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A morphological, biological and molecular approach reveals four cryptic species of Trissolcus Ashmead (Hymenoptera, Scelionidae), egg parasitoids of Pentatomidae (Hemiptera)
expand article infoFrancesco Tortorici, Elijah J. Talamas§, Silvia T. Moraglio, Marco G. Pansa, Maryam Asadi-Farfar|, Luciana Tavella, Virgilio Caleca
‡ University of Torino, Torino, Italy
§ Florida Department of Agriculture and Consumer Service, Gainesville, United States of America
| Urmia University, Urmia, Iran
¶ University of Palermo, Palermo, Italy
Open Access

Abstract

Accurate identification of parasitoids is crucial for biological control of the invasive brown marmorated stink bug, Halyomrpha halys (Stål). A recent work by Talamas et al. (2017) revised the Palearctic fauna of Trissolcus Ashmead, egg-parasitoids of stink bugs, and treated numerous species as junior synonyms of T. semistriatus (Nees von Esenbeck). In the present paper, we provide a detailed taxonomic history and treatment of T. semistriatus and the species treated as its synonyms by Talamas et al. (2017) based on examination of primary types, molecular analyses and mating experiments. Trissolcus semistriatus, T. belenus (Walker), T. colemani (Crawford), and T. manteroi (Kieffer) are here recognized as valid and a key to species is provided. The identification tools provided here will facilitate the use of Trissolcus wasps as biological control agents and as the subject of ecological studies.

Keywords

Biological control, taxonomy, brown marmorated stink bug

Introduction

Taxonomy of the genus Trissolcus Ashmead has received renewed attention in recent years (Talamas et al. 2015, 2017), largely because accurate identification of these wasps is needed to use them as biological control agents against the invasive brown marmorated stink bug (Halyomorpha halys (Stål)) in Europe and North America. Morphological similarity, sharing of hosts by various species of Trissolcus, and the historical complications presented in Talamas et al. (2017) and Buffington et al. (2018) are some of the challenges faced by taxonomists working with this group.

The revision of Palearctic Trissolcus (Talamas et al. 2017) provided keys to species, complete redescriptions, illustrations, and the utilization of new morphological characters. Many new synonymies were presented, including T. grandis (Thomson), T. artus Kozlov & Lê, T. colemani (Crawford), T. djadetshko (Rjachovskij), T. manteroi (Kieffer), T. nigripedius (Nakagawa), T. pentatomae (Rondani) and T. pseudoturesis (Rjachovskij) as junior synonyms of T. semistriatus (Nees von Esenbeck).

In support of studies on the egg-parasitoid complex of European Pentatomoidea, a survey of egg masses was conducted and previously collected specimens were also examined. Using the key to species provided by Talamas et al. (2017), Trissolcus specimens that emerged from Aelia rostrata Boheman, Arma custos (F.), Carpocoris spp., Eurygaster maura (L.), Graphosoma lineatum (L.), Palomena prasina (L.) collected between 1996 and 2017 in Piedmont (NW Italy) were identified as T. semistriatus. However, some consistent morphological differences were detected among the specimens, which instigated closer examination using multiple methods. The focus of this paper is the morphological and molecular analysis of species synonymized under T. semistriatus by Talamas et al. (2017), and the integration of mating tests, when possible, to confirm species delimitation.

Taxonomic history of T. semistriatus and related species

Species described by Walker

Telenomus belenus was described by Walker (1836), then transferred by Kieffer (1912) to Aphanurus Kieffer, then transferred to Microphanurus Kieffer (Kieffer 1926). Walker (1838) described Telenomus arminon but did not provide distinctive characters by which it could be identified or separated from Telenomus belenus. Kieffer (1912) transferred Te. arminon to Allophanurus Kieffer and provided a redescription. Kieffer did not mention if his treatment was based on type material, and we consider it unlikely that it was. Lectotypes for Te. belenus and Te. arminon were designated by Fergusson (1984, 1983), respectively, from material housed in the National Museum of Ireland, Dublin. Despite their antiquity, and thus priority, these species received no further taxonomic treatment.

Trissolcus semistriatus vs. T. grandis

In taxonomic literature, the distinction between T. semistriatus and T. grandis has long been questioned. Mayr (1879) and Nixon (1939) ascertained T. semistriatus to be a highly variable species. Masner (1959) wrote “On base of the check of type of Asolcus grandis (Thomson), the latter species was synonymized with semistriatus”. However, the meaning of this sentence is unclear because we have not found in the literature previous synonymy of T. grandis under T. semistriatus, and it is not clear that Masner sought to synonymize them for the first time. In this paper, Masner addressed characters considered to distinguish T. grandis and T. semistriatus (rugosity of the frons, leg color, longitudinal sculpture on the posterior mesoscutum, body length) based on the comparison of ~500 reared specimens and stated that these characters were variable within T. semistriatus. Viktorov (1967) considered T. grandis to be conspecific with T. semistriatus, but he did not formally treat it as a junior synonym. Subsequent authors considered T. semistriatus and T. grandis as different species, but without clearly defining the boundaries between them. Delucchi (1961) provided the first reliable character to distinguish T. semistriatus from T. grandis: the external surface of the hind femur is almost totally covered by setation in T. grandis (Figure 1), and he coupled this character with the color of the tibiae: reddish yellow in T. semistriatus, dark or black in T. grandis. Most authors continued to distinguish T. semistriatus and T. grandis by tibial color and ignored setation of the hind femora. This color-based distinction was employed in numerous previous and following papers (Delucchi 1961; Javahery 1968; Kozlov 1968, 1978; Safavi 1968; Voegelé 1969; Fabritius 1972; Kozlov and Lê 1977; Kozlov and Kononova 1983), and no substantial change was indicated in keys to species by Kononova (1995, 2014, 2015). Talamas et al. (2017) did not use tibial setation to differentiate between these species, but listed a new character, the form of the mesoscutal humeral sulcus, and mentioned setation of the first laterotergite, which was first presented as a character for species of Trissolcus by Johnson (1987). Although Talamas et al. (2017) treated these characters as variable within T. semistriatus, analysis of these characters in light of molecular and mating experiments has allowed us to use them for species delimitation.

Figure 1. 

Illustrations published by Delucchi (1961) where differences in the bare area of the external side of hind femora of Asolcus semistriatus (Fig. III, I) and A. grandis (Fig. III, H) are shown.

In a study on larval stages, Voegelé (1964) provided information about pigmentation of the membrane secreted by the larvae of different Trissolcus species reared in eggs of Eurygaster austriaca (L.). He distinguished T. semistriatus from T. grandis by the width of the pigmented band close to the margin of host egg operculum (see fig. 4 in Voegelé 1964). In his key to species, Safavi (1968) coupled color of the hind tibia (instead of mid tibia), and width of the pigmented band in larval membrane shown by Voegelé (1964), also adding different length ratios of the first two flagellomeres in males.

Trissolcus artus was distinguished by Kozlov and Kononova (1983) and Kononova (1995) from T. grandis (black tibiae) by its reddish-yellow tibiae, and from T. semistriatus by having a more elongate clava and infuscation in the fore wing. This last feature is used in the key by Kononova (2014, 2015) to distinguish T. artus from both T. grandis and T. semistriatus.

Trissolcus manteroi

Trissolcus manteroi was described by Kieffer (1909) as having the postmarginal vein (pm) slightly longer than the stigmal vein (st). In Kozlov and Kononova (1983), Koçak and Kilinçer (2003) and Kononova (2014, 2015), T. manteroi was distinguished by its postmarginal vein 1.3× as long as the stigmal vein, compared to 1.8× in Trissolcus rufiventris (Mayr), and 2× in T. grandis (=T. belenus) and T. semistriatus. Kononova (2014, 2015) also distinguished T. manteroi by the sculpture of T2, in which short longitudinal rugae are arranged medially and do not extend to the posterior half of the tergite, contrasting with longitudinal rugae throughout the anterior two thirds of T2 in T. belenus and T. semistriatus.

Trissolcus colemani

Crawford (1912) described Telenomus colemani from specimens that emerged from an egg mass of Dolycoris indicus Stål, collected in India. Masner and Muesebeck (1968) transferred this species into Trissolcus and no other information was recorded until its treatment as a junior synonym of T. semistriatus in Talamas et al. (2017).

Trissolcus pseudoturesis and T. djadetshko

The original description of Microphanurus (=Trissolcus) pseudoturesis Rjachovskij (Rjachovskij 1959) distinguished this species from M. djadetshko Rjachovskij and M. semistriatus by tibial color: completely yellow in M. pseudoturesis; reddish or yellow in M. djadetshko; almost black in M. semistriatus. Viktorov (1964) distinguished Asolcus (=Trissolcus) djadetshko and A. rufiventris by the lack of longitudinal striae on the posterior margin of the mesoscutum in contrast to their presence in A. pseudoturesis and A. semistriatus. Viktorov (1967) then modified his concept, considering the color of the hind tibia as a valid character to distinguish T. djadetshko from T. semistriatus and the color of femora to distinguish T. djadetshko from T. pseudoturesis. The keys to species by Kozlov (1968) and Fabritius (1972) distinguished T. djadetshko from T. grandis, T. pseudoturesis and T. semistriatus by the absence of longitudinal striation on the posterior mesoscutum and an absence of transverse striation on the frons, and T. pseudoturesis from T. grandis and T. semistriatus by color of the femora. Kozlov and Kononova (1983) separated T. djadetshko from both T. grandis and T. semistriatus by the absence of longitudinal striation on the posterior mesoscutum. Safavi (1968) and Voegelé (1969) separated T. djadetshko and T. pseudoturesis by their “ochraceous” femora from T. semistriatus and T. grandis (black femora), and separated T. djadetshko from T. pseudoturesis by longitudinal striae on the posterior margin of mesoscutum (vs. striate throughout) and the presence of parapsidal furrows. Koçak and Kilinçer (2003) distinguished T. djadetshko by its femora being reddish-yellow in contrast with dark brown or black femora in T. semistriatus and T. grandis, and separated T. djadetshko from T. pseudoturesis by sculpture on mesoscutum as in Voegelé (1969). Petrov (2013) again distinguished T. djadetshko on the basis of the mesoscutum without longitudinal wrinkles, contrasting with the clear longitudinal wrinkles of T. grandis, T. pseudoturesis and T. semistriatus, and he separated T. pseudoturesis from T. grandis and T. semistriatus by the color of femora. Kononova (2014, 2015) differentiated T. djadetshko by its yellow legs and mesoscutum without longitudinal rugae posteriorly from T. semistriatus and T. grandis having all femora black and mesoscutum with longitudinal rugae posteriorly, and T. pseudoturesis from T. grandis and T. semistriatus as in Kozlov (1968). Trissolcus djadetshko and T. pseudoturesis were treated as junior synonyms of T. semistriatus in Talamas et al. (2017).

Trissolcus waloffae, T. nixomartini and T. silwoodensis

Javahery (1968) described and keyed T. waloffae (Javahery) using leg color (predominantly brownish to reddish-yellow) and weakly indicated parapsidal furrows to separate it from T. grandis, T. semistriatus, T. nixomartini and T. silwoodensis, which he considered to have black femora in both sexes and be without parapsidal furrows. Characters provided to distinguish each of the last four species from each other were black vs. brown front tibiae, presence of infuscation of wings, color of wing venation, ratio between first flagellar segment and pedicel of male, sculpture of the head, distance between lateral ocelli and compound eye, and ‘weakly concave’ vs. ‘somewhat concave’ head. Trissolcus silwoodensis and T. nixomartini were previously treated as synonyms of T. grandis by Kozlov and Lê (1977).

Trissolcus crypticus

During a program for classical biological control of Nezara viridula L. in Australia, several ‘strains’ of different geographical populations of Trissolcus basalis (Wollaston) were introduced, starting in the 1930s (Clarke 1990). Of the strains introduced in subsequent years to the interior of Australia, one population imported from Pakistan (1961) was not able to efficiently control N. viridula (Clarke 1990). Clarke (1993) demonstrated that this ‘strain’ was indeed a different species, which he described as Trissolcus crypticus Clarke. Comparing T. crypticus with T. basalis, he considered the complete netrion sulcus (figure 1 in Clarke 1993) as the main diagnostic character for T. crypticus. Clarke analyzed specimens of Trissolcus rungsi (Voegelé) labelled by Voegelé and deposited in NHMUK and concluded that they were not the same species as T. crypticus, but did not present characters to support his hypothesis (Clarke 1993).

Material and methods

Collections

Primary types

Due to the challenge of historic confusion regarding species close to T. semistriatus, we treat only species for which the primary types were directly examined, or the diagnostic characters are clearly visible in photographs.

Images of the primary types of Telenomus colemani Crawford, Microphanurus djadetshko Rjachovskij, Trissolcus grandis Thomson, Telenomus Manteroi Kieffer, Microphanurus pseudoturesis Rjachovskij and Teleas semistriatus Nees von Esenbeck were made available via Specimage (specimage.osu.edu) by Talamas et al. (2017). Images of the lectotype of Telenomus nigripes Thomson, syntypes of Telenomus ovulorum Thomson, and additional images of the lectotype of Telenomus grandis were provided by Dr Hege Vårdal (Naturhistoriska Riksmuseet, Stockholm, Sweden).

Institutional acronyms

CNCI Canadian National Collection of Insects – Ottawa, Canada;

CNCI Dipartimento di Scienze Agrarie, Forestali e Alimentari, University of Torino – Torino, Italy;

EIHU Hokkaido University Museum, Entomology – Sapporo, Japan;

HMIM Hayk Mirzayans Insect Museum, Plant Pests and Diseases Research Institute – Tehran, Iran;

NHMUK, BMNH The Natural History Museum – London, United Kingdom;

NHMW Naturhistorisches Museum Wien – Wien, Austria;

NMID National Museum of Ireland – Dublin, Ireland;

MSNG, MSNG Museo Civico di Storia Naturale “Giacomo Doria” – Genoa, Italy;

MZUF Museo di Storia Naturale di Firenze, Sezione di Zoologia “La Specola”, Università degli Studi di Firenze – Florence, Italy;

NHRS Naturhistoriska Riksmuseet, Entomology – Stockholm, Sweden;

UCRC University of California, Riverside – CA, USA;

UNIPA Dipartimento di Scienze Agrarie, Alimentari e Forestali, Università degli Studi di Palermo – Palermo, Italy;

USNM National Museum of Natural History, Smithsonian Institution – Washington, DC, USA;

ZIN Zoological Museum, Academy of Sciences – St. Petersburg, Russia.

Geographical distribution and host association

The identification tools of previous literature are not reliable for identifying the species that we treat here. Hence, the geographical distribution and host associations presented in Material Examined sections derive only from specimens examined as part of this study.

Cybertaxonomy

Specimens used in this study were assigned collecting unit identifiers (CUIDs) and their associated collection and host association data were deposited in Hymenoptera Online (hol.osu.edu). In addition to the abbreviated Material examined sections, a DarwinCore archive is provided for each species (Suppl. material: S2–S5). These files contain the totality of specimens for which data is deposited in Hymenoptera Online, including specimens for which updated identification has not yet occurred, which can be assessed by the dates of determination. Taxonomic synopses, descriptions, and material examined sections were generated in the online, matrix-based program vSysLab (vsyslab.osu.edu) with a matrix based on that of Talamas et al. (2017).

Photography

A Leitz Großfeld-Stereomikroskop TS with magnification up to 160×, a Stereomicroscope Wild M3B with oculars 15×, and a spot light Leica CLS 150× were used for biometric diagnosis. A semi-transparent light shield was used to reduce glare and to diffuse the light. The lectotypes of T. belenus and T. arminon were photographed with a Macroscopic Solutions Macropod MicroKit with individual slices rendered in Helicon Focus 6. All other images were produced using a Leitz Dialux 20 EB compound microscope with a Leica DFC 290 Camera with LED spot light or dome light based on different points of view after techniques summarized in Buffington et al. (2005), Kerr et al. (2008) and Buffington and Gates (2008). LEICA APPLICATION SUITE V 3.7.0 software was used to manage image acquisition and ZERENE STACKER was used for merging of the image series into a single in-focus image.

Morphology

Terminology for surface sculpture follows the glossary by Harris (1979), Mikó et al. (2007), Yoder et al. (2010) and Talamas et al. (2017). Measurements of the head, mesosoma, metasoma, total body, and wing venation follow Masner (1980) and Tortorici et al. (2016). In the wing ratio expressed as st:pm:mg, the stigmal vein is treated as the benchmark unit (=1). Morphological terms largely follow Mikó et al. (2007) and were matched to concepts in the Hymenoptera Anatomy Ontology (Yoder et al. 2010) using the text analyzer function and a table of these terms and URI links is provided in Suppl. material: S1.

Additional abbreviations and terminology used in this paper: HL: head length; HW: head width; HH: head height, from vertex to distal end of clypeus; FCI: frontal cephalic index (HW/HH); LCI: lateral cephalic index (HH/HL); OOL:POL:LOL: ocular distance ratio, OOL as the benchmark unit (=1); IOS: interorbital space (Mikó et al. 2010); claval formula: the sequence of sensilla, from the apical antennomere (A11) to the last functional clavomere (Bin 1981), i.e. the last antennomere bearing one or two multiporous gustatory sensilla, as defined by Isidoro et al. (1996); compound eye height and width: measured when eye longitudinal axis is parallel to the focal plane.

Insect collecting and rearing

A host colony of E. maura used for rearing Trissolcus was established from adults collected on wheat in Piedmont (NW Italy) and maintained in cages under laboratory conditions (climatized chambers at 24 ± 1 °C, 65 ± 5% RH, L:D = 16:8). All eggs laid in the cages were collected and frozen at -20 °C. Because of the short egg-laying period of E. maura, freezing the eggs allowed the eggs to be used for a much longer time.

To obtain Trissolcus specimens, egg masses of E. maura and P. prasina were collected in the field in Piedmont (NW Italy) in the spring and summer of 2017. The field-collected egg masses were reared and checked daily. Trissolcus specimens that emerged from field-collected egg masses were allowed to mate. Some females were isolated in small plastic boxes (64.5 × 40.9 × 16 mm), fed with water and honey, and provided with E. maura frozen egg masses to produce progeny for use in subsequent tests.

For interbreeding experiments, specimens were isolated immediately following emergence to prevent mating, and females and males were maintained singly in plastic boxes as described above. When the parasitoids reach the early pupal stage inside the eggs, their red eyes are clearly visible through the transparent operculum of the host egg. Following observation of this feature (Figure 2), the eggs were checked at a frequency of 4–5 times per day to ensure that they were isolated prior to mating.

Figure 2. 

Pupal stage of Trissolcus sp. in Halyomorpha halys eggs, clearly indicated by the presence of eyes and ocelli, which are visible through the semi-transparent host egg.

Some of the progeny from isolated, mated females were selected for preservation, identification and molecular analysis. The remaining progeny were used in breeding experiments.

Molecular analyses

Molecular analyses were performed to confirm morphological identification and characterize the species. Genomic DNA was extracted from the metasoma of specimens from rearing experiments and pinned collection specimens according to Kaartinen et al. (2010), but doubling the proteinase K dose (5 µl of 20 mg ml−1 proteinase K). The barcode region of the cytochrome oxidase I (COI) gene was amplified using universal PCR primers for insects LCO1490 (5’-GGT CAA CAA ATC ATA AAG ATA TTG G-3’) and HCO2198 (5’-TAA ACT TCA GGG TGA CCA AAA AAT CA-3’) (Folmer et al. 1994). The PCR was performed in a 50 µl reaction volume: 2 µl of DNA, 37.9 µl molecular grade water, 5 µl 10× Qiagen PCR buffer, 3 µl dNTPs (25 mM each), 1.5 µl MgCl2, 0.2 µl of each primer (0.3 µM each), 0.2 µl Taq DNA Polymerase (Qiagen, Hilden, Germany). Thermocycling conditions were optimized to shorten reaction times and included initial denaturation at 94 °C for 300 s, followed by 35 cycles of 94 °C for 30 s, annealing at 52 °C for 45 s and extension at 72 °C for 60 s; then further 600 s at 72 °C for final extension. PCR products were purified using a commercially available kit (QIAquick PCR Purification Kit, Qiagen GmbH, Hilden, Germany) following the manufacturer’s instructions, and sequenced by a commercial service (Genechron S.r.l., Rome, Italy). The sequences were compared with the GenBank database and each other using the Basic Local Alignment Search Tool (http://www.ncbi.nlm.nih.gov/BLASTn). All sequences were aligned using ClustalW with default settings as implemented in Mega X. The pairwise nucleotide sequence distances among and within taxa were estimated using the Kimura 2-parameter model (K2P) of substitution (Kimura 1980) using Mega X (Kumar et al. 2018). The sequences generated from this study are deposited in the GenBank database. All residual DNA is archived at DISAFA.

Mating tests and reproductive isolation between T. belenus and T. semistriatus

For mating experiments, 1–2-day old virgin females and males were used. Four combinations for mating tests were done: T. semistriatus (♀) × T. belenus (♂); T. belenus (♀) × T. semistriatus (♂); T. semistriatus (♀) × T. semistriatus (♂); T. belenus (♀) × T. belenus (♂). The total number of interbreeding tests was 24: four replicates for each intraspecific mating combination and eight replicates for each interspecific mating combination. Each pair of wasps was observed at the stereomicroscope until the end of copulation or for 10 minutes if copulation did not occur. The pair then remained together in isolation for 24 hours. After the mating test, an egg mass of E. maura was provided to each female wasp for 24 hours of exposure. The egg masses were then moved to other plastic boxes until offspring emergence. Each mating test was considered successful when emerged offspring included females, because in all known Trissolcus species, only mated females can produce female offspring. We compared the percentage of mating success among the four combinations and the significance of the results was assessed with a chi-square test.

Results

Morphological analysis

The easiest task regarded the distinction of T. manteroi from T. semistriatus, T. belenus and T. colemani. Trissolcus manteroi clearly has a shorter postmarginal vein, only slightly longer than the stigmal vein; A7 has only one papillary sensillum instead of two in the other three species; and T. manteroi has no episternal foveae. The holotype of T. manteroi is thus morphologically very close to T. rufiventris, from which it can be differentiated by the length of the postmarginal vein.

The distinction of T. belenus and T. colemani from T. semistriatus is more nuanced and required an integrative approach to determine which morphological characters were congruent with the biological and molecular data. The results of this in-depth analysis demonstrate that some of the characters that Talamas et al. (2017) treated as intraspecifically variable have diagnostic power.

The presence or absence of setation on the external face of the hind femur, described in the key and figure III (I) (H) in Delucchi (1961), is a reliable character to distinguish T. grandis from T. semistriatus. However, in the lectotype of T. grandis and neotype of T. semistriatus this character is opposite to what was stated by Delucchi (1961). Furthermore, the holotype of T. colemani has the external surface of hind femur setose, as in the lectotype of T. grandis. The association proposed in Delucchi (1961): ‘external face of hind femora uncovered by hair’ – ‘reddish yellow tibiae’ is the typical combination for T. colemani, while Delucchi (1961) proposed it for T. semistriatus, and ‘external face of hind femora covered by hair’ – ‘dark or black tibiae’ is the typical combination for T. semistriatus. We conclude that this interpretation is contrary to what is found in type material.

Synonymy in T. belenus

In the analysis of original descriptions and images of lectotype of T. arminon and T. grandis, no remarkable characters were recognized to distinguish them from T. belenus, which we therefore consider it to be their senior synonym. In the analysis of type material of T. silwoodensis and T. nixomartini, previously considered junior synonym of T. grandis (Kozlov & Lê, 1977), we confirmed the findings of previous authors, and thus treat these species as junior synonyms of T. belenus. Mayr (1879) considered Telenomus ovulorum Thomson to be a junior synonym of Telenomus semistriatus Nees von Esenbeck, but through analysis of the photographs of type material of T. ovulorum Thomson, we recognized the character states of T. belenus, and therefore treat T. ovulorum as a junior synonym of T. belenus.

Synonymy in T. colemani

One paratype of T. djadetshko and three syntypes of T. pseudoturesis were analyzed via photographs and compared with the original description and photographs of the holotype of T. colemani. The character states of the two first species matched perfectly with those of the latter, leading us to treat T. colemani as the senior synonym of T. djadetshko and T. pseudoturesis. We conclude that the characters of T. crypticus match those in the holotype of T. colemani based on examination of T. crypticus paratypes collected in Pakistan and its original description (see figs 1, 3, 5 in Clarke 1993). We thus treat T. crypticus as a junior synonym of T. colemani.

Clarke (1993) also reported that “Examination of material of T. rungsi labelled by Voegelé (deposited in NHMUK) shows that this species is not the same of T. crypticus“ but he did not provide any distinguishing characters between the two species. Contrary to what was reported by Clarke (1993), in our analysis of the material deposited at NHMUK, 37 specimens labelled as “Asolcus rungsi Voegelé” were identified as T. colemani and four specimens labelled as “rungsi 1965 Voegele” were identified as T. basalis, while other 25 with the same last cumulative label were identified as T. colemani. This confirms our interpretation of the description and analysis of figures regarding A. rungsi and demonstrates confusion of species in the Moroccan rearing efforts at École Nationale d’Agriculture in Meknès.

The original description of Asolcus rungsi mentioned the presence of short traces of notauli (fig. 1, c. in Voegelé 1965); these traces are visible in all specimens T. colemani (Figure 23). However, because the location of the holotype of A. rungsi is not known, we were unable to examine it and at this time do not treat this species name as a synonym. The morphological analyses of the holotype and paratypes of T. waloffae showed the conspecificity of this species with T. colemani.

Molecular analysis

Barcode sequences were obtained from 17 Trissolcus specimens (Table 1). The Blast search showed that the sequences of T. semistriatus from Italy and from Iran had a 98% sequence identity with the GenBank sequence from Trissolcus nigripedius (accession no. AB971830). The sequences from the two specimens of T. colemani showed a 98% identity with a GenBank sequence with a Platygastridae sp. (accession no. KY839581), while the sequences from the specimens of T. manteroi, T. belenus and T. rufiventris showed a lower similarity with GenBank sequences. The final alignment consisted of 548 characters. Pairwise distance values within and among analyzed species are shown in Table 2. The genetic distances between the specimens identified as of the same species (which averaged between 0.000 ± 0.000 and 0.005 ± 0.002), were much lower than the mean pairwise distances observed between the specimens identified as of different species (from 0.105 ± 0.001 to 0.149 ± 0.000).

Specimen information and GenBank Accession Number for the sequences generated by this study.

Species Sex Country Year of collection GenBank accession number Collecting unit identifier
Trissolcus manteroi f ITALY 2010 MK906047 DISAFA-draw1465-HYM-0424
f ITALY 2010 MN603796 DISAFA-draw1465-HYM-0425
Trissolcus semistriatus f ITALY 2017 MK906048 DISAFA-draw1465-HYM-0233
f IRAN 2015 MK906049 USNMENT01223088
f ITALY 2017 MN603799 DISAFA-draw1465-HYM-0238
f ITALY 2017 MN603800 DISAFA-draw1465-HYM-0240
f ITALY 2016 MN603798 DISAFA-draw1465-HYM-0242
f ITALY 2016 MN603797 DISAFA-draw1465-HYM-0283
Trissolcus belenus f ITALY 2017 MK906050 DISAFA-draw1465-HYM-0014
f ITALY 2017 MN603802 DISAFA-draw1465-HYM-0012
f ITALY 2017 MN603803 DISAFA-draw1465-HYM-0013
f ITALY 2017 MN603804 DISAFA-draw1465-HYM-0016
f ITALY 2017 MN603806 DISAFA-draw1465-HYM-0018
f ITALY 2017 MN603805 DISAFA-draw1465-HYM-0019
Trissolcus colemani f IRAN 2015 MK906051 USNMENT01223460
f IRAN 2015 MN603801 USNMENT01223455
Trissolcus rufiventris f IRAN 2015 MN603807 UNIPA-HYM-S01347

Barcode mean pairwise genetic distances (± SE) between T. manteroi, T. semistriatus, T. belenus, T. colemani and T. rufiventris (under the diagonal), and within taxa (along the diagonal). n = number of sequences.

T. manteroi (n = 2) T. semistriatus (n = 6) T. belenus (n = 6) T. colemani (n = 2)
T. manteroi (n = 2) 0.000
T. semistriatus (n = 6) 0.139 ± 0.000 0.005 ± 0.002
T. belenus (n = 6) 0.139 ± 0.000 0.109 ± 0.000 0.000 ± 0.000
T. colemani (n = 2) 0.138 ± 0.000 0.105 ± 0.001 0.107 ± 0.000 0.000
T. rufiventris (n = 1) 0.144 ± 0.000 0.141 ± 0.001 0.149 ± 0.000 0.133 ± 0.00

Mating tests

Specimen pairs tested for intraspecific combination mated within ten minutes; pairs tested for interspecific combination did not mate within the 10-minute observation period.

All females used for the two intraspecific combinations successfully produced female offspring (Figure 3); as expected the sex ratio was similar, in T. belenus (♀ × ♂) combination 31 females and 5 males emerged, and in T. semistriatus (♀ × ♂) 21 females and 4 males emerged. Females used for the two interspecific combinations produced only male offspring, 78 males in the T. belenus (♀) × T. semistriatus (♂) combination, and 65 males in the T. semistriatus (♀) × T. belenus (♂) combination. A total of 3 females failed to reproduce, producing no offspring in either the intraspecific or interspecific combinations.

Figure 3. 

Sex ratio of emerged specimens. Combinations: T. belenus (♀ × ♂), n = 4; T. semistriatus (♀ × ♂), n = 4; T. belenus (♀) × T. semistriatus (♂), n = 8; T. semistriatus (♀) × T. belenus (♂), n = 8. Bars indicate standard deviation.

Key to Trissolcus of the Palearctic region (females)

Modified couplets for the Key to Trissolcus of the Palearctic region (females) in Talamas et al. (2017)

29 Ventral mesopleuron distinctly bulging; mesocoxa oriented parallel to long axis of body; dorsal frons with sculpture effaced, sometimes entirely smooth and shining; A7 with two papillary (basiconic) sensilla (figures 128–132 in Talamas et al. 2017) Trissolcus perepelovi (Kozlov)
Ventral mesopleuron not distinctly bulging; mesocoxa oriented at an angle of ~45° relative to long axis of body (Figure 6); dorsal frons evenly and densely covered in microsculpture; A7 with one papillary (basiconic) sensillum (Figure 10) 29A
29A Postmarginal vein in fore wing about twice as long as stigmal vein (Figure 14); metasoma yellow to dark brown, typically reddish-brown Trissolcus rufiventris (Mayr)
Postmarginal vein only slightly longer than stigmal vein (Figure 13); metasoma dark brown to black (Figure 18) Trissolcus manteroi (Kieffer)
32 Lateral mesoscutum with mesoscutal humeral sulcus present as a smooth furrow (Figure 25) 32A
Lateral mesoscutum with mesoscutal humeral sulcus comprised of distinct foveae (Figures 20–23) 32B
32A Lateral pronotum with netrion sulcus incomplete dorsally, netrion often poorly defined; medial part of occipital carina rounded in dorsal view Trissolcus basalis (Wollaston)
Lateral pronotum with netrion sulcus complete dorsally (Figures 5, 50, 53, 55, 60), netrion distinct; medial part of occipital carina angled (Figure 36), vertex of angle with short carina directed toward median ocellus Trissolcus semistriatus (Nees von Esenbeck)
32B Laterotergite 1 with line of 3 setae (Figures 30, 45) Trissolcus belenus (Walker)
Laterotergite 1 without setae (Figure 32) Trissolcus colemani (Crawford)

A matrix of the diagnostic characters used in this key is provided in Suppl. material: S6.

Trissolcus belenus (Walker)

Figures 4, 8, 12, 16, 20, 21, 26, 30, 33, 37, 41, 45–48, 49–51.

Telenomus Belenus Walker, 1836: 352 (original description).

Telenomus arminon Walker, 1838: 457 (original description).

Telenomus Nigrita Thomson, 1860: 172 (original description, synonymized by Kozlov (1968)); Kozlov 1968: 214 (junior synonym of Trissolcus grandis (Thomson)).

Telenomus frontalis Thomson, 1860: 170 (original description, synonymized by Kozlov (1968)); Kozlov 1968: 214 (junior synonym of Trissolcus grandis (Thomson)).

Telenomus grandis Thomson, 1860: 169 (original description).

Telenomus nigripes Thomson, 1860: 170 (original description, synonymized by Kozlov (1968)); Kozlov 1968: 214 (junior synonym of Trissolcus grandis (Thomson)); Fergusson 1984: 230 (lectotype designation); Johnson 1992: 629 (type information).

Telenomus ovulorum Thomson, 1860: 171 (original description, synonymized by Mayr (1879)); Mayr 1879: 704 (junior synonym of Telenomus semistriatus (Nees von Esenbeck)).

Teleas (?) Pentatomae Rondani: Rondani 1874: 135 (nomen nudum).

Teleas pentatomae Rondani, 1877: 199 (original description).

Telenomus ovulorum Thomson: Mayr 1879: 704. Junior synonym of Telenomus semistriatus (Nees von Esenbeck)

Telenomus nigritus Thomson: Dalla Torre 1898: 517 (emendation).

Telenomus pentatomae (Rondani): Dalla Torre, 1898: 518 (generic transfer).

Allophanurus Arminon (Walker): Kieffer 1912: 12 (description, generic transfer).

Aphanurus Belenus (Walker): Kieffer 1912: 83 (description, generic transfer).

Aphanurus Frontalis (Thomson): Kieffer 1912: 81 (description, generic transfer).

Aphanurus Grandis (Thomson): Kieffer 1912: 76 (description, generic transfer).

Aphanurus Nigrita (Thomson): Kieffer 1912: 79 (description, generic transfer).

Aphanurus nigripes (Thomson): Kieffer 1912: 75 (description, generic transfer).

Liophanurus Pentatomae (Rondani): Kieffer 1912: 69 (description, generic transfer).

Allophanurus arminon (Walker): Kieffer 1926: 23 (description, keyed).

Liophanurus pentatomae (Rondani): Kieffer 1926: 71 (description).

Microphanurus belenus (Walker): Kieffer 1926: 91, 102 (description, generic transfer, keyed).

Microphanurus frontalis (Thomson): Kieffer 1926: 91, 103 (description, generic transfer, keyed).

Microphanurus grandis (Thomson): Kieffer 1926: 91, 99 (description, generic transfer, keyed); Debauche 1947: 256 (description).

Microphanurus nigripes (Thomson): Kieffer 1926: 91, 98 (description, generic transfer, keyed).

Microphanurus nigritus (Thomson): Kieffer 1926: 91, 100 (description, generic transfer, keyed).

Asolcus grandis (Thomson): Masner 1959: 376. (diagnosis, variation); Delucchi 1961: 44, 60 (description, keyed); Voegelé 1964: 28 (keyed); Javahery 1968: 419 (keyed); Voegelé 1969: 150 (keyed).

Trissolcus grandis (Thomson) syn. nov.: Viktorov 1967: 91 (generic transfer, keyed); Safavi 1968: 416 (keyed); Kozlov 1968: 200, 214 (description, lectotype designation, synonymy, keyed); Fabritius 1972: 32, 35. (keyed; host catalogue; distribution); Viggiani and Mineo 1974: 156, 160, 161 (description, keyed); Kozlov and Lê 1977: 512 (synonymy, keyed); Kozlov 1978: 636 (description); Kozlov 1981: 187 (keyed); Kozlov and Kononova 1983: 110 (description); Johnson 1992: 629 (cataloged, type information); Kononova 1995: 96 (keyed); Doganlar 2001: 112 (description); Koçak and Kilinçer 2003: 302, 307 (keyed, description); Fabritius and Popovici 2007: 158 (host informations, distribution); Buhl & O’Connor, 2010: 154 (distribution); Ali 2011: 10 (keyed); Ghahari et al. 2011: 596 (host association, listed); Guz et al. 2013: 87 (description, phylogenetic relationships); Petrov 2013: 326 (keyed); Kononova 2014: 1424 (keyed); Kononova 2015: 262 (keyed); Talamas et al. 2017: 129, 135 (junior synonym of Trissolcus semistriatus (Nees von Esenbeck), type information).

Asolcus nixomartini Javahery, 1968: 419, 429 (original description, keyed, synonymized by Kozlov and Lê (1977)); Kozlov, and Lê 1977: 512 (junior synonym of Trissolcus grandis (Thomson)); Johnson 1992: 629 (type information).

Asolcus silwoodensis Javahery, 1968: 419, 425 (original description, keyed, synonymized by Kozlov and Lê (1977)); Kozlov, and Lê 1977: 512 (junior synonym of Trissolcus grandis (Thomson)); Johnson 1992: 629 (type information).

Trissolcus pentatomae (Rondani) syn. nov.: Bin 1974: 463 (generic transfer, lectotype designation); Johnson 1992: 634 (cataloged, type information); Talamas et al. 2017: 130, 135 (junior synonym of Trissolcus semistriatus (Nees von Esenbeck), type information).

Trissolcus belenus (Walker): Fergusson 1978: 120 (generic transfer); Fergusson 1984: 230 (lectotype designation); Johnson 1992: 623 (cataloged, type information); Kononova 2014: 1426 (possibly in Telenomus); Kononova 2015: 264 (possibly in Telenomus).

Trissolcus nigripes (Thomson) syn. nov.: Fergusson 1978: 120 (generic transfer).

Trissolcus nixomartini (Javahery) syn. nov.: Fergusson 1978: 120 (generic transfer); Fergusson 1984: 230 (type information).

Trissolcus silwoodensis (Javahery) syn. nov.: Fergusson 1978: 120 (generic transfer); Fergusson 1984: 230 (type information).

Trissolcus arminon (Walker) syn. nov.: Fergusson 1983: 208 (generic transfer, description, lectotype designation); Fergusson 1984: 230 (type information); Johnson 1992: 622 (cataloged, type information).

Trissolcus ovulorum (Thomson) comb. nov., syn. nov.

Diagnosis

The presence of setae on the first laterotergite (Figures 30, 45) allows T. belenus to be easily diagnosed, as only two other Palearctic species share this character: T. saakowi and T. mitsukurii (Ashmead). Both of these species have distinct notauli, which are absent in T. belenus (Figures 20, 22). Additionally, the hyperoccipital carina is entirely absent in T. belenus (Figures 33, 47, 49), whereas it is complete in T. saakowi and present posterior to the lateral ocellus in T. mitsukurii.

Description

Body length: 1.03–1.1 mm, median = 1.06 mm, SD = 0.02, n = 20. Body color: head, mesosoma, and metasoma black.

Head. FCI = 1.4; LCI = 1.9; IOS = 0.3 mm; OOL:POL:LOL = 1:12:5.8. Color of radicle: dark brown. Length of radicle: about equal to width of clypeus. Color of A1–A6 in female: distal A2 yellow to light brown, otherwise black. Color of A7–A11 in female: black. Number of papillary sensilla on A6: 0. Number of papillary sensilla on A7: 2. Facial striae: absent. Number of clypeal setae: 6. Shape of gena in lateral view: narrow. Genal carina: present only at base of mandible. Malar striae: absent. Sculpture of malar sulcus: distinctly and sparsely striate. Orbital furrow: uniform in width between midpoint of eye and malar sulcus. Macrosculpture of frons directly dorsal to the antennal scrobe: coarsely rugose. Preocellar pit: present. Setation of lateral frons: sparse; moderately dense. Punctation of lateral frons: sparse. Sculpture directly ventral to preocellar pit: dorsoventrally fluted. Rugae on lateral frons: weakly developed to absent. OOL: less than one ocellar diameter. Hyperoccipital carina: absent. Macrosculpture of posterior vertex: absent. Microsculpture on posterior vertex along occipital carina: granulate. Anterior margin of occipital carina: crenulate. Medial part of occipital carina in dorsal view: rounded.

Mesosoma. Epomial carina: present. Macrosculpture of lateral pronotum directly anterior to netrion: finely rugulose. Netrion sulcus: complete. Pronotal suprahumeral sulcus in posterior half of pronotum: undifferentiated from sculpture of dorsal pronotum. Number of episternal foveae: 2. Course of episternal foveae ventrally: distinctly separate from postacetabular sulcus. Course of episternal foveae dorsally: distinctly separate from mesopleural pit. Subacropleural sulcus: present. Speculum: transversely strigose. Mesopleural pit: extending ventrally into dorsoventral furrow parallel to mesopleural carina. Mesopleural carina: well defined anteriorly, poorly defined to absent posteriorly. Sculpture of femoral depression: smooth. Patch of striae at posteroventral end of femoral depression: present, striae oblique to long axis of femoral depression. Setal patch at posteroventral end of femoral depression: present as a line of setae. Microsculpture of anteroventral mesopleuron: present throughout. Macrosculpture of anteroventral mesopleuron: absent. Postacetabular sulcus: comprised of large cells. Mesopleural epicoxal sulcus: comprised of cells. Setation of posteroventral metapleuron: absent. Sculpture of dorsal metapleural area: absent. Posterodorsal metapleural sulcus: present as a line of foveae. Paracoxal sulcus in ventral half of metapleuron: indistinguishable from sculpture. Length of anteroventral extension of metapleuron: elongate, extending to base of mesocoxa. Apex of anteroventral extension of metapleuron: rounded. Metapleural epicoxal sulcus: present as coarse rugae. Mesoscutal humeral sulcus: comprised of cells. Median mesoscutal carina: absent. Microsculpture of mesoscutum: imbricate-punctate anteriorly, becoming longitudinally imbricate-strigate posteriorly. Mesoscutal suprahumeral sulcus: comprised of cells. Length of mesoscutal suprahumeral sulcus: two-thirds the length of anterolateral edge of mesoscutum. Parapsidal line: absent. Notaulus: absent. Median protuberance on anterior margin of mesoscutellum: absent. Shape of dorsal margin of anterior lobe of axillar crescent: acute. Sculpture of anterior lobe of axillar crescent: dorsoventrally strigose. Area bound by axillar crescent: smooth. Macrosculpture of mesoscutellum: absent. Microsculpture on mesoscutellum: imbricate-punctate laterally to granulate medially. Median mesoscutellar carina: absent. Setation of posterior scutellar sulcus: present. Form of metascutellum: single row of cells. Metanotal trough: foveate, foveae occupying more than half of metanotal height. Metapostnotum: invaginated near lateral edge of metascutellum. Length of postmarginal vein: about twice as long as stigmal vein. Color of legs: coxae dark brown to black, femora and tibia dark brown with yellowish tips, trochanters and tarsi yellow to pale brown. Anteroventral area of hind femora: not covered by setae. Anteromedial portion of metasomal depression: smooth.

Metasoma. Width of metasoma: about equal to width of mesosoma. Longitudinal striae on T1 posterior to basal costae: pair of longitudinal submedial carinae separate a lateral smooth area from an internal area where striate sculpture starts with basal grooves. Number of sublateral setae (on one side): 1. Setation of laterotergite 1: present. Length of striation on T2: extending two-thirds the length of the tergite. Setation of T2: present in a transverse line and along lateral margin. Setation of laterotergite 2: present.

Host associations. Pentatomidae: Aelia rostrata; Arma custos; Carpocoris sp.; Dolycoris sp.; Graphosoma italicum Müller; Palomena prasina; Picromerus bidens (L.); Piezodorus sp.; sentinel frozen eggs of Halyomorpha halys. Scutelleridae: Eurygaster integriceps Puton; Eurygaster maura.

Link to distribution map

Material examined

Lectotype, male Telenomus Belenus: England and Western Europe: no date, NMINH_2018_11_49 (deposited in NMID); Lectotype, female, Telenomus arminon: United Kingdom: England, Dorset County, Lyme Regis, no date, NMINH_2018_11_46 (deposited in NMID); Holotype, female, Asolcus nixomartini: United Kingdom: England, Windsor and Maidenhead Unit. Auth., Silwood Park, 1966, reared from egg, M. Javahery, B.M. TYPE HYM. 9.798 (deposited in BMNH); Paratypes of Asolcus nixomartini: United Kingdom: 1 female, 2 males, UNIPA-HYM-S01317–S01318 (BMNH); OSUC 17734 (BMNH); Holotype, female, Asolcus silwoodensis: United Kingdom: England, Windsor and Maidenhead Unit. Auth., Silwood Park, 1966, reared from egg, M. Javahery, B.M. TYPE HYM. 9.797 (deposited in BMNH); Paratypes of Asolcus silwoodensis: United Kingdom: 4 females, 4 males, UNIPA-HYM-S01309–S01316 (BMNH). Syntype males, Telenomus ovulorum Thomson: Sweden: no date, Boheman, NHRS-HEVA 000006872 (deposited in NHRS). Lectotype, female, Telenomus nigripes: Sweden: Västra Götaland, no date, Boheman, NHRS-HEVA 000006873 (deposited in NHRS). Paratype of T. nixomartini: United Kingdom: 1 male, OSUC 17734 (BMNH). Other material: (437 females, 67 males, 21 pins with multiple specimens). China: 1 female, OSUC 571231 (OSUC). Iran: 16 females, HMIM-HYM-05–06, 08–09, 011–012, 014, 027, 039 (HMIM); USNMENT01223080–01223082, 01223425, 01223430, 01223435, 01223440 (UNIPA). Italy: 366 females, 63 males, 17 pins with multiple specimens, DISAFA-draw1465-HYM-0006–0219 (DISAFA); MSNG -HYM-0001–0004, USNMENT01223249–01223258 (MCSN); USNMENT01223090–01223130, 01223132–01223139, 01223230–01223246 (UNIPA). Morocco: 24 female, 1 pin with multiple specimens, OSUC 17729 (BMNH); USNMENT01223131 (UNIPA). Portugal: 6 females, 1 male, 1 pin with multiple specimens, USNMENT00916191, 00916210–00916213, 00916217 (BMNH). Russia: 4 females, 2 males, 2 pins with multiple specimens, OSUC 17796–17797 (BMNH). Sweden: 12 females, 2 males, UNIPA-HYM-S01306–S01307, USNMENT00916047, USNMENT00916051, USNMENT00916052, USNMENT00916070, USNMENT00916302–00916309 (BMNH). Switzerland: 6 females, DISAFA-draw1465-HYM-0001–0005 (DISAFA); USNMENT01109059 (USNM). Tanzania: 1 female, USNMENT01223480 (MZUF). United Kingdom: 1 female, 1 male, UNIPA-HYM-S01308 (BMNH); USNMENT00896318 (CNCI).

Trissolcus colemani (Crawford)

Figures 5, 9, 17, 22, 23, 27, 31, 34, 38, 42, 52–55

Telenomus colemani Crawford, 1912: 2 (original description).

Microphanurus djadetshko Ryakhovskii, 1959: 84, 87 (original description, keyed).

Microphanurus pseudoturesis Ryakhovskii, 1959: 83, 85 (original description, keyed).

Microphanurus rossicus Ryakhovskii, 1959: 83, 86 (original description, keyed, synonymized by Viktorov (1964)); Viktorov 1964: 1021 (junior synonym of Trissolcus pseudoturesis (Ryakhovskii)); Johnson 1992: 635 (type information).

Asolcus nigribasalis Voegelé, 1962: 155 (original description); Voegelé 1964: 28 (keyed); Voegelé 1965: 96, 108 (variation, diagnosis, keyed); Voegelé 1969: 151 (junior synonym of Asolcus djadetshko (Ryakhovskii)).

Asolcus djadetshko (Ryakhovskii): Viktorov 1964: 1015, 1021 (description, generic transfer, removed from synonymy with Telenomus scutellaris Thomson, keyed); Voegelé 1969: 151 (synonymy, keyed, spelling error).

Asolcus pseudoturesis (Ryakhovskii): Viktorov 1964: 1013, 1021 (description, generic transfer, synonymy, keyed); Voegelé 1969: 151 (synonymy, keyed).

Asolcus bennisi Voegelé, 1964: 119 (original description); Voegelé 1965: 96, 108 (variation, diagnosis, keyed); Voegelé 1969: 151 (junior synonym of Asolcus pseudoturesis (Ryakhovskii)).

Trissolcus djadetshko (Ryakhovskii) syn. nov.: Viktorov 1967: 91 (generic transfer, keyed); Safavi 1968: 415 (keyed); Kozlov 1968: 200 (keyed); Fabritius 1972: 31 (keyed); Kozlov and Lê 1977: 512 (keyed); Kozlov 1978: 636 (description); Kozlov 1981: 187 (keyed); Kozlov and Kononova 1983: 115 (description); Johnson 1992: 626 (cataloged, type information); Kononova 1995: 96 (keyed); Koçak and Kilinçer 2000: 171 (description, diagnosis, new distribution record for Turkey); Koçak and Kilinçer 2003: 303, 313 (keyed, description); Fabritius and Popovici 2007: 159 (checklist, host information, distribution); Ghahari et al. 2011: 595 (listed); Petrov 2013: 326 (keyed); Kononova 2014: 1425 (keyed); Kononova 2015: 263 (keyed); Talamas et al. 2017: 129 (junior synonym of Trissolcus semistriatus (Nees von Esenbeck)).

Trissolcus pseudoturesis (Ryakhovskii) syn. nov.: Viktorov 1967: 91 (generic transfer, keyed); Safavi 1968: 415 (keyed); Kozlov 1968: 200 (keyed); Fabritius 1972: 31 (keyed); Kozlov and Lê 1977: 512 (keyed); Kozlov 1978: 636 (description); Kozlov and Kononova 1983: 114 (description); Johnson 1992: 635 (cataloged, type information); Kononova 1995: 96 (keyed); Koçak and Kilinçer 2003: 302, 310 (keyed, description); Ghahari et al. 2011: 596 (listed); Petrov 2013: 326 (keyed); Kononova 2014: 1425 (keyed); Kononova 2015: 263 (keyed).

Trissolcus colemani (Crawford): Masner & Muesebeck 1968: 72 (type information, generic transfer); Johnson 1992: 625 (cataloged, type information).

Asolcus waloffae Javahery, 1968: 419 (original description, keyed).

Asolcus djadestshko (Ryakhovskii): Voegelé 1969: 151 (synonymy, keyed, spelling error).

Trissolcus bennisi (Voegelé): Kozlov & Lê 1977: 516 (generic transfer, keyed); Kozlov 1978: 637 (description); Kozlov and Kononova 1983: 122 (description); Johnson 1992: 623 (cataloged, type information); Kononova 2014: 1425 (keyed); Kononova 2015: 263 (keyed).

Trissolcus nigribasalis (Voegelé): Kozlov & Lê 1977: 518 (keyed); Kozlov 1978: 637 (description); Kozlov and Kononova 1983: 124 (description); Johnson 1992: 633 (cataloged, type information); Kononova 2014: 1425 (keyed); Kononova 2015: 263 (keyed).

Trissolcus waloffae (Javahery) syn. nov.: Kozlov & Lê 1977: 516 (keyed, generic transfer); Kozlov 1978: 637 (description); Kozlov and Kononova 1983: 123 (description); Fergusson 1984: 231 (type information); Johnson 1992: 640 (cataloged, type information); Kononova 2014: 1425 (keyed); Kononova 2015: 263 (keyed).

Trissolcus crypticus Clarke syn. nov., 1993: 524 (original description); Ghahari et al. 2011: 595 (new distribution record for Iran, host association, listed); Kononova 2014: 1426 (status unknown (not examined)); Kononova 2015: 264 (status unknown (not examined)).

Diagnosis

Trissolcus colemani is identified by a combination of characters more than by the presence of a distinct feature. The foveate mesoscutal humeral sulcus (Figures 21, 23) separates it from all the species treated here with the exception of T. belenus (Figures 20, 22). Trissolcus colemani and T. belenus are very similar in general appearance and these two species can be separated most reliably by setation of laterotergite 1: present in T. belenus (Figures 30, 45) and absent in T. colemani (Figure 31, 53). The anteroventral extension of the metapleuron reaches the mesocoxa in lateral view in both T. belenus and T. colemani and exhibits difference in the shape of its apex between these species. In T. colemani, the anteroventral extension of the metapleuron is very slender (Figure 5) compared to T. belenus, in which it is thicker, and the apex is rounded (Figure 4).

Description

Body length: 0.96–1.10 mm, m = 1.01 mm, SD = 0.03, n = 22. Body color: head, mesosoma, and metasoma black.

Head. FCI = 1.5; LCI = 1.7; IOS = 0.31 mm; OOL:POL:LOL = 1:13:5.9. Color of radicle: brown. Length of radicle: about equal to width of clypeus. Color of A1-A6 in female: variably yellow to brown. Color of A7–A11 in female: brown to black. Number of papillary sensilla on A6: 0. Number of papillary sensilla on A7: 2. Facial striae: absent. Number of clypeal setae: 6. Shape of gena in lateral view: narrow. Genal carina: present only at base of mandible. Malar striae: absent. Sculpture of malar sulcus: distinctly and sparsely striate. Orbital furrow: uniform in width between midpoint of eye and malar sulcus. Macrosculpture of frons directly dorsal to the antennal scrobe: weakly rugose. Preocellar pit: present. Setation of lateral frons: sparse; moderately dense. Punctation of lateral frons: sparse. Sculpture directly ventral to preocellar pit: dorsoventrally fluted. Rugae on lateral frons: coarse. OOL: less than one ocellar diameter. Hyperoccipital carina: absent. Macrosculpture of posterior vertex: absent. Microsculpture on posterior vertex along occipital carina: granulate. Anterior margin of occipital carina: crenulate. Medial part of occipital carina in dorsal view: rounded.

Mesosoma. Epomial carina: present. Macrosculpture of lateral pronotum directly anterior to netrion: finely rugulose. Netrion sulcus: complete. Pronotal suprahumeral sulcus in posterior half of pronotum: undifferentiated from sculpture of dorsal pronotum. Number of episternal foveae: 2; 3. Course of episternal foveae ventrally: distinctly separate from postacetabular sulcus. Course of episternal foveae dorsally: distinctly separate from mesopleural pit. Subacropleural sulcus: present. Speculum: transversely strigose. Mesopleural pit: extending ventrally into dorsoventral furrow parallel to mesopleural carina. Mesopleural carina: well defined anteriorly, poorly defined to absent posteriorly. Sculpture of femoral depression: smooth. Patch of striae at posteroventral end of femoral depression: present, striae oblique to long axis of femoral depression. Setal patch at posteroventral end of femoral depression: present. Microsculpture of anteroventral mesopleuron: present throughout. Macrosculpture of anteroventral mesopleuron: absent. Postacetabular sulcus: comprised of large cells. Mesopleural epicoxal sulcus: comprised of cells. Setation of posteroventral metapleuron: absent. Sculpture of dorsal metapleural area: absent. Posterodorsal metapleural sulcus: present as a line of foveae. Paracoxal sulcus in ventral half of metapleuron: indistinguishable from sculpture. Length of anteroventral extension of metapleuron: elongate, extending to base of mesocoxa. Apex of anteroventral extension of metapleuron: acute. Metapleural epicoxal sulcus: present as coarse rugae. Mesoscutal humeral sulcus: comprised of cells. Median mesoscutal carina: absent. Microsculpture of mesoscutum: imbricate-punctate anteriorly, becoming longitudinally imbricate-strigate posteriorly. Mesoscutal suprahumeral sulcus: comprised of cells. Length of mesoscutal suprahumeral sulcus: two-thirds the length of anterolateral edge of mesoscutum. Parapsidal line: absent. Notaulus: presence of short traces. Median protuberance on anterior margin of mesoscutellum: absent. Shape of dorsal margin of anterior lobe of axillar crescent: acute. Sculpture of anterior lobe of axillar crescent: dorsoventrally strigose. Area bound by axillar crescent: smooth. Macrosculpture of mesoscutellum: absent. Microsculpture on mesoscutellum: imbricate-punctate. Median mesoscutellar carina: absent. Setation of posterior scutellar sulcus: present. Form of metascutellum: single row of cells. Metanotal trough: foveate, foveae occupying more than half of metanotal height. Metapostnotum: invaginated near lateral edge of metascutellum. Length of postmarginal vein: about twice as long as stigmal vein. Color of legs: coxae dark brown to black, femora yellow to light brown with yellowish tips, tibia trochanters and tarsi yellow to pale brown. Anteroventral area of hind femora: not covered by setae. Anteromedial portion of metasomal depression: smooth.

Metasoma. Width of metasoma: about equal to width of mesosoma. Longitudinal striae on T1 posterior to basal costae: pair of longitudinal submedial carinae separate a lateral smooth area from an internal area where striate sculpture starts with basal grooves. Number of sublateral setae (on one side): 1. Setation of laterotergite 1: absent. Length of striation on T2: extending two-thirds the length of the tergite. Setation of T2: present in a transverse line and along lateral margin. Setation of laterotergite 2: present.

Host associations

Pentatomidae: Dolycoris indicus (Type host); Aelia acuminata L.; Aelia sp.; Brachynema germarii (Kolenati); Dolycoris sp.; Graphosoma semipunctatum (F.); Graphosoma sp. Scutelleridae: Eurygaster integriceps; Eurygaster maura.

Link to distribution map

Material examined

Holotype, female, Telenomus colemani: India: Karnataka St., Hongashenhalli (Hunsmanalli), 6.II.1909, L. C. Coleman, USNMENT00989063 (deposited in USNM). Syntype, female, Microphanurus pseudoturesis: Ukraine: Donets’k (Stalinskaya) Reg., V-1952/1953–VII-1952/1953, V. Rjachovsky, USNMENT00954008 (deposited in ZIN). Syntype, female, Microphanurus pseudoturesis: Ukraine: Donets’k (Stalinskaya) Reg., V-1952/1953–VII-1952/1953, V. Rjachovsky, USNMENT00954010. Holotype, female, A. waloffae: United kingdom: England, Windsor and Maidenhead Unit. Auth., Silwood Park, VI-1965, reared, B.M. TYPE HYM. 9.795 (deposited in BMNH). Paratypes of Trissolcus crypticus: Pakistan: 3 females, 3 males, OSUC 17744, UNIPA-HYM-S01319–S01323 (BMNH). Paratype of Microphanurus djadetshko: Ukraine: 1 female, USNMENT00954012 (ZIN). Paratypes of Asolcus waloffae: United kingdom: 11 females, 11 males, 1 pin with multiple specimens, OSUC 17731, UNIPA-HYM-S01324, USNMENT0119671–0119674 (BMNH).

Other material: (144 females, 52 males, 6 pins with multiple specimens) China: 1 female, UCRC ENT 142649 (UCRC). France: 1 female, USNMENT00896254 (CNCI). Greece: 1 female, USNMENT00896062 (CNCI). Iran: 17 females, HMIM-HYM-015, 017–018, 020–021, 025, 028, 031, 036, 042 (HMIM); USNMENT01223445, 01223450, 01223455, 01223460, 01223465, 01223470, 01223475 (UNIPA). Italy: 82 females, 19 males, 2 pins with multiple specimens, DISAFA-draw1466-HYM-0483–0488 (DISAFA); USNMENT01223144, 01223146–01223221, 01223481 (UNIPA). Morocco: 39 females, 31 males, 3 pins with multiple specimens, OSUC 17728, 17743 (BMNH); UNIPA-HYM-S01325 (BMNH). Russia: 3 females, 1 pin with multiple specimens, USNMENT01223222–01223223 (MCSN). Sweden: 2 males, USNMENT00916067–00916068 (BMNH).

Trissolcus manteroi (Kieffer)

Figures 6, 10, 13, 18, 24, 28, 35, 39, 43, 56–58

Telenomus Manteroi Kieffer, 1909: 268 (original description).

Aphanurus Manteroi (Kieffer): Kieffer 1912: 84 (description, generic transfer).

Microphanurus manteroi (Kieffer): Kieffer 1926: 91, 102. (description, generic transfer, keyed); Boldaruyev 1969: 163, 170 (description, keyed)

Trissolcus manteroi (Kieffer): Kozlov 1968: 199 (keyed); Fabritius 1972: 31 (keyed); Bin 1974: 462 (type information); Kozlov and Lê 1977: 514 (keyed); Kozlov 1978: 636 (description); Kozlov and Kononova 1983: 117 (description); Johnson 1992: 631 (cataloged, type information); Koçak and Kilinçer 2000: 174 (description, diagnosis, new distribution record for Turkey); Koçak and Kilinçer 2003: 302, 310 (keyed, description of female); Koçak and Kodan 2006: 41 (description of male); Fabritius and Popovici 2007: 159. (host information, distribution); Ghahari et al. 2011: 596 (listed); Kononova 2014: 1424 (keyed); Kononova 2015: 262 (keyed); Talamas et al. 2017: 129, 135 (junior synonym of Trissolcus semistriatus (Nees von Esenbeck), type information).

Diagnosis

Trissolcus manteroi and T. rufiventris are the only two species of Palearctic Trissolcus in which females exhibit a 1-2-2-2-1 claval formula (Figure 10). These two can be separated from each other by the length of the postmarginal vein in the fore wing: slightly longer than the stigmal vein in T. manteroi (Figure 13) and about twice as long as the stigmal vein in T. rufiventris (Figure 14). These two species can also be separated from each other by the form of the mesopleural epicoxal sulcus, which is comprised of cells in T. manteroi and is a smooth furrow in T. rufiventris.

Description

Female body length: 0.99–1.09 mm, m = 1.04 mm, SD = 0.02, n = 16. Body color: head, mesosoma, and metasoma black.

Head. FCI = 1.4; LCI = 1.8; IOS = 0.3 mm; OOL:POL:LOL = 1:12:5.3. Color of radicle: dark brown. Length of radicle: less than width of clypeus. Color of A1–A6 in female: distal A2 yellow to light brown, otherwise black. Color of A7–A11 in female: black. Number of papillary sensilla on A6: 0. Number of papillary sensilla on A7: 1. Facial striae: absent. Number of clypeal setae: 6. Shape of gena in lateral view: narrow. Genal carina: present only at base of mandible. Malar striae: absent. Sculpture of malar sulcus: weakly and densely striate. Orbital furrow: uniform in width between midpoint of eye and malar sulcus. Macrosculpture of frons directly dorsal to the anterior ocellus: weakly rugose. Preocellar pit: present. Setation of lateral frons: sparse; moderately dense. Punctation of lateral frons: sparse. Sculpture directly ventral to preocellar pit: dorsoventrally fluted. Rugae on lateral frons: weakly developed to absent. OOL: less than one ocellar diameter. Hyperoccipital carina: absent. Macrosculpture of posterior vertex: absent. Microsculpture on posterior vertex along occipital carina: granulate. Anterior margin of occipital carina: crenulate. Medial part of occipital carina in dorsal view: rounded.

Mesosoma. Epomial carina: present. Macrosculpture of lateral pronotum directly anterior to netrion: finely rugulose. Netrion sulcus: complete. Pronotal suprahumeral sulcus in posterior half of pronotum: undifferentiated from sculpture of dorsal pronotum. Number of episternal foveae: 0. Subacropleural sulcus: present. Speculum: transversely strigose. Mesopleural pit: extending ventrally into dorsoventral furrow parallel to mesopleural carina. Mesopleural carina: well defined anteriorly, poorly defined to absent posteriorly. Sculpture of femoral depression: smooth. Patch of striae at posteroventral end of femoral depression: present, striae oblique to long axis of femoral depression. Setal patch at posteroventral end of femoral depression: absent. Microsculpture of anteroventral mesopleuron: present throughout. Macrosculpture of anteroventral mesopleuron: absent. Postacetabular sulcus: comprised of large cells. Mesopleural epicoxal sulcus: comprised of cells. Setation of posteroventral metapleuron: absent. Sculpture of dorsal metapleural area: absent. Posterodorsal metapleural sulcus: present as a line of foveae. Paracoxal sulcus in ventral half of metapleuron: indistinguishable from sculpture. Length of anteroventral extension of metapleuron: short, not extending to base of mesocoxa. Metapleural epicoxal sulcus: present as coarse rugae. Mesoscutal humeral sulcus: present as a simple furrow. Median mesoscutal carina: absent. Microsculpture of mesoscutum: imbricate-punctate anteriorly, becoming longitudinally imbricate-strigate posteriorly. Mesoscutal suprahumeral sulcus: comprised of cells. Length of mesoscutal suprahumeral sulcus: two-thirds the length of anterolateral edge of mesoscutum. Parapsidal line: absent. Notaulus: absent. Median protuberance on anterior margin of mesoscutellum: absent. Shape of dorsal margin of anterior lobe of axillar crescent: acute. Sculpture of anterior lobe of axillar crescent: dorsoventrally strigose. Area bound by axillar crescent: smooth. Macrosculpture of mesoscutellum: absent. Microsculpture on mesoscutellum: imbricate-punctate laterally to granulate medially. Median mesoscutellar carina: absent. Setation of posterior scutellar sulcus: present. Form of metascutellum: single row of cells. Metanotal trough: foveate, foveae occupying more than half of metanotal height. Metapostnotum: invaginated near lateral edge of metascutellum. Length of postmarginal vein: 1.1–1.2 times as long as stigmal vein. Color of legs: coxae dark brown to black, femora and tibia dark brown with yellowish tips, trochanters and tarsi yellow to pale brown. Anteroventral area of hind femora: not covered by setae. Anteromedial portion of metasomal depression: smooth.

Metasoma. Width of metasoma: about equal to width of mesosoma. Longitudinal striae on T1 posterior to basal costae: pair of longitudinal submedial carinae separate a lateral smooth area from an internal area where striate sculpture starts with basal grooves. Number of sublateral setae (on one side): 1. Setation of laterotergite 1: absent. Length of striation on T2: extending one-third the length of the tergite. Setation of T2: present in a transverse line and along lateral margin. Setation of laterotergite 2: present.

Host associations

Pentatomidae: Carpocoris sp. (Type host); Aelia rostrata Boheman; Dolycoris sp.

Link to distribution map

Material examined

Holotype, female, T. Manteroi: Italy: Liguria, Genoa, 9.VIII.1997, G. Mantero, MCSN 0013 (deposited in MCSN). Paratypes: Italy: 5 females, 1 male, 1 pin with multiple specimens, UNIPA-HYM-S01327, S01328 (MCSN). Other material: (20 females, 2 males, 1 pin with multiple specimens) Armenia: 3 females, 1 pin with multiple specimens, USNMENT00979995, 00979997 (ZIN). Iran: 4 females, USNMENT01223224–01223227 (MCSN). Italy: 13 females, 2 males, DISAFA-draw1465-HYM-0424–0438 (DISAFA).

Trissolcus semistriatus (Nees von Esenbeck)

Figures 7, 11, 15, 19, 25, 29, 32, 36, 40, 44, 59, 60.

Teleas semistriatus Nees von Esenbeck, 1834: 290 (original description); Ratzeburg 1852: 182 (description); Johnson 1992: 519 (cataloged).

Telenomus semistriatus (Nees von Esenbeck): Thomson 1860: 171 (description, generic transfer); Mayr 1879: 699, 701, 704 (description, synonymy, keyed).

Asolcus nigripedius Nakagawa, 1900: 17 (original description); Watanabe 1951: 21, 25 (description, type information, keyed); Watanabe 1954: 22 (keyed).

Aphanurus Semistriatus (Nees von Esenbeck): Kieffer 1912: 74 (description, generic transfer).

Microphanurus semistriatus (Nees von Esenbeck): Kieffer 1926: 91, 97 (description, generic transfer, keyed); Nixon 1939: 131, 134 (description, keyed); Meier 1940: 80 (description, keyed); Ryakhovskii 1959: 84 (keyed).

Microphanurus alexeevi Meier, 1949: 114 (original description, not seen: reference from Kozlov (1963), synonymized with Asolcus semistriatus (Nees von Esenbeck) by Kozlov (1963)); Ryakhovskii 1959: 83 (keyed); Kozlov 1963: 295 (junior synonym of Asolcus semistriatus (Nees von Esenbeck)).

Microphanurus schtepetelnikovae Meier, 1949: 114 (original description, not seen: reference from Kozlov (1963), synonymized with Asolcus semistriatus (Nees von Esenbeck) by Kozlov (1963)); Kozlov 1963: 295 (junior synonym of Asolcus semistriatus (Nees von Esenbeck)).

Asolcus semistriatus (Nees von Esenbeck): Masner 1959: 376 (diagnosis, variation); Delucchi 1961: 44, 59 (diagnosis, taxonomic status, keyed); Kozlov 1963: 295 (synonymy); Viktorov 1964: 1013, 1020 (variation, keyed); Kochetova 1966: 558 (description of immature stages); Javahery 1968: 419 (keyed); Voegelé 1969: 150 (keyed); Szabó 1976: 176, 178 (description, neotype designation, keyed).

Microphanurus stschepetilnicovae Meier: Ryakhovskii 1959: 83 (keyed, spelling error).

Trissolcus nigripedius (Nakagawa): Masner 1964: 146 (generic transfer); Ryu and Hirashima 1984: 37, 56 (description, keyed); Johnson 1992: 633 (cataloged); He, Chen, Fan, Li, Liu, Lou, Ma, Wang, Wu, Xu, Xu & Yao 2004: 321 (description); Fabritius and Popovici 2007: 157 (host informations, distribution); Kononova 2014: 1424 (keyed); Kononova 2015: 261 (keyed); Talamas et al. 2017: 130 (junior synonym of Trissolcus semistriatus (Nees von Esenbeck), neotype designation).

Trissolcus semistriatus (Nees von Esenbeck): Safavi 1968: 416 (keyed); Kozlov 1968: 200 (keyed); Fabritius 1972: 32, 34 (keyed, host catalogue; distribution); Kozlov and Lê 1977: 512 (keyed); Kozlov 1978: 636 (description); Kozlov and Kononova 1983: 113 (description); Graham 1984: 92 (variation); Johnson 1992: 636 (cataloged, type information); Kononova 1995: 96 (keyed); Koçak and Kilinçer 2003: 302, 305 (keyed, description); Ali 2011: 10 (keyed); Ghahari et al. 2011: 597 (listed); Guz et al. 2013: 87 (description, phylogenetic relationships); Petrov 2013: 326 (keyed); Kononova 2014: 1425 (keyed); Kononova 2015: 262 (keyed); Talamas et al. 2017: 20, 25, 128 (description, keyed, synonymy, type information, distribution).

Trissolcus artus Kozlov & Lê 1977: 512, 519 (original description, keyed); Kozlov 1978: 636 (description); Kozlov and Kononova 1983: 112 (description); Johnson 1992: 622 (cataloged, type information); Kononova 1995: 96 (keyed); Kononova 2014: 1424 (keyed); Kononova 2015: 262 (keyed); Talamas et al. 2017: 128, 135 (junior synonym of Trissolcus semistriatus (Nees von Esenbeck), type information).

Diagnosis

Trissolcus semistriatus is most similar to T. belenus and T. colemani, with which it overlaps in distribution and host range. It can be separated from both by the mesoscutal humeral sulcus present as a smooth furrow (Figure 25) and the short anteroventral extension of the mesopleuron, which does not extend to the base mesocoxa (Figure 7). Additionally, the angular form of the occipital carina in dorsal view, with a short carina extending toward the median ocellus, is found only in this species (Figure 36). The anteroventral area of the hind femur that is covered by setae (Figure 29) is useful when separating T. semistriatus from T. belenus (Figure 26), T. colemani (Figure 27) and T. manteroi (Figure 28).

Description

Body length: 1.07–1.11 mm, median = 1.08 mm, SD = 0.01, n = 20. Body color: head, mesosoma, and metasoma black.

Head. FCI = 1.4; LCI = 1.9; IOS = 0.33 mm; OOL:POL:LOL = 1:12:5.4. Length of radicle: less than width of clypeus. Color of A1-A6 in female: distal A2 yellow to light brown, otherwise black. Color of A7-A11 in female: black. Number of papillary sensilla on A6: 0. Number of papillary sensilla on A7: 2. Facial striae: absent. Number of clypeal setae: 6. Shape of gena in lateral view: narrow. Genal carina: present only at base of mandible. Malar striae: absent. Sculpture of malar sulcus: weakly and densely striate. Orbital furrow: uniform in width between midpoint of eye and malar sulcus. Macrosculpture of frons directly dorsal to the antennal scrobe: coarsely rugose. Preocellar pit: present. Setation of lateral frons: sparse; moderately dense. Punctation of lateral frons: sparse. Sculpture directly ventral to preocellar pit: dorsoventrally fluted. Rugae on lateral frons: weakly developed to absent. OOL: less than one ocellar diameter. Hyperoccipital carina: absent. Macrosculpture of posterior vertex: absent. Microsculpture on posterior vertex along occipital carina: granulate. Anterior margin of occipital carina: crenulate. Medial part of occipital carina in dorsal view: angled, vertex of angle with short carina directed toward median ocellus.

Mesosoma. Epomial carina: present. Macrosculpture of lateral pronotum directly anterior to netrion: finely rugulose. Netrion sulcus: complete. Pronotal suprahumeral sulcus in posterior half of pronotum: undifferentiated from sculpture of dorsal pronotum. Number of episternal foveae: 2. Course of episternal foveae ventrally: distinctly separate from postacetabular sulcus. Course of episternal foveae dorsally: distinctly separate from mesopleural pit. Subacropleural sulcus: present. Speculum: transversely strigose. Mesopleural pit: extending ventrally into dorsoventral furrow parallel to mesopleural carina. Mesopleural carina: well defined anteriorly, poorly defined to absent posteriorly. Sculpture of femoral depression: smooth. Patch of striae at posteroventral end of femoral depression: present, striae oblique to long axis of femoral depression. Setal patch at posteroventral end of femoral depression: absent. Microsculpture of anteroventral mesopleuron: present throughout. Macrosculpture of anteroventral mesopleuron: absent. Postacetabular sulcus: comprised of large cells. Mesopleural epicoxal sulcus: comprised of cells. Setation of posteroventral metapleuron: absent. Sculpture of dorsal metapleural area: absent. Posterodorsal metapleural sulcus: present as a line of foveae. Paracoxal sulcus in ventral half of metapleuron: indistinguishable from sculpture. Length of anteroventral extension of metapleuron: short, not extending to base of mesocoxa. Metapleural epicoxal sulcus: present as coarse rugae. Mesoscutal humeral sulcus: present as a simple furrow. Median mesoscutal carina: absent. Microsculpture of mesoscutum: imbricate-punctate anteriorly, becoming longitudinally imbricate-strigate posteriorly. Mesoscutal suprahumeral sulcus: comprised of cells. Length of mesoscutal suprahumeral sulcus: two-thirds the length of anterolateral edge of mesoscutum. Parapsidal line: absent. Notaulus: absent. Median protuberance on anterior margin of mesoscutellum: absent. Shape of dorsal margin of anterior lobe of axillar crescent: acute. Sculpture of anterior lobe of axillar crescent: dorsoventrally strigose. Area bound by axillar crescent: smooth. Macrosculpture of mesoscutellum: absent. Microsculpture on mesoscutellum: imbricate-punctate laterally to smooth medially. Median mesoscutellar carina: absent. Setation of posterior scutellar sulcus: present. Form of metascutellum: single row of cells. Metanotal trough: foveate, foveae occupying more than half of metanotal height. Metapostnotum: invaginated near lateral edge of metascutellum. Length of postmarginal vein: about twice as long as stigmal vein. Color of legs: coxae dark brown to black, femora and tibia dark brown with yellowish tips, trochanters and tarsi yellow to pale brown. Anteroventral area of hind femora: covered by setae. Anteromedial portion of metasomal depression: smooth.

Metasoma. Width of metasoma: about equal to width of mesosoma. Longitudinal striae on T1 posterior to basal costae: pair of longitudinal submedial carinae separate a lateral smooth area from an internal area where striate sculpture starts with basal grooves. Number of sublateral setae (on one side): 1. Setation of laterotergite 1: absent. Length of striation on T2: extending two-thirds the length of the tergite. Setation of T2: present in a transverse line and along lateral margin. Setation of laterotergite 2: present.

Host associations

Pentatomidae: Aelia rostrata; Brachynema germarii (Kolenati); Carpocoris sp.; Dolycoris baccarum (L.); Graphosoma semipunctatum; Rhaphigaster sp.; Scutelleridae: Eurygaster maura.

Link to distribution map

Material examined

Neotype, female, Teleas semistriatus: Palearctic: no date, NHMW 0007A (deposited in NHMW). Paratype of Trissolcus artus: Russia: 1 female, USNMENT00916276 (ZIN). Neoparatype: Palearctic: 1 female, NHMW 0007B (NHMW).

Other material: (183 females, 50 males, 2 pins with multiple specimens) Iran: 11 females, HMIM-HYM-022, 038 (HMIM); USNMENT01223083–01223089 (UNIPA); USNMENT01223228–01223229 (MCSN). Italy: 189 females, 54 males, 2 pins with multiple specimen, DISAFA-draw1465-HYM-0226–0240, 0242–0423 (DISAFA); MSNG-HYM-0005–0013 (MCSN); UNIPA-HYM-S01329–01346, USNMENT01223140–01223142, 01223482 (UNIPA). Japan: 1 female, EIHU 0003 (EIHU). Morocco: 1 female, USNMENT01223143 (UNIPA). Portugal: 3 females, USNMENT00916201–00916202, 00916236 (BMNH). Sweden: 1 female, UNIPA-HYM-S01326 (BMNH). Switzerland: 1 female, DISAFA-draw1465-HYM-0241 (DISAFA).

Figures 4–7. 

EPS, metapleural epicoxal sulcus, anterolateral extension of metapleuron: 4Trissolcus belenus [DISAFA-draw1465-HYM-0009] 5T. colemani [DISAFA-draw1466-HYM-0484] 6T. manteroi [DISAFA-draw1465-HYM-0430] 7T. semistriatus [DISAFA-draw1465-HYM-0227].

Figures 8–11. 

Basiconic sensilla, indicated by arrows, in the ventral surface of female antennal clava: 8Trissolcus belenus [DISAFA-draw1465-HYM-0009] 9T. colemani [DISAFA-draw1466-HYM-0484] 10T. manteroi [DISAFA-draw1465-HYM-0430] 11T. semistriatus [DISAFA-draw1465-HYM-0227].

Figures 12–15. 

Fore wing venations: 12Trissolcus belenus [DISAFA-draw1465-0010] 13T. manteroi [DISAFA-draw1465-0430] 14T. rufiventris [USNMENT01223145] 15T. semistriatus [DISAFA-draw1465-0229].

Figures 16–19. 

Metasomal tergites: 16Trissolcus belenus [DISAFA-draw1465-HYM-0009] 17 T. colemani [DISAFA-draw1466-HYM-0484] 18T. manteroi [DISAFA-draw1465-HYM-0430] 19T. semistriatus [DISAFA-draw1465-HYM-0227].

Figures 20–25. 

Mesonotum; mshs and traces of notauli: 20Trissolcus belenus [DISAFA-draw1465-HYM-0009] 21T. belenus [DISAFA…] after treatment in potassa solution to remove setae 22T. colemani [DISAFA-draw1466-HYM-0484] 23T. colemani [DISAFA-draw1466-HYM-0483] after treatment in potassa solution to remove setae 24T. manteroi [DISAFA-draw1465-HYM-0430] 25T. semistriatus [DISAFA-draw1465-HYM-0227].

Figures 26–29. 

Hind femur: 26Trissolcus belenus [DISAFA-draw1465-HYM-0009] 27T. colemani [DISAFA-draw1466-HYM-0484] 28T. manteroi [DISAFA-draw1465-HYM-0430] 29T. semistriatus [DISAFA-draw1465-HYM-0227].

Figures 30–36. 

30–32 Laterotergite 1 30Trissolcus belenus [DISAFA-draw1465-HYM-0009] 31T. colemani [DISAFA-draw1466-HYM-0484] 32T. semistriatus [DISAFA-draw1465-HYM-0227] 33–36 Occipital carina 33Trissolcus belenus [DISAFA-draw1465-HYM-0009] 34T. colemani [DISAFA-draw1466-HYM-0484] 35T. manteroi [DISAFA-draw1465-HYM-0430] 36 T. semistriatus [DISAFA-draw1465-HYM-0227].

Figures 37–44. 

37–40 Head; malar area and gena 37Trissolcus belenus [DISAFA-draw1465-HYM-0009] 38T. colemani [DISAFA-draw1466-HYM-0484] 39T. manteroi [DISAFA-draw1465-HYM-0430] 40T. semistriatus [DISAFA-draw1465-HYM-0227] 41–44 Head in frontal view 41Trissolcus belenus [DISAFA-draw1465-HYM-0009] 42T. colemani [DISAFA-draw1466-HYM-0484] 43T. manteroi [DISAFA-draw1465-HYM-0430] 44T. semistriatus [DISAFA-draw1465-HYM-0227].

Figures 45–48. 

Holotype of Trissolcus belenus [NMINH_2018_11_49]: 45 mesoscutal humeral sulcus and laterotergite 1 in lateral view 46 body in lateral view 47 body in antero-lateral view 48 body in dorsal view.

Figures 49–51. 

Holotype of Trissolcus arminon [NMINH_2018_11_46]: 49 body in dorsal view 50 head and mesosoma in antero-lateral view 51 body in postero-lateral view.

Figures 52–55. 

Holotype of Trissolcus colemani [USNMENT00989063]: 52 body in dorsal view 53 body in lateral view 54 head in frontal view 55 head in ventral view and mesosoma in lateral view.

Figures 56–58. 

Holotype of Trissolcus manteroi [MCSN 0013]: 56 body in dorsal view 57 head in antero-lateral view 58 body in lateral view.

Figures 59, 60. 

Trissolcus semistriatus [DISAFA-draw1465-HYM-0227]: 59 body in dorsal view 60 body in lateral view.

Discussion

More than 180 years have passed between the original descriptions of T. semistriatus and T. belenus and the development of identification tools that can reliably distinguish them. This can be viewed as a glacial rate of progress, but also as an indication that modern methods can resolve long-standing taxonomic challenges. The taxonomy of Trissolcus illustrates that the examination of primary types and detailed comparison of specimens across a broad geographical range is necessary to advance the field, and that further refinement may be required even when these practices are implemented. Talamas et al. (2017) significantly advanced the taxonomy of Palearctic Trissolcus but additional analysis was needed to distill diagnostic characters from those that were treated as intraspecifically variable. Specifically, setation on the first laterotergite, the form of the mesoscutal humeral sulcus, and the length of the anteroventral extension of the metapleuron were treated as variable within T. semistriatus. Although the utility of these characters for separating T. belenus and T. colemani was not recognized, Talamas et al. (2017) did bring attention to them, as they had not yet been used in the taxonomy of Palearctic Trissolcus. Setation of the hind femora, not mentioned by Talamas et al. (2017), represents a case in which a diagnostic character was previously recognized, but incorrectly associated with a taxon name (Delucchi 1961), and is now treated as useful for identifying T. belenus. Trissolcus manteroi is a different matter, in which reexamination of the type specimen was needed for its diagnostic characters (wing venation, claval formula, absence of episternal foveae) to be correctly characterized. These features place T. manteroi closer to T. rufiventris than to T. semistriatus, T. belenus or T. colemani.

The trail of photographic evidence provided by Talamas et al. (2017) enabled junior synonyms of T. semistriatus to be rapidly redistributed among T. belenus and T. colemani once the characters that delimit these species were identified, as well as the resurrection of T. manteroi. Given that producing a natural classification is an iterative process, explicit presentation of data that underlies taxonomic decisions accelerates further refinement. This is perhaps the only means by which the various quagmires of inadequate species descriptions in Platygastroidea can be transformed into a useful classification.

The need for reliable identification can be clearly seen in examples where quality taxonomy was absent. In the early part of the 20th century, Trissolcus specimens identified as T. semistriatus or T. grandis were reared and released in Russia and Iran as classical biological contral agents against Eurygaster (Alexandrov 1947; Saakov 1903; Vaezi 1950; Vassiliev 1913; Zomorrodi 1959). Some of these authors did not indicate how they identified the species, and in any case, the characters that reliably separate these species were not established. It is only by retroactively identifying voucher specimens, if they exist, that the results of these efforts can be interpreted in a meaningful way. The presence of H. halys in Europe has created a similar situation, with the same species involved in studies of its biological control. The refined species concepts presented here are thus of immediate relevance, given that T. belenus was recorded from frozen sentinel eggs of H. halys in Europe, and was previously identified as T. semistriatus.

Finally, it should be noted that independent testing of species concepts, ideally using multiple methods, is the best means by which they can be verified or improved. This study employed such an approach, using morphology, mating studies and molecular analysis to resolve four species from the concept of T. semistriatus provided in Talamas et al. (2017). In a manner conforming with this perspective, our results have been confirmed by a concomitant study by Talamas et al. (2019), in which a phylogeny of Trissolcus based on five molecular markers retrieved T. belenus, T. colemani and T. semistriatus as distinct entities.

Acknowledgements

We are grateful to: Dr. Hege Vårdal (NHRS) for photographing a number of Thomson types: Telenomus frontalis, Telenomus nigripes, Telenomus nigrita, Telenomus ovulorum and Trissolcus grandis; Dr. Matthew Buffington (USNM, USDA/SEL) for providing supplemental images of the holotype of Telenomus colemani; Valentina Guerini for transliteration from Cyrillic to Latin alphabet of labels; David Notton (BMNH), who hosted a visit of Virgilio Caleca; Dr. Paolo Visconti, who hosted a visit of Elijah Talamas to NMID which enabled the lectotypes of T. belenus and T. arminon to be studied and photographed and Dr. Norman Johnson (The Ohio State University), for maintaining Hymenoptera Online and vSysLab and assisting with data processing. Elijah Talamas was supported in part by a cooperative agreement with Kim Hoelmer (USDA/BIIRU) and by the Florida Department of Agriculture and Consumer Services- Division of Plant Industry. This research was funded by Fondazione Cassa di Risparmio di Cuneo (project HALY-END) and Regione Piemonte (project BIOHALY).

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