Research Article |
Corresponding author: Guang-Hong Liang ( guanghong.liang@fafu.edu.cn ) Academic editor: Miles Zhang
© 2024 Hua-Yan Chen, Elijah Talamas, Zachary Lahey, Norman F. Johnson, Ci-Ding Lu, Guang-Hong Liang.
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:
Chen H-Y, Talamas E, Lahey Z, Johnson NF, Lu C-D, Liang G-H (2024) Telenomus dendrolimi (Matsumura) (Hymenoptera, Scelionidae) reared from the eggs of Dendrolimus houi (Lajonquiere) (Lepidoptera, Lasiocampidae) from China. Journal of Hymenoptera Research 97: 1385-1402. https://doi.org/10.3897/jhr.97.139056
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The pine moth, Dendrolimus houi (Lajonquiere), is a notorious insect pest of coniferous trees in South China. A gregarious egg parasitoid in the family Scelionidae shows great potential to be mass-reared for the biological control of D. houi. This parasitoid is identified as Telenomus dendrolimi (Matsumura) based on comparison to paratype specimens of Telenomus dendrolimusi Chu, a junior synonym of T. dendrolimi. Telenomus dendrolimi is redescribed and included in a molecular analysis. In addition to parasitizing D. houi, T. dendrolimi was found to successfully parasitize six other species under laboratory conditions, with Antheraea pernyi (Guérin-Méneville) the most suitable host for mass-rearing.
Biological control, egg parasitoid, gregarious, taxonomy
The pine moth, Dendrolimus houi (Lajonquiere) (Lepidoptera, Lasiocampidae), is a notorious insect pest of several important conifers including Cryptomeria japonica var. sinensis Miquel (Cupressaceae), Cupressus funebris Endl. (Cupressaceae), Pinus yunnanensis Faranch. (Pinaceae), and Pinus kesiya Royle ex Gordon in South China, India, Myanmar, Sri Lanka, and Indonesia (
Attempts to control D. houi in China have mainly focused on chemical insecticides (
A survey for parasitoid species that attack D. houi was conducted in five provinces of China in 2021 (
Some parasitoid specimens were preserved in 100% ethanol for further morphological and molecular studies. All voucher specimens are deposited in the Insect Collection of South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China (
Abbreviations and morphological terms used in text: A1–A12: antennomere 1–12; T1–T7: metasomal tergite 1–7; S1–S7: metasomal sternite 1–7. Morphological terminology otherwise generally follows
Genomic DNA was extracted from a female and a male of T. dendrolimi, T. remus Nixon, and T. dignus (Gahan) using a TIANamp Micro DNA Kit (Tiangen Biotech (Beijing), Co., Ltd.), following an established non-destructive DNA extraction protocol (
The 28S rDNA and COI sequences from T. dendrolimi, T. remus, and T. dignus were combined with the Telenomus 28S rDNA and COI dataset of
Multifocal images of mounted specimens were made using a Nikon SMZ25 microscope with a Nikon DS-Ri 2 digital camera system and a Keyence VHX-970F imaging system. Scanning electron micrographs were produced using a JSM-6360LV scanning electron microscope (JEOL, Tokyo, Japan). Images were post-processed with Adobe Photoshop CS6 Extended.
Telenomus dendrolimi is a gregarious species, with more than one wasp emerging from a single egg of D. houi. Under laboratory conditions, it successfully parasitized two species of Lasiocampidae: D. kikuchii and D. punctatus; and four species of Saturniidae: A. sinensis, A. pernyi, C. japonica, and E. pyretorum. Similarly, more than one wasp emerged from a single host egg, indicating gregarious behavior for all of these hosts. Among the six alternative host species, A. pernyi was the most promising for mass-rearing of T. dendrolimi, with up to 20 wasps (female to male ratio was about 4:1) emerging per egg. Related biological parameters are under investigation and will be reported in future studies.
Six Telenomus specimens belonging to three species were subjected to non-destructive DNA extraction followed by amplification and sequencing of the D2 and D3 regions of the 28S rDNA and the barcode region of COI. Multiple sequence alignments for 28S and COI were 1,134 and 845 characters (nt + gaps), respectively. In the COI single gene (Suppl. material
Holcaerus (?) dendrolimi Matsumura, 1925: 44 (original description).
Telenomus dendrolimi
(Matsumura):
Telenomus (Aholcus) dendrolimi
(Matsumura):
Telenomus dendrolimusi
Chu, 1937: 60 (original description);
Telenomus (Aholcus) dendrolimusi
Chu:
Female body length: 1.07–1.21 mm (n = 10). Male body length 0.8–1.0 mm (n = 8).
Color: female body entirely black; antenna dark brown to black, with ventral side paler; coxae and femora of all legs dark brown to black, remainders of legs brown to yellow, with distal tarsomere darker; wings hyaline. Male similar to female, but antenna brown to dark brown, tibiae and tarsi of all legs paler.
Head. Female antenna 10-merous; claval formula 1-2-2-2; A2 distinctly longer than wide, A3 and A10 slightly longer than wide, A4 as long as wide, A5–A9 wider than long.
Male antenna 12-merous; A2 slightly longer than wide; A4 and A5, slightly dilated, but A5 modified, with tyloid projecting anteriorly; A6–A11 transverse; A12 1.60 × as long as wide.
Mandible with 3 teeth; clypeus with 4 setae; labrum, medially pointed, flanked by arched concavities; interantennal process present; frons coriaceous, becoming smooth around toruli and malar sulcus; frontal depression indicated by area of effaced microsculpture; gena coriaceous behind eye, becoming smooth ventrally and above occipital carina; eyes setose; vertex smoothly rounded onto occiput, without hyperoccipital carina; vertex coriaceous, becoming smooth above occipital carina; occiput entirely smooth; occipital carina present, higher and weaker medially, ventrally extending to posterior articulation of the mandible.
Mesosoma. Pronotum: pronotal cervical sulcus present as a smooth furrow; netrion smooth; netrion sulcus complete and distinct.
Mesonotum : mesoscutum evenly rounded in lateral view, with reticulate miscrosculpture except smooth narrow area along mesoscutal humeral sulcus; mesoscutal suprahumeral sulcus absent; mesoscutal humeral sulcus indicated by a mostly smooth furrow; mesoscutellum smooth, sparsely setose; axilla smooth, setae present; scutoscutellar sulcus more or less smooth medially, foveate laterally; posterior mesoscutellar sulcus foveate.
Metanotum : metascutellum rugose, slightly protruding posteriorly; metascutellar carina present; metanotal trough smooth.
Propodeum : metapostnotum medially tapering to a slender point, creating a gap between posterior margin of metanotum and anterior margin of propodeum; lateral propodeal carina present, fusing with metapleural carina to form perimeter of metasomal depression; metasomal depression mostly smooth, with short rugae radiating from propodeal foramen.
Mesopleuron : acropleural sulcus present, continuous with prespecular sulcus, forming a furrow extending ventrally to mesopleural pit; speculum weakly rugose; mesepimeral sulcus complete, foveate; mesopleural pit deep, slightly transverse; ventral mesopleuron smooth; episternal foveae absent; postacetabular patch clearly indicated, without setae; acetabular carina present; postacetabular sulcus indicated by a smooth furrow; length of intercoxal space longer than fore coxae; mesopleural epicoxal sulcus indicated by shallow foveae.
Metapleuron : Metapleural carina interrupted by propodeal spiracle; dorsal metapleural area smooth; ventral metapleural area weakly rugose along anterior and posterior margins; metapleural pit present; metapleural sulcus indicated as a weak, shallow groove posterior to the metapleural pit; metapleural epicoxal sulcus indicated by crenulae.
Combined 28S and COI maximum likelihood phylogenetic analysis of Telenomus using a modified dataset of
Wings. Length of postmarginal vein about twice as long as stigmal vein. Fore wing apex reaching beyond T6.
Metasoma. T1 with 1 pair of sublateral setae, 2 pairs of lateral setae; foveae along anterior T1 distinct, elongate; foveae along anterior T2 distinct, with short costae extending less than ¼ the length of T2; T2 with sparse setae on lateral part of mediotergite and dorsomedial part of laterotergite; T3–T6 with a transverse line of long setae, setae absent along midline; laterotergites 3–6 glabrous; foveae along anterior S1 distinct, with costae extending to mid-length; foveae along anterior S2 distinct, with short costae extending less than ¼ the length of S2; S2 felt field indicated by coriaceous sculpture and setal patch; sparse setation present in posteromedial portion of S2; S3–S5 with a transverse line of long setae, setae absent along midline; S6 setose laterally, without setae along midline.
Male genitalia. Length of aedeagal lobe about 0.3 × length of aedeago-volsellar shaft, distally pointed; digiti large, about half maximum length of aedeagal lobe, with 3 digital teeth, basal ring about 0.4 × length of aedeago-volsellar shaft.
Telenomus californicus-complex (Johnson 1984).
Telenomus dendrolimi was reared from field-laid eggs of D. houi and D. punctatus in China, and Dendrolimus spectabilis Butler in Japan. Under laboratory conditions, its alternative hosts include D. kikuchii and D. punctatus, A. sinensis, A. pernyi, C. japonica, and E. pyretorum.
Allotype of Telenomus dendrolimusi Chu, 1937, • male: China: Tangki (Tangxi), Chekiang (Zhejiang), ex. eggs of Dendrolimus punctatus Walker, 11.VI.1934, Joo-Tso Chu (deposited in Zhejiang University). Paratype of Telenomus dendrolimusi Chu, 1937, China • 1 female, same data as allotype • 1 female, same data except collected on 22.VI.1933 (deposited in Zhejiang University). Other material • 2 females 1 male, Japan: (Kyushu) Hakozaki Fukuoka Jul. 31, 1959 Col. Y. Hirose, host: Egg of Dendrolimus spectabilis Butler, OSUC 71700-702 (deposited in OSUC) • 6 females 6 males, China: Fujian, Xiapu County, 26°49'45.76"N, 119°57'55.3"E, ex. eggs of Dendrolimus houi (Lajonquiere) feeding on Cryptomeria japonica var. sinensis Miquel trees, 10.IX.2021, Guang-hong Liang,
China (Liaoning, Hebei, Shandong, Henan, Jiangsu, Anhui, Fujian, Zhejiang, Jiangxi, Hubei, Hunan, Sichuan, Fujian, Guangdong, Guangxi, Guizhou, Yunnan), Japan, North Korea (
Aholcus Kieffer (
In this study, our identification of reared specimens was facilitated by their association with Dendrolimus eggs and matching them to paratype specimens of T. dendrolimusi and three non-type specimens of T. dendrolimi from Japan.
We thank Chunhong Wang (Zhejiang University) for imaging the type materials of Telenomus dendrolimusi Chu. We also extend our sincerest thanks to Guangyi Dai from Institutional Center for Shared Technologies and Facilities of South China Botanical Garden-CAS for the SEM guidance. This study was supported by the National Natural Science Foundation of China (32370499, 31900346). ZL is a participant of the Oak Ridge Institute for Science and Education (ORISE) Agricultural Research Service (ARS) Research Participation Program, supported by the USDA-ARS U.S. Vegetable Laboratory in Charleston, SC, USA. Elijah Talamas was supported by the Florida Department of Agriculture and Consumer Services, Division of Plant Industry. The mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA.
Taxa, GenBank accession numbers, species group placement, collection location, and references associated with the sequence data used in the phylogenetic analyses
Data type: xlsx
Explanation note: Species group/complex placement mainly follows Johnson (1984) and Taekul et al. (2013).
28S ribosomal DNA cladogram of Telenomus
Data type: docx
Explanation note: Numbers on branches to the left of the forward slash indicate SH-aLRT values and numbers to the right of the forward slash are ultrafast bootstrap values.
Mitochondrial cytochrome oxidase I (COI) cladogram of Telenomus
Data type: docx
Explanation note: Numbers on branches to the left of the forward slash indicate SH-aLRT values and numbers to the right of the forward slash are ultrafast bootstrap values.Terminal labels correspond to the taxa listed in the supplementary table.
Combined 28S and mitochondrial cytochrome oxidase I (COI) cladogram of Telenomus
Data type: docx
Explanation note: Numbers on branches to the left of the forward slash indicate SH-aLRT values and numbers to the right of the forward slash are ultrafast bootstrap values.Terminal labels correspond to the taxa listed in the Suppl. material