Come and Gone: Description of a New Species of Eucharitidae (Hymenoptera) Attacking Solenopsis (Hymenoptera: Formicidae) in Texas

Come and Gone: Description of a New Species of Eucharitidae (Hymenoptera) Attacking Solenopsis... Abstract Eucharitidae (Hymenoptera: Chalcidoidea) are the only family in which all members are specialized parasitoids of ant brood, with species of Orasema Cameron (Oraseminae) parasitizing several genera of Myrmicinae, including Solenopsis Westwood and Pheidole Westwood (Formicidae). In 1988, a new species of Orasema was discovered in southern Texas attacking the brood of what is recognized as a Solenopsis geminata (Fabricius) (Hymenoptera: Formicidae) × Solenopsis xyloni McCook (Hymenoptera: Formicidae) hybrid. Adults of Orasema oviposit onto the green stems and leaves of Vachellia sp. (Fabaceae). Orasema taii n. sp. was only found attacking the hybrid colonies and was not recovered from adjacent nests of Solenopsis invicta Buren (Hymenoptera: Formicidae), which at that time were equally abundant in the area. Wasps were abundant at the time of collection, but since these initial collections, the parasitoids have not been recovered. Hybrid populations have declined precipitously with the invasion of the imported fire ant, and both the hybrid and parasitoid may have been extirpated at least from the area of discovery. Based on morphological and molecular evidence, O. taii n. sp. is placed into the Orasema bakeri species group. The adult and immature stages and their behavior in the field are described. Since its introduction into the United States in the 1930s, the red imported fire ant (RIFA), Solenopsis invicta Buren (Hymenoptera: Formicidae), has been shown to have a negative impact on the biodiversity and abundance of native ant species (Wilson and Brown 1958; Porter and Savignano 1990; Morrison 2000; Hill et al. 2013; but see Tschinkel and King 2017). In Texas, two species of Solenopsis considered as ecological homologues, Solenopsis geminata (Fabricius) (Hymenoptera: Formicidae) and Solenopsis xyloni McCook (Hymenoptera: Formicidae), as well as a common hybrid form, S. geminata × xyloni, were common before the RIFA invasion (Hung and Vinson 1977; Morrison 2000; Cahan and Vinson 2003). Habitat effects are one factor known to affect competitive interactions between the different species of Solenopsis, but although interactions were initially devastating, these effects have allowed for some populations of native Solenopsis, including the hybrid, to survive in Texas albeit in much lower numbers (LeBrun et al. 2012). The impact of parasitoids has been studied to some degree with the greatest emphasis on Pseudacteon phorid flies (Plowes et al. 2009) and less so Caenocholax strepsipterans (Cook et al. 1997). Parasitism of any of these ants in the Solenopsis saevissima complex (or geminata group sensuTrager 1991) in the United States by a eucharitid wasp has never been documented. Orasema Cameron (Eucharitidae: Oraseminae) belongs to a diverse family of specialized ant-parasitoids (Heraty 2000, 2002). Immatures parasitize the brood of the ant subfamily Myrmicinae, first by attacking the host larva and then completing their development on the pupa (Heraty et al. 1993; Heraty 1994a, b, 2000; Varone and Briano 2009; Varone et al. 2010; Herreid and Heraty 2017). Eggs are deposited away from the host into plant tissue using an expanded ovipositor, and first instars (termed planidia) then gain access to the host nest by phoretic attachment to the host ant or through attachment to an intermediate host such as thrips (Heraty 2000; Herreid and Heraty 2017). Parasitism of Solenopsis is relatively uncommon in the genus. The Orasema xanthopus species group is the only clade known to specialize on fire ants in the S. saevissima complex, but their distribution is restricted to South America (Wojcik et al. 1987; Heraty et al. 1993; Varone et al. 2010). Orasema sixaolae Wheeler & Wheeler has been reared from Solenopsis tenuis Mayr in Costa Rica (Wheeler and Wheeler 1937). Orasema coloradensis Wheeler was reared from both Pheidole bicarinata Forel and Solenopsis molesta validiscula Emery in Colorado and Texas (Wheeler 1907), and has been associated with, but not reared from Formica in Idaho (Johnson et al. 1986). No species have been reported attacking S. saevissima complex species in North America. We describe below a new species of Orasema that at the time of collection was an abundant parasitoid of the S. geminata × xyloni hybrid in Texas, but has never since been rediscovered. The Solenopsis hybrid has been largely excluded across its original range by RIFA; however, the hybrid continues to be found in low numbers in southern Texas, representing less than 8 percent of the total ant population (Plowes et al. 2009; LeBrun et al. 2012). Thus, it is possible that the parasitoid may yet be found again. The behavior of the parasitoids suggests that they are very host specific, and parasitoid pressure on the hybrid may have enhanced their competitive disadvantage. Orasema taii n. sp. is described herein along with its immature stages and its oviposition and within-nest behavior. It is placed in the Orasema bakeri group, which includes an undescribed species known to parasitize Pheidole and Tetramorium (Heraty 1994b, unpublished data). We extensively annotate the morphology of adult female Orasema in an attempt to standardize the morphological terminology being applied to the genus and Eucharitidae in general. Materials and Methods Specimens examined are housed at Texas A&M University, College Station, TX (TAMU) and at the University of California, Riverside, CA (UCRC). All specimens are identified with unique UCRC specimen identifiers that also refer to the museum of deposition. Geographic coordinates estimated from Google Earth are in italics. Morphological terminology and measurements follow Heraty (2000) and Burks et al. (2017). Abbreviations of morphological terms are listed in Table 1. All specimens were measured with Zeiss Stemi SV6 and 16× eyepiece. Images were taken using a Leica Imaging System with a Z16 APO A microscope and stacked using Zerene Stacker (version 1.04, Zerene systems, LLC). Original images were uploaded to Figshare (figshare.com/account/home#/projects/26533). Table 1. List of abbreviations 1-2vf  1st-2nd valvifers  1-3vv  1st-3rd valvulae  Acst  acrosternite  Acs  antecostal sulcus  Acy  anteclypeus  Anl  anellus (flagellomere 1)  Anr  antennal rim  Apc  anterior transverse petiolar carina  Ax  axilla  Axl  axillula  Cal  propodeal callus  Cc  costal cell  cx1-3  pro-, meso-, metacoxa  dr1  dorsal ramus  Esg  epistomal groove  F1-9  flagellomeres  f2-3p  meso- and metafurcal pit  Fra  frenal arm  Frn  frenum  Gt1  first gastral tergum  Lb  laminated bridge of ovipositor  Lcl  lateral clypeal line  lep2  lower mesepimeron  les2  lower mespisternum  Llm  lateral lobe of mesoscutum  Lmd  left mandible  Lpa  lateral panel of axilla  Mlm  median lobe of mesoscutum  Mps  multiporous plate sensillum  mr1-3  mandibular rods 1-3  Mrm  marginal rim of mesoscutellum  Msd  median scrobal depression  Mts  metascutellum  Mtsa  metascutellar arm  Mv  marginal vein  no1  pronotum  no3  metanotum  Not  notaulus  Pa  paratergite  Paa  pars articularis  Ped  pedicel  Pet  petiole  Pmu  processus muscularis  Pmv  postmarginal vein  Pre  prepectus  Prp  propodeum  Pss  postspiracular sulcus  Rad  radicle  Rmd  right mandible  Sas  subantennal sulcus  Scd  mesoscutellar disc  Scp  scape  Scr  antennal scrobe  Smv  submarginal vein  Spa  sensillar patch of 2nd valvifer  Sss  scutoscutellar suture  Stv  stigmal vein  Tgl  tegula  Tor  torulus  Tpl  tergopleural line  Tsa  transscutal articulation  uep2  upper mesepimeron  ues2  upper mesepisternum  1-2vf  1st-2nd valvifers  1-3vv  1st-3rd valvulae  Acst  acrosternite  Acs  antecostal sulcus  Acy  anteclypeus  Anl  anellus (flagellomere 1)  Anr  antennal rim  Apc  anterior transverse petiolar carina  Ax  axilla  Axl  axillula  Cal  propodeal callus  Cc  costal cell  cx1-3  pro-, meso-, metacoxa  dr1  dorsal ramus  Esg  epistomal groove  F1-9  flagellomeres  f2-3p  meso- and metafurcal pit  Fra  frenal arm  Frn  frenum  Gt1  first gastral tergum  Lb  laminated bridge of ovipositor  Lcl  lateral clypeal line  lep2  lower mesepimeron  les2  lower mespisternum  Llm  lateral lobe of mesoscutum  Lmd  left mandible  Lpa  lateral panel of axilla  Mlm  median lobe of mesoscutum  Mps  multiporous plate sensillum  mr1-3  mandibular rods 1-3  Mrm  marginal rim of mesoscutellum  Msd  median scrobal depression  Mts  metascutellum  Mtsa  metascutellar arm  Mv  marginal vein  no1  pronotum  no3  metanotum  Not  notaulus  Pa  paratergite  Paa  pars articularis  Ped  pedicel  Pet  petiole  Pmu  processus muscularis  Pmv  postmarginal vein  Pre  prepectus  Prp  propodeum  Pss  postspiracular sulcus  Rad  radicle  Rmd  right mandible  Sas  subantennal sulcus  Scd  mesoscutellar disc  Scp  scape  Scr  antennal scrobe  Smv  submarginal vein  Spa  sensillar patch of 2nd valvifer  Sss  scutoscutellar suture  Stv  stigmal vein  Tgl  tegula  Tor  torulus  Tpl  tergopleural line  Tsa  transscutal articulation  uep2  upper mesepimeron  ues2  upper mesepisternum  View Large Nomenclature This paper and the nomenclatural act(s) it contains have been registered in Zoobank (www.zoobank.org), the official register of the International Commission on Zoological Nomenclature. The LSID (Life Science Identifier) number of the publication is urn:lsid:zoobank.org:pub:F0E644BE-548F-4BB3-9DCA-B7886A3F4012 Orasema taii n. sp. (Figs 1–23) (http://zoobank.org/urn:lsid:zoobank.org:act:DA294E6D-76C6- 4BFC-AFCE-D8EDECBF4C53) Diagnosis Species in the bakeri group are recognized by having seven funicular segments, the prepectus without a carina along the anterior margin, the femora are mostly dark brown, and the petiole in females is only slightly longer than broad (in males up to 2.5× as long as broad). The new species is distinguished from other members of the group (O. bakeri Gahan, Orasema texana Gahan) by the following combination of features: clava with a distinct ventral notch separating two apical clavomeres; mesoscutellar disc between frenal line and axillae distinctly longer than broad and with a central median channel that is a more coppery colored than the surrounding dark blue–green frenum; and petiole with a weak anterior carina, no lateral carina, and strongly rugose. The clava is a single completely fused structure in all other bakeri-group species. O. bakeri has reticulate sculpture on the dorsal surface of the petiole, whereas O. taii has areolate-reticulate sculpture (Fig. 12). O. texana Gahan has the mesoscutellar disc between the frenal line and axillae at most as long as broad, scabriculous (not evenly fine reticulate) sculpture dorsally, petiole with dorsal surface relatively flat and reticulate, and in females, it has a prominent dorsolateral carinae that extends the full length of the petiole. Female: Length 2.37–3.05 mm. Color: Head and mesosoma blue green, mesosoma more greenish dorsally and mostly dark blue laterally (Figs. 10 and 11). Scape pale brown; pedicel brown; anellus yellowish brown; flagellum dark brown. Mandible, maxilla, and labium dark brown. Coxae dark blue; femora mostly dark brown to black, tips pale; tibiae yellow. Fore wing hyaline; venation pale brown. Petiole dark blue; gaster brown. Head: Head in frontal view subtriangular (Fig. 3); 1.14–1.26× broader than high; face reticulate. Occiput strigate, shallowly emarginate in dorsal view, dorsal margin abrupt; temple present, rounded. Scrobal depression shallow, laterally rounded, reticulate, dorsal scrobal depressions absent; longitudinal groove between eye and torulus absent; eye sparsely setose, appearing bare; interocular distance 1.59–1.88× eye height; malar space 0.74–0.96× eye height; malar depression weakly impressed between mouth and eye margin; supraclypeal area about as long as broad, shorter than clypeus, weakly sculptured; clypeus strongly sculptured; epistomal sulcus narrow but shallow; anterior tentorial pits shallow; anteclypeus distinct, straight. Labrum with four digits (Fig. 3). Mandibular formula 3:2 (Figs. 3 and 9); palpal formula 3:2. Scape not reaching median ocellus. Pedicel small and globose. Flagellum with seven funicular segments (Fig. 1, F2–8); flagellum length 0.96–1.1× head height; anellus disc-shaped; F2 1–1.33× as long as broad, 0.85–1.06× as long as F3; following funicular segments subequal in length, equal in width; clava subconical, with notch ventrally between first and second subsegments. Figs. 1–7. View largeDownload slide Orasema taii, female. (1) Antenna (lateral). (2) Flagellomeres F1–3 (lateral). (3) Head (anterior). (4) Mesosoma (lateral). (5) Mesosoma (oblique posterior). (6) Petiole and acrosternite (lateral). (7) Mesosoma and petiole (ventral). Figs. 1–7. View largeDownload slide Orasema taii, female. (1) Antenna (lateral). (2) Flagellomeres F1–3 (lateral). (3) Head (anterior). (4) Mesosoma (lateral). (5) Mesosoma (oblique posterior). (6) Petiole and acrosternite (lateral). (7) Mesosoma and petiole (ventral). Figs. 8–13. View largeDownload slide Orasema taii, female. (8) Apex of antenna (lateral). (9) Mandibles (posterior). (10) Mesosoma (lateral). (11) Mesosoma (dorsal). (12) Petiole (dorsal). (13) Fore wing. Figs. 8–13. View largeDownload slide Orasema taii, female. (8) Apex of antenna (lateral). (9) Mandibles (posterior). (10) Mesosoma (lateral). (11) Mesosoma (dorsal). (12) Petiole (dorsal). (13) Fore wing. Mesosoma: Mesosoma 1.08–1.23× as long as high (Figs. 4 and 10). Mesoscutal midlobe reticulate medially to rugose-reticulate laterally, with minute setae; lateral lobe strigose medially, to longitudinally reticulate laterally; notaulus deep (Fig. 11, not). Axilla reticulate medially to rugose-reticulate laterally, dorsally elevated well above scutellum (Figs. 4 and 10); scutoscutellar sulcus narrow, regularly foveate, extending to transscutal articulation medially, axilla broadly divided (Fig. 11, ax); scutellar disc slightly longer than broad, finely reticulate medially; frenal line reticulate; frenum reticulate; axillular sulcus anteriorly narrow, broad and foveate posteriorly; axillula reticulate. Propodeal disc broadly rounded, areolate-reticulate, without median carina (Fig. 5); callus areolate-reticulate, bare; callar nib absent. Prepectus areolate-reticulate, triangular dorsally, strongly narrowed ventrally (Figs. 4 and 10). Mesepisternum reticulate laterally, becoming smooth to areolate-reticulate ventrally, broadly rounded anterior to mesocoxa. Upper mesepimeron weakly reticulate; lower mesepimeron areolate-reticulate; transepimeral sulcus weakly impressed. Metepisternum laterally reticulate anteriorly, areolate-reticulate posteriorly. Propleuron convex, weakly reticulate. Postpectal carina prominent. Metacoxa 1.68–1.92× as long as broad and reticulate dorsally, becoming smooth ventrally; metafemur 4.4–5.6× as long as broad, with even cover of short, dense setae; metatibia sparsely setose. Fore wing (Fig. 13) 2.25–2.9× as long as broad, 2.36–2.87× as long as mesothorax; basal cell and speculum bare, costal cell sparsely setose, wing disc moderately setose; marginal fringe relatively long; submarginal vein bare; marginal vein with minute setae; stigmal vein about the same length as postmarginal vein, slightly angled distally; uncus absent; stigma with three clustered sensilla in a straight line and a fourth separated (Fig. 13, inset); postmarginal vein 5.0–7.2× as long as stigmal vein. Hind wing costal cell with a broad bare area. Metasoma: Petiole cylindrical (Fig. 12), linear in lateral view, 0.88–1.13× as long as broad, 0.54–0.71× as long as metacoxa, rugose with reticulate surface sculpture, anterior carina weak (Figs. 6 and 12, apc), lateral margin rounded, ventral sulcus absent. Antecostal sulcus crossed by carinae (Figs. 6 and 7, acs); acrosternite (act) posteriorly rounded; hypopygium with apical setae present, minute. Ovipositor (Figs. 14 and 15) slightly curved toward the head; subapical carina present; first (ventral) valvula with 10–11 minute, closely spaced teeth laterally (Fig. 14), second (dorsal) valvula with 8–10 annuli broadly separated dorsally by smooth area; third valvula separated from second valvifer. Figs. 14–17. View largeDownload slide Orasema taii. (14) Ovipositor, ventral view. (15) Lateral view of apex of ovipositor stylets. (16) Female pupa, lateral and ventral view. (17) Male pupa, lateral and ventral view of abdomen (inset). Except for inset, pupae are at same scale. Figs. 14–17. View largeDownload slide Orasema taii. (14) Ovipositor, ventral view. (15) Lateral view of apex of ovipositor stylets. (16) Female pupa, lateral and ventral view. (17) Male pupa, lateral and ventral view of abdomen (inset). Except for inset, pupae are at same scale. Male: No adult males have been found, but there was one male pupa with an almost fully developed adult inside (Fig. 17) collected in a parasitized Solenopsis colony. The mesoscutellum was bright blue–green and evenly fine reticulate with a coppery linear median impression, and with a dark blue frenum, suggesting that it is correctly associated with the O. taii females. Antennal flagellomere F2 was 1.10× as long as F3, whereas in O. texana, it is longer than F3 (1.14–1.33×). Behavior All observations were made at one site in the Welder Wildlife refuge near Venado Mill. O. taii was found ovipositing onto the leaves and green stem tissue of Vachellia sp., Fabaceae) (Fig. 19), commonly known as Huisatche, a dominant shrubby tree in the area. Oviposition was observed on all of the trees examined, with any green tissue saturated with egg punctures. Eggs are deposited into rows (Fig. 19), with the leaf surface hollowed by the expanded ovipositor, with a single egg deposited into each incision (Fig. 18). Immature thrips parasitized by planidia were observed on the trees, and although not observed directly, use of the thrips as an intermediate host for transport by the ants to gain access to the ant nest is possible (cf. Heraty 2000). Huisatche also has extrafloral nectaries, offering another means of interaction with the host ant and access to the ant brood (cf. Carey et al. 2012; Herreid and Heraty 2017). Figs. 18–23. View largeDownload slide Orasema taii. (18) Section through leaf showing egg within oviposition puncture. (19) Oviposition on Vachellia (Fabaceae). (20) Planidium habitus, dorsal and ventral view. (21) Magnified mandibular area of planidium. (22) Third instar larva. (23) Pupa. Figs. 18–23. View largeDownload slide Orasema taii. (18) Section through leaf showing egg within oviposition puncture. (19) Oviposition on Vachellia (Fabaceae). (20) Planidium habitus, dorsal and ventral view. (21) Magnified mandibular area of planidium. (22) Third instar larva. (23) Pupa. The host ant was identified as the S. geminata × xyloni hybrid. Colonies of this mound-building ant were found in sandy soil that was easily excavated. Immature stages and adults of Orasema were common in the nests and upon disturbance, adult ants were observed carrying parasitized ants and Orasema pupae along with their own brood (cf. Wheeler 1907). Colonies of S. invicta Buren have similar mound-building habits as the hybrid colonies and were found in close proximity to both hybrid colonies and to the infested Huisatche, but no parasitized brood was recovered. Laboratory experiments were conducted by placing planidia directly onto mature larvae of both the native host and onto S. invicta from colonies maintained at Texas A&M University. In total, 51 planidia were placed on larvae of S. geminata × xyloni and 60 planidia on larvae of S. invicta. Ant larvae were held in groups of about 20 in Petri dishes that were partially filled with Plaster of Paris and had a small nest hollowed out under a glass microscope slide. After 7 days, planidia had attacked seven larvae of S. geminata × xyloni (11 planidia found on one first-instar, four on four second-instars, and two on two third-instars). The planidia all remained external, never burrowed into the host, and never developed beyond the first-instar. Only one second-instar larvae of S. invicta was attacked, with the ant larva molting to the second instar, and the planidium had burrowed under the cuticle as is typical of parasitism by Orasema (Heraty 2000). None of the Solenopsis larvae survived to pupation, and the Orasema did not develop beyond the first instar. These results weakly support the idea that both ant species might be acceptable to O. taii, but in the field, there was clearly no evidence of parasitism of the invasive S. invicta. JH recovered O. taii at Venado Mill in 1988 (November) and 1989 (May). On both occasions, a few O. texana Gahan were collected on the same host plant, although the majority were found on another host plant (an unidentified species of Asteraceae), but no host ants were identified for O. texana. O. texana, but not O. taii were sampled from Huisatche at the same site in 1986 (June), and neither species were sampled from Huisatche in 1999 (May), 2014 (July), or 2015 (June). It is difficult to make assumptions based on such limited sampling, but the abundance of O. taii appears to be fleeting and was potentially correlated with high populations of the S. geminata × xyloni hybrid, which has been subsequently nearly replaced by S. invicta. Planidium (Figs. 20 and 21). Length 0.15–0.20 mm (n = 10). Antenna, labial plates and tergopleural line absent. A hatchet shaped sclerite (hss) is associated with the labral complex (Fig. 21). Terga I and II (TI, TII) separate. TI, TII, TIII each with dorsal seta. TII, TVI each with very short lateral seta. TI, TIII, TV, TVII each with ventral seta. TXII truncate. Caudal pad present; caudal cerci present and short, about as long as apical 3 terga. Third-Instar (Fig. 22). Length 2.91 mm (n = 1). Body smooth and without setae, body segments each slightly swollen medially, with paired or single small lateral swellings associated with each of the nine spiracles. Pupa (Figs. 16, 17, and 23). Length 3.04–3.58 (♀, n = 4), 2.46 (♂, n = 1) mm; prominent lateral swelling by mesothoracic spiracle; three pronounced tubercles over petiole, five prominent transverse ridges on abdomen; six prominent ventrolateral swellings associated with each gastral segment, anterior swelling small and tuberculate in both sexes, second much smaller than following four swellings in female (Figs. 16 and 23), male with five prominent swellings (Fig. 17); female with two pairs of ventral swellings on the abdomen, whereas male has a series of transverse bands (Fig. 17, inset). Etymology Named in honor of Iris Chien’s father, who passed away far too soon. HOLOTYPE: USA: TX: San Patricio Co., Welder Wildlife Ref. near Venado Mill, 28°06’49”N, 97°25’00”W, 1-xi-1988, J. Heraty, ex: S. geminata × xyloni hybrid [1♀, UCRCENT 00397368], deposited in UCRC. PARATYPES (56♀): USA: TX: San Patricio Co., Welder Wildlife Ref. near Venado Mill, 28°06’49”N, 97°25’00”W, 1-xi-1988, J. Heraty [3♀, TAMU: UCRCENT 00243364, UCRC: UCRCENT 00397350, UCRCENT 00397370]. same locality, 1-xi-1988, J. Heraty, on Huisatche (Vachellia) [7♀, TAMU: UCRCENT 00243368, UCRCENT 00243370; UCRC: UCRCENT 00397356, UCRCENT 00397364–66, UCRCENT 00397371]. same locality, 1-xi-1988,J. Heraty, ex: S. geminata × xyloni hybrid [6♀, TAMU: UCRCENT 00243365–67; UCRC: UCRCENT 00397348–49, UCRCENT 00397367]; same locality, 2-xi-1988, J. Heraty [3♀, TAMU: UCRCENT 00243362–63; UCRC: UCRCENT 00397353]; same locality, 2-xi-1988, J. Heraty, on Huisatche (Vachellia) [13♀, TAMU: UCRCENT 00243359–61; UCRC: UCRCENT 00397351, UCRCENT 00397354–55, UCRCENT 00397357–63]; same locality, 2-xi-1988, J. Heraty, x: S. geminata × xyloni hybrid [15♀, TAMU: UCRCENT 00243342–43, UCRCENT 00243348–58; UCRC: UCRCENT 00397352, UCRCENT 00397369]; same locality, 26-vi-1986, J. Heraty, on Huisatche (Vachellia) [5♀, UCRC: UCRCENT 00397372–76]; same locality, 1-xi-1988, J. Heraty, ex: S. geminata × xyloni hybrid [3♀, UCRC: UCRCENT 00395694–96]; Welder Wildlife Ref. near Venado Mill, 28°06’42”N, 97°24’24”W, 3.v.1989, J. Heraty [1♀, TAMU: UCRCENT 00243371]. Immature Stages: First-instar (planidia): USA: TX: San Patricio Co., Welder Wildlife Ref. near Venado Mills, 28°06’49”N, 97°25’00”W, 2-xi-1988, J. Heraty, ex: Solenopsis geminata × S. xyloni hybrid [4 slides, TAMU: UCRCENT 00478792–95]. Third instar: same data but, 1-xi-1988 [UCRC_ENT 00395702]. Pupae: same data but, 1-xi-1988 [11♀, UCRC: UCRCENT 00395697–707, 1♂ UCRCENT 00395707]. Ant hosts: USA: TX: San Patricio Co., Welder Wildlife Ref., 28°01’42”N, 97°31’50”W, 1-xi-1988, J. Heraty, on Vachellia [1♀, UCRC: UCRCENT 00395716]; Welder Wildlife Ref., 1-xi-1988, J. Heraty [10♀, 3 larvae, UCRC: UCRCENT 00395697, UCRCENT 00395703–06, UCRCENT 00395708–15]. Acknowledgments We thank the Welder Wildlife Foundation for providing access that helped make this study possible. Brad Vinson provided live colonies of fire ants. We thank Austin Baker, Roger Burks, Chrysalyn Dominguez and reviewers for their insightful comments on earlier drafts of this manuscript. This research was supported by grant NSF-DEB 1257733 to JH. References Cited Burks, R. A., J. L. Mutter, C. Dominguez, S. Heacox, and J. M. Heraty. 2017. Biting the bullet: Revisionary notes on the Oraseminae of the old world (Hymenoptera: Chalcidoidea: Eucharitidae). J. Hymenopt. Res . 55: 139– 188. Google Scholar CrossRef Search ADS   Cahan, S. H., and S. B. Vinson. 2003. Reproductive divisiton of labor between hybrid and nonhybrid offspring in a fire ant hybrid zone. Evolution  57: 1562– 1570. Google Scholar CrossRef Search ADS PubMed  Carey, B., K. Visscher, and J. Heraty. 2012. Nectary use for gaining access to an ant host by the parasitoid Orasema simulatrix (Hymenoptera, Eucharitidae). J. Hymen. Res . 27: 47– 65. Google Scholar CrossRef Search ADS   Cook, J. L., J. S. Johnston, R. E. Gold, and S. B. Vinson. 1997. Distribution of Caenocholax fenyesi (Strepsiptera: Myrmecolacidae) and the habitats most likely to contaiin its stylopized host, Solenopsis invicta (Hymenoptera: Formicidae). Environ. Entomol . 26: 1258– 1262. Google Scholar CrossRef Search ADS   Heraty, J. M. 1994a. Biology and importance of two eucharitid parasites of Wasmannia and Solenopsis, p. 332. In D. F. Williams, (ed.), Exotic Ants: Biology, Impact and Control of Introduced Species . Westview Press, Boulder, Colorado. Heraty, J. M. 1994b. Classification and evolution of the Oraseminae in the Old World, with revisions of two closely related genera of Eucharitinae (Hymenoptera: Eucharitidae). Life Sci. Contrib. Royal Ontario Mus . 157: 1– 174. Heraty, J. M. 2000. Phylogenetic relationships of Oraseminae (Hymenoptera: Eucharitidae). Ann. Entomol. Soc. Am . 93: 374– 390. Google Scholar CrossRef Search ADS   Heraty, J. M. 2002. A revision of the genera of Eucharitidae (Hymenoptera: Chalcidoidea) of the World. Mem. Am. Entomol. Inst . 68: 1– 359. Heraty, J. M., D. P. Wojcik, and D. P. Jouvenaz. 1993. Species of Orasema parasitic on the Solenopsis saevissima complex in South America (Hymenoptera: Eucharitidae, Formicidae). J. Hymenopt. Res . 2: 169– 182. Herreid, J. S., and J. M. Heraty. 2017. Hitchhikers at the dinner table: a revisionary study of a group of ant parasitoids (Hymenoptera: Eucharitidae) specializing in the use of extrafloral nectaries for host access. Syst. Entomol . 42: 204– 229. Google Scholar CrossRef Search ADS   Hill, J. K., R. B. Rosengaus, F. S. Gilbert, and A. G. Hart. 2013. Invasive ants–are fire ants drivers of biodiversity loss? Ecol. Entomol . 38: 539. Google Scholar CrossRef Search ADS   Hung, A. C. F., and S. B. Vinson. 1977. Interspecific hybridization and caste specificity of protein in Fire Ant. Science  196: 1458– 1460. Google Scholar CrossRef Search ADS PubMed  Johnson, J. B., T. D. Miller, J. M. Heraty, and F. W. Merickel. 1986. Observations on the biology of two species of Orasema (Hymenoptera: Eucharitidae). Proc. Entomol. Soc. Wash . 88: 542– 549. LeBrun, E. G., R. M. Plowes, and L. E. Gilbert. 2012. Imported fire ants near the edge of their range: disturbance and moisture determine prevalence and impact of an invasive social insect. J. Anim. Ecol . 81: 884– 895. Google Scholar CrossRef Search ADS PubMed  Morrison, L. W. 2000. Mechanisms of interspecific competition among an invasive and two native fire ants. Oikos  90: 238– 252. Google Scholar CrossRef Search ADS   Plowes, R. M., E. G. LeBrun, B. V. Brown, and L. E. Gilbert. 2009. A review of Pseudacteon (Diptera: Phoridae) that parasitize ants of the Solenopsis geminata complex (Hymenoptera: Formicidae). Ann. Entomol. Soc. Am . 102: 937– 958. Google Scholar CrossRef Search ADS   Porter, S. D., and D. A. Savignano. 1990. Invasion of polygyne fire ants decimates native ants and disrupts arthropod community. Ecology  71: 2095– 2106. Google Scholar CrossRef Search ADS   Trager, J. C. 1991. A revision of the fire ants, Solenopsis geminata group (Hymenoptera: Formicidae: Myrmicinae). J.N.Y. Entomol. Soc . 99: 141– 198. Tschinkel, W. R., and J. R. King. 2017. Ant community and habitat limit colony establishment by the fire ant, Solenopsis invicta. Funct. Ecol . 31: 955– 964. Google Scholar CrossRef Search ADS   Varone, L., and J. Briano. 2009. Bionomics of Orasema simplex (Hymenoptera: Eucharitidae), a parasitoid of Solenopsis fire ants (Hymenoptera: Formicidae) in Argentina. Biol. Control  2009: 204– 209. Google Scholar CrossRef Search ADS   Varone, L., J. M. Heraty, and L. Calcaterra. 2010. Distribution, abundance and persistence of species of Orasema (Hym: Eucharitidae) parasitic on fire ants in South America. Biol. Control  55: 72– 78. Google Scholar CrossRef Search ADS   Wheeler, W. M. 1907. The polymorphism of ants with an account of some singular abnormalities due to parasitism. Bull. Am. Mus. Nat. Hist . 23: 1– 108. Wheeler, G. C., and J. Wheeler. 1937. New hymenopterous parasitoids of ants (Chalcidoidea, Eucharidae). Ann. Entomol. Soc. Am . 30: 171– 172. Google Scholar CrossRef Search ADS   Wilson, E. O., and W. L. J. Brown. 1958. Recent changes in the introduced fire ant Solenopsis saevissima (Fr. Smith). Evolution  12: 211– 218. Google Scholar CrossRef Search ADS   Wojcik, D. P., D. P. Jouvenaz, W. A. Banks, and A. C. Pereira. 1987. Biological control agents of fire ants in Brazil, pp. 627– 628. In J. Eder and H. Rembold, (eds.), Chemistry and Biology of Social Insects . Verlag J. Peperny, Munich. © The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Insect Systematics and Diversity Oxford University Press

Come and Gone: Description of a New Species of Eucharitidae (Hymenoptera) Attacking Solenopsis (Hymenoptera: Formicidae) in Texas

Loading next page...
 
/lp/ou_press/come-and-gone-description-of-a-new-species-of-eucharitidae-hymenoptera-4jstz9req5
Publisher
Oxford University Press
Copyright
© The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
eISSN
2399-3421
D.O.I.
10.1093/isd/ixx012
Publisher site
See Article on Publisher Site

Abstract

Abstract Eucharitidae (Hymenoptera: Chalcidoidea) are the only family in which all members are specialized parasitoids of ant brood, with species of Orasema Cameron (Oraseminae) parasitizing several genera of Myrmicinae, including Solenopsis Westwood and Pheidole Westwood (Formicidae). In 1988, a new species of Orasema was discovered in southern Texas attacking the brood of what is recognized as a Solenopsis geminata (Fabricius) (Hymenoptera: Formicidae) × Solenopsis xyloni McCook (Hymenoptera: Formicidae) hybrid. Adults of Orasema oviposit onto the green stems and leaves of Vachellia sp. (Fabaceae). Orasema taii n. sp. was only found attacking the hybrid colonies and was not recovered from adjacent nests of Solenopsis invicta Buren (Hymenoptera: Formicidae), which at that time were equally abundant in the area. Wasps were abundant at the time of collection, but since these initial collections, the parasitoids have not been recovered. Hybrid populations have declined precipitously with the invasion of the imported fire ant, and both the hybrid and parasitoid may have been extirpated at least from the area of discovery. Based on morphological and molecular evidence, O. taii n. sp. is placed into the Orasema bakeri species group. The adult and immature stages and their behavior in the field are described. Since its introduction into the United States in the 1930s, the red imported fire ant (RIFA), Solenopsis invicta Buren (Hymenoptera: Formicidae), has been shown to have a negative impact on the biodiversity and abundance of native ant species (Wilson and Brown 1958; Porter and Savignano 1990; Morrison 2000; Hill et al. 2013; but see Tschinkel and King 2017). In Texas, two species of Solenopsis considered as ecological homologues, Solenopsis geminata (Fabricius) (Hymenoptera: Formicidae) and Solenopsis xyloni McCook (Hymenoptera: Formicidae), as well as a common hybrid form, S. geminata × xyloni, were common before the RIFA invasion (Hung and Vinson 1977; Morrison 2000; Cahan and Vinson 2003). Habitat effects are one factor known to affect competitive interactions between the different species of Solenopsis, but although interactions were initially devastating, these effects have allowed for some populations of native Solenopsis, including the hybrid, to survive in Texas albeit in much lower numbers (LeBrun et al. 2012). The impact of parasitoids has been studied to some degree with the greatest emphasis on Pseudacteon phorid flies (Plowes et al. 2009) and less so Caenocholax strepsipterans (Cook et al. 1997). Parasitism of any of these ants in the Solenopsis saevissima complex (or geminata group sensuTrager 1991) in the United States by a eucharitid wasp has never been documented. Orasema Cameron (Eucharitidae: Oraseminae) belongs to a diverse family of specialized ant-parasitoids (Heraty 2000, 2002). Immatures parasitize the brood of the ant subfamily Myrmicinae, first by attacking the host larva and then completing their development on the pupa (Heraty et al. 1993; Heraty 1994a, b, 2000; Varone and Briano 2009; Varone et al. 2010; Herreid and Heraty 2017). Eggs are deposited away from the host into plant tissue using an expanded ovipositor, and first instars (termed planidia) then gain access to the host nest by phoretic attachment to the host ant or through attachment to an intermediate host such as thrips (Heraty 2000; Herreid and Heraty 2017). Parasitism of Solenopsis is relatively uncommon in the genus. The Orasema xanthopus species group is the only clade known to specialize on fire ants in the S. saevissima complex, but their distribution is restricted to South America (Wojcik et al. 1987; Heraty et al. 1993; Varone et al. 2010). Orasema sixaolae Wheeler & Wheeler has been reared from Solenopsis tenuis Mayr in Costa Rica (Wheeler and Wheeler 1937). Orasema coloradensis Wheeler was reared from both Pheidole bicarinata Forel and Solenopsis molesta validiscula Emery in Colorado and Texas (Wheeler 1907), and has been associated with, but not reared from Formica in Idaho (Johnson et al. 1986). No species have been reported attacking S. saevissima complex species in North America. We describe below a new species of Orasema that at the time of collection was an abundant parasitoid of the S. geminata × xyloni hybrid in Texas, but has never since been rediscovered. The Solenopsis hybrid has been largely excluded across its original range by RIFA; however, the hybrid continues to be found in low numbers in southern Texas, representing less than 8 percent of the total ant population (Plowes et al. 2009; LeBrun et al. 2012). Thus, it is possible that the parasitoid may yet be found again. The behavior of the parasitoids suggests that they are very host specific, and parasitoid pressure on the hybrid may have enhanced their competitive disadvantage. Orasema taii n. sp. is described herein along with its immature stages and its oviposition and within-nest behavior. It is placed in the Orasema bakeri group, which includes an undescribed species known to parasitize Pheidole and Tetramorium (Heraty 1994b, unpublished data). We extensively annotate the morphology of adult female Orasema in an attempt to standardize the morphological terminology being applied to the genus and Eucharitidae in general. Materials and Methods Specimens examined are housed at Texas A&M University, College Station, TX (TAMU) and at the University of California, Riverside, CA (UCRC). All specimens are identified with unique UCRC specimen identifiers that also refer to the museum of deposition. Geographic coordinates estimated from Google Earth are in italics. Morphological terminology and measurements follow Heraty (2000) and Burks et al. (2017). Abbreviations of morphological terms are listed in Table 1. All specimens were measured with Zeiss Stemi SV6 and 16× eyepiece. Images were taken using a Leica Imaging System with a Z16 APO A microscope and stacked using Zerene Stacker (version 1.04, Zerene systems, LLC). Original images were uploaded to Figshare (figshare.com/account/home#/projects/26533). Table 1. List of abbreviations 1-2vf  1st-2nd valvifers  1-3vv  1st-3rd valvulae  Acst  acrosternite  Acs  antecostal sulcus  Acy  anteclypeus  Anl  anellus (flagellomere 1)  Anr  antennal rim  Apc  anterior transverse petiolar carina  Ax  axilla  Axl  axillula  Cal  propodeal callus  Cc  costal cell  cx1-3  pro-, meso-, metacoxa  dr1  dorsal ramus  Esg  epistomal groove  F1-9  flagellomeres  f2-3p  meso- and metafurcal pit  Fra  frenal arm  Frn  frenum  Gt1  first gastral tergum  Lb  laminated bridge of ovipositor  Lcl  lateral clypeal line  lep2  lower mesepimeron  les2  lower mespisternum  Llm  lateral lobe of mesoscutum  Lmd  left mandible  Lpa  lateral panel of axilla  Mlm  median lobe of mesoscutum  Mps  multiporous plate sensillum  mr1-3  mandibular rods 1-3  Mrm  marginal rim of mesoscutellum  Msd  median scrobal depression  Mts  metascutellum  Mtsa  metascutellar arm  Mv  marginal vein  no1  pronotum  no3  metanotum  Not  notaulus  Pa  paratergite  Paa  pars articularis  Ped  pedicel  Pet  petiole  Pmu  processus muscularis  Pmv  postmarginal vein  Pre  prepectus  Prp  propodeum  Pss  postspiracular sulcus  Rad  radicle  Rmd  right mandible  Sas  subantennal sulcus  Scd  mesoscutellar disc  Scp  scape  Scr  antennal scrobe  Smv  submarginal vein  Spa  sensillar patch of 2nd valvifer  Sss  scutoscutellar suture  Stv  stigmal vein  Tgl  tegula  Tor  torulus  Tpl  tergopleural line  Tsa  transscutal articulation  uep2  upper mesepimeron  ues2  upper mesepisternum  1-2vf  1st-2nd valvifers  1-3vv  1st-3rd valvulae  Acst  acrosternite  Acs  antecostal sulcus  Acy  anteclypeus  Anl  anellus (flagellomere 1)  Anr  antennal rim  Apc  anterior transverse petiolar carina  Ax  axilla  Axl  axillula  Cal  propodeal callus  Cc  costal cell  cx1-3  pro-, meso-, metacoxa  dr1  dorsal ramus  Esg  epistomal groove  F1-9  flagellomeres  f2-3p  meso- and metafurcal pit  Fra  frenal arm  Frn  frenum  Gt1  first gastral tergum  Lb  laminated bridge of ovipositor  Lcl  lateral clypeal line  lep2  lower mesepimeron  les2  lower mespisternum  Llm  lateral lobe of mesoscutum  Lmd  left mandible  Lpa  lateral panel of axilla  Mlm  median lobe of mesoscutum  Mps  multiporous plate sensillum  mr1-3  mandibular rods 1-3  Mrm  marginal rim of mesoscutellum  Msd  median scrobal depression  Mts  metascutellum  Mtsa  metascutellar arm  Mv  marginal vein  no1  pronotum  no3  metanotum  Not  notaulus  Pa  paratergite  Paa  pars articularis  Ped  pedicel  Pet  petiole  Pmu  processus muscularis  Pmv  postmarginal vein  Pre  prepectus  Prp  propodeum  Pss  postspiracular sulcus  Rad  radicle  Rmd  right mandible  Sas  subantennal sulcus  Scd  mesoscutellar disc  Scp  scape  Scr  antennal scrobe  Smv  submarginal vein  Spa  sensillar patch of 2nd valvifer  Sss  scutoscutellar suture  Stv  stigmal vein  Tgl  tegula  Tor  torulus  Tpl  tergopleural line  Tsa  transscutal articulation  uep2  upper mesepimeron  ues2  upper mesepisternum  View Large Nomenclature This paper and the nomenclatural act(s) it contains have been registered in Zoobank (www.zoobank.org), the official register of the International Commission on Zoological Nomenclature. The LSID (Life Science Identifier) number of the publication is urn:lsid:zoobank.org:pub:F0E644BE-548F-4BB3-9DCA-B7886A3F4012 Orasema taii n. sp. (Figs 1–23) (http://zoobank.org/urn:lsid:zoobank.org:act:DA294E6D-76C6- 4BFC-AFCE-D8EDECBF4C53) Diagnosis Species in the bakeri group are recognized by having seven funicular segments, the prepectus without a carina along the anterior margin, the femora are mostly dark brown, and the petiole in females is only slightly longer than broad (in males up to 2.5× as long as broad). The new species is distinguished from other members of the group (O. bakeri Gahan, Orasema texana Gahan) by the following combination of features: clava with a distinct ventral notch separating two apical clavomeres; mesoscutellar disc between frenal line and axillae distinctly longer than broad and with a central median channel that is a more coppery colored than the surrounding dark blue–green frenum; and petiole with a weak anterior carina, no lateral carina, and strongly rugose. The clava is a single completely fused structure in all other bakeri-group species. O. bakeri has reticulate sculpture on the dorsal surface of the petiole, whereas O. taii has areolate-reticulate sculpture (Fig. 12). O. texana Gahan has the mesoscutellar disc between the frenal line and axillae at most as long as broad, scabriculous (not evenly fine reticulate) sculpture dorsally, petiole with dorsal surface relatively flat and reticulate, and in females, it has a prominent dorsolateral carinae that extends the full length of the petiole. Female: Length 2.37–3.05 mm. Color: Head and mesosoma blue green, mesosoma more greenish dorsally and mostly dark blue laterally (Figs. 10 and 11). Scape pale brown; pedicel brown; anellus yellowish brown; flagellum dark brown. Mandible, maxilla, and labium dark brown. Coxae dark blue; femora mostly dark brown to black, tips pale; tibiae yellow. Fore wing hyaline; venation pale brown. Petiole dark blue; gaster brown. Head: Head in frontal view subtriangular (Fig. 3); 1.14–1.26× broader than high; face reticulate. Occiput strigate, shallowly emarginate in dorsal view, dorsal margin abrupt; temple present, rounded. Scrobal depression shallow, laterally rounded, reticulate, dorsal scrobal depressions absent; longitudinal groove between eye and torulus absent; eye sparsely setose, appearing bare; interocular distance 1.59–1.88× eye height; malar space 0.74–0.96× eye height; malar depression weakly impressed between mouth and eye margin; supraclypeal area about as long as broad, shorter than clypeus, weakly sculptured; clypeus strongly sculptured; epistomal sulcus narrow but shallow; anterior tentorial pits shallow; anteclypeus distinct, straight. Labrum with four digits (Fig. 3). Mandibular formula 3:2 (Figs. 3 and 9); palpal formula 3:2. Scape not reaching median ocellus. Pedicel small and globose. Flagellum with seven funicular segments (Fig. 1, F2–8); flagellum length 0.96–1.1× head height; anellus disc-shaped; F2 1–1.33× as long as broad, 0.85–1.06× as long as F3; following funicular segments subequal in length, equal in width; clava subconical, with notch ventrally between first and second subsegments. Figs. 1–7. View largeDownload slide Orasema taii, female. (1) Antenna (lateral). (2) Flagellomeres F1–3 (lateral). (3) Head (anterior). (4) Mesosoma (lateral). (5) Mesosoma (oblique posterior). (6) Petiole and acrosternite (lateral). (7) Mesosoma and petiole (ventral). Figs. 1–7. View largeDownload slide Orasema taii, female. (1) Antenna (lateral). (2) Flagellomeres F1–3 (lateral). (3) Head (anterior). (4) Mesosoma (lateral). (5) Mesosoma (oblique posterior). (6) Petiole and acrosternite (lateral). (7) Mesosoma and petiole (ventral). Figs. 8–13. View largeDownload slide Orasema taii, female. (8) Apex of antenna (lateral). (9) Mandibles (posterior). (10) Mesosoma (lateral). (11) Mesosoma (dorsal). (12) Petiole (dorsal). (13) Fore wing. Figs. 8–13. View largeDownload slide Orasema taii, female. (8) Apex of antenna (lateral). (9) Mandibles (posterior). (10) Mesosoma (lateral). (11) Mesosoma (dorsal). (12) Petiole (dorsal). (13) Fore wing. Mesosoma: Mesosoma 1.08–1.23× as long as high (Figs. 4 and 10). Mesoscutal midlobe reticulate medially to rugose-reticulate laterally, with minute setae; lateral lobe strigose medially, to longitudinally reticulate laterally; notaulus deep (Fig. 11, not). Axilla reticulate medially to rugose-reticulate laterally, dorsally elevated well above scutellum (Figs. 4 and 10); scutoscutellar sulcus narrow, regularly foveate, extending to transscutal articulation medially, axilla broadly divided (Fig. 11, ax); scutellar disc slightly longer than broad, finely reticulate medially; frenal line reticulate; frenum reticulate; axillular sulcus anteriorly narrow, broad and foveate posteriorly; axillula reticulate. Propodeal disc broadly rounded, areolate-reticulate, without median carina (Fig. 5); callus areolate-reticulate, bare; callar nib absent. Prepectus areolate-reticulate, triangular dorsally, strongly narrowed ventrally (Figs. 4 and 10). Mesepisternum reticulate laterally, becoming smooth to areolate-reticulate ventrally, broadly rounded anterior to mesocoxa. Upper mesepimeron weakly reticulate; lower mesepimeron areolate-reticulate; transepimeral sulcus weakly impressed. Metepisternum laterally reticulate anteriorly, areolate-reticulate posteriorly. Propleuron convex, weakly reticulate. Postpectal carina prominent. Metacoxa 1.68–1.92× as long as broad and reticulate dorsally, becoming smooth ventrally; metafemur 4.4–5.6× as long as broad, with even cover of short, dense setae; metatibia sparsely setose. Fore wing (Fig. 13) 2.25–2.9× as long as broad, 2.36–2.87× as long as mesothorax; basal cell and speculum bare, costal cell sparsely setose, wing disc moderately setose; marginal fringe relatively long; submarginal vein bare; marginal vein with minute setae; stigmal vein about the same length as postmarginal vein, slightly angled distally; uncus absent; stigma with three clustered sensilla in a straight line and a fourth separated (Fig. 13, inset); postmarginal vein 5.0–7.2× as long as stigmal vein. Hind wing costal cell with a broad bare area. Metasoma: Petiole cylindrical (Fig. 12), linear in lateral view, 0.88–1.13× as long as broad, 0.54–0.71× as long as metacoxa, rugose with reticulate surface sculpture, anterior carina weak (Figs. 6 and 12, apc), lateral margin rounded, ventral sulcus absent. Antecostal sulcus crossed by carinae (Figs. 6 and 7, acs); acrosternite (act) posteriorly rounded; hypopygium with apical setae present, minute. Ovipositor (Figs. 14 and 15) slightly curved toward the head; subapical carina present; first (ventral) valvula with 10–11 minute, closely spaced teeth laterally (Fig. 14), second (dorsal) valvula with 8–10 annuli broadly separated dorsally by smooth area; third valvula separated from second valvifer. Figs. 14–17. View largeDownload slide Orasema taii. (14) Ovipositor, ventral view. (15) Lateral view of apex of ovipositor stylets. (16) Female pupa, lateral and ventral view. (17) Male pupa, lateral and ventral view of abdomen (inset). Except for inset, pupae are at same scale. Figs. 14–17. View largeDownload slide Orasema taii. (14) Ovipositor, ventral view. (15) Lateral view of apex of ovipositor stylets. (16) Female pupa, lateral and ventral view. (17) Male pupa, lateral and ventral view of abdomen (inset). Except for inset, pupae are at same scale. Male: No adult males have been found, but there was one male pupa with an almost fully developed adult inside (Fig. 17) collected in a parasitized Solenopsis colony. The mesoscutellum was bright blue–green and evenly fine reticulate with a coppery linear median impression, and with a dark blue frenum, suggesting that it is correctly associated with the O. taii females. Antennal flagellomere F2 was 1.10× as long as F3, whereas in O. texana, it is longer than F3 (1.14–1.33×). Behavior All observations were made at one site in the Welder Wildlife refuge near Venado Mill. O. taii was found ovipositing onto the leaves and green stem tissue of Vachellia sp., Fabaceae) (Fig. 19), commonly known as Huisatche, a dominant shrubby tree in the area. Oviposition was observed on all of the trees examined, with any green tissue saturated with egg punctures. Eggs are deposited into rows (Fig. 19), with the leaf surface hollowed by the expanded ovipositor, with a single egg deposited into each incision (Fig. 18). Immature thrips parasitized by planidia were observed on the trees, and although not observed directly, use of the thrips as an intermediate host for transport by the ants to gain access to the ant nest is possible (cf. Heraty 2000). Huisatche also has extrafloral nectaries, offering another means of interaction with the host ant and access to the ant brood (cf. Carey et al. 2012; Herreid and Heraty 2017). Figs. 18–23. View largeDownload slide Orasema taii. (18) Section through leaf showing egg within oviposition puncture. (19) Oviposition on Vachellia (Fabaceae). (20) Planidium habitus, dorsal and ventral view. (21) Magnified mandibular area of planidium. (22) Third instar larva. (23) Pupa. Figs. 18–23. View largeDownload slide Orasema taii. (18) Section through leaf showing egg within oviposition puncture. (19) Oviposition on Vachellia (Fabaceae). (20) Planidium habitus, dorsal and ventral view. (21) Magnified mandibular area of planidium. (22) Third instar larva. (23) Pupa. The host ant was identified as the S. geminata × xyloni hybrid. Colonies of this mound-building ant were found in sandy soil that was easily excavated. Immature stages and adults of Orasema were common in the nests and upon disturbance, adult ants were observed carrying parasitized ants and Orasema pupae along with their own brood (cf. Wheeler 1907). Colonies of S. invicta Buren have similar mound-building habits as the hybrid colonies and were found in close proximity to both hybrid colonies and to the infested Huisatche, but no parasitized brood was recovered. Laboratory experiments were conducted by placing planidia directly onto mature larvae of both the native host and onto S. invicta from colonies maintained at Texas A&M University. In total, 51 planidia were placed on larvae of S. geminata × xyloni and 60 planidia on larvae of S. invicta. Ant larvae were held in groups of about 20 in Petri dishes that were partially filled with Plaster of Paris and had a small nest hollowed out under a glass microscope slide. After 7 days, planidia had attacked seven larvae of S. geminata × xyloni (11 planidia found on one first-instar, four on four second-instars, and two on two third-instars). The planidia all remained external, never burrowed into the host, and never developed beyond the first-instar. Only one second-instar larvae of S. invicta was attacked, with the ant larva molting to the second instar, and the planidium had burrowed under the cuticle as is typical of parasitism by Orasema (Heraty 2000). None of the Solenopsis larvae survived to pupation, and the Orasema did not develop beyond the first instar. These results weakly support the idea that both ant species might be acceptable to O. taii, but in the field, there was clearly no evidence of parasitism of the invasive S. invicta. JH recovered O. taii at Venado Mill in 1988 (November) and 1989 (May). On both occasions, a few O. texana Gahan were collected on the same host plant, although the majority were found on another host plant (an unidentified species of Asteraceae), but no host ants were identified for O. texana. O. texana, but not O. taii were sampled from Huisatche at the same site in 1986 (June), and neither species were sampled from Huisatche in 1999 (May), 2014 (July), or 2015 (June). It is difficult to make assumptions based on such limited sampling, but the abundance of O. taii appears to be fleeting and was potentially correlated with high populations of the S. geminata × xyloni hybrid, which has been subsequently nearly replaced by S. invicta. Planidium (Figs. 20 and 21). Length 0.15–0.20 mm (n = 10). Antenna, labial plates and tergopleural line absent. A hatchet shaped sclerite (hss) is associated with the labral complex (Fig. 21). Terga I and II (TI, TII) separate. TI, TII, TIII each with dorsal seta. TII, TVI each with very short lateral seta. TI, TIII, TV, TVII each with ventral seta. TXII truncate. Caudal pad present; caudal cerci present and short, about as long as apical 3 terga. Third-Instar (Fig. 22). Length 2.91 mm (n = 1). Body smooth and without setae, body segments each slightly swollen medially, with paired or single small lateral swellings associated with each of the nine spiracles. Pupa (Figs. 16, 17, and 23). Length 3.04–3.58 (♀, n = 4), 2.46 (♂, n = 1) mm; prominent lateral swelling by mesothoracic spiracle; three pronounced tubercles over petiole, five prominent transverse ridges on abdomen; six prominent ventrolateral swellings associated with each gastral segment, anterior swelling small and tuberculate in both sexes, second much smaller than following four swellings in female (Figs. 16 and 23), male with five prominent swellings (Fig. 17); female with two pairs of ventral swellings on the abdomen, whereas male has a series of transverse bands (Fig. 17, inset). Etymology Named in honor of Iris Chien’s father, who passed away far too soon. HOLOTYPE: USA: TX: San Patricio Co., Welder Wildlife Ref. near Venado Mill, 28°06’49”N, 97°25’00”W, 1-xi-1988, J. Heraty, ex: S. geminata × xyloni hybrid [1♀, UCRCENT 00397368], deposited in UCRC. PARATYPES (56♀): USA: TX: San Patricio Co., Welder Wildlife Ref. near Venado Mill, 28°06’49”N, 97°25’00”W, 1-xi-1988, J. Heraty [3♀, TAMU: UCRCENT 00243364, UCRC: UCRCENT 00397350, UCRCENT 00397370]. same locality, 1-xi-1988, J. Heraty, on Huisatche (Vachellia) [7♀, TAMU: UCRCENT 00243368, UCRCENT 00243370; UCRC: UCRCENT 00397356, UCRCENT 00397364–66, UCRCENT 00397371]. same locality, 1-xi-1988,J. Heraty, ex: S. geminata × xyloni hybrid [6♀, TAMU: UCRCENT 00243365–67; UCRC: UCRCENT 00397348–49, UCRCENT 00397367]; same locality, 2-xi-1988, J. Heraty [3♀, TAMU: UCRCENT 00243362–63; UCRC: UCRCENT 00397353]; same locality, 2-xi-1988, J. Heraty, on Huisatche (Vachellia) [13♀, TAMU: UCRCENT 00243359–61; UCRC: UCRCENT 00397351, UCRCENT 00397354–55, UCRCENT 00397357–63]; same locality, 2-xi-1988, J. Heraty, x: S. geminata × xyloni hybrid [15♀, TAMU: UCRCENT 00243342–43, UCRCENT 00243348–58; UCRC: UCRCENT 00397352, UCRCENT 00397369]; same locality, 26-vi-1986, J. Heraty, on Huisatche (Vachellia) [5♀, UCRC: UCRCENT 00397372–76]; same locality, 1-xi-1988, J. Heraty, ex: S. geminata × xyloni hybrid [3♀, UCRC: UCRCENT 00395694–96]; Welder Wildlife Ref. near Venado Mill, 28°06’42”N, 97°24’24”W, 3.v.1989, J. Heraty [1♀, TAMU: UCRCENT 00243371]. Immature Stages: First-instar (planidia): USA: TX: San Patricio Co., Welder Wildlife Ref. near Venado Mills, 28°06’49”N, 97°25’00”W, 2-xi-1988, J. Heraty, ex: Solenopsis geminata × S. xyloni hybrid [4 slides, TAMU: UCRCENT 00478792–95]. Third instar: same data but, 1-xi-1988 [UCRC_ENT 00395702]. Pupae: same data but, 1-xi-1988 [11♀, UCRC: UCRCENT 00395697–707, 1♂ UCRCENT 00395707]. Ant hosts: USA: TX: San Patricio Co., Welder Wildlife Ref., 28°01’42”N, 97°31’50”W, 1-xi-1988, J. Heraty, on Vachellia [1♀, UCRC: UCRCENT 00395716]; Welder Wildlife Ref., 1-xi-1988, J. Heraty [10♀, 3 larvae, UCRC: UCRCENT 00395697, UCRCENT 00395703–06, UCRCENT 00395708–15]. Acknowledgments We thank the Welder Wildlife Foundation for providing access that helped make this study possible. Brad Vinson provided live colonies of fire ants. We thank Austin Baker, Roger Burks, Chrysalyn Dominguez and reviewers for their insightful comments on earlier drafts of this manuscript. This research was supported by grant NSF-DEB 1257733 to JH. References Cited Burks, R. A., J. L. Mutter, C. Dominguez, S. Heacox, and J. M. Heraty. 2017. Biting the bullet: Revisionary notes on the Oraseminae of the old world (Hymenoptera: Chalcidoidea: Eucharitidae). J. Hymenopt. Res . 55: 139– 188. Google Scholar CrossRef Search ADS   Cahan, S. H., and S. B. Vinson. 2003. Reproductive divisiton of labor between hybrid and nonhybrid offspring in a fire ant hybrid zone. Evolution  57: 1562– 1570. Google Scholar CrossRef Search ADS PubMed  Carey, B., K. Visscher, and J. Heraty. 2012. Nectary use for gaining access to an ant host by the parasitoid Orasema simulatrix (Hymenoptera, Eucharitidae). J. Hymen. Res . 27: 47– 65. Google Scholar CrossRef Search ADS   Cook, J. L., J. S. Johnston, R. E. Gold, and S. B. Vinson. 1997. Distribution of Caenocholax fenyesi (Strepsiptera: Myrmecolacidae) and the habitats most likely to contaiin its stylopized host, Solenopsis invicta (Hymenoptera: Formicidae). Environ. Entomol . 26: 1258– 1262. Google Scholar CrossRef Search ADS   Heraty, J. M. 1994a. Biology and importance of two eucharitid parasites of Wasmannia and Solenopsis, p. 332. In D. F. Williams, (ed.), Exotic Ants: Biology, Impact and Control of Introduced Species . Westview Press, Boulder, Colorado. Heraty, J. M. 1994b. Classification and evolution of the Oraseminae in the Old World, with revisions of two closely related genera of Eucharitinae (Hymenoptera: Eucharitidae). Life Sci. Contrib. Royal Ontario Mus . 157: 1– 174. Heraty, J. M. 2000. Phylogenetic relationships of Oraseminae (Hymenoptera: Eucharitidae). Ann. Entomol. Soc. Am . 93: 374– 390. Google Scholar CrossRef Search ADS   Heraty, J. M. 2002. A revision of the genera of Eucharitidae (Hymenoptera: Chalcidoidea) of the World. Mem. Am. Entomol. Inst . 68: 1– 359. Heraty, J. M., D. P. Wojcik, and D. P. Jouvenaz. 1993. Species of Orasema parasitic on the Solenopsis saevissima complex in South America (Hymenoptera: Eucharitidae, Formicidae). J. Hymenopt. Res . 2: 169– 182. Herreid, J. S., and J. M. Heraty. 2017. Hitchhikers at the dinner table: a revisionary study of a group of ant parasitoids (Hymenoptera: Eucharitidae) specializing in the use of extrafloral nectaries for host access. Syst. Entomol . 42: 204– 229. Google Scholar CrossRef Search ADS   Hill, J. K., R. B. Rosengaus, F. S. Gilbert, and A. G. Hart. 2013. Invasive ants–are fire ants drivers of biodiversity loss? Ecol. Entomol . 38: 539. Google Scholar CrossRef Search ADS   Hung, A. C. F., and S. B. Vinson. 1977. Interspecific hybridization and caste specificity of protein in Fire Ant. Science  196: 1458– 1460. Google Scholar CrossRef Search ADS PubMed  Johnson, J. B., T. D. Miller, J. M. Heraty, and F. W. Merickel. 1986. Observations on the biology of two species of Orasema (Hymenoptera: Eucharitidae). Proc. Entomol. Soc. Wash . 88: 542– 549. LeBrun, E. G., R. M. Plowes, and L. E. Gilbert. 2012. Imported fire ants near the edge of their range: disturbance and moisture determine prevalence and impact of an invasive social insect. J. Anim. Ecol . 81: 884– 895. Google Scholar CrossRef Search ADS PubMed  Morrison, L. W. 2000. Mechanisms of interspecific competition among an invasive and two native fire ants. Oikos  90: 238– 252. Google Scholar CrossRef Search ADS   Plowes, R. M., E. G. LeBrun, B. V. Brown, and L. E. Gilbert. 2009. A review of Pseudacteon (Diptera: Phoridae) that parasitize ants of the Solenopsis geminata complex (Hymenoptera: Formicidae). Ann. Entomol. Soc. Am . 102: 937– 958. Google Scholar CrossRef Search ADS   Porter, S. D., and D. A. Savignano. 1990. Invasion of polygyne fire ants decimates native ants and disrupts arthropod community. Ecology  71: 2095– 2106. Google Scholar CrossRef Search ADS   Trager, J. C. 1991. A revision of the fire ants, Solenopsis geminata group (Hymenoptera: Formicidae: Myrmicinae). J.N.Y. Entomol. Soc . 99: 141– 198. Tschinkel, W. R., and J. R. King. 2017. Ant community and habitat limit colony establishment by the fire ant, Solenopsis invicta. Funct. Ecol . 31: 955– 964. Google Scholar CrossRef Search ADS   Varone, L., and J. Briano. 2009. Bionomics of Orasema simplex (Hymenoptera: Eucharitidae), a parasitoid of Solenopsis fire ants (Hymenoptera: Formicidae) in Argentina. Biol. Control  2009: 204– 209. Google Scholar CrossRef Search ADS   Varone, L., J. M. Heraty, and L. Calcaterra. 2010. Distribution, abundance and persistence of species of Orasema (Hym: Eucharitidae) parasitic on fire ants in South America. Biol. Control  55: 72– 78. Google Scholar CrossRef Search ADS   Wheeler, W. M. 1907. The polymorphism of ants with an account of some singular abnormalities due to parasitism. Bull. Am. Mus. Nat. Hist . 23: 1– 108. Wheeler, G. C., and J. Wheeler. 1937. New hymenopterous parasitoids of ants (Chalcidoidea, Eucharidae). Ann. Entomol. Soc. Am . 30: 171– 172. Google Scholar CrossRef Search ADS   Wilson, E. O., and W. L. J. Brown. 1958. Recent changes in the introduced fire ant Solenopsis saevissima (Fr. Smith). Evolution  12: 211– 218. Google Scholar CrossRef Search ADS   Wojcik, D. P., D. P. Jouvenaz, W. A. Banks, and A. C. Pereira. 1987. Biological control agents of fire ants in Brazil, pp. 627– 628. In J. Eder and H. Rembold, (eds.), Chemistry and Biology of Social Insects . Verlag J. Peperny, Munich. © The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.

Journal

Insect Systematics and DiversityOxford University Press

Published: Jan 1, 2018

There are no references for this article.

You’re reading a free preview. Subscribe to read the entire article.


DeepDyve is your
personal research library

It’s your single place to instantly
discover and read the research
that matters to you.

Enjoy affordable access to
over 18 million articles from more than
15,000 peer-reviewed journals.

All for just $49/month

Explore the DeepDyve Library

Search

Query the DeepDyve database, plus search all of PubMed and Google Scholar seamlessly

Organize

Save any article or search result from DeepDyve, PubMed, and Google Scholar... all in one place.

Access

Get unlimited, online access to over 18 million full-text articles from more than 15,000 scientific journals.

Your journals are on DeepDyve

Read from thousands of the leading scholarly journals from SpringerNature, Elsevier, Wiley-Blackwell, Oxford University Press and more.

All the latest content is available, no embargo periods.

See the journals in your area

DeepDyve

Freelancer

DeepDyve

Pro

Price

FREE

$49/month
$360/year

Save searches from
Google Scholar,
PubMed

Create lists to
organize your research

Export lists, citations

Read DeepDyve articles

Abstract access only

Unlimited access to over
18 million full-text articles

Print

20 pages / month

PDF Discount

20% off