Key to the New World genera of Cardiochilinae (Hymenoptera: Ichneumonoidea: Braconidae) and synopses of the genera
Ilgoo Kang1
,
Michael Sharkey2
1Department of Entomology, Kyungpook National University, Sangju, South Korea, [email protected]
2Hymenoptera Institute, 3028 Arrowhead Dr., Lexington, Kentucky 40503, USA, [email protected]
Key to the New World genera of Cardiochilinae (Hymenoptera: Ichneumonoidea: Braconidae) and synopses of the genera
Key to the New World genera of Cardiochilinae (Hymenoptera: Ichneumonoidea: Braconidae) and synopses of the genera
Ilgoo Kang1
,
Michael Sharkey2
1Department of Entomology, Kyungpook National University, Sangju, South Korea, [email protected]
2Hymenoptera Institute, 3028 Arrowhead Dr., Lexington, Kentucky 40503, USA, [email protected]
Abstract
This is an updated overview of the New World members of Cardiochilinae. It is a revision of the key by Whitfield and Dangerfield (1997). It includes a key to the New World genera and a synopsis of each genus. The synopses include the following sections: diagnosis, biology, diversity, distribution, publications, and notes. Cardiochilinae comprises 18 genera worldwide, with nine occurring in the New World. This study provides an updated overview of New World Cardiochilinae including a resurrected genus, Neocardiochiles Szépligeti, an Old World genus, Bohayella Belokobylskij, recently recorded in the New World, and a recently described genus, Dickyyuella Kang and Sharkey.
Whitfield, J.B. and Dangerfield, P.C. 1997. Subfamily Cardiochilinae. pp. 176-183. In: Wharton RA, Marsh PM, and Sharkey MJ (Eds) Manual of the New World Genera of the Family Braconidae (Hymenoptera). International Society of Hymenopterists, 439 pp.
Introduction
Cardiochilinae is a relatively small subfamily, comprising 18 genera worldwide, nine of which occur in the New World (Table 1). The current work provides a comprehensive overview of the New World genera based on recent discoveries and unpublished data. Significant recent findings in the taxonomy of this subfamily include the resurrection of Neocardiochiles Szépligeti as a valid genus (Kang et al. 2022), the discovery of species of Bohayella Belokobylskij in the New World (Kang et al. 2020b, Kang 2022a) and the description of the new Neotropical genus Dickyyuella Kang and Sharkey (Kang and Sharkey, 2024). Two new genera were recently added to the Old World fauna, Orientocardiochiles Kang and Long (Kang et al. 2020a) and Ophiclypeus Kang (Kang et al. 2023). Schoenlandella Cameron is treated as a junior synonym of Cardiochiles Nees, based on morphological evidence and molecular phylogenetic analyses (Murphy et al. 2008; Kang et al., in prep.). While it was previously recognized as a valid genus by Kang et al. (2021), our results support its inclusion within Cardiochiles. The present work includes a key to the New World genera and a synopsis of each genus. The synopses include the following sections: diagnosis, biology, diversity, distribution, publications, and notes. Images are by Kang or Sharkey. General morphological terminology can be found in Sharkey et al. (2023). More detailed information is in the morphology chapter of the New World manual (Sharkey and Wharton, 1997) and in the Hymenoptera Anatomy Ontology Portal (http://portal.hymao.org/projects/32/public/ontology/).
Overview of the subfamily
Phylogeny
A genus-level phylogeny based on morphological data was provided by Dangerfield et al. (1999). Mercado and Wharton (2003) generated a phylogeny concentrating on the relationships of species of Toxoneuron Say and Retusigaster Dangerfield, Austin, and Whitfield. A genus-level phylogeny of the Heteropteron genus group (Heteropteron, Neocardiochiles, Wesmaelella) based on morphological data was published by Kang et al. (2022).
Biology
All cardiochiline species for which host information exists, are solitary endoparasitoids of lepidopteran larvae. Cardiochiline wasps principally attack caterpillars of Pyraloidea and Noctuidae, including important insect pests such as the tobacco budworm, Chloridea virescens (F.) (previously known as Heliothis virescens) (Chamberlin and Tenhet, 1926; Brazzel et al., 1953), the cotton bollworm, Helicoverpa armigera (Hübner) (Huddleston and Walker 1988), and the melonworm, Diaphania hyalinata (L.) (Marsh, 1986; Smith et al., 1994). The following lepidopteran families also include hosts of Cardiochilinae: Apatelodidae, Cosmopterigidae, Depressariidae, Gelechiidae, and Uraniidae (Huddleston and Walker, 1988; Yu et al., 2016; Dabek et al., 2020).
Cardiochilines oviposit into early instar host larvae. Bracoviruses are also injected, as in the other microgastroid subfamilies, to protect the progeny from the host’s immune system (Vinson and Scott, 1975; Strand and Burke, 2014; Santos et al., 2022; Wang et al., 2023). Adult wasps emerge from late instar caterpillars or pre-pupae (Huddleston and Walker, 1988).
Most cardiochilines attack free-living host caterpillars (Quicke, 2015), although a few species oviposit into concealed caterpillars. For example, members of Cardiochiles tibiator (Say) are recorded as endoparasitoids of the leaf-rollers, Scotia spp. (Marsh, 1979), and members of C. minutus (Cresson) attack leaf-miners, Agnippe sp. and Stilbosis spp. (Lindquist and Bowser, 1966; Marsh, 1979; Whitfield and Wagner, 1991).
Diverse aspects of the biology and ecological importance of Toxoneuron nigriceps (Viereck) (treated as Cardiochiles nigriceps in many studies) have been investigated (Vinson and Lewis, 1965; Vinson, 1969; Vinson, 1972; Vinson and Scott, 1974; Vinson and Scott, 1975; Vinson, 1978; Strand and Vinson, 1982; Stoltz et al., 1984; Davies and Vinson, 1986; Pennacchio et al., 1992; Pennacchio et al., 1993; Pennacchio et al., 1994; Pennacchio et al., 1997; Pennacchio et al., 1998; Varricchio et al., 1999; Pennacchio et al., 2000).
Whitfield and Dangerfield (1997), Quicke (2015), and Dabek et al. (2020) observed that many cardiochilines mimic other hymenopterans, including ichneumonoids, vespids, and pompilids as well as heteropterans.
Common genera
Toxoneuron and Cardiochiles are common in the Nearctic region. In the Neotropics, members of Cardiochiles are both speciose and abundant. Cardiochiles is the most common genus worldwide.
Distribution
Cosmopolitan. As with most braconid subfamilies, cardiochilines are more diverse in tropical areas. In the Nearctic they are more common in the arid southwestern United States.
Distinguishing features
Members of Cardiochilinae can be recognized by the following combination of features: forewing vein 3RSb not tubular and evenly curved (Fig. 2B) or basally angled (Fig. 6B); second submarginal cell of forewing quadrate (Fig. 4B) or pentagonal (Fig. 9B); first metasomal tergite usually with reverse Y-shaped suture (Fig. 2E).
Checklist
Table 1. List of New World genera of Cardiochilinae.
Dickyyuella Kang and Sharkey, 2024
Neocardiochiles Szépligeti, 1908
Key to genera
Generic treatments
Bohayella Belokobylskij, 1987
Diagnosis. Propodeum sculptured with fully developed areola (Fig. 1D). First median tergite more than 4 times longer than wide apically (Fig. 1E). Lateral tergite of first metasomal on same plane as median tergite (couplet 7B, Fig. 1E); second median tergite anteromedially with ball-like projection connected to a socket-like structure of first median tergite in dorsal view (Fig. 1E).
Biology. The hosts of the New World species are unknown. An Oriental species, Bohayella adina (Wilkinson), was reared from the cotton leaf-roller, Phazaca theclata (Guenée) (Uraniidae) (Beeson and Chatterjee, 1935). An Afrotropical species, B. exiguurus (Huddleston and Walker) was reared from the citrus looper, Cleora tulbaghata (Felder & Rogenhofer) (Geometridae) (Dangerfield et al., 1999).
Diversity. Two Costa Rican species, Bohayella geraldinae Kang and B. hansoni Kang, and one Ecuadorian species, B. rodrigodiazi Kang, are described. A few more New World species are likely to be discovered.
Distribution. Neotropical (Costa Rica and Ecuador) and Old World.
Publications. Kang et al. (2020b) and Kang (2022a) described three Neotropical species and provided an identification key.
Cardiochiles Nees, 1819
Diagnosis. Eye obviously setose (couplet 5A, Fig. 2D). Propodeum sculptured with fully developed areola (Fig. 2E). First median tergite less than 3 times longer than wide apically (Fig. 2C). Occipital carina usually absent, never strong. Hypopygium often with median longitudinal fold (Fig.2F). Mouthparts (galea and glossa) variable.
Biology. All reliable host records are on caterpillars of Pyraloidea. Both exposed and concealed host caterpillars are used. Cardiochiles diaphaniae Marsh, a natural enemy of Diaphania hyalinata (L.), was released in Florida as biological control agent (Marsh, 1986).
Diversity. There are approximately 23 described species in the New World. Many more are undescribed.
Distribution. Cosmopolitan.
Publications. Mao (1945) revised the Mexican species of Cardiochiles. Mao (1949) revised species occurring in America North of Mexico. Marsh (1986) described C. diaphaniae Marsh; however, it was transferred to Schoenlandella by Mercado and Wharton (2003). Cardiochiles insculptus Mao and C. minutus Cresson, placed in Schoenlandella by Dangerfield et al. (1999), were reinstated in Cardiochiles by Mercado and Wharton (2003). Mercado and Wharton (2003) reviewed the Mexican species of Cardiochiles and defined several species groups. Kula (2016) reported distribution records of five species of Cardiochiles from Kansas, USA. Kang et al. (2021) described Cardiochiles montserratensis (Kang), as Schoenlandella montserratensis, specimens of which were collected in bitter melon fields in Montserrat and discussed potential host information.
Note. Schoenlandella is treated here as junior synonym of Cardiochiles, following Papp (2014). Phylogenetic analyses based on molecular data (Murphy et al. 2008; Kang et al., in prep.) consistently recovered a well-supported clade in which species of the two genera are intermixed. Morphologically, these taxa share key features, including presence of eye setae and a complete areola on the propodeum. The length of mouthparts, hypopygial structure, and the presence or absence of the spectral 3r crossvein of the forewing vary even among species in the same nominal genus.
Dickyyuella Kang and Sharkey, 2024
Diagnosis. Occipital carina well developed dorsally, absent ventrally (Fig. 3E). Propodeum sculptured with a fully developed areola (Fig. 3E). First median tergite less than three times longer than wide apically (Fig. 3E).
Biology. Unknown.
Diversity. A single specimen of Dickyyuella argentinensis Kang and Sharkey is known.
Distribution. Neotropics (Argentina).
Publications. Kang and Sharkey (2024) erected the genus and described the sole species, Dickyyuella argentinensis. They noted that there is some doubt as to whether or not it belongs in Cardiochilinae.
Hansonia Dangerfield, 1996
Diagnosis. Propodeum sculptured with a fully developed areola (Fig. 4F). First median tergite more than 4 times longer than wide apically (Fig. 4F). Lateral tergite of first metasomal tergum at right angle to median tergite; second median tergite smooth dorsally (Fig. 4F).
Biology. Members of Hansonia chavarriai Dangerfield are solitary endoparasitoids of Hygrochroa firmiana (Stoll) (Lepidoptera: Apatelodidae) (Dangerfield et al., 1996).
Diversity. There are two described species, Hansonia aliciae Mercado and Wharton and H. chavarriai. A few more species will be likely discovered in the Neotropics.
Distribution. Neotropics (Costa Rica and Mexico).
Publications. Dangerfield et al. (1996) described H. chavarriai and included host data. Mercado and Wharton (2003) described H. aliciae Mercado.
Heteropteron Brullé, 1846
Diagnosis. Propodeum entirely smooth (Fig. 5E). Forewing crossvein 1r absent (Fig. 5 B).
Biology. Unknown.
Diversity. Rare. Heteropteron macula Brullé is the only described species. A few more species have been viewed in major museums.
Distribution. Neotropics (Brazil).
Publications. Dangerfield (1995) and Whitfield and Dangerfield (1997) treated Heteropteron, Neocardiochiles, and Wesmaelella as valid genera. Dangerfield et al. (1999) subsumed Neocardiochiles and Wesmaelella into Heteropteron. Mercado and Wharton (2003), Papp (2014), and Dabek et al. (2020) treated Heteropteron and Wesmaelella as valid genera. Kang et al. (2022) generated a new phylogeny based on morphological data to reveal the relationships of the three taxa. Heteropteron was resolved as sister to Neocardiochiles.
Neocardiochiles Szépligeti, 1908
Diagnosis. Propodeum smooth except for a median groove (Fig. 6E). Large colorful specimens.
Biology. Little is known about their biology. Both Neocardiochiles kidonoi (Dabek and Whitfield) and N. hasegawai (Dabek and Whitfield) were reared from lepidopteran larvae (Dabek et al., 2020). Females of N. kidonoi and N. hasegawai (Dabek and Whitfield) are solitary endoparasitoids of Stenoma cathosiota (Lepidoptera: Depressariidae), and Carthara abrupta (Lepidoptera: Pyralidae), respectively. Recently, N. tropicalis Santos Neta & Shimbori was reported as a parasitoid of Stenoma decora Zeller, a major pest of cacao trees (Santos Neta et al., 2025).
Diversity. Ten described species and perhaps ten species are yet to be discovered.
Distribution. Neotropical, known from Mexico to Ecuador.
Publications. See the publications in the Heteropteron treatment above. The detailed history of the definition of Heteropteron-related genera were discussed by Dabek et al. (2020). Species descriptions of five new species are included in Kang et al. (2022).
Retusigaster Dangerfield, Austin and Whitfield, 1999
Diagnosis. Propodeum sculptured with a fully developed areola (Fig.7C). First median tergite less than 3 times longer than wide apically (Fig.7C). Occipital carina usually absent (Fig.7C). Eye apparently lacking setae, some microsetae may be barely perceptible. Apex of hind tibia lacking a flange.
Biology. Cotton (Gossypium sp.; Malvaceae) and Mexican cliffrose (Purshia mexicana (D. Don) S. L. Welsh; Rosaceae) were reported as potential food sources of the hosts of Retusigaster arugosus (Mao, 1949) and R. purshi Kang, respectively.
Diversity. Ten species are recorded worldwide, of which nine occur in the New World. Approximately ten species have yet to be discovered.
Distribution. New World (Honduras, Jamaica, Mexico and USA), Old World (Kazakhstan; Mongolia, Turkey, Turkmenistan).
Publications. Dangerfield et al. (1999) described the genus and included five New World species. Mercado and Wharton (2003) described two new species. Three new species were described by Kang (2022b), and a new illustrated key to species of Retusigaster in the New World was included in the article.
Toxoneuron Say, 1836
Diagnosis. Propodeum sculptured, often with fully developed areola bordered by carinae (Fig. 8C). First median tergite less than 3 times longer than wide apically (Fig. 8C). Occipital carina usually absent (Fig. 8C), weak if present. Eye apparently lacking setae, some microsetae may be barely perceptible. Apex of hind tibia with a flange (couplet 6A).
Biology. Most species of Toxoneuron with known hosts attack Noctuoidea. Many studies have been conducted regarding T. nigriceps (Viereck), which mainly attack the tobacco budworm. T. bicolor (Szépligeti) appears to be host specific on Heliothis zea, one of the major corn pests. Members of T. abdominale Cresson attack Schinia spp. (Peigler and Vinson, 1988).
Diversity. Twenty described species (Yu et al., 2016), and there are probably about that many undescribed in the New World.
Distribution. New World (Colombia, Costa Rica, Cuba, Mexico, USA) and Afrotropical (Ethiopia, Madagascar).
Publications. Dangerfield et al. (1999) included 19 species in the genus. Mercado and Wharton (2000) designated the neotype of T. viator (Say) and compared morphology, host information, and distributions of T. bicolor and T. nigriceps. Mercado and Wharton (2003) transferred Bohayella nigricans (Mao) to Toxoneuron, described T. giganteum Mercado, and defined several species-groups. Kula (2016) provided a distribution record for T. viator for Kansas, USA.
Wesmaelella Spinola, 1851
Diagnosis. Propodeum entirely smooth (Fig. 9C). Forewing crossvein 1r present, in part (Fig. 9B).
Biology. Unknown.
Diversity. Rare. There are two described species, i.e., Wesmaelella nigripennis (Szépligeti) and W. rubricollis (Spinola). Two undescribed species from Paraguay and Peru are deposited in the Naturalis Biodiversity Center in Leiden (Dangerfield 1995).
Distribution. Neotropics (Brazil, Paraguay, and Peru).
Publications. See the publications under the Heteropteron treatment. The detailed history of the definition of Heteropteron-related genera was discussed by Dabek et al. (2020). In the phylogenetic tree based on morphological data by Kang et al. (2022), Wesmaelella was sister to Heteropteron + Neocardiochiles.
Acknowledgements
Thank you to reviewers Jim Whitfield and Jose Fernandez-Triana for their valuable comments and to the editors at CJAI for their dedication. I.K. would also like to thank Dr. Jim Whitfield for providing helpful feedback during his PhD program, which contributed to this work. He is also grateful to Dr. Chris Carlton, Rodrigo Diaz, and Ms. Victoria Bayless for making his PhD program at LSU enjoyable.
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