Research Article
Print
Research Article
Integrated taxonomy unveils three new species of Foenobethylus (Hymenoptera, Bethylidae) from China
expand article infoYang Li, Zheng Wang§, Hua-Yan Chen|, Shi-Xiao Luo|
‡ Chengdu Normal University, Chengdu, China
§ Research Institute of Spice and Beverage, Chinese Academy of Tropical Agricultural Sciences, Wanning, China
| South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China
Open Access

Abstract

Species of the genus Foenobethylus Kieffer, 1913 are parasitoids wasps rarely collected and are only found in the Oriental region. In this study, based on both morphological and molecular evidence, we describe three new species from China: F. robusta Li & Chen, sp. nov., F. xinglongsensis Wang & Chen, sp. nov., and F. yunkaishanensis Chen & Luo, sp. nov. An updated key to species of the genus is provided. Additionally, the phylogenetic relationships between Foenobethylus and other three morphologically similar genera are discussed based on the analyses of COI and 28S genes.

Keywords

Flat wasps, key, new species, parasitoid wasp, phylogeny, Pristocerinae

Introduction

Foenobethylus Kieffer is a rare genus of Pristocerinae in the flat wasp family Bethylidae, with only 11 described species Oriental (Várkonyi and Polaszek 2007; Liu et al. 2011; Savergnini and Azevedo 2013; Chen and Azevedo 2020). Of the 11 described species, 10 species were described based on only males. Until recently, the first female of the genus was discovered by Chen and Azevedo (2020). The new finding suggested that Foenobethylus might be a synonym under Parascleroderma. Although the morphological differences between Foenobethylus and Parascleroderma were intensely discussed (Azevedo and Lanes 2007; Várkonyi and Polaszek 2007; Chen and Azevedo 2020), Chen and Azevedo (2020) concluded that the precise taxonomic delimitation of both genera only could be solved under phylogentic analyses. Interestingly, before the discovery of the female of Foenobethylus, considering the extreme sexual dimorphism in Pristocerinae, Várkonyi and Polaszek (2007) also suspected that the females of Foenobethylus might be already known to science under a different generic name and the exact phylogenetic status of Foenobethylus could be resolved by preferably molecular evidence.

Recently, we have accumulated some fresh specimens of several Foenobethylus species collected by Malaise traps in South China. In this study, we aims to identify this new material to species using an integrated taxonomic approach that combines both morphology and molecular data and to conduct a preliminary phylogenetic analysis between Foenobethylus and morphologically similar genera based on DNA sequences.

Materials and methods

Collection and identification

This work is based on specimens of Foenobethylus collected by Malaise traps (MT) set up across southern China. Specimens were identified using the keys of Chen and Azevedo (2020). All studied specimens are deposited in the Insect Collection of South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China (SCBG, curator: Huayan Chen). The morphological terms generally follow Lanes et al. (2020) and Brito et al. (2021), and the sculptural and texture of integument nomenclature follows Harris (1979).

Abbreviations and morphological terms used in text are

WH width of the head;

LH length of the head;

WF width of the frons;

HE height of the eye;

OOL ocello-ocular line;

WOT width of the ocelar triangle.

The genitalia and subgenitial plate of a male paratype were removed and cleared using 10% potassium hydroxide solution, and mounted in glycerol on slides, when examined and photographed. Images and measurements were made using Nikon SMZ25 microscope with a Nikon DS-Ri 2 digital camera system. Images were post-processed with Abobe Photoshop 2022.

DNA extraction, amplification, and sequencing

In total, 7 specimens of 4 morphospecies were used for DNA acquisition (see Table 1). Collecting information of the studied specimens are avaiable in the material examined section by the associated codes. Genomic DNA was extracted from entire specimens using a DNeasy Blood & Tissue Kit (QIAGEN, Inc.), following a nondestructive DNA extraction protocol as described in Taekul et al. (2014). Following DNA extraction, the “barcode” region of the mitochondrial cytochrome oxidase subunit 1 (COI) and nuclear 28S rRNA D1–2 (28S) were amplified using the LCO1490/HCO2198 (Folmer et al. 1994) and D2–3551F/D2–4057R (Gillespie et al. 2005) primer pairs, respectively. Polymerase chain reactions (PCRs) were performed using Tks Gflex DNA Polymerase (Takara), and conducted in a T100 Thermal Cycler (Bio-Rad). Thermocycling conditions were: an initial denaturing step at 94 °C for 5 min, followed by 35 cycles of 94 °C for 30 s, 50 °C for 30 s, 72 °C for 30s and an additional extension at 72 °C for 5 min. Amplicons were directly sequenced in both directions with forward and reverse primers on an Applied Biosystems (ABI) 3730XL by Guangzhou Tianyi Huiyuan Gene Technology Co., Ltd. (Guangzhou, China). Chromatograms were assembled with Geneious 11.0.3. All sequences generated from this study are deposited in GenBank (accession numbers see Table 1). All residual DNAs are archived (–30 °C) in the molecular laboratory of SCBG, Guangzhou, China, and are available for further study upon request.

Table 1.

List of analyzed taxa and accession numbers.

Species Code GenBank accession No.
28S COI
Ingroup
Apenesia sp.1 MG760810 MG760759
Apenesia sp.2 MG760811 MG760760
Cleistepyris sp.1 MG760830 MG760774
Cleistepyris sp.2 MG760832 MG760776
Dissomphalus sp.1 MG760834 MG760778
Dissomphalus sp.2 MG760821 MG760768
Parascleroderma sp.1 MG760813 MG760762
Parascleroderma sp.2 MG760816 MG760763
Foenobethylus emiliacasellae MG760815
Foenobethylus robusta sp. nov. SCAU 3042641 OL678509
Foenobethylus syndesis SCAU 3042642 OL678115 OL678510
Foenobethylus syndesis SCAU 3042643 OL678116 OL678511
Foenobethylus xinglongsensis sp. nov. SCAU 3042638 OL678117 OL678512
Foenobethylus xinglongsensis sp. nov. SCAU 3042656 OL678118 OL678513
Foenobethylus yunkaishanensis sp. nov. SCAU 3042639 OL678119 OL678514
Foenobethylus yunkaishanensis sp. nov. SCAU 3042658 OL678120 OL678515
Outgroup
Prorops nasuta MG760840 MG760784
Sierola gracilis MG760837 MG760781

Molecular species delimitation and phylogenetic analysis

All sequences were blasted in BOLD (Barcode of Life Database, http://www.barcodinglife.org/index.php/IDS_OpenIdEngine, only for COI) and GenBank. Sequences were aligned using MAFFT v7.470 by the G-INS-I strategy for 28S and G-INS-I strategy for COI (Katoh and Standley 2013). Genetic Kimura-2 parameter (K2P) distances of COI sequences within and between species were calculated in MEGA 7 with pairwise deletion for gaps (Kumar et al. 2016). For phylogenetic analysis, sequences of specimens of three morphologically similar or phylogenetically close genera, Apenesia Westwood, Cleistepyris Kiefer, Dissomphalus Ashmead and Parascleroderma Kieffer, as suggested by previous studies (Alencar et al. 2018; Chen and Azevedo 2020), were extracted from Alencar et al. (2018) (Table 1). The 28S sequence of Foenobethylus emiliacasellae Várkonyi and Polaszek was downloaded from Genbank. Prorops nasuta (Waterston, 1923) and Sierola gracilis Fullaway, 1920 (Hymenoptera, Bethylidae) selected as outgroups as used by Alencar et al. (2018). The concatenated sequences of 28S and COI were then analyzed using RAxML as implemented in Geneious 11.0.3 under the GTRGAMMA evolutionary model to generate a maximum likelihood (ML) tree.

Results

This study generated seven sequences of COI and six sequences of 28S for seven specimens. These seven voucher specimens were subjected to further morphological examination and four species were recognized, of which three are described as new. The COI sequences do not show a high match with sequences in both BOLD and GenBank databases. The closes match is an undetermined species of Parascleroderma, with 86.4% identical base pairs. Genetic distances of COI sequences among Foenobethylus species and representative species of four other morphologically similar or purported phylogenetically close genera and outgroups are in Table 2. Intraspecific distances of the COI sequences of Foenobethylus are identical. Interspecific distances among Foenobethylus speces range between 10.3% and 13.6%. Intergeneric distances between Foenobethylus and the four potential close genera and the outgroups range between 14.3% and 28.6%, with Parascleroderma is the most close genus, which shows 14.8–18.6% divergence. The morphology-based delimitations of species are congruent with the molecular species identification based on COI sequences. Phylogenetic relationships between Foenobethylus and the studied genera are shown in Fig. 1. Foenobethylus was recovered as a monophyletic clade, with Parascleroderma as a sister group.

Table 2.

Genetic distances of COI sequences among studied taxa (%).

Taxon 1 2 3 4 5 6 7 8 9 10 11 12 13 14
1 Apenesia sp1
2 Apenesia sp2 1.4
3 Cleistepyris sp1 20.3 19.4
4 Cleistepyris sp2 19.8 19.4 15
5 Dissomphalus sp1 27.3 26.9 26.5 25.4
6 Dissomphalus sp2 23.4 23.5 27.2 22.6 26.4
7 Parascleroderma sp1 19.8 19.2 19.4 17.4 24.9 21
8 Parascleroderma sp2 17 16.4 21.1 20.8 26.2 23.4 17.3
9 Foenobethylus robusta sp. nov. 18.7 18.7 20.9 18.6 25 23.5 14.3 18.6
10 Foenobethylus syndesis 21.4 21.2 22.5 19.9 25.2 24.6 15.4 17.4 11.3
11 Foenobethylus xinglongensis sp. nov. 20.1 19.6 20.9 17.7 24.8 24.7 14.6 16.4 13.1 13.6
12 Foenobethylus yunkaishanensis sp. nov. 19.8 19.6 21.2 19.4 31.5 23.9 14.8 16.7 10.8 10.3 12.3
13 Sierola_gracilis 25.2 24.7 27.1 27 28.6 27.4 24.7 25.5 27 28.6 27.8 27.5
14 Prorops_nasuta 25 24.7 26.2 25.5 25.5 27 23.7 25.5 25.3 27.5 26.4 25.2 27.2
Figure 1. 

Maximum likelihood tree demonstrating the clustering of Foenobethylus and related genera based on concatenated sequences (COI and 28S).

Species treatment

Foenobethylus robusta Li & Chen, sp. nov.

Figures 2, 3

Diagnosis

Male. Head rectangular and elongate (Fig. 2B). Clypeus with median lobe truncate, median carina incomplete, not reaching anterior clypeal margin, and straight in dorsal profile. Eye glabrous (Fig. 2B). Notaulus very weakly converging posteriorly, complete and deep (Fig. 2C). Propodeum polished (Fig. 2C). Pterostigma broad, about 0.4× as wide as long (Fig. 2F). Metatrochanter without spine (Fig. 3G). Metafemur with only one acute spine in ventral midline, 0.26× as long as metafemoral width, touching apical margin of metatrochanter, and with one small, broad and dentate protuberance ventrally, 0.04× metafemoral width, located on second quarter of metafemur (Fig. 3G). Posterior hypopygeal margin strongly incurved, lateral lobe without conical protuberance (Fig. 3E). Basivolsella large, 0.6× as long as gonostipe, basal half about as wide as apical half, basal margin incurved (Fig. 3C, D).

Description

Male holotype. Body length 4.52 mm. Forewing length 3.10 mm. Colors. Head, mesosoma, metasoma, antenna and apex of mandible dark castaneous; palpi, base of mandible, all tibiae and tarsi castaneous; wings subhyaline, fore wing somewhat infuscate medially.

Head. Head (Figs 2B, 3A) rectangular and elongate, 1.2× as long as wide. Mandible with five apical sharpened teeth, posterior tooth largest, middle three teeth smaller, anterior tooth smallest. Clypeus with median lobe truncate, median carina incomplete, not reaching anterior clypeal margin, and straight in dorsal profile. Eye glabrous, almost touching mandible base at anterior corner. Malar space reduced. Frons weakly coriaceous, almost polished, punctures very sparse and small. WH 0.84× LH. WF 0.66× WH. WF 1.63× HE. OOL 1.44× WOT. Frontal angle of ocellar triangle obtuse. Anterior ocellus far posterior to supra-ocular line. Temple divergent anterad, corner rounded. Vertex badly outcurved. First four antennomeres in ratio of about 25:12:11:11 (Fig. 2E). All flagellomeres distinctly longer than wide, pubescence erect, about 0.48× as long as flagellomeral width. Maxillary palpus with five palpomeres (Fig. 3A). Labial palpus with two palpomeres (Fig. 3A). Occipital carina complete. Medioccipito-genal carina complete. Hypostomal carina thick, almost straight, angled medially.

Figure 2. 

Foenobethylus robusta Li & Chen, sp. nov., male, holotype (SCAU 3042645) A lateral habitus B head, dorsal view C mesosoma, dorsal view D mesosoma, lateral view E antenna F wings.

Figure 3. 

Foenobethylus robusta Li & Chen, sp. nov., male, A, B, G holotype (SCAU 3042645) C–F paratype (SCAU 3042641) A head, ventral view B mesosoma, ventral view C genitalia, dorsal view D genitalia, ventral view E subgenital plate F 7th sternite G metaleg, lateral view.

Mesosoma (Figs 2C, D, 3B). Mostly polished and weakly coriaceous. Pronotal flange short, exposing propleuron dorsally. Dorsal pronotal area short, without anterior carina strongly progressively narrowing anterad, lateral surface concave. Notaulus very weakly converging posteriorly, complete, deep, and progressively more evident posteriorly. Parapsidal signum sinuous, absent anteriorly. Mesoscutellum shorter than anteromesoscutum. Mesoscutum-mesoscutellar sulcus deep, arched, sides wider than middle. Metanotum conspicuous, metascutellum wide and short, metanotal trough not trabeculate, metanotal fovea outlined. Metapectal-propodeal disc polished, metapostnotal median carina complete, although weak posteriorly, lateral and transverse posterior carinae complete; propodeal spiracle circular, located on lateral surface of propodeum, ventral to lateral carina. Propodeal declivity transverse sculptured, without median carina. Mesopleuron with mesopleural pit large and well defined. Pleurosternum small, triangular, with vertex directed posterad. Prepectus with epicnemial medial projection complete, posterior prepectal flange thick. Wings (Fig. 2F). Forewing with three closed cells (Costal, Radial and First Cubital); pterostigma about 0.4× as wide as long, anterior board outcurved; 2r-rs&Rs sector vein long; Rs&M reaching Sc+R far from pterostigma. Hind wing with one straight hamulus, and four distal hamuli equally distant, and strongly curved. Legs. Profemur swollen, 2.7× as long as wide, apical half of ventral margin serrulate. Metatrochanter (Fig. 3G) without spine. Metafemur (Fig. 3G) with one acute spine in ventral midline, 0.26× as long as metafemoral width, touching apical margin of metatrochanter, and with one small, broad and dentate protuberance ventrally, 0.04× metafemoral width, located on second quarter of metafemur.

Metasoma. Weakly longer than mesosoma. Seventh sternite (Fig. 3F) with posterior margin incurved at about middle third. Hypopygium (Fig. 3E) with spiculum longer than median length of hypopygium, and 1.3× longer than anteromedial apodeme, latter strongly curved mesad apically; posterior margin strongly incurved, lateral lobe obtuse rounded. Genitalia (Fig. 3C, D). Harpe shorter than gonostipe; aedeagus slightly wide, 2.32× as long as wide, apex aedeagus posterior to posterior margin of gonostipe, 0.6× as long as gonostipe; basivolsella large, 0.6× as long as gonostipe, basal half about as wide as apical half, basal margin incurved.

Variation

Mesosoma more polished, expecially pronotum and propodeum.

Etymology

The specific epithet derived from the Latin word for robust, and refers to the robust body of this species.

Material examined

Holotype , male, China: Yunnan, Dali, Yunlong County, 2608 m, 25°50'57.94"N, 99°14'30.58"E, 27.xiii–12.ix.2020, MT, SCAU 3042645 (SCBG). Paratypes: 2 males. 1 male, same collecting data as holotype, SCAU 3042641 (SCBG); 1 male, China: Yunnan, Dali, Yunlong County, 2537 m, 25°50'49.91"N, 99°14'22.95"E, 28.v–14.vi.2020, MT, SCAU 3042657 (SCBG).

Distribution

Oriental region, China, Yunnan Province.

Remarks

This new species is very similar to F. syndesis Chen & Azevedo [Yunnan and Hainan, China], but can be separated from the latter by the following characters: median carina of clypeus incomplete (complete in F. syndesis); notaulus complete and deep (incomplete and shallow in F. syndesis); declivity of propodeum without median carina (with median carina in F. syndesis); metafemur with only one acute spine in ventral midline (with two acute spines in F. syndesis); lateral lobe of hypopygium without conical protuberance (with conical protuberance in F. syndesis).

Foenobethylus syndesis Chen & Azevedo, 2020

Foenobethylus syndesis Chen & Azevedo, 2020: 1241–1246 (diagnosis, description, distribution, key).

Material examined

Other material. 1 male, China: Hainan, Mt. Diaoluoshan, 18°40'2.4"N, 109°54'32.09"E, 31.x–30.xi.2020, MT, Long-long Chen, SCAU 3042642 (SCBG); 1 male, China: Hainan, Mt. Jianfengling, 18°41'42.37"N, 108°51'36.11"E, 688.01m, 30.iv–10.v.2020, MT, Chun-yang Xu, SCAU 3042643 (SCBG).

Distribution

Oriental region, China, Yunnan and Hainan Provinces.

Foenobethylus xinglongensis Wang & Chen, sp. nov.

Figures 4, 5

Diagnosis

Male. Head rectangular and elongate (Fig. 4B). Clypeus with median lobe obtuse rounded, median carina complete, reaching anterior clypeal margin, high, straight in lateral profile. Eye glabrous (Fig. 4B). Frons almost polished (Fig. 4B). Notaulus converging posteriorly, incomplete and shallow (Fig. 4C). Metapostnotal median carina incomplete, posterior third absent. Declivity of propodeum transversely rugulose (Fig. 4D). Metatrochanter without spine (Fig. 5F). Metafemur with only one proximal acute spine in ventral midline, 0.19× as long as metafemoral width, touching apical margin of metatrochanter (Fig. 5F). Posterior hypopygeal margin strongly incurved, lateral lobe with conical protuberance (Fig. 5B). Basivolsella large, 0.6× as long as gonostipe, basal half about as wide as apical half, basal margin incurved (Fig. 5C, D).

Figure 4. 

Foenobethylus xinglongensis Wang & Chen, sp. nov., male, holotype (SCAU 3042798) A lateral habitus B head, dorsal view C mesosoma, dorsal view D mesosoma, lateral view E antenna F wings.

Figure 5. 

Foenobethylus xinglongensis Wang & Chen, sp. nov., male, A, F holotype (SCAU 3042798), B–E paratype (SCAU 3042638). A head and mesosoma, ventral view B subgenital plate C genitalia, dorsal view D genitalia, ventral view E 7th sternite F metaleg, lateral view.

Description

Male holotype. Body length 2.32 mm. Forewing length 1.67 mm. Colors. Head, mesosoma (but pronotum and propleura castaneous), metasoma castaneous; base of scape, flagellomeres, apex of mandible, all coxae, all trochanter, all femora, basal half of all tibiae and claws pale castaneous; apex of scape, pedicel, base of mandible, palpi, protibia, apical half of all tibiae and tarsi yellow; wings subhyaline.

Head. Head (Figs 4B, 5A) rectangular and elongate, 1.2× as long as wide. Mandible with five apical sharpened teeth, posterior tooth largest, middle three teeth smaller, anterior tooth smallest. Clypeus with median lobe obtuse rounded, median carina complete, reaching anterior clypeal margin, high, straight in lateral profile. Eye glabrous, almost touching mandible base at anterior corner. Malar space reduced. Frons very weakly coriaceous, almost polished, punctures very sparse and small. WH 0.86× LH. WF 0.62× WH. WF 1.35× HE. OOL 1.19× WOT. Frontal angle of ocellar triangle obtuse. Anterior ocellus far posterior to supra-ocular line. Temple divergent anterad, corner rounded. Vertex badly outcurved. First four antennomeres in ratio of about 35:15:14:13 (Fig. 4E). All flagellomeres distinctly longer than wide, pubescence erect, about 0.63× as long as flagellomeral width. Maxillary palpus with five palpomeres (Fig. 5A). Labial palpus with two palpomeres (Fig. 5A). Occipital carina complete. Medioccipito-genal carina complete. Hypostomal carina thick, almost straight, angled medially.

Mesosoma (Figs 4C, D, 5A). Mostly polished and weakly coriaceous. Pronotal flange short, exposing propleuron dorsally. Dorsal pronotal area short, without anterior carina strongly progressively narrowing anterad, lateral surface concave. Notaulus converging posteriorly, incomplete, shallow, faint, but progressively more evident posteriorly. Parapsidal signum almost straight, absent anteriorly, but wide and deep posteriorly. Mesoscutellum slightly shorter than anteromesoscutum. Mesoscutum-mesoscutellar sulcus deep, arched, sides wider than middle. Metanotum conspicuous, metascutellum wide and short, metanotal trough trabeculate, metanotal fovea outlined. Metapectal-propodeal disc polished, metapostnotal median carina incomplete, absent posteriorly, lateral and transverse posterior carinae complete; propodeal spiracle circular, located on lateral surface of propodeum, ventral to lateral carina. Propodeal declivity transversely rugulose, without median carina. Mesopleuron with mesopleural pit large and well defined. Pleurosternum small, triangular, with vertex directed posterad. Prepectus with epicnemial medial projection complete, posterior prepectal flange thick. Wings (Fig. 4F). Forewing with three closed cells (Costal, Radial and First Cubital); pterostigma about 0.24× as wide as long, anterior board outcurved; 2r-rs&Rs sector vein long; Rs&M reaching Sc+R far from pterostigma. Hind wing with one straight hamulus, and four distal hamuli equally distant, and strongly curved. Legs. Profemur swollen, 2.4× as long as wide, apical half of ventral margin serrulate. Metatrochanter (Fig. 5F) without spine. Metafemur (Fig. 5F) with only one proximal acute spine in ventral midline, 0.19× as long as metafemoral width, touching apical margin of metatrochanter.

Metasoma. Weakly longer than mesosoma. Seventh sternite (Fig. 5E) with posterior margin incurved at middle two fifths. Hypopygium (Fig. 5B) with spiculum about as long as median length of hypopygium, and 1.5× longer than anteromedial apodeme, latter slightly curved mesad apically; posterior margin strongly incurved, lateral lobe with conical protuberance. Genitalia (Fig. 5C, D). Harpe shorter than gonostipe; aedeagus wide, 2.26× as long as wide, apex aedeagus posterior to posterior margin of gonostipe, 0.6× as long as gonostipe; basivolsella large, 0.6× as long as gonostipe, basal half about as wide as apical half, basal margin incurved.

Variation

Notauli are more well impressed; metapostnotal median carina slightly longer.

Etymology

The specific epithet refers to the locality (Xinglong Tropical Botanical Garden) where the type specimens were collected.

Material examined

Holotype , male, China: Hainan, Wangning, Xinglong Tropical Botanical Garden, 18°44'24"N, 110°11'38"E, 30.i–30.ii.2021, MT, Zheng Wang, SCAU 3042798 (deposited in SCBG). Paratypes: 2 males. 1 male, China: Hainan, Wangning, Xinglong Tropical Botanical Garden, 18°43'52"N, 110°11'30"E, 18.vii–25.viii.2020, MT, Zheng Wang, SCAU 3042638 (SCBG); same data as holotype, but 9.vi–18.vii.2020, SCAU 3042656 (SCBG).

Distribution

Oriental region, China, Hainan Province.

Remarks

This new species is very similar to F. sharkeyi Savergnini & Azevedo [Thailand], but can be separated from the latter by the following characters: frons almost polished (coriaceous in F. sharkeyi); metapostnotal median carina incomplete, posterior third absent (complete in F. sharkeyi); declivity of propodeum transversely rugulose (areolate-rugose in F. sharkeyi); profemur 2.4× as long as wide (1.2–1.3× in F. sharkeyi).

Foenobethylus yunkaishanensis Chen & Luo, sp. nov.

Figures 6, 7

Diagnosis

Male. Head rectangular and elongate (Fig. 6B). Clypeus with median lobe truncate, median carina incomplete, not reaching anterior clypeal margin, but high and straight in lateral profile. Eye glabrous (Fig. 6B). Distance between posterior margin of compound eye and occipital carina longer than length of compound eye in dorsal view. Notaulus converging posteriorly, almost complete except the apex (Fig. 6C). Metatrochanter without spine (Fig. 7G). Metafemur with acute spine in ventral midline, proximal one 0.35× as long as metafemoral width, touching apical margin of metatrochanter, distal one 0.14× metafemoral width, located on basal two fifth of metafemur (Fig. 7G). Posterior hypopygeal margin strongly incurved, lateral lobe with conical protuberance (Fig. 7E). Basivolsella large, 0.6× as long as gonostipe, basal half distinctly wider than apical half, basal margin incurved (Fig. 7C, D).

Figure 6. 

Foenobethylus yunkaishanensis Chen & Luo, sp. nov., male, holotype (SCAU 3048315) A lateral habitus B head, dorsal view C mesosoma, dorsal view D mesosoma, lateral view E antenna F wings.

Figure 7. 

Foenobethylus yunkaishanensis Chen & Luo, sp. nov., male A, B, G holotype (SCAU 3048315), C–F paratype (SCAU 3042639) A head, ventral view B mesosoma, ventral view C genitalia, dorsal view D genitalia, ventral view E subgenital plate F 7th sternite G metaleg, lateral view.

Description

Male holotype. Body length 3.14 mm. Forewing length 2.08 mm. Colors. Head, mesosoma, metasoma, base of scape, all flagellomeres, apical half of mesotibia and metatibia, all trochanter, and claws dark castaneous; apex of scape, pedicel, palpi, protibia, basal half of mesotibia and metatibia, and tarsi castaneous; wings subhyaline.

Head. Head (Figs 6B, 7A) rectangular and elongate, 1.2× as long as wide. Mandible with five apical sharpened teeth, posterior tooth largest, middle three teeth smaller, anterior tooth smallest. Clypeus with median lobe truncate, median carina incomplete, not reaching anterior clypeal margin, but high and straight in lateral profile. Eye glabrous, almost touching mandible base at anterior corner. Malar space reduced. Frons very weakly coriaceous, almost polished, punctures very sparse and small. WH 0.86× LH. WF 0.61× WH. WF 1.19× HE. OOL 1.20× WOT. Frontal angle of ocellar triangle obtuse. Anterior ocellus far posterior to supra-ocular line. Temple divergent anterad, corner rounded. Vertex badly outcurved. First four antennomeres in ratio of about 21:8:8:7 (Fig. 6E). All flagellomeres distinctly longer than wide, pubescence erect, about 0.67× as long as flagellomeral width. Maxillary palpus with five palpomeres (Fig. 7A). Labial palpus with two palpomeres (Fig. 7A). Occipital carina complete. Medioccipito-genal carina complete. Hypostomal carina thick, almost straight, not angled medially.

Mesosoma (Figs 6C, D, 7B). Mostly polished and weakly coriaceous. Pronotal flange short, exposing propleuron dorsally. Dorsal pronotal area short, without anterior carina strongly progressively narrowing anterad, lateral surface concave. Notaulus converging posteriorly, almost complete except the apex, deep, distinct, and progressively more evident posteriorly. Parapsidal signum sinuous, absent anteriorly. Mesoscutellum shorter than anteromesoscutum. Mesoscutum-mesoscutellar sulcus deep, arched, sides wider than middle. Metanotum conspicuous, metascutellum wide and short, metanotal trough trabeculate, metanotal fovea outlined. Metapectal-propodeal disc polished, metapostnotal median carina incomplete, absent posteriorly, lateral and transverse posterior carinae complete; propodeal spiracle circular, located on lateral surface of propodeum, ventral to lateral carina. Propodeal declivity transverse sculptured, and without median carina. Mesopleuron with mesopleural pit large and well defined. Pleurosternum small, triangular, with vertex directed posterad. Prepectus with epicnemial medial projection complete, posterior prepectal flange thick. Wings (Fig. 6F). Forewing with three closed cells (Costal, Radial and First Cubital); pterostigma about 0.3× as wide as long, anterior board outcurved; 2r-rs&Rs sector vein long; Rs&M reaching Sc+R far from pterostigma. Hind wing with one straight hamulus, and four distal hamuli equally distant, and strongly curved. Legs. Profemur swollen, 2.6× as long as wide, apical half of ventral margin serrulate. Metatrochanter (Fig. 7G) without spine. Metafemur (Fig. 7G) with acute spine in ventral midline, proximal one 0.35× as long as metafemoral width, touching apical margin of metatrochanter, distal one 0.14× metafemoral width, located on basal two fifth of metafemur.

Metasoma. Much longer than mesosoma. Seventh sternite (Fig. 7F) with posterior margin incurved at middle third. Hypopygium (Fig. 7E) with spiculum much longer than median length of hypopygium, and 1.2× longer than anteromedial apodeme, latter distinctly curved mesad apically; posterior margin strongly incurved, lateral lobe with conical protuberance. Genitalia (Fig. 7C, D). Harpe shorter than gonostipe; aedeagus wide, 1.93× as long as wide, apex aedeagus posterior to posterior margin of gonostipe, 0.65× as long as gonostipe; basivolsella large, 0.6× as long as gonostipe, basal half distinctly wider than apical half, basal margin incurved.

Variation

Body size maller and color lighter.

Etymology

The specific epithet refers to the locality (Mt. Yunkaishan) where the type specimens were collected.

Material examined

Holotype , male, China: Guangdong Yunkaishan National Nature Reserve, 1480 m, 22°17'40.72"N, 111°12'37.97"E, 29.v–4.vii.2020, MT, Long-long Chen, SCAU 3048315 (deposited in SCBG). Paratypes: 2 males. 1 male, China: Guangdong Yunkaishan National Nature Reserve, 22°16'22.67"N, 111°11'38.7"E, 30.vi-23.vii.2020, MT, Long-long Chen, SCAU 3042639 (SCBG); 1 male, China: Guangdong Yunkaishan National Nature Reserve, 22°17'40"N, 111°12'37.97"E, 1480 m, 9.v–4.vii.2020, MT, Long-long Chen, SCAU 3042658 (SCBG).

Distribution

Oriental region, China, Guangdong Province.

Remarks

This new species is very similar to F. bidentatus Várkonyi & Polaszek [Brunei, Thailand], but can be separated from the latter by the following characters: distance between posterior margin of compound eye and occipital carina longer length of compound eye in dorsal view (as long as in F. bidentatus); seventh sternum with distal margin strongly emarginated (narrowly emarginated in F. bidentatus); posterior margin of hypopygium strongly incurved (broadly and almost evenly emarginate in F. bidentatus).

Key to males of Foenobethylus

1 Metatrochanter with one ventral spine or tooth 2
Metatrochanter without ventral spine or tooth 5
2 Metafemur with one long proximal spine, 0.5× as long as metafemur width 3
Metafemur with one short proximal spine, 0.6× as long as metafemur width 4
3 Pronotum with anterior horizontal flange medially very narrow; metatrochanter with one needle-like long spine ventrally; metafemur with a ventral oblique furrow F. emiliacasellae Várkonyi & Polaszek
Pronotum with anterior horizontal flange medially as broad as laterally; metatrochanter with one tooth or broad spine; metafemur ventrally flattened, without oblique furrow F. elongatus Várkonyi & Polaszek
4 Hypopygium with posterior margin strongly concave, base of paramere with triangular protuberance on dorsal margin F. pyramidis Savergnini & Azevedo
Hypopygium with posterior margin weakly concave, base of paramere without triangular protuberance on dorsal margin F. thomascokeri Várkonyi & Polaszek
5 Metafemur with one spine 6
Metafemur with two spines 8
6 Middle of metafemur with one small, broad and dentate protuberance ventrally F. gracilis Kieffer
Middle of metafemur without protuberance ventrally 7
7 Frons almost polished; metapostnotal median carina incomplete, posterior third absent; declivity of propodeum transversely rugulose F. xinglongensis Wang & Chen, sp. nov.
Frons coriaceous; metapostnotal median carina complete; declivity of propodeum areolate-rugose F. sharkeyi Savergnini & Azevedo
8 Proximal spine locates at basal 1/3 of metafemora and close to distal spine, and tips of two spines slightly convergent 9
Proximal spine locates on very base of metafemora and distantly separated from distal spine, and tips of two spines almost parallel 10
9 Aedeagus wide, 2.0× as long as wide F. hainanensis Liu, Chen & Xu
Aedeagus narrower, 1.2× as long as wide F. thaianus (Terayama)
10 Distal spine locates before midpoint of metafemora and close to proximal spine 11
Distal spine locates at or after midpoint of metafemora and distanly separated from proximal spine 12
11 Distance between posterior margin of compound eye and occipital carina as long as length of compound eye in dorsal view; seventh sternum with distal margin narrowly emarginated; posterior margin of hypopygium broadly and almost evenly emarginate F. bidentatus Várkonyi & Polaszek
Distance between posterior margin of compound eye and occipital carina longer than length of compound eye in dorsal view; seventh sternum with distal margin strongly emarginated; posterior margin of hypopygium strongly incurved F. yunkaishanensis Chen & Luo, sp. nov.
12 Distal spine obtuse 13
Distal spine acute F. syndesis Chen & Azevedo
13 Lateral lobe of hypopygium without conical protuberance; propodeum polished; pterostigma broad, about 0.4× as wide as long F. robusta Li & Chen, sp. nov.
Lateral lobe of hypopygium with conical protuberance; propodeum coriaceous, areas along metapostnotal median carina rugose; pterostigma relatively slender, about 0.3× as wide as long F. zhejiangensis Liu, Chen & Xu

Discussion

Based on a preliminary phylogenetic analysis using morphological data, Várkonyi and Polaszek (2007) first assigned Foenobethylus to the subfamily Pristocerinae. However, the phylogenetic position of Foenobethylus within Pristocerinae was still unclear in their study. According to Azevedo and Lanes (2007), Afgoiogfa, Foenobethylus and Parascleroderma are closely related genera. However, currently no molecular sequences of Afgoiogfa are available for phylogenetic analysis. From the results of Alencar et al. (2018), the clade of Foenobethylus + Parascleroderma + Cleistepyris was recovered as the sister-group of Apenesia. In the light of the first discovery of Foenobethylus female, Chen and Azevedo (2020) suggested that Foenobethylus might be a synonym under Parascleroderma due the extreme similarity they share in females. Foenobethylus also shares some similar characters with Apenesia and Dissomphalus (Chen and Azevedo 2020), although Dissomphalus was never found close to Foenobethylus in any phylogenetic analyses (Alencar et al. 2018). The molecular data seem to support the relatedness between Foenobethylus and Parascleroderma, as suggested by their similar morphology. In the present study, all of the five studied Foenobethylus species form a monophyletic clade, with Parascleroderma as a sister group (Fig. 1). This result is congruent with that of Alencar et al. (2018), in which Parascleroderma is sister to Foenobethylus. The intergeneric distances between Foenobethylus and Parascleroderma ranged between 14.8–18.6%, generally higher than interspecific distances within Foenobethylus. This high genetic distance suggests that Foenobethylus is likely a distinct genus, as similar intergeneric distances have been found in Epyrinae of Bethylidae (Colombo et al. 2020). However, given that the two Parascleroderma species together with all the Foenobethylus also form a monophyletic group in this study, the possibility that these two genera are synonymous cannot be ruled out. The precise taxonomic delimitation of both genera could be resolved by accumulating molecular data of more Parascleroderma taxa for phylogenetic analyses.

The relatively high interspecific genetic distances (10.3%–13.6%) indicate that the use of DNA barcoding for delimitating morphologically similar species of Foenobethylus may be promising. For example, F. robusta is very similar to F. syndesis, but the genetic distance between them is up to 11.3% and they are well supported as different species. Future comprehensive taxon sampling and molecular analyses should be able to test the power of DNA barcoding in delimitating morphologically similar species.

With the three newly described species, the total number of Foenobethylus is raised from 11 to 14 (Table 3). Species of Foenobethylus mainly occur in tropical forests (Savergnini and Azevedo 2013). All of the three new species described in this study were also collected in tropical or subtropical forests, indicating that species diversity of Foenobethylus from tropical and subtropical forests of Southeast Asia is still undersampled and intensive study is required. The wingless feature of the females allows these parasitoids to adapt to the restricted environments such as tunnels under the tree bark, where the females look for preys (Chen and Azevedo 2020). However, the host of Foenobethylus speices is still unknown. As other members of Pristocerinae, species of Foenobethylus are likely ectoparasitoids of bettle larvae in concealed habitat (Terayama 2006). Searching for wood boring bettle larvae in tropical and subtropical forests should be a promsing direction in finding the hosts of these parasitoids.

Table 3.

List of the world species of Foenobethylus (updated from Chen and Azevedo 2020).

Species Distribution
Country Region
F. bidentatus Várkonyi & Polaszek, 2007 Brunei, Thailand Oriental
F. elongatus Várkonyi & Polaszek, 2007 Malaysia, Indonesia Oriental
F. emiliacasellae Várkonyi & Polaszek, 2007 Thailand Oriental
F. gracilis Kieffer, 1913 Philippines, Thailand Oriental
F. hainanensis Liu, Chen & Xu, 2011 China Oriental
F. pyramidis Savergnini & Azevedo, 2013 Thailand Oriental
F. robusta Li & Chen, sp. nov. China Oriental
F. sharkeyi Savergnini & Azevedo, 2013 Thailand Oriental
F. syndesis Chen & Azevedo, 2020 China Oriental
F. thaianus (Terayama, 1998) Thailand Oriental
F. thomascokeri Várkonyi & Polaszek, 2007 Malaysia, Thailand Oriental
F. xinglongsensis Wang & Chen, sp. nov. China Oriental
F. yunkaishanensis Chen & Luo, sp. nov. China Oriental
F. zhejiangensis Liu, Chen & Xu, 2011 China Oriental

Acknowledgements

Thanks to Dr. Yan-Qiong Peng (Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences) for providing some of the fresh specimens. We thank the subject editor Dr. Michael Ohl and the two reviewers, Dr. Colombo and Dr. Azevedo for their valuable suggestions. This material is based upon work supported in part by the Program of Ministry of Science and Technology of China (2018FY100406), the Foundation of Chengdu Normal University Talent Introduction Research Funding (YJRC202009, No. 111/111158701), and the Agricultural Ecology and Green Food Development Project (CSCXTD2020B11).

References

  • Alencar IDCC, Waichert C, Azevedo CO (2018) Opening Pandora’s box of Pristocerinae: molecular and morphological phylogenies of Apenesia (Hymenoptera, Bethylidae) reveal several hidden genera. Systematic Entomology 43: 481–509. https://doi.org/10.1111/syen.12295
  • Azevedo CO, Lanes GO (2007) Rediscovery of Oriental Foenobethylus Kieffer, 1913 with discussion of allied genus (Hymenoptera, Bethylidae). Mittelugen des Internationalen Entomologischen Vereins 32: 133–141.
  • Chen HY, Azevedo CO (2020) Discovery of a couple of Foenobethylus (Hymenoptera, Bethylidae) in copulation suggests a synonym under Parascleroderma. Journal of Asia-Pacific Entomology 23: 1241–1247. https://doi.org/10.1016/j.aspen.2020.10.001
  • Colombo WD, Waichert C, Azevedo CO (2020) Molecular and morphological species delimitation of Epyrinae (Hymenoptera: Bethylidae) from Papua New Guinea. In: Robillard T, Legendre F, Villemant C, Leponce M (Eds) Insects of Mount Wilhelm, Papua New Guinea – volume 2. Muséum national d’Histoire naturelle, Paris, 209–319.
  • Folmer O, Black M, Hoch W, Lutz R, Vrijenoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.
  • Gillespie JJ, Munro JB, Heraty JM, Yoder MJ, Owen AK, Carmichael AE (2005) A Secondary Structural Model of the 28S rRNA Expansion Segments D2 and D3 for Chalcidoid Wasps (Hymenoptera: Chalcidoidea). Molecular Biology and Evolution 22: 1593–1608. https://doi.org/10.1093/molbev/msi152
  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. https://doi.org/10.1093/molbev/mst010
  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33: 1870–1874. https://doi.org/10.1093/molbev/msw054
  • Liu J, Chen H, Xu Z (2011) Two new species of genus Foenobethylus Kieffer, 1913 (Hymenoptera, Bethylidae) from China with a key to the known species. Zootaxa 2806: 53–59. https://doi.org/10.11646/zootaxa.2806.1.4
  • Savergnini JR, Azevedo CO (2013) Taxonomy of Foenobethylus Kieffer (Hymenoptera, Bethylidae) with description of two new species. Journal of Asia-Pacific Entomology 16: 433–441. https://doi.org/10.1016/j.aspen.2013.06.004
  • Taekul C, Valerio AA, Austin AD, Klompen H, Johnson NF (2014) Molecular phylogeny of telenomine egg parasitoids (Hymenoptera: Platygastridae s.l.: Telenominae): evolution of host shifts and implications for classification. Systematic Entomology 39: 24–35. https://doi.org/10.1111/syen.12032
  • Terayama M (2006) The Insects of Japan. Vol. I, Bethylidae (Hymenoptera). Fukuoka, (Japan): Entomological Society of Japan, 319 pp.