Research Article |
Corresponding author: John M. Heraty ( john.heraty@ucr.edu ) Academic editor: Mark Shaw
© 2020 John M. Heraty, Nokuthula Mbanyana, Simon Van Noort.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Heraty JM, Mbanyana N, Van Noort S (2020) A new species of Eucharissa Westwood (Eucharitidae) from South Africa, with an evaluation of the importance of pupae for assessing relationships in these ant parasitoids. Journal of Hymenoptera Research 79: 43-55. https://doi.org/10.3897/jhr.79.56042
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Eucharissa (Hymenoptera: Eucharitidae) is an enigmatic genus within Chalcidoidea. Adults have at least 16 antennal segments, which is shared only by the closely related genus, Saccharissa, with some species of Eucharissa having as many as 22 antennal segments. At most, other Chalcidoidea have up to 14 segments. Phylogenetic analyses place Eucharissa within the poneromorph-ant attacking clade, but until now, the host and immature stages of this genus were unknown. Eucharissa insolita sp. nov. was discovered in two cocoons of Bothroponera granosa (Ponerinae) from South Africa; one a fully developed male and the other a second-instar larva. The larval exuviae present within the cocoons allowed for description of the life stages and comparison with other members of the poneromorph-attacking clade of Eucharitidae. Morphology of the pupa across Eucharitidae is reviewed, and synapomorphies of the immature stages are identified that support monophyly of the poneromorph-attacking clade within the tribe Eucharitini.
ants, Formicidae, immatures, morphology, parasitism, pupa
Members of the family Eucharitidae are all parasitoids of the immature stages of ants. Their first-instar larvae, planidia, are carried into the ant nest by workers and transfer to the ant larvae where they initially attack and parasitize the host larva, but do not develop until the host pupates (
Features of the pupa have not been used for discussions of phylogenetics in Chalcidoidea. Chalcidoid pupae are exarate, and can usually be grouped into those that are dorsoventrally flattened, as found in many Aphelinidae or Eulophidae or subcylindrical and more typically hymenopteriform as for most other Chalcidoidea (cf.
In Eucharitidae, there can be excessive ornamentation and exaggeration of various structures on the pupa. In some cases the ornamentation is associated with exaggerated features of the adults but, in other cases, they are peculiar only to the pupa. Pupae have been documented in detail for Gollumiellinae: Gollumiella Hedqvist (
Here we describe a new species from this group that was collected within cocoons of Bothroponera Mayr (Ponerinae) in South Africa. The developed adult, exuviae, and immature stages, including the pupa, allowed for an almost complete description of the life history of the parasitoid. We also describe other pupae from genera of Eucharitinae and examine their morphological traits within a phylogenetic context across the family.
Terms for adults follow
This species shares the following features with Eucharissa natalica Westwood: 16 antennal segments, flagellomeres of male with long dorsal rami, absence of a pronounced interantennal process, labrum transverse and hidden behind clypeus, hind tibia with one spur, and head and mesosoma dark blue. The major difference is the presence of basket-like, double-branched rami on all but the last flagellomere. This form of the antenna is most similar to E. stigmatica Westwood (cf.
Male. Length, 5.6 mm. Antenna dark brown; head, mesosoma, coxae, petiole, and most of gaster dark metallic blue; basal two-thirds of femora dark brown to black; apical gastral terga mostly brown; apex of femora, tibiae, and tarsi yellow; wings hyaline, venation brown.
Head 1.7× as broad as high. Frons rugose and covered by long fine setae, vertex bare just lateral to ocelli; vertexal carina sharp and extending laterally to eye margin. Eyes separated by 2.5× their height. Posterior genal margin carinate; malar space 0.8× height of eye and concave. Scrobes broadly impressed, laterally with weak vertical carinae in line with outer torular margin, and single median vertical carina extending to torulus. Toruli separated by a narrow ridge but not noticeably pronounced. Tentorial pits strongly impressed, supraclypeal area not demarked, clypeal region nearly smooth with sparse long setae. Labrum transverse and hidden behind clypeus, ventral margin with 5 tuberculate digits, each with a long seta that extends beyond clypeal margin. Mouthparts reduced, palpi absent. Antenna with 16 segments; scape almost reaching median ocellus; pedicel rounded and smooth; length of flagellum 1.3× height of head, F2 0.4× as long as broad basally, F2 as long as F3, following segments progressively longer along axis, F2–F10 with long paired flattened rami, decreasing in length apically, no distinct clava, F14 spatulate; flagellum pilose; multiporous plate sensilla not apparent.
Mesoscutum rugulose, about as long as broad and covered with long fine decumbent setae; notauli vaguely impressed and reaching transscutal articulation. Mesoscutellum and axilla rugose-areolate; mesoscutellar disc medially impressed and slightly longer than broad, dorsally flat in profile and on same plane as axilla, axillula lacking; frenum separated from mesoscutellum by non-carinate sulcus; entire surface of mesoscutellum with long fine decumbent setae. Propodeum broadly rounded, rugose-areolate, densely setose; propodeal spiracle circular with long narrow ventral excision of propodeum about as long as spiracle diameter. Mesopleuron rugose-areolate, lower mesepimeron mostly bare. Prepectus coarsely rugose-alveolate, upper half slightly swollen, distinguished from pronotum by shallow furrow. Hind coxa mostly smooth and shining, all coxae and femora with long fine setae; protibial spur thin and acuminate; one metatibial spur. Wings subtriangular; fore wing 2.9× as long as broad; venation complete (not interrupted); postmarginal vein 0.4× as long as marginal vein; stigmal vein about twice as long as broad and slightly recurved distally; entire wing with sparse short setae, marginal fringe absent. Hind wing with microsetae and sparse marginal fringe.
Petiole 3.0× as long as broad and 1.7× as long as the hind coxa, smooth with mediolateral patch of long setae, ventrally with thin medial sulcus. Gastral tergites smooth with sparse long recumbent setae and scattered micropunctuations; no tergal scar on Gt1. First gastral sternite (Gs1) smooth without any constriction. Gs9 broadly rounded apically and setose. Aedeagus stout, digitus discoidal with short marginal spines, paramere broad with two apical setae. Cerci absent.
Female. Unknown.
First instar (from exuvium, without head capsule, Fig.
Second instar (Fig.
Pupa (from detached exuvium, antennal exuvium still attached to adult, Figs
Eucharissa insolita sp. nov. 5–8 male: 5 head and mesosoma in place in cocoon 6 adult in place in cocoon 7 exuvium of body and host ant remains 8 exuvium cap from face and antenna, anterior 9 planidial exuvium taken from last-instar larva 10 last instar larva, lateral. Abbreviations: dlp2, dorsolateral process; T, tergum.
South Africa: Mpumalanga: 2km E R532 on God’s Window sideroad, 1495m, 24°54'32"S, 30°51'38"E, 07 Dec 2016, N. Mbanyana & S. van Noort; nest #48 found at the base of a grass tussock with soil and gravel around the entrance; ex Bothroponera granosa (1 ♂, SAM-HYM-P095050); deposited in
One second-instar larva (SAM-HYM-P095052,
From the Latin insolitus for unusual or strange; gender feminine.
Stilbula sp. (Fig.
Material examined. South Africa: Natal: Mzuke Game Res., Mantuma Rest Camp, 27°36'0"S, 32°13'0"E, 7.xii.1986, H.G. Robertson, ex: Camponotus [1♂ adult, 2♀ pupae, 4 larvae, SANC: SANC-HYMC00000245a-g].
Chalcura near polita (Fig.
Material examined. Australia: NSW: Royal N.P., 7.xii.1975, P.S. Ward, ex: Rhytidoponera chalybaea, 1551 [1♂ teneral adult, 4♀ teneral adults, 1♀ pupa, UCRC: UCRCENT00478869–73].
Schizaspidia nasua (Figs
Material examined. West Malaysia: Negri Sembilan: Pasoh Forest Reserve, 2°58'56"N, 102°18'20"E, 24.i.1991, Roscizewski, rotten wood, ex: Odontomachus rixosus [3♂ adults, 1♀ adults, 1? adult, 23♀ pupae, 28♂ pupae, 7? pupae, 5 larvae, 2 planidia, UCRC: UCRCENT00435815–74, UCRCENT00435886, UCRCENT00435890].
Kapala sp. (Figs
Material examined. Ecuador: Galapagos: Isabela Island, Cerro Azul, 4 km E Caleta Iguana, 300m, 0°56'7"S, 91°27'30"W, 24.v.1991, J. Heraty, pampa transition, ex. Odontomachus bauri, H91-060 [1♀ pupa, UCRC: UCRCENT00478868].
11–16 pupae of Eucharitini described herein: 11 Stilbula 12 Chalcura 13–14 Schizaspidia (14 head in dorsal view) 15–16 Kapala: 15 lateral view 16 dorsolateral view 17 characters of immatures mapped onto pruned phylogeny from
The relationships of the genera of Eucharitidae with known pupae, pruned from
Characteristic features of the planidium when compared to other members of the Chalcura, Schizaspidia and Kapala clades (cf.
Pupae of Gollumiellinae and Oraseminae are nearly identical and both lack any ornamentation on the head, but all have 3–4 spherical nodules (3:1, character:state, Fig.
Within Eucharitinae, there are two tribes. Neolosbanus (Psilocharitini) lack any ornamentation of the head or mesosoma and at most have small, sublateral, rounded swellings along metasomal segments 2 and 3 that are similar to those in Oraseminae. Within the Eucharitini, Pseudometagea and members of the Eucharis ‘clade’ (not monophyletic) also lack any ornamentation other than prominent sublateral swellings that come to an acute tip (vlp2) on metasomal tergites 2–4 in some of the species but not all. Within the Stilbula clade, Lophyrocera and Pseudochalcura lack ornamentation; however, Stilbula, as illustrated by
What is remarkable are the seemingly specialized structures that are associated with the poneromorph ant parasitoids as represented by the Chalcura, Schizaspidia, and Kapala clades (Fig.
Within Eucharitidae, immatures can be extremely conserved and can offer valuable insights into the relationships at all levels of the phylogeny (Fig.
Eucharissa is perhaps one of the most unique of the genera in Eucharitidae and even Chalcidoidea, but beyond their phylogenetic placement with molecular data, their highly specialized immature stages and host association provide strong morphological and biological evidence for their evolutionary position within this family of ant parasitoids.
Austin Baker contributed valuable comments on an early draft. We would like to thank Mpumalanga Parks Board provided collecting permits 5158 and 5536. This study was supported by an NRF grant GUN 98115 to SvN, and NSF grants DEB-1257733 and 1555808, and UCR Hatch grants to JMH.