FLIES BREEDING IN
ACCUMULATED ORGANIC WASTES
Musca domestica L., Fannia spp., Stomoxys spp., etc. -- Muscidae
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Synanthropic flies that breed in accumulated wastes are a major problem for poultry and dairy producers and feed-lot operators in many areas of the United States. The problem is particularly acute in southern California where rapid suburban expansion has encroached on agricultural areas. Because of problems associated with unilateral chemical fly control, integrated management programs for these flies have been under development (Axtell 1970, Legner & Dietrick 1974, Petersen & Meyer 1983, Ripa 1966). Natural enemies are important control components, particularly in the more stable manure communities found in many poultry, dairy and feed-lot operations. Povolny (1971) calling these flies endophilic considered them primarily dependent on human and domestic animal wastes. Musca domestica L. is by far the best known example; however, some Drosophila and Psychoda spp. also fall into this category. Certain Fannia spp. are more on the periphery but are also included.
The common housefly, Musca domestica L. has been a constant associated of humans over much of our modern history. Attempts to control its populations by biological means have been extensive and on occasion successful in special situations. More frequently, they have failed to reduce numbers to acceptable levels. It should be emphasized that control of M. domestica populations as well as other endophilic flies pestiferous to humans, would be largely unnecessary if waste products produced by human activities could be appropriately managed. Since this is not the case, efforts towards the biological control of these species have been emphasized.
Parasitic wasps have been the most commonly studied natural enemies. Most of the published work has dealt with seasonal occurrence of parasitoids (Legner & Brydon 1966, Ables & Shepard 1976a,b; Legner & Greathead 1969, Legner & Olton 1971, Rutz & Axtell 1980, Petersen & Meyer 1983, Mullens et al. 1986) and their experimental releases (Legner & Brydon 1966, Legner & Dietrick 1974, Morgan et al. 1975c, Olton & Legner 1975 , Rutz & Axtell 1979).
History of Biological Control Attempts
Beginning at the turn of the 20th Century to about 1968, biological control of flies that breed in waste habitats was attempted by the introduction of a broad range of different natural enemies into areas where the flies presented problems. The Pacific Islands were a focus of much attention with the introduction of dung beetles, several parasitoids and predators during this period. It was believed that the accidental introduction of an ant, Pheidole meagcephala Fab., combined with the introduction of the coprophagous dung beetle, Hister chinensis Quensel, caused significant fly reductions on the islands of Fiji and Samoa (Simmonds 1958). The Islands of Hawaii had 16 introductions from 1909 to 1967 of which 12 established. However, the exact role of these natural enemies in overall regulation of flies on the islands is still not well understood (Legner et al. 1974, Legner 1978).
Rodriguez & Riehl (1962) in California used the novel and successful approach of chicken cockerels as direct predators of fly larvae in chicken and rabbit manure. However, this technique is not utilized today because of the threat that roving birds pose to the spread of avian pathogens.
Research during 1970-1990 centered on the more highly destructive parasitoid and predatory species. Examples such as the encyrtid Tachinaephagus zealandicus Ashmead, five species of the pteromalid genus Muscidifurax and Spalangia sp. were evaluated for their capabilities of attacking dipterous larvae and pupae in various breeding sources. They are believed to be capable of successful fly suppression if the right species and strains are applied in the right locality (Gold & Dahlsten 1981, Morgan et al. 1975c, 1977, Olton & Legner 1975, Pickens et al. 1975, Morgan & Patterson 1977, Rutz & Axtell 1979, Propp & Morgan 1985, Axtell & Rutz 1986, Legner 1988, Mandeville et al. 1988, Pawson & Petersen 1988). Other approaches have included the use of pathogens and predatory mites, and inundative releases of parasitoids and predators (Ripa 1986). Although partially successful, none of these strategies have become the sole method for fly control, and the wrong choice of a parasitoid strain may have detrimental results (Legner 1988). Instead, the focus is on integrated controls including other methods such as cultural, adult baiting and aerosol treatments with short residual insecticides. However, it is generally agreed that existing predatory complexes exert great influences on fly densities (Legner et al. 1975, 1980; Geden 1984, Geden et al. 1987, 1988; Geden & Axtell 1988) and that many biological control agents of endophilous flies have not been thoroughly surveyed, nor their potential adequately assessed (Mullens 1986, Mullens et al. 1986).
Modeling The Organic Waste Ecosystem
A computer simulation model for house fly management was developed by Wilhoit et al. (1991d). The following information pertinent to utilization of models for fly management is quoted from their section on "Manure Ecosystem”:
"The amount and age of accumulated manure depends on the type of animal and the housing system. The typical pounds (kg) of manure per day per 100 lbs (45.4 kg) of animal weight are: laying hen 5.3 (2.4), broiler hen 7.1 (3.2), swine 6.5 (3.0), dairy cattle 8.2 (3.7), and beef cattle 6.0 (2.7) (Hart 1963; Hahn & Rosentreter 1988; Sweeten 1989). Expressed another way, poultry excrete about 5% of their body weight per day, and the manure contains 75% moisture. Cattle (dairy and beef) and swine excrete 6 to 8% of their body weight per day, and the manure contains 80 to 85% moisture. The handling and disposal of such large quantities of manure is a serious problem. Daily removal by flushing and/or scraping is used in some animal housing systems. If done properly and without equipment failures, this will eliminate most of the fly problem. However, daily manure removal is not always practical, appropriate for the animal husbandry system, or cost-effective. The alternative is to clean less frequently and provide for the accumulation of manure."
"Accumulated poultry and livestock manure provides a habitat supporting a variety of interacting arthropods, including flies (Diptera), mites (Acarina), beetles (Coleoptera), and fly parasites (Hymenoptera), as well as nematodes, fungi, bacteria and other microorganisms (Anderson & Poorbaugh 1964; Greenberg 1971; Legner & Olton 1970; Legner et al. 1975; Peck & Anderson 1969, 1970; Pfeiffer & Axtell 1980; Robertson & Sanders 1979). The age of the accumulated manure, the animal nutrition, and whether or not there is added bedding material affect the manure fauna. Although this ecosystem is complex and varies among animal production systems and climatic regions, there are basic cosmopolitan components relevant to house flies and other filth flies (Axtell 1986a, 1986b)."
"Flies.--The most common flies are species in the family Muscidae, which includes the common housefly, Musca domestica L., the little house fly, Fannia canicularis (L.), the false stable fly, Muscina stabulans (Fallén), and black garbage flies or "dump flies," Ophyra aenescens (Wiedemann). The genus Ophyra is considered part of the genus Hydrotaea by some authorities (Farkas & Papp 1990). Other species of Fannia and Ophyra may be present (Adams 1984; Chillcott 1960). In poultry houses during certain times of the year, Fannia become extremely abundant in some regions. The larvae of Ophyra and Muscina prey on the larvae of other muscoid flies and on occasion become very abundant in the manure. Another species of Muscidae, Stomoxys calcitrans (L.), the stable fly, may be present (especially where manure is mixed with bedding materials or feed). This species differs from the other muscoid species, as it is a blood-feeder, attacking humans as well as poultry and livestock. The stable fly is more often a problem in dairy-cattle facilities and beef-cattle feedlots (Morgan et al. 1983). Larvae of these muscoid species compete for an optimal habitat in the manure, and their relative abundance varies. However, the house fly is usually the most abundant species in all types of confined-animal facilities."
"Other Diptera in the manure include several species of blow flies (Calliphoridae) although these are usually in low numbers and restricted to areas where protein is concentrated, such as in animal carcasses and broken eggs. Common species are in the genera Phormia, Phaenicia, and Calliphora (Hall & Townsend 1977; Greenberg 1971). These blow flies have the same basic life cycle as the house fly. Predators (mites and beetles) and hymenopterous parasites of the house fly also attack the immature stages of blow flies."
"Species of small flies, especially in the families Drosophilidae and Sphaeoceridae, often coexist with muscoid fly species in the manure habitat. In poultry houses, and perhaps in other confined-animal facilities, these may be abundant enough to be significant prey for mites and beetles, which usually feed on the immatures of muscoid flies. Large populations of Drosophila may become a nuisance."
"The black soldier fly, Hermetia illucens (L.), is a distinctive species in the family Stratiomyidae, whose occurrence in animal production facilities is erratic, but which sometimes is present in large numbers in poultry and swine houses. The larvae develop through five instars (in contrast to the three instars of the other Diptera described above). Although soldier fly and house fly larvae can be found coexisting, there are situations in which the soldier fly larvae cause drastic reduction in the numbers of house fly larvae due to habitat modification. The large, robust larvae churn the manure and by their activities cause the manure to become more liquified and less suitable for the house fly larvae or for oviposition by the house fly (Axtell & Edwards 1970d; Booth & Sheppard 1984; Bradley & Sheppard 1984; Furman et al. 1959; Sheppard 1983). AT the same time, manure in this liquified condition will not support populations of other arthropods, including beneficial mites and beetles. In caged-layer poultry houses, the soldier fly may nearly eliminate the house fly, but in the process it so liquifies the manure that removal becomes difficult and the manure may flow onto walkways or undermine the foundations of the house. Under the slats in breeder houses, excessive populations of soldier fly larvae will cause the manure to flow out of the slatted area soiling the feet of birds, and subsequently, the eggs. Contamination on the eggs with manure is unacceptable because of the risk of pathogen transmission into the hatching egg."
"House Fly.--Understanding the biology and behavior of the house fly and the major species of predators and parasites is basic to the construction of a fly management model. The life cycle of the house fly and factors affecting the population size are represented in figure 5 (Lysyk & Axtell 1987; West 1951; West & Peters 1973). The stages in the house fly life cycle are egg, larva, pupa, and adult. The larva molts twice, so there are first-, second-, and third-instar larvae"...," with each being larger than the preceding instar. A prepupal stage is sometimes designated and is used in the model, to refer to the period when the late third-instar ceases feeding and begins pupation. Eggs are laid in batches where the manure has an attractive odor and suitable moisture. The first-instar larva hatches from an egg usually within 24 hours, depending on temperature. The overall life cycle from egg to adult is about 10 days in the summer in temperate areas. The rate of development through the three instars is usually 5 to 7 days at 25 to 30°C."
"The fly larvae are adapted for survival in the manure habitat. The larva is white and cylindrical, with the posterior end broad and flattened at the terminus; the anterior is tapered. A complex of anterior sensory structures (dorsal organ, terminal organ, and ventral organ) allow the larva to detect temperature, moisture, odors, chemical constituents of food and habitat, and other aspects of its environment (Chu & Axtell 1971; Chu-Want & Axtell 1972a, 1972b)."
"Anteriorly, there is an interior cephalopharyngeal skeleton with a mouthhook to assist in feeding by rasping at food. Light is detected by internal receptors located dorsally between the posterior flanges of the cephalopharyngeal skeleton. First-instar larvae are negatively phototactic and move away from light and downward in the manure. Last (third) instar larvae react more positively to light and move outward to lighter and drier areas to begin pupation. Eggs and first-instar larvae are exposed to predation by mites, beetles, and other predators in the manure. Usually the later instars are not suitable prey for mites and beetles, although the second instar may be successfully attacked by a few large beetle species and by larvae of Ophyra and Muscina."
"The pupa is formed within the thickened, darkened integument of the third-instar larva. This pupal case, called a puparium, gradually darkens to a dark brown. Pupation occurs mostly in the drier portions of the manure, especially near the margins and surface. The pupa within the puparium develops into an adult fly ready to emerge in 4 to 7 days at 25 to 30°C. The pupa is subject to parasitism by various species of Pteromalidae (Hymenoptera), which oviposit through the puparium onto the surface of the pupa. A few large species of beetles and ants as well as mice may feed on the pupae."
"The adult emerges by pushing off the anterior end of the puparium by means of the ptilinum, an eversible sac that protrudes from the frontal region of the head. The male/female ratio is 1:1. The adult crawls about while the wings unfold and the exoskeleton hardens and dries; it exhibits limited activity for the firs day after emergence. Although adults may disperse after hardening of the cuticle, they often remain in the vicinity if the habitat is conducive to feeding, mating, and oviposition (Lysyk & Axtell 1986b, 1986c; Pickens et al. 1967). Adult flies spend considerable time on the surface of the manure in the daytime, but at night rest on surfaces, mostly in the upper parts of the animal housing (Anderson & Poorbaugh 1964; Keiding 1965; Tsutsumi 1966)."
"Although protected adults provided ample food may live for as long time in the laboratory (e.g., 26 days at 25°C), adults probably survive for only about a week in nature (Fletcher et al. 1990; Krafsur et al. 1985; Kristiansen & Skovmand 1985; Lysyk 1991). Adult fly mortality may be caused by various pathogens as well as by unfavorable environmental conditions."
"The fly has sponging-sucking mouthparts and feeds by means of a proboscis consisting of a fleshy bilobed structure (labellum) with extensive ridges that channel food to the mouth opening. The fly ingests by sucking up liquid foods or by using the prostomal teeth to scrape the surface of foods moistened with regurgitated liquids so that a liquified material can be ingested. Regurgitation and defecation by flies causes tell-tale spotting of building surfaces, equipment, and light fixtures. Fly populations are sometimes monitored by observing this spotting on "spot" or "speck" cards (Axtell 1970a; Lysyk & Axtell 1985, 1986a; Pickens et al. 1972)."
"Mites.--Mites are abundant in accumulated animal manure and include nonpredaceous and predaceous species (Axtell 1961, 1963a; Hulley 1983, 1986; Ito 1970; Toyama & Ikeda 1976b). Several species of acarids are especially abundant in the presence of spilled feed. Species of Caloglyphus are frequently found in poultry manure and probably in other animal facilities. These mites feed on organic matter and microscopic organisms in the manure, and are themselves food for predaceous arthropods."
"The predaceous mites prey on the immature stages of the house fly and other muscoid flies, as well as on the less common species of small Diptera (Axtell 1963b; Rodriguez et al. 1970). In addition, they feed on the smaller acarid mites and on free-living nematodes, which are common in manure (Geden et al. 1988; Ito 1971, 1973, 1977; Rodriguez et al. 1961). These nematodes are important for adequate nutrition of the preadult stages of some predaceous mites, whereas the acarids are relatively less important prey."
"The most common cosmopolitan predaceous mites species are in the families Macrochelidae, Uropodidae, and Parasitidae. Although many species of Macrochelidae have been reported from animal manure (Axtell 1969a), the most important and common are Macrocheles muscaedomesticae (Scopoli), M. glaber Müller), and Glyptholaspis confusa Foŕ. Other smaller macrochelids common in manure but much less effective as predators are: M. subbadius (Berlese), M. robustulus (Berlese), and M. merdarius (Berlese). Among the Uropodidae, Fuscuropoda vegetans (DeGeer) is a common predator (O'Donnell & Axtell 1965; Willis & Axtell 1968; Ito 1970). Another smaller uropodid, Leiodinychus krameri (Canestrini), is abundant in older manure, but it is a fungal-feeder and not a predator (Radinovsky 1965). The Parasitidae are poorly known, but an important species is Poecilochirus monospinosus Wise, Hennessey, and Axtell, which has been reported from poultry manure (Geden et al. 1989; Wise et al. 1988). Species of Parasitus may be found in dairy and cattle manure but less often in poultry houses, and their importance as predators of the immature stages of muscoid flies is not documented (Ito 1977)."
"These parasitid, macrochelid, and uropodid mites are complementary predators due to their feeding preferences and behavior in the manure (Axtell & Rutz 1986; Geden 1990; Willis & Axtell 1968). This conclusion is based largely on studies of their feeding habits in accumulated manure under caged hens. The parasitids colonize fresh manure before the other species, and dispersal is by the deutonymphs being phoretic on flies and beetles. Both the adults and the deutonymphs feed on house fly eggs and first instars. Adult P. monospinosus prefer first instars over fly eggs and can destroy up to 24 fly immatures per day, while deutonymphs destroy fewer fly immatures (about five per day); nematodes and acarid mites are also prey (Geden et al. 1988; Wise et al. 1988)."
"Parasitids are fast-moving and live almost exclusively on the manure's surface. Macrochelids reside on the surface and slightly beneath, and move less rapidly than the parasitids. Fly eggs and first-instar larvae are fed upon by deutonymphs and adults (to a much lesser extent by protonymphs) of M. muscaedomesticae, which prefer the eggs (Geden et al. 1988). Macrochelids also feed on nematodes and to a very limited extent on acarid mites. The adult macrochelid prefers fly eggs to nematodes, while the reverse is true for the nymphal stages. Up to 20 fly immatures may be destroyed per day by a deutonymph or adult M. muscaedomesticae. The adult female is dispersed by being phoretic on flies (Axtell 1964a; Farish & Axtell 1971; Borden 1989)."
"The uropodid F. vegetans is very slow-moving and predaceous on the first-instar fly larvae but is unable to pierce the chorion and feed on the fly egg (O'Donnell & Axtell 1965; Willis & Axtell 1986). it also feeds on manure-inhabiting nematodes and organic matter. uropodids reside deeper in the manure, where they are well situated to feed on the first-instar fly larvae, which move downward in the manure from the surface where the fly eggs are deposited. uropodids tend to aggregate and engage in group attacks and gregarious feedings on the fly larvae. Dispersal of the uropodids is by a specialized deutonymphal stage adapted to be phoretic on beetles."
"The rates of predation on house fly immatures (eggs and first-instar larvae) by the three most common species of parasitids, uropodids, and macrochelids vary greatly with the experimental procedures and the predator-prey densities. Based on recalculations of published data obtained with similar techniques, Axtell (1991) estimated the overall relative rates of predation by the three species as follows: M. muscaedomesticae adult females = 1.0; F. vegetans adult (both sexes) and deutonymph = 0.25; P. monospinosus adult (both sexes) = 0.40; and P. monospinosus deutonymph = 0.20."
"Macrocheles muscaedomesticae.--Worldwide, the most important and extensively investigated predaceous mite in poultry and other confined animal manure is Macrocheles muscaedomesticae... (Axtell 1963a, 1969; Cicolani 1979; Filipponi & Petrelli 1967; Wade & Rodriguez 1961). ..." "Females are diploid and males haploid (arrhenotoky). Thus, unfertilized eggs produce male offspring. Offspring are commonly about 40% female. males are shorter-lived and are not important as predators on house fly. The mite life cycle consists of egg, six-legged larva, protonymph, deutonymph, and adult. The life cycle from egg to adults requires only 2 to 3 days under favorable temperatures (25 to 30°C). Most predation is by the adult female and deutonymph feeding on house fly eggs and first-instar larvae, with a preference for the eggs. The mites will feed on immatures of other muscoid flies, if present, as well as on eggs of Carcinops pumilio. Free-living rhabditid nematodes are fed on by the nymphal and adult stages of the mite and are important in maintaining a high rate of survival and reproduction by the mite. The mites also feed on the eggs and larvae of species of small flies, such as Drosophilidae and Sphaeroceridae, which may be abundant in the manure under some conditions. Acarid mites are another food, although less important than the nematodes and small Diptera."
"The adult female mite is phoretic on the house fly and other muscoid filth flies (Axtell 1964a; Borden 1989; Farish & Axtell 1971; Ho 1990). This phoresy is regulated by olfactory responses in the flies and the aging manure, resulting in dispersal to the most favorable fly breeding areas. The first pair of legs of the mite are not used for walking, but rather are waved about in the air like antennae and possess olfactory sensilla on the tarsi (Coons & Axtell 1973; Farish & Axtell 1966). The mite can detect odors of manure and adult flies; the balance between the two determines whether or not the mite stays in the manure. If the manure is aged and less odoriferous, the mite will leaves by attaching to a visiting fly. Attachment of the mite to the fly is with the chelicerae; normally, no feeding occurs."
"Macrochelids as well as other predaceous mites are able to reproduce and prey effectively on house fly eggs and first-instar larvae in manure that is of reasonable moisture level so that the mites can freely move and locate prey. Wet, fluid manure is physically unsuitable for mite survival and also limits the populations of suitable prey. It is likely that other species, especially beetles, sometimes prey on macrochelid mites in their early life stages, but his is not well documented."
"Beetles.--A great diversity of beetle species has been found in confined animal manure, although the fauna of poultry manure are best known (Hulley 1983, 1986; Hulley & Pfleiderer 1988; Legner et al. 1975; Peck 1969; Peck & Anderson 1969; Pfeiffer & Axtell 1980). The most common families are Histeridae and Staphylinidae. Minor families are Anthicidae, Hydrophilidae, Mycetophagidae, Nitidulidae, and Scarabaeidae. In addition, Dermestes maculatus DeGeer (Dermestidae) and Alphitobius diaperinus (Panzer) (Tenebrionidae) are common in some regions, especially in poultry manure, and are special cases because these beetles tunnel into the insulation materials of the animal houses and cause extensive damage costly to repair. Adults and larvae of A. diaperinus mix and aerate the manure, and prey on house fly immatures, but these benefits are usually outweighed by the structural damage (Despins et al. 1987, 1988; Ichinose et al. 1980; Safrit & Axtell 1984; Vaughan et al. 1984; Wallace et al. 1985). Staphylinidae are known to be predators on other arthropods, including fly immatures, but species identification is difficult and quantitative data on their biology and predation are very limited. Overall, the generally most abundant and significant predaceous beetles in confined animal manure are histerids of the genera Carcinops, Dendrophilus, Margarinotus, Hister, and Gnathoncus."
"Carcinops pumilio.--In poultry manure, and probably in other confined animal manure, the most important predaceous beetle species is the histerid Carcinops pumilio (Erichson)... (Armitage 1986; Bills 1973; Geden 1984; Geden & Stoffolano 1987, 1988; Hulley & Pfeiderer 1988; Pfeiffer & Axtell 1980). The life cycle of C. pumilio and factors affecting its population size are diagrammed... (Fletcher et al. 1991; Geden 1984; Geden & Axtell 1988; Morgan et al. 1983). The life stages are egg, two larval instars, pupa, and adult. The beetle has a long life cycle, requiring about 25 days to develop from egg to adult, with the pupal stage accounting for about one-half of this period. Adults live up to 200 days at 25 to 30°C."
"Adult and second-instar larvae prey on house fly eggs and first-instar larvae, as well as on eggs and larvae of small Diptera in the manure. An adult typically consumes 25 to 50 fly immatures per day, and up to 100 if previously starved. A second-instar larva consumes about 25 fly immatures per day. Although this beetle prefers to feed on muscoid fly immatures, it is opportunistic and will feed on nematodes and acarid mites, as well as immatures of macrochelid mites. It is also highly cannibalistic, which appears to be a(n) significant factor in limiting its populations. The first-instar larvae are too small to be important house fly predators. Eggs and larvae of Carcinops are subject to destruction by other predators in the manure. The condition of the manure affects beetle populations; they do not survive in very wet manure. Also, for successful pupation and adult emergence, an undisturbed site in the manure is required. Adults are rarely observed flying but apparently will do so if subject to sudden limitations in food supply (Geden 1990; Geden et al. 1987). This behavior provides a mechanism for dispersal, but the details are poorly known."
"Parasites.--Parasites of fly pupae are common in poultry houses, feedlots, and other confined-animal production systems having accumulations of manure (Legner & Brydon 1966; Legner & Olton 1971; Patterson & Rutz 1986; Petersen & Meyer 1983; Rueda & Axtell 1985a, 1985b; Rutz & Axtell 1980; Rutz & Patterson 1990; Toyama & Ikeda 1976a). These small parasitic wasps (Hymenoptera) are primarily in the genera Spalangia, Muscidifurax, and Pachycrepoideus in the family Pteromalidae... Species vary among the types of confined-animal systems and climatic regions, but common ones are S. endius Walker, S. cameroni Perkins, S. nigroaenea Curtis, S. nigra Latrielle, M. raptor Girault and Sanders, M. zaraptor Kogan & Legner, and P. vindemiae Rondani. In wet manure, especially outdoors in dairy and cattle feedlots, the species Urolepis rufipes (Ashmead) may be important (Petersen et al. 1985; Smith et al. 1989; Smith & Rutz 1991a, 1991b). Another species, Nasonia vitripennis Walker, is sometimes abundant, and its biology differs from the other species in that many eggs, rather than one, are laid on a fly pupa, and several adult parasites develop and emerge (Legner 1976)."
"Spalangia and Muscidifurax.--Hymenopterous parasites (Pteromalidae) of house fly have significant impacts on house fly populations (Legner 1971; Legner & Brydon 1966; Legner & Dietrick 1974; Legner et al. 1990; Morgan et al. 1975c, 1981; Olton & Legner 1975 ; Petersen et al. 1983a; Rutz & Axtell 1979, 1981; Weidhaas et ala. 1977). The life cycle of these parasites and factors affecting population size is diagrammed in... (Ables & Shepard 1974; Ables et al. 1976; Coats 1976; Mann et al. 1990a, 1990b; Moon et al. 1982; Propp & Morgan 1983). The common species in the genera Spalangia and Muscidifurax have basically the same biology. The life stages are egg, three larval instars, pupa, and adult. Eggs are deposited through the puparium onto the surface of the pupa. All of the larval instars and the pupal stages are inside the puparium. The adult parasite cuts a hole in the puparium and emerges about 3 weeks (25 to 30°C) after egg deposition. Except for a few rare strains, all species of pteromalids are arrhenotokous. In laboratory studies, the offspring of Spalangia and Muscidifurax are often 60 to 70% female, but the sex ratio under natural conditions is not known."
"Normally, one adult parasite destroys the fly pupa during development and emerges from each puparium. Additional fly pupae are destroyed by the effects of host-feeding by the adult parasite. The female parasite cuts a hole (with the ovipositor) in the puparium and feeds on the exudate (Legner & Gerling 1976). As a result of both parasitism and host-feeding, a parasite may destroy up to 15 fly pupae per dan (Mann et al. 1990a, 1990b). Adult parasites are able to locate the fly puparia in the drier parts of the manure, but species differ in their searching abilities (Legner 1977; Rueda & Axtell 1986). Generally, Spalangia spp. are able to locate fly puparia at greater depths in the manure than are Muscidifurax spp. Usually, a fly pupae is parasitized only once. However, incases of multiple parasitism by species of two genera, the Muscidifurax is more likely than the Spalangia to develop to adulthood. Adult parasites spend considerable time on the surface of the manure, where presumably they feed as well as search for fly puparia. These parasites are not restricted to using the house fly as host and will parasitize the pupae of other muscoid filth flies, including Fannia and Stomoxys, as well as calliphorid blow flies (Mandeville & Mullens 1990a, 1990b; Mandeville et al. 1988)."
Omissions from the Model.--The Wilhoit et al. (1991d) model was developed along the central eastern seaboard of the United States and emphasizes parasitoids and predators obviously of primary importance to the area. However, there is great geographic diversity in species complexes in accumulated animal wastes which necessarily requires substituting different species in different areas (Legner & Greathead 1969, Legner & Olton 1970, 1971, Legner et al. 1980 & 1981). For the southwestern United States the histerids Euspilotus liticolus Fall, Gnathoncus nanus Scriba, the staphylinid Philonthus sordidus Gravenhorst, the dermapteran Euborellia annulipes (Lucas), the anthocorid Lyctocoris campestris (F.), and several species of Hydrophylidae are abundant and important predators. Additionally, scavengers in the Dermestidae, Scarabaeidae, Tenebrionidae and Lepidoptera are especially numerous and through their tunneling activities accelerate the composting process. The Wilhoit et al. (1991d) model does consider racial differences in the several species of Spalangia and Muscidifurax, all with different temperature, RH and other ecological requirements. Vagility and dispersal patterns in the different species are not considered. Nevertheless, appropriate adjustments can be included for specific areas.
Important Biological Control Experiments
Significant increases in parasitism and mortality of Musca domestica L. pupae in sentinel bags in open poultry houses were observed after spring inoculative releases of three parasitic wasps, Spalangia endius Walker, Muscidifurax zaraptor Kogan & Legner and Muscidifurax raptorellus Kogan & Legner (Legner et al. 1991). However, natural parasitism was depressed for a period of several weeks following initial inoculations. Experimental Dibrom-8 treatments had significantly lower parasitism than controls. Muscidifurax raptorellus, a South American species, which bears a genetic marker for gregarious oviposition, dispersed 110 meters from release areas in 8 weeks. This species' activity was also significantly correlated with higher temperature. These results were found in studies comparing treatments that were inoculated with three species of parasitic pteromalid wasps and those that received insecticides or were left as controls were conducted in the early 1990's. Seven poultry ranches devoted to egg production, of 200,000-280,000 birds each, were selected in the area between Upland and Highland, California during the spring of 1989, to study the effects of inoculative releases of parasitic wasps on synanthropic fly host, Musca domestica L. Birds were confined in open-sided wooden slat and chicken wire houses covered by a solid roof. Each ranch contained 185-200 m-long rows of opposed wire cages housing 2-3 birds per cage. Manure accumulated under the cages in a typical cone configuration, and was about 0.5 m high when the experiment began. Manure rows were separated by concrete walkways.
Each ranch was divided into four equal quarters; one quarter received applications of Dibrom-8 emulsive (1,2-dibromo-2, 2-dichloroethyl dimethyl phosphate) sprays to structural surfaces at 10-14 day intervals from 23 March through 1 June. The second quarter was left as a control (no insecticide applications nor parasitoids released). The third quarter received weekly inoculations of cohorts from a population of Muscidifurax zaraptor Kogan & Legner (Legner 1988) from Denver, Colorado, and a population of Spalangia endius Walker (Legner et al. 1982) from New Zealand. The fourth quarter received weekly inoculations of Spalangia endius and a Muscidifurax raptorellus Kogan & Legner gregarious hybrid (i.e., >3 parasitoid individuals developed per host), produced by crossing cohorts from populations secured in Peru and Chile (Legner 1988).
Inoculative releases of parasitoids began on 20 April and continued through 8 June (eight releases) to permit attack of M. domestica during the time of year populations increase in numbers. The weekly releases were made at the center of each treatment with numbers of females as follows: 2000 S. endius, 2000 M. zaraptor and 8000 M. raptorellus.
Parasitoid releases were confined to the mid 15.2 m section of four 185-200-m long rows in any given treatment. At least 106 m separated the areas of release.
Sampling for Weekly Population Trends. The sentinel beg technique (Rutz & Axtell 1979, Mullens et al. 1986) was used to estimate parasitism. Bags were constructed of 6.3 mesh/cm fiberglass window screen and each contained 25 12-18 hr old M. domestica puparia. Each week eight bags were placed in each of four 185-200 m long rows (32 bags). These bags were evenly spaced along the 15-m midsection of a row, in dry friable manure (natural larval fly pupation sites) along the edges of the walkways. The bags were covered with 1-2 cm of dry manure. During placement, bags were shaken to ensure even distribution of the puparia within. Upon collection one week later, bags were opened in the laboratory and puparia transferred to 46 cm3 plastic screened vials. Sampling was terminated when manure removal operations began on two ranches in late June.
Ten random sites in the center of each treatment were also sampled for Fannia spp. puparia each week to assess parasitism of another naturally occurring group of hosts during the study interval.
Measurement of Parasitoid Dispersal. Dispersal of M. raptorellus from four release rows was measured by monitoring neighboring rows with sentinel bags at a separate ranch near Highland. These rows were spaced 5, 20, 35, 50, 65, 95 and 110 meters from the release rows and 16 sentinel bags were used in each row. This ranch
did not receive other species of parasitoids.
Thermographs were placed at three ranches with probes placed to record air temperature along the edge of walkways, for the purpose of correlating parasitoid activity with temperature.
Experiments followed a completely random design, with ranches selected at random in the Upland to Hiland area. Treatments in the form of parasitoid releases, Dibrom-8 applications and a control, were assigned at random to each of the four quarters of any given ranch. Analyses of variance were performed on percentage data after arcsin transformation, these data being analyzed on the basis of a completely random design with unequal subreplicates to account for damaged or lost sentinel bags. Duncan's multiple range test (Steel & Torrie 1980) was used to detect significant differences (P <0.05) for any given sample interval. Correlation analyses on untransformed data was used to examine the effects of temperature on parasitization and total host mortality.
Results of these experiments were discussed according to several categories as follows:
Parasitism and Host Mortality. The percentage of sentinel bags attacked and host mortality was significantly higher (P <0.05) in the control from 23 March to 15 May. This was the time parasitoid inoculations were being made (Fig. 1). A similar, but nonsignificant, trend was observed in the percentage of parasitized hosts (Fig. 1).
The principal parasitoid found attacking hosts in the control was a resident strain of Spalangia cameroni Perkins, although a smaller percentage of parasitism also was contributed by Spalangia endius and Muscidifurax zaraptor (Fig. 2).
Activity of parasitoids was significantly curtailed throughout the study period in the Dibrom-8 treated areas, which was especially noticeable by the lower percentage of sentinel bags attacked and hosts parasitized (Fig. 1). Nevertheless, host mortality in the Dibrom-8 blocks steadily increased, probably as a result of insecticide residue accumulating in the breeding habitat as it dripped down from applications applied to the ceiling and beams of the houses (Fig. 1). The activity of Spalangia cameroni was especially curtailed in the Dibrom-8 treatments.
Although parasitism in the parasitoid release treatments was initially significantly lower than in the control (e.g., 6 April to 11 May interval), parasitism gradually became significantly greater in the release blocks than in the controls (Fig. 1). Host mortality and parasitism data showed similar trends (Fig. 1). Spalangia endius and M. zaraptor accounted for most of the parasitism increases, although M. raptorellus appeared to be steadily increasing its activity as temperatures were warming in late June (Fig. 2).
Temperature Influences. Average minimum and maximum temperatures during the parasitoid release period increased only slightly (Fig. 3), and there was a noticeable drop in temperature for a brief period after 11 May. Thus, the observed increases in parasitism were probably due to a combination of population trends and cumulative effects of parasitoid releases (Fig. 2). Random samples of pupae from manure showed that native Fannia spp. accounted for >80% of the natural fly breeding distributed rather uniformly over the available habitat as previously observed (Legner & Brydon 1966, Legner & Dietrick 1974). The Fannia were parasitized by all four parasitoids, thereby serving as wild hosts for parasitoid population increases.
Correlation analyses performed to examine the relationship between parasitism and temperature during the first three days of pupal exposure, when more than 90% of parasitism occurred, indicated no significant relationships for M. zaraptor, S. cameroni and S. endius. However, parasitism by M. raptorellus was positively correlated with maximum and average temperatures (r = 0.572, 0.531, 94 df, significant at P <0.01). Thus, M. raptorellus, of South American origin, may have a slight preference to parasitize at warmer temperatures.
Parasitoid Dispersal. Muscidifurax raptorellus recoveries were made 5 m from release sections of the Highland ranch selected for this study on 18 May and at increasing distances from the release rows on succeeding dates (Table 1). By the last exposure date on June 9th, parasitoids were evenly distributed throughout the rows in which sentinel bags were placed.
Thus, as there were no barriers to parasitoid dispersal out of the sample areas, the degrees of parasitism observed in the present study probably do not fully represent the capacity of any given released species, because of the diluting effects of dispersal.
Relevance of Results to Managing Flies. Much data supports inoculative releases of parasitoids to increase parasitism in poultry manure as a long term strategy. Instantaneous fly suppression from such releases were not observed; in fact, an initial depression of parasitism was produced. But after several weeks the initial depressive effects were countered by an overall increase in parasitism at a time when fly population densities were peaking. Because parasitoids spread gradually from release sites, manual distribution of them at inoculation times would also be desirable in order to accelerate distribution to all breeding sites in a given locality. Because manure removal also eliminates a significant portion of parasitoids by removing hosts in which they are developing, it would be desirable to use an alternate row removal scheme, allowing dispersal from older desposits to new deposits left after cleaning. Further research on removal would be desirable to determine optimum times of year and spacing of such operations.