PROC. ENTOMOL. SOC. WASH. 109(4), 2007, pp. 779-790 A KEY TO NORTH AMERICAN SPECIES OF TRIOXYS HALIDAY (HYMENOPTERA: BRACONIDAE: APHIDIINAE), WITH A SUMMARY OF THE GEOGRAPHIC DISTRIBUTION, HOSTS, AND SPECIES DIAGNOSTIC FEATURES J. L. FuLBRiGHT, K. S. Pike, and P. Stary (JLF, KSP) Entomologists, Washington State University, Irrigated Agriculture WA Research and Extension Center, 24106 N. Bunn Road, Prosser, 99350, U.S.A. (e-mail: [email protected]); (PS) Entomologist, Institute of Entomology, Academy of Sciences of the Czech Republic, Branisovska 31, 370 05 Ceske Budejovice, Czech Republic — Abstract. A key to North American species of Trioxys (Hymenoptera: Braconidae: Aphidiinae) is provided along with summary tables on geographic origin, distribution, hosts, and diagnostic features. Accompanying the key are illustrations of the anterior portion of the forewing (stigma, Rl and Rs veins), propodeum, petiole, and genitalia, including the seventh metasomal sternite prongs and ovipositor sheaths. Key Words: Aphidiinae, aphid, key, parasitoid, Acanthocaudus, Betuloxys, Binodoxys, Trioxys Trioxys Haliday 1833, and other Trioxys, Smith (1944) recognized 11 spe- genera in Aphidiinae (Hymenoptera: cies, and since then Trioxys has been Braconidae), include larval endoparasi- broken into several distinct genera or toids ofaphid nymphs and adults. There subgenera (Mackauer 1960, Mackauer are over 70 species in Trioxys worldwide 1965, Stary and Schlinger 1967, Stary (Smith 1944; Mackauer 1959, 1960, 1961, 1981, Stary and Remaudiere 1982, van 1965, 1967; Takada 1966, 1979; Stary Achterberg 1997, Chen and Shi 2001, and Schlinger 1967; Stary 1969, 1976, Davidian2005). Keyshavebeendeveloped 1978, 1979; Carver and Stary 1974; Stary for individual aphidiine genera in North and Remaudiere 1977, 1982; Stary and America, including Johnson's (1987) key Bhagat 1978; Stary and Juchnevic 1978; to Praon Haliday, and Pike et al.'s (1999) Marsh 1979; Stary and Marsh 1982; key to Ephedrus Haliday. Keys specific to Gardenfors 1990; Mescheloff and Rosen certain plant-aphid associations also exist, 1993; Stary and Zuparko 1995; Pike et such as a key to the small grain aphid al. 2000; Chen and Shi 2001; Tomanovic parasitoids (Pikeet al. 1997a). An updated and KavaUieratos 2002; Davidian 2005; review of aphid parasitoids of the Pacific Fulbright and Pike 2007). Northwest USA (Pike et al. 2000) brought Few keys exist for distinguishing North together extensive information on tri- America aphidiines, and none are compre- trophic associations and descriptions of hensive for Trioxys. An early key by new species, including species of Trioxys, Gahan (1911) recognized four species of but no keys were presented. — - PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON 780 Trioxys can be recognized by the USNM]; T ductus - 2 UCB (University female's distinctive paired prongs, which of California-Berkeley), 1 Czech; T. are extensions of the seventh metasomal betulae - 5 Czech; T. bonnevillensis — sternite, and the petiole bearing spiracu- 156 WSU, 20 Czech; T californicus - lar tubercles only. Four other aphidiine type UCB; T. cirsii- 1 WSU, 1 Czech; T genera in North America, Acanthocaudus complanatus - 21 WSU, 11 Czech; T. Smith, Betuloxys Mackauer, Binodoxys curvicaudus-20 UCB, 5 WSU, 1 1 Czech; Mackauer, and Cristicaudus Stary and T. exareolatus~ type USNM; T gahani Remaudiere, also possess metasomal type USNM, 2 WSU; T ibis - 2 Czech; sternite prongs. Acanthocaudus, Bino- T. infrequens ~ type USNM; T latgei~ 6 doxys, and Cristicaudus differ in having Czech; T. mexicanus - 2 Czech; T. secondary, as well as spiracular tuber- rnonelliopsis - 3 Czech; T. pcdlidus - 261 cles, on the petiole. Betuloxys bears only WSU, 35 Czech; T rosae - type USNM, spiracular tubercles, but the apical por- 6 paratypes [4 WSU, 6 Czech, 2 USNM]; tions of the prongs are differentiated, T. setaceus - type USNM, paratypes (3 dilated, and bear several lanceolate, WSU, 2 Czech); T. sunnysidensis - type perpendicular setae on the dorsal sur- USNM, 40 paratypes [WSU 26, 8 face. Acanthocaudus further differs from USNM, 6 Czech]; T. tenuicaudus - 2 Trioxys, Betuloxys, Binodoxys, and Cris- WSU, 1 Czech). Authors' collections ticaudus in having a secondary projection were preserved in 70-95% ETOH, some on its prongs (Stary 1981). as whole mounts on pointed or rectan- Species within Trioxys can be distin- gular paper tabs, and some as whole and/ guished by one or more of the following or dissected mounts on glass slides. features: propodeal areola presence or Slide mounted whole specimen prepa- — absence, antennal flagellomere number, ration. Parasitoids were cleared and metasomal sternite prong shape and mounted using techniques by P. Stary, length, prong dorsal and ventral setae and modified by G. Graf of Washington number, prong apical bristle type and State University as follows: (1) parasitoid number, ovipositor sheath shape, and immersed in 95% ETOH; (2) specimen forewing stigma and Rl(=metacarpus) transferred to new test tube ofwater and length. Information on host specificity is inverted several times; (3) water decanted also helpful for species differentiation. and specimen placed in test tube of 10% The North American and world distribu- KOH; (4) test tube placed in heating tions, as well as host aphid associations block for approximately 2 minutes at of each species, as presently recognized, 98 C (heating time varied depending on are provided in the paper. sclerotization and state of specimen; dry materials required more time); (5) speci- Materials and Methods men removed from KOH, placed in test Material examined. Trioxys species tube of water and washed and inverted examined were from authors' field col- several times to rinse off KOH; (6) lections and museum loans. Numbers of specimen placed in 3 drops of mounting specimens examined and location are as medium (200 g gum arable, 550 g chloral follows T. anieraceris - type USNM hydrate, 60 ml glycerin, and 400 ml dis- : (National Museum of Natural History, tilled water mixed and filtered through Washington), 2 paratypes Czech (Czech glass wool) and positioned; (7) coverslip Academy of Sciences, P. Stary collec- placed over specimen; (8) code number tion); T artemisiarum - type USNM, 24 written on slide and slide allowed to dry WSU paratypes [19 (Washington State horizontally for2-3 weeks on slidewarm- University-Prosser), 3 Czech and 2 er at 50°C; (9) mount sealed around VOLUME NUMBER 109, 4 781 coverslip with glyptal, an alkyd-based 77-84 were authors' original drawings; sealant, to prevent dehydration and crys- Fig. 50 was authors' conceptual illustra- talhzation (Pike et al. 2003); and (10) slide tion of the propodeum based on the fully labeled. — originaldescription (Smith 1944); Figs. 5, Parasitoiddissection. Specimenswere 6, and 8 were redrawn after Pike et al. sometimes dissected for better feature 1997b; Fig. 9 after Mackauer 1959; viewing after placement in mounting Fig. 10 after Takada 1966; Figs. 11-12, medium as follows: (1) head cut from 36 after Stary 1976; Fig. 14 after Toma- body with antennae attached or separat- novic and Kavallieratos 2002; Figs. 15- ed; (2) mesonotum separated from body 16 after Stary 1979; Fig. 24 after Stary with wings attached or separated; (3) and Zuparko 1995; Figs. 53-56 after propodeum separated from body, petiole Stary and Remaudiere 1977; Figs. 57-60 sometimes left connected to propodeum after Stary and Remaudiere 1982; in smaller specimens; (4) hind legs sepa- Figs. 66c, 68 after Stary 1978; Figs. 69- rated from body; (5) metasoma cut and 72 after Pike et al. 1996; and Figs. 73-76 positioned for (a) dorsal view of petiole after Pike et al. —2000. and (b) posterior view of metasoma, Terminology. Descriptive morpholo- including lateral view of genitalia; and gy was after Sharkey and Wharton (6) genitalia removed from metasoma if (1997). not protruding or visible. Results and Discussion Slide mounted specimen measure- — ments. Whole and dissected mounts A listing of aphidiine parasitoids of were reticle measured using a compound North America can be found in Marsh microscope at magnifications of 50- (1979). Research within the past decade 400X. — (Pike et al. 1996, 1997a, 2000) has Dry mounted specimens. Whole supplemented the listing of taxa and mounts were placed on pin-pointed or aphid host range information. Table 1 rectangular paper tabs. summarizes the full listing of North — Illustrations. Line drawings of many American species of Trioxys. Host range, specimens were based on features cap- faunal composition, and ecology of tured with a Nikon Coolpix 990tm Trioxys parasitoids for much of North digital camera through an Olympus America have not been explored thor- SZX12TMdissectingmicroscopeorwitha oughly. As indicated in the introduction, DEC13MTM digital eyepiece camera there is a lack of updated keys for many through a Zeiss Axiolab^M compound genera of Aphidiinae, including Trioxys. microscope. Illustrations of the wing, Table 2 outlines distinguishing charac- propodeum, petiole, genitalia and associ- ters used in the key. ated structures were provided for each The North American Trioxys fauna is species. For some rare species, illustra- currently comprised of 22 species, 15 tions were drawn from the type, i.e., T. native and 7 introduced (Table 1). Mem- californicus from the University of Cali- bers of the genus are associated with fornia Essig Museum of Entomology, assorted groups of aphids in arborico- and T. exareolatus, T. gahani, and T. lous, grassy riparian, sagebrush, and infrequens from the National Museum of selected agroecosystem habitats. Eleven Natural History, Washington, DC. Other species of Trioxys utilize aphids in species were drawn from the type, para- Myzocallidinae and Drepanosiphinae, type or other material, or redrawn after most of which are arboricolous (i.e., previously published drawings. Figs. 1^, aphids on alder, birch, crepe myrtle, 7, 13, 17-23, 25-35, 37-52, 61-66b, 67, elm, hazel, linden, maple, oak, pecan. 782 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON T. a/fieracen's „„;„„,.;,„,..,,.„,h ^j, ovipositor prong T.a/7e/fiis/amm prongapex dilatedbristles \. 7 -.iOJAuL prongdorsalsetae T. ai/cfi/s T.betu/ae T.do/mevi7/ensis 20 prongapex T. ca/ifomi'cus clawlikebristle 21 Figs. 1-24. Trioxysmorphological features [columns 1, 2, 3, and 4 (left to right) = wings (part only), propodea, petioles, genitalia (includes last metasomal sternite prongand ovipositorsheath), respectively]. 1^, T. ameraceris. 5-8, T. artemisiarum. 9-12, T. auctus. 13-16, T. betulae. 17-20, T. bonnevillensis. 21- 24, T. californicus. VOLUME NUMBER 109, 4 783 T. c/rs/7 T. comp/anatus T. cufvicaudus T. exareo/atiis T.ga/ia/ii '^=^^ T. ibis Figs. 25-48. Trioxysmorphological features[columns 1, 2, 3, and4(leftto right) = wings (part only), propodea, petioles, genitalia (includes last metasomal stemite prong and ovipositor sheath), respectively. 25-28, T. cirsii. 29-32, T. complanatus. 33-36, T. curvicaudus. 37^0, T. exareolatus. 41-^4, T. gahani. 45- 48, T. ibis. 784 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON T. infrequens T. /a/gei T.mex/ca/ius T. /no/ie///ops/s T.pa//idus 66a 66b i 66c Figs. 49-68. Trioxysmorphological features [columns 1. 2, 3, and4(leftto right) = wings(part only), propodea, petioles, genitalia (includes last metasomal sternite prong and ovipositor sheath), respectively. 49-52. T. infrequens. 53-56, T. latgei. 57-60, T. mexicaniis. 61-64, T. monelliopsis. 65-68, T. pallidus. and walnut). Trioxys compkmatus Quilis water lily aphid, Rhopalosiphum nym- uses a myzocallidine aphid on alfalfa, phaeae (L.) and bird cherry-oat aphid, R. viz. the spotted alfalfa aphid, Therioaphis padi (L.); T. sunnysidensis Fulbright and thfolii (Monell) (Table 1). Nine species Pike on bird cherry-oat aphid; T. arte- of Trioxys attack solely aphids in Aphi- misiarum Pike and Stary and T. bonne- diinae as follows: T. auctus (Haliday) on villensis Smith on sage aphids, T. exar- VOLUME NUMBER 109, 4 785 T. rosae T.setaceiis T.sunnysi'densis T. temiicaudiis Figs. 69-84. Trioxysmorphological features [columns 1, 2, 3, and4 (leftto right) = wings (part only), propodea, petioles, genitalia (includes last metasomal sternite prong and ovipositor sheath), respectively. 69-72, T. rosae. 11>-16, T. setaceus. 77-80, T. sunnysidensis. 81-84, T. tenuicaudns. eolatus Viereck and T. rosae Pike and adapted to native and/or long established Stary on rose aphids; T. gahani Smith on introduced aphids. blueberry aphid, Ericaphis scainmelli Parasitoid determinations should be (Mason) and Chaetosiphon; T. latgei based on multiple factors whenever Stary and Remaudiere on juniper aphid, possible. Parasitoids which have been Sanbornia juniperi Pergande; and T. identified through the key should be setaceus Pike and Stary on serviceberry checked against primary distinguishing aphid, Acyrthosiphon macrosiphum (Wil- features (Table 2), compared to the son) (Table 1). For two species of illustrations, and checked against the Trioxys, T. infrequens Smith and T. host aphid and distributional records ovalis (Provancher), the hosts are un- where available. known. Of the Trioxys species acciden- Success in identifying parasitoids is tally or purposely introduced into North facilitated when quality and quantity America \T. auctus (Haliday), T. betulae material are available. Freshly reared, Marshall, T. cirsii (Curtis), T. complana- cleared and mounted specimens are best. tus Quilis, T. ibis Mackauer, T. pallidus One of the challenges in making deter- (Haliday), and T. tenuicaudns Stary], minations with confidence is being able some have become adapted or partially to see the key features. With point- PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON 786 Table L Trioxrs ofNorth America: origin, hosts. North American distribution. Species Origin HostAphidsSubfamily(Genus) Reported Distribution ameruceris Smith 1944 Nearctic Drepanosiphinae (Drepanaplns) E. Can., E. USA (Smith 1944, Marsh 1979) WA arteniisiariim Pike and Stary Nearctic Aphidinae [Aphis (Zyxaphis), (Pike and Stary 1997b) 1997 Microsiphoniella] aiictus (Haliday 1833) Palearctic Aphidinae {Rhopalosiphum) E. Can. (QC) betulae Marshall 1896 Palearctic Myzocallidinae {Calaphis, E. Can. (NB, ON, QC), NH Clethrobius, Symydobius) (Marsh 1979) bonnevillensis Smith 1944 Nearctic Aphidinae (sage aphids') ID, WA, UT, Mexico (Smith 1944, Stary and Remaudiere 1982, Pike et al. 2000) californicus Stary and Nearctic Myzocallidinae {Eucallipterus) CA (Stary and Zuparko Zuparko 1995 1995) WA cirsii (Curtis 1831) European Drepanosiphinae {Drepanosiphum) (Pike et al. 2000) complanatus QuiWs 1931 Eurasian Myzocallidinae (Therioaphis) Can., USA (Marsh 1979, Pike et al. 2000) curvicaudus Mackauer 1967 Nearctic Myzocallidinae {Eucallipterus, CA (Mackauer 1967, Stary Tuberculatus) 1978) exareolatiis Viereck 1916 Nearctic Aphidinae (Macrosiphum) CT (Viereck 1916, Marsh 1979) WA galumi Smith 1944 Nearctic Aphidinae (Evicapliis, NJ, (Smith 1944, Marsh Chaetosiphon) 1979) ibis Mackauer 1961 European Myzocallidinae (Betulaphis) E. Can. (NB) (Mackauer 1961, Marsh 1979) infreqiiens Smith 1944 Nearctic Unknown W. Can., CO (Marsh 1979) ME latgei Stary and Nearctic Aphidinae {Sanbornid) (Stary and Remaudiere Remaudiere 1977 1977) mexicanus Stary and Nearctic Myzocallidinae {Myzocallis) Mexico (Stary and Remaudiere 1982 Remaudiere 1982) monelliopsis Stary and Nearctic Myzocallidinae (Monelliopsis) GA (Stary and Marsh 1982) Marsh 1982 ovalis (Provancher 1886) Nearctic Unknown2 E. Can. (Smith 1939, 1944, Marsh 1979) pallidus (Haliday 1833) Palearctic Myzocallidinae (tree aphids^) W. USA (Marsh 1979, Pike et al. 2000) WA rosae Pike and Stary 1996 Nearctic Aphidinae {Macrosiphum) (Pike et al. 1996, 2000) setaceus Pike and Stary 2000Nearctic Aphidinae {Acyrthosiphon) MT, WA (Pike et al. 2000) WA sunnysidensis Fulbright Nearctic Aphidinae {Rhopalosiphum) (Fulbright and Pike and Pike 2007 2007) WA tenuicaudus Stary 1978 Palearctic Myzocallidinae {Eucallipterus, (Stary 1978, Pike et al. Myzocallis, Tinoccdlis, 2000) Tuberculatus) 1 Aphis {Zyxaphis), Artemisaphis, Epameibaphis, Elabellomicrosiphum, Microsiphoniella, Obtusicauda, Pleotrichophorus, Pseudoepameibaphis. ~ Reared from an aphid on Helianthus sp. (Smith 1939). 3 Chromaphis, Eucallipterus, Hoplocallis, Monelliopsis, Myzocallis, Panaphis, Tinocallis, Tuberculatus. mounted specimens on pins, it is not erly sealed and labeled, become perma- always possible to see or see clearly all of nent holdings and are easily viewable. the distinguishing characters used in the key. Clearing and slide mounting repre- Key to Female Trioxys of sentative specimens is recommended, if North America not essential. Slide mounts, when prop- [Trioxys ovalis (Provancher) de- VOLUME NUMBER 109, 4 787 Table2. TrioxysofNorthAmerica: Antennalsegmentno., prongdorsalsetaeno., prongapical bristle type and no., and propodeal sculpture. Species 788 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON Myzocallis on oak; Mexico) (Figs. 57- - Petiole length/width at spiracles 1.5-1.9 60) mexicanus Stary and Remaudiere (Figs. 39, 43, 75); propodeum with some - Prongdorsal surfacewith setae; 1-3 dilated carinae (Figs. 38, 42, 74) 17 apical bristles (Figs. 4, 28) 9 17(16). Prongventral surfacewith > 12 setae 9(8). Prong dorsal surface with 2-3 setae (Fig. 76) (host, Acyrthosiphonmacrosiphum (Fig. 4) (host, Drepanaphis on maple; east- on western serviceberry; Montana and ern Canada, Florida, Missouri, Ohio, Washington) (Figs. 73-76) Tennessee) (Figs. 1^) ameraceris Smith setaceus Pike and Stary . . . - Prong dorsal surface with 6-8 setae - Prong ventral surface with usually < 10 (Fig. 28) (host, Drepanosiphum on maple; setae (Figs. 40, 44) (host,not Acyrthosiphon known distribution, Asia, Australia, Eur- macrosiphum) 18 ope, Washington) (Figs. 25-28) cirsii(Curtis) 18(17). Prong dorsal surface bearing 4 distal 10(2). Prongshortandstraight,withtwolong setaeapproximately twiceaslongas4basal apical bristles (Fig. 56); petiole short, only setae; tip of Rl vein yellowish or light slightly longer than wide (Fig. 55) (host, ferruginous (Smith 1944); stigma length Sanbornia juniperi on juniper; Maine) about 2X Rl vein; Fl and F2 antennal (Figs. 53-56) latgei Stary and Remaudiere segments long, 0.19 and 0.16 mm, respec- . . . - Not with the combination of features tively (host, rose aphid; Connecticut, rare, above 11 described from a single specimen) 11(10). Prong dorsal surface with one pre- (Figs. 37^0) exareolatus Viereck apical seta (Fig. 84); ovipositor sheathvery - Prongdorsal surface setaenot as above; Fl shallowly emarginate on ventral side and F2 antennal segmentsshort, each0.11- (Fig. 84) (host, various tree aphids - 0.12 mm (hosts, Ericaphis, Chaetosiphon; Eucallipterus, Myzocallis, Tinocallis, Tiiber- New Jersey and Washington (Figs. 41- ) citlatus; Australia, Europe, Russia, and 44) gahani Smith Washington) (Figs. 81-84) tenuicaudus Stary 19(15). Propodeum entirely smooth - Prong dorsal surface with 4 or more setae (Fig. 18), Rl vein short, < 0.25X stigma (Fig. 80) 12 length (Fig. 17) (hosts, sage aphids- Aphis 12(11). Petiole with numerous longitudinal (Zyxaphis), Artemisaphis, Epameibaphis, striations in proximal half (Fig. 11) (host, FlabeUomicrosiphum, Microsiphoniella, Ob- Rhopalosiphum; Eurasia and Ontario [in- tusicauda, Pleotrichophorus, Pseudoepamei- troduced]) (Figs. 9-12) ductus (Haliday) baphis; Idaho, Mexico, Utah, and Wash- . . . - Petiole without striations (Fig. 79) (host, ington (Figs. 17-20) ) Rhopalosiphum on wheat; Washington) bonnevillensis Smith (Figs. 77-80) - Propodeum with at least some carinae sunnysidensis Fulbright and Pike (Figs. 30), Rl vein length variable 20 13(1). Antenna 13-segmented (host, Euccd- 20(19). Propodeum smooth except for di- Upterus tiliae; California; species rare, de- vergent carinae in posterior declivity scribed from a single specimen) (Figs. 21- (Fig. 70); Rl vein 0.3X stigma length 24) ccdifornicus Stary and Zuparko (Fig. 69); (host, Macrosiphum rosae on - Antenna 11-12 segmented 14 rose; Washington (Figs. 69-72) ) 14(13). Petiole dilating from poorly promi- rosae Pike and Stary nent spiracular tubercles to apex (Fig. 7); - Propodeum with irregular lateral carinae antenna 12-segmented; (hosts, various (Figs. 30, 66a, 66b); Rl vein 0.4X stigma sagebrush aphids - Aphis (Zyxaphis), Mi- length or greater (Figs 29, 65) 21 crosiphoiue/la; Washington) (Figs. 5- 21(20). [Species in couplet morphologically 8) artemisiarum Pike and Stary similar - check for a match with correct - Petiole spiracles on prominently visible host] Ovipositorsheath ventral marginwith tubercles (Fig. 51) antenna usually 11- 5-7 setae excluding apical setae (Fig. 68) segmented; 15 (hosts, various tree aphids - Chromaphis, 15(14). Prong dorsal surface with 6-8 setae Eucallipterus, Hoplocallis, Monellia, Monel- (Fig. 52) 16 liopsis, Myzocallis, Tuberculatum, Tinocallis, - Prong dorsal surface with 2-5 setae Panaphis; California, Oregon, Washington (Fig. 20) 19 (Figs. 65-68) .... pallidus(Haliday) (in part) 16(15). Petiole length/width at spiracles > 2 - Ovipositor sheath ventral margin with 3-A (Figs. 51); propodeum smooth (host, un- setaeexcludingapical setae(Fig. 32)(hosts, known; Colorado, western Canada) Therioaphis-NorthAmerica;, Pterocallis- (Figs. 49-52) infrecpiens Smith Eurasia) (Figs. 29-32) compkmatus Quilis . .