31 October 1996 PROC. ENTOMOL. SOc. WASH. 98(4), 1996, pp. 625-629

BIOLOGY AND LARVAL OF EUCELATORIA BRYANI SABROSKY AND E. RUBENTIS (COQUILLETT) (DIPTERA: )

STUART R. REITZ AND PETER H. ADLER

Department of Entomology, Clemson University, Clemson, SC 29634, U.S.A. Present address (SRR): Department of Entomology, University of California, Riverside, CA 92521, U.S.A.

Abstract.-The tachinid Eucelatoria bryani Sabrosky and E. ruhentis (Coquillett) are similar in their reproductive behaviors and will mate with one another under laboratory conditions; however, sperm is not transferred. Both spe~ies parasitize noctuid caterpillars, with the host range of E. rubentis being about four times broader than that of E. bryani, which is essentially restricted to Heliothis virescens, H. subfiexa and Helicoverpa zea. Larvae of the two species can be separated from one another as second and third instars primarily by the shape of the dorsal cornu of the tentoropharyngeal sclerite. Both tachinids offer great promise as biological control agents of noctuid pests. Key Words: Diptera, Tachinidae, Eucelatoria, Heliothis, Helicoverpa, host-parasite re­ lations

The Tachinidae comprise the largest fam­ Young and Price 1975, Sabrosky 1981, ily of parasitic Diptera and have great po­ Steward et at. 1990). Eucelatoria rubentis tential economic importance as biological occurs across the southeastern USA from control agents. However, of the approxi­ Delaware south through Florida, and west mately 8000 described species of Tachini­ to Arkansas, Texas and Tamaulipas, Mexico dae in the world, most are only known on (Sabrosky 1981). Eucelatoria bryani and E. the basis of adult morphology. Often, the rubentis can be differentiated on the basis characters used for distinguishing species or of adult characters (Sabrosky 1981). Here genera are subtle and of uncertain biologi­ we provide further diagnostic information cal importance (Wood 1987). This lack of by presenting the larval taxonomy and a information constrains the use of tachinids synopsis of biological characters for both as biological control agents, a problem that species. could be alleviated by information on other life stages and biological traits. MATERIALS AND METHODS Eucelatoria bryani Sabrosky and E. rub­ Our colony of E. bryani was derived entis (Coquillett) are two potentially impor­ from material originally collected from corn tant biological control agents (Knipling (Zea mays L.) in Arizona and later cultured 1992). These two tachinids are sympatric in USDA laboratories in College Station across the south-central USA and north­ and Weslaco, Texas. The colony of Euce­ eastern Mexico. The geographic range of E. latoria rubentis was deri ved from material bryani extends from western Arkansas and collected and maintained in culture at the eastern Oklahoma, south and west to Ari­ USDA laboratory in Tifton, Georgia. Both zona and Mexico (Jackson et al. 1969, colonies were reared at Clemson University 626 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON in Helicoverpa zea (Boddie) and Heliotlzis microspines around the body, although the virescens (F), according to methods de­ terminal (12th) band, surrounding the pos­ scribed by Nettles et al. (1980) and Reitz terior spiracles, is weakly developed. and Adler (1991). Second and third instars of the two spe­ Larvae for taxonomic study were dis­ cies can be distinguished most readily by sected from singly-parasitized hosts (H. the development of the dorsal cornu of the zea), boiled in lactic acid, slide-mounted tentoropharyngeal sclerite, which is signif­ (cephalopharyngeal skeletons in lateral icantly greater in height and more massive view) in Euparal®, and examined with an anteriorly in E. rubentis than E. bryani (Ta­ Olympus BH-2 compound microscope fit­ ble I, Fig. I). Additionally, third instars of ted with an ocular micrometer. Voucher ma­ E. bryani have significantly more papillate terial is deposited in the Clemson Univer­ openings (range: 3-5 each) at the apex of sity Collection. the anterior spiracles than do those of E. Methods for interspecific mating trials rubentis (2 or 3) (Table I). The posterior follow those of Reitz and Adler (1991). spiracles of the third instar (Fig. ID) are Briefly, 2-day old, virgin males were placed similar, although the scierotization between in a plexiglass arena (15 X lOX 10 cm). spiracular slits tends to be darker in E. rub­ Five minutes later, one newly eclosed entis. First instars cannot be separated re­ heterospecific female was introduced into liably. the arena and all interactions were recorded. Interspecific matings.-Under laboratory Additional heterospecific groups were held conditions, these two species are reproduc­ together for up to 5 days, after which fe­ tively isolated. For both species, the emer­ males were dissected in physiological saline gence pattern is protandrous, females are and examined for the presence of sperm in monogamous, and males are polygamous. the spermathecae and embryonated eggs in The courtship behaviors of E. rubentis are the common oviduct. similar to those described for E. bryani To determine the suitability of various (Reitz and Adler 1991). Males of both spe­ species of Noctuidae as hosts, feeding-stage cies mounted heterospecific females and fifth instars (2:20) of each noctuid were pre­ initiated courtship. These interspecific sented to individual 2-wk old females, or courtships continued in a manner similar to larvae were placed in cages containing 50­ that described for E. bryani by Reitz and 100 adult flies for 30-120 min. Larvae Adler (1991), with males of both species were then returned individually to 31-ml attempting intromission with heterospecific plastic cups containing a suitable meridic females. However, based on examination of diet and inspected daily for the pr~sence of spermathecae after mating attempts, sperm parasitoids. transfer did not occur and these females did not produce embryonated eggs (n = 8 for RESULTS AND DISCUSSION E. bryani male X E. rubentis female; n = Larval taxonomy.-The three larval in­ 6 for E. rubentis male X E. bryani female). stars of each species can be distinguished Host specificity.-We successfully reared on the basis of size and development of the E. bryani from H. zea, H. virescens, and cephalopharyngeal skeletons (Fig. I). The Heliotlzis subflexa (Guenee). Attempts to posterior spiracles are well-developed, with rear E. b,yani from other Noctuidae includ­ three slits each, only in the third instar (Fig. ing HUbner, Pseu­ I). Instar I has three blunt hooks surround­ doplusia inc/udens (Walker), Spodoptera ing the posterior spiracles, whereas instar 2 ornitlzogalli (Guenee), and Triclzoplusia ni has two pairs of hook plates around the pos­ (HUbner) were unsuccessful. Eucelatoria terior spiracles; hook plates are absent in hryani has been reared from field-collected third instars. All instars have 12 bands of A. gemmatalis, Spodoptera jrugiperda VOLUME 98, NUMBER 4 627

D

Fig. 1. Larval features of Eucelatoria. A-C, E. bryani, cephalopharyngeal skeletons (lateral). A, First instar. B, Second instar. C, Third instar. D, E. bryani, posterior spiracle of third instar. E-G, E. rubentis, cephalophar­ yngeal skeletons (lateral). E, First instar. F, Second instar. G, Third instar.

(Smith) and T. ni, but these host records are males to oviposit in hosts. Nettles (1980) rare compared with those from H. zea and found E. bryani females were attracted to H. virescens (Butler 1958, Sabrosky 1981). H. virescens but not to Spodoptera eridania In contrast, we successfully reared E. (Cramer) or acrea (Drury). rubentis from H. zea, H. virescens, and H. Females of both species deposit progeny subflexa, A. gemmatalis, and P. includens. in proportion to host size (Reitz 1996a), but Based on field collections, host species for progeny of E. bryani tend to be smaller and E. rubentis include these species as well as develop more rapidly than those of E. rub­ 12 other species of Noctuidae and Pyralidae entis. Because of its more rapid develop­ (Arnaud 1978, Sabrosky 1981). The basis ment, E. bryani is a superior intrinsic com­ for this interspecific difference in host range petitor compared with E. rubentis when appears to be the failure of E. bryani fe- parasitizing H. zea (Reitz 1996b). 628 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

Table I. Selected larval features, mean ::t: SE, n, of Eucelmoria bryani and E. ruben/is. Means with different letters are significantly different for each character within each instar (Hest; P < 0.005); other values are not significantly different (P > 0.05); n.O., not observed.

Cephalopharyngeal Number of Anterior 2 Species Instar Skeleton. Lenglh' Dorsal Cornu, Height Spiracular Openings E. bryani I 0.16::t: 0.004 (lO)a 0.02 ::t: 0.001 (lO)a n.o. E. rubentis 1 0.18 ::t: 0.011 (8)a 0.02 ::t: 0.002 (7)a n.o. E. bryani 2 0.33 ::t: 0.008 (lO)a 0.07 ::t: 0.002 (lO)a n.o. E. ruben/is 2 0.34 ::t: 0.007 (6)a 0.09 ::t: 0.002 (6)b n.o. E. bryani 3 0.67 ::t: o.on (ll)a 0.16 ::t: 0.003 (ll)a 3.7 ::t: 0.17 (ll)a E. ruben/is 3 0.76 ::t: 0.020 (lO)b 0.19 ::t: 0.006 (lO)b 2.6::t: 0.17 (lO)b

I Tip of mandible to posterior of dorsal cornu in mm. 2 Greatest height in mm.

Potential for biological control.-Given No. 4177 of the South Carolina Agricultur­ that both species are facultatively gregari­ al Experiment Station, Clemson University. ous (Reitz 1996a) and have relatively high fecundities (Gross and Rogers 1995, Reitz LiTERATURE CITED and Adler 1995), both species could be im­ Arnaud, P. H., Jr. 1978. A host-parasite catalog of portant biological control agents. Knipling North American Tachinidae (Diptera). United (1992) considered E. bryani to be one of States Department of Agriculture Miscellaneous Publication 1319, 860 pp. the most important parasitoids of H. zea Bratti, A. and W. C Nettles. 1992. In vitro rearing of and H. virescens and proposed a plan for Eucelatoria bl}'ani-improvements and evalua­ using E. bryani to suppress these host pop­ tion of factors affecting efficiency. Entomologia ulations. The possibility exists for using E. Experimentalis et Applicata 63: 213-219. rubentis in a similar program against other Butler, G. D. 1958. Tachinid flies reared from lepi­ pest noctuids. While host specificity is a de­ dopterous larvae in Arizona, 1957. Journal of Economic Entomology 51: 561-562. sirable attribute of biological control agents Ehler, L. E. and R. van den Bosch. 1974. An anal­ (e.g. Greathead 1986), polyphagy is not ysis of the natural biological control of Tricho· necessarily a detrimental attribute, if a po­ plusia ni (: Noctuidae) on cotton in lyphagous parasitoid attacks several sym­ California. Canadian Entomologist 106: 1067­ patrie pest species (Ehler and van den 1073. Greathead, D. J. 1986. Parasitoids in classical biolog­ Bosch 1974). The potential for using aug­ ical control, pp. 290-318. In Waage, J. and D. mentative releases of E. bryani and E. rub­ Greathead, eds., Parasitoids. Academic entis would be further enhanced with con­ Press, London. tinued refinement of in vitro rearing meth­ Gross, H. R. and C E. Rogers. 1995. Reproductive ods (Bratti and Nettles 1992). No one bio­ biology of Eucelatoria rubentis (Diptera: Tachin­ idae) reared on larvae of Helicoverpa zea (Lepi­ logical control agent is likely to manage a doptera: Noctuidae). Biological ControlS: 285­ pest population completely, but if used 289. properly, E. bryani offers an excellent op­ Knipling, E. F. 1992. Principles of insect parasitism portunity to help manage H. zea, and E. analyzed from new perspectives. Washington, rubentis offers a similar opportunity to help United States Department of Agriculture, Agri­ culture Handbook 693, 337 pp. manage several other noctuid pests. Nettles, W. C, Jr. 1980. Adult Eucelatoria sp.: Re­ sponse to volatiles from cotton and okra plants ACKJ"JOWLEDGMENTS and from larvae of Heliothis virescens, Spodop­ tera eridania, and ESligmene acrea. Environmen­ We thank J. P Norton for rendering the tal Entomology 9: 759-763. illustrations, and C. N. Watson for technical Nettles, W. C., Jr., C M. Wilson, and S. W. Ziser. assistance. This is technical contribution 1980. A diet and method for the in vitro rearing VOLUME 98. NUMBER 4 629

of the tachinid. Eucelatoria sp. Annals of the (Lepidoptera: Noctuidae). Annals of the Entomo­ Entomological Society of America 73: 180­ logical Society of America 84: 23-30. 184. ---. 1995. Fecundity and oviposition of Eucela­ Reitz, S. R. I996a. Development of Eucelatoria bry­ roria bryani (Diptera: Tachinidae), a gregarious ani and Eucelatoria ruben/is (Diptera: Tachinidae) parasitoid of Helicoverpa zea and Heliothis vires­ in different instars of Helicoverpa zea (Lepidop­ cens (Lepidoptera: Noctuidae). Entomologia Ex­ tera: Noctuidae). Annals of the Entomological So­ perimentalis et Applicata 75: 175-181. Sabrosky, C. W. 1981. A partial revision of the ciety of America 89: 81-87. Eucelatoria (Diptera: Tachinidae), including im­ ---. 1996b. Interspecific competition between two portant parasites of Heliothis. United States De­ parasitoids of Helicoverpa zea: Eucelaroria bry­ partment of Agriculture, Technical Bulletin 1635, ani and Eucelatoria ruben/is. Entomologia Exper­ 18 pp. imentalis et Applicata 79: 227-234. Wood, D. M. 1987. Tachinidae, pp. 1193-1269. In Reitz, S. R. and P. H. Adler. 1991. Courtship and mat­ McAlpine, J. F, ed., Manual of Nearctic Diptera. ing behavior of Eucelaroria bryani (Diptera: Ta­ Volume 2. Research Branch, Agriculture Canada, chinidae). a larval parasitoid of Heliothis spp. Monograph 28: 675-1332.