Hymenoptera: Braconidae) on Six Different Pyralid Host Species
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ARTHROPOD BIOLOGY Oviposition and Reproductive Performance of Habrobracon hebetor (Hymenoptera: Braconidae) on Six Different Pyralid Host Species 1,2,3 1 MUKTI N. GHIMIRE AND THOMAS W. PHILLIPS Ann. Entomol. Soc. Am. 107(4): 809Ð817 (2014); DOI: http://dx.doi.org/10.1603/AN14046 ABSTRACT Habrobracon hebetor Say (Hymenoptera: Braconidae) is a gregarious ecto-parasitoid that attacks larvae of several species of Lepidoptera, mainly pyralid moths infesting stored products. Host quality strongly inßuences the reproductive success of the parasitoid. In this study, we assessed the reproductive performance of the parasitoid, H. hebetor in a series of laboratory experiments using six different pyralid host species: Indianmeal moth, Plodia interpunctella (Hu¨ bner), Mediterranean ßour moth, Ephestia kuehniella (Zeller), almond moth, Ephestia cautella (Walker), rice moth, Corcyra cephalonica (Stainton), navel orangeworm, Amyelois transitella (Walker), and greater wax moth, Galleria mellonella L. Experiments were conducted using petri dishes (100 by 15 mm) as experimental arenas at 29 Ϯ 1ЊC, 65 Ϯ 5% relative humidity, and a photoperiod of 14:10 (L:D) h. Two-day-old H. hebetor females were introduced singly into experimental arenas and given a single host larva every day throughout their lifetime. The numbers of hosts paralyzed and parasitized, numbers of eggs laid each day on each host, egg-to-adult survivorship, and progeny sex ratio were used as parameters for assessing host suitability. Paralysis of hosts by H. hebetor females was signiÞcantly affected by host species. H. hebetor paralyzed Ͼ95% of the preferred host larvae that were offered and also used Ϸ90% of those for oviposition. Daily fecundity was highest on G. mellonella (22.1 Ϯ 0.4) and C. cephalonica (21.6 Ϯ 0.3), and lowest on E. cautella (13.4 Ϯ 0.2). The egg-to-adult survivorship and progeny sex ratio were also signiÞcantly affected by the host species. The highest percentage of parasitoid survival was on A. transitella (75.7 Ϯ 2.0) and C. cephalonica (75.4 Ϯ 2.5), and lowest on G. mellonella (49.7 Ϯ 4.8). Our studies clearly showed that H. hebetor females can paralyze and lay eggs on several pyralid species, but it cannot necessarily develop and reproduce optimally on all host species that it can paralyze and parasitize. KEY WORDS stored-product pest, biological control, parasitoid, reproduction, host quality The use of biological control agents in food storage insects are exempted for their use and occurrence in situations is not a new concept, but it has long been stored raw commodities and processed food (Brower neglected because of the potential contamination of et al. 1996). Thus, biological control can be a legal, food products by introducing natural enemies and the safe, and viable method of stored-product protection. low tolerance limit for pest insect damage (Arbogast Stored-product pyralid moths (Lepirdoptera: Pyr- 1983). Recently attention has been focused on alidae; Phycitinae) are among the most destructive nonchemical methods of stored-product protection, pests of stored-food commodities because their larvae including biological control of stored-product pests, infest the value-added, Þnished food products that are due to negative impacts of pesticides, such as restric- packaged and ready for retail use. The Indianmeal tions on the use of certain pesticides and the evolution moth, Plodia interpunctella (Hu¨ bner), Mediterranean of insecticide resistance in pest populations (Arbogast ßour moth, Ephestia kuehniella (Zeller), almond moth, 1984, Hagstrum et al. 1999, Phillips et al. 2000, United Ephestia cautella (Walker), navel orangeworm, Amy- Nations Environment Program 2006). The use of ben- elois transitella (Walker), tobacco moth, Ephestia elu- eÞcial insects in stored-product systems received gov- tella (Hu¨ bner), and the raisin moth, Ephestia figuliella ernment approval as a pest mitigation practice in the (Gregson) are among a cosmopolitan group of stored- United States, and is exempted from a requirement for product pests in the subfamily Phycitinae, including minimum tolerance levels (Environmental Protection the rice moth, Corcyra cephalonica (Stainton) and the Agency [EPA] 1992). All genera of parasitoids and greater wax moth, Galleria mellonella L. in the sub- predators that are known to attack stored-product family Galleriinae (Lepidoptera: Pyralidae) (Sim- mons and Nelson 1975; Chauvin and Chauvin 1985; 1 Department of Entomology, 123 Waters Hall, Kansas State Uni- Vick et al. 1987; Cox and Bell 1991; Johnson et al. 2000, versity, Manhattan, KS 66506. 2002). 2 Current Address: USDA-APHIS-PPQ-CPHST, 1398 West Truck Rd., Buzzards Bay, MA 02542. Habrobracon hebetor Say (Hymenoptera: Braconi- 3 Corresponding author, e-mail: [email protected]. dae) is a gregarious, idiobiont, ectoparasitic wasp that 0013-8746/14/0809Ð0817$04.00/0 ᭧ 2014 Entomological Society of America 810 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 107, no. 4 attacks larvae of several species of Lepidoptera, Table 1. List of host species (Lepidoptera: Pyralidae) used in (12 ؍ mainly, pyralid moths infesting stored products this study and their average larval body weight (mg ؎ SE; n (Brower et al. 1996). H. hebetor is considered one of Larval Subfamily Common name ScientiÞc name the potential biological control agents for stored-prod- weight uct pests because of its cosmopolitan distribution and Phycitinae Navel orangeworm A. transitella 55.00 Ϯ 1.90 ability to regulate populations of stored-product Almond moth E. cautella 18.66 Ϯ 1.31 moths (Simmons and Nelson 1975; Hagstrum and Mediterranean ßour E. kuehniella 24.56 Ϯ 0.96 Smittle, 1977, 1978; Krombein et al. 1979; Press and moth Flaherty 1981; Brower et al. 1996). H. hebetor females Indianmeal moth P. interpunctella 20.15 Ϯ 0.92 Galleriinae Rice moth C. cephalonica 48.89 Ϯ 1.66 Þrst paralyze their host larva by stinging and then Greater wax moth G. mellonella 262.78 Ϯ 15.17 laying variable numbers of eggs on or near the surface of paralyzed hosts (Antolin et al. 1995). The paralyzed host larvae are then used as food sources for both punctella. The parasitoids were then cultured and developing wasps and also adult females. Normally the mass-reared on full-grown larvae of P. interpunctella in female H. hebetor paralyzes several larvae and returns the laboratory at a temperature of 29 Ϯ 1ЊC, 65 Ϯ 5% afterwards to Þnd and oviposit on some immobile relative humidity (RH), and a photoperiod of 14:10 larvae (Ullyett 1945). H. hebetor females paralyze (L:D) h. Full-grown larvae of P. interpunctella were many more hosts than needed for oviposition, and obtained from a laboratory culture that was reared on paralysis is always fatal, though life may continue for a standardize diet of corn meal, chick laying mash, nearly a month if not parasitized by wasp larvae. Un- chick starter mash, and glycerol (Phillips and Strand der the natural conditions, only a small proportion of 1994) at a volumetric ratio of 4:2:2:1, respectively, at a the paralyzed larvae are actually used for oviposition temperature of 28 Ϯ 1ЊC, 65 Ϯ 5% RH, and a photo- (Doten 1911, Richards and Thomson 1932). period of 14:10 (L:D) h. Host quality strongly inßuences the main compo- Host Species. Four species of phycitine pyralids and nents of parasitoid Þtness, such as fecundity, devel- two species of nonphycitine pyralids were studied in opmental time, survivorship, secondary sex ratio, and these experiments (Table 1). The larvae of phycitine size of the emerging adult wasps (Vinson and Iwantsch pyralids were obtained from laboratory colonies at 1980, Charnov 1982, Godfray 1994). Successful iden- Oklahoma State University. The initial culture of G. tiÞcation of host quality, and adjusting the clutch size mellonella was obtained from a local pet store that was accordingly, has important consequences for the Þt- supplied through Timberline Live Pet Foods Inc., ness of a gregarious parasitoid (Godfray 1987, Taylor Marion, IL. The initial culture of A. transitella was 1988). Several studies have shown that the clutch sizes obtained from the U.S. Department of Agriculture, of gregarious parasitoids are correlated with the size of Agriculture Research Station, Commodity Protection the hosts at oviposition (Hardy et al. 1992, Zaviezo and and Quality Laboratory at Parlier, CA. The culture of Mills 2000). Therefore, attacking large hosts and pro- C. cephalonica was obtained from Insects Limited Inc, visioning the host with optimum clutch size maximizes WestÞeld, IN. the female parasitoidÕs reproductive success and is The larvae of phycitine species except those of A. considered adaptive in terms of parasitoid Þtness. In transitella were reared on the same diet as used for contrast, recent work has shown that host size at the rearing P. interpunctella, and these were all maintained time of oviposition may have little inßuence on the at the same environmental condition (see Parasitoid Þtness functions in some of the koinobiont species Origin and Rearing). A. transitella was reared on a (Harvey 2000, Harvey et al. 2004). However, little mixture of 11.355 liter of ßakey red food bran, 900 ml information is available on whether such a situation of honey, 800 ml of deionized water, 100 gm of brew- occurs in H. hebetor, a gregarious idiobiont ectopara- erÕs yeast, and 10 ml of Vanderzants vitamins solution sitoid of lepidopterous moth pests of stored-food prod- (1%). G. mellonella was reared on a mixture of wheat ucts. The experiments presented here compare and ßour, honey, glycerol, bee wax, and brewerÕs yeast at examine the effects of six pyralid host species from two a weight basis ratio of 0.44:0.23:0.18:0.04:0.11, respec- different subfamilies, with considerable variation in tively. C. cephalonica was reared on a mixture of wheat larval body size, on several reproductive parameters of bran, wheat germ, rolled oats, glycerin, and brewerÕs H. hebetor. Basic and applied aspects of parasitoid yeast at a ratio of 1:1:1:1:0.5, respectively.