Research Article
Print
Research Article
A new species of Metaurus Stål, 1866 (Hemiptera, Fulgoromorpha, Dictyopharidae), supplemented with mitogenome data from China
expand article infoYan-Li Zheng‡§, Thierry Bourgoin|, Lin Yang§, Xiang-Sheng Chen§
‡ Guizhou Education University, Guiyang, China
§ Guizhou University, Guiyang, China
| MNHN-CNRS-Sorbonne Université-EPHE-Univ. Antilles, Paris, France

Corresponding author: Xiang-Sheng Chen ( xschen@gzu.edu.cn )

Academic editor: Mike Wilson
© 2024 Yan-Li Zheng, Thierry Bourgoin, Lin Yang, Xiang-Sheng Chen.
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: Zheng Y-L, Bourgoin T, Yang L, Chen X-S (2024) A new species of Metaurus Stål, 1866 (Hemiptera, Fulgoromorpha, Dictyopharidae), supplemented with mitogenome data from China. ZooKeys 1215: 53-64. https://doi.org/10.3897/zookeys.1215.128976
ZooBank: urn:lsid:zoobank.org:pub:6C46F16B-B4D7-429C-A218-3967DE86DD81
Open Access

Abstract

A new planthopper species, Metaurus mohanensis Zheng & Chen, sp. nov., is described and illustrated from Yunnan, China. A key to differentiate species within the genus Metaurus is provided. The geographical distribution of Metaurus species and mitochondrial genome data of the newly described species are also included.

Key words

Auchenorrhyncha, distribution, Fulgoroidea, identification key, morphology, planthoppers, taxonomy

Introduction

With a global distribution of 748 species across 160 genera (Bourgoin 2024), the family Dictyopharidae Spinola, 1839 represents a moderately sized taxon within the Hemiptera: Fulgoromorpha. Like all planthoppers, Dictyopharidae are strictly phytophagous insects, known to feed on over 25 families. Their diet predominantly includes dicots, particularly Asterales (13%), Caryophyllales (9%), Fabales (9%), and Fagales (7%), as well as monocots such as Poales (13%) and Liliales (7%) (Bourgoin 2024). Several dictyopharid species are recognized as economically significant agricultural pests (Wilson and O’Brien 1987; Wilson et al. 1994).

Dictyopharidae is currently classified into 19 tribes, plus two fossil ones, divided between two subfamilies: Dictyopharinae Spinola, 1839 and Orgeriinae Fieber, 1872 (Song et al. 2018; Bourgoin 2024). The genus Metaurus Stål, 1866 was initially placed in the tribe Dictyopharini Spinola, 1838, but was transferred to Orthopagini Emeljanov, 1983 by Emeljanov (2011) and later revised by Song and Liang (2012). In this latter study, the authors described a new species, M. ramusitis Song & Liang, 2012 from Laos and China (Yunnan), in addition to the type species M. reticulatus Stål, 1866 known from Cambodia. They also identified an unnamed species from Thailand, which is definitively distinct but could not be formally described due to the absence of its abdomen.

We formally describe here a third species of Metaurus from Yunnan, China, M. mohanensis sp. nov. In addition to its morphological description, we also provide its complete mitogenome.

Materials and methods

Morphology

The specimens examined have been deposited in the Institute of Entomology, Guizhou University, Guiyang, China (GUGC). Dry specimens were used for the descriptions and illustrations. Genital segments of the specimens were macerated in a boiling solution of 10% NaOH, transferred to preparations of glycerin jelly, and examined under a Leica MZ12.5 stereomicroscope. Photographs of adult habitus were obtained using a Keyence VHX-1000 system. Illustrations were scanned with Canon Cano Scan LiDE 200 and imported into Adobe Photoshop CS6 for labeling and composition of figures.

The morphological terminology follows Yang and Yeh (1994) for the head and body, Bourgoin et al. (2015) for the forewing venation, and Bourgoin (1987, 1993) and Yang and Yeh (1994) for male and female genitalia, respectively. The usual standardized notation is used for the wing venation as follows: A1 first anal vein; bc, basal cell; CuA cubitus anterior; CuP cubitus posterior; MP: media posterior; R: radius; Sc: subcosta. The following abbreviations are used in the text for measurements: BL body length (from apex of cephalic process to tip of forewings); HL head length (from apex of cephalic process to base of eyes); HW head width (including eyes); FWL forewing length.

Biogeographical realms are named according to Holt et al. (2013).

Molecular methods

Total genomic DNA was extracted from the muscle tissue from the hind legs of the holotype specimen using the Takara Genome DNA Extraction Kit (Sangon Biotech, Shanghai, China) according to the manufacturer’s instructions. The mitogenome was sequenced using a next-generation sequencing platform with Illumina Hiseq 2500 at OriGene (Beijing, China).

The quality of the raw sequences was evaluated using FastQC v.0.11.4 (www.bioinformatics.babraham.ac.uk/projects/fastqc). Putative mitogenome reads with an average quality value of < Q30 were removed before assembly. Then, the clean sequences were assembled using MitoZ v.2.4 software with default parameters and the mitogenome of Orthopagus splendens (Fulgoroidea: Dictyopharidae; GenBankNo. MW441850) as a reference (Zheng et al. 2021). The mitogenome was initially annotated using Galaxy Community 2022 with invertebrate genetic codes. PCGs were predicted by determining their open reading frames using the invertebrate mitochondrial genetic codon. rRNA genes and the AT-rich regions were determined by comparisons with the homologous sequences of other planthoppers from GenBank. Mitogenomic circular maps were depicted and annotated using Geneious R9. Strand asymmetry was calculated according to the following formulas: AT skew = (A-T)/(A+T) and GC skew = (G-C)/(G+C). The mitogenome sequences of the new species have been deposited in GenBank under the accession number PP863288.

Taxonomy

Subfamily Dictyopharinae Spinola, 1839

Tribe Orthopagini Emeljanov, 1983

Metaurus Stål, 1866

Metaurus Stål, 1866a: 151. Type species: Metaurus reticulatus Stål, 1866; by subsequent designation by Melichar (1912).

Metaurus Stål: Stål 1866b: 391; Atkinson 1886: 24; Melichar 1912: 46; Metcalf 1946: 38; Song and Liang 2012: 2564.

Diagnosis

See Song and Liang (2012).

Distribution

Oriental region (Cambodia; Laos; southwestern China; Thailand) (Song and Liang 2012).

Key to the species of Metaurus Stål (modified from Song and Liang 2012)

1 In lateral view, cephalic process in front of eyes distinctly longer than distance from curved point to posterior margin of eyes, with the ratio about 1.4: 1 M. indet. sp.
– In lateral view, cephalic process in front of eyes slightly shorter or as long as distance from curved point to posterior margin of eyes 2
2 In lateral view, cephalic process in front of eyes slightly shorter than distance from curved point to posterior margin of eyes, with the ratio about 0.7–0.8: 1. In dorsal view, segment X of males short and small, with ratio of the maximum length to width near base about 1.1: 1. In lateral view, apical ventral margins protruded ventrally into a small process. Aedeagus with ventral outer apical lobes curved anteriorly in ventral view M. ramusitis Song & Liang
– In lateral view, cephalic process in front of eyes as long as distance from curved point to posterior margin of eyes. In dorsal view, segment X of males large and elongate, with ratio of the maximum length to width near base > 1.5. In lateral view, apical ventral margins protruded ventrally into a large rounded process. Aedeagus with ventral outer apical lobes directed posteriorly in ventral view 3
3 In dorsal view, segment X of males with ratio of the maximum length to width near base about 1.6: 1; its ventral margins irregularly incised at midlength in lateral view. Aedeagus with ventral outer apical lobes directed posteriorly in ventral view M. reticulatus Stål
– In dorsal view, segment X of males with ratio of the maximum length to width near base about 2.3: 1; its ventral margins only slightly concave, not incised at midlength in lateral view. Aedeagus with dorsal apical lobes (Figs 11, 16) produced in a pair of long lobes, directed posteriorly in lateral view, and two lobes on it, base extends forward to form a leaf projection; ventral lobes (Figs 10, 17) with two pairs of lobes M. mohanensis Zheng & Chen, sp. nov.

Metaurus mohanensis Zheng & Chen, sp. nov.

https://zoobank.org/9761682E-75C4-449E-BF12-10C12713C931

Type material

Holotype • ♂, China: Yunnan, Xishuangbanna Mengla County, Mohan, 16 June 2019, Feng-E Li (GUGC, no. GUGC-20220811-Y13). Paratypes • 2♂♂, same collection site as the holotype but 22 June 2019, Yalin Yao (GUGC).

Diagnosis

The new species is similar to Metaurus ramusitis Song & Liang, but can be distinguished from the latter by the shape of the phallobase and segment X: dorsal apical lobes of the phallobase (Figs 11, 16) produced in a pair of long lobes, directed posteriorly in lateral view, and two lobes on it, base extends forward to form a leaf projection in dorsal view (not in M. ramusitis). Segment X in dorsal view is relatively narrow, with ratio of the maximum length to width near base about 2.3: 1 (Fig. 13); ventral margin is protruded ventrally into a large rounded process at base in lateral view and slightly concave, not incised medially (Figs 8, 12); in M. ramusitis: segment X is relatively broader in dorsal view, and with an irregular incision medially in lateral view.

Description

Measurements (in mm). ♂, BL: 17.3–17.1 mm; HL: 3.6–3.7 mm; HW: 1.7–1.8 mm; FWL: 12–12.1 mm.

Coloration. Body green. General colour greenish ochraceous; darker on apical part of cephalic process, on a longitudinal spot before eyes on genae, and on a small anterior spot on lower lateral carina behind eyes on pronotum. Rostrum blackish at extreme apex. Fore and hind wing membrane transparent, veins green, stigmal area green, anterior margin yellow. Legs green, apex of hind femora and base of hind tibiae black, tips of lateral spines on hind tibiae and tips of apical teeth on tarsomeres black.

Morphology. Head and thorax (Figs 1–5). Cephalic process in front of eyes strongly upturned (about 45°), as long as distance from curved point to posterior margin of eyes in lateral view. Head shorter than pronotum and mesonotum combined, its ratio of length: width about 1:0.45 . Vertex relatively narrow, median longitudinal carina distinct only at the base, and lateral carina deeply concave and strongly tapered in front of the compound eyes. Frons elongate, with median carina complete and elevated, 2.5 times as long as wide, anterior portion distinctly narrowed and protruded anteriorly and upwardly in ventral and lateral views; lateral carinae ridged, frons distinctly expanded outwards below antennae. Postclypeus and anteclypeus strongly convex at middle, with distinct median carina. Rostrum long, extending up to abdominal sternite VI. Pronotum distinctly shorter than mesonotum medially, ratio length about 0.4:1, narrow anteriorly, broad posteriorly. Mesonotum tricarinate, lateral carinae incurved anteriorly towards median carina.

Forewings (Figs 1, 2, 6) hyaline, much longer than abdomen, nearly three times as long as broad; anterior margin distinctly expanded into a narrow, sclerotized costal area; costal cell without transverse veins, Sc+R forked apicad of junction of claval veins; MP first branching in MP1+2 and MP3+4 veins near basal one-third, anterior to first CuA branching, MP1+2 fork situated posterior to MP3+4 fork and then branching into a dozen of terminals; numerous transverse veins among Sc+R, MP and CuA on apical two-thirds; 22 apical cells; Pcu and A1 fused into a short Pcu+A1 vein at apical third of clavus; pterostigmal area not differentiated, elongate, with nine cells.

Figures 1–7. 

Metaurus mohanensis Zheng & Chen, sp. nov. 1 male, holotype, dorsal view 2 male, lateral view 3 male, head and thorax, dorsal view 4 male, frons and clypeus, ventral view 5 male, head and pronotum, lateral view 6 male, forewing 7 male, hind wing. Scale bars: 1 mm.

Hindwings (Fig. 7) hyaline. CuA first branching into CuA1 and CuA2 near middle; MP and CuA1 branching to several accessory veins on apical two-thirds, with several transverse veins; 14 apical cells.

Legs narrow and long, fore femora flattened and dilated, with a distinct spine near apex, hind tibiae with 7 lateral spines and 7 apical teeth, hind tarsomeres I with 10 and tarsomeres II with 11 apical teeth. Metatibiotarsal formula: 7-7/10:11

Male genitalia. Pygofer large and broad, ventrally distinctly longer than dorsally (about 5: 1); posterior margin with two obtuse processes near middle in lateral view (Figs 8, 12), upper process slightly smaller than lower one. Segment X (anal tube) large and broad in dorsal view, with ratio of the maximum length to width near base about 2.3: 1 (Figs 8, 12, 13); ventral margins in basal third protruded ventrally into a large triangular process in lateral view. Gonostyli relatively small in lateral view, posterior margin with directed tooth-like dorsal process medially and a directed tooth-like ventral process submedially on outer upper edge; apical part elongate and rounded (Figs 8, 12, 14); dorsal process short, acute apically. Aedeagus (Figs 9–13) large and robust, dorsal and lateral parts and most of ventral part of phallobase sclerotized and pigmented, the remainder membranous; with 3 pairs of apical membranous lobes; dorsal apical lobes (Figs 15, 16) long, directed posteriorly in lateral view, each bearing two smaller projections (Figs 15c, 16c) on it, base extending forward to form a leaf-like projection (Figs 15a, 16a); ventral lobes (Figs 10, 15, 17) large and slender, with two pairs of projections (Figs 10, 15, 17): the inner ones very slender (Figs 15f, 17f), directed posteriorly, with additional two smaller membranous projections on their median part (Fig. 17h), and one large basal lobe (Figs 15d, 17d); the outer ones slender and elongate, directed posteriorly (Fig. 17e), with two small projections medially in ventral view (Figs 15g, 17g).

Etymology

The species name “mohanensis” refers to the collecting site in the town of Mohan, in the Yunnan Province in southwestern China. Adjective.

Mitochondrial genome of the new species

The complete mitogenome of Metaurus mohanensis Zheng & Chen, sp. nov. is 15,469 bp in length and consists of 13 protein-coding genes (PCGs), 2 ribosomal RNA genes (rRNAs), 22 transfer RNA genes (tRNAs) and one large non-coding region (D-loop: [A+T]-rich region) (Fig. 18). The D-loop part is 1233 bp, taking place between 12S rRNA and trnI. The overall base composition is A: 48%, T: 28.8%, C: 15%, and G: 8.2%. AT skew ((A-T)/(A+T)) and GC skew ((G-C)/(G+C)) are 0.25 and - 0.293, respectively. All 13 PCGs started with ATN, GTG (nad1, nad5) and ended with TAN or a single T (nad1, nad4, atp6 and nad5) residue. The length of 22 tRNA ranged from 57 bp (trnV) to 70 bp (trnK). Genes of 16S rRNA and 12S rRNA are 1, 201 bp and 732 bp, respectively.

The genomic data from this study are openly available in the National Center for Biotechnology Information (NCBI) at https://www.ncbi.nlm.nih.gov, accession number: PP863288. Associated BioProject, SRA, and BioSample accession numbers are PRJNA1114399, SUB14549433 and SAMN41484364 respectively (https://www.ncbi.nlm.nih.gov/bioproject/PRJNA1114399).

Figures 8–11. 

Metaurus mohanensis Zheng & Chen, sp. nov. 8 genitalia, lateral view 9 aedeagus, lateral view 10 aedeagus, ventral view 11 aedeagus, dorsal view. Scale bars: 1 mm (8); 0.5 mm (9–11).

Figures 12–17. 

Metaurus mohanensis Zheng & Chen, sp. nov. 12 genitalia, lateral view 13 segment X, dorsal view 14 gonostyles, lateral view 15 aedeagus, lateral view 16 aedeagus, dorsal view 17 aedeagus, ventral view a–h 3 pairs of apical membranous lobes (same letters representing the same parts). Scale bars: 1 mm (12); 0.5 mm (13–17).

Discussion and conclusions

The Oriental genus Metaurus exhibits a continental distribution in southeastern Asia, being restricted to Thailand, Cambodia, Laos and southwestern China(Fig. 19). Metaurus ramusitis Song & Liang, 2012 is known from Laos and only by one female from Yunnan, China. The new species in this study was also collected from Yunnan, China.

Species of Metaurus are externally quite similar to those of Centromeria Stål, 1870, a more diversified genus of Orthopagini with 14 species known to date (Song et al. 2016; Bourgoin 2024), but with a wider southeastern Asian distribution corresponding to the Oriental zoogeographic region as defined by Holt et al. (2013). Metaurus can be separated from Centromeria by the following characters: 1) Head in front of the eyes is strongly upturned, forming a slender, straight process, with the vertex’s median carina only weakly ridged at the base (versus a frontal process that is moderately to strongly curved upwards in Centromeria); the vertex in Centromeria has lateral carinae that are moderately or abruptly constricted, strongly upturned in front of the eyes, and then gradually convergent anteriorly, culminating in an acuminate apex; 2) MP vein first forks into MP1+2 and MP3+4 veins before CuA, close to the basal one-third of corium, which is branched and with numerous accessory veins on the apical two-thirds of the corium (while MP bifurcating into MP1+2 and MP3+4 near middle, and posterior to CuA in Centromeria); and 3) Hind tibiae in Metaurus have 7 apical teeth, compared to only 6 apical teeth in Centromeria.

Figure 18. 

Circular map of the mitogenome of Metaurus mohanensis Zheng & Chen, sp. nov.

Figure 19. 

Geographical distribution of Metaurus species.

The mitogenome of Metaurus mohanensis Zheng & Chen, sp. nov. differs from Orthopagus splendens (Fulgoroidea: Dictyopharidae: Orthopagini; GenBankNo. MW441850) (Zheng, Bourgoin et al. 2021) by the following characteristics: 1) full length 15469 (15346 in O. splendens); 2) overall base composition: A: 48%, T: 28.8%, C: 15%, and G: 8.2%. AT skew ((A-T)/(A+T)) and GC skew ((G-C)/(G+C)) 0.25 and - 0.293, respectively (versus A: 47.2%, T: 30.2%, C: 14.6%, and G: 8%. AT skew ((A-T)/(A+T)): 0.22 and GC skew ((G-C)/(G+C)): - 0.294 in Orthopagus splendens); and 3) In M. mohanensis, all 13 PCGs start with ATN or GTG (nad1, nad5) and end with TAN or a single T (nad1, nad4, atp6 and nad5) residue. The length of 22 tRNA ranges from 57 bp (trnV) to 70 bp (trnK). Genes of 16S rRNA and 12S rRNA are 1,201 bp and 732 bp, respectively. In O. splendens, all 13 PCGs start with ATN and end with TAN or a single T (nad1, nad5 and atp6) residue. The length of 22 tRNA ranges from 59 bp (trnS) to 70 bp (trnK). Genes of 16S rRNA and 12S rRNA are 1,177 bp and 729 bp, respectively.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

The project was supported by the 2021 Guizhou Normal University award and subsidy fund project (No. 2023GZJB009); Guizhou Provincial Department of Education College Humanities Society, scientific research project No. 23RWJD191; Scientific research fund project of Guizhou Normal University (No. 2021ZD001).

Author contributions

All authors have contributed equally.

Author ORCIDs

Yan-Li Zheng https://orcid.org/0000-0002-6964-5988

Thierry Bourgoin https://orcid.org/0000-0001-9277-2478

Data availability

All of the data that support the findings of this study are available in the main text.

References

  • Atkinson ET (1886) Notes on Indian Rhynchota. No. 5. Journal of the Asiatic Society of Bengal 55: 12–83.
  • Bourgoin T (1987) A new interpretation of the homologies of the Hemiptera male genitalia, illustrated by the Tettigometridae (Hemiptera, Fulgoromorpha). In: Vidano C, Arzone A, Consiglio nazionale delle ricerche (Eds) Proceedings of the 6th Auchenorrhyncha meeting Turin, Italy, 7–11 September, 113–120.
  • Bourgoin T (2024) FLOW (Fulgoromorpha Lists On the Web), a world knowledge base dedicated to Fulgoromorpha. Version 8. [accessed 2024-5-1]
  • Bourgoin T, Wang RR, Asche M, Hoch H, Soulier-Perkins A, Stroiński A, Yap S, Szwedo J (2015) From micropterism to hyperpterism: recognition strategy and standardized homology-driven terminology of the forewing venation patterns in planthoppers (Hemiptera: Fulgoromorpha). Zoomorphology 134(1): 63–77. https://doi.org/10.1007/s00435-014-0243-6
  • Emeljanov AF (2011) Improved tribal delimitation of the subfamily Dictyopharinae and description of new genera and new species (Homoptera, Fulgoroidea, Dictyopharidae). Entomologicheskoe Obozrenie 90: 299–328. [English translation in Entomological Review 91: 1122–1145, 2011] https://doi.org/10.1134/S0013873811090053
  • Holt BG, Lessard JP, Borregaard MK, Fritz SA, Araujo MB, Dimitrov D, Fabre PH, Graham CH, Graves GR, Jonsson KA, Nogues-Bravo D, Wang ZH, Whittaker RJ, Fjeldsa J, Rahbek C (2013) An update of Wallace’s zoogeographic regions of the world. Science 339(6115): 74–78. https://doi.org/10.1126/science.1228282
  • Melichar L (1912) Monographie der Dictyophorinen (Homoptera). Abhandlungen der K. K. Zoologisch-Botanischen Gesellschaft in Wien 7(1): 1–221. [In German]
  • Metcalf ZP (1946) General catalogue of the Hemiptera, Fasc. IV. Fulgoroidea, Part 8 Dictyopharidae. Smith College, Northampton, MASS., 246 pp.
  • Song ZS, Liang AP (2012) Taxonomic revision of the Oriental genus Metaurus Stål (Hemiptera: Fulgoromorpha: Dictyopharidae), with description of a new species. Journal of Natural History 46: 41–42, 2563–2575. https://doi.org/10.1080/00222933.2012.708456
  • Song ZS, Webb MD, Liang AP (2016) Phylogenetic analysis of the Oriental genera of Orthopagini Emeljanov, 1983 (Hemiptera: Fulgoromorpha: Dictyopharidae: Dictyopharinae), with a systematic revision of the genus Centromeria Stål, 1870. Zoological Journal of the Linnean Society 178: 33–87. https://doi.org/10.1111/zoj.12401
  • Song ZS, Bartlett CR, O’Brien LB, Liang AP, Bourgoin T (2018) Morphological phylogeny of Dictyopharidae (hemiptera: fulgoromorpha). Systematic Entomology 43(4): 637–658. https://doi.org/10.1111/syen.12293
  • Stål C (1866a) Hemiptera Homoptera Latr. Hemiptera of Africa 4: 1–276.
  • Wilson SW, O’Brien LB (1987) A survey of planthoppers pests of economically important plants (Homoptera: Fulgoroidea). In: Proceedings of the 2nd Inter. Workshop on Leafhoppers and Planthoppers of Economic Importance. Commonwealth Institute of Entomology, London, 343–360.
  • Wilson SW, Mitter C, Denno RF, Wilson MR (1994) Evolutionary patterns of host plant use by delphacid planthoppers and their relatives. In: Denno RF, Perfect J (Eds) Planthoppers: Their Ecology and Management. Chapman and Hall, New York, 7–113. https://doi.org/10.1007/978-1-4615-2395-6_2
  • Yang CT, Yeh WB (1994) Nymphs of Fulgoroidea (Homoptera: Auchenorrhyncha) with descriptions of two new species and notes on adults of Dictyopharidae. Chinese Journal of Entomology, Special Publication 8: 1–187.
  • Zheng YL, Bourgoin T, Yang L, Chen XS, Luo XQ, Luo GJ (2021) Complete mitochondrial genome of the planthopper Orthopagus splendens (Germar, 1830) (Hemiptera: Fulgoromorpha: Dictyopharidae). Mitochondrial DNA, B 6: 2667–2668. https://doi.org/10.1080/23802359.2021.1964400
login to comment