Research Article |
Corresponding author: Elijah J. Talamas ( elijah.talamas@fdacs.gov ) Academic editor: Zachary Lahey
© 2021 Fateme Ranjbar, M. Amin Jalali, Mahdi Ziaaddini, Zahra Gholamalizade, Elijah J. Talamas.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Ranjbar F, Jalali MA, Ziaaddini M, Gholamalizade Z, Talamas EJ (2021) Stink bug egg parasitoids (Hymenoptera, Scelionidae) associated with pistachio in Iran and description of a new species: Trissolcus darreh Talamas. In: Lahey Z, Talamas E (Eds) Advances in the Systematics of Platygastroidea III. Journal of Hymenoptera Research 87: 291-308. https://doi.org/10.3897/jhr.87.72838
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Surveys for egg-parasitoid wasps were conducted in Rafsanjan, Iran, on two species of Pentatomidae (Hemiptera) found in pistachio orchards, Acrosternum arabicum Wagner and Brachynema signatum Jakovlev. Five species of Scelionidae (Platygastroidea) were recovered, including one that is here described as new: Psix saccharicola (Mani), Trissolcus colemani (Crawford), T. darreh Talamas sp. nov., T. perepelovi (Kozlov), and T. semistriatus (Nees). In addition to describing a new species, we report new host associations, provide COI barcodes for four of these species, and discuss host-related intraspecific variation in T. darreh and T. perepelovi.
Trissolcus, biological control, Platygastroidea
Pistachio nuts, Pistacia vera L., comprise one of the most important and valuable crops cultivated in Mediterranean countries (Greece, Turkey, Spain, Italy, and Tunisia), the Middle East (Syria and Iran), Australia and the southwestern United States (Arizona and California) (
The damage of stink bugs according to the pistachio fruit phenology is divided into two stages. The first, epicarp lesion, occurs early in the season when the nuts are small, prior to shell hardening. The second, kernel necrosis, occurs during kernel development between complete shell hardening and complete ripening of the kernel. At this stage, stink bugs act as the vector of Nematospora coryli Kurtzman (Saccharomycetales: Saccharomycetaceae), the causal agent of stigmatomycosis which can cause serious damage to the pistachio yield during outbreaks of pentatomid bug populations (
Parasitoids are the most dominant natural enemies due to their high rates of parasitism and diversity and have great potential for control of pentatomid populations (
The goal of this study is to investigate the scelionid fauna associated with stink bug eggs in pistachio orchards and better support future control of these pests. Although not the first such study, it is the first since Palearctic Trissolcus was revised by
The initial populations of Acrosternum arabicum and Brachynema signatum (adults and eggs) were collected from pistachio plantation areas around Rafsanjan (30°42'2"N and 55°53'51"E) (2016–2018) and transferred to a climate-controlled room (27±1°C, L:D 16:8, and 65±5% RH). The stink bugs were kept in ventilated plastic boxes (13 × 20 × 30 cm) and were reared on an alternative diet, Phaseolus vulgaris L. (pods of green bean) for A. arabicum and Kali turgidum (Dumort.) Guterm. (Amaranthaceae), a common weed in pistachio orchards, for B. signatum. Female adult individuals were provided with paper towels as ovipositional substrates. Plastic boxes were checked daily, and egg masses were collected and used to maintain the colony and for collecting and rearing egg parasitoids. Furthermore, every two days, the boxes were cleaned and food was replaced (
Sentinel egg masses were used to collect parasitoid wasps. For this purpose, more than 50 egg masses of A. arabicum and B. signatum (<1 h old) were glued on yellow cards (7 × 7 cm) then were attached at different heights in pistachio trees in various locations in the orchard (
DNA extraction, PCR and sequencing were conducted at the Florida State Collection of Arthropods, Gainesville, Florida, USA, as outlined in
eps episternal foveae (Figures
hoc hyperoccipital carina (Figure
mshs mesoscutal humeral sulcus (Figure
nes netrion sulcus (Figure
of orbital furrow (Figures
The COI barcoding region was amplified and sequenced from three parasitoid species retrieved in this study (Table
Species | Collecting Unit Identifier (CUID) | Genbank accession |
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Psix saccharicola | DPI_FSCA 00009835 | MZ715050 |
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MZ715051 | |
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MZ715052 | |
Trissolcus darreh |
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Suppl. material |
Trissolcus semistriatus | DPI_FSCA 00009834 | MZ715053 |
Trissolcus perepelovi | DPI_FSCA 00009837 | MZ715054 |
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MZ715055 |
List of specimens photographed. Full resolution images are deposited at mbd-db.osu.edu and can be retrieved via the CUID.
Species | CUID |
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Psix saccharicola |
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Trissolcus colemani |
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Trissolcus darreh |
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Trissolcus perepelovi |
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Trissolcus semistriatus |
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Psix saccharicola was identified by the dark brown radicle and more brightly colored scape, metascutellum (dorsellum) with ventral lip smooth, frons without submedian carina, apex of T2 smooth, acetabular field glabrous, and S2 sulci nearly continuous posteriorly.
Rafsanjan, Kerman Prov., Iran, 2019, reared from eggs of Acrosternum arabicum, 15 females, 14 males:
Psix saccharicola has also been reported to parasitize the eggs of Acrosternum breviceps and Brachynema germari (
Trissolcus colemani was identified using characters presented in
Rafsanjan, Kerman Prov., Iran, 2019, reared from eggs of Brachynema signatum; 6 females:
Female body length: 0.93–1.17 mm (n = 24). Male body length: 0.92–1.02 mm (n = 6).
Antenna. Color of radicle: yellow. Length of radicle: less than width of clypeus. Color of A1–A6 in female: variably yellow to brown. Color of A7–A11 in female: brown to black. Claval formula: 1-2-2-2-2.
Head. Facial striae: absent. Number of clypeal setae: 2. Shape of gena in lateral view: narrow. Genal carina: absent. Malar striae: absent. Sculpture of malar sulcus: unknown. Orbital furrow: constricted or poorly defined ventrally. Macrosculpture directly dorsal to the antennal scrobe: absent. Preocellar pit: present. Setation of lateral frons: moderately dense. Punctation of lateral frons: absent. Sculpture directly ventral to preocellar pit: smooth. Rugae on lateral frons: absent. OOL: less than one ocellar diameter. Hyperoccipital carina: present, weakened medially. Macrosculpture of posterior vertex: absent. Microsculpture on posterior vertex along occipital carina: coriaceous. 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: incomplete, not well-defined dorsally. Pronotal suprahumeral sulcus in posterior half of pronotum: undifferentiated from sculpture of dorsal pronotum. Number of episternal foveae: 0; 1; 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; smooth. Mesopleural pit: extending ventrally into slender, shallow furrow. Mesopleural carina: absent. Sculpture of femoral depression: smooth. Patch of striae at posteroventral end of femoral depression: absent; indicated by lines of microsculpture. Setal patch at posteroventral end of femoral depression: present as a line of setae. Microsculpture of anteroventral mesopleuron: present only on anterior face of mesopleuron bulge. Macrosculpture of anteroventral mesopleuron: absent. Postacetabular sulcus: comprised of small crenulae. Mesopleural epicoxal sulcus: present as a smooth furrow. 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: absent. Length of anteroventral extension of metapleuron: short, not extending to base of mesocoxa. Apex of anteroventral extension of metapleuron: acute. Metapleural epicoxal sulcus: present as coarse rugae. Mesoscutal humeral sulcus: present as a simple furrow. Median mesoscutal carina: absent. Microsculpture of mesoscutum: granular throughout. Mesoscutal suprahumeral sulcus: comprised of foveae. Length of mesoscutal suprahumeral sulcus: two-thirds the length of anterolateral edge of mesoscutum. Parapsidal line: present. Notaulus: present. Median protuberance on anterior margin of mesoscutellum: absent. Shape of dorsal margin of anterior lobe of axillar crescent: unknown. Sculpture of anterior lobe of axillar crescent: dorsoventrally strigose. Area bound by axillar crescent: smooth. Macrosculpture of mesoscutellum: absent. Microsculpture on mesoscutellum: unknown. Median mesoscutellar carina: absent. Setation of posterior scutellar sulcus: present. Form of metascutellum: single row of foveae along anterior margin, rugulose posteriorly. Metanotal trough: foveate, foveae occupying less than half of metanotal height. Metapostnotum: invaginated near lateral edge of metascutellum. Anteromedial portion of metasomal depression: smooth.
Wings. Length of postmarginal vein: about 1.5 times as long as stigmal vein. Color of setae on fore wing: white throughout, brown at distal end.
Legs. Color of legs: coxae and femora dark brown to black, otherwise pale brown to yellow. Anteroventral area of hind femora: not covered by setae.
Metasoma. Width of metasoma: about equal to width of mesosoma. Number of sublateral setae (on one side): 0. Setation of laterotergite 1: absent. Length of striation on T2: extending two-thirds the length of the tergite. Setation of T2: present only in posterolateral corner. Setation of laterotergite 2: present.
Rafsanjan, Kerman Prov., Iran, 2019; Holotype female (
In the specimens reared from B. signatum, the mesopleuron directly ventral to the femoral depression projects more sharply than in the specimens reared from A. arabicum. However, because we have only three females and one male reared from B. signatum, more specimens are needed to confirm that this difference is host related. Other characters with notable variation are the orbital furrow, the hyperoccipital carina, the color of setae on the fore wing and subtle differences in the episternal foveae. In females, the orbital furrow tends to become constricted ventrally, but in some specimens the medial edge of the furrow is not defined where it intersects the malar sulcus. This condition was typical for the small number of males that we examined. The hyperoccipital carina is medially weakened in all specimens and in some it is essentially absent between the lateral ocelli. Variation in the color of the wing setae can be difficult to assess without slide-mounting the wings because the perception of the color is influenced by what is behind the wing, and the color difference is subtle. However, it should still be noted that setae at the apex of the fore wing appear to vary from pale to medium brown. The episternal foveae in T. darreh are shallow and may be irregular in shape. In most specimens, there is a single fovea, but occasionally there are two. Rarely, and usually in males, no foveae are visible.
Trissolcus darreh arrives at couplet 16 in the key to Trissolcus species of the Palearctic region by
Multiple attempts were made to amplify COI from specimens of T. darreh and from one specimen we were able to produce a faint band with LepF1/LepR1 primers. Sequencing produced a quality read in only in the forward direction, precluding us from uploading it to GenBank, which requires bidirectional sequencing. This sequence is unique in BOLD and GenBank. The closest match in GenBank is to Trissolcus euschisti (Ashmead) (MG939339.1, 84% sequence identity). In BOLD, the best matches are all ~89.5% to BINs BOLD:AAZ3289 (Telenomus Haliday), BOLD:ACB8142 (Trissolcus), and BOLD:ACB8142 (Phanuromyia Dodd). Identification of the latter two BINs was made based on images provided in BOLD. A FASTA file of this sequence is provided in Suppl. material
Trissolcus perepelovi was identified using the key of
Rafsanjan, Kerman Prov., Iran, 2019, reared from eggs of Acrosternum arabicum and Brachynema signatum, 85 females, 41 males:
Among the specimens analyzed here, we found that there is more variation in the microsculpture of the frons (Figures
In this study, T. perepelovi was reared from the eggs of Acrosternum arabicum and Brachynema germari. It was previously reported by
Trissolcus semistriatus was identified using diagnostic characters presented in
Rafsanjan, Kerman Prov., Iran, 2019, reared from eggs of Acrosternum arabicum, 13 females, 13 males: DPI_FSCA 00009834;
This study is the first to document scelionid parasitoids associated with stink bug eggs in pistachio orchards since the taxonomy of Palearctic Trissolcus was treated by
Names of Trissolcus species used on previous studies and their current status.
Names used in |
Valid name | Most recent taxonomic treatment |
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T. agriope (Kozlov & Lê) | T. agriope (Kozlov & Lê) | Kozlov and Kononova (1983) |
T. delucchii Kozlov | T. tumidus (Mayr) |
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T. deserticola (Kozlov) | T. perepelovi (Kozlov) |
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T. mitsukurii (Ashmead) | T. mitsukurii (Ashmead) |
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T. niceppe (Kozlov & Lê) | T. oobius (Kozlov) |
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T. oobius (Kozlov) | T. oobius (Kozlov) |
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T. semistriatus (Nees) | T. semistriatus (Nees) |
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T. volgensis (Viktorov) | T. scutellaris (Thomson) |
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Given the amount of attention that Palearctic Trissolcus has received during recent years, it is somewhat surprising that the region contains a previously undescribed species. This discovery emphasizes the importance of continuous collaboration between those conducting field and laboratory studies, as each provides the other with the necessary specimens and data to maximize effectiveness.
We are grateful to Vali-e-Asr University of Rafsanjan, Iran, for financial support to Fateme Ranjbar (PhD student no. 95368001). Elijah Talamas was supported by the Florida Department of Agriculture and Consumer Services-Division of Plant Industry (FDACS-DPI). We are grateful to Jonathan Bremer, Matthew Moore, Cheryl Roberts, and Lynn Combee (FDACS-DPI) for contributing images and generating molecular data.
FASTA file
Data type: molecular data