Filth Fly Impacts to Animal Production in the United States and Associated Research and Extension Needs

Abstract

Many flies are considered serious pests of livestock, poultry, and equids. These pests can negatively impact animal welfare and contribute to considerable production losses. Management of filth fly pests in particular, including the house fly (Musca domestica L.), stable fly (Stomoxys calcitrans (L.)), horn fly (Haematobia irritans (L.)), face fly (Musca autumnalis De Geer) (Diptera: Muscidae), and little or lesser house fly (Fannia canicularis (L.) (Diptera: Fanniidae)), has been a research and Extension priority of veterinary entomologists for many decades. However, ongoing changes to animal husbandry and production practices, coupled with an increasing development of behavioral and physiological resistance to insecticides require renewed focus on new and more effective management strategies. This article is the first in a series of updates to these historical reports and the purpose is to serve as a resource for veterinary practitioners, consultants, funding agencies, veterinary entomologists, industry, commodity groups, and the scientific community working towards control of these pests. Companion articles will review individual filth fly species of importance to animal agriculture in the United States

Of the many thousands of species of flies (order Diptera), only a few are classified as “filth flies” due to their close association with animal feces, food waste, or carrion. Some of these flies are a major concern to animal production, including the house fly (Musca domestica L.), stable fly (Stomoxys calcitrans (L.)), horn fly (Haematobia irritans (L.)), face fly (Musca autumnalis De Geer), and little or lesser house fly (Fannia canicularis (L.)). These filth flies are often closely associated with animals and animal feces that these flies preferentially or even exclusively use for immature development. Animals also provide food (e.g., blood, exudates, or other body secretions) for adult flies of some of these species. Given their association with animals, especially animal waste, filth flies are recognized as important potential vectors for many pathogens of animals and humans (Nayduch and Burrus 2017).

Successful management of some important fly species has been achieved through targeted research on fly biology coupled with the education of producers regarding effective methods for control. The eradication of the primary screwworm Cochliomyia hominivorax (Coquerel) (Diptera: Calliphoridae) from North America and the resulting $1.3B in economic benefit to the U.S. resulting from this eradication (Vargas-Teran et al. 2005) is an excellent example of what can be achieved by focused effort on fly management. Yet many filth flies remain challenging pests for animal producers.

The impact of the primary screwworm eradication program example illustrates the importance of supporting researchers in veterinary entomology and veterinary parasitology in the United States (Mullens et al. 2018). Recognizing the importance of such research, the United States Department of Agriculture (USDA) organized a workshop in 1979 in Manhattan, Kansas to identify needs and opportunities for improving pest management in livestock, poultry, and equine facilities. Participating veterinary entomology experts from the United States and Canada were charged with assessing the availability and effectiveness of IPM programs for filth flies and other arthropod pests of animals and recommending priorities for future research and Extension (Anonymous 1979). In 1994, a similar workshop was held in Lincoln, Nebraska to update these previous findings which lead to a final report often referred to as “the Lincoln Document” (Geden and Hogsette 1994) which was further revised in 2001 (Geden and Hogsette 2001). However, since the 2001 revisions, many changes in animal housing and husbandry practices have occurred and which may have altered the production and management of filth flies in animal production.

This article is the first in a series of updates to these historical reports and the purpose is to serve as a resource for veterinary practitioners, consultants, funding agencies, veterinary entomologists, industry, commodity groups, and the scientific community working towards control of these pests. This introductory article reviews the effect of filth flies on eight animal commodities in the United States: range beef cattle, confined beef cattle, dairy, poultry, swine, ovine (sheep and goats), and equids (horses, mules, and donkeys). The types of economic loss resulting from filth fly activity, attributes of animal production systems associated with filth flies, and specific animal commodities are discussed. Companion articles reviewing individual filth fly species of importance to animal agriculture in the United States. Currently, the collection includes articles reviewing the stable fly (Rochon et al. 2021), horn fly (Brewer et al. 2021), face fly (Trout Fryxell et al. 2021), house fly (Geden et al. 2021), Fannia flies (Murillo et al. 2021), and economic assessments of filth flies (Smith et al. 2021)

Filth Fly Damage to Animals and Pest Categorization

Filth fly species commonly associated with animal production may be categorized as intermittent ectoparasites, temporary ectoparasites, or environmental (nuisance) pests depending upon their degree of association with their animal hosts (Table 1) (Gerry 2018). Intermittent ectoparasites maintain long-term contact with a single host throughout one or more life stages, while temporary ectoparasites are those that contact any individual host animal only briefly (generally to feed) and may contact more than one host animal during a single life stage. Temporary ectoparasites often move among different host animals, a behavior supporting the transmission of pathogens among hosts. Environmental pests require no direct contact with an individual host animal, although they may feed on animal exudates if available, but are attracted to or develop within animal waste, where they can acquire animal pathogens which are then transported and deposited elsewhere as an environmental contaminant. Filth fly species categorized as environmental pests are often those that cause nuisance to people.

Filth flies negatively impact animals and animal production by causing direct or indirect damage, or by peripheral effects related to fly activities such as spotting and discoloration of facility structures or nuisance to the surrounding community (Williams 2009). Because of variable husbandry practices and management techniques, control of filth flies is not formulaic. Management programs must account for the biology of each fly species, their phenology, facility design (e.g., housing), and management, and include the tolerance of affected animals and humans.

Direct Damage

Biting flies, including stable flies and horn flies, cause direct damage to animals from blood loss, tissue damage, and allergic reactions to fly bites. The relationship between fly abundance or biting rate and the degree of damage to animals is not always clear. However, high levels of biting activity of stable flies and horn flies can reduce cattle weaning weight (Campbell 1976, Campbell et al. 1977), weight gain (Campbell et al. 1987, Wieman et al. 1992, Campbell et al. 2001), feed conversion efficiency (Miller et al 1973, Campbell et al. 2001), milk production (Bruce and Decker 1958, Harris et al. 1987, Basiel 2020), and overall farm profitability (Catangui et al. 1997, Berry et al. 1983). Biting flies can also elevate physiological stress of animals as indicated by increased cortisol levels (Schwinghammer et al 1986, Vitela-Mendoza et al. 2016). Stress responses are associated with animal age with younger cattle reacting more strongly to biting flies than older animals (Schofield and Torr 2002), potentially resulting in greater economic damage as young cattle are in a period of rapid growth.

Indirect Damage

Indirect damage includes animal disturbance and pathogen transmission. Indirect damage and its economic impacts can be difficult to assess and are particularly challenging to quantify.

Disturbance

Some filth flies have painful bites resulting in animal disturbance, alteration of normal animal behaviors, or self-inflicted wounds as animals attempt to avoid or evade pests. Irritation caused by biting flies can cause animals to express fly-repelling behaviors such as head shaking, ear flicking, leg stamping, skin twitching, tail swishing, or scratching (Harvey and Launchbaugh 1982; Keiper and Berger 1982; Harris et al. 1987; Warnes and Finlyson 1987; Dougherty et al. 1993a,b,c, 1994; McDonnell 2003; Mullens et al. 2006; Vitela-Mendoza et al. 2016). Incidence of these fly-repelling behaviors is generally related to the number of flies on the animal (Harris et al. 1987, Dougherty et al. 1994, Mullens et al. 2006). Monitoring fly-repelling behaviors may be a better indicator of fly impacts to animals than recording fly abundance on those animals (Mullens et al. 2006). In addition to fly-repelling behaviors, animals may also demonstrate fly-avoidance behaviors including defensive aggregation or “bunching” into tight groups with individual animals attempting to move into the interior of the group to avoid biting fly attack (Hart 1992). This fly avoidance behavior occurs in cattle (Wieman et al. 1992, El Ashmawy et al. 2019) and horses (Duncan and Vigne 1979). For some fly species, even low pest numbers can influence animal behaviors. For example, cattle bunching can occur when stable fly attack rates exceed a pen-level mean biting rate of just one stable fly per cow foreleg (El Ashmawy et al. 2019). Even non-biting face flies have been associated with bunching in cattle (Schmidtmann and Valla 1982). If free to roam, animals may move to areas where fly numbers are lower (e.g., a windy ridgeline), even if forage availability at that location is poor (Keiper and Berger 1982, Belanger et al. 2020). Fly avoidance and repelling behaviors can result in reduced growth and loss of condition because the time spent in performing these behaviors is time lost from grazing (Dougherty et al. 1993b, 1994, 1995), resting, or feeding young (Keiper and Berger 1982).

Pathogen transmission. Filth flies can carry and transmit numerous animal and human pathogens including protozoa, bacteria, viruses, and nematodes (Greenberg 1971, 1973; Olsen 1998; Graczyk et al. 2001; Nayduch and Burrus 2017). Filth flies are typically mechanical vectors of these disease agents, acquiring pathogens on the body or mouthparts during contact with a contaminated surface and transporting them to another location where the pathogen can infect a new susceptible host. However, some filth flies can be true biological vectors where the fly is a required intermediate host for a parasite. For example, nematodes in the genus Thelazia are spread among animal hosts by flies feeding on eye secretions of animals (Világiová 1967), and infection of cattle and horses with these worms greatly increased after the introduction of face flies into North America in the 1950s (Kennedy and Moraiko 1987).

Peripheral Damage

Negative impacts other than damage to animals are categorized as peripheral effects. These include fly nuisance to persons on the animal facility or in the surrounding community, and aesthetic damage to structures, trees, or other surfaces caused by deposition of fly fecal and regurgitation spots. Additional peripheral effects can include mandated quarantine due to animal pathogens or infections, unintended impacts of pesticide application for fly control (environmental contamination, increased pesticide resistance, and human exposure to insecticides), or economic cost associated with changes to animal husbandry practices or facility design in order to reduce fly production.

Fly nuisance can be a source of considerable tension between animal producers and surrounding communities, often leading to complaints or even in lawsuits filed against the animal producer (Thomas and Skoda 1993, Winpisinger et al. 2007). Case law that includes flies associated with animal production can be found as early as the 1960s, and in the last several decades’ case filings have increased as residential homes have become increasingly common in historically rural areas. Although any animal facility can produce filth flies, facilities with high-density confined cattle, poultry, or swine are often the target of fly nuisance litigation (Thomas and Skoda 1993). Litigation has also targeted non-animal facilities where the application of feces to field sites results in emerging adult flies, emphasizing that feces management does not end at the animal facility. Significant fly production can also be associated with urban sites including waste landfills (Dhillon and Chalet 1985, Lole 2005, Goulson et al. 1999, Howard 2001).

Animal Production Systems

Animal production systems can have a direct influence on the type and density of filth fly pests that may be present. Therefore, it is necessary to understand how systems operate to develop relevant IPM programs for filth fly control. In addition, the value and scale of each commodity may influence the accessibility of fly control products and priority for filth fly research. For example, significantly more federal, state, and commodity-specific organization funds are available for research in high-value and scale animal production systems like poultry, beef cattle, and dairy cattle that are not available for equine facilities, swine, and goats and sheep.

Animal production systems can be generally categorized as extensive (Fig. 1), intensive (Fig. 2), or mixed (Fig. 3) depending upon the level of mechanization and automation, human control over animal feed and nutrition management, amount of labor directed toward animal care, and to some extent animal density (Gerry 2018) (Table 3).

Extensive animal production is primarily pasture or range-based with animals foraging freely on grasses or other available vegetation, and with animals handled or viewed irregularly throughout the year. Supplemental feed may be provided to animals in extensive systems, but this is typically limited to providing needed nutrients or increasing food options when pasture conditions are poor. Overall animal density in extensive production is generally low as pastures must be protected to ensure sustainability and quality of available forage. Some filth fly species (horn fly and face fly) require fresh, undisturbed cattle feces (Harris et al. 1968) and are thus abundant only in extensive (pasture) cattle systems.

In contrast, intensive animal production is typically synonymous with high-density animal production. Axtell (1986) further classified intensive production systems as either outdoor confined or indoor confined systems. Here, animals are confined to a limited physical area where they are fed a controlled diet to achieve greater feed conversion efficiency thereby increasing animal production at a reduced cost to the producer for land and labor. Technological innovations have increased the efficiency and productivity of many animal production facilities and have concentrated larger numbers of animals into smaller spaces. Confinement systems include outdoor pens (drylots and feedlots) or indoor housing with animals allowed to range freely or group into pens, stalls, or cages. Beef cattle, dairy cattle, and swine may be held in outdoor pens with feed controlled by facility employees. Relative to pasture-based production systems, outdoor pens also allow for increased worker contact with animals, including the ability to apply medication and insecticides. Indoor confinement further increases production efficiencies through increased animal density, greater control over animal activity and environmental conditions, and more contact between animals and facility employees. Swine, poultry, and in some regions, dairy cattle, are held in indoor confinement systems with limited or no exposure to the outdoors. Swine and poultry, in particular, are often housed in intensive confinement and held indoors in individual or group pens or cages allowing for more efficient delivery of feed, leading to an additional increase in animal growth rate and production efficiency. However, to address animal welfare concerns in animal agriculture recent trends are toward reduced use of individual or small group cages (Centner 2010). Organic and free-range animal production is also moving counter to the increasing intensification of animal production (McBride and Greene 2009).

Intensive animal production often results in the production and accumulation of a substantial quantity of animal feces often within a relatively small area. This necessitates routine management of waste for the health of the animals and to reduce the production of filth flies. Animal feces in intensive animal production are routinely collected by facility workers and often temporarily stored on-site for later disposal. Intensive animal production also requires on-site storage of animal feed, as confined animals lack natural forage. Several filth fly species readily develop in fermenting animal feed including spilled or waste feed (Meyer and Peterson 1983, Broce et al. 2005). Without appropriate management, accumulation of animal feces and waste feed in intensively managed animal facilities provides numerous sites for filth fly development.

Mixed production systems have elements of both extensive and intensive husbandry. Equids and free-range poultry are frequently provided open pasture but also often have an element of indoor confinement in stalls or coops.

It is important to note that classification into one of these three systems on an individual farm may change according to season or region. For example, a dairy farm in a northeastern state may follow an extensive model in the summer months with cattle grazing freely on pasture but move to an intensive model in the winter with cattle brought into high-density sheltered winter housing. Some farms may have extensive and intensive operations on the same property. These individual farm characteristics play a role in fly production and management.

To improve control of filth flies in different animal systems it is important to understand the systems themselves and the husbandry practices that may lead to filth fly production. In subsequent sections, the common animal production systems in the United States are reviewed based on current surveys from the United States Department of Agriculture (USDA) and other research. Practices that may result in fly pressure and health concerns that may be related to pathogen transmission by flies are described, if known. It is important to note that many of the effects of filth flies, direct, indirect, and peripheral, and control options for filth fly pests are not reported nationally. Similarly, surveys are not consistent among animal production systems.

Extensive Animal Production Systems

Cow-Calf

Cow-calf production is the sector of the beef industry that is the most diversified in terms of management practices, with the average beef cow herd having fewer than 50 heads (USDA-ERS 2019). Operations with 100 or more beef cows compose approximately 9% of all beef operations and 56% of the beef cow inventory. Beef cow inventory as of July 2019 was 41.7 million head of animals with an additional 36.3 million calves (USDA-ERS 2019).

Most resources for cow-calf production systems are devoted to maintaining a herd of cows producing one calf crop per year either in the spring or in the fall. The overall product is weaned calves that are sold to backgrounding lots (calves developing in drylots until transferred to a stocker or feedlot), stocker operators (postweaning growing programs that produce commercial feeder cattle and are primarily raised on forages), or beef feedlots (outdoor pens typically without growing native forage) (Drouillard 2018). This type of beef production is considered an extensive system, with many operations relying on pasture or native rangelands as the main food resource for the animals (Gerry 2018). These cattle systems have limited management inputs in comparison to a beef feedlot and use larger areas of land per animal (Talley and Machtinger 2020).

Filth flies impacting the cow-calf sector include horn flies and face flies which exclusively use fresh cattle feces for development (Harris et al. 1968), as well as stable flies which develop in older cattle feces and silage or other plant waste. Horn flies and stable flies feed on animal blood and can cause direct damage when biting rates are high. In addition to causing damage from their painful bites, horn flies can also transmit pathogens such as Staphlyococcus aureus that can cause mastitis (Owens et al. 1998). Face flies often feed along the margin of cattle eyes where their scraping mouthparts can cause eye irritation resulted in increased discharge from the eyes. Face flies can also transmit pathogens including Thelazia eyeworms (Moolenbeek and Surgeoner 1980) and Moraxella bovis, the causative agent of infectious bovine keratoconjunctivitis (i.e., bovine pinkeye) (Hall 1984). Pinkeye incidence rates coincide with face fly population peaks in mid to late summer, with up to 28% of preweaned beef calves being infected (Snowder et al. 2005).

Fly control in cow-calf systems is challenging because of the large land areas encompassed by these operations and the development of insecticide resistance in some fly populations. In 2008, about one-half of all producers with herd sizes of <50 cattle used pour-on products for fly control (USDA- NAHMS 2010). This increased to over 75% in facilities with >50 heads. Most cow-calf producers base their management decisions on forage availability. In times of limited forage, large round hay bales are often fed to animals in pastures or in pens. This concentrated feeding of forages can lead to major stable fly developmental sites because of the mixture of hay, urine, feces, and rainwater that result (Broce et al. 2005, Talley et al. 2009).

Stocker

Stockers are considered an extensive production system due to their reliance on pasture/range forage systems. The stocker industry produces commercial feeder cattle for feedlots using a variety of postweaning growing programs (Peel 2003). Stocker cattle inventory includes weaned animals from 300 to 600 lbs and yearlings from the previous year’s calf crop for an estimated 15.6 million heads (Peel 2003, USDA-NASS 2020a). This represents 17% of all cattle and calves within the United States with most stocker operators located in Colorado, Iowa, Kansas, Nebraska, Oklahoma, and Texas (Peel 2003).

The beef stocker sector uses forage-based diets for weight gains on weaned calves that graze on pastures and rangelands. Grazing occurs from 75 to 300 d for more than 60% of the total calf population coming from cow-calf herds (Drouillard 2018). Stocker operators seek to limit the stress that can reduce weight gain efficiency, including stress caused by fly pests such as horn flies and stable flies (Talley and Machtinger 2020). Most of these operations are considered extensive systems, though stockers may also be held under intensive management on drylots or when animal stocking rates are increased to improve profitability (Owensby et al., 1988). Stocker operators growing calves in background systems experience fly pests like those in beef feedlot systems but can also experience horn fly infestations if the drylot is proximal to pastured cattle.

Sheep

There are 5.23 million sheep in the United States (USDA- NAHMS 2014). Top states for sheep production are Texas, California, and Colorado, which make up nearly one-third of total production. Commercial sheep production in the United States primarily consists of range operations for large flocks and improved pasture or feedlots for smaller flocks. Sheep are primarily raised for lamb meat and wool for textiles, but newer markets include dairy products, exhibition, or hobby. The industry has declined significantly since the 1940s and wool production has declined more rapidly than lamb production (USDA- NAHMS 2014). In many areas of the country, this downward trend has leveled off or reversed in part with the increased popularity of hair sheep breeds which are easier to maintain than wool breeds. The emergence of new markets for sheep and an expanded consumer base may lead to an increase in sheep production which will require new technologies and products.

Sheep feces are round and dry and are generally not suitable for fly development unless concentrated (high animal density) and moistened by urine or water. This is a very important consideration when sheep are being raised for dairy production. Nearly one-third of sheep facilities report treating mastitis in sheep (USDA- NAHMS 2013a), and the pathogen that causes this condition can be transmitted by biting flies (Bramley et al. 1985). Nearly one-third of all sheep operations and nearly 50% of large operations with over 500 animals report using fly control (USDA- NAHMS 2013a).

Goat

Much like sheep, goats are raised for meat, dairy, and fiber products. On a small scale, goats are used for brush control, exhibition, and as pets (USDA-APHIS 2011). Goat numbers are about half those of sheep in the United States with 2.66 million heads, but goat production in the United States increased 19% from 2012 to 2017 (USDA-NASS 2020b). There are 2.09 million meat goats in the United States (USDA-NASS 2020b). Goats are efficient biological converters because of their unique eating habits and resistance to many environmental stressors. Thus, goat production has been cited as an alternative to cattle in areas degraded by climate change (Silanikove and Koluman 2015).

Nearly 43% of goat operations focus on meat production. Texas dominates the national meat goat market with nearly one-third of all meat goats, or >7 times as many meat goats as Tennessee, the next top producing state (USDA-NASS 2020b). From 2002 to 2007 the number of meat goats sold increased 29% (USDA 2010). Larger meat goat operations primarily raise animals on fenced range or pastures.

Milk goats make up a smaller segment of the industry with 440,000 heads (USDA NASS 2020b), but the industry saw a > 50% increase in animal numbers from 1997 to 2002, and another 30% increase was reported from 2012 to 2017 (USDA-NASS 2019). In 2018, there were over 35,000 farms with dairy goats, a 20% increase from 2007 (USDA-NASS 2019). Wisconsin and California are the top producers of dairy goats. Increases in the dairy goat industry are likely the result of an increasing interest in artisan cheeses and shifting demographics including immigrants with a culture including strong goat traditions (Lu and Miller 2019). About 20% of dairy goat producers keep animals on drylots, possibly to facilitate milking (USDA-NAHMS 2011a). As with sheep, mastitis is of concern in dairy goat production. Over 20% of goat producers reported mastitis or udder inflammation within the last 12 mo (USDA-NAHMS 2011a). While filth flies may be associated with mastitis in goats this has not yet been demonstrated.

Intensive Animal Production Systems

Dairy

The dairy industry is the second highest-grossing animal production industry in the United States with $42 billion in cash receipts (USDA-ERS 2020) and $628 billion in overall economic impact (O’Keefe 2018). In the past 40 yr, the consumption of milk has increased >50% worldwide, and the United States is a top milk exporter with $6.7 billion in dairy products exported worldwide (O’Keefe 2018). United States dairy farms are growing larger and more mechanized, and cow nutrition is managed more closely to maximize milk production per animal. Organic dairy production is also increasing in the United States and has been one of the fastest-growing segments of organic agriculture (Green and Kremen 2003; McBride and Greene 2007, 2009).

In intensive dairy systems, filth flies commonly develop in disturbed cattle feces, calf feces mixed with bedding, fermenting animal feed (haylage and silage), and feed waste, all of which are plentiful whether cows are housed outdoors in drylots or indoors in covered housing systems such as tie stall or free stall barns (Meyer and Peterson 1983). In indoor housing systems, bedding materials are often provided (such as straw, wood shavings, or even composted dry manure) to increase animal comfort and reduce lameness (van Gastelen et al. 2011). Over time, the mixture of bedding, feces, and urine can be a significant source of flies. Calf housing in intensive settings, such as calf hutches and co-housed in small pens, is of particular concern for fly production due to the unique bedding, feeding, and multi-week feces accumulations.

House flies and stable flies are typically the most abundant pest fly species in intensive dairy production facilities (Meyer and Peterson 1983, Williams 2009). Horn flies and face flies are rarely a problem in intensive dairy production since cattle density results in disturbance to fresh fecal pats thereby disrupting development of these flies. Filth flies can result in production and health consequences to dairy cattle with nearly one-quarter of United States dairy farms reporting on-site clinical mastitis (USDA- NAHMS 2018) which can be transmitted by biting flies (Bramley et al. 1985).

Beef Cattle

Beef cattle production is the most important national agricultural enterprise in the United States, accounting for 18% of the total cash receipts from all agricultural commodities in 2018 (USDA-ERS 2019). Beef cattle in the United States is unusual in being separated from the dairy industry as many other countries use dual-purpose cattle for milk and meat production. There were approximately 103 million beef cattle in the United States as of July 2019, with 14% of those housed in feedlots (USDA-ERS 2019).

A beef feedlot is the final stage of meat cattle production. Here, cattle are intensively managed in outdoor confined area with high animal density. Most large beef feedlots are located in the Great Plains region with Colorado, Nebraska, Kansas, and Texas accounting for up to 74% of these cattle. The feedlot industry is shifting toward fewer operations with increasing animal number and density. Feedlots with >32,000 cattle comprised 40% of fed cattle in 2019 (USDA-ERS 2020). Although more numerous, feedlot operations with fewer than 1,000 cattle account for only a small market share in comparison to the large feedlots (USDA-ERS 2019).

With high numbers of animals in intensive confinement, cattle feedlots are at risk for pest outbreaks. A combination of fly management methods is used in feedlots. Most feedlots (96.4%) use feces removal as part of a fly control program (USDA-NAHMS 2011b). Over half of feedlots use insecticide sprays or fly baits. Biological control was reported to be used in over 30% of feedlots and was more common in facilities with > 8,000 cattle. Nearly a quarter of feedlots used pour-ons or sprays, however application of these materials is a challenge with large animal numbers.

Swine

Globally, the United States is the third-largest producer of pork (Giamalva 2014). The value of swine production has increased over 60% to over $27.1 billion in 2020 from 12.8 billion in 2009 (USDA-ERS 2020). As of July 2020, there were an estimated 79.6 million hogs in the United States, a 5% increase from 2019 (USDA-NASS 2020c). Over the past few decades, swine production has trended toward reductions in farm numbers and increased concentration of animals (USDA- NAHMS 2013b). This has been associated with technological change in hog husbandry and management and evolving economic relationships with foreign ownership within the industry. Since 1990, the number of farms with swine decreased by over 70%. Though swine are produced in all 50 states, 87% of the animal inventory is in Iowa, North Carolina, and Minnesota, accounting for 55% of the total value of sales in the country (USDA- NAHMS 2013b).

Most commercial swine are produced in specialized confinement facilities. The structure of these facilities allows for year-round production by protecting animals from major seasonal or weather changes, increasing biosecurity, and decreasing predation risk. There are three major production systems in the swine industry: farrow-to-finish, feeder pig, and feeder-pig finishing. Farrow-to-finish operations are the most common and most intensive production system, covering the entire process from breeding to sale of market hogs. Feeder-pig facilities produce young pigs that are then sold to finishing operations to feed until they reach market weight.

Waste management on swine facilities is a challenge and several systems have been developed for handling swine waste. Hogs commonly are housed on slatted floors where waste drops through the slats into an under-building pit. Shallow pits are frequently washed into a lagoon or holding tank. Deeper pits may accumulate and store waste and then are pumped onto cropland. The most common methods of feces storage in swine facilities are pit-holding followed by flush under slats with 59% and 26.3% of facilities, respectively (USDA-NAHMS 2015). Other methods of feces management reported to the USDA were mechanical cleaning, hand cleaning, flush gutter system, and no management; however, only facilities with >100 swine were surveyed, and large-scale feces management may not be necessary for smaller facilities. When managed well, the wet feces in swine facilities does not promote development of the primary filth fly pests of livestock; however, house flies and black dump flies (Hydrotaea aenescens [Wiedemann]) have been reported in confined swine facilities (Machtinger and Burgess 2020).

Poultry

Poultry production includes chickens or related birds raised for meat or eggs. The United States is a world leader in the production of poultry meat and second only to China in the production of eggs (Conway 2016a,b). In the United States, meat and egg-laying poultry are typically managed in intensive production systems, with birds housed in covered barns (egg-layers) or in environmentally controlled housing (meat birds, breeder birds, and some egg-layers). However, organic poultry production is increasing in the United States (Green and Kremen 2003), as is the prevalence of ‘backyard poultry’ (Elkhoraibi et al. 2014). These are generally extensive production systems.

In intensive poultry production, filth flies develop in feces that accumulates undisturbed within the poultry house. The house fly, and Fannia flies (including the lesser house fly and the coastal fly (Fannia femoralis [Stein])) are the most common fly pests (Axtell 1986). The design of poultry housing depends upon the purpose for the birds (meat, eggs, breeding). Poultry may be raised in barns or houses containing suspended wire cages (egg-layers), cage-free housing including aviaries (egg-layers), laying houses with elevated nesting boxes (breeders), or open floor houses (broiler or meat birds). Egg-layer chickens are often held in rows of suspended wire cages with feces accumulating on the ground or in a pit below the rows of cages. Depending upon the facility design and management practices, bird feces can be scraped and removed frequently or remain in place for weeks, months, or even a year or more in some deep-pit manure storage designs. At cleanout, feces are typically moved outside the poultry house where it is stacked and stored in a covered location, immediately spread on fields, and/or composted for eventual removal.

Aviaries are open housing systems where birds can move freely between an open floor area and nesting boxes arranged in vertical tiers. In aviary systems, bird feces fall below the nesting box onto manure belts that transport the feces outside the poultry house. Laying houses typically have nesting boxes placed on top of raised slats that cover one-third to one-half of the floor space of the house with the remainder of the floor covered in a layer of wood shavings or straw. In laying houses, bird feces fall through the raised slats to accumulate in the area beneath that is difficult to impossible to clean until the flock is removed. Lastly, in open floor houses common in turkey, game, and broiler (meat) birds the entire floor is covered with litter of wood shavings or straw, there are no cages or nesting boxes, and birds can move freely throughout the house. Housing designs with suspended wire cages or raised slats that allow feces to accumulate undisturbed beneath the birds can produce substantial numbers of pest flies if feces do not dry rapidly.

Mixed Management and Animal Production

Equine

Before the automobile, transportation and agriculture were intimately dependent upon equines, including horses, donkeys, and mules. In modern times, the equine industry has a unique position in the United States economy. Though not truly production animals like dairy cattle or poultry, horses and other equids maintain some elements of the original agricultural market. For example, horses usually in rural areas and require pasture and housing. Waste production requires management, and horses are fed forage and concentrated feeds. Currently, entertainment in the form of racing and competition is the primary way the industry contributes to the United States economy (AHC 2017). Equids also contribute to the economy by their consumption of feed, use of pasture, the need for riding instructors and equipment, and use of veterinary services. The equine industry is one of the largest industries that is, to some degree, hidden in plain sight with many having a limited understanding of the industry’s global scale and significance.

In the 1920s, the population of equids in the United States was at an all-time high of over 25 million (USDA-NAHMS 2016). That number decreased to just 3 million by the 1960s but increased again to 7.3 million by 2017 in all 50 states, with California, Texas, and Florida leading in total numbers (AHC 2017). Equine facilities range from housing one horse to hundreds of horses, although small farms (those with 9 or less equids per facility) account for over 60% of all operations (USDA-NAHMS 2016). As of 2017, 17.3% of United States households either own a horse or participate in equine activities. Equine owners are economically diverse, and equestrians of all ages keep horses for leisure, show, racing, farm work, and other reasons. The industry supports nearly 1 million jobs and adds $50 billion to the United States economy. Live-animal export of equids represents over half of all live-animal exports in the United States with a value of over $362 million (USDA-NAHMS 2016).

Fly pests can be a major nuisance to equids during warmer months, with house flies, and stable flies being the most common. Horn flies and face flies may also occasionally be found on horses, but since these fly species require fresh cattle feces for development their presence at horse facilities is indicative of nearby cattle. More than 88% of equine facilities use at least one form of insect control (USDA-NAHMS 2017), with 76% of facilities using repellents. Fly sheets or masks, sticky tape or insect traps, parasitoids, feed-through control, and residual applications of insecticides are also used for fly management. Equine facilities most frequently spread feces on fields (77.9%), but 35.4% of facilities reported leaving feces to decompose (i.e., feces pits or piles) making a suitable substrate for immature fly development (USDA-NAHMS 2016). Most equids are considered large companion animals with individual values generally much higher than traditional livestock, thus the human tolerance for flies and ectoparasites is generally considered to be lower (Machtinger et al. 2013).

Backyard Chicken Flocks

Backyard or hobby chicken flocks are becoming increasingly popular in the United States, especially in urban and suburban areas. These flocks can vary widely in size, density, housing, and even purpose (Pollock et al. 2012, Beam et al. 2013) though most are likely kept for egg or meat consumption and/or as pets (Elkhoraibi et al. 2014).

Flies are not normally a key pest in backyard poultry because flock densities are typically low and feces accumulation is limited. Also, birds are rarely kept in cages which allows them to scratch and forage in their feces to find and consume developing immature flies. There are, however, major biosecurity concerns with backyard chicken flocks. Multiple outbreaks of virulent Newcastle disease over the last two decades in California were thought to have originated in backyard poultry flocks before moving to commercial poultry facilities (Crespo et al. 1999, Garber et al. 2007, CDFA 2020). Filth flies carrying Newcastle disease virus have been collected from backyard poultry (Chakrabarti et al. 2009) and there is concern that these flies could move pathogens among backyard flocks or even to nearby commercial poultry facilities. Zoonotic pathogens, including Salmonella, also are of major concern in backyard chickens (Kauber et al. 2017, CDC 2020).

Organic Livestock Production

Although the term “organic” can have many meanings or connotations in everyday language, the USDA has a specific set of guidelines that must be followed to certify organic production, though this is not indicative of product quality. Governed by the National Organic Program (NOP), the USDA defines organic agriculture as “the application of a set of cultural, biological, and mechanical practices that support the cycling of on-farm resources, promote ecological balance, and conserves biodiversity” (USDA 2015). Organic livestock practices require animals to be housed in living areas that allow for the good health and the display of natural behaviors. All organic livestock practices require animal access to the outdoors and anything beyond temporary confinement is prohibited (e.g., cages are allowed for transport). Ruminants are specifically required to have access to pasture during the grazing season.

Many small dairy farms have switched to organic production to improve profitability and competitiveness against larger and more intensively managed dairy farms (McBride and Greene 2007), however, the transition to organic production is often driven by a few large producer cooperatives that process most of the organic milk (Greene and Kremen 2003). Organic production is necessarily an extensive production system as cows must be allowed access to pasture for grazing (Greene and Kremen 2003) and grazing is required for all animals over six months of age (McBride and Greene 2007).

The “PAMS” strategy (prevention, avoidance, monitoring, and suppression) is encouraged for the management of pests in organic livestock systems (USDA 2015). To be proactive, prevention, avoidance, and monitoring must rely on understanding arthropod pest threats. Suppression should first include mechanical and physical control tactics, with pesticides used only as a last resort. Few pesticides are approved for use in organic livestock. These typically include naturally occurring microorganisms and plant-derived compounds, although some synthetic compounds may also be used (USDA 2015). The National List of Allowed and Prohibited Substances (https://www.ams.usda.gov/rules-regulations/organic/national-list) lists the synthetic and non-synthetic substances that may be used in organic production.

Filth Fly Control in Animal Production

An IPM approach is recommended to control filth flies in animal production (Campbell and McNeal 1979, Axtell 1970, Greene and Guo 1997, Urech et al. 2011). To guide control measures, an established action threshold serves as an indicator that immediate, reactive control of the pest is warranted because sustained pest activity above this level will result in a financial cost to the producer (Stern et al. 1959). A quantitative model of economic loss resulting from stable fly activity on beef cattle has been published (Taylor et al. 2012). Where economic loss can be modeled, an action threshold is often determined to provide guidance for pest management. Unfortunately, determining economic impacts of filth flies, and non-biting flies in particular, is a challenge. For non-biting flies, a treatment threshold derived to avoid fly nuisance due to flies dispersing from an animal facility is perhaps more appropriate than a traditional economic-based action threshold (Axtell 1981). However, the development of a nuisance threshold is complex because local variation in fly tolerance and characteristics of the local geography and land use near the animal facility must be accounted for (Gerry 2020). Once control is deemed necessary, IPM tactics to maintain fly abundance or fly activity below a suitable action threshold. include cultural, mechanical, biological, and chemical control options and have been described for the major filth fly species (Brewer et al. 2021, Geden et al. 2021, Murillo et al. 2021, Rochon et al. 2021, Trout Fryxell et al. 2021).

Future Filth Fly Management and Education Focus

Increased Training in Veterinary Entomology

One of the biggest challenges facing continued management of filth flies is the loss of trained veterinary entomologists in North America that can address filth fly management. Since the 1980s, approximately half the veterinary entomology faculty positions at United States research universities have been lost (Mullens et al. 2018). This loss limits the ability of remaining veterinary entomologists to address the impacts of animal pests, particularly as these relate to changes in climate, land-use patterns, global travel, animal husbandry, and animal production. There is a critical need to increase the number of veterinary entomologists trained in applied animal agriculture who have the training and knowledge to develop and conduct research that will identify improved methods to manage insects pests associated with animal production as agricultural practices change or pest outbreaks occur.

Economic Impact Assessments

Filth fly activity may result in significant financial loss to animal producers. While losses due to the activity of filth flies has been estimated for some animal commodities (Table 2), most animal commodities lack detailed loss estimates related to the activity of these flies (Smith et al. 2021).

Assessing economic value to the damage associated with filth flies is a challenge, and unfortunately it can be difficult to support the need for additional research without a quantifiable understanding of the cost or burden to a producer. There is a need for comprehensive economic analyses for each filth fly species impacting each animal industry, with analysis including losses (up-to-date efficiency measures) and expenses (control costs, labor, nuisance litigation). Costs attributed to the activity of biting flies can be difficult to define, and more studies are needed to identify the “point of diminishing return” for animal producers to establish better relationships between animal performance measurements and fly abundance or fly activity. Associations with pathogens or nuisance must be further evaluated for development of appropriate action thresholds. Also, action thresholds that consider some of the indirect impacts such as modified animal behavior due to the flies’ presence must be established.

Novel Filth Fly IPM Tools and Techniques

Insecticides have been the standard method for immediate pest fly control. However, insecticide resistance has been documented in many of the major filth fly species including house flies (Scott et al. 2013), horn flies (Oyarzun et al. 2011, Holderman et al. 2018), and stable flies (Cilek and Green 1994). A better understanding of the physiological mechanisms associated with resistance and adaptive chemical control methods are required to manage and prevent insecticide resistance. Furthermore, behavioral resistance to insecticides may be more common than is currently appreciated and should be further examined (e.g., Hubbard and Gerry 2020).

New cultural, mechanical, and biological control technologies for managing pest fly populations also are needed to reduce insecticide reliance. Trapping technologies that utilize fly behavior to attract and capture flies, development of repellents for use in push–pull trapping systems, methods to limit movement and dispersal of adult flies, and manipulation of immature development sites through alteration of pH, temperature, or microbial community are all potential areas for new filth fly management research efforts. In addition, while nearly all animal facilities experience fly pressure, information on impacts of filth flies by species, control options available, impact of management or production choices, and ecology of pest flies is extremely limited for some animal commodity types such as equids, goats, and sheep.

Roles of Filth Flies as Vectors of Animal and Human Disease

The role of filth flies associated with livestock operations is becoming increasingly important as we recognize their role in animal and public health as part of the “One Health” concept (Destoumieux-Garzón et al. 2018). Additional research on the association of filth flies with pathogenic microbes or parasites is needed across animal production sectors and housing types, particularly within the context of the One Health framework. The role of flies in the spread of antibiotic-resistant pathogens (Zurek and Ghosh 2014) or in the horizontal transfer of antibiotic resistance genes among bacteria (Akhtar et al. 2009) must be further evaluated. Moreover, improved methods are needed for limiting the movement or spread of pathogens or parasites by filth flies to develop improved biosecurity programs at animal facilities (Gerry and Murillo 2018).

Assessment of Novel Management Tools and Techniques Through Applied Research

As new pest management technologies become available to livestock producers, there will be a need for entomologists to assist in the evaluation of these tools at the basic and applied levels. A challenge will be the development of area-wide efforts for filth fly management, at least within livestock sectors, rather than farm-by-farm fly control. This pathway has already proven effective with the success of the primary screwworm fly eradication program (Davis and Hoelscher 1985). Newer genetic techniques are currently being applied for pest population control, such as those that utilize gene editing or gene drive (i.e., “the CRISPR revolution” (Barrangou 2014, Baltzegar et al. 2018)), but these methods have not yet been developed or tested for filth fly control. Filth fly associations with microbial communities and resulting immune functions should be explored for novel control tools. A continued exploration of basic ecology and population dynamics is also necessary to improve not only targeted control methods but also to provide valuable information that can be used in population monitoring. The increasing diversity and complex management across livestock sectors will also require adaptive pest management strategies.

Extension and Outreach Activities

As early as the 1920s, producer education was recognized as a critical step for fly control. The livestock producer education program included videos to teach producers how to identify and treat the primary screwworm to reduce the harm of this pest (USDA, APHIS 2020). Similar research-based education and Extension is employed today to assist producers with minimizing the impacts of pest flies on animal agriculture. Often this information is available through University Extension services in each state. Unfortunately, Extension systems within the United States have declined in funding (federal and state) and number of full-time employees allocated to livestock Extension programs (Wang 2014). This has resulted in a gap of subject matter experts on fly control for all livestock commodities. Thus, there is a critical need for focused regional and national coordination of veterinary entomologists to develop and disseminate educational materials across all commodity groups to facilitate area-wide IPM practices for filth fly control.

Nuisance Assessments

Nuisance lawsuits may make livestock production unsustainable in some areas. This can be a significant economic crisis for rural areas that rely on jobs associated with production. However, there are challenges with understanding nuisance litigation risk relative to pest fly complaints. Cases often settle out of court, making assessment of potential financial risk to animal producers difficult or impossible. In addition, often “flies” are included in these cases, but the species, numbers, or other identifying characteristics are not specified. Along with flies, legal cases will list many concerns associated with CAFOs such as odor, noise, dust, declining property values, and social stigma. These other concerns are commonly included in litigation making it difficult to determine the portion of a settlement attributable to flies. Assessments of fly complaints should be made to identify nuisance fly complaints and quantify thresholds for fly numbers as a baseline for normal production.

Increased Biosecurity Measures Focused on Filth Flies

Because filth flies may carry animal and human pathogens, effective biosecurity programs on animal facilities should include fly management protocols to limit transport of pathogens by pest flies to off-site locations (Gerry and Murillo 2018). Biosecurity includes all preventative measures employed by an animal facility to limit the spread of pathogens among animals and to limit the spread of pests to/from another location. Regulated biosecurity measures are already in place in the poultry industry. To reduce the risk of food-borne illness spread by flies, the Food and Drug Administration has mandated fly monitoring and control in poultry facilities as part of the “egg rule” (FDA 2011) for flocks with over 3,000 birds, although this does not have a regulatory counterpart in other animal production systems. Food production demands are expected to increase, thus the development, implementation, and adoption of effective biosecurity measures focused on filth flies for all animal production systems is needed.

Acknowledgments

We would like to thank the members of the S-1076: Multistate research project Fly Management in Animal Agriculture Systems and Impacts on Animal Health and Food Safety for their support and review of this manuscript. This multi-state Extension work is/was supported by the USDA National Institute of Food and Agriculture Extension Smith Lever funding under Project #PEN04540 and Accession #1000356 and by the various Multistate Hatch projects from collaborators.

References Cited