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Zoology in the Middle East
ISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/tzme20
Additions to the knowledge of Trichogramma from
Turkey (Hymenoptera: Trichogrammatidae), with
description of a new species
Andrew Polaszek, Paul Rugman-Jones, Hakan Çelik & Halil Bolu
To cite this article: Andrew Polaszek, Paul Rugman-Jones, Hakan Çelik & Halil Bolu (2022):
Additions to the knowledge of Trichogramma from Turkey (Hymenoptera: Trichogrammatidae), with
description of a new species, Zoology in the Middle East, DOI: 10.1080/09397140.2022.2145801
To link to this article: https://doi.org/10.1080/09397140.2022.2145801
Published online: 22 Nov 2022.
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Zoology in the Middle East, 2022
http://dx.doi.org/10.1080/09397140.2022.2145801
*Corresponding author. Email: a.polaszek@nhm.ac.uk
© 2022 Taylor & Francis
Additions to the knowledge of Trichogramma from Turkey
(Hymenoptera: Trichogrammatidae), with description of a
new species
Andrew Polaszeka,*, Paul Rugman-Jonesb, Hakan Çelikc and Halil Boluc
aInsects Division, Natural History Museum, London, United Kingdom; bDepartment of
Entomology, University of California, California, U.S.A.; cDepartment of Plant Protection,
Faculty of Agriculture, Dicle University, Diyarbakır, Turkey
(Received 14 October 2022; accepted 2 November 2022)
New country and host records of Trichogramma species for Turkey are presented.
Trichogramma aurosum Sugonjaev & Sorokina is recorded for the first time from Tur-
key, and a new species, T. zerynthiae Polaszek & Bolu, is described. Morphological
identification based on dissected male genitalia is supplemented by molecular se-
quence data.
http://www.zoobank.org/urn:lsid:zoobank.org:pub:9CFF5E39-F1D2-42FB-86B8-
FC8475EC3560
Keywords: Ooparasitoid; egg parasitoid; host-associations; Symphyta; rose sawfly;
Lepidoptera; Papilionidae
Introduction
As part of a series of crop pest surveys in southern Anatolia, Turkey, eggs of the rose
sawfly Allantus viennensis (Schrank, 1781) (Hymenoptera: Tenthredenidae: Allantinae)
and southern festoon butterfly Zerynthia polyxena (Denis & Schiffermüller, 1775) (Lep-
idoptera: Papilionidae) were collected on rose (Rosa sp., Rosaceae) and Aristolochia
rotunda (Aristolochiaceae) respectively. Several parasitoid species in the genus
Trichogramma Westwood (Hymenoptera: Trichogrammatidae) were reared from these
eggs, representing a new species and country records.
Material and Methods
Material. On 12.xi,2019 eggs of Allantus viennensis (Schrank, 1781) on the shoots of rose plants
in Diyarbakır Province (Kayapınar District) were brought to the laboratory. In May 2020 eggs of
Zerynthia polyxena on leaves of Aristolochia rotunda collected in Diyarbakır Province (Bağlar
District (22-27.v.2020) and Eğil District (17-31.v.2020) were brought to the laboratory. For both
hosts, eggs and infested plant parts were kept in plastic boxes covered with cloth, and maintained
at 26±1°C, rh 65±5, L:D 16:8. Parasitoids emerging were preserved in 70% ethanol and sent to
the fist author (AP) for identification.
DNA extraction, amplification, and sequencing. DNA was extracted from individual wasps using
the Chelex method described in Polaszek et al. (2012). The polymerase chain reaction (PCR) was
used to amplify the internal transcribed spacer 2 (ITS2) using the primers 58SF (Porter & Collins
1991) and ITS4 (White et al. 1990) as described in Morse et al. (2016). In a separate PCR, the
“barcoding” region of the mitochondrial cytochrome c oxidase subunit I gene (COI) was ampli-
fied using LCO1490 and HCO2198 (Folmer et al. 1994) as described in Rugman-Jones et al.
Published online 22 Nov 2022
2 A. Polaszek et al.
Figure 1. Genital capsule and aedeagus of Trichogramma indicating terms and abbreviations used
in this paper: A. Dorsal structures of genital capsule; B. Ventral structures of genital capsule; C.
Dorsal measurements of genital capsule; D. Aedeagus; E. Ventral measurements of genital cap-
sule.
(2012). All reactions were performed in 25 µL volumes on a Mastercycler® ep gradient S ther-
mocycler (Eppendorf North America Inc., New York, USA). Amplification was confirmed by gel
electrophoresis and PCR products were cleaned using a DNA Clean & Concentrator™-5 kit
(Zymo Research Corporation, Irvine, California, USA). Amplicons were direct sequenced in both
directions at the Institute for Integrative Genome Biology, University of California at Riverside.
The parity of forward and reverse reads was checked using SEQUENCHER 4.9 (Gene Codes
Corporation, Ann Arbor, Michigan, USA) and priming regions were removed manually in Bi-
oEdit version 7.0.5.3 (Hall, 1999). COI sequences were translated into their amino acid chains to
confirm the absence of indels and pseudogenes. ITS2 sequences were subject to BLAST searches
of GenBank® (NCBI: Benson et al., 2010). Similar sequences were retrieved and manually
aligned with those from our specimens, in BioEdit. The COI sequences were subject to linear
searches of the Barcode of Life Data System (BOLD: Ratnasingham & Hebert 2007) again to
identify similarities with existing accessions. Finally, our sequences were deposited in GenBank
(accession nos. OP580118-OP580124 [COI] and OP581338-OP581344 [ITS2]).
Zoology in the Middle East 3
Morphological identification. Specimens received in 70% ethanol were slide-mounted using the
technique described by Noyes (1982) with modifications following Schmidt and Polaszek (2007).
Several specimens of Trichogramma aurosum Sugonjaev & Sorokina, T. zerynthiae Polaszek &
Bolu, sp. n. and Trichogramma sp. near urquijoi Cabello Garcia were partially dissected, and
male genitalia slide-mounted before sending the remainder of the specimens to UCRC for DNA
sequencing. Species-level identification was undertaken using published keys by Pintureau
(2008), Sorokina (1984), and Sugonyaev & Sorokina (1976), as well as by reference to specimens
in the NHMUK collection.
Terminology and abbreviations. Terminology (see Figure 1) broadly follows Pinto (2006) and
Polaszek et al. (2002). The following abbreviations are used: AD = apical distance; AL = ae-
deagus length; AW = apical width; BD = basal distance; DA = dorsal aperture; DLA = dorsal
lamina; GL = genital length; GW = genital width; IVP = intervolsellar process; PM = paramere;
VP = ventral process; VR = ventral ridge. – NHMUK = Natural History Museum, London, UK;
UCRC = Entomology Research Museum, University of California, Riverside, USA.
Results
Genetic Analysis
Trichogramma aurosum Sugonjaev & Sorokina, 1976
Sequences were obtained for three specimens (one female, 2 males: UCRC molecular
vouchers PR20-009, PR20-010, and PR20-011, respectively). BLAST searches of Gen-
Bank identified several ITS2 sequences attributed to T. aurosum as having the highest
levels of similarity to our specimens (e.g., EF710754-710772; Samara et al., 2008).
Although similarity was reported only at around 96%, subsequent alignment of our
sequences with those from GenBank revealed that the overwhelming majority of the
differences resulted from simple length variation in a long microsatellite repeat region; a
common source of intraspecific variation in Trichogramma (Stouthamer et al., 1999).
Searches of BOLD revealed a 99.69-100% match to BIN (barcode index number)
BOLD:ADW8071, identified only to family (Trichogrammatidae) and containing public
records from Germany and Belarus, plus private records from Bulgaria and Sweden.
Trichogramma evanescens Westwood, 1833
Sequences were obtained for only a single specimen (PR20-383). BLAST searches of
GenBank and comparison of the ITS2 with those of earlier isolates from the Canary
Islands (JF415940-JF415944) confirmed this species was the cosmopolitan and highly
polyphagous T. evanescens. Similarly, comparison with BOLD revealed >98.7% match
with sequences attributed to T. evanescens, BIN BOLD:AAD6262.
Trichogramma zerynthiae Polaszek & Bolu sp. n.
Sequences of ITS2 and COI were variously obtained for four specimens (PR20-381,
PR20-382, PR20-459, and PR20-460). BLAST searches of the ITS2 sequences with
Genbank and comparison with those held in the UCRC Trichogramma database
(Stouthamer, unpubl.) did not reveal a significant match, the closest (93.7%) being a
unisexual species known only from Nova Scotia, Canada (U74600). However, compari-
son with BOLD revealed a 98.36–99.28% with an undetermined species referred to as
Trichogramma sp. 1 SW-2021a (BIN BOLD:AEM9723; GenBank MW834374-376).
This species, reared from Z. polyxena together with T. evanescens at Bağlar, is de-
scribed formally below. Voucher specimens of “Trichogramma sp. 1 SW-2021a” reared
from Iphiclides podalirius ?Author (Papillionidae) in Var, France, if available, should
be compared with the description of T. zerynthiae below, as they may be conspecific.
4 A. Polaszek et al.
Figure 2. A. Trichogramma aurosum genital capsule. a. Dorsal; b. Ventral; c. Aedeagus. B.
Trichogramma evanescens. Genital capsule. a. Dorsal; b. Ventral. C. Trichogramma zerynthiae.
Genital capsule. a. Dorsal; b. Ventral; c. Aedeagus. D. Trichogramma nr urquijoi. Genital cap-
sule. a. Dorsal; b. Ventral; c. Aedeagus.
Trichogramma sp. near urquijoi Cabello Garcia, 1986
No sequence data were obtained from the specimens reared from Zerynthia polyxena
from Eğil.
Taxonomy
Trichogramma aurosum Sugonjaev and Sorokina 1976. (Figures 2A, 3A)
Trichogramma aurosa Sugonjaev & Sorokina, 1976: 778.
Material examined. 7♀, 7♂: TURKEY: Diyarbakır, Kayapınar District (37'57'26"N
40'10'36"E), 744m, 2.xii.2019, from eggs of Allantus viennensis on Rosa sp., H. Bolu &
H. Çelik leg. (NHMUK, UCRC).
Zoology in the Middle East 5
Figure 3. A. Trichogramma aurosum. Male antenna. B. Trichogramma zerynthiae. Male antenna.
C. Trichogramma nr urquijoi. Male antenna.
Diagnosis. Male genitalia as in Figure 2A, posterior extension of DLA extending to
level of volsellar apical spines (Figure 2Aa). Posterior extension of DLA tapering rather
uniformly towards its rounded apex, only slightly concave laterally (Figure 2Aa).
Shoulder of DLA clearly visible, not prominent (Figure 2Aa). IVP very prominent,
reaching level of bases of volsellar apical spines (Figure 2Ab). VR extending to 1/3 the
length of DA (Figure 2Ab). Aedeagal apodemes slightly less than ½ AL (0.46 x; Figure
2Ac). Antenna (Figure 3A), 5.5 x maximum basal width. Longest seta 2.75 x maximum
basal width of antenna.
Host. Allantus viennensis (Schrank). Also recorded from the following hosts: Cimbex
femorata (Hym. Cimbicidae); Caliroa cerasi, Nematus tibialis, Pristiphora geniculate,
Profenusa thomsoni (Hym. Tenthredinidae); Trichoplusia ni (Lep. Noctuidae); Cydia
pomonella (Lep. Tortricidae) (Noyes, 2019).
Distribution. Bulgaria, Canada, Russia, Turkey (new country record), USA.
Trichogramma evanescens Westwood, 1833 (Figure 2B)
Trichogramma evanescens Westwood, 1833: 444.
Material examined. 3♂: TURKEY: Diyarbakır, Bağlar (37'50'04"N 39'54'02"E) 1048
m, vii.2020, from eggs of Zerynthia polyxena on Aristolochia rotunda, H. Bolu leg.
(NHMUK, UCRC).
Diagnosis: The identification of this problematic species is based on the most recent
interpretations linking male genitalia morphology and reference DNA sequences as in,
for example, Polaszek et al. (2012). The extant holotype of T. evanescens is a female,
while morphological species identification in Trichogramma relies almost entirely on
male genitalia. For a fuller discussion of the problems of species identification of T.
evanescens and other Trichogramma species, see Noyes et al. (2000) and Triapitsyn
(2016).
Male genitalia as in Figure 2B, posterior extension of DLA extending beyond level
of volsellar apical spines (Figure 2Ba). Posterior extension of DLA tapering rather ab-
ruptly at about half its length towards its rounded apex, clearly concave laterally (Figure
2Ba). Shoulder of DLA clearly visible, prominent (Figure 2Ba). IVP very prominent,
reaching level of bases of volsellar apical spines (Figure 2Bb). VR extending beyond
1/2 the length of DA (Figure 2Bb). Aedeagal apodemes about ½ AL (0.51 x; Figure
2Bc).
Hosts. Extremely polyphagous. A list of recorded hosts is in Polaszek (2010).
Distribution. Cosmopolitan (Polaszek, 2010).
6 A. Polaszek et al.
Figure 4. Trichogramma zerynthiae. A. Fore wing. B. Metasoma.
Trichogramma zerynthiae Polaszek & Bolu sp. nov. (Figures 2C, 3B, 4)
Material examined. Holotype: Male, TURKEY: Diyarbakır, Bağlar (37'50'04"N
39'54'02"E), 1048 m. vii.2020, from eggs of Zerynthia polyxena on Aristolochia rotun-
da, H. Bolu leg. (complete, dissected on a slide, NHMUK). – Paratypes: 6♂ (genitalia
only – remainder ground during DNA extraction), same data as holotype (NHMUK,
UCRC). Representative DNA sequences of the COI and ITS2 loci are deposited in
GenBank (OP580121-OP581023 and OP581341-OP581343, respectively).
Note. Morphological characters, relative measurements and ratios are based largely on
characters used by Pinto (1998) and explained here fully with reference to figures pro-
vided. The specialized terminology of the male genitalia is given in Figure 1, modified
from Pinto (1998). Trichogramma zerynthiae belongs to the subgenus Trichogramma
(Trichogramma).
Diagnosis. The form of the male genitalia, as with most Trichogramma species, is diag-
nostic. In particular the strongly narrowed sides of the genital capsule at the level of the
IVP. The very sparsely setose vein track RS1 of the fore wing is unusual for the genus.
In the key of Sorokina (1993), T. zerynthiae keys to T. polychrosis Chen & Pang, 1981.
However, using Pintureau (2008), the new species keys to T. gicai Pintureau and
Stefanescu, 2000, a species that was not yet described when Sorokina’s 1993 key was
published. Trichogramma zerynthiae can be distinguished from both species by the very
narrow and elongate DLA.
Description. Colour unremarkable, largely brown including legs, with the tibiae and
tarsi paler. Fore wings (Figure 4A) basally slightly infuscate. – Morphology: Flagellum
of antenna (Figure 3B) relatively short, 2x length of scape. Flagellar length 6x maxi-
mum basal flagellar width (not including setae); setae moderately long, gradually taper-
ing to apex, maximum flagellar setal length / basal flagellar width 3.2. Terminal placoid
sensilla extending beyond the end of the flagellum. Fore wing (Figure 4A) rather nar-
row, maximum width / maximum length 0.42. Marginal vein evenly curving onto stig-
mal vein; premarginal vein with 1 seta; marginal vein with two strong dorsal setae. RS1
unusually sparsely setose for the genus, with only 4 setae. Longest marginal fringe seta
0.16x maximum wing width. Anterior scutellar setae only slightly narrower and shorter
than posterior pair (Figure 4B). Genital capsule (figs 2C a-c) 3x longer than wide, sides
strongly narrowed at level of IVP. DLA (Figure 2Ca) originating anterior to middle of
Zoology in the Middle East 7
GC, elongate triangular, pointed at apex. Narrower in width to that of aedeagus at level
of IVP (Figure 2Ca). No shoulders present at base of DLA. AD/GL = 0.15; AW/GW =
0.29; DA length/GL = 0.50. Parameres straight, with apex normal. Volsellae with inner
margin arcuate, without any seta-like apical process. IVP (Figure 2Cb) prominent, nar-
row and parallel-sided. VR extending to ½ length of DA. Aedeagus (Figure 2Cc) sube-
qual in length to GL; apodemes approximately 0.5 X length AL.
Trichogramma sp. nr urquijoi Cabello Garcia, 1986 (Figures 2D, 3C)
Despite the lack of a formal identification or description of these specimens, figures and
a brief diagnosis are provided below so that host and distributional data can be assimi-
lated with other data should an identification be possible in future.
Diagnosis. Male genitalia as in Figure 2D a-c, posterior extension of DLA extending to
level of volsellar apical spines (Figure 2Da). Posterior extension of DLA tapering rather
uniformly towards its rounded apex, not concave laterally (Figure 2Da). Shoulder of
DLA not present (Figure 2Da). IVP prominent, but reaching only to level of bases of
volsellae (Figure 2Db). VR extending to just over 1/3 the length of DA (Figure 2Db).
Aedeagus clearly shorter than GL aedeagal apodemes ½ AL (0.5 x; Figure 2Dc). An-
tenna (Figure 3C), 5.4 x maximum basal width. Longest seta 3.6 x maximum basal
width of antenna.
Material examined. 1♂: TURKEY: Diyarbakır, Eğil (38'13'56"N 40'05'53"E), 895m,
vii.2020, from eggs of Zerynthia polyxena on Aristolochia rotunda, H. Bolu leg. (com-
plete, dissected on a slide, NHMUK).
Discussion
Eleven Trichogramma species have been recorded from Turkey (Öztemiz et al., 2013;
Ercan et al., 2022). The discovery in Turkey of T. aurosum and T. zerynthiae brings the
total number of Trichogramma now known from the country to 13. Unfortunately, three
Turkish species, T. buluti Bulut & Kilincer, Trichogramma kilinceri Bulut & Kilincer,
and T. turkeiense Bulut & Kilincer (Bulut & Kilincer, 1991), are not recognizable from
their descriptions, nor was it possible to locate any material. Originally attributed by the
authors to Kostadinov, no descriptions of these species by that author were ever pub-
lished.
Acknowledgements
HB and HC thank Dr Önder Çalmaşur (Atatürk University, Faculty of Agriculture, Department of
Plant Protection) for the identification of Allantus (Allantus) viennensis and Dr Felipe Gil (Grana-
da, Spain) for the identification of Zerynthia polyxena. AP is grateful to Dr Serguei Triapitsyn
(Entomology Research Museum, University of California, Riverside, USA) for access to his
English translation of Sorokina (1993), and for extremely useful comments on an earlier form of
this paper.
Disclosure Statement
No potential conflict of interest was reported by the authors.
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