Trichomalopsis dubius (Ashmead) and Dibrachys cavus (Walker): Newly Discovered Pupal Parasitoids (Hymenoptera: Pteromalidae) of House Flies and Stable Flies Associated with Livestock Manure E. RICHARD HOEBEKE AND DONALD A. RUTZ Department of Entomology, Comstock Hall, Cornell University, Ithaca, New York 14853 Ann. Entomol. Soc. Am. 81(3): 493-497 (1988) ABSTRACT Trichomalopsis dubius (Ashmead) and Dibrachys cavus (Walker), pteromalid parasitoids of pupae of various muscoid flies, are reported for the first time from the hosts Musca domestica L. and Stomoxys calcitrans (L.) (Muscidae) associated with livestock manure in New York. Morphological descriptions of the male and female of both species are given, as are field and laboratory observations, biological notes and hosts summarized from the literature, and known geographic distribution. An existing illustrated key to pupal parasitoids of muscoid flies associated with livestock manure is modified to include T. dubius and D. cavus. KEY WORDS Insecta, pupal parasitoids, house fly, stable fly DURING THE PAST TWO DECADES, extensive research has studied the exploitation of hymenopterous parasitoids as biological control agents to suppress populations of muscoid flies that are pests of livestock, poultry, and humans (Axtell & Rutz 1986). In confined livestock and poultry production facilities, the common parasitoids are predominantly those in the family Pteromalidae, including species in the genera Spalangia, Muscidifurax, Pachycrepoideus, and Nasonia. In addition, the parasitoid Urolepis rufipes (Ashmead) recently was discovered parasitizing muscoid fly pupae in dairy manure in New York (Smith & Rutz 1985) and in Nebraska (Petersen et al. 1985). In this paper we call attention to two newly discovered pteromalid parasitoids of muscoid fly pupae, Trichomalopsis dubius (Ashmead) and Dibrachijs cavus (Walker). Rueda & Axtell (1985) recently summarized available information on some common species of Pteromalidae that parasitize muscoid flies and provided an illustrated key for the identification of these parasitoids. To complement this important and useful guide, we have altered their illustrated key to include T. dubius and D. cavus; couplet #5 (Rueda & Axtell 1985, 16) is modified to read as follows: 5. Compound eyes with long, conspicuous hairs (Fig. 1 and 2); solitary parasitoid Urolepis rufipes (Ashmead) Compound eyes usually without hairs, or hairs much less conspicuous (Fig. 3 and 4); gregarious parasitoid 5a 5a. Apical margin of forewing with distinct fringe of short or long setae (Fig. 7 and 8) 5b Apical margin of forewing without fringe setae Dibrachys cavus (Walker) 5b. Mesoscutum and scutellum bearing delicate, nonraised reticulations (Fig. 5); forewing apex with marginal fringe of short setae (Fig. 7)....Nasonia vitripennis (Walker) Mesoscutum and scutellum bearing slightly raised reticulations (Fig. 6); forewing apex with marginal fringe of noticeably long setae (Fig. 8) Trichomalopsis dubius (Ashmead) In the section below, following a format similar to that given by Rueda & Axtell (1985), we provide morphological descriptions for both sexes, biological notes, field and laboratory observations, geographical distribution, and hosts. Voucher specimens of both parasitoid species are deposited in the Cornell University Insect Collection, Ithaca, N.Y. Trichomalopsis dubius (Ashmead) Meraporus dubius Ashmead 1896: 219. Eupteromalus dubius: Gahan 1920 (1921): 240. Trichomalopsis dubius: Kamijo & Grissell 1982: 77. The following descriptions of the female and male were taken, in part, from Ashmead (1896). Body Length. 1.5-2.0 mm. Female. Aeneous-black, punctate, upper part of thorax and temples more decidedly metallic; scape and legs, except coxae, brownish yellow; tarsi paler; flagellum aeneous-black, pubescent. Wings (Fig. 8) hyaline, veins pale; subcostal vein almost white, nearly three times as long as marginal vein; latter 0013-8746/88/0493-0497$02.00/0 1988 Entomological Society of America
494 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 81, no. 3 Fig. 1-4. Morphological structures of pteromalid spp. (1) Head, frontal aspect (female), Urolepis rufipes. (2) Head, lateral aspect (female), U. rufipes. (3) Head, frontal aspect (female), Nasonia vitripennis. (4) Head, lateral aspect (male), N. vitripennis. Fig. 1-4 were taken from Rueda & Axtell 1985. only slightly longer than stigma. Head slightly more than three times as wide as long anteroposteriorly; occiput delicately margined, gena slightly rounded. Thorax (Fig. 6) with parapsidal furrows distinct half length of mesonotum anteriorly, or little more; metanotum strongly punctate, produced into a subglobose neck, and tricarinate; middle carina extending only to base of neck, lateral carinae strongly curved. Abdomen ovate, shorter than thorax, flat above, convex or strongly carinate below; second segment longest, with large fovea at base above; third segment about one-third length of first; fourth, fifth, and sixth segments very short, subequal, and combined shorter than third; seventh segment as long as third; eighth segment visible as slight conical projection. Male. Characters same as female, except head and thorax more metallic green, abdomen more rotund-oval, third abdominal segment half as long as second, or as long as following segments combined. Biological Notes and Hosts. Published records of hosts of this species, as well as for the genus, include the orders Diptera (Syrphidae, Calliphoridae, and Tachinidae), Lepidoptera (Noctuidae and Pyralidae), and Hymenoptera (Braconidae and Ichneumonidae). A reference list of host species can be consulted in Peck (1963) and Krombein et al. (1979). Field Observations. In 1984, populations of T. dubius were discovered on dairy farms in Cayuga County, New York (in the towns of Conquest, Aurelius, and Sempronius). The parasitoid was reared from sentinel pupae of Musca domestica L. and Stomoxys calcitrans (L.) on at least 20 occasions between 6 June and 24 October 1984. The para-
May 1988 HOEBEKE & RUTZ: PUPAL PARASITOIDS OF HOUSE AND STABLE FLIES 495 Fig. 5-8. Morphological structures of pteromalid spp. (5) Middle lobe of mesoscutum, N. vitripennis; arrow denotes fine, delicate reticulations of the surface. (6) Middle lobe of mesoscutum, Trichomalopsis dubius; arrow denotes raised reticulations of the surface. (7) Apical margin of forewing, N. vitripennis, showing fringe of short setae. (8) Apical fringe of forewing, T. dubius, showing fringe of long setae. Fig. 5 was taken from Rueda & Axtell 1985. sitized pupae were found nearly always at outdoor sites, in or near dry lots, near silos, and at manure pits. However, on two occasions, parasitized pupae were discovered indoors in heifer freestalls next to dry lots with the outside doors open. The substrate was usually dry, earthy manure. In 1985, this parasitoid was reared on 14 occasions from sentinel pupae of M. domestica from 2 July through 24 September on some of the same dairy farms in Cayuga County (Conquest, Aurelius, Sempronius, and Moravia) and also in Schuyler County (Montour). During this period, parasitized pupae were always found in outdoor sites with dry, earthymanure substrates, usually at or near dry lots, manure pits, or under calf hutches. Laboratory Observations. A colony of T. dubius has been maintained in the laboratory; the soufce material originated from the Lockwood Dairy, Aurelius, N.Y. (Cayuga County). The colony is maintained at 24-26 C and 45-60% RH; fresh pupae of M. domestica are provided weekly. Parasitoid emergence usually occurs 12-15 d after oviposition, with an average of 12.6 adults emerging per fly puparium (n = 63, s 2 = 55.1). The average sex ratio (female/male) per puparium is 1.4:1. From field-collected material, an average of only 2.4 parasitoids per fly puparium (n = 89, s 2 = 24.6) emerged. Distribution. This parasitoid appears to be widely distributed in eastern North America, with records
496 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 81, no. 3 known from the District of Columbia, Ohio, Indiana, Wisconsin, Illinois, Minnesota, Iowa, Nebraska (Krombein et al. 1979), and New York. Dibrachys cavus (Walker) Pteromalus cavus Walker 1835: 477. Dibrachys cavus: Kurdjumov 1913: 11. The following descriptions of the female and male were taken from Graham (1969). Body Length. 1.50-2.75 mm (depending on number emerging from host). Female. Head and thorax bronze, dark bluish, or dark greenish blue, confluently punctate. Antennal scape often entirely fuscous, but sometimes testaceous proximally; pedicellus and flagellum usually fuscous to black, occasionally pedicellus paler beneath. Flagellum subclavate, finely pubescent, pedicellus longer than two ring-joints and first funicular segment combined, or slightly longer than three-segmented club. Metanotum short, tricarinate. Wing veins varying from brownish testaceous to almost white. Legs variable in color, from entirely black to extensively testaceous; in those having palest legs, only coxae black, remainder testaceous, with femora and tibiae slightly brownish. Abdomen acute-ovate, somewhat longer than head and thorax combined, aeneous-black. Tarsi sometimes testaceous but more often brown or fuscous. Marginal vein 2.0-2.9 times as long as stigmal vein; postmarginal vein usually as long as or even very slightly longer than stigmal vein, rarely very slightly shorter. Male. Head and thorax greenish to bluish, confluently punctate. Axillae and scutellum concolorous, or scutellum at most slightly tinged with bronze. Abdomen much depressed, oblong-oval, shorter than thorax, aeneous or metallic, and nearly always without, or with very small or indistinct pale spot at base, rarely with spot distinct. Antennae variable in color, often entirely testaceous but sometimes with pedicellus and scape infuscate, occasionally with flagellum brownish. Antennae with scape slender, 6.5-7.5 times as long as broad, without projecting lobe at distal end; pedicellus shorter than in female, hardly more than twice as long as broad; funicle slender, segments quadrate, or proximal segments slightly longer than broad; clava 2.3-3 times as long as broad; flagellum clothed with curved, subdecumbent hairs. Biological Notes and Hosts. Much literature has been devoted to the biology of this notorious hyperparasitoid; a list of references can be consulted in Krombein et al. (1979). Peck (1963) and Krombein et al. (1979) provide an extensive list of host records for D. cavus. If all records prove to be accurate, D. cavus must be considered a very polyphagous species. It is a secondary parasitoid in the cocoons of Hymenoptera (Ichneumonidae and Braconidae) that parasitize Lepidoptera and sometimes Coleoptera. It is also a primary parasitoid of the larvae of Lepidoptera and Coleoptera. It has been reared from the puparia of Tachinidae and has been recorded parasitizing other Chalcidoidea and even other individuals of its own species. Balduf (1937) remarked that this species is reported more frequently in the literature than any other chalcidoid. Field Observations. In 1984 and 1985, populations of D. cavus were discovered on dairy farms in Cayuga (Sempronius and Auburn) and Schuyler (Odessa) counties. The parasitoid was reared from sentinel pupae of M. domestica and S. calcitrans on four occasions, between 20 June and 5 September. Parasitized pupae were found most frequently indoors under manure ramps in sheds and in strawmanure mixtures. Laboratory Observations. From a total of six field-collected puparia (both fly species combined), 40 parasitoids emerged, an average of 6.7 parasitoids per puparium (s' 2 = 6.0). The range of parasitoid emergence was from 3 to 10 parasitoids per puparium. The average sex ratio (female/male) per puparium was 5.7:1. Distribution. This pteromalid occurs throughout most of Europe and is also widespread in Canada and the United States (Graham 1969; Krombein et al. 1979); it has been recorded from China, Korea, North Africa, and Uruguay (Graham 1969) as well. Acknowledgment We greatly appreciate the technical assistance of Clare Stokes, Link Smith, and Glen Scoles (Department of Entomology, Cornell University). In addition, we acknowledge the taxonomic assistance provided by E. E. Grissell (Systematic Entomology Laboratory, USDA-ARS, Washington, D.C.) in confirming the identification of the parasitoids discussed in this paper. This paper is a publication of the Cornell University Agricultural Experiment Station, New York State College of Agriculture and Life Sciences, a statutory college of SUNY. The research was supported by Hatch Project 139428. References Cited Ashmead, W. H. 1896. Descriptions of new parasitic Hymenoptera (Paper No. 2). Trans. Amer. Entomol. Soc. 23: 179-234. Axtell, R. C. & D. A. Rutz. 1986. Role of parasites and predators as biologicalflycontrol agents in poultry production facilities, pp. 88-100. In R. S. Patterson & D. A. Rutz [eds.], Biological control of muscoid flies. Miscellaneous Publication 61, Entomological Society of America, College Park, Md. Balduf, W. V. 1937. Bionomic notes on the common bagworm, Thyridopteryx ephemeraeformis Haw., (Lepid., Psychidae) and its insect enemies (Hym., Lepid.). Proc. Entomol. Soc. Wash. 39: 169-184. Gahan, A. B. 1920(1921). On the identity of several species of Chalcidoidea (Hymenoptera). Proc. Entomol. Soc. Wash. 22: 235-243. Graham, M. W. R. de V. 1969. The Pteromalidae of northwestern Europe (Hymenoptera: Chalcidoidea). Bull. Brit. Mus. (Nat. Hist.), Suppl. 16. Kamijo, K. & E. E. Grissell. 1982. Species of Trich-
May 1988 HOEBEKE & RUTZ: PUPAL PARASITOIDS OF HOUSE AND STABLE FLIES 497 omalopsis Crawford (Hymenoptera, Pteromalidae) from rice paddy, with descriptions of two new species. Kontyu, Tokyo 50: 76-87. Krombein, K. V., P. D. Hurd, Jr., D. R. Smith & B. D. Burks. 1979. Catalog of Hymenoptera in America north of Mexico, vol. I, Symphyta and Apocrita (Parasitica). Smithsonian Institution, Washington, D.C. Kurdjumov, N. 1913. Notes on Pteromalidae (Hymenoptera, Chalcidodea). Rev. Russe Entomol. (Entomol. Obozr.) 13: 1-24. Peck, O. 1963. A catalogue of the Nearctic Chalcidoidea (Insecta: Hymenoptera). Can. Entomol., Suppl. 30. Petersen, J. J., O. R. Guzman & B. M. Pawson. 1985. Urolepis rufipes (Hymenoptera: Pteromalidae), a new parasite record for filth flies (Diptera: Muscidae) in Nebraska, USA. J. Med. Entomol. 22: 345. Rueda, L. M. & R. C. Axtell. 1985. Guide to common species of pupal parasites (Hymenoptera: Pteromalidae) of the house fly and other muscoid flies associated with poultry and livestock manure. North Carolina Agricultural Research Services Technical Bulletin 278. Smith, L. & D. A. Rutz. 1985. The occurrence and biology of Urolepis rufipes (Hymenoptera: Pteromalidae), a parasitoid of house flies in New York dairies. Environ. Entomol. 14: 365-369. Walker, F. 1835. Monographia Chalcidum. Entomol. Mag. 2: 476-502. Received for publication 10 August 1987; accepted 28 December 1987.