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Citation: Sottile, S.; Cerasa, G.;
Massa, B.; Lo Verde, G. Andricus
cydoniae Giraud, 1859 Junior
Synonym of Cynips conifica Hartig,
1843, as Experimentally
Demonstrated (Hymenoptera:
Cynipidae: Cynipini). Insects 2022,13,
200. https://doi.org/10.3390/
insects13020200
Received: 12 January 2022
Accepted: 11 February 2022
Published: 15 February 2022
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insects
Article
Andricus cydoniae Giraud, 1859 Junior Synonym of
Cynips conifica Hartig, 1843, as Experimentally Demonstrated
(Hymenoptera: Cynipidae: Cynipini)
Salvatore Sottile 1, Giuliano Cerasa 2, * , Bruno Massa 2and Gabriella Lo Verde 2
1Museo Civico di Lentate Sul Seveso, Via D. Aureggi 25, 20823 Lentate Sul Seveso, Italy;
salvatore.sottile73@gmail.com
2Department of Agricultural, Food and Forest Sciences (SAAF), University of Palermo,
Viale delle Scienze Bd. 5A, 90128 Palermo, Italy; bruno.massa@unipa.it (B.M.);
gabriella.loverde@unipa.it (G.L.V.)
*Correspondence: giucerasa@gmail.com
Simple Summary:
Phytophagous members of the family Cynipidae induce a spectacular diversity
of plant galls that are often complex in structure. Knowledge of the biology, life cycle, and life history
of known cynipid species is largely fragmentary; gall wasps can exhibit an alternation of generations
known as heterogony in which an all-female alternates with a bisexual generation. The unisexual
generation produces eggs parthenogenetically, and these are usually inserted into a specific plant
part. At the site of oviposition, galls are induced, within which a bisexual generation develops and
later emerges. Emergent males and females mate, and females in turn induce galls from which the
unisexual generation emerges. Females of the two generations may be morphologically dissimilar
and may induce galls that differ greatly morphologically. Differences in the morphology of both
wasps and galls between generations of the same species, coupled with incomplete knowledge of life
cycles, have led to considerable taxonomic confusion. Alternating generations of numerous species
have been described as separate species or even genera. Here, we demonstrate experimentally that
two cynipid species, Cynips conifica (presently Andricus conificus) and Andricus cydoniae, which are
morphologically different and produce very different galls on different host oaks, represent alternate
generations of a single species.
Abstract:
We demonstrated the life cycle closure of Cynips conifica Hartig, 1843 (presently
Andricus conificus
),
previously supposed on the basis of molecular data, and the identity of the sexual generation,
through laboratory experiments. As a consequence, Andricus cydoniae Giraud, 1859 became a junior
synonym of A. conificus (Hartig, 1843). We provide illustrations and a diagnosis for adults and galls,
observations on biology, and information on distribution. Moreover, as sexual galls of A. conificus
cannot be distinguished from those of Andricus multiplicatus, a detailed comparison between sexual
galls and adults of these two species is reported.
Keywords:
oak gallwasp; heterogonic life cycle; biology; sexual generation; taxonomy; morphology;
distribution; Quercus
1. Introduction
Approximately 1300 gall-forming wasp species have been described within the fam-
ily Cynipidae [
1
–
3
], and among these 174 species are reported at present for the Italian
fauna [
4
]. The most numerous genus associated with Quercus spp. is Andricus Hartig, 1840,
which in Italy includes 70 species. Among them, heterogony has been demonstrated in
37 species [5–11].
The large number of observations conducted by Adler on several different species [
12
]
and some recent studies in which the use of DNA sequencing allowed one to discover
Insects 2022,13, 200. https://doi.org/10.3390/insects13020200 https://www.mdpi.com/journal/insects
Insects 2022,13, 200 2 of 18
alternate generations (e.g., [
11
,
13
,
14
]) seem to show that the alternation of generations is
the norm in the Cynipidae. In almost all remaining species for which only the sexual or
asexual form is known, it is likely that alternate generation occurs but is yet to be described.
This happens because in heterogonic gall wasps, the gall structure, phenology, and adult
morphology differ between the asexual and sexual generations, even within the same
species. Thus, it is possible that further studies on the biological cycle of these insects will
lead to a reduction of the number of species to be considered as valid.
Andricus conificus was described by Hartig [
15
] as Cynips conifica with few morpho-
logical characters as was usual at that time. It was then transferred by Rohwer and
Fagan [
16
] to Adleria, which was subsequently synonymised with Andricus (Benson in
Marsden-Jones [17]).
Andricus cydoniae was described by Giraud [
18
], and in this case with few morphologi-
cal characters. Moreover, descriptions of both species do not provide illustrations but give
a good description of the galls induced.
Cook et al. [
19
] showed that Andricus conificus (Hartig, 1843), for which at present
only the asexual generation is known, has the same DNA sequence for the cytb fragment
found in wasps of the sexual generation of Andricus cydoniae Giraud, 1859 and supposed
that these two gall-inducing cynipids could represent the alternate generations of a single
species. Afterwards, Melika [
20
] reported the same hypothesis, without establishing
their synonymy.
In the present study, we report results of laboratory assays and morphological identi-
fication, allowing to demonstrate that the sexual generation of A. cydoniae belongs to the
previously described species A. conificus. Therefore, Andricus cydoniae Giraud, 1859 is here
confirmed as junior synonym of Andricus conificus (Hartig, 1843).
We also provide information on the species distribution, illustrations, and diagnosis for
adults and galls, highlighting the morphological differences between the asexual and sexual
generation individuals and galls of this species and closest Western
Palaearctic congeners.
2. Materials and Methods
2.1. Abbreviations Used in the Text
GCPC: Private collection of Giuliano Cerasa, Giuliana, Palermo, Italy
SSPC: Private collection of Salvatore Sottile, Cinisello Balsamo, Milan, Italy
MCLSS: Museo Civico Lentate Sul Seveso, Milan, Italy
2.2. Study Material Used in the Experiments
(1)
Asexual females placed in contact chamber (Experiment 1):
1
♀
: ITALY: Lombardy, Pavia (Milano), loc. Orridi di Torrazza Coste Nature Park ex
galls of A. conificus (ag) on Quercus petraea, 05.IX.2020, 44
◦
57
0
03.6
00
N 9
◦
05
0
11.2
00
E, 380 m,
emerged 15.II.2021 (sample N. 4049), S. Sottile leg. (GCPC). 2
♀
: with the same label as the
previous one but (SSPC).
(2)
Sexual generation obtained from Experiment 1
3
♀
: ITALY: Lombardy, Cinisello Balsamo (Milano), ex galls of A. cydoniae (sex) in con-
tact chamber on Quercus cerris (labelled as “Cerro A”), emerged 17.V.2021 (
sample N. 4141
),
S. Sottile leg.
(GCPC). 48
♀
: with the same label as the previous one but emerged
17-31
.V.2021,
(SSPC). 3
♂
: ITALY: Lombardy, Cinisello Balsamo (Milano), ex galls of A. cydoniae (sex) in
contact chamber on Quercus cerris (labelled as “Cerro A”), emerged 17.V.2021 (
sample N. 4140
),
S. Sottile leg.
(GCPC). 25
♂
: with the same label as the previous one but emerged 17-
31.V.2021, (SSPC& MCLSS).
(3)
Sexual generation obtained from Experiment 1 and used in the Experiment 2:
4
♀
& 3
♂
: ITALY: Lombardy, Cinisello Balsamo (Milano), ex galls of A. cydoniae (sex)
in contact chamber on Quercus cerris (labelled as “Cerro A”), emerged 23.V.2021, S. Sottile
leg. (SSPC).
Insects 2022,13, 200 3 of 18
2.3. Additional Material Examined for Morphological Diagnosis
5
♀
: ITALY: Lombardy, Pavia (Milano), loc. Orridi di Torrazza Coste Nature Park
ex galls of A. conificus (ag) on Quercus petraea, 05.IX.2020, 44
◦
57
0
03.6
00
N 9
◦
05
0
11.2
00
E,
380 m
, emerged 15-28.II.2021 (sample N.4048, N.4050), S. Sottile leg. (SSPC and MCLSS).
1♀: ITALY: Lazio
, Monti Aurunci, Lenola (Latina) ex galls of A. conificus (ag) on
Quercus petraea
,
13.VIII.2020, 41
◦
25
0
05.6
00
N 13
◦
28
0
47.8
00
E, 400 m, emerged 25.II.2021 (sample N.4047),
S. Sottile leg.
(SSPC). 1
♀
: ITALY: Piemonte, Candelo (Novara), 45
◦
32
0
12.5
00
N 8
◦
08
0
46.8
00
E,
300 m, ex galls of A. conificus (ag) on Quercus petraea, 3.XI.2019, emerged 15.II.2021 (sample
N. 4046), S. Sottile leg. (SSPC).
5
♂
& 2
♀
: ITALY: Emilia-Romagna, Castelnovo néMonti (Reggio Emilia), ex galls of
A. cydoniae (sex) on Quercus cerris, 28.V.2021, 44◦25038.10 0 N 10◦19058.300 E, 800 m, emerged
05.VI.2021 (sample N. 4161, 4162, 4163), S. Sottile leg. (SSPC). 29
♀
: ITALY: Liguria, Vobbia
(Genova), Antola Natural Regional Park, ex galls of A. cydoniae (sex) on Quercus cerris,
27.V.2018, 44
◦
35
0
10.1
00
N 9
◦
04
0
28.5
00
E, 960 m, emerged 01.VI.2018 (sample N. 3624–3631),
S. Sottile leg.
(SSPC and MCLSS). 32
♂
: ITALY: Emilia-Romagna, Bagno di Romagna (Forlì-
Cesena), lago Pontini ex galls on Quercus cerris, 09.VI.2018, 43
◦
50
0
29.3
00
N
12◦00012.500 E
,
770 m, emerged 30.VI.2018 (sample N. 3506–3514), S. Sottile leg. (SSPC & MCLSS).
2♀: ITALY: Sicily,
Castelbuono (Palermo), loc. S. Guglielmo, ex galls of A. multiplicatus
(sex) on Quercus cerris, 24.VI.2014, emerged 10-12.VII.2014 (sample N. 5447), G. Cerasa
leg. (GCPC).
2.4. Laboratory Assays
2.4.1. Experiment 1
On 5 September 2020, fifteen galls of asexual generation of A. conificus were collected,
near maturity, on branches of durmast oak (Quercus petraea (Matt.) Liebl.) at the Orridi di
Torrazza Coste Nature Park, Pavia, Italy.
The twigs containing galls were maintained for about a month at room temperature,
with their bottom end in water to preserve leaf turgidity, thus allowing for the maturation
of the larvae. In October, they were transferred into 100 mL plastic tubes (Figure 1c,d), with
tulle on the bottom and lid, which were placed in a plastic box with the bottom covered
with soil and rotting turkey oak leaves (Figure 1e). The box containing galls was then
placed outdoor in shady condition, checked every two weeks, and water was added when
needed to maintain substrate moisture, until the emergence of gall-inducers, inquilines,
parasitoids, and other inhabitants.
The first asexual females of gall-inducers emerged on 15.II.2021 and later at the end of
February 2021. On 7 March 2021, three females (8 days-old) were placed into a “contact
chamber” (Figure 1a,b,f,g) consisting of a tulle polyester bag (length 70 cm; width 40 cm;
mesh size: mm 0.275
×
0.275; thread thickness: 50
µ
m) including a branch of a pot grown
tree of Quercus cerris L. (11-year-old, labelled as “Cerro A”). To prevent oviposition by wild
gall wasps, the branch chosen for the experiment was covered in the contact chamber about
a month before the experiment started and the tulle bag was positioned to make sure that
distance between tulle and the branch inside was at least 1 cm. The branch to be used in the
experiment was chosen in a part of the tree, remaining always in shady conditions, to avoid
a greenhouse effect inside the contact chamber, and at the same time with an exposure such
as to ensure a good ventilation. A vial containing water-saturated cotton wool was placed
inside the contact chamber to provide water for the insects during egg-laying (Figure 1h).
The three females inside the contact chamber laid eggs on the oak buds present in
the branch and remained active until 14 March 2021. Afterwards, they were removed and
mounted for subsequent morphological observations. The branch was left inside the tulle
bag and checked every 2–3 days until the emergence of adult gall wasps, which started on
17 May.
Insects 2022,13, 200 4 of 18
Insects 2022, 13, x 4 of 19
Figure 1. (a) Contact chambers on branches of young oak tree of Quercus robur L.; (b) S. Sottile during
a periodic monitoring of the contact chamber; (c,d) details of plastic tubes in which the galls were
kept; (e) plastic box with the bottom covered with soil and rotting oak leaves in which the galls are
maintained for rearing in outdoor area; (f) contact chamber; (g) inner view of the contact chamber,
the arrows show the wire framework maintains the tulle walls far from the branch; and (h) vial
containing water-saturated cotton wool placed inside the contact chamber to provide water for the
insects during egg-laying.
The first asexual females of gall-inducers emerged on 15.II.2021 and later at the end
of February 2021. On 7 March 2021, three females (8 days-old) were placed into a “contact
chamber” (Figure 1a,b,f,g) consisting of a tulle polyester bag (length 70 cm; width 40 cm;
Figure 1.
(
a
) Contact chambers on branches of young oak tree of Quercus robur L.; (
b
) S. Sottile during
a periodic monitoring of the contact chamber; (
c
,
d
) details of plastic tubes in which the galls were
kept; (
e
) plastic box with the bottom covered with soil and rotting oak leaves in which the galls are
maintained for rearing in outdoor area; (
f
) contact chamber; (
g
) inner view of the contact chamber,
the arrows show the wire framework maintains the tulle walls far from the branch; and (
h
) vial
containing water-saturated cotton wool placed inside the contact chamber to provide water for the
insects during egg-laying.
Insects 2022,13, 200 5 of 18
2.4.2. Experiment 2
On 24 May, 3
♂
and 4
♀
(7 days-old) obtained from Experiment 1 were transferred into
50 mL plastic jar with tulle on the lid in order to allow mating. In the following two days,
several copulatory acts were observed.
On 26 May, the insects were placed in a contact chamber (see above) (Figure 1a,b,f,g)
that had been set up on a branch of young oak tree of Quercus robur L. (8-year-old, labelled
as “Farnia 1F”) grown in a green peri-urban area (Gessate, Milano Province, Italy). Ad-
ditionally, in this case the contact chamber was placed about a month before experiment,
making sure that distance between tulle and the branch inside was at least 1 cm, to avoid
the oviposition by wild wasps. Moreover, as galls of asexual form of A. conificus develop on
adventitious buds in trunks and branches, the shoots were topped before being included
in the contact chamber, to induce the adventitious buds development. A vial containing
water-saturated cotton wool was placed inside the contact chamber to provide water for
the insects during egg-laying (Figure 1h).
The adults in the contact chamber were checked daily, until male and female deaths
occurred, after two days and after a week, respectively. Insects were then removed and
mounted for subsequent morphological observations. The branch was left inside the
tulle bag and checked every week for gall development (Figure 1b). No clear signs of
gall development were recorded until mid-September, when, surprisingly, three devel-
oping
A. conificus
galls were found. After four weeks, the galls had already reached full
development and turned a greyish colour (Figure 2c–e).
2.5. Morphological Study
Identification of adult wasps was performed using the keys and the morphological
description provided by Melika [
20
] and Dalla Torre and Kieffer [
21
]. The original descrip-
tions by Hartig [
15
] and Giraud [
18
] have been also considered. Insects were examined
through a Wild-Heerbrugg M8 (Wild Heerbrugg, Heerbrugg, Switzerland) and a Kyowa
Optical SD-2PL stereomicroscopes (Kyowa Optical, Tokyo, Japan) and with a Zeiss Univer-
sal Photomicroscope III compound microscope (Carl Zeiss, Oberkochen, Germany). Images
were taken using a Leica DM series compound microscope (Leica, Benzheim, Germany) and
a Leica DFC series mounted camera with Leica Application Suite software (LAS EZ 3.4.0,
Leica, Switzerland). All insect photos were integrated using the freeware CombineZP [
22
]
and processed in Adobe Photoshop CS4.
Galls were photographed with a Canon Eos 600D and Canon Eos 6D Mark II digital
camera equipped with a Canon compact-macro lens EF 50 mm 1:2.5 and Canon macro lens
EF 100 mm 1:2.8 L. (Canon Inc., Tokyo, Japan).
We follow the current terminology and abbreviations for morphological structures
[20,23–25]
,
antennal morphology and sensillar description [
26
], forewing venation [
27
], cuticular sur-
face [
28
] and microsculpture [
29
]. Measurements and abbreviations used here include
F1–F12, 1st and subsequent flagellomeres; POL (post-ocellar distance) is the distance be-
tween the inner margins of the posterior ocelli; OOL (ocellar-ocular distance) is the distance
from the outer edge of a posterior ocellus to the inner margin of the compound eye; LOL is
the distance between lateral and frontal ocelli; the diameter of a median or lateral ocellus
is along its major axis; and tsa stands for transscutal articulation. Gula is the cranial area
ventral to the posterior tentorial pits, defined laterally by the gular sulci, which converge in
the postgenal suture. Acetabular carina is the area that is located medially on the epicnemial
carina and posteriorly delimits the epicnemium; the width of the forewing radial cell is
measured from the margin of the wing to the Rs vein; the petiole is the first metasomal
tergite (T1); metasomal tergite 2 (T2) is the first obvious tergite; T3–T9 indicate subsequent
tergites; and Ts1–Ts5 indicate first and subsequent tarsomeres.
Insects 2022,13, 200 6 of 18
Insects 2022, 13, x 6 of 19
Figure 2. Andricus conificus asexual generation: (a) general appearance of the young gall on Quercus
petraea; (b) habitus of adult (lateral view); (c–e) mature galls obtained from the second experiment;
and (f) dissected gall, showing the larval chamber surrounded by spongy-suberous tissue. (g) This
dissection shows the larval chamber surface covered in small protruding humps.
2.5. Morphological Study
Figure 2. Andricus conificus asexual generation: (a) general appearance of the young gall on Quercus
petraea; (
b
) habitus of adult (lateral view); (
c
–
e
) mature galls obtained from the second experiment;
and (
f
) dissected gall, showing the larval chamber surrounded by spongy-suberous tissue. (
g
) This
dissection shows the larval chamber surface covered in small protruding humps.
Insects 2022,13, 200 7 of 18
Most of the anatomical terms used can be found in the Hymenoptera Anatomy Ontol-
ogy (HAO) [
30
,
31
]. Most of the definitions can be also found at http://glossary.hymao.org
(accessed on 20 September 2021).
3. Results
3.1. Laboratory Assays
After removing the gall wasp females, the development of the branch of “Cerro A”
inside the contact chamber followed its natural spring progression until the second half of
April, when several newly formed leaves appeared withered and did not develop regularly.
On 2 May 2021, about 20 globular clusters of galls were observed, which continued to grow
until maturity. Few galls reached 1.8 cm in diameter size, while most of them remained
smaller than 1.5 cm at maturity, probably due to the fact that the host plant was a pot
grown oak.
In the second half of May, the gall-inducers started to emerge, initially only males and
then, from 21 May, both females and males with a peak on 26 May; the adults’ emergence
was recorded until 5 June 2021. A total of 51 females and 28 males that emerged from the
galls were identified as A. cydoniae, on the basis of morphological characters.
Therefore, according to the International Code of Zoological Nomenclature (ICZN) [
32
],
a new synonymy is here established: Andricus cydoniae Giraud, 1859 as junior synonym of
A. conificus (Hartig, 1843).
3.2. Gall
The asexual galls (Figure 2a,c–g) develop on the buds of thicker branches and on
the main trunk to which they are attached by a thin stalk. Young galls are whitish with
thin longitudinal red-purplish or brown veins from base to tip, covered with stellate hairs
that fall at maturity when the galls turn darker and assume a suberous consistency. The
galls are monolocular, about 10–15 mm high, subconical in shape with obtuse apex, and
have a well-differentiated central larval chamber surrounded by spongy-suberous tissue
(Figure 2f). The larval chamber consists of very compact woody tissue with a surface
covered in small protruding humps (Figure 2g).
The galls of the sexual generation (Figure 3c–f) consist of a hypertrophic degeneration
of the terminal or lateral shoot buds; these buds are transformed into an ovoid or subspher-
ical swelling with a diameter that can vary from 10 to 40 mm (often the galls are coalescent,
forming large conglomerates and reaching sizes greater than 50 mm); they are light-green
when young (Figure 3c) and dark-green and then brown when mature, bearing more or
less deformed or normal leaves on the upper part.
The typical structure of the gall consists of a layer of compact vegetative tissue, 3
to 10 mm thick, which takes the shape of a more or less concave thalamus. This woody
‘thalamus’, sometimes ‘closed’ like a ceramic pot (Figure 3e), in other cases ‘open’ like a
plate (Figure 3d), provides support and protection for the larval chambers (5 to 20) that
develop above (Figure 3e). The surface of the gall ‘thalamus’ is externally covered with
soft hairs that confer a velvety, silvery appearance to the gall. On the thalamus, curled,
rakish leaves and twigs develop, and in some of these, larval cells can be ‘dragged along’
during development; these metamorphosed leaves wither as the galls mature and after
adult emergence the galls may remain on the plant for some years. The inner part of
the gall is covered with a dense layer of white single-celled hairs (Figure 3f) that also
extends to the larval chambers, which are egg-shaped (Figure 3d,e) with enlarged base
and apical extension more or less pointed and slightly curved, measuring 3.3–4.5 mm in
height ×1.8–2.8 mm
in width measured at 1/3 from the base. They develop cohesively,
with each embedded in a socket of the supporting thalamus tissue like teeth in the gums
(Figure 3d). Sometimes the constipated proximity of the chambers alters their egg shape
to rectangular parallelepiped with rounded corners. When the gall thalamus is “opened”,
the larval chambers are visible from above. In the inner part of the socket, the surface is
coated with dense coverage of white hollow single-cell hairs (Figure 3f); these structures
Insects 2022,13, 200 8 of 18
in a less dense form coat the larval cells with a distinct supporting cell layer. Whitish
hairs are longest at the base of the larval chamber and become shorter at the apex. The
inner layer of the larval chamber is thin and hard, composed of sub-rectangular cells
arranged longitudinally to the length of the chamber; the emergence hole is in the apical or
sub-apical part.
Insects 2022, 13, x 8 of 19
are monolocular, about 10–15 mm high, subconical in shape with obtuse apex, and have
a well-differentiated central larval chamber surrounded by spongy-suberous tissue (Fig-
ure 2f). The larval chamber consists of very compact woody tissue with a surface covered
in small protruding humps (Figure 2g).
The galls of the sexual generation (Figure 3c–f) consist of a hypertrophic degenera-
tion of the terminal or lateral shoot buds; these buds are transformed into an ovoid or
subspherical swelling with a diameter that can vary from 10 to 40 mm (often the galls are
coalescent, forming large conglomerates and reaching sizes greater than 50 mm); they are
light-green when young (Figure 3c) and dark-green and then brown when mature, bear-
ing more or less deformed or normal leaves on the upper part.
Figure 3. Andricus conificus sexual generation: (a,b) habitus, female and male (lateral view); (c) gen-
eral appearance of gall; (d) dissected gall, showing the layer of compact vegetative tissue, which
takes the shape of ‘open’ thalamus; (e) dissected gall, showing the layer of compact vegetative tissue,
Figure 3.
Andricus conificus sexual generation: (
a
,
b
) habitus, female and male (lateral view);
(c) general
appearance of gall; (
d
) dissected gall, showing the layer of compact vegetative tissue, which takes
the shape of ‘open’ thalamus; (
e
) dissected gall, showing the layer of compact vegetative tissue,
which takes the shape of ‘closed’ thalamus and the egg-shaped larval chambers; and (
f
) histological
preparation showing the single-cell hairs.
Insects 2022,13, 200 9 of 18
3.3. Similar Galls
Based on gall characteristics and host plant information, numerous gall-inducing
insects can be identified to the species level. However, some exceptions have recently
been reported in gall wasps and gall midges. For example, two congeneric gall midges,
Asphondylia gennadii (Marchal, 1904) and Asphondylia capsicicola Uechi, Yukawa et Tokuda,
2016, induce the same kind of galls on the same plant organ and host plant species, but the
gall midges themselves can be distinguished from each other based on pupal morphology
and molecular differences [
33
]. With regard to the gall wasps, the sexual generation
gall of a species recently described, Latuspina jinzhaiensis Abe, Ide, Su, et Zhu, 2021, is
indistinguishable from that produced by L. abemakiphila Ide et Abe, 2021, which is induced
on leaves of the same oak species in Japan [34].
In our case, sexual generation galls of A. conificus are very similar only to those of
A. multiplicatus
(Figure 4c–g), and both develop on the same host plants. Melika [
20
]
observed that the two galls can be confused and added that the galls of sexual generation
of A. conificus are genuinely multilocular, with many larval chambers inside a solid mass of
tissue, while those of A. multiplicatus are an aggregation of distinct galls.
Insects 2022, 13, x 10 of 19
Figure 4. Andricus multiplicatus sexual generation: (a,b) habitus, female and male (lateral view); (c)
general appearance of gall; (d–f) dissected gall, showing the egg-shaped larval chambers embedded
in a socket of the supporting thalamus tissue; and (g) magnification of the larval chambers.
The gall of A. conificus sexual generation is generally described as a concave ‘closed’
structure with an apical opening, in which are enclosed the larval chambers; however, we
also found galls with ‘open’ thalamus in which the larval chambers are visible from above.
This ‘open’ thalamus conformation has been described for A. multiplicatus, but we have
also found closed galls for this species. In conclusion, we did not find any macro- or micro-
morphological characters to distinguish the two galls with absolute certainty. Moreover,
all the characters show variability in both species; therefore, we consider that it is impos-
sible to identify the species only from the gall morphology. On the other hand, species
identification through adults is relatively easy on the basis of morphological differences
listed in Table 1.
Figure 4.
Andricus multiplicatus sexual generation: (
a
,
b
) habitus, female and male (lateral view);
(c) general
appearance of gall; (
d
–
f
) dissected gall, showing the egg-shaped larval chambers embed-
ded in a socket of the supporting thalamus tissue; and (g) magnification of the larval chambers.
Insects 2022,13, 200 10 of 18
The gall of A. conificus sexual generation is generally described as a concave ‘closed’
structure with an apical opening, in which are enclosed the larval chambers; however,
we also found galls with ‘open’ thalamus in which the larval chambers are visible from
above. This ‘open’ thalamus conformation has been described for A. multiplicatus, but we
have also found closed galls for this species. In conclusion, we did not find any macro-
or micro-morphological characters to distinguish the two galls with absolute certainty.
Moreover, all the characters show variability in both species; therefore, we consider that it is
impossible to identify the species only from the gall morphology. On the other hand, species
identification through adults is relatively easy on the basis of morphological differences
listed in Table 1.
Table 1.
Morphological differences between sexual form of A. conificus (=A. cydoniae) and
A. multiplicatus.
Features A. conificus ♀(=A. cydoniae)A. multiplicatus ♀
Body color
Mostly dark brown to black, with yellow
legs, except for proximal part of hind
coxae being dark brown (Figure 3a)
Mostly reddish yellow, legs slightly
lighter than body (Figure 4a)
Head sculpture Frons, vertex, and occiput reticulate
(Figure 6a,b)
Frons, vertex, and occiput uniformly
coriaceous (Figure 6c,d)
Striae on mesopleuron With very marked striae (Figure 6e) With or without very indistinct striae
(Figure 6f)
Sculpture, shape, and size
of mesoscutellum
As long as is broad; uniformly strongly
areolate-rugose with distinct mainly
longitudinal sharp rugae with emarginate
posterior margin (Figure 6e,j)
Broader than long; reticulate rugose
around its limits, more delicate in the
central part of disk with unemarginate
posterior margin (Figure 6f,i)
Shape of scutellar foveae Scutellar foveae subtriangular
well-delimited posteriorly (Figure 6g,j)
Subrectangular not or very slightly
delimited posteriorly (Figure 6h,i)
Mesoscutum sculpture Deeply colliculate (Figure 6g) Shallowly colliculate (Figure 6h)
White setae on prominent part of ventral
spine of hypopygium
Very few, short (approximately as long as
the median diameter of the hypopygium
in lateral view), erect, and not extending
behind apex of ventral spine (Figure 7a, c)
Few, long (about one and a half times the
median diameter of the hypopygium in
lateral view), curved, and slightly
extending behind apex of spine
(Figure 7b,d)
Features A. conificus ♂(=A. cydoniae)A. multiplicatus ♂
Body color
Mostly dark brown to black, with yellow
legs, except for proximal part of hind
coxae being dark brown (Figure 3b)
Mostly reddish yellow, legs slightly
lighter than body (Figure 4b)
Ratio of diameter of torulus (including
rims) to eye-torulus distance
Nearly 1.6 times eye-torulus distance
(Figure 7f) Equal to eye-torulus distance (Figure 7g)
Ratio of eye-torulus distance to distance
between toruli
Nearly 1.4 times as large as distance
between toruli (Figure 7f)
Nearly 3.0 times as large as distance
between toruli (Figure 7g)
Frons and vertex sculpture Rugose (Figure 7e,f) Coriaceous (Figure 7g,h)
Shape of scutellar foveae Subtriangular well-delimited posteriorly
(Figure 7i)
Subrectangular
Not or very slightly delimited
posteriorly (Figure 7j)
Sculpture, shape, and size
of mesoscutellum
Around its limits, strongly reticulate
rugose; more delicate or colliculate in the
central part of disk, with emarginate
posterior margin (Figure 7i)
Around its limits, reticulate rugose; more
delicate or coriaceous in the central part
of disk, with unemarginate posterior
margin (Figure 7j)
Insects 2022,13, 200 11 of 18
Table 1. Cont.
Features A. conificus ♀(=A. cydoniae)A. multiplicatus ♀
Mesoscutum sculpture Deeply colliculate (Figure 7i) Shallowly colliculate (Figure 7j)
Striae on mesopleuron With very marked striae (Figure 8a) With or without very indistinct striae
(Figure 8b)
Ratio of breadth to height
of metascutellum More than 2.0 (Figure 8c) Less than 1.5 (Figure 8d)
3.4. Diagnosis of the Asexual Form
Asexual females of A. conificus belong to “Adleria-non kollari” group, a large group
of 13 Andricus species [
35
], with the anterior surface of foretibia bearing long oblique
setae (Figure 5k,l); antenna 14-segmented (rarely 13 or 15) (Figure 5d); the mesoscutum
coriaceous, without punctures (Figure 5f); and all metasomal tergites with dense white
setae laterally (Figure 5h) and the prominent part of the ventral spine of the hypopygium
needle-like and very long [35].
More specifically, in A. conificus (Figures 2b and 5a–l) the prominent part of ven-
tral spine of hypopygium is very long and slender, 6.25–7.0 times as long as broad in
ventral view, with relatively short setae (Figure 5h–j). It closely resembles A. truncicolus;
however, in A. conificus the body is reddish brown with black marks between notauli
(
Figures 2b and 5e,f
); the head is less rounded in front view, and the gena is broader than
the compound eye for the entire height of the head (Figure 5a), while in A. truncicolus the
body is blackish brown and the head is more rounded in front view and the gena is broader
than the compound eye only behind and ventrally.
Andricus conificus resembles A. synophri Pujade-Villar, Tavakoli and Melika, 2015,
from which it differs in having the body colour reddish brown, the body length around
4.0 mm
, F1 longer than F2 (Figure 5d), and the metasomal tergites without micropunctures
(Figure 5g,h), while A. synophri is smaller in size, around 3.0 mm, and has F1 slightly shorter
than F2, micropunctures on the metasomal tergites, and a black body.
3.5. Diagnosis of the Sexual Form
Andricus conificus sexual form belongs to the group of species with a transversely
striate mesopleuron (Figure 6e). Most closely resemble A. cryptobius. In sexual females
(Figure 3a, Figure 6a,b,e,g,j and Figure 7a,c) with rounded mesoscutellum, the disk of the
scutellum is dull rugose along sides, with much smaller units in the centre of the disk
(Figure 6j); in males (Figure 3b, Figure 7e,f,i and Figure 8a,c), POL is at least 2.0 times as long
as length of lateral ocellus (Figure 7e), and ocelli are much smaller, while in A. cryptobius,
sexual female has slightly elongated mesoscutellum, the disk of scutellum is uniformly
dull rugose, and main strong rugae are directed longitudinally (appearing parallel at low
magnification). In males, POL is less than 2.0 times as long as the length of the lateral
ocellus, and ocelli are large.
3.6. Biology and Host Plant
This species has a heteroecic cycle; the galls of sexual generation begin to develop on
Cerris section oak in early April and mature in May, and the adults emerge from the second
half of May to the first half of June. The asexual galls begin development on Quercus section
oaks in early summer, reach maturity in late August and September, and the adults emerge
in February-March of the following year or in the second-year, as demonstrated for the first
time by our sampling/emerging data (sample N. 4046), spending one year in diapause.
The diapause is common in Cynipidae, and a high proportion of the asexual generation
larvae of several species of cynipids shows diapause for periods ranging from 1 to, less
frequently, 8 years [1].
Insects 2022,13, 200 12 of 18
Insects 2022, 13, x 12 of 19
3.4. Diagnosis of the Asexual Form
Asexual females of A. conificus belong to “Adleria-non kollari” group, a large group of
13 Andricus species [35], with the anterior surface of foretibia bearing long oblique setae
(Figure 5k,l); antenna 14-segmented (rarely 13 or 15) (Figure 5d); the mesoscutum coria-
ceous, without punctures (Figure 5f); and all metasomal tergites with dense white setae
laterally (Figure 5h) and the prominent part of the ventral spine of the hypopygium nee-
dle-like and very long [35].
Figure 5.
Andricus conificus asexual female: (
a
) head, (front view); (
b
) head (dorsal view); (
c
) head
(lateral view); (
d
) antenna; (
e
) mesosoma (lateral view); (
f
) mesosoma (dorsal view); (
g
) metasoma
(dorsal view); (
h
) metasoma (lateral view); (
i
) ventral spine of hypopygium (lateral view); (
j
) ventral
spine of hypopygium, ventral view; (
k
) foretibia (the arrows show the long oblique setae on the
anterior surface); and (l) foreleg on microscope slide.
Insects 2022,13, 200 13 of 18
Insects 2022, 13, x 14 of 19
Figure 6. Comparison between females of sexual generation of Andricus conificus (a,b,e,g,j) and A.
multiplicatus (c,d,f,h,i): (a,d) head (dorsal view); (b,c) head, (front view); (e,f) mesosoma (lateral
view); (g,h) mesosoma (dorsal view); and (i,j) mesoscutellum (dorsal view).
Figure 6.
Comparison between females of sexual generation of Andricus conificus (
a
,
b
,
e
,
g
,
j
) and A.
multiplicatus (
c
,
d
,
f
,
h
,
i
): (
a
,
d
) head (dorsal view); (
b
,
c
) head, (front view); (
e
,
f
) mesosoma (lateral
view); (g,h) mesosoma (dorsal view); and (i,j) mesoscutellum (dorsal view).
3.7. Distribution
The species is widely distributed in the Western Palaearctic region: Austria, France,
Bulgaria, Hungary, Romania, Kosovo, Poland, Greece, Ukraine (Transcarpathian Region
only) [
20
], Switzerland [
36
], Serbia [
37
], Croatia [
38
] (including Cres-Lošinj Archipelago [
39
]),
Slovakia [
40
], and Turkey [
41
,
42
]. Concerning Italy, it is reported for the northern and
southern regions, including Sicily [
43
]. Regarding Sicily, records of A. conificus should be
Insects 2022,13, 200 14 of 18
considered doubtful, as no record of A. conificus (ag) is known from literature, and it is con-
sidered impossible to distinguish the galls of A. conificus (sex) from those of
A. multiplicatus
Insects 2022, 13, x 15 of 19
Figure 7. Comparison between females of sexual generation of Andricus conificus (a,c) and A. multi-
plicatus (b,d): (a,b) metasoma (lateral view); (c,d) ventral spine of hypopygium (ventral view); (e–j)
comparison between males of sexual generation of Andricus conificus (e,f,i) and A. multiplicatus
(g,h,j): (e,h) head (dorsal view); (f,g) head (front view); and (i,j) mesosoma (lateral view).
Figure 7.
Comparison between females of sexual generation of Andricus conificus (
a
,
c
) and
A. multiplicatus
(
b
,
d
): (
a
,
b
) metasoma (lateral view); (
c
,
d
) ventral spine of hypopygium (ventral view);
(
e
–
j
) comparison between males of sexual generation of Andricus conificus (
e
,
f
,
i
) and
A. multiplicatus
(g,h,j): (e,h) head (dorsal view); (f,g) head (front view); and (i,j) mesosoma (lateral view).
Insects 2022,13, 200 15 of 18
Insects 2022, 13, x 16 of 19
Figure 8. Comparison between males of sexual generation of Andricus conificus (a,c) and A. multipli-
catus (b,d): (a,b) mesosoma (lateral view); (c,d) metascutellum and propodeum (posteroventral
view).
3.6. Biology and Host Plant
This species has a heteroecic cycle; the galls of sexual generation begin to develop on
Cerris section oak in early April and mature in May, and the adults emerge from the sec-
ond half of May to the first half of June. The asexual galls begin development on Quercus
section oaks in early summer, reach maturity in late August and September, and the
adults emerge in February-March of the following year or in the second-year, as demon-
strated for the first time by our sampling/emerging data (sample N. 4046), spending one
year in diapause. The diapause is common in Cynipidae, and a high proportion of the
asexual generation larvae of several species of cynipids shows diapause for periods rang-
ing from 1 to, less frequently, 8 years [1].
3.7. Distribution
The species is widely distributed in the Western Palaearctic region: Austria, France,
Bulgaria, Hungary, Romania, Kosovo, Poland, Greece, Ukraine (Transcarpathian Region
only) [20], Switzerland [36], Serbia [37], Croatia [38] (including Cres-Lošinj Archipelago
Figure 8.
Comparison between males of sexual generation of Andricus conificus (
a
,
c
) and
A. multiplicatus
(
b
,
d
): (
a
,
b
) mesosoma (lateral view); (
c
,
d
) metascutellum and propodeum (pos-
teroventral view).
4. Discussion
The “life cycle closure”, i.e., the process of determining the alternate generation of a
heterogonic species or synonymizing two previously described univoltine species [
5
,
44
,
45
],
can be problematic as the adults and gall morphology of both generations can differ
markedly. Moreover, rearing experiments are often difficult, time-consuming, and do not
always lead to positive results. Nevertheless, they can be considered essential to assess life
cycle closure [8,9,46–49].
On the other hand, molecular methods may allow for pairing of currently unmatched
sexual and asexual generations into a single species lifecycle, given that both generations
within a species have identical (or nearly so) DNA sequences [
11
,
13
,
14
]; the two approaches
are complementary and mutually reinforcing.
The results of the present study and our recent studies (e.g., [
50
,
51
]) show that much
remains to be revealed about Cynipidae, even in the Western Palaearctic, where they are
considered a relatively well studied family. Further studies will probably lead to a reduction
of the number of valid species as a result of life cycle closure, as sexual and parthenogenetic
Insects 2022,13, 200 16 of 18
generations of many species still remain unpaired. However, other new species remain to
be described, and many biological aspects remain to be investigated.
Author Contributions:
Conceptualization, S.S., G.L.V., B.M. and G.C.; investigation, S.S. and G.C.;
writing—review and editing G.C., B.M. and G.L.V.; supervision, B.M. and G.L.V. All authors have
read and agreed to the published version of the manuscript.
Funding:
The research was carried out with the financial support of the University of Palermo (Fondo
di Finanziamento per la Ricerca—FFR 2018/2021, G. Lo Verde).
Institutional Review Board Statement: Not applicable.
Data Availability Statement: The data presented in this study are available in article.
Acknowledgments:
The authors are grateful to three anonymous referees for their remarks
and comments.
Conflicts of Interest:
The authors declare no conflict of interest. The funders had no role in the design
of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or
in the decision to publish the results.
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