Research Article
Print
Research Article
First confirmed parasitism of pleasing fungus beetles (Coleoptera, Erotylidae) by a tropical rhyssine ichneumonid, and first record for Cyrtorhyssa moellerii Bingham (Hymenoptera, Ichneumonidae) from Thailand
expand article infoKittipum Chansri, Kanoktip Somsiri§, Donald L. J. Quicke, Buntika A. Butcher
‡ Chulalongkorn University, Bangkok, Thailand
§ Sakaerat Environmental Research Station, Nakhon Ratchasima, Thailand
Open Access

Abstract

The first record of the Darwin wasp, Cyrtorhyssa moellerii Bingham, 1898 (Hymenoptera, Ichneumonoidea, Rhyssinae) from Thailand is presented. Members of both sexes are fully described and illustrated. The biology of C. moellerii, a parasitoid of the pleasing fungus beetle Encaustes opaca Crotch, 1876 (Coleoptera, Erotylidae), is reported for the first time. Hosts were associated with standing deadwood of Anthoshorea henryana (Pierre ex Laness.) P. S. Ashton & J. Heck (Dipterocarpaceae) in dry evergreen forest, Nakhon Ratchasima province, northeastern Thailand. DNA barcodes (cytochrome c oxidase subunit 1 sequence (COI)) were generated for both host and parasitoid and phylogenetic trees constructed for these and other members of the same family and subfamily respectively. A key is provided to separate the three known species of Cyrtorhyssa. This is the first confirmed host record for a tropical species of Rhyssinae as well as the first from Erotylidae.

Keywords

Coleoptera, dead wood, Encaustes, host record, Rhyssinae

Introduction

Rhyssine Darwin wasps (Ichneumonidae) have mostly been recorded as parasitoids of various woodwasps belonging to the families Siricidae, Xiphydridae and the monotypic Anaxyelidae from northwest America (Hanson 1939; Couturier 1949; Quicke 2015). In India and Pakistan, Rhyssa persuasoria himalayensis Wilkinson, 1927 is reported to attack many species of Siricidae (Kamath and Gupta 1972). In Costa Rica, Epirhyssa mexicana Cresson, 1874 have been recorded probing dead wood with cerambycid larvae inside (Gauld 1991), and Porter (1978) also suggested that Neotropical Epirhyssa Cresson, 1865 species were parasitoids of xylophagous beetles but without any definitive records. In China although most hosts records involve siricid woodwasps (Sheng and Sun 2010), there are also several reports of long horn beetles (Cerambycidae) acting as hosts. Moechotypa diphysis (Pascoe, 1871) is reported as being attacked by E. lurida Sheng & Sun, 2010, Rhyssella approximator (Fabricius, 1793) and Triancyra galloisi (Uchida, 1928); Anoplophora glabripennis (Motschulsky, 1854) and Cerambyx cerdo Linnaeus, 1758 are reported to be hosts of Megarhyssa praecellens (Tosquinet, 1889), M. jezoensis (Matsumura, 1912) and R. approximator (Sheng and Sun 2010). Massicus raddei (Blessig & Solsky, 1872) has been recorded as the host of M. praecellens (Cao et al. 2020).

Cyrtorhyssa Baltazar, 1961 is an endemic Asian genus known only from the Indo-Chinese region. It comprises three species: C. moellerii Bingham, 1898 from India (Sikkim) and Myanmar (Tenasserim), C. mesopyrrha Mocsary, 1905 from Indonesia (Sumatra, Java, Kalimantan), Malaysia (Sarawak) and the Philippines (Kamath and Gupta 1972) and C. xishuangensis Wang, 1982 from China (Wang 1982). Up until now, no host records have been reported for any members of the genus.

Only one species of rhyssine wasp has previously been recorded from Thailand, viz Myllenyxis kuchingensis Kamath & Gupta, 1972 (Kamath and Gupta 1972). The record is more than 50 years old and there is no associated biological information. Thus, this discovery of C. moellerii in 2021 is the second officially reported rhyssine wasp from Thailand and the last published information on C. moellerii dates from over a century ago. Here we establish the first host record of C. moellerii which was reared from a particularly large-bodied, wood-boring erotylid beetle (E. opaca). Moreover, this is also the first confirmed case of an erotylid as a host for rhyssine ichneumonids.

Methods

Observation were made in the dry evergreen forest at Sakaerat Environmental Research Station, Nakhon Ratchasima Province, northeastern, Thailand (Fig. 1A). The parasitoid wasps and their host were collected from a standing dead Anthoshorea henryana (Pierre ex Laness.) P. S. Ashton & J. Heck (Dipterocarpaceae) tree (Fig. 1B) during January and February 2021. Adults male and female C. moellerii (Fig. 2A, B) were collected on and around the tree, approximately 0.5–2.0 m above the ground (Fig. 1C, D), and preserved in 95% ethanol. Hosts and their remains were dissected from the wood using a hammer and chisel. Living immature beetles and wasps were also collected and reared in a clear plastic container at room temperature. Morphological terminology follows Broad et al. (2018) except for wing venation which follows Sharkey and Wharton (1997); see also fig. 2.2 in Quicke (2015). We provide the alternative nomenclature in parentheses in the relevant places below. Specimens were imaged using a Leica M205C, Leica DMC5400, Digital Camera, and LAS X software.

Figure 1. 

Dry evergreen forest, Sakaerat Environmental Research Station, Thailand (A), dead wood of A. henryana (B), teneral stage of Encaustes opaca inside the deadwood (C), pupa of C. moellerii inside the deadwood (D).

Figure 2. 

Adult female C. moellerii in the natural habitat (A), male of C. moellerii during tergal stroke behaviour to marking the location of closely emergence female (B), male aggregation be-haviour (C), mating behaviour of female and male C. moellerii in natural habitat (D–F).

DNA barcodes (cytochrome c oxidase subunit 1 sequence, COI) were generated from the wasps and the beetle host legs by the Center for Biodiversity Genomics, University of Guelph, using standard methods (Hebert et al. 2003). Host and parasitoid barcodes, as well as sequence from all available relatives, and close outgroups from GenBank database (National Center for Biotechnology Information [NCBI] (2023)) were assembled for phylogenetic analysis. Details of the sequences used in the analyses are presented in Tables 1, 2, respectively, together with specimen provenances and Genbank Accession Number. For the Ichneumonidae analysis, DNA sequences were available for an additional 27 species of Rhyssinae representing seven genera. In addition, four species of the closely related subfamily Poemeniinae were included as outgroups (Quicke et al. 2009; Spasojevic et al. 2021). For the analysis of Erotylidae, barcodes from 25 other species were available, representing five subfamilies. Members of two genera of Languriidae were included as outgroups (Bocak et al. 2014). Maximum likelihood phylogenic analyses were carried out using RAxML version 8.2.12 (Stamatakis 2006) with a GTRGAMMA substitution model and rapid bootstrap option with 100 randomizations (-f a -# 100). The three-codon position were treated as separated data partitions.

Table 1.

List of rhyssine wasp species, including Thai C. moellerii and outgroups, with their provenance, GenBank Accession Number, and references.

Subfamily Species Provenance GenBank accession No. Reference
Poemeniinae Deuteroxorides elevator Germany JF963193 Quicke et al. 2012
Neoxorides caryae USA MK959447 Bennett et al. 2019
Poemenia albipes Canada MG355017 Dewaard 2017 unpublished
Poemenia hectica Russia MZ627402 Roslin et al. 2022
Rhyssinae Cyrtorhyssa moellerii Thailand OQ272136 present study
Cyrtorhyssa moellerii Thailand OQ272137 present study
Epirhyssa latimandibularis Thailand OQ272138 present study
Epirhyssa corralesi Costa Rica OQ272125
Epirhyssa curtisi Costa Rica OQ272126
Epirhyssa frohbergi Costa Rica OQ272135
Epirhyssa mexicana Costa Rica OQ272133
Epirhyssa oranensis Costa Rica OQ272132
Epirhyssa porteri Costa Rica OQ272131
Epirhyssa praecincta Costa Rica OQ272134
Epirhyssa prolasia Costa Rica OQ272129
Epirhyssa sapporensis South Korea KU753248 Suk and Won 2016 unpublished
Epirhyssa theloides Costa Rica OQ272130
Megarhyssa atrata Canada OQ272127
Megarhyssa greenei USA HM422919 iBOL 2010 unpublished
Megarhyssa nortoni USA KU496775 Sikes et al. 2017
Megarhyssa n. nortoni Canada KR787310 Hebert et al. 2016
Megarhyssa macrura Canada KR929825 Hebert et al. 2016
Myllenyxis sp. Malaysia JF963636 Quicke et al. 2012
Rhyssa amoena Germany JF963813 Quicke et al. 2012
Rhyssa crevieri Canada KR799965 Hebert et al. 2016
Rhyssa howdenorum USA MN556947 Landry and Landry 2019 unpublished
Rhyssa persuasoria Norway OQ272128
Rhyssella humida Canada KM997713 Eagalle 2014
Rhyssella nitida Canada KM996159 Eagalle 2014
Rhyssella furanna Japan MW056244 Spasojevic et al. 2021 9
Rhyssella approximator Finland MZ625985 Roslin et al. 2022
Triancyra galloisi South Korea KU753388 Suk and Won 2016 unpublished
Triancyra tricolorata South Korea KU753389 Suk and Won 2016 unpublished
Table 2.

List of erotylid beetles, including Thai E. opaca and outgroups, with their provenance, GenBank Accession Number and references.

Family Species Provenance GenBank accession No. Reference
Erotylidae Dacne bipustulata Germany HQ954205 iBOL 2011 unpublished
Dacne picta NA KC510126 Cho et al. 2013 unpublished
Dacne quadrimaculata Canada JN288175 iBOL 2011 unpublished
Dacne rufifrons France MN182895 Sire et al. 2019
Dacne sp. France MN182938 Sire et al. 2019
Aulacochilus quadripustulatus NA MN603446 Liu 2019 unpublished
Aulacochilus xingtaiensis NA MN615269 Li 2019 unpublished
Encaustes cruenta ormosana NA MN615271 Li 2019 unpublished
Encaustes opaca Thailand OQ272139 present study
Iphiclus sp. NA KC966646 Cline et al. 2014
Iphiclus sedecimmaculatus NA KP134126 McElrath et al. 2014 unpublished
Episcapha fortunii Japan LC619112 Saito et al. 2021 unpublished
Megalodacne fasciata Canada GU013623 Park et al. 2010
Ischyrus quadripunctatus United States HM433801 iBOL 2010 unpublished
Triplax aenea Finland MZ659828 Roslin et al. 2022
Triplax dissimulator Canada KM843753 Hebert et al. 2014 unpublished
Triplax frosti Canada KR487395 Hebert et al. 2016
Triplax lacordairei France MN182940 Sire et al. 2019
Triplax lepida France KM285906 Rougerie 2014 unpublished
Triplax rufipes Belgium HQ954016 iBOL 2011 unpublished
Triplax russica Poland MH115489 Kolasa et al. 2014 unpublished
Triplax scutellaris Finland MZ631796 Roslin et al. 2022
Triplax thoracica Canada KT706260 Telfer et al. 2015
Tritoma bipustulata Finland KJ964373 Pentinsaari et al. 2014
Tritoma pulchra Canada KR489305 Hebert et al. 2016
Languriidae Acropteroxys gracilis Canada MG059564 Dewaard 2017 unpublished
Languria mozardi mozardi Canada MF635178 deWaard et al. 2019

Results

Parasitoid behaviour

As in many rhyssine wasps, males C. moellerii emerge before females and they can detect where the female will emerge from. Some males were observed performing a tergal stroking behaviour (which is thought to be involved in marking the location of a conspecific that was nearing emergence). Male aggregation behaviour (Fig. 2C, Suppl. material 1) was observed, with some individuals showing aggressive guarding behaviour of their marked location. Mating behaviour was also video-recorded (Fig. 2D, Suppl. material 2). Even though the metasoma of male is not extremely slender, larger males inserted their metasomas into the chewed tunnel of female before her completing emergence process (Fig. 2E, Suppl. material 3). The smaller males that did not insert their metasomas into the wood still waited nearby and tried to mate with females when they exited the tree (Fig. 2F, Suppl. material 4).

Host-parasitoid interaction

The adult host beetles were identified as the pleasing fungus beetles, Encaustes opaca Crotch, 1876 (Coleoptera, Erotylidae) (Fig. 4A–C) (Crotch 1876; Deelder 1942; Chujo 1968b). Of 12 parasitoid wasp cocoons found, seven were empty and had a sub-apical emergence hole (Fig. 3B). The others five cocoons contained living parasitoid pupae. Two of these were opened to allow observation of parasitoid development (Fig. 3A) and three were reared until the wasps (one male and two females) emerged. The captive longevity for the virgin male and two females when fed with 50% honey solution were 14, 16 and 31 days, respectively.

Figure 3. 

Pupa of female C. moellerii (A), empty pupa cocoon of C. moellerii with one emergence hole (B), pupa cocoon of C. moellerii fused with the teneral stage carcass of E. opaca, ventral view (C), lateral view (D).

Figure 4. 

Adult male specimen of E. opaca dorsal view(A), ventral view (B), lateral view (C).

Two C. moellerii cocoons were found firmly attached to dried carcasses of a teneral adult of the host beetle (Fig. 3C, D). We concluded that C. moellerii is at least facultatively able to develop on teneral adults of E. opaca.

Key to species of Cyrtorhyssa

1 Female 2
Male 4
2 Face yellow with a black longitudinal line; frons with a long tapered ridge that is depressed in the center; fore wing areolet absent; ovipositor sheaths 1.3× length of the body C. xishuangensis Wang, 1982
Face all yellow; frons with a median carina and with a semicircular groove around ocellar triangle or a shallow furrow on either side; fore wing areolet present; ovipositor sheaths less than 1.3× length of the body 3
3 Face strongly, transversely striated on its upper 0.6, lower 0.3 coarsely punctate; frons with a median carina and with a semicircular groove around ocellar triangle; clypeus broadly concave at apex; epicnemial carina weakly curved towards anterior edge, about 0.6× height of mesopleuron; propodeum with median longitudinal shallow groove on basal 0.8; fore wing areolet short triangular; abdominal tergites black with broad apical yellow bands; ovipositor sheaths 1.05–1.1× length of the body C. moellerii Bingham, 1898
Face strongly transversely striated on its upper 0.3; frons with a shallow furrow on either side; clypeus strongly concave; epicnemial carina less than 0.5 (0.3) × height of mesopleuron, weakly sinuate; propodeum median longitudinal shallow groove present or absent (if present weakly impressed on basal 0.3–0.5); fore wing areolet widely triangular; first to third abdominal tergites reddish, tergite 2 and 3 without any apical yellow bands; ovipositor sheaths 1–1.2× length of the body C. mesopyrrha Mocsary, 1905
4 Tubercle on metapleuron well developed; fore wing areolet shortly triangular or absent; fifth tergite without any broad transvers apical yellow band C. moellerii Bingham, 1898
Tubercle on metapleuron not so well developed and weak; fore wing areolet present or absent; fifth tergite with a broad transverse apical yellow band C. mesopyrrha Mocsary, 1905

Redescription of Cyrtorhyssa moellerii Bingham, 1898 modified from Kamath and Gupta 1972 (adding male details)

Cyrtorhyssa moellerii

Material examined

Five females, twenty males. Thailand, Nakhon Ratchasima, Wang Nam Khiao district, Udom Sap subdistrict, Sakaerat Environmental Research Station, dry evergreen forest, 14°29.8'N, 101°54.96'E, 496 m, aerial net, col. K. Chansri (CUMZ) (1♀ 27.i.2021, 1♀ 28.i.2021, 2♀ 15.ii.2021, 1♀ 16.ii.2021, 2♂ 21.i.2021, 2♂ 22.i.2021, 2♂ 23.i.2021, 2♂ 24.i.2021, 1♂ 25.i.2021, 1♂ 27.i.2021, 1♂ 29.i.2021, 5♂ 8.ii.2021, 1♂ 15.ii.2021, 3♂ 25.ii.2021).

Diagnosis

Cyrtorhyssa moellerii is clearly different from C. xishuangensis in which face with black longitudinal line. In addition, frons of C. xishuangensis has a tapered ridge rather than distinct carina, and female fore wing has no areolet. Cyrtorhyssa moellerii can be separated from C. mesopyrrha because the fore wing areolet of C. moellerii, when present, is quite short, whereas the fore wing areolet of female C. mesopyrrha is wider (Kamath and Gupta, (1972). The ground colour of tergites 1–3 of female C. moellerii is black with yellow bands, while in female C. mesopyrrha it is reddish without yellow bands.

Description

Female (Figs 5, 6). Body length, mean = 38.0 mm (range = 36.5–39.0 mm); fore wing length, mean = 27.8 (range = 27.0–28.0 mm); ovipositor sheath length, mean = 40.5 mm (range = 40.0–41.0 mm) (Fig. 5A).

Figure 5. 

Light micrograph of female C. moellerii dorsal view of habitus (A), face (B), lateral view of head (C), dorsal view of head (D), lateral view of mesosoma (E).

Figure 6. 

Light micrograph of female C. moellerii dorsal view of mesosoma and propodeum (A), fore wing (B), dorsal view of propodeum (C), lateral view of metasoma (D), dorsal view of metasoma (E), ventral view of metasoma (F), lateral view of ovipositor (G).

Head. Antenna with 40–41 flagellomeres, terminal flagellomere acuminate; face strongly, transversely striated on its upper 0.6, lower 0.3 coarsely punctate, interspaces 0.5 their diameter, towards orbits punctures finer and sparser; clypeus minutely, finely punctate, broadly concave at apex (Fig. 5B); malar space mat, 0.4× basal width of mandible (Fig. 5C); frons smooth, subpolished with a median carina and with a semicircular groove around ocellar triangle bordered laterally by fine striations; vertex with a few scattered punctures, smooth and polished; interocellar distance 0.5 ocello-ocular distance; occiput without a median groove dorsally (Fig. 5D). Occipital carina absent medio-dorsally.

Mesosoma. Mesoscutum coarsely transversely scutellum rugose, notauli meeting approximately 0.4 distance from anterior of mesoscutum; scutellum strongly, coarsely punctate; median area of metanotum smooth and polished (Fig. 6A); mesopleuron sparsely punctate, punctures on lower 0.3 separated by 2‒3× their diameter, epicnemium with more crowded punctures, interspace 0.5‒1.0 their diameter; epicnemial carina weakly curved towards anterior edge, about 0.6 the height of mesopleuron; mesosternum coarsely punctate, punctures sometimes coalescent; metapleuron punctate, interspaces 1‒2× their diameter (Fig. 5E); propodeum largely smooth and polished, with very sparse, minute punctures dorsally, dorsolateral corners and lateral sides shallowly punctate, interspace 4–6× their diameter, broadly depressed at extreme base in middle, and medially with a distinct, shallow groove on basal 0.8 (Fig. 6A, C).

Wing. Areolet of fore wing short triangular, lengths of veins 2RS (=2rs-m): 1M: rs-m (= 3rs-m) = 0.6: 0.8: 1.0; vein 2m-cu joining M interstitial with rs-m (= 3rs-m) (Fig. 6B).

Metasoma. First tergite smooth and shiny 2.1× its apical width; second tergite weakly mat at base, with few scattered punctures; third tergite with basal 0.5 distinctly punctate medially, interspace 0.5‒1× diameter of punctures, rest smoother (Fig. 6C, E); fourth tergite with basal 0.5 coarsely punctate, elsewhere punctures minute, becoming smoother towards apex with moderately dense, brownish pubescence; basal 0.7 of fifth and following tergites punctate, punctures becoming finer on succeeding segments and with dense brownish pubescence (Fig. 6D, E); ovipositor sheath 2.1× the length of fore wing.

Coloration. Black. Face and clypeus yellow, malar area black; mandibles basally reddish-brown with a yellow macula in middle, teeth black; malar space black; temple yellow; frons with two broad lateral spots touching eye margin, median carina on frons yellow; antenna with scape yellowish in front, flagellum dark brown; occiput largely yellow, dorsally black; pronotum, yellow with black band curving from postero-ventral to anterior margin, and anteriorly pointed mediodorsal mark; mesoscutum black with narrow yellow mark alongside notauli medially; tegula, subtegular tubercle and anterior 0.5 of mesopleuron, and metapleuron with posterior 0.6 including tubercle, yellow; axillae yellow, scutellum, with yellow patch antero-medially; metascutellum black except for small yellow spot medio-dorsally; propodeum yellow except extreme dorsolateral corners, spiracular region and extreme apical margin, black; fore legs yellow ventrally from coxa to tibia, coxa dorsally black; middle leg, coxa black with yellow dorsal patch, trochanter black except small dorsal yellow spot, and brownish distal margin, trochantellus black with brownish dorsal part, tibia without apical black, femur black basally, apical 0.3, tibia yellow with dorsal blackish mark on basal 0.5, tarsus black; hind legs as middle leg except trochanter largely yellow, tibia black with medial 0.3 brown-yellow around subgenual organ, femur with narrow longitudinal yellow line except basal 0.1; wings yellowish-hyaline with apical margins infuscate; stigma brownish and vein dark brown; metasomal tergites black with the following yellow: tergite 1 subposterior dorsal patch, tergites 2 and three, complete (except laterally) transverse subposterior band, tergites 4 and 5 with large triangular sub posterior patches, tergite 6 large lozenge-shaped postero-dorsal patch, tergite 7 broad yellow posterior transverse band. Ovipositor sheaths black with reddish tinge.

Male (Figs 7, 8). Body length, mean = 23.9 mm (range = 14.0–32.0 mm); fore wing length, mean = 16.8 mm (range = 11.5–24.0 mm) (Fig. 7A).

Figure 7. 

Light micrograph of male C. moellerii dorsal view of habitus (A), face (B), dorsal view of head (C), lateral view of head (D), lateral view of mesosoma (E), dorsal view of mesosoma and propodeum (F).

Figure 8. 

Light micrograph of male C. moellerii fore wing areolet present morph (A), fore wing areolet absent morph (B), dorsal view of propodeum (C), lateral view of metasoma (D), dorsal view of metasoma (E), ventral view of metasoma (F).

Head. Antennae with 34–41 flagellomeres, terminal flagellomere acuminate; face strongly transversely striated on its upper 0.8, lower 0.2 coarsely punctate, interspaces 0.5 their diameter, towards orbits punctures finer and sparser; clypeus minutely, finely punctate, broadly concave at apex (Fig. 7B); malar space mat, 0.6× basal width of mandible (Fig. 7D); frons smooth, subpolished with a median carina and with a semicircular groove around ocellar triangle, vertex with a few scatter punctures, smooth and polished; interocellar distance 0.5× ocello-ocular distance; occiput without a median groove dorsally (Fig. 7C).

Mesosoma. Scutellum strongly, coarsely punctate; median area of metanotum smooth and polished (Fig. 7F); mesopleuron sparsely punctate, punctures on lower 0.3 separated by 2‒3× their diameter, epicnemium with more crowded punctures, interspace 0.5‒1.0× diameter; epicnemial carina weakly curved towards anterior edge, about 0.5 the height of mesopleuron; mesosternum coarsely punctate, punctures sometime coalescent; metapleuron punctate, interspaces 1‒2× their diameter (Fig. 7E); propodeum largely smooth and polished, with very sparse, minute punctures dorsally, dorsolateral corners and lateral sides shallowly punctate, interspace 4‒6× their diameter, broadly depressed at extreme base in middle, and medially with a distinct, shallow groove on basal 0.8 (Figs 7F, 8C).

Wing. Areolet of fore wing short triangular, length of veins 2RS (=2rs-m): 1-M: rs-m (=3rs-m) = 0.6: 0.8: 1.0 (Fig. 8A) or absent (Fig. 8B); vein 2m-cu joining M interstitial with rs-m (= 3rs-m).

Metasoma. First tergite smooth and shiny 2.0× its apical width (Fig. 8C); second and third tergites smooth and polished with few scattered punctures; fourth tergite with basal 0.2 coarsely punctate, elsewhere punctures minute, becoming smoother towards apex with moderately dense, brownish pubescence; fifth to seventh third tergites smooth and polished with few scattered punctures with dense brownish pubescence (Fig. 8D, E).

Coloration. Yellow. Mandibles basally with brownish and with a yellow macula in middle, teeth black; malar space brownish-yellow; frons with two broad lateral spots touching eye margin, antenna with scape yellowish in front, flagellum dark brown; occiput dorsally brownish; pronotum, yellow with a curved incomplete black band dorsally and with a reddish-brown stripe in centre; median and lateral lobe of mesoscutum reddish-brown, posterior of merging notauli extending into a black midlongitudinal stripe; scutellum largely dull yellow with posterior 0.2 of piceous; median area of metanotum yellow; tegula, epicnemium, posterior transverse carina of mesosternum, juxtacoxal carina black; propodeum yellow except extreme dorsolateral base, spiracular region and extreme apical margin black; Legs yellow with tarsi gradually infuscate towards apex except: fore femur ventrally brown; fore tibia narrowly brown dorsally on basal 0.7, fore; middle leg similar to fore leg except dark mark on femur on medial side; hind coxa ventrally black, hind femur brown-black basally and medioventrally, hind tibia dorsally with basal 0.5 and distal 0.2 posteriorly dark brown; wing yellowish-hyaline with apical margin infuscate, stigma brownish and vein dark brown; metasomal tergites black with yellow marks as follows: tergite 1 with large, sub-posterior yellow patch, tergites 2 and 3 with broad sub-posterior yellow bands, tergite 4 with yellow patches mediolaterally.

Comment

Male and female of the C. moellerii display sexual dimorphism with different colour patterns. Fore wing areolet of female always present according to the keys to species of this genus by Kamath and Gupta, (1972) (Fig. 6B), however, male of C. moellerii shows variation of fore wing areolet, either present of absent (Fig. 8A, B) same as male C. mesopyrrha (Kamath and Gupta 1972).

Phylogenetic analyses

A preliminary molecular phylogeny based on the available DNA barcodes of the rhyssines is shown in Fig. 9. Cyrtorhyssa was recovered as sister group to Myllenyxis but with low bootstrap support (37%), and the two together as derived from within Epirhyssa, with 75% support.

Figure 9. 

Maximum likelihood tree of C. moellerii and other rhyssine wasps based on the barcoding region of cytochrome oxidase subunit 1 (COI) with RaxML rapid bootstrap support values.

The ML phylogeny including the new sequence from the host Encaustes opaca with other available erotylid sequences is shown in Fig. 10. Dacninae, Eucaustinae, Megalodacninae and Trominae+Erotylinae were each recovered as monophyletic with strong bootstrap support (84‒100%). Encaustes opaca was recovered in a polytomy with the only other represented congener Encaustes cruenta formosama, and the genus Aulacochilus, the only other member of Encaustinae included represented by two species (Fig. 10).

Figure 10. 

Maximum likelihood tree of E. opaca (Encaustinae) and other erotylid beetles based on the barcoding region of cytochrome oxidase subunit 1 (COI) with RaxML rapid bootstrap support values.

Discussion

The protandry observed in C. moellerii is similar to what is known for other rhyssine wasps. Most males were observed aggregating in the area where a female was about to emerge (Baker 1992; Eggleton 1991). Tergal stroking behaviour has previously been reported for the males of the genus Megarhyssa (Matthews et al. 1979) and here we report it for the first time in Cyrtorhyssa. Male rhyssines that have long slender metasomas, e.g. Megarhyssa rixator (Schellenberg, 1802), are able to insert their abdomens into the female emergence tunnel for mating (Quicke 2015). However, males of C. moellerii are not so slender. Further, in C. moellerii only the larger males have a sufficiently long metasoma that can be inserted into the emergence tunnel to achieve copulation. The observed adult lifespan of C. moellerii is comparable to that reported for Megarhyssa spp. which can live at least 27 days (Heatwole and Davis 1965).

Our molecular study is the first to include a substantial number of representative rhyssines since Klopfstein et al. (2019), which included representatives of only three genera. In agreement with that study, we recovered Rhyssa as sister group to the remaining included genera (Fig. 9). We recovered Cyrtorhyssa and Myllenyxis as sister groups nested within Epirhyssa, however, additional molecular data would be needed before any conclusions can be drawn about possible non-monophyly of the latter. Both are endemic Asian genera, being known from in India, southern China and both mainland and island of Southeast Asia (Kamath and Gupta 1972; Wang 1972). In contrast, the genera Epirhyssa and Megarhyssa have considerably more cosmopolitan distributions. Myllenyxis is the only genus of Rhyssinae that has the upper tooth of the mandible subdivided thus appearing tridentate. Moreover, fore wing areolet is always present in Megarhyssa and Rhyssella and always absent in Epirhyssa, but some variation in this character is found in males of C. moellerii and C. mesopyrrha.

The host genus Encaustes is widespread in the Old-World tropics and subtropics being reported from Africa, South Asia, East Asia, Southeast Asia to Australia (Chujo 1968a; Chujo 1968b; Chujo 1969; Chujo 1973; Chujo and Chujo 1987; Chujo and Chujo 1988; Chujo et al. 1993). Its distribution completely overlaps that of Cyrtorhyssa. Only two species of Encaustes have been recorded in Thailand previously, E. cruenta montana Schenkling, 1919 and E. opaca Crotch, 1876, both from Chiang Mai province in 1957 (Chujo 1968b; Chujo and Chujo 1988). The relationships between the subfamilies of Erotylidae recovered here using just COI (Fig. 10) are essentially identical to those obtained by Robertson (2004) using combined 16S and 28S data.

Acknowledgements

We are grateful to Mr Surachit Waengsothorn for providing facilities at the Sakaerat Environmental Research Station; Samai Sewakhonburi and Arthit Janthadee for identification of the tree; Sakaerat bird team for collecting insect specimens; and Dr Michael Geiser, The Natural History Museum (London) for confirming identification of the beetle. We also thank Shen-Horn Yen (National Sun Yat-sen University, Taiwan) and Zhipang Huang (Insitute of Eastern-Himalaya Biodiversity Research) for help with literature. This research was funded by National Research Council of Thailand (NRCT) (N42A650262) and Chulalongkorn University, RSPG-Chula to BAB; DLJQ was supported by Rachadaphiseksomphot Fund, Graduate School, Chulalongkorn University; KC was supported by CU Graduate School Thesis Grant (GCUGR1225641025D), the Overseas Research Experience Scholarship for Graduate Student from CU Graduate School and Faculty of Science; and The Second Century Fund (C2F), Chulalongkorn University.

References

  • Baker BR (1992) Emergence and pairing of Rhyssa persuasoria L. (Hymenoptera: Ichneumonidae). British Journal of Entomology and Natural History 5: 184–185.
  • Bennett AMR, Cardinal S, Gauld ID, Wahl DB (2019) Phylogeny of the subfamilies of Ichneumonidae (Hymenoptera). Journal of Hymenoptera Research 71: 1–156. https://doi.org/10.3897/jhr.71.32375
  • Bocak L, Barton C, Crampton‐Platt ALEX, Chesters D, Ahrens D, Vogler AP (2014) Building the Coleoptera tree‐of‐life for> 8000 species: composition of public DNA data and fit with Linnaean classification. Systematic Entomology 39: 97–110. https://doi.org/10.1111/syen.12037
  • Broad G, Shaw M, Fitton M (2018) The Ichneumonid Wasps of Britain and Ireland (Hymenoptera: Ichneumonidae). Royal Entomological Society, Telford.
  • Cao LM, Achterberg CV, Tang YL, Wang XY, Yang ZQ (2020) Revision of parasitoids of Massicus raddei (Blessig Solsky) (Coleoptera, Cerambycidae) in China, with one new species and genus. Zootaxa 4881: 104–130. https://doi.org/10.11646/zootaxa.4881.1.7
  • Chujo M (1968a) Erotylid beetles from south-China, Hainan, Taiwan and the Ryukyus. Studies on the erotylid beetles (20). Pacific Insects 10: 539–550.
  • Chujo M (1968b) Erotylid beetles from Thailand, Laos and Viet-Nam. Studies on the erotylid beetles (21). Pacific Insects 10: 551–573.
  • Chujo M (1969) Erotylidae (Insecta: Coleoptera). Fauna Japonica, Insecta Coleoptera Erotylidae. Academic Press of Japan, Tokyo.
  • Chujo M (1973) Coleoptera: Erotylidae and Languriidae from Ceylon. Entomologica Scandinavica. Supplementum 4: 195–198.
  • Chujo M, Chujo M (1987) Erotylidae from New Guinea and her adjacent islands I (Coleoptera). Esakia 25: 5–36. https://doi.org/10.5109/2492
  • Chujo M, Chujo M (1988) A catalog of the Erotylidae (Insecta, Coleoptera) from the Old World (excl. the Ethiopian Region). Esakia 26: 139–185. https://doi.org/10.5109/2510
  • Cline AR, Smith TR, Miller K, Moulton M, Whiting M, Audisio P (2014) Molecular phylogeny of Nitidulidae: assessment of subfamilial and tribal classification and formalization of the family Cybocephalidae (Coleoptera: Cucujoidea). Systematic Entomology 39: 758–772. https://doi.org/10.1111/syen.12084
  • Couturier A (1949) Observations sur Rhyssa approximator F. cleptoparasite de Rh. persuasoria L. (Hym. Ichneumonidae). Bulletin de la Société Entomologique de France 54: 62–63. https://doi.org/10.3406/bsef.1949.18366
  • Crotch GR (1876) A revision of the coleopterous family Erotylidae. Cistula Entomologica [1869–1876]: 359–572.
  • Deelder CL (1942) Revision of the Erotylidae (Coleoptera) of the Leiden Museum. Zoologische Mededelingen 24: 49–115.
  • DeWaard JR, Ratnasingham S, Zakharov EV, Borisenko AV, Steinke D, Telfer AC, Perez KH, Sones JE, Young MR, Levesque-Beaudin V, Sobel CN (2019) A reference library for Canadian invertebrates with 1.5 million barcodes, voucher specimens, and DNA samples. Scientific data 6: 1–12. https://doi.org/10.1038/s41597-019-0320-2
  • Eagalle T (2014) Latitudinal Effects on Diversity and Body Size: A Case Study with Parasitoid and Parasitic Wasps. Unpublished Ph.D. thesis, University of Guelph.
  • Heatwole H, Davis DM (1965) Ecology of three sympatric species of parasitic insects of the genus Megarhyssa (Hymenoptera: Ichneumonidae). Ecology 46: 140–150. https://doi.org/10.2307/1935265
  • Hebert PDN, Cywinska A, Ball SL, DeWaard JR (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London, Series B: Biological Science 270(suppl_1): S96–S99. https://doi.org/10.1098/rsbl.2003.0025
  • Hebert PDN, Ratnasingham S, Zakharov EV, Telfer AC, Levesque-Beaudin V, Milton MA, Pedersen S, Jannetta P, DeWaard JR (2016) Counting animal species with DNA barcodes: Canadian insects. Philosophical Transactions of the Royal Society B: Biological Sciences 371: e20150333. https://doi.org/10.1098/rstb.2015.0333
  • Kamath MK, Gupta VK (1972) Ichneumonologia Orientalis, Part II. The Tribe Rhyssini (Hymenoptera: Ichneumonidae). Oriental Insects Monographs 2: 1–300.
  • Klopfstein S, Langille B, Spasojevic T, Broad GR, Cooper SJ, Austin AD, Niehuis O (2019) Hybrid capture data unravel a rapid radiation of pimpliform parasitoid wasps (Hymenoptera: Ichneumonidae: Pimpliformes). Systematic Entomology 44: 361–383. https://doi.org/10.1111/syen.12333
  • Matthews RW, Matthews JR, Crankshaw O (1979) Aggregation in male parasitic wasps of the genus Megarhyssa: I. Sexual discrimination, tergal stroking behavior, and description of associated anal structures. The Florida Entomologist 62: 3–8. https://doi.org/10.2307/3494037
  • National Center for Biotechnology Information [NCBI] (2023) [Internet]. Bethesda (MD): National Library of Medicine (US), National Center for Biotechnology Information; [1988] – [cited 2023 Sep 14]. https://www.ncbi.nlm.nih.gov/
  • Park DS, Suh SJ, Oh HW, Hebert PDN (2010) Recovery of the mitochondrial COI barcode region in diverse Hexapoda through tRNA-based primers. BMC Genomics 11: 1–7. https://doi.org/10.1186/1471-2164-11-423
  • Pentinsaari M, Hebert PDN, Mutanen M (2014) Barcoding beetles: a regional survey of 1872 species reveals high identification success and unusually deep interspecific divergences. PLoS ONE 9: e108651. https://doi.org/10.1371/journal.pone.0108651
  • Porter CC (1978) A revision of the genus Epirhyssa (Hymenoptera: Ichneumonidae). Studia Entomologia 20: 297–411.
  • Quicke DLJ (2015) The Braconid and Ichneumonid Parasitic Wasps: Biology, Systematics, Evolution and Ecology. Wiley Blackwell, Chichester, 681 pp. https://doi.org/10.1002/9781118907085
  • Quicke DLJ, Laurenne NM, Fitton MG, Broad GR (2009) A thousand and one wasps: a 28S rDNA and morphological phylogeny of the Ichneumonidae (Insecta: Hymenoptera) with an investigation into alignment parameter space and elision. Journal of Natural History 43: 1305–1421. https://doi.org/10.1080/00222930902807783
  • Quicke DLJ, Smith MA, Janzen DH, Hallwachs W, Fernandez-Triana J, Laurenne NM, Zaldivar-Riveron A, Shaw MR, Broad GR, Klopfstein S, Shaw SR, Hrcek J, Hebert PD, Miller SE, Rodriguez JJ, Whitfield JB, Sharkey MJ, Sharanowski BJ, Jussila R, Gauld ID, Chesters D, Vogler AP (2012) Utility of the DNA barcoding gene fragment for parasitic wasp phylogeny (Hymenoptera: Ichneumonoidea): data release and new measure of taxonomic congruence. Molecular Ecology Resources 12: 676–685. https://doi.org/10.1111/j.1755-0998.2012.03143.x
  • Robertson JA, McHugh JV, Whiting MF (2004) A molecular phylogenetic analysis of the pleasing fungus beetles (Coleoptera: Erotylidae): evolution of colour patterns, gregariousness and mycophagy. Systematic Entomology 29: 173–187. https://doi.org/10.1111/j.0307-6970.2004.00242.x
  • Roslin T, Somervuo P, Pentinsaari M, Hebert PD, Agda J, Ahlroth P, Anttonen P, Aspi J, Blagoev G, Blanco S, Chan D 2022. A molecular‐based identification resource for the arthropods of Finland. Molecular Ecology Resources 22: 803–822. https://doi.org/10.1111/1755-0998.13510
  • Sharkey MJ, Wharton RA (1997) Morphology and terminology. In: Wharton RA, Marsh PM, Sharkey MJ (Eds) Identification manual to the New World genera of Braconidae. Special Publication of the International Society of Hymenopterists 1: 19–37.
  • Sheng ML, Sun SP (2010) Parasitic Ichneumonids on Woodborers in China (Hymenoptera: Ichneumonidae). Science Press, Beijing, 338 pp. [in Chinese with English summary]
  • Sikes DS, Bowser M, Morton JM, Bickford C, Meierotto S, Hildebrandt K (2017) Building a DNA barcode library of Alaska’s non-marine arthropods. Genome 60: 248–259. https://doi.org/10.1139/gen-2015-0203
  • Sire L, Gey D, Debruyne R, Noblecourt T, Soldati F, Barnouin T, Parmain G, Bouget C, Lopez-Vaamonde C, Rougerie R (2019) The challenge of DNA barcoding saproxylic beetles in natural history collections–exploring the potential of parallel multiplex sequencing with Illumina MiSeq. Frontiers in Ecology and Evolution 7: e495. https://doi.org/10.3389/fevo.2019.00495
  • Spasojevic T, Broad GR, Sääksjärvi IE, Schwarz M, Ito M, Korenko S, Klopfstein S (2021) Mind the outgroup and bare branches in total-evidence dating: a case study of pimpliform Darwin wasps (Hymenoptera, Ichneumonidae). Systematic Biology 70: 322–339. https://doi.org/10.1093/sysbio/syaa079
  • Telfer AC, Young MR, Quinn J, Perez K, Sobel CN, Sones JE, Levesque-Beaudin V, Derbyshire R, Fernandez-Triana J, Rougerie R, Thevanayagam A (2015) Biodiversity inventories in high gear: DNA barcoding facilitates a rapid biotic survey of a temperate nature reserve. Biodiversity Data Journal 3: e6313. https://doi.org/10.3897/BDJ.3.e6313
  • Wang SF (1982) A new species of the genus Cyrtorhyssa (Ichneumonidae: Ephialtinae). Sinozoologia 2: 59–60. [in Chinese with English summary]

Supplementary materials

Supplementary material 1 

Video Online Resource 1

Kittipum Chansri, Kanoktip Somsiri, Donald L. J. Quicke, Buntika A. Butcher

Data type: mp4

Explanation note: Tergal stroking behaviour of male Cyrtorhyssa moellerii.

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Download file (23.97 MB)
Supplementary material 2 

Video Online Resource 3

Kittipum Chansri, Kanoktip Somsiri, Donald L. J. Quicke, Buntika A. Butcher

Data type: mp4

Explanation note: Aggressive guarding behaviour of male Cyrtorhyssa moellerii.

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Download file (42.89 MB)
Supplementary material 3 

Video Online Resource 2

Kittipum Chansri, Kanoktip Somsiri, Donald L. J. Quicke, Buntika A. Butcher

Data type: mp4

Explanation note: Mating behaviour of male Cyrtorhyssa moellerii.

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Download file (24.89 MB)
Supplementary material 4 

Video Online Resource 4

Kittipum Chansri, Kanoktip Somsiri, Donald L. J. Quicke, Buntika A. Butcher

Data type: mp4

Explanation note: Emergence of female Cyrtorhyssa moellerii.

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Download file (57.92 MB)
login to comment