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New Data on the Parasitoid-Inquiline Community of Andricus quercustozae (Bosc, 1792) (Hymenoptera: Cynipidae) in Bulgaria

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Abstract

New data on parasitoids and inquilines occurring in galls of the cynipid hymenopteran Andricus quercustozae (Bosc, 1792) from the Lozenska Mts., Bulgaria, are presented. Bootanomyia stigmatizans (Fabricius, 1798) (Hymenoptera: Torymidae) is the most abundant parasitoid species in galls of A. quercustozae. The inquiline Pammene amygdalana (Duponchel in Godart, 1842) (Lepidoptera: Torticidae) is recorded from A. quercustozae galls from Bulgaria for the first time. Co-existence of two inquilines, P. amygdalana and Synergus umbraculus (Olivier, 1791) (Hymenoptera: Cynipidae), within the same gall on Quercus dalechampii is documented. In addition, a new gall association for Torymus cyaneus Walker, 1847 (Hymenoptera: Torymidae) is recorded.
301
ACTA ZOOLOGICA BULGARICA
Acta zool. bulg., 71 (2), 2019: 301-303
Short Communication
Introduction
The gall wasp Andricus quercustozae (Bosc, 1792)
is a Western Palaearctic species causing some of the
most striking and easy recognisable oak galls. Only
asexual females are known but some authors sup-
pose the existence of unknown sexual generation.
Galls develop on the buds of the previous year shoots
and grow up to 40 mm in diameter, having spherical
form and brownish colour. Besides the gall-inducer
larva, a number of parasitoids and inqulines could
invade the gall, where they develop as primary or
secondary parasitoids or compete for plant tissue
with the host larva. Amongst the 27 known parasi-
toids in A. quercustozae galls ( 2018), only
11 species are recorded on this host from Bulgaria
( 2005, 2006,  et al. 2013, 
&  2015). In addition, nine cynipid in-
quilines are associated with this host ( et al.
2013) but just one, Synergus umbraculus (Olivier)
(Cynipidae), has been found to attack A. quercusto-
zae galls in Bulgaria (- 1976,
1987, 1989).
The present study aimed to obtain new informa-
tion on parasitoids and inqulines in galls of Andricus
quercustozae from oak forests in Bulgaria.
Materials and Methods
During the winter-spring periods of 2015-2017,
we collected 224 overwintered mature galls of A.
quercustozae from six oak species, i.e. Quercus cerris
L., Q. dalechampii Ten., Q. pedunculiora K. Koch,
Q. petraea (Matt.) Liebl., Q. polycarpa Schur and
Q. pubescens Willd., in the Lozenska Mts., Bulgaria.
Every single gall was placed in a plastic cup and

Emerged parasitoids and inquilines were dehydrated
following  &  (1998). Emerged moths
were killed with ethylacetate and, when necessary,
New Data on the Parasitoid-Inquiline Community
of Andricus quercustozae (Bosc, 1792)
(Hymenoptera: Cynipidae) in Bulgaria
Ivaylo Todorov1, Anelia Stojanova2, Boyan Zlatkov1, Georgi Hristov1 & George Melika3
1 -
garia; E-mails: i.toddorov@abv.bg; bzlatkov@gmail.com
2 Department of Zoology, University of Plovdiv, 24 Tsar Assen Street, 4000 Plovdiv, Bulgaria; E-mail: stanelia@uni-plovdiv.bg
3 Plant Health and Molecular Biology Laboratory, Directorate of Plant Protection, Soil Conservation and Agri-environment, Na-

Abstract: New data on parasitoids and inquilines occurring in galls of the cynipid hymenopteran Andricus quercus-
tozae (Bosc, 1792) from the Lozenska Mts., Bulgaria, are presented. Bootanomyia stigmatizans (Fabricius,
1798) (Hymenoptera: Torymidae) is the most abundant parasitoid species in galls of A. quercustozae. The
inquiline Pammene amygdalana (Duponchel in Godart, 1842) (Lepidoptera: Torticidae) is recorded from
A. quercustozaeP. amygdalana and
Synergus umbraculus (Olivier, 1791) (Hymenoptera: Cynipidae), within the same gall on Quercus dale-
champii is documented. In addition, a new gall association for Torymus cyaneus Walker, 1847 (Hymenop-
tera: Torymidae) is recorded.
Key words: Torymus cyaneus, oak galls, Pammene amygdalana.
302
Todorov I., A. Stojanova, B. Zlatkov, G. Hristov & G. Melika
the genitalia were dissected ( 1976). In
the list below, we use the following abbreviations:
S – south of; em. – emerged on; h.pl. - host plant of
the gall. The new association is marked with one as-
terisk. Observed co-existence of S. umbraculus and
Pammene amygdalana (Duponchel in Godart, 1842)
(Tortricidae), i.e. specimens emerged from a single
gall, are marked with two asterisks.
Results
The following insect species were recorded from
the examined galls:
Hymenoptera
 
Eurytoma brunniventris Ratzeburg, 1852
Material: S Lanina mogila,
42°34’24.25”N/23°29’33.02”E, 948 m a.s.l.,
Q. petraea.
Sycophila biguttata Swederus, 1795
Material: S Lanina mogila,
42°34’24.25”N/23°29’33.02”E,948 m a.s.l., 1
     Q. petraea; Kurlevite
dupki, 42°34’36.26”N/23°30’11.93”E, 1015 m
   Q. polycarpa;
Rakovichka mogila, 42°35’6.14”N/23°28’14.39”E,
         
    Q. dale-
champii.
 
Ormyrus nitidulus (Fabricius, 1804)
Material: Kurlevite dupki,
42°34’38.12”N/23°30’35.81”, 1030 m a.s.l., 1
   
Q. cerris; Rakovichka
mogila, 42°35’6.14”N/23°28’14.39”E, 1130 m a.s.l.,
Q. dalechampii.
 
Bootanomyia stigmatizans (Fabricius, 1798)
Material: S Lanina mogila,
42°34’24.25”N/23°29’33.02”E, 948 m a.s.l., 2
      
Q. petraea;
S Lanina mogila, 42°34’10.00”N/23°29’54.37”E,

Q. pedunculiora.
Torymus auratus (Müller, 1764)
Material: S Lanina mogila,
42°34’24.25”N/23°29’33.02”E, 948 m a.s.l.,
  Q. petraea; Kurlevite
dupki, 42°34’38.12”N/23°30’35.81”E, 1030 m a.s.l.,
    
Q. cerris.
*Torymus cyaneus Walker, 1847
Material: S Lanina mogila,
42°34’24.25”N/23°29’33.02”E, 948 m a.s.l., 1
 Q.
petraea.

Synergus umbraculus (Olivier, 1791)
Material: Rakovichka mogila,
42°35’6.14”N/23°28’14.39”E, 1130 m a.s.l., 8


  
pl. Q. dalechampii.
Fig. 1. A gall of Andricus quercustozae with emerging holes of two specimens of Pammene amygdalana (PA1 and
PA2) and three specimens of Synergus umbraculus (SU). A total of six female cynipids emerged from that gall; A. view
from the upper side; B. view from the lower side.
New Data on the Parasitoid-Inquiline Community of Andricus quercustozae (Bosc, 1792) in Bulgaria
303
Lepidoptera

Pammene amygdalana (Duponchel, 1842)
Material: Kurlevite dupki,
42°34’38.12”N/23°30’35.81”E, 1030 m
       
vi.2016, h. pl. Q. cerris; Rakovichka mogila,
     
   
Q. dalechampii.
Discussion

that Bootanomyia stigmatizans is the most abun-
dant among the inhabitants of A. quercustozae galls.
Bootanomyia stigmatizans accounted 32.35% of
the parasitoids and 15.71% of all parasitoid-inqui-
line material in our samples. In her work on chal-
cids from Bulgaria,  (2006) analysed
the collection of - and listed
24 specimens of B. stigmatizans emerged from A.
quercustozae galls, which are 42.85% of all record-
ed parasitoids reared from this host. However, no
species of the Pteromalidae have been recorded in
that paper. Although  et al. (2013) listed eight
pteromalid species emerged from this host from
       
of them in our rearings. Torymus cyaneus, known
to emerge from many oak galls ( 2018),
A.
quercustozae galls. Regarding the other gall inhab-

     
(2006); however, no conclusions can be drawn.
  
that Synergus umbraculus is the only species of
this group associated with A. quercustozae galls in
Bulgaria. An uncommon co-existence of two inqui-
line species in a single gall was also found. These
were two males of P. amygdalana and six females
of S. umbraculus (Fig. 1) emerged from the same
gall.
Acknowledgements: This study was partly supported by the
project ANIDIV 3, funded by the Institute of Biodiversity and
Ecosystem Research, Bulgarian Academy of Sciences. We are
        
getting images shown on Fig. 1.
References
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
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Received: 24.07.2018
Accepted: 18.09.2018
... The galls of oak trees produced by phytophagous wasps are exploited by various organisms, including inquilines and parasitoids that compete for the host or attack it (Todorov et al., 2019). In galls produced by cynipids, chalcidoid parasitoids are, in general, the most important natural enemies, while species of ...
... Las agallas de encinos producidas por fitófagos son explotadas por diversos organismos, entre ellos, inquilinos y parasitoides que compiten por el hospedante o lo atacan (Todorov et al., 2019). En las agallas producidas por cinípidos, los parasitoides calcidoideos son, en general, the tribe Synergini (Cynipidae), lethal or non-lethal (facultative), are the main group of inquilines (Sanver & Hawkins, 2000). ...
Article
Full-text available
Introducción: Loxaulus hyalinus es un cinípido (Hymenoptera) que ataca encinares (Quercus laeta Liebm.) de la Ciudad de México. La biología y el potencial de daño del insecto se desconoce. Objetivos: Describir la biología de la fase sexual de L. hyalinus y sus efectos en Q. laeta, así como enlistar los inquilinos y parasitoides asociados. Materiales y métodos: Para determinar el periodo de cada estado de L. hyalinus se recolectaron agallas de ramillas infestadas que se disecaron periódicamente, para describir su desarrollo y la presencia de inquilinos y parasitoides en el periodo 2019- 2022. Resultados y discusión: La generación sexual inició a partir de octubre cuando se observaron los primeros síntomas del desarrollo de las agallas en ramillas, y concluyó en mayo del siguiente año, cuando los adultos emergieron. La presencia de una gran cantidad de agallas altera el patrón de crecimiento de la copa de los árboles. Se encontraron dos especies de Synergus como inquilinos y nueve géneros de parasitoides calcidoideos asociados a L. hyalinus. Conclusiones: La generación sexual de L. hyalinus se desarrolla en las agallas de ramilla y su único hospedante confirmado es Q. laeta. Dicha plaga no ocasiona la muerte de su hospedante, pero sí afecta severamente la forma de la copa.
... The chalcidoid fauna of the mountain has not been intensively studied until now. Excluding Pteromaidae, only six species belonging to Eurytomidae, Ormyridae and Torymidae were listed previously (Todorov et al. 2019). Thuróczy (1990) recorded one pteromalid species, Stenomalina gracilis (Walker, 1834) (Stenomalina muscarum auct.), collected in a wheat field. ...
Article
Full-text available
The diversity of the family Pteromalidae is poorly studied in Lozenska Mountain, Bulgaria, and only three species were previously recorded from this area. To increase our knowledge on the diversity of these parasitic wasps in the mountain habitats, we sampled sixteen localities in grasslands using classic sweep-netting for the collection of minute insects. A number of cynipid galls (Cynipidae) were gathered from Quercus cerris L. and Q. pubescens Willd. for the subsequent rearing of their inhabitants. As a result, twenty one pteromalid species were recorded as new for the fauna of the mountain. Six species represent new records for the fauna of Bulgaria: Catolaccus ater (Ratzeburg), Norbanus meridionalis (Masi), Psilocera confusa Graham, Pteromalus albipennis Walker, Stenomalina laticeps (Walker) and Stinoplus etearchus (Walker). Two parasitoid-host associations in the oak galls are new to the Bulgarian fauna. Data on the flying periods, zoogeographical classification and discussion on the species with superpalaearctic ranges are also presented.
Article
Full-text available
A quantitative catalogue of the parasitoids (almost exclusively Chalcidoidea) and inquiline Cynipidae recorded in the western Palaearctic from galls induced on Quercus by Cynipidae (Cynipini) is presented. Quantitative and national data are included with bibliographic references to almost all records published in 2011 and earlier. The catalogue is followed by two checklists, firstly one of the Chalcidoidea with numbers of each species recorded from each type of host gall (galls of the sexual and asexual generations of the host gall wasps are listed separately), and secondly one of inquiline Cynipidae with host galls. Compared to non-oak gall wasps, the Cynipini support a much larger parasitoid and especially inquiline fauna, and this fauna is very largely restricted at the species level to Cynipini galls. About one hundred chalcidoid species are recorded from galls of Cynipini, distributed over six families: Pteromalidae and Eulophidae (29 species each), Torymi-dae (21 species), Eurytomidae (10 species), Eupelmidae (8 species) and Ormyridae (at least 2 species). Polyphagy is usual in the chalcidoid parasitoids, most species having a broad host gall range, but quantitatively the fauna of each type of oak gall is rather characteristic and is strongly influenced by gall morphology, situation on the tree, season of growth and host tree species. These and other extrinsic factors restrict the full exploitation of the chalcidoids’ potential host gall range
Article
Two methods of chemically drying softbodied Chalcidoidea (Hymenoptera) are compared: critical-point drying (CPD) and hexamethyldisilazane (HMDS). For three groups of Eulophidae, Encyrtidae and miscellaneous Chalcidoidea, the CPD specimens were of consistently higher quality for all groups, although the overall differences between CPD and HMDS specimens were marginal.
Published data and new records to the fauna of Eupelmidae (Insecta: Hymenoptera) in Bulgaria
  • M Antov
  • A Stojanova
Antov M. & Stojanova A. 2015. Published data and new records to the fauna of Eupelmidae (Insecta: Hymenoptera) in Bulgaria. ZooNotes 83: 1-11.
Universal Chalcidoidea Database
  • J Noyes
Noyes J. S. 2018. Universal Chalcidoidea Database. World Wide Web electronic publication. http://www.nhm.ac.uk/ chalcidoids
Ormyridae family (Hymenoptera: Chalcidoidea) in Bulgaria
  • A Stojanova
Stojanova A. 2005. Ormyridae family (Hymenoptera: Chalcidoidea) in Bulgaria. In: Proceedings of the Balkan Scientific Conference, Plovdiv, Bulgaria, 19-21 May 2005. pp. 392-396.
Chalcid wasps (Hymenoptera: Chalcidoidea) from the collection of Dr. L. Vassileva-Samnalieva at the Institute of Zoology, Bulgarian Academy of Sciences
  • A Stojanova
Stojanova A. 2006. Chalcid wasps (Hymenoptera: Chalcidoidea) from the collection of Dr. L. Vassileva-Samnalieva at the Institute of Zoology, Bulgarian Academy of Sciences. Acta Zoologica Bulgarica 58: 57-72.
A contribution to the study of cynipid fauna in Bulgaria. Inquilins
  • L Vassileva-Samnalieva
Vassileva-Samnalieva L. 1976. A contribution to the study of cynipid fauna in Bulgaria. Inquilins. In: Terrestrial Fauna of Bulgaria. Materials, Bulgarian Academy of Sciences, Sofia. pp. 202-211.
A study of the cynipidic fauna (Hymenoptera, Cynipidae) of the Strandza Mountain
  • L Vassileva-Samnalieva
Vassileva-Samnalieva L. 1987. A study of the cynipidic fauna (Hymenoptera, Cynipidae) of the Strandza Mountain. Acta Zoologica Bulgarica 35: 23-33.
Notes on the variability of Synergus umbraculus (Hymenoptera, Cynipinae) from Bulgaria
  • L Vassileva-Samnalieva
Vassileva-Samnalieva L. 1989. Notes on the variability of Synergus umbraculus (Hymenoptera, Cynipinae) from Bulgaria. Acta Zoologica Bulgarica 38: 46-53.