Effects of Parasitization by the Nematode, Heterotylenchus autumnalis, on Mating and Oviposition in the Host, Musca autumnalis

Abstract

Male face flies parasitized by the nematode Heterotylenchus autumnalis are capable of mating and inseminating females. However, less than 50% of the flies inseminated by infected males oviposit. Female hosts are castrated by the nematodes which penetrate and destroy the ovaries. Although the testes are not destroyed by the nematode, acessory glands are lacking in many heavily infected males 9 to 12 days old. The fate of the nematode in male hosts appears to be a dead end, since there is no natural means for the parasite to exit from male flies. Mating appears to be necessary for infected females to deposit nematodes. Heterotylenchus autumnalis is a nematode parasite of the face fly, Musca autumnalis, one of the leading pests of dairy and beef cattle in the United States and Canada. The life cycle of the parasite involves an alternation of gamogenetic and parthenogenetic stages, with infection of host larvae occurring in bovine feces, the breeding site of the fly (Stoffolano and Nickle, 1966; Nickle, 1967). Female hosts are castrated by the larval nematodes which penetrate and destroy the ovaries of the flies. Infected female flies go through a mock and deposit larval nematodes, instead of fly eggs, into manure. Heterotylenchus autumnalis may prove to be an effective biological control agent against M. autumnalis since the nematode sterilizes female flies and is naturally disseminated by the host. There is also some evidence to suggest the parasite is host-specific (Jones and Perdue, 1967; Stoffolano and Streams, 1971; Nappi and Stoffolano, 1971, 1972; Stoffolano, 1973), but additional experimental evidence is needed to determine the relationships of the nematode with other dung-breeding Diptera. Information is also needed concerning the fate of the nematode in male flies, and the effects of parasitization on the reproductive biology of the host. The present investigation was undertaken to determine whether nematode-infected male face flies could successfully mate and inseminate female flies, and if mating stimuli were necessary for parasitized flies to deposit nematodes. Since the ovipositor of the female is Received for publication 16 July 1973. positioned within the genital atrium of the male during copulation, the possibility of a transfer of infection was also considered. MATERIALS AND METHODS Fa e flies used in this study were maintained at 27 ? 2 C, 16 hr photophase, and 50 to 55% relative humidity. The adult flies were fed powdered milk, sugar, and water. Fresh bovine feces was used as the oviposition and larval rearing medium. The nematodes were obtained from a laboratory colony of infected face flies maintained at the Entomology Research Division, USDA, Lincoln, Nebraska. To propagate the nematodes the abdomens of 12-day-old infected adult flies were dissected and the parasites spread over the surface of manure containing face fly larvae. Infected and noninfected flies were reared separately. To obtain virgin flies of known age, fly pupae were individually placed into glass vials and covered. Following eclosion the flies were sexed, removed from the vials, and transferred to separate wire-screen cages. Mating experiments were performed with 7-day-old females and infected males 5 to 12 days old. Each pair of flies was placed within a screen cage for 24 hr to allow for mating. No individual was used more than once. After 24 hr the males were dissected to determine whether they were parasitized. Female flies that had been paired with infected males were each reared in isolation and provided with fresh bovine feces twice a week for a period of 2 weeks. The surface of the manure was examined to determine the presence of eggs. Females that did not oviposit and produce offspring were dissected or examined histologically for the presence of spermatozoa in the spermathecae. For histological examinations the flies were fixed in either Kahle's or Mahdissan's solution (8 hr), cleared in 2 changes of dioxane (6 to 8 hr each), and vacuum infiltrated in a paraffin oilParaplast series for 1 to 2 days. Longitudinal