" ,. Biological Control of Muscoid 1 Status J~nd Potential of Biological Control Agents in Livestock and Poultry Pest Management Systems

Richard C. Axtell North Carolina State University Raleigh, NC 27695, USA

Introduction

Livestock production systems are biological systems which have been organized and structured by humans for filfillment of the goals set by humans (Spedding 1975). Consequently, we should take a broad ecological view of livestock production in relation to our societies and environment as we focus on specific components (subsystems) of livestock production systems (Knapp 1981). One important subsystem is the managtjment of pests of livestock. , ticks, and mites attacking the cause substanHal direct economic losses, estimated to be four billion dollars per year in the USA (Anon. 1979, Steelman 1976). Many pathogens are vectored, or at least maintained, by which necessitates suppression of these arthropod populations in order to reduce the incidence of livestock diseases and the corresponding economic losses. Further, in many cases the arthropods affecting animal production also affect humans, either directly by annoyance and/or biting or by fostering the maintenance and spread of human diseases. Those public health ec;onomic losses cannot be accurately estimated but may be tremendous. Concentrated animal production often increases the populations of arthropod pests affecting the livestock and humans in an area. This is abundantly evident in the case of synanthropic filth flies (e.g., house flies, Musca domestica, and other manure-breeding higher Diptera). ~Ianagement of arthropod pests is not a simple process. :\lany different species of pests with unique biological traits are involved. This is further complicated by several different animal hosts along with different animal management and production schemes. Regional and climatic differences further complicate the picture. It is more and more apparent that an arthropod pest management system must include an integration of methods in a manner compatible with current animal production practices. Among the factors fostering this realization are: (1)lack of effective insecticides and/or application methods for some pests, (2) rapid development of resistance to insecticides by some pests, (3) problems with insecticide residues in animal tissues and products, (4) changing animal production systems, especially the trend to higher density confined systems which encourage high pest populations, (5) greater awareness of ecology and the environment in relation to agri- cultural production, and (6) realization that the economics of livestock production requires that pest management be cost effective. Of particular significance is the realization that situations allowing eradication of an arthropod pest are rare. For most pests it is necessary to maintain suppression measures in an integrated pest management (IPM) program designed to keep the pest population below the level of economic injury (Fig. 1) (Axtell 1979). Usually, control measures are implemented to keep the pest population at a level slightly lower than the economic injury level and this is referred to as the economic threshold. This lower pest population level compensates for the lag time in effectiveness of any control measures that may be utilized. Thus a multipest, ecological approach to managing livestock pests is becoming more widely accepted. The interre- lationships between livestock production, pest densities, and pest management options in livestock and poultry IPM are illustrated in Fig. 2 (Axtell 1981a). In this context, greater utilization of biological control agents is needed and inevitable. These must be meshed with the other categories of control methods as appropriate in each livestock production system. Other categories of control methods to be considered are: cultural (physical and habitat alteration), chemical, and genetic manipulations (sterile release method, chromosomal trans locations, cytoplasmic incompatibility, host resistance, etc.). The major categories of biological control agents are: pathogens (microbials), predators, and parasites. Microbial control involves the use of viruses, fungi, bacteria, and protozoans. These are 2 Miscellaneous Publication No. 61

IPM

>- A MEAN LEVEL ...... - - - - - ~CQtiO_MlC-LN::!l2.R}'_L~~~L- z(f) w ECONOMIC THRESHOLD--- 0

...... (f) MEAN LEVEL B W 0... "

0 TIME .t:::::::-

Figure 1. Diagram of natural fluctuations of the density of a pest population, over a period of time, above and below a \ mean population level A. The objective of IPM is to lower the mean population level to B. The relationship of ~ ; economic injury level and economic threshold are shown (from Axtell 1979).

MANAGEMENT MANAGEMENT -« ------. ACT! ON I -- - - - I PRED IC T I V E MODELS I I I I I Pest Pest I Population I Monoqement I I Dynamics Options ~ Costs vs --- Benefits ! / 1 I Livestock I ---' -' ./ . i;;~ci' .-. ,/ I I Dynomics I I I I I I I I I I I '- - - - -;,- PEST PEST POPULATION ------_I MONITORING I - - - -;,-I PREDICTIVE MODELS

Figure 2. Diagram of the interrelationships among the major components in the de\'elopment of an appropriate IP",I program for a livestock production system. The inner boxes represent research inputs required for the dcsign of an IPM program. The outer boxes connected by a broken line represent the operational inputs of an IPM program based on pest monitoring and predictive modelling (from A.xtell 1981a). Biological Control of ?\1uscoid Flies 3 promising agents for the control of aquatic pests (especially mosquitoes and blackflies) affecting lh'estock and humans. l\tarketing and operational use of the bacteria Bacillus tlwringiensis var. israelensis for mosquito control is a remarkable success. Various fungi hold promise for the control

. of mosquitoes. Certain nematodes also hold promise for the control of mosquitoes. AlthDugh microbial agents are potentially useful they are beyond the scope of this symposium. There are several excellent reviews of the field (e.g., Burgess 1981, Davidson 1981, Laird 1981a,b, Roberts et a1. 1983). ~Hcrobial agents should be considered in the development of any IPM program for livestock and poultry production.

Livestock Production Systems

Livestock production systems and the concurrent arthropod pest problems vary with the livestock species and the goals and practices of the producer. Generally, production systems can be classified as: (1) pasture or range, (2) outdoor confined, and (3) indoor confined. Large pastures are used for beef cattle, sheep, and to some extent for dairy cattle. The economics of livestock production have more and more led to confining the animals in higher densities. Beef cattle are grown to marketable weight in outdoor pens (feedlots). Dairy cattle and sometimes s\\oinemay be maintained in similar outdoor feedlots. Indoor confinement is becoming more common with increasing automation. Dairy cattle may be kept in "free-stall," shed-type housing. Swine and poultry production have been rapidly changing to indoor confinement using buildings vvith open sides or totally enclosed with fan systems or air conditioning, for environmental control. In these systems the swine are held on slatted or expanded metal mesh flooring suspended over waste pits. Poultry may be in cages (especially for commercial egg production) or confined on a bed of wood shavings or rice hull litter. Indoor confined systems allow high density of the animals, which aids in achieving higher feed conversion efficiency and lower costs in labor and land. In these high density confined systems, problems of manure handling and disposal become intense and arthropod pest population can explode.

Flies and Production Systems

The nature of the arthropod pest problems is related to the three categories of production systems. Although ectop:nasites (lice, ticks, mites) are important and the species and their ah.lll- dance are affected by the livestock production system, we will not consider them further. Rather we will focus on muscoid flies associated with livestock manure. In the pasture system the discrete dung pats of beef and dairy cattle are the breeding habicats for horn flies (Haenwtobia spp.), face flies (Musca autumnalis) and bush flies (Musca sorbens complex, especially Musca vetutissirrw in Australia). The quality of the livestock diet affects the dung characteristics and hence the production. The flies lay their eggs on the very fresh dung and larval development is rapid with pupation being in the drier fringes of the dung or adjacent soil. Adult Haematobia are bloodsuckers and spend most of their time on the cattle. Adult face flies and bush flies are not bloodsuckers but have rasping mouthparts, are extremely annoying to the cattle, and may be factors in the spread of eye diseases. Destruction of the fly eggs and/or larvae by predation, parasitism, or alteration (spread and breakdown) of the dung naturally tends to suppress the fly population. Australia is a special case where the lack of a fauna in the dung has caused very slow breakdown of the droppings and loss of pasture quality (Hughes 1975, Waterhouse 1974). Introductions of dung to speed up the breakdown is in progress. In the outdoor confined production system the high density of the cattle results in the dung being concentrated in areas oflittle or no vegetation. The feces are trampled and the soil compacted. The conditions are usual1y not suitable for the pasture flies described above although they may move into the lots from adjacent pastures if there are any. However, conditions are created which favor other fly species. The manure accumulations along fences and the manure-feed mixture around the feeders in the lots are conditions suitable for the production oflarge numbers of house flies (Musca domestica)and biting stable flies (StOllWXYSspp.). Also, piles of silage used for cattle 4 Miscellaneous Publication No. 61 feed in these lots are breeding sites for those fly species. An assortment of other minor species of ~Juscidae and Calliphoridae (blow flies) may occur. With the indoor confined system for dairy, swine, and poultry, the fly problem intensifies, with the most abundant pest species being the house fly. Stable flies. can be major pests in situations where there is an accumulation of manure mixed with feed and/or bedding materials such as in dairy calf pens. Additional frequently abundant manure-breeding flies in these systems are the false stable fly (Mllscina stablllans), garbage flies (Ophyra spp.), little house flies (Fannia, spp.), sphaerocerid dung flies (Coproica, Leptocera), and a variety of calliphorid blow flies (Phrienicia, Calliphora, Phormia). In highly automated systems with daily manure removal, the fly breeding is very low. However, such systems usually require scrappers or flushing equipment which can malfunction frequently resulting in a severe fly problem. }"lanure from such systems may be flushed into a lagoon which commonly is a prolific breeder of Culex mosquitoes (Rutz and Axtell 1978). Like the outdoor cattle feedlots, the indoor confined dairy cattle systems require the storage of large amounts of silage for feed which may breed house flies and stable flies. Indoor swine facilities may use slatted floors ",.ith a pit beneath for the manure and flush water. Crusting and uneven piling of material in the pit may fo;;ter fly breeding. Poultry houses for commercial egg production may have flush or scrape systems for manure removal. In others, the manure is allowed to accumulate under the caged birds and is an exce1lent fly breeding habitat. Broken eggs and dead chickens that are not frequently removed and incin- erated or buried are favored breeding sites for calliphorid blow' flies. Poultry production systems which house the birds on litter (used for broilers and turkeys) have few flies because the litter is too dry. In some chicken breeder flocks, used to produce hatching eggs, the houses have elevated slatted floors in part of the house and the manure accumulation under those slats is a source of muscoid flies. .

Manure Arthropod Fauna

In the manure ecosystem producing muscoid flies, there is a diverse faunal population of com- petitors, predators, and parasites (Blume 1984, Ferrar 1979, Legner and Olton 1970, Merritt 1976, ~'1erritt and Anderson 1977, Valiela 1974). In the pasture system, the scattered dung is exposed to invasion by a diverse heterogeneous fauna. Dung beet1es are important competitors of muscoid flies and important in breaking up, stirring, and aiding in the spreading and decomposition of the dung. This habitat a1teration is important in limiting the production of pestiferous muscoid flies from pasture dung. Additional suppression of pestiferous flies developing in the dung results from the competition by non- pestiferous fly larvae, predation by some beetle larvae and mites, and parasitism of fly pupae by some staphylinid beetles and hymenopterous parasites. The pasture dung fauna of beneficial arthropods includes the following major groups of Coleop- tera: Scarabaeidae (competitors and habitat alterers): Canthon, Boreocanthon, Onthophagus> Phan- aeus, Aphodius; (predators): Rister, Saprinus, Phelister, Euspilotus; Hydrophilidae (predators): Sphaeridium, Cercyon; Staphylinidae (predators and parasites): Aleochara, Philonthus, Oxyteills, Aleocharoia. Among the Diptera, at least 24 families are found in pasture dung with the most species being in the families Calliphoridae, Muscidae, Sarcophagidae, Sepsidae, Antho- myiidae, Ceratopogonidae, Dolichop6didae, Psychodidae, Spaeroceridae, Stratiomyidae, and Tachinidae. Mites in the families Macrochelidae and Parasitidae are found and many are predators on fly eggs and first-instar larvae. Common hymenopterous parasites are in the families Braconidae (Aphaereta), Cynipidae (Eucolia), Diapriidae (Trichopria), and (, Mllsci-

difurax, Pachycrepoidells). . In the livestock and poultry confined systems (outdoors and indoors) there are somewhat different species in the manure fauna than in the pasture dung, although most of the same major groups of arthropods are represented. Scarab beetles are of less consequence in the confined systems and the diversity of fly species is reduced. Species of predacious mites differ in the confined systems from the pasture. Some differences in hymenopterous parasites exist while some species are found both in the pasture and confined systems. Among the major groups of beetle predators and parasites Biological Control of ~luscoid Flies 5 are the following: Histeridae: Hister, Gnatl1Onws, Carcinops, Dendrophilus, Margarinotus; Hy- drophilidae: Cercyoll; Scarabaeidae: Aplzodius; Dermestidae: Dermestes; Tenebrionidae: Alphi- tobius; Staphylinidae: Aleochara, Philonthus, Aleocharinae. Among the Diptera the most common and abundant are several species of 1-.-1uscidae and Calliphoridae. Also occurring are Stratiomyiidae (especially Hennetia), Ceratopogonidae, and . Mites in the families Macrochelidae, Uropodidae, and Parasitidae are often abundant and are predators of fly eggs and first-ins tar larvae. Common hymenopterous parasites are those in the family Pteromalidae (Spalangia, Muscidifurax, Pachycrepoideus, and Nasonia).

Biological Control of Muscoid Flies

With this diverse fauna in pasture dung and confined animal manure it is logical to attempt to exploit some of these organisms as biological control agents to suppress populations of muscoid flies which are pests of livestock and/or humans. Research has been extensive on some species but. overall rather fragmented. Much remains to be done in order to fully evaluate the potential use of the various species of predators and parasites as biological control agents. For reviews and further references see: Axtell (1963a,b, 1969); Bay et a1. (1976); Legner (1978, 1981); Legner and Poorbaugh (1972); Rueda and Axtell (1985a,b). In the pasture dung ecosystem, considerable attention is being given in several areas of the world to enhancing the beetle fauna to increase the rate of dung breakdown and to suppress populations of Haematobia, Musca bush flies (in Australia) and face flies (in North America). In Australia, a program of beetle introductions is being expanded to include introductions of macro- chelid mites. In the USA, a program of beetle investigations and introductions is in progress by the USDA. Worldwide, most attention has been given to Scarabaeidae (especially species of Ap11Odius, Coprinus, Cantlzon. and Onthoplwgus) and Histeridae (especially species of Hister). Parasitic and predacious staphylinid beetles (Aleochara) have been introduced and extensh-ely studied as possible agents for face fly and horn fly control. Some attention has been given to competing and predacious flies, especially Orthelia, Oxysarcodexia, and Ravinia. Next to studies on beetles, the greatest overall attention has been given to hymenopterous parasites in the pasture dung ecosystem. Over the years, many introductions and studies in different locations have been conducted with particular attention to the pteromalids Spalangia haematobia, S. nigroaenea, S. cameroni, S. nigra, and several species of Muscidifurax along with the encyritid TachinaeplwgtLs zealandicus. The pasture dung fauna is genera1ly quite we1l known but the complexity changes in different range habitats. Success in the use of beetles, mites, and hymenopterous parasites for biological control of muscoid pest flies in the different habitats is not predictable. The free roaming of livestock on pastures limits the possibilities for manipulating the management practices to maximize the effects of biological control agents. To date, the emphasis has been on introducing species and/or strains of biological control agents into new areas with the hope that "something will happen"; but there are, in fact, too little data for before and after such releases. - In the confined animal production systems we have a more manageable situation. There are, of course, considerable variations among regions and types of livestock and poultry confinement and housing. In these operations, the emphasis in biocontrol of muscoid flies has been primarily on hymenopterous parasites, predacious mites, and to a lesser extent on a few beetles. Most attention has been given to the more common pteromalid parasites: Spalangia endius, S. nigroaenea, S. cameroni, and Muscidifurax raptor. Recently there has been interest in another species, Urolepis rufipes, which has been found in temperate regions in very wet cattle manure. Among the mites, most effort has been devoted to the predacious Macrochelidae (especially Macrocheles muscae- domesticae), and Uropodidae (especially Fuscuropoda t;egetans) (Willis and Axtell 1968, Farish and Axtell 1971). Predacious parasitid mites are common but have received very little attention (Wise 1970). Among the confined animal production systems, the poultry houses offer a highly managed system and often tremendous populations of muscoid filth flies, mostly Musca domestica. These systems, especially caged layer houses, have been studied extensively (see following and references therein: Anderson and Poorbaugh 1964; Axtel1 1969; Geden 1984; Legner et a1. 1975; Peck 1969; 6 ~fiscel1aneous Publication No. 61

Peck and Anderson 1969, 1970; Pfeiffer and Axtell 1980; Rutz and Axte111980a; Willis and A.xtell 1968). The principles for utilizing biocontrol agents in this system have a \,ider application to other types of confined livestock operations (Axtell 1970a,b, 1981ab). These principles are: (1) maintain the manure in as dry a condition as possible by proper drainage, grading, controlled water systems, adequate air movement; (2) stagger the manure removal schedule and leave a base of old manure to absorb moisture and provide harborage for predators and parasites; and (3) use insecticides selectively to minimize adverse impacts on the predators and parasites. These measures are de- signed to promote the heterogeneity of the fauna and to protect and preserve the beneficial predators and parasites. The primary biocontrol agents for muscoid flies in poultry houses are the mites Macrocheles muscaedomesticae, Fuswropoda vegetans, and Poecilochinls sp., the beetle Carcinops pumilia (Geden 1984, Morgan et a!. 1983), and the hymenopterous parasites Spalangia endius, S. camerani, S. nigroaenea, and Muscidifurax raptor. The composition and abundance of the parasites varies in different climatic regions. Although management of the manure and insecticide usage is the key to enhancing the naturally occurring population offly predators and parasites, there are prospects for augmentation. Attempts to release additional parasites in poultry houses have often, but not always, increased the degree of fly control. Most efforts have been with S. endius and jH. raptor (Legner 1981; ~Iorgan et al. 1975a,b, 1981; Rutz and A,xtell1979, 1980b,1981). One approach is to rear and release indigenous species and strains. The other: is to introduce new species or strains, which often has produced inconclusive results or clear failures. Strain differences in parasite survival and behavior are thought to be very important but have not been adequately investigated. Routine augmentation and/or importation of parasites for fly control in poultry operations holds promise but cannot be done in a reliable manner with present knowledge. Further basic studies on the parasites and their strains are critically needed. The use ofbiocontrol agents for fly control in poultry houses illustrates that a multi-agent approach is needed. One should not seek a single agent as the ideal one. Instead, a combination of parasites and predators should be used. The problem, of course, is how to choose these and mesh them together in a biocontrol program. Based on our knowledge to date, it appears that we should use macrochelid mites, Carcinaps beetles, and pteromalid parasites (perhaps 2 species) in poultry houses. These biocontrol agents are not a panacea. They will be successfully used in an integrated control approach which also includes minimizing fly breeding and ma.;dmizes the heterogeneity of the manure fauna by means of proper manure management. ~fanure management and biocontrol are complementary ap- proaches which are the basis for muscoidfilth fly control in all types of confined animal production facilities. The use of insecticides must be such as to be complementary to those approaches. This means minimal larviciding of the manure with wide spectrum pesticides. Regrettably, most in- secticides that are effective against flies also kill beneficial predators and parasites (Axtell 1966, 1968, 1970b; Axtell and Edwards 1970). Selective chemicals which would allow larviciding are needed. Conceivably, the use of selective chemicals in feed additives could become available. At present, the chemical cyromazine is highly effective against house flies and appears to be non- toxic to manure-inhabiting beetles and mites (Axtell and Edwards 1983). The potential for wide use ofbiocontrol agents for muscoid fly suppression in poultry production facilities is high. This is because considerable knowledge has been accumulated on the fauna of the system and the major predators and parasites, because the production system is highly organized with "integrators" controlling production and management practices, and because the fly problem is severe. As confined production systems for other livestock develop similar characteristics, the potential for use ofbiocontrol agents in those systems is increasing. Presently, however, only crude empirical biocontrol measures can be undertaken. We still lack sufficient detailed data on all aspects of the biology and behavior of most of the important predators and parasites and even on the major fly species. These basic data are needed in order to move to the next level of sophistication, i. e., to develop population models. Crude motlels can be developed now but they are too simplistic and the necessary data are lacking to make the motlels useful in practical programs of fly man- agement. Research is progressing in the direction of producing useful models, however (Weidhaas 1981, Weidhaas et a1. 1977). Biological Control of ~luscoid Flies 7

From this summary of the status and potential ofbiocontrol agents in livestock and poultry pest management systems, it is clear that the potential is great. The use of biocontrol agents fits well iGto IP~l programs. The greatest potential exists in management programs for muscoid flies de- veloping in animal manure and especially in confined-animal production facilities. The present status concerning such biocontrol is that we can empirically improve fly management by using present knowledge of fly predators and parasites, but that our present knowledge isstill too little for full utilization of these biocontrol agents. Coordinated and intensified research on all aspects of the biology, ecology, population dynamics, and behavior of the agents and the target species of flies is obviously still needed.

References Cited

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REFRINTm:M:

Patterson, R. S. and D. A. Rutz (editors). 1986. Biological Control of Muscoid Flies. Entomol. Soc. Amer. Misc. Publ. 61, p 1-9.