Face Fly (Diptera: Muscidae)—Biology, Pest Status, Current Management Prospects, and Research Needs

Native to Europe and Central Asia, face flies ( Musca autumnalis De Geer, Diptera: Muscidae) were unintentionally introduced into North America and became pests of pastured beef cattle, dairy cattle, and horses. Female and male flies use their sponging proboscis with prestomal teeth to feed around moist, mucus membranes of an animal’s face and other body parts. While feeding, face flies agitate livestock and elicit defensive behaviors (e.g., ear flapping, head shaking and batting, hiding in deep shade, and adjustment of grazing), and they can transmit eye-inhabiting nematodes and pathogenic bacteria that cause pinkeye. Face flies can be partially controlled with feed-through insecticides that prevent development of face fly maggots in fresh cattle dung pats. Adults can be partially controlled with repellents and insecticides applied directly to animals. Trap-out tactics can be effective and may involve sticky traps placed around high animal traffic areas, such as waterers and feeders in pastures, dairy entryways, or wherever else livestock congregate in pastures. A review of the insect biology and life stages, physical and economic damages, surveillance strategies, and management options for the face fly is presented.

. Face fly females (6-10 mm) have a dull gray thorax with four thoracic stripes (Williams 2009) and sponging mouthparts used to ingest fluids. The female (left) has a wider vertex between compound eyes, and darkly checkered abdomen that is gray-black, except for the first abdominal tergite which has yellow patches at its lateroventral margins. The male (right) has a shiny black thorax, a narrower vertex, and a bright golden abdomen starting at the second segment with one black stripe down the middle. Both sexes have a sharply curved M1 wing vein (arrows), characteristic of Musca spp., and distinctive tufts of setae on alary sclerites ventral to wing bases and tiny setae ('hairs') between the 1st thoracic spiracle and the head (Loomis et al. 1971). Photo credit: Matt Bertone.  sub-zero temperatures for a few hours as opposed to a few minutes in non-diapausing flies (Rosales et al. 1994).

Geographic Distribution
Face flies are native to Europe and Central Asia but were discovered in the 1950's in Nova Scotia and New Jersey (Vockeroth 1953). It is reported the North American population was discovered in Nova Scotia and likely originated from western Europe (Bryant et al. 1981, Krafsur and Black 1992, Cummings et al. 2005. Since its discovery, populations established and spread west across North America (Krafsur and Moon 1997), and are now a concern to cattle and horse owners from New England through the Pacific Northwest, and to a southern limit at approximately 35°N (Fig. 5). Current explanations for the lack of face flies in the southern United States (e.g., Florida, Texas, southern California) include host distribution and climate, but neither explanation truly explains this phenomenon (Krafsur and Moon 1997).

Effects on Host Animals
Face flies cause direct and indirect damage as well as peripheral effects to host cattle and horses (Williams 2009). Direct damage results from contact between a pest and its host and includes direct injury to skin and other host tissues through bites, allergies or myiasis, as well

Humans
Species author(s) and lettered journal references are listed in superscript above the species or common name.
as behavioral and physiological responses to irritation (e.g., reduced fertility, growth, and lactation). Indirect damage results from diseases caused by fly-transmitted pathogens, such as bacteria and nematodes that cause eye injury and disfigurement. Lastly, peripheral effects result from increased pest management expenses that ultimately increase production costs, negatively affect non-target organisms, or result in policy changes and quarantines imposed by regulatory agencies. Face flies cannot pierce skin, so they cannot feed on blood directly; however, their mouthparts have prestomal teeth that can rasp, scrape, and penetrate the conjunctivae of host eye tissues triggering tear production (Broce and Elzinga 1984). Both sexes have sponging mouthparts that imbibe plant nectar and fluids from eyes, faces, and other body orifices. One to five face flies per eye per day can cause serious ocular lesions that mimic the symptoms of bovine pinkeye Adkins 1972, Shugart et al. 1979). Such mechanical damage, whether sustained by face fly mouthparts, dust, weed, pollen, or excessive sunlight, predisposes the eye for infection, and increases epithelial discharges (Shugart et al. 1979, Arends et al. 1982. Fly feeding also prompts animals in pasture and rangeland to exhibit a variety of defensive behaviors, including head throws, tail flicks, and bunching together with their heads inwards to avoid attacking flies Valla 1982, Woolley et al. 2018).

Bacterial Transmission
The face fly mouthparts are particularly suited for sucking up fluids. The labellum is composed of a pair of labellar lobes covered with pseudotrachea (striations) to channel liquids into the oral opening surrounded by prestomal teeth (Broce and Elzinga 1984). Surfaces of fly mouthparts, bodies, legs, and tarsi (or 'feet') can be contaminated with bacteria that remain viable for hours, and once ingested, up to 3 d in the fly alimentary tract (Glass et al. 1982;Gerhardt 1983, 1984). While the fly is capable of harboring bacteria, evidence suggests that the primary means of transmission is mechanical.
Infectious bovine keratoconjunctivitis (IBK), also known as pinkeye, is a common but preventable eye disease of cattle caused primarily by Moraxella bovis (Hauduroy), M. bovoculi, and M. ovis (Lindqvist) (Broce and Elzinga 1984, Hall 1984, O'Connor et al. 2012, Loy and Brodersen 2014, Angelos 2015. Clinical signs of IBK are excessive lacrimation, inflammation of the eye, conjunctival edema, corneal opacity, and ulceration (Postma et al. 2008, Alexander 2010, Angelos 2015. Animals with IBK may exhibit weight loss, impaired vision, eye disfigurement, and blindness. These gram-negative bacteria enter the eye using pilin proteins to attach to the eye and cytotoxins to erode the cornea. Commercial and autogenous IBK vaccines are promoted for disease prevention (Angelos et al. 2007(Angelos et al. , 2010. Some of these vaccines target the pilin protein attachment to the eye but are unable to effectively protect cattle from disease (Cullen et al. 2017, O'Connor et al. 2019. Both M. bovis and M. bovoculi have been isolated from bovine eyes in the absence of IBK symptoms, suggesting there are gaps in our understanding of these bacteria in the epidemiology of IBK. Face flies transmit M. bovis by regurgitating droplets from the foregut and midgut, by externally contaminated mouthparts, legs, and tarsi (Steve and Lilly 1965, Berkebile et al. 1981, Glass et al. 1982, Glass and Gerhardt 1984. Although the face fly can spread M. bovis from animal to animal, the relatively short residency of the bacteria, as well as absence of the causative agent in the hemolymph, indicate that this species does not propagate in the fly (Glass et al. 1982). The pathogen does not overwinter in the fly, and the herd is the likely source of contamination (Steve andLilly 1965, Alexander 2010). The prevalence of M. bovis in flies was shown to be 1-9% when detected with culturing techniques (Berkebile et al. 1981, Gerhardt et al. 1981), but it is likely greater with more sensitive and specific molecular methods currently available (Nayduch et al. 2019).
Economic losses associated with IBK include weight loss, culling infected animals, fly control, pinkeye treatment, labor costs, and reduced cattle prices for unthrifty animals (Sinclair et al. 1986). IBKassociated losses are estimated to exceed $150 million in beef and dairy systems and are prevalent in young cattle (Hansen 2001). Purebred Hereford and Angus X Hereford crossbred cattle, which have mostly white faces, are more susceptible to IBK than Brahman, Boran, and Tuli crossbreeds (Snowder et al. 2005). Calves lose between 5 and 8 kg (2.2-17.6 lbs) and 16-29.5 kg (35.3-65 lbs) in singular and double-eye infections, respectively (Hall 1984), although single-eye infections are threefold more frequent (Slatter et al. 1982a). These losses become significant, considering that 8-50% of farmers report having annual infections of herds (Cheng 1967, Harris et al. 1980, Webber and Selby 1981, Sinclair et al. 1986, Martin et al. 2019. To monitor bovine pinkeye, typical signs include excessive tears, excessive blinking, opaqueness, photophobia, lesions, and squinting or involuntary eye closure (Hall 1984, Brown et al. 1998. Figure 6 illustrates the progression of bovine pinkeye infection. Brucellosis is caused by several strains of gram-negative bacteria in the genus Brucella (Rhizobiales: Brucellaceae) (Seleem et al. 2010). Brucella abortus (Schmidt) Meyer and Shaw is a blood-borne pathogen infecting cattle and humans. In cattle, B. abortus causes fetal abnormality and abortion, and there is no vaccine. Elk and bison serve as reservoirs for B. abortus that can be spread to susceptible cattle. Prevention of brucellosis in cattle is key to limiting or preventing human infections (Corbel 1997). In cattle, B. abortus is shed from the mammary gland and is likely transmitted from cow to calf. When B. abortus was administered in a nutrient broth to face flies, researchers were able to recover the bacterium from flies for 12 h, but not more than 72 h after which the fly's digestive enzymes neutralize the bacterium (Cheville et al. 1989).
Strangles, caused by the bacterium Streptococcus equi (Lactobacillales: Streptococcaceae) (Sand and Jensen), is an infection in the respiratory tract of horses. Mild forms of the disease result in nasal discharge and minor lesions that resolve quickly; whereas, severe cases cause suffocation resulting from the obstruction of the airways (Sweeney et al. 2005). Strangles is a highly communicable disease passed through close physical contact such as horse-to-horse, respiratory droplets, and fomites. The role of face flies as a vector of these bacteria has not been resolved. During a strangles outbreak in California these bacteria were detected with qPCR from face flies collected from that site, but 0.54% of flies were positive (Pusterla et al. 2020). This suggests that face flies can get infected, but is not sufficient to incriminate face flies in transmission of strangles (Pusterla et al. 2020).

Nematode Transmission
Thelazia eyeworms (Spirurida: Thelaziidae)are nematodes that infect the eyes of mammals, including humans, ruminants, equids, felids, and canids (Otranto et al. 2003, Otranto and Traversa 2005, Bradbury et al. 2018. They are cosmopolitan and are found on nearly every continent. Non-biting flies serve as intermediate hosts and vectors. Face flies transmit T. gulosa Railliet and Henry, T. lacrymalis (Gurlt), and T. skrjabini Erschow in North America. A complete list of Thelazia species, their preferred hosts, known vectors, and geographic distributions can be found in Otranto and Traversa (2005) and additional information on Thelazi development in face flies is also available elsewhere (Geden and Stoffolano 1980, 1981. Thelazia L1, L2, and L3 larvae develop in their adult face fly host. The L3 larvae are transmitted to the animal host when an infected fly feeds on a host's eyes. Adult eyeworms occur under eyelids and nictitating membranes and inside conjunctival sacs and lachrymal excretory ducts of the eye. Clinical signs of infection resemble mild cases of pinkeye, including lacrimal secretions, conjunctivitis, corneal opacity, and lesions on the eye and surrounding tissues. Within the United States, the four Thelazia spp. that occur in cattle and horses are exclusively transmitted by the face fly (Krafsur and Church 1985).
Parafilaria bovicola (Spirurida: Filariidae) (Tubangui 1934) is a nematode that causes subcutaneous lesions on the backs and sides of cattle. The lesions ooze blood and serum containing the nematode's L1 microfilaria, which attracts hungry face flies. Once ingested, the nematode develops from L1 to L3 in the face fly hemocoel and fat body (Bech-Nielsen 1982). Face flies and close relatives transmit P. bovicola among cattle in Europe, northern Africa, Middle East, southern Asian, and south Africa, where the nematode is endemic. The nematode has been identified in Europe from Austria, Belgium, the Netherlands, Germany, Italy, Bosnia, and Herzegovina, where isolated occurrences are managed either by euthanasia or ivermectin treatments (Borgsteede et al. 2009, Hamel et al. 2010, Galuppi et al. 2012, Stevanovic et al. 2014).

Virus Transmission
Face flies acquire animal viruses, but they appear to be dead-end hosts, with little or no transmission potential. For example, face flies can carry bovine viral diarrhea virus (BVD) and contaminate surfaces (Gunn 1993), but their role in transmission has yet to be investigated. Similarly, bovine herpesvirus-1 (BHV-1) administered in albumin to starved face flies did not persist beyond 48 h, nor was the BHV-1 virus transmitted to naïve calves (Johnson et al. 1991).

Economic Damage
Peripheral effects associated with face flies on livestock include economic losses, quarantined animals, and reduced animal health and welfare. Annual losses in face fly control costs and lost animal production were estimated to exceed $52 million for U.S. range cattle (Drummond et al. 1967), which would be approximately $423 million in 2020 dollars (https://www.usinflationcalculator.com/). When Parafilaria was introduced in Sweden during the 1980s, losses were estimated at $8 million (= $13 million now) in meat and hide damages (Bech-Nielsen et al. 1983).
Other effects are more difficult to assess. Cattle increased the rate of dry matter intake as the number of face flies increased on animals (Dougherty et al. 1993); however, several studies assessed effects of face fly stress on dairy and beef cattle and failed to find substantial losses (Schmidtmann et al. 1981a(Schmidtmann et al. , 1984Arends et al. 1982;Schmidtmann 1985a;Schmidtmann and Berkebile 1985). While it remains challenging to measure the direct economic impact of face flies on cattle, the prevention of disease, especially pinkeye, is a strong incentive for producers to manage flies. In our experience, cattle producers are more concerned about pinkeye than face flies. While face flies can transmit bacteria that causes pinkeye (see below), the presence of face flies does not imply pathogen transmission, nor does their absence imply no transmission. This is why estimating pinkeye risk based on face fly numbers is problematic. Also, an indirect measure of fly pressure is animal behaviors: tail flicks, head tosses, flank twitches, etc. In recent years, consumer groups have taken a proactive stand on animal welfare, focusing on livestock care, treatment, housing, and comfort (Barkema et al. 2015). The absence of large economic effects suggest an economic threshold for treatment is probably >15 flies per face (Krafsur and Moon 1997); however, expression of defensive behaviors suggests an annoyance threshold may be lower (Schmidtmann et al. 1981b;Schmidtmann and Valla 1982;Schmidtmann 1985a,b;Schmidtmann and Berkebile 1985).

Traditional Management Strategies
Extensive livestock production is an animal management system characterized by large areas of native or improved pastures that provide the sole food source for livestock during the growing season. Compared with intensive systems, extensive systems are generally lower in productivity per animal and per pasture area; but they utilize lower levels of external inputs, capital, and labor. Face flies are most common in extensive livestock product systems such as cow/ calf and stocker animals housed mainly on pasture and rangeland.
Management strategies for face flies include insecticide ear tags, dust bags, oiler/rubs, pour-ons, sprays, feed-throughs, and air-projected capsules. Non-chemical control methods include walk-through traps, sticky traps, and conservation of beneficial insects such as predaceous dung-inhabiting beetles. Commercial and autogenous pinkeye vaccines are available and should be administered before animals are sent to summer pasture.
Organic livestock production systems integrate cultural, biological, and mechanical practices to foster a cycling of resources, promote an ecological balance, and conserve biological diversity. Within the organic system, according to the pasture rule, ruminants must be given daily Downloaded from https://academic.oup.com/jipm/article/12/1/5/6125217 by guest on 10 February 2021 access to pasture and acquire 30% of their annual dry matter intake from pasture (Rinehart and Baier 2011). Consequently, organic and conventional cattle in extensive systems are likely to be more exposed to dung pat breeding face flies and horn flies (Haematobia irritans L.) than are dairy and beef cattle raised in conventional, dry lot-based intensive systems. Prevalence of face flies and the pathogens they transmit within conventional and organic systems has not been evaluated.
Face fly and pinkeye management are likely to be needed during summer in extensive production systems. Conventional producers may use traditional synthetic control products for face fly control (see below). Organic systems have a more restricted list of available essential oils and botanicals such as pyrethrins applied as sprays, oiler/rubs, or as a wipes. Diatomaceous earth may be used in dust bags in force-use or free-choice arrangement, but efficacy against face flies is questionable. If a pasture is rather small, a mechanical option for control of face fly (and horn fly) larvae could be to disrupt the pasture at 1-3 d intervals to break apart the dung pats and stop larval development. Before using any ectoparasite control product on a certified or transitional farm, organic certifiers should be consulted (e.g., FDA National Organic Program).

Monitoring Methods
Few monitoring methods are used to assess face fly populations on cattle or horses. Normally, the producer visually inspects the animal, and if the animal 'has flies', or shows signs of irritation, then flies on those animals are considered problematic. Early on, monitoring face flies typically consisted of visual observations of flies on animals' faces (McGuire andSailer 1962, Hansens andValiela 1967). Researchers would count the number of flies on the faces of 15 animals within a herd (Ode and Matthysee 1967). More recently, photography has been used to document numbers of face flies, and horn flies, too. Animal behaviors can also be used to gauge animal comfort. For example, heifers not treated for face fly control had significantly more bunching episodes and spent more time bunched per day compared with treated herds (Schmidtmann and Valla 1982). The number of episodes and time bunched was also positively correlated with increasing face fly pressure, and bunching was indicative of 9-12 flies per face (Schmidtmann and Valla 1982). Behavioral responses were also reported where face flies (or house flies as the authors did not differentiate) were positively and significantly associated with partial tail flicks and leg stamps in Holstein dairy cows (Woolley et al. 2018). Monitoring fly numbers, animal discomfort, disease presence, financial records, and fly control costs should be key to improving a farm's fly management program.

Traps to Remove Flies From Animal Environment
Sticky traps of different designs were used to measure abundance of face flies for research purposes (Pickens and DeMilo 1977, Kaya and Moon 1978, Peterson and Meyer 1978, Johnson and Campbell 1987. Traps consisted of glossy-white plywood pyramids coated with an adhesive. These captured more face flies than alternative shapes and colors . Numbers captured were greatest on traps closest to cattle, but traps needed to be placed outside of fencing to prevent damage by cattle; however, current technology might allow traps to be placed closer to cattle. Based on presumption that flies disperse among neighboring farms, white tetrahedral sticky traps were evaluated alone and in combination with tetrachlorvinphos (a feed-thru organophosphate insecticide) in a 4-yr area-wide control program in Maryland . Face fly control with pyramids alone was insufficient, even with as many as one trap for every three cattle. A further practical limitation of sticky traps for face fly control is that pastures and rangeland, where face flies occur, can be relatively inaccessible, which makes maintenance to replenish sticky trap surfaces prohibitively expensive. Traps placed at water tanks and salt or grain feeding stations may be more practical, especially for herds managed with rotational grazing. It remains to be seen if placement there could provide a satisfactory level of control.
Walk-thru and vacuum traps provide another alternative to insecticides. An early design for horn fly control required cattle to walk through a darkened, building-like structure where brushes disturbed flies from passing animals. Disturbed flies would then move to lighted trap sides where they were passively captured (Bruce 1938). Bruce traps were successful in reducing numbers of horn flies, but were less effective in trapping other fly species like face flies and stable flies. An alternative trap is a fly vacuum system available commercially (CowVac, Spalding Laboratories). Instead of passive fly collection, disturbed flies are sucked by vacuum into a cage. The FlyVac was developed for controlling horn flies, but also will capture face flies and stable flies (Denning et al. 2014); however, others found that the vacuum system only controlled horn flies and that face and stable fly populations were not reduced (Kienitz et al. 2018). Further, dairy herd productivity and discomfort behaviors did not change when traps were activated.

Cultural Control
Cultural control methods for face fly control are often not practical simply because methods involve too much effort or simultaneously destroy pastures. Confined cattle systems with trampled dung rarely have face fly populations unless they are emigrating from other locations. If dung pats in pasture systems are too watery, larvae will suffocate because tunnels made for airflow will collapse. Drying dung pats or those that dry quickly after being spread will desiccate horn fly larvae (McLintock and Depner 1954); so it can be speculated that face fly larvae will be desiccated as well. Thus, spreading or inundating dung on pastures by dragging or flooding is possible, but again it will likely damage the pasture or it is simply not practical.

Conservation Biological Control
Biological control results from activities of beneficial organisms that kill target pests (Drummond et al. 1988a, Darwish et al. 1990, Fincher 1990, Rutz and Scott 1990. A rich fauna of predators, competitors, parasitoids, and entomopathogenic organisms occur naturally in pasture habitats. Livestock producers can conserve those beneficial organisms by avoiding use of broad-spectrum insecticides and anthelmintics at times when those beneficial organisms are active, which is generally during the growing season. Like cultural control methods, the utility of buying and using these agents for face fly control is not practical for most producers.

Competitors
Dung beetles and dung feeding flies can compete with face fly larvae for fresh dung. Scarab beetles (Scarabaeidae) in different subfamilies can shred, disperse, and bury dung within days of dug pat deposition. In the process, those beetles can damage fly eggs and larvae directly, and reduce dung supply and quality for fly larvae and gastrointestinal parasites (Nichols 2008). Other large dung feeding Muscidae, Anthomyidae, Sarcophagidae, and Scathophagidae may reduce face fly larval success (Valiela 1969, Moon 1980, Fowler and Mullens 2016.

Parasitoids
Species in five families of parasitic Hymenoptera and one family of Coleoptera have been reared from face flies in bovine dung in North American pastures (Blickle 1961, Benson and Wingo 1963, Sanders and Dobson 1966, Thomas and Wingo 1968, Wylie 1973, Wingo et al. 1974, Figg et al. 1983, Moon and Cervenka 1991. Two commonly encountered species are braconid larval-pupal endoparasites; Aphaereta pallipes (Say) is a gregarious species and Alysia species are solitary. The remaining four are solitary pupal parasites, a cynipid, Eucoilia impatiens (Say), a figitid Xyalophora quinquilineata (Say), and two pteromalids, Spalangia nigra Latreille and Muscidifurax raptor Girault and Sanders. Most of these parasitoids are generalists that also attack pupae of dung inhabiting muscid, anthomyiid, and sarcophagid flies. While these wasps are geographically widespread, they cause far lower levels of apparent mortality in the introduced face fly (<10%) than among other dung-breeding flies, which are indigenous to North America (Turner et al. 1968, Hayes andTurner 1971). Interestingly, A. pallipes is notably unable to exit a face fly's calcified puparium, and the other wasp species have difficulty locating face flies that have dispersed from dung pats into the surrounding pasture habitat. In North America, five Aleochara (staphylinid) dung-inhabiting species were reared from exposed face fly puparia (Klimaszewski 1984, Maus et al. 1998, Bezanson and Floate 2019. Aleochara females lay their eggs in and around dung pats, where free-living larvae hatch and then penetrate host fly puparia, including face fly pupae that have pupated away from the natal pats. The beetle first instars develop within the puparia next to the pupae proper. The adults then emerge from the puparia and feed on eggs and larvae of cyclorraphous flies. Aleochara parasitism is typically <5% in face flies because these beetles also parasitize other dung-breeding flies (Thomas and Wingo 1968). In Europe, A. tristis Gravenhorst was tested as a biological control agent against face flies (Jones 1967, Heller 1976). Although A. tristis established, it could not increase face fly mortality (Klimaszewski and Cervenka 1986). While mass-rearing and storage methods were developed for A. bulineata (Gyllenhal) on Delia antique (Meigen) (Whistlecraft et al. 1985), it remains unknown if these methods could be used for A. tristis in an augmentative control program for face flies.

Entomopathogenic Bacteria
Early studies with Bacillus thuringiensis (Bt) using exotoxinproducing Bt strains against filth flies, such as the house fly, offered encouraging results (Burns et al. 1961, Miller et al. 1971, Carlberg 1986, Rupes et al. 1987. Bacillus thuringiensis was evaluated as a feed additive, and it effectively reduced face fly development (Hower and Cheng 1968); however, safety concerns about vertebrate toxicity in the 1980s prohibited the use of exotoxin-containing Bt products in the United States (McClintock et al. 1995). Strains of Bt lacking exotoxins (exotoxin-free strains) were identified (Choi et al. 2000, Labib and Rady 2001, Oh et al. 2004), but these exotoxin-free strains have not been assayed against face fly larvae.

Entomopathogenic Fungi
Beauveria bassiana (Balsamo-Crivelli) Vuillemin and Metarhizium anisopliae (Metschnikoff) Sorokin, were evaluated against house fly larvae and adults and stable fly larvae under laboratory conditions (Hall et al. 1972, Barson et al. 1994, Watson et al. 1995, Angel-Sahagun et al. 2005, Lecuona et al. 2005, Kaufman et al. 2008, Weeks et al. 2017. Steenberg et al. (2001) reviewed the entomopathogens in Denmark and found a low natural presence of B. bassiana and Entomophthora muscae (Cohn) Fresenius in fieldcollected face flies (Steenberg et al. 2001). Additional experimental studies should be conducted to determine entomopathogen efficacy at controlling face flies.

Entomopathogenic Nematodes
Entomopathogenic nematodes have been studied extensively for effects on face flies. Paraiotonchium autumnale (Nickle) (= Heterotylenchus autumnalis) was identified as a natural control option for face flies because it sterilizes females. The potential for H. autumnalis to control face flies was identified (Stoffolano and Nickle 1966, Stoffolano 1970, Thomas et al. 1972, Kaya and Moon 1978, Kaya et al. 1979, Krafsur et al. 1983, Chirico 1990, Soto et al. 2014, but applications at the commercial scale have been limited by inability to mass produce and distribute nematodes into face fly infested pastures and rangeland. The nematode, P. autumnale, is naturally found in 10-20% of face fly adults, with occasional reports of parasitism rates being >50% (Briggs andMilligan 1977, Soto et al. 2014). Once mated, female nematodes burrow from dung fluid into the larval face fly cuticle and then live inside the fly during the rest of the fly's life. In the female face fly, the female nematode produces asexual nematodes that invade the ovaries. The infected fly will then lay nematodes ('nemaposit'), as if ovipositing (Stoffolano 1970, Soto et al. 2014). Further research indicated P. autumnale could not control the entire face fly population (Kaya et al. 1979, Soto et al. 2014. Instead, P. autumnale could stop cyclical protein feedings as infected face flies feed on dung rather than blood or other animal secretions; thereby, preventing or limiting the second gonadotrophic cycle and sterilizing the flies (Kaya and Moon 1978).

Chemical Control
Insecticides applied via ear tags, as sprays, and pour-on and feedthrough products are used to manage face flies. Various modes of action are available for face fly management and control (Hall and Foehse 1980;Herald and Knapp 1980;Pickens and Miller 1980;Williams and Westby 1980;Miller et al. 1981Miller et al. , 1986Miller et al. , 1991Knapp and Herald 1981, 1983, 1984Miller, Hall, et al. 1984;Krafsur 1984;Knapp et al. 1985;Hogsette and Ruff 1986;Scott et al. 1986;Broce and Gonzaga 1987;Skoda et al. 1987;Miller and Miller 1994;Nauen et al. 2019). Compounds with various modes of action are available at the VeterinaryPestX database (https://www. veterinaryentomology.org/vetpestx) (Gerry 2018) and include avermectins/milbemycins (group 6), benzoylureas (group 15), organophosphates (Group 1B), juvenile hormone analogs (Group 7A), and synthetic pyrethoids (Group 3A) ( Table 2). These materials are applied as air-projected capsules, dusts, feed-throughs, injections, insecticidal ear tags, pour-ons, and sprays. For more information about the Insecticide Resistance Action Committee (IRAC) codes, visit www. irac-online.org. Current recommendations involve alternating compounds with different modes of action, i.e., alternating to a compound with a different IRAC code from the one used in the preceding year.
Feed-through insecticides include larvicides and insect growth regulators (IGRs) that animals consume with feed or minerals, and are eventually excreted in manure. Female flies ovipositing in treated manure exposes immatures to a treatment that either kills them or arrests their development. The active ingredients diflubenzuron, tetrachlorvinphos, and methoprene kill face fly larvae Uebel 1974, Pickens andDeMilo 1977), although not all are available in every state. Efficacy for individual herds may be limited by face fly dispersal, as adult flies will move from neighboring herds where feed-through products are not used (Pickens and Miller 1980). Feed-throughs could be valuable if used in area-wide control programs enough to reduce the effects of migration.
Off-target impacts associated with feed-through insecticides include effects on non-target populations (Cook andGerhardt 1977, Fincher 1991). Feed-through formulations are administered to cattle continuously, and efficacy depends on the animal consuming the correct amount of additive daily: too low allows immatures to survive and too high can have non-target effects. Nevertheless, the label instructions should always be followed.
Avermectins/milbemycins (macrocyclic lactones or MLs, group 6) are closely related 16-membered ML derivatives produced through fermentation by soil-dwelling Streptomyces. Common veterinary MLs include abamectin, doramectin, eprinomectin, ivermectin, selamectin, and milbemycin oxime. Avermectins bind at gamma-aminobutryic acid (GABA) receptors in the nervous systems of insects and nematodes, thus blocking electrical transmission between nerves and muscle cells, which leads to hyperpolarization and subsequent paralysis of neuromuscular systems (Bloomquist 1993(Bloomquist , 1996. MLs are not labeled for face fly larval control, but a study using ivermectin excreted from cattle dung (applied via subcutaneous injection or via pour-on to the animal) demonstrated that dung with ML reduced survival of face fly larvae for 14 to 28 d posttreatment (Sommer et al. 1992).
Use of MLs in livestock is a concern from an ecotoxicological standpoint. Persistence of MLs in manure of treated cattle may harm invertebrates that are important for manure pat degradation and nutrient recycling into soil (Floate 2006). Effects vary among MLs, their formulations, and susceptibility of insect species in treated areas (Floate et al. 2005).
Abamectin ear tags were introduced in the early 2000s and provided an alternative to organophosphate and synthetic pyrethroid insecticide ear tags. A combination ear tag combining abamectin, a synthetic pyrethroid, and piperonyl butoxide was introduced in the late 2000s and reduced face fly numbers on tagged cattle by 70% over 6 wk (Boxler, unpublished).
Benzoylureas (group 15) inhibit chitin biosynthesis and have been used against the face fly as feed-throughs (diflubenzuron) (Pickens and DeMilo 1977;Miller et al. 1986Miller et al. , 1991. Organophosphates (OPs) (Group 1B) intoxicate insects and mammals by inactivation of the enzyme acetylcholinesterase (Fukuto 1990). Application options for OP insecticides include dusts, feedthroughs, insecticidal ear tags, oilers/rubs, and sprays. Self-treatment devices such as dust bags and oilers/rubs commonly used by livestock are often positioned near water stations or mineral feeders for use on a 'free-choice' basis. Forced daily use would be better.
Currently, two emulsifiable concentrate OP products, Phosmet and Co-Ral, are labeled for direct animal application, but both carry age application restrictions. Presently, there is one organophosphate, tetrachlorvinphos, used as a feed additive that is typically incorporated into mineral blocks or added to mineral or feed.
Synthetic pyrethroids (Group 3A) are insecticides that delay closing of the voltage-sensitive sodium channel leading to death; in some instances, causing uncontrolled, uninterrupted nerve firing. Synthetic pyrethroid insecticides for face fly control are formulated as dusts, pour-ons, sprays, ear tags, and air-projected capsules. Synthetic pyrethroid insecticides have been used by livestock producers since the early 1980s (EPA 738-F-06-012, June 2006).

Natural Products/ Bio-pesticides
Pyrethrum is probably the most widely used botanical insecticide worldwide. The flowers of chrysanthemum, Tanacetum cinerariifolium Schultz and Bipontinus, are ground into powder and extracted using solvents (Casida and Quistad 1995). Two natural pyrethrum compounds from another plant, Chrysanthemum cinerariifolium (Treviranus), are neurotoxic to insects (Yang et al. 2012). Pyrethrum and pyrethrins are contact insecticides, and their mode of action is a result of neurotoxic action, which block voltage-gated sodium channels in nerve axons, which affects face flies in the exact same method as pyrethroids (Duke et al. 2010). Pyrethrum and pyrethrins were initially applied as synergized animal sprays, but studies reported short-term to no effect on face fly populations because these compounds act as a repellent and face flies spend very little time on their host (Granett and Hansens 1961, Ode and Matthysse 1964, Poindexter and Adkins 1970. Poor results may be due to pyrethrins being very unstable in UV conditions and heat, which limits the areas where they are effective (Casida 1980). Neem (azadirachtin) is derived from a group of plants from the family Meliaceae that grow in India, Africa, Central and South America, China, Vietnam, and Thailand. Neem can have multiple effects in insects, including antifeedancy, growth regulation, fecundity suppression, sterilization, oviposition repellency, and other changes in biological fitness (Mulla and Su 1999). Azadirachtin at low concentrations caused 11 % mortality to third instar face flies, and subsequent adult numbers were reduced by 52% by interfering with pupal formation and adult emergence (Gaaboub and Hayes 1984a,b).
Essential oils are mixtures of volatile extracted plant compounds that include various alcohols, terpenes, and aromatic compounds (Khater 2012). Many essential oils are bioactive against a variety of arthropod pests of crops (Cloyd et al. 2009). Daily applications of lemongrass and geranium essential oils or mixtures to organic dairy cattle were evaluated and researchers observed lower face fly Downloaded from https://academic.oup.com/jipm/article/12/1/5/6125217 by guest on 10 February 2021 densities, reduced cattle defensive behaviors, and increased grazing times compared with untreated animals (Woolley et al. 2018).

Genetic Modifications of Face Flies
Use of genetic technologies (e.g., gene-drive, genetic editing) to manage face fly populations has been considered. Knowing that face fly diapause is a heritable trait that also responds to environmental factors (Kim et al. 1995), it was suggested as a potential genetic mechanism for management (Geden and Hogsette 1994). This is because temperature and day length induce diapause and the rate of fat body hypertrophy is temperature-dependent (Stoffolano and Matthysse 1967, Valder et al. 1969, Caldwell and Wright 1978, Read and Moon 1986, Evans and Krafsur 1990. The use of radiation to control face flies was evaluated by inducing a dominant lethal mutation that killed sperm; however, treatment of males did not affect insemination rates or eclosion, and fecundity and fertility were determined to be inversely proportional to the radiation dose (Mansour and Krafsur 1991). Mansour and Krafsur (1991) did speculate that local eradication could be possible with coordinated releases. Future research should include sequencing and annotating the face fly genome in order to develop, evaluate, and validate additional genetic modes of management as well as the role that epigenetics has in diapause.

Genetic Modifications of Host Animals
Few studies have addressed host tolerance and host resistance to face flies. We define pest tolerance as an animal that is not bothered or effected by the feeding of face flies and may not have flyassociated losses. Conversely, pest resistance is the idea that some hosts are not a preferred host to face flies and rarely have flies on them. Researchers identified darker haired cattle with more face flies compared with white or Holstein cattle (Engroff et al. 1972), but these findings have not been repeated (Teskey 1960, Schmidtmann and Berkebile 1985, Steelman et al. 1993b. Damage caused by face flies, transmission of pinkeye, and microlacerations on eyes, vary by breed. Susceptibility to pinkeye infection was most prevalent in Angus, Herefords, Shorthorns, Jerseys, and Friesians (Steelman et al. 1993a). Additionally, there are reports that tropical cattle breeds (Bos indicus Linnaeus) are more resistant to pinkeye infection than temperate breeds (Bos taurus Linnaeus) (Slatter et al. 1982b, Snowder et al. 2005. Light-skinned animals, such Jerseys, Guernseys, Friesians, and especially Herefords, are more pinkeyeprone (Webber and Selby 1981, Slatter et al. 1982b, Sinclair et al. 1986, Steelman et al. 1993b, Snowder et al. 2005. While there is much debate about whether face flies prefer certain colors over others (Steelman et al. 1993b), it's more likely because light-skinned tissue around the eyes is more sensitive to UV radiation-one of the causes of bovine pinkeye (Slatter et al. 1982a). Previously infected cattle become immune to clinical pinkeye symptoms, but also remain carriers of the same pathogens Selby 1981, Brown et al. 1998). Older, immune cattle are reservoirs to the largest susceptible age group-the calves (Webber and Selby 1981, Slatter et al. 1982a, Sinclair et al. 1986. Calves are developing their bodies at the same time as their immune systems and so are often gravely affected by pinkeye; this explains the heterogeneity of pinkeye on farms as well as why calves are the largest group affected. The Three I's: IPM, Immigration, and Insecticide Resistance Integrated pest management (IPM) is highly recommended for face fly control because IPM uses multiple controls simultaneously to suppress pest populations (Moon 2019); however, using IPM tactics to control face flies is difficult and the problem is threefold. First, the most useful strategy is to eliminate dung (face fly development site), but this is difficult in pastures because of the space and time required to spread, dry, and/or bury dung. Second, while pasture may include a diverse group of biological agents, there are, unfortunately, no effective biocontrol agents of face flies commercially available at this time. Third, face flies spend limited time on their hosts and travel among herds Pickens 1978, Moon 2019). Thus, cattle producers implementing good face fly and pinkeye control could still see significant infections sourced from neighboring herds.
Because of these particular shortcomings, many farmers rely almost exclusively on chemical controls (e.g., ear tags, sprays, feedthroughs) to suppress face fly populations. Repeatedly exposing and killing most, but not all, face flies allows the survivors to develop resistance and pass it to their progeny genetically. In fact, face fly immatures exposed to insecticides intended for other arthropods or adults can develop resistance before they become adults. This problem is exacerbated when considering how else resistance might form. Face flies resistant to a particular insecticide within a class are more likely to develop resistance to insecticides with similar chemical structures in that class in a process known as 'cross resistance' (Axtell 1986). In general, face flies across the United States have shown resistance primarily to older insecticide classes, such as organochlorines (Drummond et al. 1988b). As of this writing, face flies have not been evaluated for insecticide resistance and this may be due to the fly's avoidance behavior spending little time on the host. We suspect that insecticide resistance varies from population to population because individual livestock producers may use different pesticides. Consequently, there is a need to evaluate face for insecticide resistance to different modes of actions.
Producers can slow resistance development by monitoring their fly populations, starting fly control early in the season, using multiple management strategies, managing the use of insecticides with mode of action rotation, and develop a community of producers who are aware of face flies and pinkeye. Face fly abundance on 10% of the animals in a herd should be estimated weekly to identify the most fly-ridden individuals or groups. To understand which control strategies work, producers should record all control efforts and diseases weekly. These records should include recording the approximate fly numbers before, during, and after a fly season, recording any changes in profit margins or animal production, and comparing control-free herds with controlled herds on the same farm. By beginning control efforts in mid-spring, when the first flies begin to start feeding can help to keep the fly population at a low level throughout a grazing season. When beginning face fly management programs, multiple strategies are necessary. This includes adding shelters in pastures to concentrate dung and increase the rate of trampling, herding cattle into screened-in shelters if a pinkeye outbreak occurs to prevent fly immigration and breeding, and quarantining, monitoring, and treating infected animals. Upon discovering pinkeye, producer should immediately begin fly control, antibiotic regiments, quarantine infected cattle, and vaccination of healthy cattle. Use insecticides only in case of disease and fly outbreaks. This generally includes using insecticides only intended for that fly species and life stage, treating the face and surrounding eye regions of cattle with insecticide when used, treating diseased animals with insecticides until they are disease-free, and using multiple modes of action to mitigate development of resistance (see the IRAC or ask your local extension agent). Face flies are strong fliers and can disperse great distances (Sabrosky 1961, Peck et al. 2014); thus, neighboring areas with large face fly populations are usually supplying face flies to areas surrounding them. Therefore, keep in contact with local cattle farmers. This is not only helpful for synchronizing control efforts but can be useful in forewarning against any disease outbreaks.

Future Strategies and Challenges for Sustainable Management
While face flies remain an important pest of pastured animals and a vector of a number of different pathogens that negatively affect animals, the pace of face fly research has declined dramatically from the 1960s to present. A quick Web of Science search comparing face fly research to other filth flies over the past 70 yr highlights the dearth of research on face flies (Fig. 7). This lack of research may be due to a number of factors, including elimination or merging of entomology programs, lack of replacement hires, shift to medical entomology, lack of funding in veterinary entomology, and lack of training opportunities for graduate and professional students (Mullens et al. 2018). We argue that this insect is still important and warrants future research, some strategies and ideas are presented below.
1. Sensors, monitoring, analysis, and reporting technologies (SMART). The current norms of monitoring and managing face flies are as responses to pinkeye or the onset of other pests (e.g., horn flies) or pathogens (e.g., Brucellosis). The current strategies do not emphasize prevention and detection, but instead are responsive to a problem. It is essential that SMART improvements be made to prevent disease onset by improving face fly monitoring and action thresholds that encompass fly populations around the farm and on the animal, as well as responses to animal health, welfare, and economics. As described, SMART technologies are not preventative but a substitute scouting technology leading to a treat/no-treat decision; a response to a problem detected by a SMART device instead of human sampling or observation. SMART technologies can include wearable technologies that detect change in pressures or animal defense responses, visual technology that automates detection of a fly's morphology, or auditory technology that recognizes a fly's wing beat frequency or an animal's distress call. Use of drones around a farm for pest management is coming in agricultural-row-crop entomology; perhaps drones can be used for face fly management as well. Results from the SMART technologies should be incorporated into a dynamic managing platform that helps a producer monitor face fly populations and prevent a problem from occurring. Such a platform can incorporate climatic and economic data to help a producer decide if it is currently economical or sustainable to treat the pest population or if the population is tolerable. 2. Developing sustainable and/or organic face fly management options for producers. Current face fly management strategies are designed to take advantage of their use of fresh dung pats for oviposition. IGRs are fed to cattle and the active ingredient is excreted in dung, resulting in termination of the fly's immature stage of development. Since beef herds can be quite numerous, adult treatment applications are designed to be efficient and a combination of methods are often used (e.g., pour-ons, back rubbers, dust bags, ear tags). However, face fly insecticide resistance, nontarget effects, and use of chemicals on food animals limit the sustainable and environmentally healthy use of chemical control methods. Thus, it is essential that sustainable methods are developed for limiting the damage and economic losses caused by face flies. There is a need for improved trapping for control of face flies because few traps are designed to target this specific species. Face flies are incidentally collected in traps designed for stable and horn flies. Additionally, there is a need not only to develop new modes of action for face fly control, but more importantly to improve delivery mechanisms of the current management strategies that can help reduce the development rate of insecticide resistance. Biological control options show little practical feasibility at present, yet natural enemies become more important as few products are available that can be used in organic systems. Downloaded from https://academic.oup.com/jipm/article/12/1/5/6125217 by guest on 10 February 2021 Genetic methods for face fly control should be evaluated as well as identifying potential mechanisms for host tolerance and resistance to face flies (and their pathogens). Importantly, all methods of management should include the use of sustainable economic thresholds. 3. Systems approach to managing face flies populations. External factors (e.g., environment, climate, human behavior and perception, host genetics, and consumer preferences) alter face fly populations. Organic dairy herds that have significant face fly problems may be at a greater risk of increased incidence of pinkeye if the pathogen is present. Because few management options exist and are often ineffective, consumer preference for organic dairy milk is likely increasing face fly populations. High face fly populations may result in decreased animal health and welfare and milk production, a simultaneous increase in pathogen incidence, increased fly management efforts by the producer, and negative non-target effects. Additionally, these problems are likely heterogeneous over space and time due to the environment and climate. Thus, there is a current need to assess face fly populations in different systems to identify baseline populations. Having these baseline datasets will allow us to identify positive and negative effects associated with face fly population responses to farm changes, land use changes, and/ or changes in producer management practices. As public perception continues to drive economic markets, it is important to understand how producers and consumers perceive face fly populations and what changes each are willing to adopt to reduce populations and manage disease incidence. In the process of managing face flies, it is essential that future research encompass not only effects of management, climate, and perceptions of face flies but also any additional positive or negative effects associated with management practices in different systems. 4. The ongoing need to understand the fundamental biology of face flies. While face flies are not a primary pest in livestock production, their presence contributes to economic losses as well as losses associated with animal health and welfare. It is critical that fundamental research continues to focus on understanding the face fly's biology, ecology, distribution, physiology, genetics, and then learn how each responds to different climates, environments, and management practices. It is essential that the face fly genome is completed and annotated which will allow for further research into comparative genomics (e.g., useful for identifying mechanisms for resistance), population genetics/genomics (e.g., useful for understanding dispersal), and to design and evaluate novel management approaches (e.g., lethal-gene drive). The combination of physiology and genomic studies can lead to understanding the epigenetics of the face fly and how populations respond to nature. Habitat and distribution studies which involve the immature development sites (e.g., microbial community studies) and pasture habitats (e.g., ecological and/or remote sensing studies) can help describe the ecological niche of face flies.