BIOLOGICAL CONTROLÑPARASITOIDS AND PREDATORS Host Ranges of Gregarious Muscoid Fly Parasitoids: Muscidifurax raptorellus (Hymenoptera: Pteromalidae), Tachinaephagus zealandicus (Hymenoptera: Encyrtidae), and Trichopria nigra (Hymenoptera: Diapriidae) 1 2 CHRISTOPHER J. GEDEN AND ROGER D. MOON USDAÐARS, Center for Medical, Agricultural, and Veterinary Entomology, PO Box 14565, Gainesville, FL 32607 Environ. Entomol. 38(3): 700Ð707 (2009) ABSTRACT Attack rates, progeny production, sex ratios, and host utilization efÞciency of Muscidifurax raptorellus (Kogan and Legner) (Hymenoptera: Pteromalidae), Tachinaephagus zealandicus Ashmead (Hymenoptera: Encyrtidae), and Trichopria nigra (Nees) (Hymenoptera: Dia- priidae) were evaluated in laboratory bioassays with Þve dipteran hosts: house ßy (Musca domestica L.), stable ßy (Stomoxys calcitrans L.), horn ßy (Hematobia irritans L.), black dump ßy [Hydrotaea aenescens (Weidemann)] (Diptera: Muscidae), and a ßesh ßy (Sarcophaga bullata Parker) (Diptera: Sarcophagidae). M. raptorellus killed and successfully parasitized all Þve host species and produced an average 2.6 parasitoid progeny from each host. Host attack rates were highest on stable ßy and lowest on horn ßy; there were no differences among hosts in the total number of progeny produced. T. zealandicus killed larvae of all ßy host species in similar numbers, but parasitism was most successful on H. aenescens and S. bullata and least successful on horn ßy and house ßy hosts. SigniÞcantly more parasitoid progeny emerged from S. bullata (10.2 parasitoids per host) than the other hosts; only 2.5 progeny were produced from parasitized horn ßy hosts. Most of the killed puparia that produced neither adult ßies nor parasitoids (“duds”) contained dead parasitoids; in house ßy, stable ßy, and horn ßy hosts, Ͼ30% of these dudded pupae contained adult wasps that failed to eclose. T. nigra successfully parasitized pupae of all host species except house ßy and was most successful on stable ßy. SigniÞcantly more parasitoid progeny emerged from S. bullata (30.6 parasitoids per host) than the other hosts; only 5.7 progeny were produced from horn ßy hosts. KEY WORDS Muscidifurax raptorellus, Tachinaephagus zealandicus, Trichopria nigra, house ßy, stable ßy Parasitoids of muscoid ßy immatures have been stud- feed, and lay a single egg between the puparium and ied extensively for many years. (Rutz and Patterson the developing host within. Parasitoid larvae consume 1990). Efforts to use parasitoids for operational ßy the killed host externally within the comparative control have often followed an algorithm involving safety of the puparium. These characteristics place the surveys to determine locally dominant species fol- pteromalid ßy parasitoids within the group described lowed by augmentative releases of that species (Mor- as idiobionts (Askew and Shaw 1986). gan and Patterson 1990; Geden et al. 1992; Weinzierl Gregarious parasitoids received less attention until and Jones 1998; Crespo et al. 1998, 2002; Skovgard and the discovery that the gregarious form of Muscidifurax Nachman 2004). In nearly every case, the parasitoids aptorellus Kogan and Legner, once thought to be na- selected for release have been solitary pupal parasi- tive to Chile, had become established in parts of the toids of the pteromalid genera Muscidifurax and Spal- United States (Kogan and Legner 1970, Legner 1987, angia. Although different species in this group show Petersen and Cawthra 1995, Antolin et al. 1996, Taylor authentic differences with regard to environmental et al. 1997, Taylor and Szalanski 1999). Gregarious M. and behavioral determinants (Geden 1996, 1997, 1999, raptorellus is now available from commercial insecta- 2002), these species differ little in their fundamental ries, and it has shown potential as a biocontrol agent bionomics. All attack pupae of a prescribed age from under a range of production systems and in different a wide range of host species (Geden et al. 2006), host geographic areas (Petersen and Cawthra 1995, Pe- tersen and Currey 1996, Floate et al. 2000, Kaufman et al. 2001, Geden and Hogsette 2006). 1 Corresponding author, e-mail: [email protected]. 2 Department of Entomology, University of Minnesota, 1980 Fol- Another gregarious species that has received re- well Ave., St. Paul, MN 55108. newed attention is the encyrtid larval parasitoid Tachi- June 2009 GEDEN AND MOON:HOST RANGES OF GREGARIOUS FLY PARASITOIDS 701 naephagus zealandicus Ashmead. T. zealandicus is (22Ð23 d) at 25ЊC. Sarcophaga bullata was the most thought to be indigenous to the Southern Hemisphere commonly used host for colony maintenance, but the (Olton 1971). It was imported from Australia and New other species used in this study were used occasionally Zealand and released in California poultry houses in as well. T. nigra were held under the same environ- 1967 (Legner and Olton 1968, Olton and Legner 1974). mental and food conditions as T. zealandicus. Pupae of In subsequent years, this species was recovered in S. bullata or stable ßy were exposed to cages of adult otitid ßies in Ohio (Downing 1975) and from house parasitoids for 3Ð4 d of exposure to oviposition and ßies, calliphorids, and sarcophagids in South Carolina removed and held for ßy and parasitoid emergence (Ables 1977). Although the status of this species in the (26Ð27 d) at 25ЊC. United States at present is unknown, there has been Fly Colonies. House ßies and stable ßies were from considerable interest in T. zealandicus in Brazil, where long-established colonies maintained at the Center for it seems to be an important natural enemy of ßies in Medical Agricultural and Veterinary Entomology poultry houses (Costa 1989; Monteiro and Pires do (CMAVE), Gainesville, FL, and were reared using Prado 2000; Ferreira de Almeida et al. 2002a, b). standard methods and diets (Hogsette 1992). Black During a collecting trip to Russia and Kazakhstan, dump ßies, Hydrotaea aenescens, were from a colony one of the authors (R.D.M.) collected specimens of a established from Florida poultry farms in 1989 and diapriid found attacking stable ßy pupae on dairy reared using the methods described in Hogsette and farms. A colony was established at the USDA labora- Washington (1995). Two-day-old pupae were sepa- tory in Gainesville for further study. This species has rated from rearing media by water ßotation and dried since been identiÞed as Trichopria nigra (Nees), a in a forced air blower designed for this purpose palearctic species that occurs in Russia, Moldavia, Ka- (Bailey 1970). zakhstan, Greece, Germany, Denmark, and Sweden Horn ßies were from a colony established in the (Petrov 2002, Medvedev 1988, Anonymous 2007). In 1970s. Adults were reared in cages at 26ЊC, 60Ð80% preliminary laboratory tests, we found that this was a RH, and constant light and given bovine blood daily by gregarious species that looked promising as a biocon- placing blood-soaked pads on the tops of the cages. trol agent for several species of pest ßies (C.J.G., un- Blood for the colony was collected every 2 wk at a local published data). To our knowledge, the life history, abattoir in 8.5-liter batches and treated with 30 g of host range, and habits of this species are unknown. sodium citrate, 1.5 g of kanamycin sulfate, and 250,000 Tachinaephagus zealandicus and T. nigra are koino- U of nystatin. Eggs were collected daily on water- biont gregarious endoparasitoids whose host range has soaked cotton pads placed 1 cm below the screened not been examined. The objective of this study was to cage bottoms. Larvae were reared by placing 1 ml of examine the performance of the ectoparasitoid M. eggs on a rearing medium composed of 1 liter of steer raptorellus and these two endoparasitic species on a manure, 1 liter of pelletized peanut hulls soaked over- range of host species that are commonly found in night in 750 ml water, and 115 g of a prepared mixture association with animal production systems. of wheat ßour (44%), Þsh meal (33%), alfalfa meal (18%), and baking soda (5%). The manure was col- lected from pastured animals and frozen before use to Materials and Methods kill any arthropods present. Larval trays were kept in Parasitoid Colonies. The M. raptorellus colony was the same room as the adult ßies, and pupation oc- established from specimens collected on a New York curred on day 5 under these rearing conditions. Pupae poultry farm where commercially produced parasi- were separated from media by water ßotation and toids had been released in previous years. The com- dried in a forced-air blower 7 d after egg placement. mercial source is believed to have originated from The colony of the ßesh ßy, S. bullata Parker, was material collected from Nebraska feedlots. The T. zea- founded with ßies obtained from Carolina Biological landicus colony was established from samples col- Supply (Burlington, NC). Adult ßies were given water lected from a poultry farm in Santa Cruz de Concieri- and moist sugar-yeast cakes. The cakes were prepared cao, Sao Paulo, Brazil. Two T. nigra colonies were by mixing three parts sugar and one part yeast hydro- tested; these had been established from samples col- lysate (by volume) and holding the mixture in pans at lected on dairy farms near Kraznodar, Russia, and 90% RH for 3 d. Flies were presented with fresh beef Almaty, Kazakhstan. All of the colonies were 1Ð2 yr old liver for larviposition. Larvae were reared on beef liver at the time of testing. and pupated Ϸ7 d after larviposition on paper towels Muscidifurax raptorellus were maintained by pro- or vermiculite placed under larval rearing pans. viding parasitoids with 2-d-old house ßy pupae three Samples of 100 pupae of each species were weighed times per week at a host: parasitoid ratio of Ϸ10:1 in for each cohort used in the bioassays and averaged as chambers maintained at 25ЊC and 60Ð80% RH under follows: 106 (S. bullata), 18 (house ßy), 15 (stable ßy constant darkness. T. zealandicus were maintained at and H.