PROC. ENTOMOL. SOC. WASH. 99(4), 1997. pp. 748-755 LIFE HISTORY AND DESCRIPTION OF IMMATURE STAGES OF TRUPANEA SIGNATA FOOTE (DIPTERA: TEPHRITIDAE) ON GNAPHALIUM LUTEO-ALBUM L. IN SOUTHERN CALIFORNIA Richard D. Goeden and Jeffrey A. Teerink CA Department of Entomology, University of California, Riverside, 92521, U.S.A. — Abstract. Trupanea signata L. is a narrowly oligophagous, multivoltine, gregarious, obligately gallicolous fruit fly (Diptera: Tephritidae) studied in southern California on Gnaphaliiim luteo-albiim L. This host plant is an introduced weedy annual of Old World origin to which this tephritid has transferred from indigenous, congeneric hosts, an un- common occurrence among nonfrugivorous North American Tephritidae. The egg, third- instar larva, and puparium are described and figured. The eggs are inserted into apical and axillary buds. From one to six larvae feed gregariously within an open cavity in the expanded pith parenchyma ofgalls on axillary branches and stems during all three instars. The galls are elongate-obclavoidal, sometimes bear axillary branches and flower heads, and are covered by a wooly investiture. Pupariation occurs inside the gall. The adults emerge and exit the gall through a common channel by pushing aside a thin, pre-formed, apical, "gall cap." The adults are long-lived and are the overwintering stage. The life cycle follows the aggregative pattern and at least two generations, one each in spring and fall, are produced annually on G. hiteo-album. Two species of solitary, larval-pupal, hy- menopterous endoparasitoids are reported: Eurytoma sp. (Eurytomidae) and Pteromalus sp. (Pteromalidae). Key Words: Insecta, Trupanea, Gnaphalium, biology, taxonomy of immature stages, galls, oligophagy, parasitoids The genus Trupanea (Diptera: Tephriti- immature stages of three of these species dae) occurs worldwide and is a numerically also described (Cavenderand Goeden 1982, large and widespread taxon of nonfrugivo- Headrick and Goeden 1991, Knio et al. rous fruit flies in North America and Cali- 1996a). This and our next five papers will fornia (Foote and Blanc 1963, Foote et al. more than double the number of species of 1993). As such, the adults are among the Trupanea for which life histories and im- most commonly encountered, reared or mature stages are well known, beginning swept tephritids; however, the life histories here with the indigenous, obligate gall-for- of most species remain little known, and ^^^^^ ^- ^^8^^^^^ Foote. several species are difficult to distinguish Materials and Methods morphologically (Foote 1960, Foote et al. 1993). Detailed life histories offive species Our field studies on T signata mainly fo- of Trupanea from southern California have cused on laboratory dissections ofgalls col- been published (Cavender and Goeden lected on Gnaphalium luteo-album L. at 1982, Goeden 1987, 1988, Headrick and different locations in central and southern Goeden 1991, Knio et al. 1996b), and the California during 1989-91: (1) N end of — — VOLUME 99, NUMBER 4 749 Hemet Lake at 1424-m elevation, San Ber- spotted with honey (Headrick and Goeden nardino Nat. Forest (S section). Riverside 1991, 1994) for observations oftheir court- Co., 29.ix.1989 and ll.ix.l990; (2) along ship and copulation behavior. Deer Creek in the Morton Flat area at 550 Plant names used in this paper follow m. Tulare Co., 14.vi.1990; (3) Box Springs Munz (1974, as updated by Hickman Grade between Moreno Valley and River- 1993); tephritid names and adult terminol- side at 470 m. Riverside Co., 20- ogy follow Foote et al. (1993). Terminology 28.ii.1991. Excised galls and uprooted gall- and telegraphic format used to describe the bearing shoots were transported in cold- immature stages follow Knio et al. (1996a) chests in an air-conditioned vehicle to the and Goeden and Teerink (1996a, b, c, laboratory and stored under refrigeration 1997a, b) and our earlier works cited there- for subsequent dissection, photography, de- in. Means ± SE are used throughout this scription, and measurement. Fifteen eggs paper. Voucher specimens of T. signata and recovered from ovipositional cagings and its parasitoids reside in the research collec- two second- and eight third-instar larvae, tions ofRDG; preserved specimens ofeggs, and four puparia dissected from galls were larvae and puparia are stored in a separate preserved in 70% EtOH for scanning elec- collection of immature Tephritidae main- tron microscopy (SEM). Additional puparia tained by JAT were placed in separate, glass shell vials stoppered with absorbant cotton and held in Results and Discussion humidity chambers at room temperature for Taxonomy adult and parasitoid emergence. Specimens for SEM were hydrated to distilled water in Adult. Trupanea signata was described a decreasing series of acidulated EtOH. from reared and swept adults collected from They were osmicated for 24 h, dehydrated various locations in California by Foote through an increasing series of acidulated (1960), who also pictured the wing of a fe- EtOH and two, 1-h immersions in Hexa- male. Foote et al. (1993) illustratedthe head methlydisilazane (HMDS), mounted on of an adult in side view and the wing pat- stubs, sputter-coated with a gold-palladium tern of a female, and noted that the wing alloy, and studied with a JEOL JSM C-35 pattern ofthe male ". .does not differ from . SEM in the Department of Nematology, that of the female in any important re- University of California, Riverside. spect." Most adults reared from isolated puparia Immature stages. Egg: Twenty-one were individually caged in 850-ml, clear- eggs of T. signata were white, opaque, plastic, screened-top cages with a cotton smooth; with an elongate-ellipsoidal body, mm wick and basal water reservoir and provi- 0.69 ± 0.005 (range, 0.65-0.74) long, mm sioned with a strip of paper toweling im- 0.21 ± 0.004 (range, 0.17-0.23) wide, pregnated with yeast hydrolyzate and su- smoothly rounded at tapered posterior end, crose. These cages were used for longevity and with a peg-like anterior pedicel, 0.02 studies, and those with the wicks wrapped nmi long (Fig. 1); a single row ofaeropyles around root-bearing shoots of G. luteo-al- circumscribes the pedicel (Fig. 1). biim for oviposition studies, in the insectary The egg of T. signata is similar in shape of the Department of Entomology, Univer- to the eggs of other Trupanea species pre- sity of California, Riverside, at 25 ± 1°C, viously described. The egg is larger in and 14/10 (L/D) photoperiod. Virgin male width and length than T. californica Mal- and female flies obtained from emergence loch, approximately the same size as T. im- vials were paired (n = 16) in clear-plastic perfecta (Coquillett), and shorter than T. petri dishes provisioned with a flattened, conjuncta (Adams), T. bisetosa (Coquillett) water-moistened pad of absorbant cotton and T. nigricornis (Coquillett) (Goeden 750 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON segment smooth medially, circumscribed anteriorly by minute acanthae (Fig. 2F-1); posterior spiracular plates (Fig. 2F-2), with mm three ovoid rimae, ca. 0.038 in length (Fig. 2G-1), and four interspiracular pro- cesses each with 3-6 branches, longest mm measuring 0.013 (Fig. 2G-2); inter- mediate sensory complex ventrad of pos- terior spiracular plates among the minute acanthae (Fig. 2F-3), consist of a medusoid sensillum (Fig. 2H-1), and a stelex sensil- lum (Fig. 2H-2). Triipanea signata is similar in general Fig. 1. Egg of Tnipcmea signata: pedicel with appearance to other described species, i.e., aeropyles. Trupanea califomica (Headrick and Goe- den 1991), T. bisetosa and T. nigricomis 1987, 1988; Headrick and Goeden 1991; (Knio et al. 1996a). The anterior portion of Knio et al. 1996a). The single row of aero- the prothorax is circumscribed by minute pyles circumscribing the pedicel is similar acanthae and rugose pads, which appear to to T. nighcomis, whereas, T. bisetosa com- be characteristic of the genus Trupanea monly has two rows of aeropyles (Knio et (Headrick and Goeden 1991, Knio et al. al. 1996a). 1996a). Differences among Trupanea spe- Third instar: White, barrel-shaped, taper- cies described to date are found in the ab- ing anteriorly, rounded posteriorly; minute dominal lateral spiracular complex. This acanthae circumscribe each thoracic and ab- complex in T. califomica includes a single dominal segment anteriorly, gnathocephalon verruciform sensillum; in T. nigricomis, conical (Fig. 2A), rugose pads dorsally and two verruciform sensilla; and in T. bisetosa, laterally, rugose pads laterad of mouth lu- two verruciform sensilla and a placoid type men serrated on ventral margin (Fig. 2A-1); sensillum (Headrick and Goeden 1991, dorsal sensory organ consists of a single Knio et al. 1996a). Trupanea signata also dome-shaped papilla (Fig. 2A-2, B-1); an- differs slightly in the number of branches terior sensory lobe bears four sensory or- in the interspiracular processes; T. califor- gans, lateral sensory organ with a distinct nica and T. bisetosa possess 6-8 branches, central papilla (Fig. 2B-2); stomal sense or- T. nigricomis is similar to T. signata in gan ventrolaterad of anterior sensory lobe having 3-6 branches (Headrick and Goeden (Fig. 2B-3); mouth hooks tridentate; rugose 1991, Knio et al. 1996a). pads circumscribe prothorax posteriorly of Puparium: Puparium of T. signata shiny minute acanthae (Fig. 2C-1), single row of black, elongate-ellipsoidal, anterior end verruciform sensilla circumscribe prothorax bears the invagination scar (Fig. 3A-1), and medially (Fig. 2C-2); anterior thoracic spir- acles on posterior margin ofprothorax, bear anterior thoracic spiracles (Fig. 3A-2), cau- 4-5 rounded papillae (Fig. 2C-3, 2D); me- dal segment bears the posterior spiracular tathoracic lateral spiracular complex con- plates (Fig. 3B-1), a band of minute acan- sists of a spiracle and a single verruciform thae (Fig. 3B-2), and the intermediate sen- sensillum; abdominal lateral spiracular sory complex (Fig. 3B-3). Forty-four pu- complex consists of a spiracle (Fig. 2E-1), paria of T. signata averaged 3.23 ± 0.04 a verruciform sensillum (Fig. 2E-2), £md (range, 2.55-3.80) mm in length; 1.48 ± mm placoid-type sensillum (Fig. 2E-3); caudal 0.03 (range, 1.10-2.35) in width. —— VOLUME 99. NUMBER 4 751 — Fig. 2. Third instar of Trupanea signata: (A)—gnathocephalon, anterior v—iew, 1 serrated rugose p—ads, 2 dorsal sensory organ; (B) anterior—sensory lobe, 1 dorsal sen—sory organ. 2 lateral sen—sory organ, 3 stomal sense organ; (C) anterior view. 1 prothoracic rugose pads, 2 verruciform sensilla, 3 anterio—r thoracic spi- racle; (D) anterior thoraci—c spiracle; (E) fourth abdominal segment, lateral—spiracularcomplex. 1—spiracle, 2 verruciform sen—sillum, 3 placoid-type sensillum; (F) caudal segment, 1 minu—te acanth—ae, 2 posterior spi- racular plate, 3 intermediate sensory com—plex: (G) posterior spira—cular plate, 1 rima, 2 interspiracularpro- cess; (H) intermediate sensory complex, 1 medusoid sensillum, 2 stelex sensillum. 752 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON indigenous, host-plant species that is con- generic with native hosts in the southern California flora (Munz 1974). Besides Campiglossa genalis (Thomson) on Senecio spp. (Goeden et al. 1994), few other ex- amples of such host-plant transfer by indig- enous, oligophagous, nonfrugivorous Te- phritidae have been documented (Goeden 1996). The biological significance of the sweep record for a female of T. signata re- ported by Goeden (1986) and Foote et al. (1993) was its location on Santa Cruz Is- land, not the nonhost, Baccharis pilularis de Candolle from which it was swept, which like all-too-many sweep records for adult, nonfrugivorous Tephritidae are poor and often misleading indicators of repro- ductive-host-plant affinities. Accordingly, T. signata is oligophagous on certain spe- cies of Anaphalis and Gnaphalium of the subtribes Cassiniinae and Gnaphaliinae, re- spectively, and the tribe Gnaphalieae ofthe Asteraceae (Bremer 1994). Unlike T. con- juncta, T. signata apparently is an obligate, not a facultative gall former, and has not been reared from flower heads ofAnaphalis Fig. 3. —Puparium of Trupanea—signata: (A) ante- or Gnaphalium spp. (Foote 1960, Foote et rior end, 1 invagination scar,—2 anterior thoracic al. 1993, Goeden 1983, 1987, 1992, unpub- spiracles—; (B) caudal segment,—1 posterior spiracular lished data). Also, our study sites 1 and 2 plate, 2 minute acanthae. 3 intermediate sensory were in grazed, disturbed, riparian areas and complex. site 3 was in a regularly and well irrigated, roadside flower bed, so all galled plants Distribution and Hosts were well-watered. The distribution of T. signata mapped by Biology Foote et al. (1993) included the western — U.S. north ofMexico and Canada, with this Egg. Eggs were inserted pedicel-last, species recorded from Arizona, California, singly or side-by-side, in small clusters of Colorado, Nebraska, New Mexico, Oregon, two to four for ca. two-thirds their lengths Texas, and Washington as well as British in terminal buds of stems or upper axillary Columbia. Foote (1960) and Foote et al. branches (Fig. 4A). Unlike T. conjuncta, (1993) reported Anaphalis sp. and Gna- which also forms galls, the egg clusters phalium stramineum Kunth as hosts, be- were not glued together posteriorly (Goe- sides G. luteo-album reported by Goeden den 1987)—. (1992). Gnaphalium luteo-album is an in- Larva. Newly-hatched first instars tun- troduced annual plant species ofOld World nelled basipetally into the pith of the stem origins (Munz 1974). Thus, T. signata like or axillary branch to which they confine T. californica (Headrick and Goeden 1991), their feeding (Fig. 4B-D). The larvae feed provide examples of indigenous, oligopha- singly or gregariously in open, elongate gous tephritids that have adopted this non- central cavities on proliferating pith paren- VOLUME 99, NUMBER 4 753 Fig. 4. Life stages of Tnipanea signata on Gnaphalium luteo-album: (A) pair of eggs (arrow) inserted in axillary bud, (B) third instar in feeding cavity below partially dislocated gall cap, (C) exterior view of apical bud gall, (D) gall ofaxillary branch with flowerhead at apex, (E) Four puparia incommon feedingcavitybelow apical exit channel and gall cap. (F) Female adult at rest. Lines = 1 mm. chyma (callose tissue), shallowly pitting the which it coats inside with voided liquid fe- walls, and continually expanding the ces. The feces dry, harden, and hold this lengths and widths ofthe cavities during all cap in place during pupariation (Fig. 4D). three stadia (Fig. 4D). The gall cavities re- The larva then returns to the main gall cav- mained free offrass and solid waste, except ity, where it and other mature larvae within for the discarded cephalopharyngeal skele- pupariate with their heads facing the gall tons ofthe first and second instars. The ful- apex. — ly grown third instar extends the cavity dis- Pupa. One hundred thirteen full-sized tally by eating out a 5.2 ± 0.3 (range, 2-8) galls collected at all three study sites each mm-long, exit tunnel (n = 25) through the contained an average of 2 ± 1 (range, 1-6) shoot tip to just beneath the apex, leaving puparia (Fig. 4-E). These galls were elon- a hollow, tomentum-covered gall "cap," gate-clavoidal in shape and covered with a 754 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON whitish tomentum (Fig. 4B, C). They av- gan in the mornings, usually after 0900 h eraged 14.9 ± 0.6 (range, 6.0-41) mm in PST and ended ca. midday. The courtship length and 4.8 ± 0.1 (range, 1.7-7.8) mm display was similar to that described for in widest width near the apices, expanding other species of Trupanea by Headrick and gradually distally from a basal, greenish, to- Goeden (1991, 1994) and Knio et al. mentose, side branch or stem, and incor- (1996b). Males of T. signata regularly hung porating an average of 3.9 ±0.1 (range, 1- upside down from the covers of arenas 7) nodes. The galled branch or shoot tips when displaying and distending their ab- were not shortened in length, but rather domens. When the abdomen was distended, mainly expanded in width, and like their it was held flexed and synchronous or asyn- ungalled counterparts, bore no or from one chronous wing displays were exhibited; to five vegetative or floral branches laterally however, when a female was near, males and apically (Fig. 4). Some of these apical always reverted to synchronous wing exten- branches were killed when the bud caps sions. Mating was not observed in this spe- were formed. The cavities within these ma- cies, but see Headrick and Goeden (1994) ture galls measured 7.1 ± 0.3 (range, 3.1- for descriptions of mating behaviors com- 18.9) mm long by 2.6 ± 0.1 (range, 1.3- mon to several southern California species 6.9) mm in maximum width. Larger galls of Trupanea. — typically contained the most puparia, which Seasonal history. The life cycle of T. lay freely, touching laterally or apically, signata in southern California follows the within the—common cavity (Fig. 4E). aggregative pattern in which the long-lived Adult. Adults emerged through the adults in reproductive diapause overwinter same exit tunnel after pushing aside the gall probably in riparian habitats and aggregate cap. Adults were long-lived under insectary on preblossom host plants during the fol- conditions, as males averaged 48 ± 15 lowing spring to mate and reproduce (range, 21-158) days, and 18 females (Fig. (Headrick and Goeden 1994). A second 4F) averaged 74 ± 1 1 (range, 31-172) late-summer or early-fall generation repro- A days. 7 week-old female contained 35 duces on flowering shoots of G. luteo-al- full-size ova, and eight 3-4 week-old fe- bum, and another generation or two may be males laid an average total of 24 ± 4 produced on the above-mentioned, or as yet (range, 7-34) eggs in ovipositional cagings. unidentified, alternate host plants, especial- No free-living adults were observed in na- ly at higher elevatio—ns. ture. Natural enemies. Two species of Hy- In petri dish arenas, both sexes displayed menoptera were reared from puparia of T. synchronous and asynchronous supinations signata as solitary, larval-pupal endopar- along with wing vibrations and hamation. asitoids: Eurytoma sp. (Eurytomidae) and During asynchronous supination, one wing Pteromalus sp. (Pteromalidae). Among 49 was extended forward 90° to a point per- adult parasitoids recovered, nine (18%) pendicular to the body, and supinated to 90° were Eurytoma sp. and 40 (82%) were with respect to the substrate. As the wing Pteromalus sp. was extended it was vibrated in a plane par- Acknowledgments allel to the wing blade faster than was ob- served with other Trupanea spp. studied Once again we sincerely thank A. C. (Headrick and Goeden 1994). When the Sanders, Curator of the Herbarium, Depart- wing reached its maximum forward posi- ment of Botany and Plant Sciences, Uni- tion, it was held for ca. 1 second, then re- versity of California, Riverside, for identi- turned to the resting position, flat upon the fication of plants from southern California dorsum, and held still while the other wing mentioned in this paper. The parasitoids was extended. Male courtship displays be- were identified by Harry E. Andersen, Hun- VOLUME 99. NUMBER 4 755 tington Beach, California. We also are ifornia. Proceedings ofthe Entomological Society grateful to F. L. Blanc and D. H. Headrick ofWashington 96: 612-629. for their helpful comments on and contri- Goedaennd,dRe.scDr.ipatnidonJs. Ao.fTadeuelrtisnka.nd19i9m6maa.tuLirfeeshtiasgteosrioesf butions to earlier drafts of this paper. two cryptic species, Aciurinaferrugenia (Doane) andA. michaelinewspecies (Diptera:Tephritidae) Literature Cited on Chiysothamnus viscidiflorus (Hooker) Nuttall in southern California. Proceedings of the Ento- Bremer, K. 1994. Asteraceae Cladistics & Classifica- mological Society ofWashington 98: 415-438. tion. Timber Press, Inc. Portland, Oregon. . 1996b. Life history anddescriptionsofadults and immature stages of Aciurina idahoensis Cavender, G. L. and R. D. Goeden. 1982. Life history of Trupanea bisetosa (Diptera: Tephritidae) on Steyskal (Diptera: Tephritidae) on Cluysothamnus wild sunflower in southern California. 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