
evolutionary lineages with independent origins within the Aylacini assemblage:
(i) rose-associates inquilines in Synophromorpha and Periclistus, (ii) oak-
associated inquilines in Ceroptres, (iii) oak-associated inquilines in Synophrus-
Saphonecrus-Synergus-Ufo and the Afrotropical genus Rhoophilus attacking
moth-induced galls (Fig. 10) (Nylander 2004a, Melika 2006, van Noort et al.
2007, Liljeblad et al. 2008). However, the contradiction related to the origin of
inquilines can not be considered as fully resolved. Phylogeny based on a more
detailed taxon sampling is required.
Oak associated inquilines in Ceroptres form a distinct lineage, with
independent origin, however, only western palaearctic species were involved into
all molecular and morphological analyses. Morphologically Ceroptres species are
quite distinct from all species within the Synergus complex. However, North
American species resemble other inquilines more closely and some of them show
apomorphic similarities with Synergus in the structure of the petiolar annulus
(Ritchie 1984, Liljeblad and Ronquist 1998). Thus, it is possible that inclusion of
the nearctic Ceroptres species might affect the conclusions reached earlier on
inquilines relationships.
Rhoophilus loewi is the sister group of a lineage leading to a group of four
genera of inquiline cynipids (Saphonecrus, Synergus, Synophrus and Ufo)
attacking oak galls. This pattern allows two alternative hypotheses for the
evolution of this oak cynipid lineage. One is that Rhoophilus is the sole known
survivor of a once more diverse basal lineage of inquilines attacking a taxonomic
diversity of host gall inducers on plants other than oaks. For some reason the oak
cynipid inquilines represent a particularly successful descendant lineage of this
group. The alternative is that Rhoophilus itself represents a southern African
offshoot of an ancestral lineage otherwise closer in ecology and host plant
association to the extant oak cynipid inquilines (van Noort et al. 2007).

41
42
 Figure 11. (on the left) Preliminary phylogenetic tree of the Synergus complex.
Known species are shown in bold and the newly established lineages are numbered.
Group column assigns names to the lineages referred in the main text. The tree is based on
a Bayesian reconstruction from a segment of 28S D2 and cytochrome oxidase I (coxI)
gene sequences using MrBayes 3.1.2 parallel version (Ronquist and Huelsenbeck 2003).
Ceroptres was set as the outgroup for rooting the tree. Posterior probabilities of clades are
shown at the nodes. For wasp rearing, DNA laboratory protocol and sequencing we used
the same methods as in Pénzes et al. (2009), except that a shorter, 636 bp fragment was
used from the coxI gene. Sequences were aligned using Muscle 3.6 (Edgar 2004), with the
default settings. Separate data partitions were defined for 28S D2 and the different coxI
codon positions. According to MrModeltest 2.3 (Nylander 2004b), GTR+I+G substitution
model was choosen for 28S D2 and 2nd codon positions of coxI, while GTR+G for the
others. During the reconstruction, all four partitions were “unlinked” and rate parameter
was set to variable. All other priors and MCMC settings were kept at their default value.
Out of the 15 million generations of Markov chains, the first 8 million were dropped
(burn-in). Convergence was acceptable according to the visual inspection, small average
standard deviation of split frequencies and PSRF values. Details will be published
elsewhere.

Ufo species are known only from the Eastern Palaearctic and the Oriental
Region, synapomomorphies and generic diagnostic characters of which were
discussed in details (Melika et al. 2005, 2007, 2012). Ufo shares some
morphological characters with two allied genera, Saphonecrus and Synergus. Ufo
and Saphonecrus, have the radial cell along the forewing margin opened and the
female antenna is 13-segmented; both Ufo and Synergus have a distinct pronotal
carina but in Synergus the forewing is with a closed radial cell and the female
antenna is 14-segmented (Melika et al. 2005). These shared morphological
characters place Ufo into the Synergus complex of inquiline genera, phylogenetic
analysis of which was recently published without Ufo and thus the phylogenetic
position of which was still uncertain (Ács et al. 2010).
The recent phylogenetic reconstructions within the Synergus complex of
species support the monophyly of the large genus Synergus and the smaller
Synophrus, while the monophyly of Saphonecrus was rejected (Pénzes et al.
2009, Ács et al. 2010). These results are also supported by the new molecular
phylogeny which we propose for the first time in this review (Table 9, Fig. 11).
Three main clades can be established, althought their relationships are
unresolved: “Synophrus+barbotini’’, “connatus’’ and all others. The latter can be
divided into two (or three as discussed below) lineages. One of them is the genus
Synergus.

43
Table 9. Source of data in the phylogenetic reconstruction.

Lineage GenBank Accession number; D2, coxI (source)

Ceroptres clavicornis EF487120, EF486871 (Ács et al 2010)
Rhoophilus loewi EF487123, EF486876 (Ács et al 2010)
Saphonecrus barbotini EF487124, EF486877 (Ács et al 2010)
Saphonecrus connatus EF487125, EF486878 (Ács et al 2010)
Saphonecrus haimi EF487126, EF486879 (Ács et al 2010)
Saphonecrus lusitanicus EF487131, EF486881 (Ács et al 2010)
Saphonecrus shirakashii JX468370, JX468365 (Melika et al 2012)
Saphonecrus shirokashicola JX468368, JX468362-63 (Melika et al 2012)
Saphonecrus sp 13 Unpublished
Saphonecrus sp 15 Unpublished
Saphonecrus sp 18 Unpublished
Saphonecrus sp 23 Unpublished
Saphonecrus sp 32 Unpublished
Saphonecrus sp 35 Unpublished
Saphonecrus sp 4 Unpublished
Saphonecrus sp 46 Unpublished
Saphonecrus sp 48 Unpublished
Saphonecrus sp 50 Unpublished
Saphonecrus sp 51 Unpublished
Saphonecrus undulatus EF487133, EF486883 (Ács et al 2010)
Saphonecrus_sp 21 (TWTl12) JX468369, JX468364 (Melika et al 2012)
Saphonecrus_sp 44 (JP03) JX468371, JX468366 (Melika et al 2012)
Saphonecrus_sp_29 Unpublished
Saphonecrus_sp_30 Unpublished
Saphonecrus_sp_31 Unpublished
Saphonecrus_sp_34 Unpublished
Saphonecrus_sp_49 Unpublished
Synergus chinensis EF487140, EF486890 (Ács et al 2010)
Synergus consobrinus EF487189, EF486954 (Ács et al 2010)
Synergus crassicornis EF487147, EF486898 (Ács et al 2010)
Synergus flavipes EF487151, EF486903 (Ács et al 2010)
Synergus japonicus EF487167, EF486927 (Ács et al 2010)
Synergus mikoi EF487169, EF486928 (Ács et al 2010)
Synergus physocerus EF487185, EF486950 (Ács et al 2010)
Synergus plagiotrochi EF487187, EF486952 (Ács et al 2010)
Synergus sp 12 Unpublished
Synergus sp 24 Unpublished

44
 Synergus sp 24B Unpublished
Synergus sp 28 Unpublished
Synergus sp 7 Unpublished
Synergus thaumacerus EF487191, EF486956 (Ács et al 2010)
Synergus variabilis EF487219, EF486967 (Ács et al 2010)
Synergus xiaolongmeni EF487220, EF486968 (Ács et al 2010)
EF583959, EF579725 (Pénzes et al 2009, Ács et
Synophrus olivieri al 2010)
EF487224, EF579725 (Pénzes et al 2009, Ács et
Synophrus pilulae al 2010)
EF487223, EF579710 (Pénzes et al 2009, Ács et
Synophrus politus al 2010)
Ufo cerroneuroteri JX468367, JX468357-58 (Melika et al 2012)
Ufo nipponicus JX468367, JX468359-61 (Melika et al 2012)

However, what concern the monophyly of Synergus, it is important to state

that only western and eastern palaearctic Synergus species were involved into
these analyses, so the monophyly of worldwide Synergus must be treated
carefully. Many species assigned to the nearctic Synergus morphologically
strongly differs from palaearctic ones. Preliminary unpublished analysis showed
at least three distinct morphological groups within the nearctic Synergus and thus
involving those into phylogenetic analyses might strongly change our current
interpretation of the genus. Ács et al. (2010) showed that the palaearctic Synergus
is a monophyletic group, and the Eastern Palaearctic S. chinensis, S. xiaolongmeni
and S. japonicus nested among the Western Palaearctic species and thus, there is
no evidence that the Eastern and Western Palaearctic Synergus species represent
discrete radiations. Ács et al. (2010) also showed that Mayr’s long-accepted
morphology-based sections I and II within the genus Synergus do not represent
natural groups, and should be abandoned. For example, the widely-used Folmer
barcode region of the mitochondrial coxI gene has excellent potential to define
“molecular taxa” (MOTU) in the Synergus complex: some recognised Synergus
species corresponded to MOTUs others clearly do not (Ács et al. 2010). There is
one split within Synergus (“Synergus 1” and “Synergus 2”, Figs. 11, 17).
“Synergus 2” group includes 3 western palaearctic species, S. flavipes, S.
variabilis, S. plagiotrochi, all known to associate with section Cerris oaks, while
“Synergus 1” group includes those species, which prefer non-cerris section oaks.
However, subclade “Synergus sp. 28, 12, 24” within “Synergus 1” includes
undescribed eastern palaearctic species which from “Synergus sp 12, 24”
associate with section Cerris, while “Synergus sp 28” with section Quercus oaks.
Three species in the “Synergus 2” subclade bear two morphological peculiarities:
the absence of lateral pronotal and lateral frontal carinae while species in
“Synergus 1” subclade have strong lateral pronotal and frontal carinae except S.

45
consobrinus which lack these two characters. Thus, the two subclades within
Synergus hard to tell apart based on their morphology.
Synophrus with the 7 known western palaearctic species forms a monophyletic
group, morphologically similar to Saphonecrus in the absence of the lateral frontal
carinae, opened radial cell in the forewing, but the lateral pronotal carina is
absent, the pronotum is rounded in dorsal view and the male antennae has 13
flagellomeres; while in Saphonecrus the lateral pronotal carina present, the
pronotum with sharp angles in dorsal view and the male antennae has 12
flagellomeres. Phylogeny of Synophrus has been recently evaluated in details
(Pénzes et al. 2009).
Earlier data had been supported the hypothesis that all Synophrus species,
together with Saphonecrus gallaepomiformis and S. barbotini, form a
monophyletic group (Pénzes et al. 2009, Ács et al. 2010). Neither molecular nor
morphological data support the maintenance of Saphonecrus as a monophyletic
group, and hence it cannot be diagnosed as a distinct genus. The main features
that can be used to associate the two above-mentioned Saphonecrus species with
Synophrus are (i) the absence of the lateral pronotal carina, the pronotum is
rounded in dorsal view and (ii) the male antennae with 13 flagellomeres. This
indicates that Saphonecrus barbotini and S. gallaepomiformis, should be
transferred to Synophrus. However, some peculiarities of their biology,
distribution, host gallwasp and host plant associations as well as morphological
differences (shape of the head and metasoma, the sculpture of the mesoscutum,
completeness of notauli, Figs. 4, 7) suggest that they might be well treated as
separate genera (nomenclatorial changes will be done elsewhere).
The placement of Saphonecrus connatus, the type species of Saphonecrus, is
crucial to decide the status of Saphonecrus. The “connatus” clade with S.
connatus (Fig. 5) and two other Eastern Palaearctic lineages (sp 50 and sp 51
from Russia and Japan, respectively, Fig. 11), shares the two above mentioned
synapomorphies of Saphonecrus barbotini, S. gallaepomiformis and Synophrus
spp. The molecular evidence is equivocal with regard to the position of S.
connatus and allied species. All the molecular data together with some
morphological peculiarities, suggests that it is clearly a distinct unit (genus),
different from the “barbotini” clade. It is a separate early lineage within the
complex of species.
The third clade of eastern Saphonecrus, the “undulatus” group, known also
earlier (Pénzes et al. 2009, Ács et al. 2010) is very distant from “barbotini” and
“connatus” clades and not only by molecular evidences but also morphologically
they possess a number of synapomorphies: the shape of the head and its
sculpturing, the presence of a strong lateral propodeal carina, the absence of
notauli, very short mesoscutum and others (Fig. 3). Consistently with the
molecular phylogeny (posteriori probability 1, Fig. 11), all other clades of
Saphonecrus, including the Ufo genus, bear the same morphological peculiarities

46
as the “undulatus” group and thus differs from the “connatus” and “barbotini”
groups and Synophrus.
The “shirakashii” clade is a sister clade to “saphonecrus #1”+Ufo. In
“shirakashii” lineages the mesoscutum is always with short irregular transverse
striae and the surface between them is shiny, smooth; the head is quadrangular in
front view, more robust; the metasoma of females more elongated (Fig. 12) while
in “saphonecrus #1” the mesoscutum is delicately alutaceous or punctuate,
without distinct short irregular transverse striae; the head is ovate and less robust
from above, the female metasoma is more rounded (Fig. 13). The Ufo species
strictly associate with section Cerris oaks only and their morphology is also very
peculiar (Fig. 8), synapomorphies and genetic distances of Ufo from the
“shirakashii” group were discussed in details in Melika et al. (2012). All species
of the “shirakashii” and “saphonecrus #1” are known to associate exclusively with
the Quercus subgenus Cyclobalanopsis (see the chapter on host plant associations
below).
“Saphonecrus #2”, the sister group of “shirakashii” + “saphonecrus #1” +
Ufo, is known to associate with Lithocarpus and Cyclobalanopsis. In the females
of “saphonecrus #2” species the lower face and malar space is uniformly striate,
with striae reaching antennal toruli; the height of eye is 1.9 times as high as the
length of the malar space; the occiput and gena are smooth, shiny; antennal
pedicel 1.7 times as long as broad; the mesoscutum+mesoscutellum as long as
height of the mesosoma; scutellar foveae with smooth, shiny bottom while in “
saphonecrus #1” species the malar space with striae, the lower face only laterally
striate, with indistinct striae do not reaching antennal toruli, the mid part of the
lower face without striae; the occiput and gena are uniformly alutaceous; the
height of the compound eye 1.7 times as high as length of the malar space;
antennal pedicel 2.5 times as long as broad; the mesoscutum+mesoscutellum 1.2
times as long as height of the mesosoma; scutellar foveae with smooth, shiny
bottom, with few wrinkles (Fig. 14).
Morphological peculiarities of “shirokashicola” (Fig. 15) and “saphonecrus
group #3”, both associated with Cyclobalanopsis, are given in details in Melika et
al. (2012).
Morphologically a very distinct group is “saphonecrus #4”, species of which
exclusively associated with Lithocarpus, and possess a number of unique
morphological features in between all known Saphonecrus clades: rounded robust
head with strong frontal carinae, strong wrinkles in scutellar foveae and the
metasoma of which is punctuated (Fig. 16). Note also that its phylogenetic
position within the third main lineage is weakly supported (posteriori probability
0.53, Fig. 11).

47
 Figure 12. Saphonecrus shirakashii (shirakashii group): a–g, female: a, head, anterior
view, b, head, dorsal view, c, head, lateral view, d, antenna, e, mesosoma, lateral view, f,
mesosoma and propleura, anterior view, g, pronotum and mesoscutum, dorsal view, h,
mesoscutellum, dorsal view, i, metasoma, lateral view. j, metasoma, lateral view, male.

48
 Figure 13. Saphonecrus “sp23, sp35” (saphonecrus group #1, Fig. 11), female: a,
head, anterior view, b, head, dorsal view, c, head, lateral view, d, antenna, e, mesosoma
and propleura, anterior view, f, mesosoma, lateral view, g, pronotum and mesoscutum,
dorsal view, h, mesoscutellum, dorsal view, i, metasoma, lateral view.

49
 Figure 14. Saphonecrus “sp30, 32, 34” (saphonecrus group #2, Fig. 11), female: a,
head, anterior view, b, head, dorsal view, c, antenna, d, mesosoma and propleura, anterior
view, e, pronotum and mesoscutum, dorsal view, f, mesoscutellum, dorsal view, g,
mesosoma, lateral view.

50
 Figure 15. Saphonecrus shirokashicola (shirokashicola group, Fig. 11), female: a,
head, anterior view, b, head, dorsal view, c, antenna, d, mesosoma, part, lateral view, e,
pronotum and mesoscutum, dorsal view, f, mesoscutellum, dorsal view, g, mesosoma and
propleura, anterior view, h, metascutellum and propodeum, anterodorsal view.

51
 Figure 16. Saphonecrus “sp31, 13, 29, 4” (saphonecrus group #4, Fig. 11): a–b,
female: a, head, anterior view, b, head, dorsal view. c–d, antenna: c, female, d, male. e–j,
female: e, mesosoma, lateral view, f, mesosoma and propleura, anterior view, g, pronotum
and mesoscutum, dorsal view, h, mesoscutellum, dorsal view, i, metasoma, lateral view, j,
metasoma, part, lateral view.

52
 No doubts, that the current limits of the Saphonecrus genus must be changed,
a number of new monophyletic genera must be established. Nomenclatorial
changes with the erection of new genera and detailed morphological diagnoses,
with the description of new species from the Eastern Palaearctic and the Oriental
Region (Taiwan) will be done elsewhere. Also the two known Saphonecrus
species from Phillipinnes as well as some of the nearctic Saphonecrus species
must be tretaed in separate genera.

Host gall associations of oak cynipid inquilines

The world catalogue of cynipid inquilines with host gallwasp and host plant
associations is quite old (Dalla Torre and Kieffer 1910); the most recent
comprehensive study can be found in Ritchie (1984). The oak gallwasp
associations of the Western Palaearctic oak inquilines, Ceroptres, Saphonecrus,
Synergus and Synophrus, were under research prolong centuries and a huge
literature concerning the gall-inducer – inquilines relations is available (e.g.,
Hartig 1840, 1843, Mayr 1872, Eady and Quinlan 1963, Nieves-Aldrey and
Pujade-Villar 1985, 1986, Pujade-Villar 1992, Pujade-Villar and Nieves-Aldrey
1990, 1993, Nieves-Aldrey 2001, Pujade-Villar et al. 2003, Melika 2006 and
many others). Recently all available host association data on the Western
Palaearctic inquilines was collected in one review (Askew et al. 2012, in press),
except those species described from Iran (Sadeghi et al. 2006). Last review for the
Eastern Palaearctic was made by Abe et al. (2007). Rather less has been published
on the Nearctic fauna and all relevant earlier published data were collected in
Weld (1952) and Burks (1979). The Neotropical (Ritchie and Shorthouse 1987a,
Nieves-Aldrey 2005, Nieves-Aldrey and Medianero 2010, 2011) and Oriental
(Abe et al. 2007, Wang et al. 2010, Liu et al. 2012, Melika et al. 2012) Regions
are the most poorly studied, fragmentary data only available.
The host associations of non-oak cynipid inquilines, Periclistus, Rhoophilus,
Synophromorpha, were briefly introduced earlier. Here we deal only with those
genera which are associated with gallwasps on oaks and near oak genera:
Ceroptres and the Synergus complex (Agastoroxenia, Saphonecrus, Synergus,
Synophrus and Ufo). Most oak cynipid inquiline species tracking the distributions
of their host galls, which in turn track the ranges of their host oak species. The
inquilines with the most extensive geographic ranges are generalists associated
with widely distributed oaks. The most extreme example is Synergus facialis,
which attacks 53 different oak cynipid hosts (Askew et al. 2012, in press). Data to
date show some oak inquiline species to have restricted, regional ranges. For
example, Synergus plagiotrochi, S. ibericus, S. ilicinus, Synophrus olivieri, S.
pilulae, Saphonecrus gallaepomiformis and S. undulatus tend to attack only a
narrow range of host galls, and are often associated with Quercus species that

53
themselves have relatively limited geographical distributions (e.g. Quercus cerris,
Q. ilex, Q. suber, Q. coccifera, Q. faginea in Europe). Synergus ibericus and S.
ilicinus are only known from Spain and France, Synergus subterraneus only from
Spain, S. consobrinus only from Austria and Hungary, and S. diaphanus from the
Balkans eastwards towards Iran (Pujade-Villar et al. 2003). These patterns
suggest that, as for gall-inducers, inquiline cynipids show region specific faunas
that coincide with long-established glacial refuges in southern Europe (Stone et
al. 2001, Rokas et al. 2003) as shown recently for a generalist species, Synergus
umbraculus (Bihari et al. 2011). Based on the essential knowledge of the oak
cynipid inquilines of the Western Palaearctic, they can be classified into three
general categories.
One group of species are virtually host-specific, having been recorded from
only a single host, e.g. Synergus diaphanus, S. physocerus, S. subterraneus,
Synophrus species, some Saphonecrus species. The proportion of species in this
category contrasts with other zoogeographical regions, where majority of cynipid
inquiline species are known only from a single host gall (Burks 1979 for the
Nearctic; Abe et al. 2007 for the Eastern Palaearctic; Ritchie and Shorthouse
1987a, Nieves-Aldrey 2005, Nieves-Aldrey and Medianero 2010, 2011 for the
Neotropics). However, cynipid inquilines from other zoogeographical regions are
far less studied than the Western Palaearctic fauna, and many personal records
show that the apparent specificity in those regions is an artefact of limited
sampling (GM unpubl. data). In other cases, notably for Synophrus, it is hard to
establish host diversity (discussed above).
A second group of species (e.g. Ceroptres cerri, Saphonecrus
gallaepomiformis and Synergus hayneanus) show moderate host ranges for the
group, and are associated with up to 20 different host galls. The host galls
generally share some biological characteristics, such as the host gall shape, the
host oak taxon or the host plant organ on which the host gall is induced. This fact
suggests “entry points’’ for inquilines, but this topic is not yet explored.
The third group contains those inquilines known to attack more than 20
different host galls (e.g. Ceroptres clavicornis, Synergus pallicornis, S. pallipes
and S. umbraculus). The European inquiline species recorded from the largest
number of different galls is S. facialis with 53 different host galls, S. umbraculus
is one of the commonest oak cynipid inquilines in the Western Palaearctic, and
attacks more than 30 different oak gall hosts (Pujade-Villar et al. 2003, Askew et
al. 2012, in press).
Inquiline host specificity can also be considered in terms of the inquiline
richness associated with specific galls. The majority of gallwasp species are
attacked by 1 or 2 inquiline species, around 50% of known Western Palaearctic
species support 2–5 inquiline species while only ca. 10% support more than 5
inquilines species. The most extensively studied European oak galls for which the
most inquiline species have been recorded are those of the asexual generation of

54
Andricus kollari complex (14 species), A. lignicolus, A. quercustozae, A.
quercuscalicis and A. coriarius, and the sexual generation galls of Andricus
curvator and Neuroterus quercusbaccarum. Of course, that in interpreting host
ranges, we must take into account that the well-studied taxa are much better
sampled than those of less studied gall species and thus the records are highly
biased (Sanver and Hawkins 2000).
Little is known about the factors determining inquiline host range in oak gall
hosts. Phenological matching with the host gall – an appropriate developmental
stage – must be crucial, particularly for lethal species that must attack the host
larval chamber early in gall development. Host associations of such species are
more likely to be defined by phenological “windows of opportunity”. No doubts,
that the developing of special morphological structures (hairs, spines, surface
coatings of sticky resins), increases in gall wall thickness, that have been
interpreted as gall defences, probably enhance protection of the gall inducer
against lethal inquilines and parasitoids (Stone and Cook 1998, Stone and
Schönrogge 2003, Bailey et al. 2009, Stone et al. 2012). The significance of
resource availability is illustrated by the fact that the small pip-like bud and catkin
sexual generation galls of many Andricus species have few or no inquilines
(Stone et al. 1995).
Majority of inquiline species are associated with species within a single host
genus while some of them are present in galls of five or even more host genera.
The number of inquiline species associated with each host cynipid genus
increases with the number of host gall forms per genus (Melika 2006). There is a
weaker positive correlation between the number of host specific inquiline species
and the total number of inquiline species associated with each host cynipid genus.
Exceptions to this trend are the genera Plagiotrochus with more host-specific
inquiline species than expected, and Neuroterus with fewer host-specific inquiline
species. It is not clear yet what the selective benefits of specialisation for
inquilines are. Are they better synchronised with their host galls, or, compared to
generalists, more competent to manipulate the tissues in their host galls?
Similarities in the inquiline faunas associated with different host genera
might be explained by other factors, namely history. In the Western Palaearctic,
for example, two main generic groupings are apparent: (i) one group includes
Plagiotrochus, Chilaspis, Dryocosmus and Aphelonyx, while the second includes
the remaining genera, including Andricus. The phylogenetic relationships among
genera of oak cynipid gallwasps suggest that closely related gall inducers share
inquilines recruited by their common ancestors (Ronquist 1994, 1995, 1999,
Liljeblad and Ronquist 1998, Ronquist and Liljeblad 2001, Liljeblad et al. 2008,
Stone et al. 2009, Ács et al. 2010).
It is also possible that the groupings reflect similarities in traits used by
inquilines to select hosts, regardless of gallwasp and inquiline relatedness.
Aphelonyx, Chilaspis, Dryocosmus, Plagiotrochus and some other genera are

55
associated entirely or predominantly with oak hosts in the oak section Cerris
while others associate with other Quercus section and oak related genera. The
host plant associations of inquilines are considered further below.
Further we shall discuss in details the host gallwasp associations within
different oak cynipid inquiline genera.

Ceroptres. Two western palaearctic Ceroptres species are known only.

Ceroptres clavicornis is a generalist, has been reared from 30 different cynipid
host galls, on section Quercus oaks (white oaks) (Askew et al. 2012, in press). No
preferred gallwasp genus was found for this species, it was reared mainly from
galls of Andricus (usually asexual forms), but also associates with Callirhytis,
Cynips and Neuroterus (Pujade et al. 2003). Ceroptres cerri appears to be more
specialised and attacks galls of a some sexual forms of Andricus species,
Aphelonyx cerricola (Giraud), Dryocosmus cerriphilus (Giraud), Cerroneuroterus
and Plagiotrochus species and was recorded also in galls affected by Synophrus
politus (Pujade et al. 2003), all on section Cerris oaks (Pujade et al. 2003, Melika
2006).
Four eastern palaearctic Ceroptres species, C. distinctus, C. kovalevi, C.
masudai, and C. setosus are known (Abe et al. 2007, Wang et al. 2012).
Ceroptres kovalevi was reared from unidentified galls (Belizin 1973). C. masudai
is known from galls of Andricus kashiwaphilus, A. mukaigawae and Trigonaspis
(=Ussuraspis) nervosa (Kovalev) from Japan and Russia (Abe 1997, GM,
personal data); from A. targionii in Japan (Abe 1997); from leaf galls of
undescribed Trigonaspis (=Ussuraspis) sp. in Russia (GM, personal data);
occassionally emerged from galls of Callirhytis hakonensis Ashmead (= A.
symbioticus Kovalev) (Wachi and Abe 2009). Gall host associations of two
species described from China are unknown (Wang et al. 2012).
Nearctic Ceroptres species are known to associate with 4 Andricus Hartig , 2
Callirhytis Förster, 1 Bassettia Ashmead, 1 Acraspis Mayr, 1 Xanthoteras
Ashmead and 1 Neuroterus Hartig species (Burks 1979). One nearctic species, C.
montensis, known from California only, was reared from the galls of Andricus
reniformis McCracken et Egbert which associate with the Protobalanus section
oaks (Weld 1952).
One nearctic species, C. inermis, is known to associate with a gall-midge,
Cincticornia pilullae (Osten Sacken) (Diptera: Cecidomyiidae) (Burks 1979);
another Ceroptres has been recorded from rose cynipid galls (Ritchie 1984),
however, this record should be confirmed.
No species of Ceroptres are known yet from the Neotropics.

Agastoroxenia. This genus, with only one known species, Agastoroxenia

panamensis Nieves-Aldrey & Medianero, is distributed in Panama, an inquiline in

56
unidentified Andricus induced stem galls on Q. lancifolia (red oaks) (Nieves-
Aldrey and Medianero 2010).

Saphonecrus. Currently 23 species of Saphonecrus are known worlwide

(Table 5). All known Saphonecrus species except two, are inquilines in oak and
oak-related cynipid galls.
The western palaearctic species are associated mainly with galls induced on
section Cerris oaks, including Mediterranean evergreen species (Q. ilex, Q. suber,
Q. coccifera) and Q. cerris in Central Europe. Three species, Saphonecrus haimi,
S. irani and S. undulatus, which form a monophyletic group and have one
generation per year, attack galls of Aphelonyx cerricola (Giraud),
Cerroneuroterus lanuginosus (Giraud), Chilaspis nitida (Giraud), Ch. israeli
(Sternlicht), Pseudoneuroterus saliens (Kollar) and galls modified by Synophrus
politus (Pujade-Villar et al. 2003, Melika 2006). Two species, S. barbotini and S.
gallaepomiformis, which formed the second monophyletic lineage within
Saphonecrus and associated with Mediterranean evergreen oak species (Q. ilex,
Q. suber, Q. coccifera) and have two generations per year, attacks Plagiotrochus
galls only, especially woody galls of P. britaniae Barbotin and P. coriaceus
(Mayr) in twigs (Pujade-Villar and Nieves-Aldrey 1990). The third clade is
formed by the western palaearctic S. connatus and two undescribed eastern
palaearctic Saphonecrus species reared from galls on white oaks in the Far East of
Russia and Japan (Hokkaido) (GM, personal data). Saphonecrus connatus attacks
some Andricus species and galls of Callirhytis glandium (Giraud), Cynips
quercusfolii (L.), Neuroterus anthracinus (Curtis) and N. quercusbaccarum (L.).
Two undescribed Saphonecrus species from the Far East of Russia and Japan
were reared from undescribed bud galls and the asexual galls of Callirhytis
hakonensis (= Andricus symbioticus).
From 13 described Eastern Palaearctic and Oriental Saphonecrus species for
8 species no gallwasp and plant host associations are known (Table 5).
Saphonecrus excisus was reared from Neuroterus haasi Kieffer galls (Dalla Torre
and Kieffer 1910). Two species, S. shirakashii and S. shirocashicola, were reared
from undescribed leaf galls which belong to the newly described Cycloneuroterus
genus (Tang et al. 2012b). Number of new Taiwanese Saphonecrus species and
new genera, related to Saphonecrus, which for the host gallwasp associations are
known also, are under description and will be published elsewhere soon.
For three nearctic Saphonecrus species host gall associations are known: S.
brevis was reared from galls of Andricus ruginosus Bassett, S. favanus
(taxonomic position of which is problematic) – from root galls of Dryocosmus
favus Beutenmüller (taxonomic assignment of which is problematic, Ács et al.
2007), S. gemmariae – from stem swelling-like galls of Callirhytis
quercusgemmariae (Ashmead) (Burks 1979).

57
 Two Saphonecrus species are known to associate with non-cynipid oak galls.
Saphonecrus haimi may occasionally occur in cecidomyiid galls and was reared
from Janetia cerris (Kollar) (Diptera: Cecidomyiidae) galls on Q. cerris leaves
(Melika 2006). Saphonecrus yukawai described from Japan, known to associate
with the gall midge Ametrodiplosis acutissima (Monzen) (Diptera:
Cecidomyiidae) on Cerris section oak, Q. acutissima only (Wachi et al. 2011a).
Because S. yukawai has been reared only from A. acutissima galls on Q.
acutissima, this new inquiline is probably the first known species specialized to
depend on cecidomyiid galls. Numerous cecidomyiid species are known to induce
galls on Fagus sp., however, only a few species of this family are known to
induce galls on Quercus sp. (Yukawa and Masuda 1996, Yukawa et al. 2005).

Synergus. Host gall associations of the western palaearctic Synergus species

are well-known and were analysed in many works in details (Nieves-Aldrey 2001,
Pujade et al. 2003, Melika 2006, Askew et al. 2012, in press) and already were
presented above.
Data on the gallwasp associations of the nearctic Synergus is very poor and
majority of records are only those given in the original description of species, all
data on which was collected in Burks (1979). Only one species, S. agrifoliae, is
known to associate with genus Neuroterus; one-one species with Acraspis,
Belonocnema, Xanthoteras, 2 with Atrusca, 3 with Amphibolips, 3 with
Heteroecus, 6 with Andricus, 11 with Disholcaspis, and 12 with Callirhytis.
Usually only one species of Synergus is known for one-one gallwasp species,
however, some of them support more, for example, Heteroecus pacificus
(Ashmead) – 3 species, Callirhytis quercuspomiformis (Bassett) – 5 species
(Burks 1979).
Gall associations of the neotropical species were also discussed (Ritchie and
Shorthouse 1987a, Nieves-Aldrey 2005, Nieves-Aldrey and Medianero 2011).
From 10 Eastern Palaearctic Synergus species only for two species, the
bivoltine S. gifuensis and univoltine S. japonicus, the host associations are known
(Abe et al. 2007). The first generation of Synergus gifuensis develops in the
asexual galls of Andricus mukaigawae and A. kashiwaphilus while the second
emerges from sexual galls of Biorhiza weldi; S. japonicus associates with the
asexual galls of A. mukaigawae and A. kashiwaphilus (Abe 1990, 1992, Pujade-
Villar et al. 2002). One species, S. itoensis, appeared to have a capability to
induce its own gall in the seed coat of the acorn of Q. (C.) glauca (Abe et al.
2011). Eight new Synergus species from Japan, Far East of Russia and Taiwan,
which for the host gallwasp associations are known also, are under description
and will be published elsewhere soon.
One western palaearctic species, Synergus variabilis, has been also reared
from galls of the cecidomyiid gall midges Janetia cerris (Kollar) and Dryomyia
circinnans Giraud (Diptera, Cecidomyiidae) (Askew 1999).

58
 Synophrus. Pujade-Villar et al. (2003) observed that Synophrus politus
emerged from irregularly spherical and highly lignified stem swelling galls that
developed over the summer in the exact location in which spring bud galls of a
known gall inducing wasp, Andricus burgundus Giraud, were initiated. This
modification of the host gall is extreme among cynipid inquilines, and in contrast
to some inquiline cynipids, attack by Synophrus is always lethal to the host
gallwasp. The host of Synophrus is very small at the time of inquiline attack, and
is crushed and disintegrates in the first stages of inquiline takeover. The resulting
Synophrus-controlled gall morphologies are specific to particular Synophrus
species, as is also the case in true gall inducers. Other gallwasp hosts may be
usurped in this way, but remain undetected due to the completeness of inquiline
control of the gall phenotype. This possibility is suggested by the fact that
Synophrus can be abundant even where A. burgundus is unknown. Recent
evidence suggests that multiple gallwasps have cryptic sexual generations that are
morphologically indistinguishable or very similar to Andricus burgundus (Stone
et al. 2008) and these may also serve as hosts for Synophrus species.

Ufo. Ufo cerroneuroteri, known from Taiwan only, was reared exclusively
from the spangle galls of the asexual generation of Cerroneuroterus vonkuenburgi
(Dettmer), while U. nipponicus, known from Japan, was reared from spangle galls
of asexual generations of Cerroneuroterus monzeni (Dettmer) and C.
vonkuenburgi, and also from asexual galls of Trichagalma acutissimae (Monzen).
A few wasps emerged from leaf galls of Andricus kunugifoliae (Shinji) [for the
current status of this species see Abe et al. 2007] (Melika et al. 2012).

Plant host associations of oak cynipid inquilines

The Fagaceae has its centre of generic diversity in Southeast Asia, and it was
thought that the Cynipini only attack a relatively small group of predominantly
temperate taxa within this diverse family. Almost all oak gallwasps, which with
the majority of Ceroptres and Synergus complex inquiline species are associated,
induce galls on oaks, species in the genus Quercus subgenus Quercus, and within
it attack all four sections of oaks: Quercus sensu stricto, Lobatae, Cerris and
Protobalanus (see the chapter on Plant hosts of oak cynipid inquilines). Gallwasps
attack all of these sections, however, with the exception of the host-alternating
species, they attack only closely related members of a single oak section (Cook et
al. 2002). In North America, for example, the gallwasp faunas of white and red
oaks are completely distinct, and no gallwasps attack species in both groups
(Cornell 1985, 1986, Abrahamson et al. 1998, Melika and Abrahamson 2002).
Kinsey’s surveys of the Nearctic oak gallwasp fauna found host associations to be

59
strongly conserved within large groups of genera. For example, all 96 species
recognised as belonging to the genus Cynips L. are associated only with oaks in
Quercus sensu stricto (Kinsey 1936). With the exception of the host-alternating
species and few others, the same specificity is seen on the two oak sections
(Cerris and Quercus sensu stricto) native to the Palaearctic (Stone et al. 2002).
Nearly all known oak cynipid inquilines associate with gallwasps on all four
sections of Quercus subgenus Quercus.
Two gallwasp species are known to attack the two endemic western US
Chrysolepis (Ch. chrysophylla and C. sempervirens): Dryocosmus castanopsidis
(Beutenmueller) from Oregon and California (Burks 1979), and Dryocosmus
rileypokei Morita & Buffington also from California (Buffington and Morita
2009). Only one inquiline species, Synergus castanopsidis was reared from D.
castanopsidis galls (Beutenmüller 1918, Pujade-Villar and Melika 2005); no other
inquilines are known to associate with Chrysolepis.
A single cynipid, Andricus mendocinensis Weld, galls Notholithocarpus
densiflorus in Mendocino County, California (Burks 1979). No inquilines were
described yet which are known to associate with Notholithocarpus.
Dryocosmus kuriphilus (Yasumatsu), one of very few economically
important gallwasps, attack different species of chestnuts, Castanea. Outbreaks of
this species, native to China, have caused serious damage to local chestnut
industries following their introduction to Japan, Korea, the United States and
Europe (Payne et al. 1975, Kato and Hijii 1993, Gibbs et al. 2011). Only a single
female Synergus sp. was reared from D. kuriphilus in Japan (Ôtake et al. 1982),
which might emphasize the extreme rarity of inquilines in this gall or it is a false
data due to a non-acurate rearing technique.
Despite the significance of Quercus subgenus Cyclobalanopsis in Asia, only
a handful of gallwasps were known to induce galls on them: six unnamed cynipid
species were reported that depend on species of Cyclobalanopsis in Japan
(Yukawa and Masuda 1996). Recent research in the Eastern Palaearctic and
Oriental region (Japan, China and Taiwan), however, showed that the diversity of
cynipids galling Quercus subgenus Cyclobalanopsis and also Castanopsis and
Lithocarpus is high, a new genus, Cycloneuroterus Melika & Tang with new
species, number of new Dryocosmus species were described revealing the high
diversity of cynipid gallwasps and their inquilines in this region (Ide et al. 2010,
2012, Melika et al. 2010, 2011, Tang et al. 2009, 2011a,b, 2012a,b).

Ceroptres. Ceroptres clavicornis has been reared from galls on section

Quercus oaks (white oaks) (Askew et al. 2012, in press) while C. cerri attacks
galls on section Cerris oaks only, including Quercus cerris and the Mediterranean
evergreen species Q. ilex, Q. coccifera and Q. suber (Pujade-Villar et al. 2003,
Melika 2006). There are some confusing records for the both western palaearctic

60
species when they are mentioned in galls from other oak sections, however, those
records must be confirmed and might be misidentifications.
Two eastern palaearctic Ceroptres, C. kovalevi and C. masudai, are
associated with galls on white oaks only, Q. crispula, Q. dentata, Q. mongolica
and Q. serrata (Abe 1997, Abe et al. 2007, GM, personal data). Plant host
associations of two species described from China are unknown (Wang et al.
2012).
The nearctic Ceroptres species showed no preference toward a particular oak
section and were reared from cynipid galls associate with white (10 species) and
red (four species) oaks, one species, C. montensis, known from California only,
was reared from the galls on the Protobalanus section of oaks (Weld 1952).
Thus, Ceroptres is associated with all four sections of Quercus subgenus
Quercus and showed no host plant preference, however, no Ceroptres species are
known to associate with Quercus subgenus Cyclobalanopsis and oak related
genera, Castanopsis, Castanea, and Lithocarpus.

Synophrus. All seven known Synophrus species are associated with section
Cerris oaks: Q. cerris throughout Europe, Q. trojana in northern Greece, Q.
ithaburensis in the Middle East, Q. brantii, Q. castaneifolia and Q. libani in Iran,
Q. suber in North Africa (Pénzes et al. 2009). In this way, one of the early main
lineages is associated with section Cerris (Fig. 17).

Saphonecrus and Ufo. Phylogenetic reconstruction, proposed in this review,

divided Saphonecrus into several clades (Fig. 17). Three western palaearctic
lineages of Saphonecrus are associated with different sections of Quercus
subgenus Quercus: (i) “undulatus” group (S. haimi, S. irani and S. undulatus)
with Cerris oaks; (ii) “barbotini” (S. barbotini and S. gallaepomiformis) group
with Cerris section, Ilex subgroup, and (iii) “connatus” (S. connatus and two
undescribed eastern palaearctic species) with Quercus section Quercus. The latter
is the second early lineage, associated with section Quercus. Two nearctic
Saphonecrus species are associated with section Lobatae oaks, one with Quercus
section Quercus s.s., for one species plant host associations are unknown and they
were not included yet into any phylogenetic reconstructions. From 13 described
eastern palaearctic and oriental Saphonecrus species for 7 species plant host
associations are unknown (Table 5).

61
62
Figure 17. Plant host associations of the Synergus complex of species. For details of phylogenetic reconstruction
see Fig. 11. Host associations are shown by colours.
 Two Andricus species described from Japan on Q. glauca by Shinji (1940,
1941) have been regarded as inquilines (Yukawa and Masuda 1996). Wachi et al.
(2011b) erroneously put them into genus Ufo, where from they were moved to
Saphonecrus (Melika et al. 2012). Till now, these are the only two described
eastern palaearctic Saphonecrus species known to associate with
Cyclobalanospis: S. shirakashii (Japan and Taiwan) with Q. (Cyclobalanospis)
glauca and Q. (C.) globosa, while S. shirokashicola (also known from Japan and
Taiwan) with Q. (C.) glauca and Q. (C.) longinux (Melika et al. 2012).
Saphonecrus excisus is the only species known to associate with Lithocarpus
elegans (= Q. spicata) (Dalla Torre and Kieffer 1910). Saphonecrus
hupingshanensis, is the only species known to associate with Castanopsis carlesii
(Liu et al. 2012). Saphonecrus yukawai is associated with section Cerris oaks
(Wachi et al. 2011a). A large number of Saphonecrus and near Saphonecrus
species from the Eastern Palaearctic and Oriental Region (Taiwan) are under
description and their plant host associations are quite interesting (Fig. 17).
Saphonecrus species associated with Quercus subgenus Cyclobalanopsis are
divided into four clades: “shirakashii”, “saphonecrus #1”, “saphonecrus #3”, and
“shirokashicola”. “Shirakashii” clade with Saphonecrus shirakashii and 5
undescribed species from Taiwan and “saphonecrus #1” with 2 undescribed
species from Taiwan form distinct groups. These groups are separated from
“saphonecrus #3” and “shirakoshicola” clades, which might suggest that at least
two or three host plant shifts onto Cyclobalanopsis occured during the evolution
of the group. Alternatively, this pattern can be explained by host shifts from
Cyclobalanopsis toward other hosts assuming Cyclobalanopsis host for the
common ancestor of the clade between “shirokashicola” and “shirakashii” (Fig.
17). The “saphonecrus #2” clade, which includes also undescribed species from
Taiwan, is associated with Cyclobalanopsis and Lithocarpus. Host associations of
these species must be checked, misidentification of host plants is possible, thus
any conclusions would be premature.
The phylogenetic position of Ufo shows a clear indication for host shift
between Quercus subgenera. Ufo species are associated with section Cerris oaks
only: Q. acutissima in Japan, Q. variabilis in Japan, Korea and Taiwan (Melika et
al. 2012). Considering the Ufo, “saphonecrus #1’’ and “shirakashii’’ clade only,
shift from Cyclobalanopsis to Cerris is the most parsimonious interpretation. The
phylogenetic position of “undulatus group’’ may provide a further example.
Finally, the “saphonecrus #4” clade, which includes 4 undescribed Taiwanese
species, associate with Lithocarpus species only, which suggests relatively early
host shift onto this host genus within the third main clade.
We have to emphasize that in between undescribed Taiwanese Saphonecrus
and near Saphonecrus species mentioned until now (the clades
between ,,saphonecrus #4’’ and ,,shirakashii’’, Fig. 17) there are no lineages

63
which associate with Quercus subgenus Quercus. This suggests a deeper division
among Quercus subgenus Quercus sections comparing to the levels of subgenera
(Quercus and Cyclobalanopsis) or even genera (Lithocarpus and Quercus).
However, our data set can not be considered as representative for going into
further details of this question.
Except S. hupingshanensis, no other Saphonecrus species are known to
associate with galls on Castanopsis (Liu et al. 2012). Species from only two
genera of gallwasps, Cycloneuroterus and Dryocosmus, described from Taiwan
and Japan, are associated with Cyclobalanopsis and Lithocarpus (Tang et al.
2011a,b, Ide et al. 2012). Recently new Cycloneuroterus species from Taiwan and
oriental China were found to associate with Castanopsis species (under
description), however, no inquilines were reared from those galls, while inquilines
in Cycloneuroterus and Dryocosmus species which associate with
Cyclobalanopsis and Lithocarpus are quite common. An interesting observed
paculiarity of Saphonecrus and near Saphonecrus species from Taiwan and
oriental China is that all species associate with hosts (Cycloneuroterus and
Dryocosmus) which inducing galls on Cyclobalanopsis, Lithocarpus and
Castanopsis, while those species never were reared from galls of Andricus,
Cerroneuroterus, Latuspina, Plagiotrochus, and Trichagalma which associate
with Quercus subgenus Quercus species (T.C-T, personal data). In the latter galls,
Synergus and Ufo inquilines species were found only.

Synergus. The host plant associations of the western palaearctic Synergus

species are well-known. The majority of Synergus species are associated only
with deciduous oaks in the section Quercus while part of them entirely or
predominantly associated with oaks in the section Cerris. Two European species,
S. plagiotrochi and S. ilicinus appear to be specific to Mediterranean evergreen
species in the oak section Cerris (Q. ilex, Q. suber and Q. coccifera); S. synophri
is specific to Q. suber, further four species, S. dacianus, S. flavipes, S.
consobrinus and S. variabilis, are associated with Q. cerris and/or further east
with Q. brantii and Q. castaneifolii (Sadeghi et al. 2006). There is a clear split
between Synergus faunas associated with the oak sections Cerris (Q. cerris, Q.
coccifera, Q. ilex and Q. suber) and Quercus (Q. canariensis, Q. faginea, Q.
petraea, Q. pubescens and Q. robur) (Fig. 17). Within the oak section Quercus,
there is a further split between faunas associated with the marcescent (semi-
deciduous) Iberian and North African oaks (Q. pyrenaica, Q. faginea and Q.
canariensis) and faunas associated with the more broadly distributed deciduous
oaks. This split is congruent with the known taxonomic and phylogenetic
relationships between these groups (Manos et al. 1999). However, the split
between “Synergus 2” (S. flavipes, S. variabilis and S. plagiotrochi) and
“Synergus 1” (all other eastern and mainly western palaearctic species) groups on
Fig. 17 probably does not reflect strict track in the plant host associations. Three

64
species in “Synergus 2”, limited to the Western Palaearctic, associate exclusively
with the section Cerris, while species in “Synergus 1” – mainly with section
Quercus oaks. Some species in “Synergus 1” (e.g. S. consobrinus) and two
species in a separate subclade Synergus sp. 28, 12, 24, Synergus sp. 12 and
Synergus sp. 24, were reared from galls of Trichagalma formosana on Q.
variabilis in Taiwan (section Cerris oaks) while Synergus sp. 28 from section
Quercus oaks. Host plant associations in the eastern palaearctic Synergus species
are less known and very limited data is avalaible.
Our knowledge of the nearctic and neotropic Synergus fauna is very
superficial. All species are known to associate with one or few gallwasp species
which induce galls on the same oak sections. However, data on gallwasp and
plant hosts of Synergus species is very fragmentary, based mainly on original
species descriptions only. Six species are known to associate with the section
Protobalanus, near 60% of species, which for the host plant associations are
known, are inquilines in galls on white oaks, and around 40% of species are
associated with red oaks. Thus, whether there is the same split between species
associate with the three sections of oaks, Quercus s.s., Lobatae and Protobalanus,
or they can develop in galls on different oak sections needs further research.
There is an evidence for very strong evolutionary conservatism of gallwasp
host plant associations at the level of sections within the oak genus Quercus L.
Recent analyses primarily of Western Palaearctic oak gallwasps have revealed a
deep phylogenetic divide between gallwasp taxa galling oaks in the section Cerris
on one hand and those galling oaks in the sections Quercus and the nearctic
section Lobatae on the other (Cook et al. 2002; Ács et al. 2007; Liljeblad et al.
2008; Stone et al. 2009). No doubts that distantly related oaks and related genera
commonly support very different gallwasp communities. As a result, grouping of
oak species on the basis of similarity in their gallwasp faunas closely matches the
phylogenetic relationships between oak species and oaks and other related genera
of Fagaceae. The same pattern is seen in the oak host associations of inquiline
cynipids (Fig. 17). The plant host associations of inquilines seems to be more
important in the biogeography of inquilines than the gallwasp host associations,
however, further detail research is necessary to make undoubtfull conclusions.

Conclusions and future directions

Many aspects of the biology, taxonomy and systematics of the oak associated
inquiline genera, especially Ceroptres, Synergus and Saphonecrus, remain
unanswered. Little is known about the host gallwasp and host plant associations,
host preferences and a real taxonomic assignment of the nearctic species. Detailed
research in the taxonomy and systematics of the nearctic species might cardinally
change our current understanding of the group.

65
 Novel approaches are allowing advance in the systematics of the group.
Integrative taxonomy and molecular phylogenetics are crucial tools to understand
evolution of inquilines including history and biogeography, it will help to
understand how the inquilines spread all over the world, how they colonized
different plant hosts. Involving samples from the Eastern Palaeartic and the
Oriental Region, many new hypotheses are established. Most notably, does the
plant host shifts within inquilines rare evolutionary events, like in gallwasps, or
they occur much more frequently? All these questions are awaiting answers.

Acknowledgements
This work was supported by HURO/0901/205/2.2.2, TÁMOP-4.2.1/B-
09/1/KONV-2010-0005, TÁMOP-4.2.2/B-10/1-2010-0012, KTIA-OTKA CNK
80140; George Melika is supported by OTKA K101192 and Chang-Ti Tang was
supported by the National Scientific Council of Taiwan (Grant No. NSC 100-
2313-B-005-010).

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