Research Article |
Corresponding author: Francesco Tortorici ( francesco.tortorici@unito.it ) Academic editor: Zachary Lahey
© 2024 Francesco Tortorici, Bianca Orrù, Alexander V. Timokhov, Alexandre Bout, Marie-Claude Bon, Luciana Tavella, Elijah J. Talamas.
This is an open access article distributed under the terms of the CC0 Public Domain Dedication.
Citation:
Tortorici F, Orrù B, Timokhov AV, Bout A, Bon M-C, Tavella L, Talamas EJ (2024) Telenomus Haliday (Hymenoptera, Scelionidae) parasitizing Pentatomidae (Hemiptera) in the Palearctic region. Journal of Hymenoptera Research 97: 591-620. https://doi.org/10.3897/jhr.97.127112
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In recent years, the collection of eggs of stink bugs (Pentatomidae) has intensified because of the attention given to egg parasitoids in classical biological control strategies against Halyomorpha halys (Stål) in Europe. Several specimens belonging to the genus Telenomus Haliday emerged from field-collected pentatomid eggs. Taxonomic knowledge to date has not been sufficient to enable the research community to identify these specimens to species level. Three species of scelionid wasps (Scelionidae) associated with Pentatomidae, Telenomus gifuensis Ashmead, Telenomus truncatus (Nees von Esenbeck) and Telenomus turesis Walker, have been characterized on a morphological basis. A COI barcode analysis confirmed the genetic distance between the latter two species. An identification key to the three Telenomus species occurring in the Palearctic region associated with stink bugs is provided. Telenomus heydeni Mayr is here considered conspecific with Telenomus truncatus (Nees von Esenbeck).
Biological control, DNA barcoding, identification key, Platygastroidea, species description, taxonomy
The subfamily Telenominae (Hymenoptera, Scelionidae), particularly the genera Trissolcus Ashmead and Telenomus Haliday, have been studied, in part, because of their potential as biological control agents (BCAs) of economically important pests. Species of Trissolcus parasitize eggs of stink bugs (Pentatomoidea), particularly Pentatomidae and Scutelleridae, and a few are phoretic on leaf-footed bugs (Coreidae) (
Telenomus is by far the largest genus in the subfamily and includes a considerable number of species that cannot be reliably identified. This taxonomic challenge has its roots in the diversity and size of the genus, and in what
The taxonomy of Telenomus in the western Palearctic received little attention in the 21st century until the arrival of the brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera, Pentatomidae). The pestiferous nature of this stink bug and the potential risk of dispersal to other countries (
Trissolcus japonicus (Ashmead) and Tr. mitsukurii (Ashmead) (Hymenoptera, Scelionidae) have been shown in Europe to be the most promising BCAs of H. halys in terms of habitat suitability (
In Europe, some authors have reported Te. chloropus (Thomson) from their surveys (
Our work includes examination of historical type specimens, some of which are nearly 200 years old, which is essential for resolving long-standing ambiguity. An updated morphological diagnosis section provides previously unexplored or unused character systems, and we provide simplified descriptions that focus on diagnostic characters. As other Old-World species of the Te. podisi group are treated taxonomically, these descriptions are likely to expand to include characters used for the species group more broadly. We complement our analysis with molecular data that is helpful for establishing which characters are prone to interspecific variation and which are diagnostically stable. For the analyzed species, we provide host associations and biological observations.
The earliest species, described by
Telenomus specimens were reared from naturally laid egg masses (Pentatomidae and Scutelleridae) collected in different sites in Piedmont, Italy, from 2019 to 2022 during surveys to investigate the egg parasitoid populations of native and exotic bugs. Each egg mass was isolated in a plastic Petri dish (6 cm diameter) and reared in a climate-controlled chamber at 24 ± 1 °C, 65 ± 5% r.h., and L16:D8 photoperiod. All egg masses were examined under a stereomicroscope and identified to the species or family level according to
Telenomus specimens were also reared from egg masses of Palomena prasina (Linnaeus) (Hemiptera, Pentatomidae) or collected by sweeping in their natural habitats in Moscow Province, Russia, in 2016 for a cytogenetic study (
A Wild M5 steromicroscope with 15× oculars and a spotlight were used for biometric diagnosis. Slides were mounted with Eukitt mounting medium (Merck Life Science, Milan, Italy) and examined under a Leitz Dialux 20 EB compound microscope. Male genitalia were prepared by following the protocol of
Images of primary type specimens were taken with a Macropod imaging system using 10× and 20× Mitutoyo objective lenses (Mitutoyo Corporation, Kawasaki, Japan) and rendered with Helicon Focus (HeliconSoft Limit., Kharkiv, Ukraine). Photographs of non-type specimens were taken using a Canon 90D camera (Canon Inc., Tokyo, Japan) equipped with an extension tube; 5×, 10×, 20×, and 50× LWD microscope lenses mounted on a macro-rail and illuminated with two speedlight flashes. The frames were merged with Zerene Stacker (PMax algorithm, Zerene Systems LLC, Richland, WA, USA).
The ultrastructures of non-type specimens were examined under a Jeol JSM-6380 scanning electron microscope (SEM) after critical point drying (Hitachi HCP-2) of the specimens and sputter coating with gold (Giko JSM-6380).
DNA extraction, amplification, and sequencing were performed at multiple institutions. At the Florida State Collection of Arthropods (
The sequences were compared with the GenBank database using the Basic Local Alignment Search Tool (http://www.ncbi.nlm.nih.gov/BLASTn). All sequences obtained from this study are deposited in GenBank or BOLD (
Geographic records of specimens used for molecular and morphological analysis were retrieved from GPS latitude and longitude coordinates and from available data on the GenBank and BOLD dataset as obtained above. A distribution map was created using QGIS.org (2023).
DISAFA Dipartimento di Scienze Agrarie, Forestali e Alimentari, University of Torino, Torino, Italy
INRAE INRAE UMR Institut Sophia Agrobiotech, Sophia-Antipolis, France
The data for the examined specimens were uploaded onto the BOLD platform (www.barcodinglife.org), and the list of material examined was generated as a supplementary spreadsheet file (Suppl. material
Two species were detected in our surveys, Te. truncatus and Te. turesis, which we identified by comparison to type material (Table
Images of primary type | Original combination | Valid name |
---|---|---|
https://zenodo.org/record/7846207 | Teleas truncatus Nees von Esenbeck | Telenomus truncatus (Nees von Esenbeck) |
https://zenodo.org/record/7622511 | Teleas Linnei Nees von Esenbeck | Telenomus truncatus (Nees von Esenbeck) |
https://zenodo.org/record/7846277 | Telenomus Turesis Walker | Telenomus turesis Walker |
https://www.flickr.com/photos/127240649@N08/50121706058/in/photostream/ | Phanurus chloropus Thomson | Telenomus turesis Walker |
https://zenodo.org/record/7442921 | Telenomus heydeni Mayr | Telenomus truncatus (Nees von Esenbeck) |
https://zenodo.org/record/7443068 | Telenomus Sokolowi Mayr | Telenomus turesis Walker |
According to
The present study reports a similar composition of hosts for Te. truncatus and Te. turesis as reported by previous authors (
Host associations. “X” indicates an association recorded during the present study.
Stink bugs species | Telenomus turesis | Te. truncatus | |
---|---|---|---|
Pentatomidae | Acrosternum sp. | X | |
Aelia acuminata (L.) | ( |
||
Aelia furcula Fieber | ( |
||
Aelia rostrata Boheman | ( |
||
Arma custos (F.) | X | ||
Carpocoris sp. | X | X | |
Carpocoris fuscispinus (Boheman) | ( |
||
Dolycoris baccarum (L.) | ( |
X | |
Graphosoma lineatum (L.) | ( |
X | |
Halyomorpha halys (Stål) | X | X | |
Holcostethus strictus (F.) | X | ||
Palomena prasina (L.) | ( |
( |
|
Palomena viridissima (Poda) | ( |
( |
|
Picromerus bidens (L.) | ( |
( |
|
Piezodorus lituratus (F.) | ( |
( |
|
Rhaphigaster nebulosa (Poda) | ( |
||
Scutelleridae | Eurygaster austriaca (Schrank) | ( |
|
Eurygaster integriceps Puton | ( |
( |
|
Eurygaster maura (L.) | ( |
||
Eurygaster testudinaria (Geoffroy) | ( |
We identified specimens of Te. truncatus and Te. turesis based on characters in the following species treatments:
Teleas truncatus
Nees von Esenbeck, 1834: 289 (original description);
Teleas Linnei
Nees von Esenbeck, 1834: 288 (original description);
Teleas
Zetterstedtii
Telenomus truncatus
(Nees von Esenbeck):
Telenomus Heydeni Mayr, 1879: 702, 706 (original description, keyed). syn. nov.
Telenomus Giraudi Kieffer, 1906: 163 (original description).
Prophanurus Giraudi
Kieffer:
Prophanurus Heydeni
(Mayr):
Prophanurus Truncatus (Nees von Esenbeck):
Telenomus giraudi
Kieffer:
Telenomus heydeni
Mayr:
Telenomus (Telenomus) heydeni
Mayr:
Teleas linnei
Nees von Esenbeck:
Female. Head: compound eye with sparse and short setation throughout (Figs
Mesosoma
: mesoscutal humeral sulcus (mshs) present as a smooth furrow (Figs
Metasoma
: first metasomal tergite with one or rarely two pairs of sublateral setae (ss) (Figs
Male. Head: antennal length ratio A3:A2 = 1.2:1 (n=20), antennomeres A6–A11 bead-like, subequal (Fig.
From the analysis of the lectotype of Te. heydeni (
Host species associated: Table
Barcode sequences were obtained from 49 specimens of Te. truncatus. Pairwise distance values within species are shown in Suppl. material
Suppl. material
Suppl. material
Telenomus Turesis Walker, 1836: 353 (original description).
Phanurus chloropus Thomson, 1861: 173 (original description).
Telenomus turesis
Walker:
Telenomus Sokolowi
Mayr, 1897: 442 (original description);
Telenomus Mayri Sokolov, 1904: 29 (original description).
Aphanurus Turesis
(Walker):
Prophanurus Sokolowi
(Mayr):
Microphanurus turesis
(Walker):
Telenomus chloropus
(Thomson):
Telenomus sokolowi
Mayr:
Telenomus tischleri
Nixon, 1939: 129 (original description);
Telenomus sokolovi
Mayr:
Telenomus mayri
Sokolov:
Trissolcus turesis
(Walker):
Telenomus (Telenomus) chloropus
(Thomson):
Female. Head: dense setation on compound eyes (Figs
Mesosoma
: mesoscutal humeral sulcus (mshs) indicated by cells (Figs
Metasoma
: first metasomal tergite with one or rarely two pairs of sublateral setae (ss) (Figs
Male. Antennal length ratio A3:A2 = 2:1 (n=20), antennomeres A6–A11 elongate, uniform in length (Fig.
Barcode sequences were obtained from 46 specimens of Te. turesis. Pairwise distance values within species are shown in Suppl. material
The analysis of COI sequences discovered that Te. turesis includes samples KY843528 (
Suppl. material
Suppl. material
The distance between the inner margin of the compound eyes is smaller than the width of the compound eyes in frontal view (Fig.
Telenomus gifuensis. Female paralectotype (USNMENT01109267): head in frontal view (A); female lectotype (USNMENT01109265): habitus in lateral view (B); female paralectotype (USNMENT01109266): habitus in dorsal view (C). Scale bars: 0.2 mm.
Suppl. material
1 | Metasomal tergite 1 with two pairs of sublateral setae (Fig. |
Telenomus gifuensis Ashmead |
– | Metasomal tergite 1 with one pair of sublateral setae (Fig. |
2 |
2 | Female | 3 |
– | Male | 4 |
3 | Compound eyes with sparse, short setation throughout (Figs |
Telenomus truncatus (Nees von Esenbeck) |
– | Compound eyes with dense setation throughout (Figs |
Telenomus turesis Walker |
4 | Compound eyes with sparse and short setation throughout (Fig. |
Telenomus truncatus (Nees von Esenbeck) |
– | Compound eyes with dense setation throughout (Fig. |
Telenomus turesis Walker |
The analysis involved 105 nucleotide sequences. All positions with less than 95% site coverage were eliminated, i.e., fewer than 5% alignment gaps, missing data, and ambiguous bases were allowed at any position (partial deletion option). There was a total of 492 positions in the final dataset. Barcode sequences were obtained from 95 Telenomus specimens (Suppl. material
In recent years, researchers have limited the identification of Telenomus to genus level or grouped all of the specimens, referring only to Te. chloropus when they emerged from eggs of pentatomids in western Palearctic region. Despite the setbacks of these misidentifications, the taxonomy of Palearctic species of Telenomus associated with stink bugs has advanced, and we here provide a more solid foundation for continued research. For the first time, the West Palearctic species of the Te. podisi species group associated with the Pentatomidae can be reliably identified, with diagnostic tools based on multiple lines of evidence. The logical next test of our species concepts would be interbreeding studies, as were performed for cryptic species of the genus Trissolcus (
This study was carried out within the Agritech National Research Center and received funding from the European Union Next-GenerationEU (PIANO NAZIONALE DI RIPRESA E RESILIENZA (PNRR) – MISSIONE 4 COMPONENTE 2, INVESTIMENTO 1.4 – D.D. 1032 17/06/2022, CN00000022). This manuscript reflects only the authors’ views and opinions; neither the European Union nor the European Commission can be considered responsible for them. Elijah Talamas was supported by the Florida Department of Agriculture and Consumer Services, Division of Plant Industry. Some of the sequence data were produced by Matthew R. Moore, Cheryl G. Roberts and Lynn A. Combee at the Molecular Diagnostics Laboratory (FDACS/DPI). We are very thankful to the colleagues from the Interdepartmental Laboratory of Electron Microscopy (Faculty of Biology, Lomonosov Moscow State University) for the provided facilities and help during electron microscopic studies.
We are also grateful to Silvia Teresa Moraglio, Paolo Navone, and Sara Scovero for collecting specimens used in our analyses.
Phylogeny reconstruction of COI of Telenomus truncatus and Te. turesis
Data type: tif
Explanation note: The tree of life was inferred by using the Maximum Likelihood method and Tamura-Nei model with an interior branch test and 1000 bootstrap replications. The percentage of trees in which the associated taxa clustered together is shown next to the branches. This analysis involved 97 nucleotide sequences. There was a total of 492 positions in the final dataset. Star (*) indicates sequences mined from online datasets.
Distribution map
Data type: tif
Explanation note: Distribution map indicating the points for Telenomus truncatus (blue spots) and for Te. turesis (red spots) retrieved from material examined and from BOLD barcodes.
Estimates of Evolutionary Divergence between Sequences
Data type: xlsx
Explanation note: The number of base substitutions per site from between sequences are shown. Analyses were conducted using the Maximum Composite Likelihood model (Tamura and Kumar 2004). The rate variation among sites was modeled with a gamma distribution (shape parameter = 1). This analysis involved 105 nucleotide sequences. All ambiguous positions were removed for each sequence pair (pairwise deletion option). There were a total of 861 positions in the final dataset. Evolutionary analyses were conducted in MEGA X (
List of the specimens examined
Data type: xlsx
Explanation note: Images and sequence data for species of Telenomus that are classified in the podisi species group (sensu Johnson 1984).