Integrated Pest Management Reviews4: 53–73, 1999.© 1999Kluwer Academic Publishers. Printed in the Netherlands.

Poultry integrated pest management: Status and future

Richard C. Axtell∗

Department of Entomology, North Carolina State University, Raleigh, NC 27695-7613 USA;∗Address forcorrespondence (3427 Churchill Road, Raleigh, NC 27607-6809 USA; Tel.: 919-787-1321 or 919-781-2499;Fax: 919-515-7746 or 919-781-2499; E-mail: richardaxtell@ncsu.edu)

Received 9 August 1998; accepted 26 November 1998

Key words:poultry pests, integrated pest management, poultry ectoparasites, muscoid flies, filth flies,manure arthropods, rodents

Abstract

Modern commercial poultry production under large companies is expanding worldwide with similar methods andhousing, and the accompanying arthropod and rodent pest problems. The pests increase the cost of production andare factors in the spread of avian diseases. The biology, behavior and control of ectoparasites and premise pests aredescribed in relation to the different housing and production practices for broiler breeders, turkey breeders, growout(broilers and turkeys), caged-layers, and pullets. Ectoparasites includeOrnithonyssusfowl mites, Dermanyssuschicken mites, lice, bedbugs, fleas, and argasid fowl ticks. Premise pests includeAlphitobiusdarkling beetles,Der-mesteshide beetles, the house fly and several related filth fly species, calliphorid blow flies, moths, cockroaches,and rodents. Populations of these pests are largely determined by the housing, waste, and flock management prac-tices. An integrated pest management (IPM) approach, tailored to the different production systems, is required forsatisfactory poultry pest control. Biosecurity, preventing the introduction of pests and diseases into a facility, iscritical. Poultry IPM, based on pest identification, pest population monitoring, and methods of cultural, biological,and chemical control, is elucidated. The structure of the sophisticated, highly integrated poultry industry providesa situation conducive to refinement and wider implementation of IPM.

Introduction

Commercial poultry production is rapidly expand-ing worldwide to meet the needs of the increasinghuman population. Per capita poultry meat consump-tion is increasing with the reduced cost and enhancedincomes. This large poultry industry requires extensivehousing for the birds and produces large quantities ofwastes (manure, used litter, dead birds) which presentample habitats for the development of arthropod androdent pests. The industry has been growing at 4–5%per year and is expected to continue expansion in theforeseeable future. Effective pest management is a sig-nificant part of the poultry industry operational needs.

The magnitude of the poultry industry is impres-sive (1997 data from U.S. Government, 1998). The

worldwide total of all types of poultry meat production(ready-to-cook equivalents) is about 52 million met-ric tons. The percentages of the world total by regionsand major producing countries are: North America33.2 (United States 28.3), South America 12.3 (mainlyBrazil 8.6), European Union 15.7 (France 4.3, UnitedKingdom 2.8, Italy 2.2, Spain 1.8), Eastern Europe1.8, Russia and Ukraine 1.6, Middle East 2.4 (mainlySaudi Arabia and Turkey), Africa 2.4 (mainly Egyptand Republic of South Africa), and Asia 29.5 (Peo-ple’s Republic of China 21.8, Japan 2.3, Thailand 1.8).The bulk of poultry meat production is broiler chick-ens with the total broiler meat production worldwidebeing about 37 million metric tons. The percentages ofthe world total broiler production by regions and majorproducing countries are: North America 39.2 (United

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States 33.1), South America 15.6 (mainly Brazil 12.0),European Union 15.4 (France 3.2, United Kingdom2.9, Spain 2.4, Italy 1.8, Netherlands 1.7), EasternEurope 1.6, Russia and Ukraine 1.1, Middle East 1.7(mainly Saudi Arabia), Africa 2.7 (mainly Egypt andRepublic of South Africa), and Asia 21.3 (People’sRepublic of China 15.5, Japan 3.0, Thailand 2.4). Thereare an estimated 24 billion broiler chickens raised eachyear in the world; about 8 billion in the United States.Turkey meat production worldwide is about 4.6 millionmetric tons with most of the production in the UnitedStates (53.1%) and the European Union (36.8%).

Egg production in the world is about 707 billion peryear. This requires about 2.8 billion laying hens. Thepercentages of world total egg production by regionsand major producing countries are: North America15.6 (United States 11.0, Mexico 3.8), South America2.8 (mainly Brazil 1.8), European Union 11.7 (France2.3, Germany 2.0, Italy 1.7, United Kingdom 1.5,Netherlands 1.4, Spain 1.4), Eastern Europe 1.6, Russiaand Ukraine 5.7, Middle East 1.3 (mainly Turkey), andAsia 61.2 (People’s Republic of China 47.5, Japan 6.1,India 4.2).

The modern poultry production systems are largeoperations, using high densities of animals, financedand managed by large companies. These productionmanagement systems are highly structured and sophis-ticated, and under the control of a parent company(‘integrator’) who owns the feed mills, hatcheries, pro-cessing plants, transportation, and some of the poul-try houses. The integrator contracts with individualproducers (‘growers’) who raise the poultry, with theyoung birds and feed supplied by the integrator. Thecontract producer usually supplies the poultry houses,utilities and labor. The producer is paid on a per unitbasis (number of eggs, weight of birds) and has to fol-low the instructions of the integrator who employesveterinarians and technical personnel (service persons)who routinely inspect the flocks and records of thecontract producers. With such large scale operations,even very small losses due to pest and disease problemshave a large economic impact on the integrator and thecontract producer. The threat of arthropod and rodentpests is serious and control of these pests requires anintegrated pest management (IPM) approach consistentwith the sophisticated poultry production systems andmanagement strategies.

The objective of this paper is to describe impor-tant poultry pests and principles of their managementin relation to modern, large-scale commercial poultry

production systems. The intent is to synthesize currentknowledge based not only on the extensive literaturebut also on the author’s observations and experiencegained from research and interacting with other ento-mologists and persons in the poultry industry since the1960s. The reader should refer to Axtell and Arends(1990) for a review of arthropods associated with poul-try which contains an extensive list of references. Fur-ther information and references on poultry pests anddiseases are provided by Calnek et al. (1991) andWilliams et al. (1985).

Production systems

Modern commercial poultry production uses fully inte-grated production techniques that allow for the produc-tion of a large number of eggs, or birds for meat, ona small amount of land. This change from old smallflock, low bird densities to large flock, high bird densi-ties has completely changed the environment in whichthe birds are reared and in the stressors that can altergrowth and production. In these high density produc-tion systems, management of the arthropod pests isdirectly related to the type of product being produced(meat or eggs), housing type, feed and water equip-ment, manure disposal, and the environmental qualitywithin the houses. For each type of poultry being pro-duced, there are specific requirements for temperature,air quality and movement, feed, and housing for maxi-mum production at the least cost. The pest populationsare related to the flock management and productionpractices and any pest management strategies must becompatible with the poultry production requirements.

The ecology of the pests is tied to the artificial envi-ronment in which they and the birds exist, and changesin the environment that impact pests can be made only ifthey are not detrimental to the birds. Because the envi-ronment of the various types of production facilitiesdiffer, the complex of pests differs among the systems.As examples, flies (the house fly and related filth flies)are a major problem in caged-layer and breeder housesbut usually not a problem in broiler facilities; northernfowl mites are a problem on the birds in caged-layerand breeder flocks but are rare in broilers which are in ahouse for too short a time (7–8 weeks) for a detrimentalmite population to develop. Although the details varyto meet climatic and geographic needs, the facilitiesand techniques for modern poultry production are verysimilar worldwide. For further information on poultry

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production consult North and Bell (1990) and Parkhurstand Mountney (1988).

In relation to pest management, five categoriesof facilities and production systems for chickensand turkeys are important: broiler-breeders, turkey-breeders, growout (broilers and turkeys), caged-layers,and pullets (caged and floor-grown).

Broiler breedersBroiler breeders or ‘heavy breeders’ are chickens thatare managed for the production of fertile hatching eggswith the offspring being broiler chicks. The breederbirds are genetically selected to produce fast growingoffspring (broilers that reach 2.2 kg in 45–50 days).Male and female adult broiler breeders (in a 1 : 10 or1 : 12 ratio) are maintained in flocks of 4,000–8,000in one-story houses (12–19 m by 120–180 m) at den-sities of about 5 birds per sq. m. The house usuallyhas the middle one-third of the floor (dirt or concrete)covered with litter (wood shavings or other absorbentmaterial) and raised slats along the outer one-third ofeach side of the house. The slat area consists of nar-row wood strips elevated 0.5–0.75 m above the floor.The automatic water and feed equipment are on top ofthe slats which encourages the birds to defecate whileon the slats resulting in manure accumulating beneaththe slats for the duration of the flock. Eggs are laid innest boxes arranged along the edge of the slatted areas.The eggs are collected by hand or an automatic beltsystem. With hand collection, the boxes contain somewood shavings or a tufted plastic floor; with the auto-matic system the boxes have an inclined floor pad and afabric collecting belt. The breeder house environmentis regulated by circulating air with fans and there maybe closed sides with adjustable vents or open sides withadjustable curtains to provide natural ventilation.

Broiler breeders at 18–24 weeks of age are placed inthe house and remain there for 9–12 months after whichthey are removed and the house thoroughly cleaned.The water and feed equipment, nest boxes and slatsare removed and the inside of the house is washed anddisinfected after removing the litter and manure. Thehouse is empty for 3–6 weeks between flocks to allowtime for cleaning and replacing equipment and litter.

Turkey breedersTurkey breeders are maintained for the production offertile turkey eggs to produce offspring to be grown tomarket weight. The female birds (hens) are maintainedin groups of 1,500–2,000 per house (about 4 birds per

sq. m) and the males (toms) in a separate adjacenthouse. The hens are artificially inseminated, usuallyonce a week. Due to the large size of these geneti-cally selected birds (females, 6.8–11.3 kg and males15.8–25.0 kg), natural mating is inefficient and ofteninjurious. The hens are allowed access to nests for onlya short time daily and the eggs are collected frequentlyin order to prevent the hens from attempting to sit or‘brood’ a clutch of eggs and cease further egg produc-tion. The groups of nest boxes rest on the floor andcontain a layer of gravel or other appropriate material.Egg collection is usually by hand but there may be anautomatic system with nest pads and collecting belt.The turkey house is one-story with litter on the dirt orconcrete floor; there are no raised slates. The automaticwater and feed equipment are suspended slightly abovethe litter in rows along the length of the house.

Growout (broilers and turkeys)Broilers and turkeys produced for meat are usuallyraised to market weight in ‘growout’ houses (12–19 mby 92–184 m) on a dirt or concrete floor covered withlitter (wood shavings, peanut hulls or other absorbentmaterial). The house is one-story with adjustable cur-tains on the sides to allow control of air flow and tem-perature; alternatively the house may be closed withfans and vents to control ventilation. There are typi-cally 12,000–25,000 broilers or 5,000–6,000 turkeysper house. Although the litter may be removed and thehouse cleaned between flocks, it is more common touse the same litter for several flocks prior to cleaningthe house about once a year. Some new litter may beadded between flocks after ‘decaking’ (removing areasof hard compacted litter or breaking up the litter with atilling machine). These practices result in an accumula-tion of 15–20 cm of litter in the houses which fosters thebuildup of arthropods in the litter. The automatic waterand feed equipment are suspended slightly above thelitter in several rows along the length of the house.

The 1-day-old broiler chicks are placed in the houseand remain there until market weight (2.0–2.5 kg). Thebroiler chicks are usually confined in a portion of thegrowout house and provided with heaters for 1–2 weeksafter which the temporary partitions are removed andthe birds have access to the entire house (a practicecalled ‘partial brooding’). The broilers remain in ahouse for 42–55 days and a house can be used for 5–6flocks per year. The young turkeys (poults) are segre-gated by sex and raised separately. They are usuallyraised in a separate brooder house for 4–5 weeks and

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then moved to a nearby growout house until they reachmarket weight (hens, 6.3–8.2 kg; toms, 13.6–18.1 kg).The turkey hens require 14–16 weeks to reach marketweight; the toms 18–20 weeks. The practice of grow-ing turkeys in outdoor lots has been largely abandoned,due partially to pest and disease problems.

There is beginning to be use of cage systems forbroiler growout in some regions. In the caged systems,the birds have no contact with the floor and the housesare most often totally enclosed with fans and ventsfor control of air flow. There may be a belt systemfor removing the manure from beneath the cages. Thisarrangement is less favorable for the buildup of arthro-pod pests than the conventional growout system.

Caged-layersCommercial layers are chickens housed for the produc-tion of eggs for eating or used in edible products. Thesebirds are maintained in wire mesh cages in several dif-ferent types of houses. Water and feed is provided to thecages by automatic equipment. Usually the feed line isin front of the cages and water is provided by cups ornipples attached to pipes running on top or behind thecages. The eggs roll out of the cages onto an automaticconveyer belt, although in some older houses the eggsmay be collected by hand. The feces from the birdsfalls through the mesh bottom of the cages and accu-mulates on the floor or falls onto a conveyer belt whichremoves the manure to the end of the house. In the caseof manure falling to the floor, the manure may be left toaccumulate for weeks or months or it may be frequentlyremoved by a scraper or water-flushing system.

The layers are placed in the cages as pullets (16–18weeks old) and remain in the house for 12–18 months.Typically there are 3–4 birds per cage which is about30 cm wide by 30 cm tall by 45 cm deep, although vari-ations in dimensions are common. Other sizes of cagesmay be used including larger ‘colony cages’ with awider front and containing more birds. To maximizethe number of birds per house, the cages are usuallyarranged in stacks of 3–5 tiers of back-to-back cagesattached to steel supports and arranged along the lengthof the house. The only access to the birds is fromthe front of the cages. There may be slanted plasticpanels (dropping boards) between each tier of cagesto deflect the feces and prevent them from falling onthe birds in the lower cages. Most houses are wideenough for several rows of these stacked cages withnarrow walkways between. A house may have opensides with movable curtains for regulating natural air

flow or may be enclosed with fans and adjustable lou-vers and thermostats for temperature control. Housesmay contain 50,000 or more birds with smaller housesholding 10,000–20,000. Several houses of caged lay-ers may be grouped together in a complex containing asmany as 5 million birds. The trend is for larger housesand larger complexes with on-site egg processing facil-ities owned and operated by a company rather than bya contract producer.

There are a variety of caged-layer housing typeswhich may be categorized as (1) high-rise deep pit,and (2) one-story wide-span. The deep pit house is two-story with 30,000–100,000 birds in cages in the secondstory raised 3.6–5.5 m above the dirt or concrete floorof the first story. The manure accumulates for 2–4 yearsin the first-story and is removed with a tractor-mountedfront-end loader. The wide-span houses have the cages1.0–1.5 m above the floor (dirt or concrete). In somecases the manure is allowed to accumulate under thecages for several weeks or months and is removed byhand or with a tractor-mounted scoop. In other houses,the concrete floor has a 15–20 cm deep shallow pitbeneath the rows of cages which is cleaned frequentlyby scraping or flushing. In the ‘scraper’ houses, themanure is moved to the end of the house daily by ascraper pulled by motor-driven cables; in the ‘flush’houses, the manure is moved to the end of the houseand to an outside lagoon daily by flushing the shal-low pit with water pumped from the lagoon. The wastelagoons are usually deep and designed to break downthe manure anaerobically and to be useable for manyyears. In some cases, the lagoons are shallow to allowmore aerobic action to reduce odors.

PulletsPullets are replacement chickens grown from hatch-ing to 16–24 weeks old when they are moved to broilerbreeder or layer houses. The pullets are raised in a vari-ety of housing types including litter-covered floor, wiremesh flooring, and cages. The same types of feeders,waterers, and manure disposal systems as describedabove are used according to the type of housing.

Poultry pests

The pests affecting poultry production may be catego-rized as (1) ectoparasites and (2) premise pests. Theectoparasites include mites, lice, bedbugs, fleas, andsoft ticks. The premise pests include darkling beetles

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(‘litter beetles’), flies, moths, cockroaches, and rodents(mice and rats). Rodent control is an important part ofIPM although the emphasis of this paper is on arthro-pod pests. Arends (1991) describes rodent control inpoultry facilities.

In order to visualize poultry IPM, it is necessary toexamine the biology and control strategies for thesepests in relation to the types of poultry management andhousing. Modern commercial poultry production prac-tices have resulted in exploding populations of many ofthese pests. What were minor pests in small flocks arenow often major pests in high-density large productionsystems.

Ectoparasites

MitesThe northern fowl mite,Ornithonyssus sylviarum(Canestrini and Fanzago) [Acari: Macronyssidae], isthe most common and widely spread ectoparasite(Hogsette et al. 1991, Lemke and Kissam 1986). Intropical areas the species may be replaced with thetropical fowl mite, O. bursa(Berlese), but the biol-ogy, behavior, and control measures are the same forboth species of fowl mites. Fowl mites are common onchickens, turkeys, and all kinds of wild birds; the mitesmay accidentally occur on rodents but do not repro-duce there. The entire life cycle ofOrnithonyssusfowlmites is spent on the bird. The eggs are laid at the baseof the feathers, especially in the vent area, and hatchinto a minute six-legged stage (larva). This is followedby the eight-legged stages: protonymph, deutonymph,and adult. Only the protonymph and adult stages feedon the host. The protonymph feeds twice before molt-ing. The adults feed repeatedly and lay several eggsafter each blood meal. The life cycle is short (as few as5 days) and large populations develop quickly on thebirds. Although the entire life cycle is on the host, somelater stages may wander off the host or be dislodgedand can survive for at least a week thereby offering anopportunity for transmission. The sources of infestationin a flock are infested pullets, wild birds, contaminatedworkers, egg flats, and other equipment brought into thefacility (Kells and Surgeoner 1996, 1997). Mite controldepends on preventing these sources of introductioninto a flock. When an infestation is found, chemicalspraying with high pressure is the common practice.However, it is difficult to achieve control due to poorpenetration of the feathers and a second application isnecessary.

Fowl mites are often a problem in caged-layers, andbreeder flocks. This reflects the type of housing and thelength of time (9–18 months) the birds are in the house.Fowl mites are of little importance in broiler and turkeygrowout houses due primarily to the relatively shorttime the birds are in the house. In commercial caged-layers and broiler breeders, infestations are often theresult of restocking with infested pullets and by visit-ing wild birds. The transport of contaminated egg casesfrom one farm to another is a source of infestation in thebreeder flocks. Laying hens usually have the greatestmite infestation in the vent region while the infestationis more widely spread on roosters. In broiler breederflocks, infested roosters spread the infestation amongthe hens. In turkey breeder flocks, mite transmissionfrom the separate toms to the hens may be by contam-inated workers involved in the insemination process.The infestation in the turkey breeder hens is likely tobe due to using infested poults and wild birds visitingthe houses.

The second type of mites affecting poultry produc-tion are in the genusDermanyssus[Acari: Dermanys-sidae] withD. gallinae(De Geer) the most important(Fletcher and Axtell 1991, Maurer and Baumgartner1992). It is known as the chicken mite, red mite, androost mite. The chicken mite biology is very differentfrom that of fowl mites. The chicken mite is on the birdonly to feed (mostly at night) and spends the rest of thetime concealed in cracks and crevices and litter. Its eggsare laid in the hiding places and hatch into six-leggedlarvae in 2–3 days. The larvae molt into eight-leggednymphs without feeding. The two nymphal stages andadults feed on the birds intermittently. The adults areable to live off the host without feeding for up to 34weeks. The temperature in the habitat used by the lifestages of the mite largely determine the length of timerequired to complete the life cycle from egg to adult.Overall, the chicken mites are likely to complete a lifecycle in a poultry house in about 2 weeks. The chickenmite is seldom seen on the birds because of its intermit-tent feeding at night but skin lesions (especially on thebreast and lower legs) are evidence of the feeding. Thepossibility of differences in behavior among strains ofchicken mites is suggested by reports from Japan of themites staying on chickens to feed and propagate evenin the daytime (Nakamae et al. 1997a,b).

Dermanyssuschicken mites are likely to be a prob-lem in poultry production systems which are favorableto the mite life cycle by providing easy bird access andample hiding places. Therefore, chicken mites most

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often occur in broiler breeder houses; the litter, slats,and nest boxes provide excellent hiding places and easyaccess to the birds. Chicken mites may also be a prob-lem in turkey breeder flocks. The mites may on occa-sions be a problem in broiler and turkey growout housesif the litter is not removed for several flocks. This resultsin plenty of hiding places and time for a significantmite population to develop. There is very little chanceof a chicken mite infestation in caged-layer houses.However, changes in production systems to eliminatethe cages for layers in Europe to meet animal welfareregulations is resulting in more cases of chicken miteinfestations in layers (Hoglund et al. 1995).

Control of chicken mites depends on prevention ofintroduction. Because the mites live most of the time offthe host, they may easily be transported from one farmto another by contaminated workers and equipment.Chicken mites are found on wild birds and may acci-dentally occur on rodents. When an infestation occursin a house, it is necessary to spray not only the birds butthe entire house and its contents; a second spraying isusually needed for effective control. More satisfactorycontrol is achieved between flocks by total removal oflitter and manure, cleaning the house and equipment,and spraying before restocking with birds known to bemite free. The limited number of effective, registeredinsecticides and the development of resistance by themites are problems (Fletcher and Axtell 1991, Beugnetet al. 1997).

LiceSeveral species of lice are known to infest poultry, butthe most common and important in modern poultry pro-duction facilities is the chicken body louse,Menacan-thus stramineus(Nitzsch) [Mallophaga: Menoponidae](Price and Graham 1997). The entire life cycle occurson the host (similar to fowl mites). The eggs are glued indense clusters on the feathers. These masses of eggs areeasily seen and may be especially common on the neckand thighs. The eggs hatch in 4–7 days into nymphswhich rapidly develop through three instars to adultlice. The life cycle requires 2–3 weeks. The nymphsand adults move rapidly on the feathers and skin andare readily seen when the feathers are parted. The licehave biting and chewing (not sucking) mouthparts andtheir feeding leaves rough skin lesions. They also chewon feather barbs and barbules making the feathers lessfull and the habitat less favorable for fowl mites; usu-ally fowl mite populations cannot coexist with chickenlice. Although several species of lice in other genera

may be found on small ‘backyard’ flocks of poultry,those are apparently rare in modern commercial pro-duction systems (Arends 1991).

Chicken lice infestations are most commonlyencountered in caged-layer flocks but may be a prob-lem also in broiler breeder flocks. They are not likely tobe found in broiler and turkey growout flocks due to therelatively short time the birds are housed. Infestationsmay be due to restocking with infested birds, introduc-tion by wild birds, and transmission by contaminatedworkers and equipment. Rodents will harbor lice acci-dentally but are not a natural host. The common sourceof reinfestation in caged-layer houses is egg masses onbroken feathers which are left in the house betweenflocks.

Control of lice infestations by spraying the birds ispartially effective and a repeat spraying is required.For adequate lice control it is necessary to completelyclean the houses between flocks and spray the housethoroughly. It is extremely important that all manureand feathers be removed to assure that some egg massesare not left behind.

BedbugsThe bedbug,Cimex lectulariusLinnaeus [Hemiptera:Cimicidae], is a blood-feeder attacking humans andpoultry worldwide (Usinger 1966). In some tropicaland subtropical areas it may be replaced with anotherspecies,Cimex hemipterusFabricius. Bedbugs occursporadically in modern poultry production facilitiesand an infestation of broiler breeder houses can be aserious problem causing reduced egg production.

Bedbugs, like chicken mites, are on the birds inter-mittently to feed (mostly at night). All stages of the bed-bugs (eggs, five nymphal stages, and adults) are foundconcealed in cracks and crevices in the poultry houseand especially in the slats and nest boxes in breederhouses. The eggs hatch in about 6 days and each of thefive nymphal instars takes a blood meal. The adults feedmany times. Bedbugs are very resistant to starvation;nymphs may survive without a blood meal for 70 daysand adults can live without food for up to 12 months.When feeding, the bedbugs engorge rapidly (10 min orless). The night feeding bedbugs are rarely seen on thebirds and can only be monitored by examining poten-tial hiding places, looking for evidence of fecal spots(on posts, nest boxes, and other surfaces), and by thepresence of lesions on the breast and legs of the birds.

Because the bedbugs spend nearly all of their livesoff the host, development times depend on the house

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environment and the ability of the bedbugs to quicklyobtain a blood meal which is not a problem with somany hosts conveniently nearby. Overall, the bedbugsare likely to complete a life cycle in a poultry house inabout 4 weeks. They readily survive without food in thehouse between flocks making total elimination from ahouse very difficult. The ability of bedbugs to surviveadverse conditions results in certain breeder housesbeing repeatedly infested in spite of attempts to controlthe insects. Similar to the situation with chicken mites,spraying the birds is not an adequate means of con-trol. Control requires thorough cleaning of the houseand equipment between flocks followed by insecticideapplication, although the number of effective and reg-istered chemicals is limited (Fletcher and Axtell 1993).

Although data are limited, damage from bedbugshas been reported as allergic reaction of the grow-ers, egg spots due to fecal deposits, lower production,and increased feed consumption. Poultry workers maybe ‘attacked’ by hungry bedbugs and be inadvertentlycarried to the workers houses where a bedbug popula-tion might be established. Although bedbugs are nor-mally nocturnal, after birds have been removed from aninfested house for several days the insects may activelyseek a host in the daylight.

FleasOn rare occasions fleas [Siphonaptera] become abun-dant ectoparasites in poultry houses, mainly breederand growout housing. The most common speciesare the cat flea,Ctenocephalides felis(Bouche), andthe European chicken flea,Ceratophyllus gallinae(Schrank) (Cotton 1970, Dryden and Rust 1994). Eventhe human flea,Pulex irritans(Linnaeus), may be foundinfesting flocks. Fleas may be introduced into poultryhouses by infested cats, rodents and wild birds. All ofthese species have the same basic life cycle. The adultsblood feed on the host and lay their eggs which easilyfall off the host. The habitat in the litter and nest boxesin breeder houses provides a suitable habitat for theeggs to hatch into larvae which develop through threeinstars (while feeding on organic matter) and form apupae from which the adult flea emerges. The life cyclefrom egg to adult requires about 30 days depending onthe habitat temperature and food supply for the larvalstage.

These flea species should be easily seen movingrapidly through the feathers on the birds. Although theadult fleas prefer to stay on the host some will fall offand be found in the litter and nest boxes along with the

larval stages and pupae. Control of a heavy flea infes-tation requires complete cleaning and spraying of thehouse and equipment as well as spraying the birds.

The sticktight flea, Echidnophaga gallinacea(Westwood), has a different behavior from the otherflea species on poultry. It partially embeds in the skinof the bird, especially around the neck and head region.The flea eggs drop off the host into the habitat anddevelop in the same manner as the other flea species.The sticktight flea is cosmopolitan but rather uncom-mon in modern poultry production. Its biology is poorlyknown. Control is very difficult because the fleas arepartially embedded on the birds and insecticide treat-ment of individual birds is necessary but usually notpractical.

TicksFowl ticks [Acari: Argasidae],Argas persicus(Oken)andArgas radiatus(Raillet), are frequently mentionedas poultry pests but are rare in modern poultry produc-tion. (Kohls et al. 1970). Wild birds may be a sourceof an infestation. Any infestation is most likely to bein breeder houses where the habitat is most compati-ble with the tick biology (similar to the situation withchicken mites and bedbugs). The fowl ticks feed inter-mittently on the birds and spend most of their time in thehabitat. The stages in the life cycle are egg, larva (six-legged), two or three nymphal stages (eight-legged) andadult. The mobile stages feed on the blood of a bird fora few days at a time and then drop off into the litter ornesting material. The adults feed many times and con-tinue to produce eggs at intervals after each feeding.The nymphs and adults can survive for several monthswithout a blood meal. If an infestation occurs, controlmeasures would be essentially the same as used for thechicken mite and bedbug.

Premise pests

Litter beetlesThe major beetle pest infesting poultry litter andmanure is the darkling beetle or ‘lesser mealworm’,Alphitobius diaperinus(Panzer) [Coleoptera: Tenebri-onidae]. This worldwide pest reaches immense popu-lations in litter in broiler breeder houses and growouthouses as well as in the accumulated manure undercaged layers and under the slats in breeder houses(Pfeiffer and Axtell 1980, Rueda and Axtell 1997).The beetle life cycle includes eggs, larvae (6–9 stages),pupae, and adults all of which are found in the litter

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or manure. A complete life cycle from egg to adultrequires about 5 weeks, depending on the tempera-ture (Rueda and Axtell 1996). The adults are extremelylong-lived (at least a year) and able to survive adverseconditions. Some of the beetle larvae in the presenceof dense populations move into the building insula-tion to pupate and in the process destroy the insulat-ing value (Geden and Axtell 1987). Repair of damageto houses is costly and the reduced insulation inter-feres with bird production by making temperature con-trol more difficult. In addition to this costly structuraldamage, the beetles are excellent reservoirs for dis-ease organisms affecting both humans and birds andare a significant hazard to bird production (Jones et al.1991a,b, McAllister et al. 1994, 1995, 1996). Youngbirds can eat large numbers of beetle larvae which inter-feres with normal feed consumption and growth andprovides an avenue for disease transmission (Despinsand Axtell 1994, 1995, Despins et al. 1994). Adultbeetles are capable of flying and flight takes placemostly at night. When beetle infested litter is removedfrom poultry houses and spread on fields, the adultsquickly leave the unsuitable habitat and fly to nearbyhuman dwellings causing great annoyance and oftenlawsuits.

Control of the darkling beetle in the litter of growouthouses is usually attempted by spraying the litterbetween flocks (Weaver 1996). In addition, treatmentof the soil beneath the litter at the time of removalof old litter improves beetle control because many ofthe larvae burrow into the underlying soil to pupate.The popular practice of delaying removal of old lit-ter to only once for every 4 or 5 broiler flocks toreduce the costs of production, has increased the bee-tle problem and made control more difficult. Thereare seldom attempts to control beetles in the manureunder caged layers or under the slats in breeder housesbecause penetration by spraying would be inadequateand chemical treatment may kill the natural predatorsand parasites which suppress the pestiferous fly pop-ulation (discussed later). Although the beetles tend tochurn the manure and assist in drying and may evenprey to a minor extent on fly larvae (Wallace et al.1985), the detrimental characteristics of the beetlesoutweigh any benefits.

A second important pest species of beetles in poultrylitter and manure is the hide beetle,Dermestes mac-ulatus (De Geer) [Coleoptera: Dermestidae] (Jeffries1980). This species is generally less abundant thanthe lesser mealworm in poultry houses but in some

situations it, or a closely related speciesD. lardariusLinnaeus, may be a serious pest. This is especially truein high-rise, deep pit caged layer houses. The biologyand behavior of the hide beetles is very similar to thelesser mealworm. The hide beetles not only bore intoinsulation but also into wood causing significant struc-tural damage. All stages of the beetle (eggs, larvae [5–7 instars], pupae, and adults) are found in the litterand manure. The spilled poultry feed, supplementedby feathers and broken eggs, provides suitable nutrientsfor these beetles. The entire life cycle from egg to adultrequires about 30–40 days. Effective control measuresfor hide beetles have not been developed although sev-eral insecticides are toxic and spray applications mayyield some beetle population reduction.

FliesPoultry manure which is moist is an ideal habitat forthe development of large populations of the commonhouse fly,Musca domesticaLinnaeus [Diptera: Musci-dae], and related species of ‘filth flies’ (Axtell 1986).Excessive numbers of the house fly and other filthflies in poultry facilities are unacceptable because theflies annoy workers, disperse to nearby residences andbusinesses (engendering disputes and lawsuits), andoften constitute a violation of local public health lawsand regulations. Flies are a reservoir and vector of awide variety of pathogenic organism affecting humansas well as poultry. Also, the flies by defecation andregurgitation cause spotting on the structure and equip-ment, on light fixtures (reducing illumination levels),and on eggs (presenting potential for transmission ofpathogens into the freshly laid egg).

The fly populations become greatest in the varioustypes of caged-layer production systems and under theslats in broiler breeder houses. In those situations, accu-mulations of manure provides ample breeding habitatfor flies. Even the scraper and flush systems of frequentmanure removal under caged-layers may produce fliesbecause the equipment leaves pockets of manure dueto poor design or improper operation. In broiler andturkey growout houses, the litter is normally too dryfor fly production but exceptions occur with wet areasaround leaking water systems and high moisture levelsin the litter due to rainwater draining into the houses.The longer birds are kept in a house to reach heaviermarket weights, the greater the risk of higher mois-ture levels and litter compaction leading to greater flyproduction.

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House fly. The house fly is usually the most abundantand pestiferous fly species in poultry houses and it isthe primary object of most fly management and con-trol programs (Wilhoit et al. 1991a). Fly productionis greatly influenced by manure quality, moisture, andtemperature (Barnard and Geden 1993, Barnard et al.1995, Fatchurochim et al. 1989, Wilhoit et al. 1991b).The life cycle usually requires about 6–10 days. Theeggs are deposited in batches in the upper portions ofmanure having the most attractive odor and moisturelevels. The eggs hatch quickly (less than 24 h) to first-stage larvae which subsequently molt into a second-and third-stage larvae. The larvae (‘maggots’) are nearwhite, elongated, cylindrical and the largest last stageis readily seen in the manure. The late third-stage larvaforms a pupal stage inside the altered larval integument(puparium). The puparium containing the pupa is oval,dark brown and immobile. It is readily seen. Pupationoccurs in the drier portions of manure near the surfaceor edges. If pupae and third-instar larvae are present inthe manure when it is removed and spread on fields,adult flies may emerge and disperse causing distress toneighboring homes and businesses.

FanniaFlies. Other muscoid flies common in poul-try manure include several species in the genusFannia [Diptera: Muscidae] (Skidmore 1985). Themost widespread isF. cannicularis(Linnaeus), the ‘lit-tle house fly’, which may be a major pest in someregions. It is about one-half the size of the commonhouse fly. This species often flies slowly in circles inthe house, will disperse to neighbors, and may har-bor human and avian disease organisms. This specieshas the same basic biology as the house fly but thelarvae are different. TheFannia larvae are flattened,brown, and with numerous spiny projections; the pupaehave a similar appearance. Development from egg toadult requires 15–30 days, a longer duration than forthe house fly. OftenFannia larvae will be found in themanure along with house fly larvae. A few other speciesof Fannia with very similar appearance and behaviorto the little house fly occur in poultry houses in someregions and are most readily distinguished by detailsof the arrangement and types of spines on the larvae.

Dump flies. Muscoid flies in the genusHydro-taea(=Ophyra) [Diptera: Muscidae] are often called‘dump flies’ or ‘black garbage flies’. They are com-mon in caged-layer and broiler breeder houses. Thecommon species areH. aenescens(Wiedemann),

H. ignava (Harris) [=H. leucostoma(Wiedemann)]andH. capensis(Wiedemann) (Adams 1984, Skidmore1985). The adults are shiny black, slender, and aboutone-half the size of house flies. The larvae of dumpflies are similar to house fly larvae but more slenderand active. The dump fly larvae prey on small arthro-pods in the manure, including house fly larvae, andH. aenescensis sometimes promoted as a biologicalcontrol agent against the house fly. Dump flies are oftenseen flying slowly in circles in a poultry house simi-lar to the behavior ofFannia flies. In some cases ofhigh populations, dump flies will be an annoyance toneighbors although the dump flies tend to disperse lessreadily than the house fly. Dump flies will leave fecaland regurgitation spots on the structure, light fixtures,equipment, and eggs in a manner similar to that of houseflies.

Soldier fly. The black soldier fly,Hermetia illucens(Linnaeus) [Diptera: Stratiomyidae], is common inpoultry manure worldwide and may be especially abun-dant in high-rise deep pit caged layer houses and underthe slats in breeder houses (Shepard et al. 1994). Therobust larvae churn the manure and physically renderthe habitat less suitable for the house fly and other mus-coid flies. The solder fly oviposits egg masses on thedrier portions of the manure. Larval development (5instars) is slow (2 weeks or more) and the pupal stagelasts 2 weeks or more. A complete life cycle from eggto adult in poultry houses requires 40–60 days, andconsequently larvae can become extremely abundant.Although these larvae discourage the development ofthe house fly and other muscoid flies, the larvae causethe manure to become liquified so that it is difficult toremove and may flow onto the walkways and under-mine foundations of the houses. In breeder houses, theliquified manure may flow from beneath the slats andadhere to the feet of hens. The manure on the feet mayadhere to the surface of the eggs as they are laid in thenest boxes and pathogens may enter the egg through themoist shell. Some pathogens transmitted in this mannercan cause decreased hatch and chick growth.

Adult soldier flies are large, slender and slow fly-ing. They may be found resting on vegetation around apoultry house as well as on the manure and surfacesin the house. They do not readily disperse in suffi-cient numbers to cause problems in nearby residencesor businesses. Large numbers of the soldier fly larvaediscourage house fly development and in rare circum-stances the larvae have been observed to actually prey

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on other fly larvae. The use of soldier flies as a bio-logical control agent against the house fly has beenadvocated. However, the disadvantages of soldier fliesoutweigh any benefits. Also, harvesting the larvae asfish bait and animal feed has been proposed.

Drosophilaflies. Very small non-biting flies breed-ing in poultry manure may become a nuisance due tothe large numbers. A common species worldwide isDrosophila repletaWollaston [Diptera: Drosophilidae]which is dull brown and prefers the cooler areas of poul-try houses for resting (Harrington and Axtell 1994). Itis most abundant in caged-layer houses even if there isa flush or scraper manure removal system. Small accu-mulations of manure are sufficient for the developmentof large fly populations. The adults often congregatearound the feed troughs and along the manure-crustededges of the walkways. Invasion of the adjacent eggsorting and packing facilities causes annoyance to theworkers. Several species of other small non-biting fliesin the families Phoridae and Sphaeroceridae are alsocommon in poultry manure.

Blow flies. Flies [Diptera] in the family Calliphori-dae are commonly called ‘blow flies’. They lay theireggs on media rich in proteins (animal carcasses,broken eggs) where the larvae rapidly develop inless than a week to robust adults. Depending on thespecies, the adults are green, bronze, or black. Com-mon genera associated with poultry production areLucilia (=Phaenicia), Phormia, andCalliphora. Mostblowflies result from improper disposal of dead birds ina poultry operation with very little production of thoseflies from manure. In caged-layer operations, defectiveegg handling equipment may result in broken eggs pro-viding a place for blow fly development. The speciesL. cuprina(Wiedemann) andL. sericata(Meigen) areoften associated with poultry and certain geographicstrains are also known as ‘sheep blow flies’ due to theirlaying eggs and developing larvae in the soiled fleeceof sheep (Stevens and Wall 1996, 1997).

Biting flies. All of the flies described above havesponging type mouthparts, do not pierce the skin and donot feed on the birds. Other flies which have piercing–sucking mouthparts and are able to take a blood mealfrom the birds, include the stable fly,Stomoxys cal-citrans (Linnaeus) [Diptera: Muscidae], and variousspecies of mosquitoes [Culicidae], biting midges [Cer-atopogonidae], and black flies [Simuliidae] (Arends1991). The stable fly may breed in the litter and manure

in poultry houses but seldom in significant numbers.Most stable flies breed outside the houses in accumu-lations of rotting vegetative matter and in livestockmanure mixed with straw or other bedding material.The mosquitoes develop outside the houses in anystanding water. An important mosquito breeding sourceis the poultry waste lagoons if they are not properlydesigned and managed; the major species areCulexquinquefasciatusSay in warm climates andC. pipiensLinnaeus in cool climates (Rutz and Axtell 1978). Thebiting midges (Culicoides) develop outside the housesin very moist soil (especially when contaminated withanimal manure) and in nearby lowlying wet areas. Theblack flies (various species) develop outside the housesin moving water in streams. The invasion of poultryhouses by mosquitoes, biting midges, and black fliessometimes is a major problem and a source of diseasetransmission among poultry operations.

MothsInfested feed can cause the development of substantialmoth populations in litter and manure. Moth infesta-tions in the auger feed delivery systems results in clog-ging and inadequte feed delivery to the birds; this isthe major economic consequence of moth infestations.Control of the moths once a house and the feed deliv-ery system are infested is difficult and requires thor-ough cleaning of the entire system. The most commonspecies of moths [Lepidoptera: Pyralidae] are the mealmoth,Pyralis farinalisLinnaeus, mediterranean flourmoth, Anagasta kuehniella(Zeller), and the Indianmeal mothPlodia interpunctella(Hubner). All have thesame basic biology with the eggs, three larval stages,and pupae in the feed and litter. The late stage larvaeproduces a webbing material which causes the feed andlitter to form clumps.

CockroachesAlthough not common, sometimes tremendous infes-tations of cockroaches occur in poultry houses, espe-cially caged-layers and broiler breeders. The roachesnot only infest the chicken house but invade the egghandling and storage facilities where their large num-bers are a nuisance and the odor is unpleasant. Theroaches stain the surfaces and leave fecal deposits.Roaches are easily transported from one facility toanother in contaminated egg cases. The species ofcockroaches [Dictyoptera] likely to occur are theGerman,Blattella germanica(Linnaeus), American,

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Periplaneta americanum(Linnaeus), and Oriental,Blatta orientalis(Linnaeus).

Factors affecting pest populations

The size of a pest population in and around poultryhouses depends on abiotic and biotic factors. Abi-otic factors refers to conditions of the environment.The most important are temperature and the physi-cal/chemical traits of the habitat. Biotic factors referto the effects of living organisms; this includes natu-ral enemies (predators, parasites, and pathogens), andcompetition among the species. Three factors in poul-try production determine the nature of the abioticand biotic factors. These are: housing type and man-agement, waste management, and flock management.These factors are, of course, interrelated.

Housing managementThe housing type and management are dictated by thetype of poultry being produced, economics, and thepreferences in a particular region and climate. In allcases, the confined poultry housing means that theenvironment is more closely regulated than outside.The temperatures are kept within a range, wheneverpossible, that is most conducive to egg or meat pro-duction. Temperature, moisture, and odor (primarilyammonia) are controlled in part by the use of fans and(in open curtain-sided houses) natural airflow. Properair flow is necessary for bird health and optimal pro-duction. Also, proper air flow is needed to assist indrying the manure and litter to reduce fly breeding. Airflow in open-sided houses is facilitated by cutting theweeds and grass around the house; this also helps inrodent control by reducing harborage. Basic to hous-ing type and management is the initial construction ofthe facility. The houses should be sited on land gradedto promote drainage of rainwater away from the house.Poor drainage that allows rainwater to seep into poul-try houses creates fly problems and undermines housefoundations. Frequent inspection and repair of feed andwater equipment in a house is required to reduce thespillage of feed into the manure and litter, and excessmoisture due to leaking water systems. This routinemaintenance reduces the cost of production and at thesame time reduces the populations of flies and beetlesdeveloping the manure and litter.

Waste managementWaste management refers to how the manure, litter,and dead birds are handled. In wide span caged-layerhouses, manure accumulates under the cages for sev-eral months to a year. In high-rise deep pit caged-layerhouses, the manure is allowed to accumulate for 2–4years. Management of this manure to encourage dryingdepends largely on the air flow, drainage, and elimina-tion of leaking water systems described under housingmanagement. This drying of the manure is necessaryto facilitate the easy manure removal and spreading onfields as well as to reduce fly production. In a similarfashion, proper management of manure under the slatsin broiler breeder houses is required to promote drying.Manure removal systems in the caged-layer houses thatuse flushing or scrapers require optimal maintenance ofthe removal equipment and frequent (daily) use to avoidresidual deposits of manure that build up over time.Such accumulations of manure reduce the efficiency ofthe removal equipment and provide fly breeding habi-tat. Flushing the manure into a lagoon is a commondisposal method that recycles the lagoon water for theflushing process. Proper design and management of thelagoon is required to prevent mosquito breeding. Deeplagoons with steep sides and the margins free of vege-tation do not usually support mosquito breeding.

Litter used in parts of breeder houses and in growouthouses contains a mixture of some feces, spilled feed,and feathers in the wood shavings (or other dry materialinitially provided). Excess spilled feed is undesirableeconomically and because it encourages beetle produc-tion. Dry litter is accomplished by the same dryingfactors described above for manure: proper air flow,drainage, and elimination of water leaks. The frequencyof litter removal from growout houses is often dictatedby economics but the longer the litter is allowed toremain the greater the build up of the beetle population.

Bird mortality is a normal part of poultry produc-tion. Even though mortality may be only 1–3%, withthe large number of birds in a house this results insizable numbers of carcasses requiring disposal. Deadbirds should be removed daily. Dead birds left in thehouse or piled outside the house promote insect devel-opment, especially blow flies, and may be a sourceof disease pathogens. Incineration, composting, andburial are acceptable methods of disposal.

Flock managementFlock management refers to the supervision of thegeneral health of the birds including feed and water

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consumption. Excessive water consumption may berelated to the salt content of the feed, the timing ofwater availability, and high temperatures. Too muchwater consumption by the birds, as well as impropernutrition or a disease condition, can result in fluid feceswhich causes wet manure or litter and encourages flyproduction.

Pest problems are often an indicator of improperhousing, waste, and flock management. Obviously,these management practices affect the abiotic factors inthe poultry production system with the main effects ontemperature, moisture and the condition of the manureand litter. Less directly, these practices also affect thebiotic factors. The populations of natural enemies isinfluenced greatly by abiotic conditions resulting fromthe management practices. In particular, the conditionof the accumulated manure or litter affects how favor-able the habitat is for the survival of predators, par-asites and pathogens that regulate populations of thepest species.

Pest control methods

Methods for controlling pests in poultry productionmay be grouped into three categories: Cultural, biolog-ical, and chemical. Cultural methods are basic to anycontrol program. Included are biosecurity, waste man-agement, equipment management, and housing man-agement (primarily control of moisture and airflow).

Cultural controlBiosecurity is a term used in the poultry industryreferring to all types of measures to prevent the intro-duction of pests and disease organisms into a poultryfacility. Restricting human traffic in and out of a facility,and disinfecting personnel and equipment that do enter,reduces the chances of introducing certain pests, espe-cially ectoparasites which are able to survive withoutbird hosts for a few days to several weeks. Transmis-sion of fowl mites, chicken mites, and bedbugs mayaccidentally occur on workers and equipment. Cock-roaches, either as the mobile stages or as ootheca (theegg case) may be transmitted by contaminated equip-ment, especially poultry egg cases. Contaminated feeddelivered from the feed mill may be a route for theintroduction of beetles and moths into a house; thefeed bins and pipes of the feed delivery system shouldbe periodically cleaned to prevent the build up of pestpopulations. Restricting access by wild birds reduces

the chances of introducing fowl mites, other ectopar-asites, and avian diseases. Control of rodent popula-tions removes these incidental hosts for ectoparasitesand reservoirs for disease organisms. Domestic cats,which may harbor fleas, should not be allowed in thepoultry facilities.

Critical to biosecurity is the thorough cleaning of thehouse and equipment followed by the proper use of dis-infectant and insecticide applications between flocks.The birds used to restock the house must be carefullyinspected to assure that they are free of ectoparasites.Restocking caged-layer houses and broiler breederhouses with 18–20 week old birds can result in a seriousproblem later in the house if even a few of these birdsare infested with ectoparasites. Pullet houses should befree of ectoparasites and treated with insecticides if anyectoparasites are detected.

Waste management includes the proper disposal ofmanure, litter, and dead birds. In housing systems usingscraper or flush systems for daily manure removal, themanure may be directed to a lagoon which may bea source of mosquitoes if not properly designed andmanaged. To minimize mosquito breeding in lagoonsthe sides must be steep and kept free of vegetation.If the lagoon is too small for the number of birds itwill be overloaded and floating masses of manure canbe a source of filth flies. In the absence of a lagoondisposal system, the manure which is removed from ahouse must be either piled and covered to minimize flydevelopment or immediately spread on fields. Manureor litter must be thinly spread on fields and, if possible,turned into the soil. The field spreading should be doneduring the cooler times of the year in temperate cli-mates to minimize odor and fly problems. Dead birdssupport the development of blow flies and should becollected daily and removed from the house for dis-posal by burying, composting, or incineration. In somecases, dead birds are stored and periodically collectedfor transport to a rendering plant in which case the stor-age must be in tightly sealed containers away from thepoultry house.

Equipment management in relation to pest controlrefers mainly to the proper maintenance and adjustmentof water and feed delivery systems. Leaking water sys-tems results in wet manure or litter which fosters flydevelopment. Poorly adjusted feeding systems resultsin feed spillage into the manure or litter which not onlyprovides additional nutrients fostering fly and beetlepopulations, but also increases production costs due towasted feed. Poultry egg collection systems should be

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adjusted and maintained so that little or no egg break-age occurs because the high protein egg contaminationencourages pest populations, especially blow flies.

Housing management involves grading and con-struction so that rainwater flows away from the house,as well as the proper adjustment and operation of fans,vents, and side curtains (depending on the particu-lar housing system) to provide adequate air flow andmoisture control in the manure and litter. Keeping themanure or litter as dry as possible is essential to controlpest populations, especially flies. Keeping the vegeta-tion around the houses cut low is essential for properairflow and removes harborage for rodents.

Biological controlThe use of biological control against pests in poultryproduction is most advanced in the case of the house flyand closely related filth flies, mainly in production sys-tems (caged-layer and broiler breeder houses) in whichthe manure is allowed to accumulate for long periods oftimes (Axtell 1986, 1990, Legner 1995, Wilhoit et al.1991a). There are two basic approaches to biologicalcontrol: the encouragement of the populations of nat-ural enemies already present or augmentation throughperiodic releases (Rutz and Patterson 1990). Parasitesattacking the pupal stage of the house fly are soldand released with varying success. Natural populationsof parasites usually exist and may be encouraged toincrease by assuring that the manure is kept as dry aspossible to provide easy access to the pupal stage of theflies. Likewise, keeping the manure as dry as possibleencourages natural populations of fly predators.

The most common species of fly parasites[Hymenoptera: Pteromalidae] in poultry houses areMuscidifurax raptorGeralt and Sanders,M. zaraptorKogan and Legner,Spalangia cameroniPerkins, andS. nigroaeneaCurtis (Geden 1996, Mann et al. 1990a,b,Rueda and Axtell 1985, Wilhoit et al. 1991c). Themost important predators are the histerid beetle,Car-cinops pumilio (Erichson) [Coleoptera: Histeridae],and the macrochelid mite,Macrocheles muscaedomes-ticae(Scopoli) [Acari: Macrochelidae] (Fletcher et al.1991, Geden and Axtell 1988a, Geden et al. 1988,Stafford and Bay 1994, Wilhoit et al. 1991a,d, Wills andMullens 1991). Other manure-inhabiting mite preda-tors are the parasitid mite,Poecilochirus monospinosusWise, Hennessey and Axtell [Acari: Parasitidae], andthe uropodid mite,Fuscuropoda marginata(Koch)[=F. vegetans(De Geer)] [Acari: Uropodidae] (Axtell1991a, Wise et al. 1988). A variety of other arthropods

inhabiting the manure may assist in reducing house flypopulations by preying on the fly eggs and early instarlarvae (Pfeiffer and Axtell 1980). Consequently, keep-ing the manure as dry as possible contributes to thedevelopment of a heterogeneous manure fauna whichresults in low house fly populations. Encouragementof biocontrol agents by means of manure managementis essential to a fly control program in poultry sys-tems involving manure accumulation (Mullens et al.1996a,b).

The use of other flies to suppress populations ofhouse flies has been advocated but remains question-able due to inconsistent results and objections to highnumbers of flies of any species. The larvae of the dumpfly Hydrotaea(=Ophyra) aenescenspreys on house flylarvae and in some circumstances has been effective insuppressing numbers of house fly adults in caged-layerhouses (Hogsette and Washington 1995). The larvaeof the soldier fly,Hermetia illucens, churn the manuremaking it physically less suitable for house fly ovipo-sition and larval development. Consequently, substan-tial soldier fly populations may result in low numbersof house flies in a poultry house. However, in mostcircumstances large numbers of soldier fly larvae area nuisance and render the manure too fluid for easyremoval and disposal.

In addition to parasites and predators, variouspathogens affecting flies and beetles occur in poul-try production systems. Certain strains of the ento-mopathogenic fungiEntomophthora muscae(Cohn)Fresenius [Zygomycotina: Entomophthorales] andBeauveria bassiana(Balsamo) [Deuteromycotina:Hyphomycetes] are widespread and naturally suppressfly populations (Kuramoto and Shimazu 1997, Mullenset al. 1987, Six and Mullens 1996, Watson et al.1995, Watson and Peterson 1993). These have not beenexploited commercially for fly control. Some nema-todes kill the house fly experimentally but those strainstested have not survived in poultry manure althoughsome nematode formulations are promising (Renn1995). The darkling beetle,Alphitobius diaperinus, isaffected by the fungus,Beauveria bassiana, and com-mercial use may be possible in the future (Steinkrauset al. 1991). The beetle is also naturally suppressed by aparasitic mite,Acarophenax mahunkaiSteinkraus andCross [Acari: Acrophenacidae] which destroys beetleeggs (Rueda and Axtell 1997, Steinkraus and Cross1993). Laboratory experiments have shown the effec-tiveness of various nematodes for beetle control buta suitable strain for field use has not been identified

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(Geden and Axtell 1988b, Geden et al. 1987a). Certainstrains of the bacteria,Bacillus thuriengensisBerliner,are effective against the house fly and darkling beetlein experimental situations but commercial applicationhas not been developed.

Chemical controlApplications of chemicals for control of arthropod androdent pests in poultry production systems is com-mon and often necessary in the absence of alternatives.Insecticides commonly used for applications to thestructure, manure, litter and birds (depending on labelregistrations) are: carbaryl, tetrachlorvinphos, dichlor-vos, cyfluthrin, fenvalerate, lambda-cyhalothrin, chlor-pyrifos, and cyromazine. Methomyl is commonly usedin fly baits. Use of disinfectants for disease control isa standard procedure between flocks. Mixing insecti-cides and disenfectants in one application is often donefor convenience and to reduce labor costs. However,this mixing is risky because there is often inactivation ofeither the insecticide or the disenfectant or both (Gedenet al. 1987b).

Fly control is a critical area requiring judicious andselective application of insecticides to avoid interferingwith the natural population of predators and parasitesattacking the house fly immature stages in caged-layerand broiler breeder houses (Axtell 1986). Protectionof those natural enemies from the adverse effects ofinsecticide applications for fly or other pest control isessential. Chemicals which control house flies are alsousually toxic to the natural enemies. Some selectiv-ity is achieved by restricting the insecticide applica-tions to residual treatments of building surfaces wherethe adult flies rest and by the use of insecticide-baits.Direct insecticide treatment of the manure is not advis-able except in very limited areas of exceptionally largefly maggot populations. A feed additive, cyromazine, isan insect growth regulator (IGR) which is selective forfly larvae and effective in fly control with little adverseeffect on predacious beetles and mites in the manure;it is used mainly in caged-layer and broiler breederflocks (Axtell and Edwards 1983). Cyromazine is alsoused as a spray on manure. House fly control is com-plicated by the rapid development of insecticide resis-tance, including some resistance to pyrethroids andcyromazine (Liu and Scott 1995, Pap and Farkas 1994,Popischil et al. 1996). The use of chemicals, such as tri-flumuron, for autosterilization of house flies has beenproposed and demonstrated experimentally (Howardand Wall 1996a,b).

Beetle control relies mainly on insecticide treatmentof the litter, and sometimes the underlying soil, inbroiler and turkey growout houses. In most cases, bee-tle populations rebound a few weeks after treatment.The most satisfactory control is achieved by treatingbetween each flock. Likewise, the control of ectopara-sites relies on applications of insecticides to the birdsand to the housing. Although some chemicals used asfeed additives have shown effectiveness for ectopara-site control, none are in commercial use due to insecti-cide residue problems in the meat and eggs. Fowl mitecontrol requires penetration of the feathers with a rela-tively high presssure spray which is difficult to achieve,especially in caged-layer houses with the cages stackedclose together (Arthur and Axtell 1983a, Fletcher andAxtell 1991). Mites can be controlled with insecticide-impregnated strips hung in the cages or placed in nestboxes but the costs and labor required for installationhave limited their use (Axtell 1991b). Chicken mitesand bedbugs, which spend most of their time off thehost, require thorough spraying of the house and equip-ment, especially in the cracks and crevices (Fletcherand Axtell 1993).

Special formulations of insecticides with pheromonesand attractants improve control. These are limited inapplications for poultry production pests. Formulationsfor house fly baits containing the sex pheromone (Z)-9-tricosene (muscalure) or other attractants are effectivefor adult fly control (Mitchell et al. 1975, Learmountet al. 1996). Also, muscalure improves the effective-ness of fly-electrocuting black light devices (Rutz et al.1988). Residual insecticide sprays with sugar addedimprove control of resting adult house flies. A bait for-mulation for darkling beetle control is commerciallyavailable. There is a need for more research and devel-opment on the use of pheromones and attractants in thecontrol of poultry pests.

Poultry IPM components

Integrated pest management is a holistic concept beingwidely adopted. The concept in general is discussed byDent (1995) and in relation to livestock and poultry pro-duction by Axtell (1981). Poultry integrated pest man-agement is based on applied ecology – understandingthe pest biology and behavior in the habitat as describedabove in this paper. The first step in an IPM programis proper identification of the pests. Given the artificialhabitat in poultry production facilities there are oftencases of usually minor pests developing into a major

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problem. Overall, the most common pest problems arehouse flies, litter beetles, fowl mites, and rodents. Pestdiagnosis is facilitated by a computer expert systemprogram (PPES – Poultry Pest Expert System) avail-able for downloading from the Internet (World WideWeb) at http://ipmwww.ncsu.edu/vetent/expert.html.

MonitoringPest population monitoring is the basis of poultry IPM.A monitoring program usually is focused on a fewpests most likely to be encountered in a particular typeof poultry production facility. Ectoparasites are mon-itored in a flock by inspection of selected birds forthe presence of fowl mites and lice or symptoms (skinlesions) of feeding by chicken mites and bedbugs. Fowlmites are most abundant in the vent region of hens. Incaged-layer systems, the birds occurring singly (dueto death of cage mates) in a cage should be inspectedfirst because they are most likely to have the great-est fowl mite populations (Arthur and Axtell 1983b).Inspection of crack and crevices, roosts, slats, and nestboxes for the presence of chicken mites and bedbugs isrequired due to those pests feeding only intermittentlyon the host and spending most of their life cycle in thehabitat.

House fly monitoring methods are well developedand involve visual inspection of the manure and lit-ter for fly larvae and sampling of the adult fly activityby spot cards, baited jug traps, and sticky ribbons orsticky cards, and visual observations of flies restingin designated areas (Lysyk and Axtell 1986, Hogsetteet al. 1993). The use of spot cards (Axtell 1970), whichmeasure fly activity by the numbers of regurgitation andfecal spots over several days, has been widely acceptedas a convenient sampling method. The actual density ofhouse flies has been related to the fly abundance indexobtained with spot cards (Lysyk and Axtell 1985).

Monitoring litter beetle populations in the litter ofgrowout houses is by visual inspection and the use oftube traps consisting of a roll of corrugated cardboardinside an open-ended section of plastic pipe placed onthe litter for several days (Safrit and Axtell 1984). Bothadults and larvae of the beetle accumulate in the card-board and give an indication of the population level inthe litter. Rodents are monitored by inspection for thepresence of fresh feces in the house and for openings toburrows in and outside the house. In housing systemswith manure accumulations, mouse burrow openingscan be observed in the piled manure. The depletion of

rodent baits placed in bait stations and in burrow open-ings is another measure of rodent populations.

All of these monitoring methods should be routinelyapplied to detect pest problems early enough to applycorrective actions before the problem becomes too dif-ficult to correct in a reasonable time. The monitoringprocedures also are useful in measuring the effective-ness of control actions after they are applied.

The meaning of monitoring data depends on the cir-cumstance. Accurate records of the monitoring dataallows the producer and integrator to detect any corre-lations of pest intensity with poor flock performance.Because the integrators have accurate records on flockperformance for their large operations, they are ableto fine-tune all aspects of production, including pestmanagement, to achieve the highest rate of return. Thishas been facilitated by the recent widespread use ofcomputers for poultry production records and analy-sis. Those records are confidential but conversationswith integrators often reveal that they have consid-erable insight into what levels of ectoparasites, litterbeetles, rodents, etc. adversely impact their operations.Because those records are not open to the public, thereis a lack of detailed economic loss data in the litera-ture. Experiments to determine economic losses frompest infestations are of limited value due to the practi-cal necessity to use relatively small numbers of birds.With the large numbers of birds involved in commer-cial poultry production even a very small loss per bird(in terms of feed conversion, weight gains, egg produc-tion, etc.) becomes a significant cost to the producer andintegrator. In general, detection of only a few ectopar-asites on a few birds or in the habitat is justificationfor instigating further control measures to prevent thespread of the parasites throughout a flock. An exceptionto this approach may be when the flock is old and near-ing the time for replacement, in which case additionalectoparasite control measures may not be cost effective.Complete ectoparasite control on pullets is necessaryto prevent introduction of the pests into other houses atthe time of restocking.

The significance of the numbers of flies detected bymonitoring is related to the nearness of human hous-ing and businesses to the poultry facility. Generally, thecloser the neighbors the fewer flies which can be tol-erated. Lawsuits and actions under public health lawsdue to fly annoyance can result in significant economicloss and even closing the poultry operation. Low bee-tle numbers are desired to avoid the cost of repair todamaged buildings, the interference with normal feed

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consumption and growth of the birds, and the lossesdue to various avian disease organisms maintained bythe beetles. Also, low beetle numbers are desirable tominimize dispersal to other poultry houses and dis-persal to human dwellings when used litter is spreadon fields. Low rodent numbers, likewise, are an objec-tive to reduce building damage and feed loss, and toeliminate a potential reservoir for disease organisms.Rodents may also move to nearby human dwellingscreating a legal and public health problem.

Control measuresPest control in poultry facilities requires a judiciousmeshing of the cultural, biological, and chemical meth-ods described previously. Biosecurity is always a pri-mary element for preventing as much as possible theintroduction of disease organism and pests into theoperation. Optimal flock, housing, and waste manage-ment procedures should be continuously practiced toassist in suppressing pest populations and to encour-age natural control factors, including moisture control,fly parasites and fly predators. When monitoring indi-cates unacceptable pest levels, additional actions arerequired to improve the implementation of the manage-ment practices. In addition, chemical applications maybe necessary. The timing of insecticide applicationsmust be meshed with the poultry management prac-tices. Very often this restricts applications to betweenflocks in a house when thorough cleaning and spray-ing is possible as for beetle, chicken mite, and bedbugcontrol. Chemical applications for fly control by resid-ual spraying, insecticide–bait mixtures and occasionalmisting are sometimes necessary to bring the adult flypopulation down to an acceptable level. However, thoseapplications must be made with minimal contamina-tion of the manure to preserve the natural populationsof fly parasites and predators (Wills et al. 1990). Onlyspot treatment of the manure in areas of exceptionallylarge numbers of fly larvae and not overall treatmentwith insecticide is recommended. In some cage-layerflocks, the addition of cyromazine to the feed is an inte-gral part of the fly control program and is usually usedfor several weeks and then stopped for several weeksto lessen the rate of resistance development and thecost. Fly population monitoring in those facilities isimportant for refining the timing of the use of the feedadditive. Rodent control, after infestations are detected,is routinely accomplished by the use of one or more ofseveral rodenticide bait formulations applied to rodentburrows and placed in bait stations.

Laws and regulationsA part of a poultry IPM program is conforming withlocal laws and regulations relevant to waste disposal,water quality, and public health. This is variable withinregions of a nation and among nations. More and more,however, restrictions are being placed on the spread-ing of manure and litter, on the use of lagoons formanure disposal and on the disposal of dead birds.In some nations, especially western Europe, restric-tions are being placed on the type of cages and degreeof confinement of poultry. There is a trend to ‘freerange’ poultry production in which the birds are notconfined in cages and have free access to outdoor areasadjacent to the houses; this complicates the pest prob-lems with greater chances for ectoparasite infestationsand disease transmission. Public health laws in mostplaces provide restrictions on any activity which pro-duces insect and rodent pests which may affect humanwelfare.

ImplementationInstituting and operating poultry IPM is a joint respon-sibility of the integrator and contract producers. Ser-vice persons employed by the integrator regularly visiteach producer and oversee flock health and production.These workers are most often trained in poultry scienceand have limited or no background in entomology andpest management. Additional training is usually neededfor those persons and the producer to initiate and main-tain a poultry IPM program. The IPM program is onepart of the total poultry production endeavor and is mostsuccessful when implemented as an interrelated com-ponent of the system. The system approach takes intoaccount all aspects of animal nutrition and production,pest biology and control options, results of pest pop-ulation monitoring, and the comparative costs versusbenefits of pest management.

Summary and prospects

Poultry IPM is possible with the techniques and knowl-edge currently available. Although the interactions arecomplex, a judicious combination of cultural, biolog-ical and chemical control methods meshed with opti-mal flock, waste, and housing management practicesin a systems approach is feasible. In the case of housefly population management a computer simulation pro-gram incorporating the dynamics of fly predators and

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parasites as well as various manure removal and chem-ical control measures has been developed. This pro-gram (FMS – Fly Management Simulator) is availablefor downloading on the Internet (World Wide Web) athttp://ipmwww.ncsu.edu/vetent/expert.html. This sim-ulation model and its components are documented ina technical manual which contains an extensive list ofreferences (Wilhoit et al. 1991a). Computer simula-tion models for other pests need to be developed in thefuture to deal with the complexities of pest manage-ment in poultry production systems. It is difficult toanalyze all of the interactions without the assistance ofsuch models.

In the future, new techniques and knowledge willfacilitate improvements in poultry IPM. New classesof insecticides and insect growth regulators (IGRs), aswell as improved formulations, such as microencapsu-lation, are being developed and some will be applica-ble to the poultry pest problems. Likewise, new speciesand strains of biological control agents will be found.Improved baits, attractants, and traps will provide bet-ter tools. These developments will allow more effec-tive integration of biological and chemical methods inpoultry IPM.

Actual implementation of poultry IPM programshas been limited and not well documented. In someregions of the United States programs have been pro-moted by University personnel (Arends and Robertson1986, Loomis 1986). Shortage of service persons inthe poultry industry with training in IPM has been amajor limitation. In the future that needs to be changedwith special training courses and improved knowledgetransfer through computer aids targeted to the problemsof the poultry industry.

The prospects for wider use of IPM in the poultryindustry are bright. The highly integrated nature ofthe industry means that a structure exists for knowl-edge transfer through the companies and their rep-resentatives to large numbers of contract producers.This organized production system is ideal for dissem-inating IPM information more rapidly and effectivelythan in the more diverse crop production area whichis not often under the direction of large companies.Because the poultry industry is integrated in all phases(feed mill, hatchery, production, processing, and finalproduct distribution), future IPM programs must beexpanded to include all phases of the system and notsimply the bird production aspect. This means provid-ing IPM knowledge for feed mills, hatcheries, process-ing plants, and the warehouses and distribution system.

With the extensive data bases accumulated by the inte-grators, the industry is becoming increasingly awareof the significant cost : benefit ratios associated withimproved pest management. An overall fear and con-cern for avian and human diseases being maintained orvectored by pests will continue to cause the industryto pay more attention to pest management. The IPMapproach offers a means to minimize the use of insec-ticides which corresponds with a desire in the poultryindustry to avoid any presence of foreign chemicals intheir products. Also, the IPM approach offers the indus-try a way to reduce the likelihood of financial lossesdue to regulatory and legal actions related to nui-sance pests. Most important is the fact that the IPMapproach is needed to achieve satisfactory levels of pestcontrol.

The specifics of IPM must continually evolve toadapt to new housing and production practices and theintroduction of new genetic breeds of birds. The pri-mary breeders (companies who select optimal geneticstrains of birds and provide the breeding stock toproduction companies) are operating worldwide. Thenew bird strains selected for optimal feed conver-sion and production efficiency may simultaneouslyhave different susceptibilities to ectoparasites and dis-eases. Although theoretically ectoparasites might becontrolled by vaccines and breed selection, theseapproaches are not practical and the key to effectivepest control will remain the IPM approach based onapplied ecology.

The worldwide expansion of poultry production willcontinue. This will increase adoption of IPM programs.The expansion of the poultry industry in many nationswill necessitate the wider dissemination of IPM knowl-edge and the World Wide Web will be one importantmechanism. The pattern of an integrated poultry pro-duction industry with large companies and contractproducers is being adopted worldwide as the mostefficient and practical business plan. Many compa-nies in developed nations are becoming global as theyenter joint ventures with poultry production compa-nies in the less developed nations. The methods ofpoultry housing and production are similar worldwide.These factors will facilitate future research, develop-ment, and implementation of poultry IPM. The prac-tical question is: Who will provide the funding andpersonnel? In the absence of more University and gov-ernment research and education efforts, in the futurethe poultry industry will have to fund advances inpoultry IPM.

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Acknowledgements

Numerous entomologists, poultry scientists, veterinar-ians, and poultry producers have contributed over manyyears to the author’s understanding of poultry pest man-agement problems. The research and intellectual con-tributions of many graduate students and postdoctoralresearch associates has been critical. The practicalinsights and suggestions provided by M. Stringham(Extension Entomologist) and T. Carter (ExtensionPoultry Scientist) at North Carolina State Univer-sity are gratefully acknowledged. However, the authoraccepts full responsibility for the content and viewsexpressed in this publication.

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