Guidelines for fly control

Public Health Significance of Urban Pests 229 • Refine our knowledge of the infestation rate of natural fly populations in urban areas.

7.10 Conclusions

For dealing with fly infestations, the following items are suggested. 1. Proper sanitation is the key to fly control. Deny flies access to food, shelter and a place to lay their eggs. 2. Do not allow flies to come in contact with contaminated substances and thus conta- minate themselves. 3. Although management of adult flies can provide temporary relief, the location and eli- mination of development sites for immature stages is the best method for long-term control. Although people make the distinction between urban and rural flies, flies do not, so fly management in urban areas may involve surveillance at and management of potential fly-producing sites outside the urban perimeter. 4. Prevent flies from entering buildings, by keeping doors closed and window screens in proper repair. 5. If flies do enter structures, eliminate them with traps or other suitable methods as quic- kly as possible. 6. If people experience fly problems, particularly if such problems are associated with ill- ness, health authorities should be contacted immediately. 7. Health authorities with entomological expertise should have properly trained person- nel to identify flies and assess the extent of fly outbreaks with or without associated pathogenic organisms. Should their assistance be needed, health authorities should have contacts with outside entomologists and medical personnel. 8. There is a need to improve education in entomology at the biological branches of uni- versities. Such education will establish and produce expertise and knowledge, which is currently being eroded dramatically, because of the lack of financial support. 9. Public awareness and educational programmes are essential to minimize the trans- mission of pathogens by flies, especially in times of disaster. It is particularly impor- tant to teach the benefits of exclusion of flies from foods and from food-preparation and dining areas. 10.Communities should develop fly-management guidelines that indicate action thres- holds for adult populations and that suggest corrective measures to be taken when thresholds have been exceeded. Corrective measures may include legal action to be taken against individuals or companies that fail to control flies when a nuisance situa- Flies 228 increases in efficacy have not been substantiated.

7.8.11. Air flow

To prevent or minimize flies from entering structures, airflow from air curtains can be used around doorways Mathis, Smith Schoof, 1970. In some places, air curtains are required on service entrances where doors remain open for long periods. Air curtains can also be used over entrances used by customers, although customer acceptance is usually low. New research is revealing improved methods for air curtain use that will maximize results and improve customer satisfaction. Also, ceiling fans can be used indoors to prevent flies from entering and resting in selected areas, such as on counters or in food preparation areas in commercial establishments. Airflow does not need to be extremely high to keep flies away. Fans can be used in conjunction with ultraviolet light traps in a push–pull system, by placing fans over areas where fly exclusion is desired and placing light traps in nearby dead air spaces, to capture the flies.

7.9. Guidelines for fly control

The following guidelines are used to control flies. • Monitor regularly the urban fly populations, with a special focus on hospitals, retire- ment facilities, kindergartens and the like. Evaluate their pathogen load and determine the percentage of infected flies. • Devise a system to better estimate when disease outbreaks are related to pathogens transmitted by flies. • Restrict pesticide usage to outbreak scenarios. Determine the peak season of various pest species, to predict potential outbreaks. These flies could then be managed with the focused use of pesticides during a small window of time. • Develop improved attractants to use in traps and baits. • Improve trap designs. • Improve fly-exclusion and trapping devices for use around entrances. • Develop effective perimeter barriers or perimeter control techniques that do not involve the use of pesticides. • Educate the public about the biology, ecology and control of nuisance flies, the role of flies as transmission agents and the need for proper sanitation to prevent flies from beco- ming contaminated. • Refine our knowledge of fly biology and of their habits and behaviour in urban areas. Public Health Significance of Urban Pests 231 References 1 Allen SJ et al. 2004. Flies and Helicobacter pylori infection. Archives of Disease in Childhood , 89:1037–1038. Armed Forces Pest Management Board 2006. Filth flies: significance, surveillance and control in contingency operations. Washington, DC, Armed Forces Pest Management Board, Defense Pest Management Information Analysis Center Technical Guide No. 30; http:www.afpmb.orgpubstimsTG30TG30.htm, accessed 14 August 2006. Betke P, Schultka H , Ribbeck R 1986. Stomoxys calcitrans: Plage in einer Milchviehanlage. Angewandte Parasitologie, 27:39–44. Bishopp FC, Laake EW 1921. Dispersion of flies by flight. Journal of Agricultural Research , 21:729–766. Brownstein JS, Holford TR, Fish D 2005. Effect of climate change on Lyme disease risk in North America. EcoHealth, 2:38–46. CDC [web site] 2006. Atlanta, GA, Centers for Disease Control and Prevention http:www.cdc.govaboutdefault.htm, accessed 26 November 2006. Clavel A et al. 2002. House fly Musca domestica as a transport vector of Cryptosporidium parvum . Folia Parasitologica, 49:163–164. Cohen D et al. 1991. Reduction of transmission of shigellosis by control of houseflies Musca domestica. Lancet, 337:993–997. De Jesus AJ et al. 2004. Quantitative contamination and transfer of Escherichia coli from foods by houseflies, Musca domestica L. Diptera: Muscidae. International Journal of Food Microbiology , 93:259–262. Demény A 1989. [Filth fly breeding sites on a H ungarian large-scale cattle farm]. Parasitologica Hungarica , 22:99–107. Ebeling W 1975. Urban entomology. Los Angeles, CA, University of California, Division of Agricultural Sciences. ECDC 2006. Eurosurveillance [web site]. Stockholm, European Centre for Disease Prevention and Control http:www.eurosurveillance.orgindex-02.asp, accessed 26 November 2006. Flies 230 tion has been identified. 1 The literature cited is a representative sample of what is relevant and important to the topic, but is not intended to constitute a com- prehensive systematic review. The references are considered to be highly reputable and will give the reader an overview of the state- of-the-art knowledge in this field. Public Health Significance of Urban Pests 233 pods in the central Philippines. The Southeast Asian Journal of Tropical Medicine and Public Health , 3:45–51. Grübel P et al. 1997. Vector potential of houseflies Musca domestica for Helicobacter pylori . Journal of Clinical Microbiology, 35:1300–1303. Grübel P et al. 1998. Detection of Helicobacter pylori DNA in houseflies Musca domes- tica on three continents. Lancet, 352:788–789. H all MJR, Wall R 1995. Myiasis in humans and domestic animals. Advances in Parasitology , 35:258–334. Hansens EJ 1951. The stable fly and its effect on seashore recreational areas in New Jersey. Journal of Economic Entomology, 44:482–487. Harwood RF, James MT 1979. Entomology in human and animal health, 7th ed. New York, Macmillan Publishing Company, Inc. Hemingway J, Ranson H 2000. Insecticide resistance in insect vectors of human disease. Annual Review of Entomology , 45:371–391. Hogsette JA 1981. Fly control by composting manure at a south Florida equine facility. In: Patterson RS et al., eds. Status of biological control of filth flies: proceedings of a works- hop. Gainesville, Florida, United States Department of Agriculture Science and Education Administration:105–113. Hogsette JA, Farkas R 2000. Secretophagous and haematophagous higher Diptera. In: Papp L, Darvas B, eds. Contributions to a manual of palaearctic Diptera. Vol. 1. General and applied dipterology . Budapest, Science Herald: 769–792. Hogsette JA, Ruff JP 1985. Stable fly Diptera: Muscidae migration in Northwest Florida. Environmental Entomology, 14:206–211. Hogsette JA, Ruff JP, Jones CJ 1987. Stable fly biology and control in northwest Florida. Journal of Agricultural Entomology , 4:1–11. Hogsette JA, Ruff JP, Jones CJ 1989. Dispersal behaviour of stable flies Diptera: Muscidae. In: Petersen JJ, Greene GL, eds. Current status of stable fly Diptera: Muscidae research. Miscellaneous Publications of the Entomological Society of America, 74:23–32. Houghton JT et al., eds. 2001. Climate change 2001: the scientific basis. Cambridge, United Kingdom, Cambridge University Press. James MT 1947. T he flies that cause myiasis in man. Washington, DC, United States Government Printing Office United States Department of Agriculture Miscellaneous Publications, No. 631. Flies 232 Farkas R, Hogsette JA 2000. Control possibilities of filth-breeding flies in livestock and poultry production. In: Papp L, Darvas B, eds. Contributions to a manual of palaearctic Diptera . Vol. 1. General and applied dipterology. Budapest, Science Herald:889–904. Farkas R, Papp L 1989. [Species composition and breeding sites of fly communities Diptera in caged-layer houses in Hungary]. Parasitologica Hungarica, 22:93–98. Faulde M 2002. Vorkommen und Epidemiologie vektorassoziierter Infektionserkrankungen in Mitteleuropa . Augsburg, Germany, U-Books Verlag. Foil LD, Hogsette JA 1994. Biology and control of tabanids, stable flies, and horn flies. Revues Scientifique et Technique de l’Office Internationale des Epizooties , 13:1125–1158. Fotedar R et al. 1992. The housefly Musca domestica as a carrier of pathogenic micro- organisms in a hospital environment. The Journal of Hospital Infection, 20:209–215. Goulson D et al. 2005. Predicting calyptrate fly populations from the weather, and pro- bable consequences of climate change. Journal of Applied Ecology, 42:795–804. Graczyk TK, Knight R, Tamang L 2005. Mechanical transmission of human proto- zoan parasites by insects. Clinical Microbiology Reviews, 18:128–132. Graczyk T K et al. 1999. H ouse flies Musca domestica as transport hosts of Cryptosporidium parvum . T he American Journal of Tropical Medicine and Hygiene, 61:500–504. Graczyk TK et al. 2000. Mechanical transport and transmission of Cryptosporidium par- vum oocysts by wild filth flies. The American Journal of Tropical Medicine and Hygiene, 63:178–183. Graczyk TK et al. 2001. The role of non-biting flies in the epidemiology of human infectious diseases. Microbes and Infection, 3:231–235. Greenberg B 1964. Experimental transmission of Salmonella typhimurium by house flies to man. American Journal of Hygiene, 80:149–156. Greenberg B 1971. Flies and disease. Vol I. Ecology, classification, and biotic associations. Princeton, Princeton University Press. Greenberg B 1973. Flies and disease. Vol II. Biology and disease transmission. Princeton, Princeton University Press. Greenberg B 1991. Flies as forensic indicators. Journal of Medical Entomology, 28:565–577. Gregorio SB, Nakao JC, Beran GW 1972. Human enteroviruses in animals and arthro- Public Health Significance of Urban Pests 235 Nayduch D, Noblet GP, Stutzenberger FJ 2002. Vector potential of house flies for the bacterium Aeromonas caviae. Medical and Veterinary Entomology, 16:193–198. Newson H D 1977. Arthropod problems in recreation areas. Annual Review of Entomology , 22:333–353. Nichols GL 2005. Fly transmission of Campylobacter. Emerging Infectious Diseases, 11:361–364. Ogden NH et al. 2006. Climate change and the potential for range expansion of the Lyme disease vector Ixodes scapularis in Canada. International Journal for Parasitology, 36:63–70. Olsen AR 1998. Regulatory action criteria for filth and other extraneous materials. III. Review of flies and foodborne enteric disease. Regulatory Toxicology and Pharmacology, 28:199–211. Olsen AR, Hammack TS 2000. Isolation of Salmonella spp. from the housefly, Musca domestica L., and the dump fly, Hydrotaea aenescens Wiedemann Diptera: Muscidae, at caged-layer houses. Journal of Food Protection, 63:958–960. Osato MS et al. 1998. Houseflies are an unlikely reservoir or vector for Helicobacter pylori. Journal of Clinical Microbiology , 36:2786–2788. Parmesan C, Yohe G 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature, 421:37–42. Peterson AT, Shaw J 2003. Lutzomyia vectors for cutaneous leishmaniasis in Southern Brazil: ecological niche models, predicted geographic distributions, and climate change effects. International Journal of Parasitology, 33:919–931. Post K et al. 1999. Fly larvae and pupae as vectors for scrapie. Lancet, 354:1969–1970. Poulin R 2006. Global warming and temperature-mediated increases in cercarial emer- gence in trematode parasites. Parasitology, 132:143–151. Prüss A et al. 2002. Estimating the burden of disease from water, sanitation, and hygiene at a global level. Environmental Health Perspectives, 110:537–542. Rady MH et al. 1992. Bacterial contamination of the housefly Musca domestica, collec- ted from 4 hospitals at Cairo. Journal of the Egyptian Society of Parasitology, 22:279–288. Rahuma N et al. 2005. Carriage by the housefly Musca domestica of multiple-antibio- tic-resistant bacteria that are potentially pathogenic to humans, in hospital and other urban environments in Misurata, Libya. Annals of Tropical Medicine and Parasitology, 99:795–802. Flies 234 Jones CJ et al. 1985. Effects of natural saccharide and pollen extract feeding on stable fly Diptera: Muscidae longevity. Environmental Entomology, 14:223–227. Keen JE et al. 2003. Isolation of Shiga-toxigenic Escherichia coli ST EC from livestock pest flies. In: Proceedings of the 84th Annual Meeting of the Conference of Research Workers in Animal Diseases , Chicago, IL, 9–11November 2003 https:www.ars.usda.govresearchpublicationspublications.htm?seq_no_115=138624, accessed 2 March 2007. Kettle DS 1995. Medical and veterinary entomology, 2nd ed. Cambridge, United Kingdom, CAB International. Khalil K et al. 1994. Flies and water as reservoirs for bacterial enteropathogens in urban and rural areas in and around Lahore, Pakistan. Epidemiology and Infection, 113:435–444. Killough RA, McKinstry DM 1965. Mating and oviposition studies of the stable fly. Journal of Economic Entomology , 58:489–491. Kobayashi M et al. 1999. Houseflies: not simple mechanical vectors of enterohemor- rhagic Escherichia coli O157:H7. The American Journal of Tropical Medicine and Hygiene, 61:625–629. LaBrecque GC, Meifert DW, Weidhaas DE 1972. Dynamics of house fly and stable fly populations. Florida Entomologist, 55:101–106. Larsen EB, Thomsen M 1940. The influence of temperature on the development of some species of Diptera. Videnskabelige meddelelser fra Dansk Naturhistorisk Forening, 104:1–75. Levine OS, Levine MM 1991. Houseflies Musca domestica as mechanical vectors of shi- gellosis. Reviews of Infectious Diseases, 13:688–696. Luger SW 1990. Lyme disease transmitted by a biting fly. The New England Journal of Medicine , 322:1752. Lysyk TJ, Axtell RC 1987. A simulation model of house fly Diptera: Muscidae deve- lopment in poultry manure. Canadian Entomologist, 119:427–437. Mathis W, Smith EA, Schoof HF 1970. Use of air barriers to prevent entrance of house flies. Journal of Economic Entomology, 63:29–31. Melnick JL 1951. Poliomyelitis and poliomyelitis-like viruses of man and animals. Annual Review of Microbiology , 5:309–332. Murvosh CM, Thaggard CW 1966. Ecological studies of the house fly. Annals of the Entomological Society of America , 59:533–547. Public Health Significance of Urban Pests 237 Tarry DW, Bernal L, Edwards S 1991. Transmission of bovine virus diarrhoea virus by blood feeding flies. The Veterinary Record, 128:82–84. T homas GD, Skoda SR, eds 1993. Rural flies in the urban environment? Lincoln, University of Nebraska North Central Regional Research Publication No. 335. Treese RE 1960. Distribution, life history, and control of the face fly in Ohio. In: Proceedings of the N orth-Central Branch of the Entomological Society of America , 15:107–108; Milwaukee, 23–25 March 1960. Urban JE, Broce AB 2000. Killing of flies in electrocuting insect traps releases bacteria and viruses. Current Microbiology, 41:267–270. Wallace GD 1971. Experimental transmission of Toxoplasma gondii by filth-flies. The American Journal of Tropical Medicine and Hygiene , 20:411–413. Ward R, Melnick JL, Horstmann DM 1945. Poliomyelitis virus in fly-contaminated food collected at an epidemic. Science, 101:491–493. Watt J, Lindsay DR 1948. Diarrheal disease control studies: I. Effect of fly control in a high morbidity area. Public Health Reports, 63:1319–1334. WHO 2002. Food safety and food-borne illnesses. Geneva, World Health Organization WHO Fact Sheet No. 237; http:www.who.intmediacentrefactsheetsfs237enprint.html, accessed 7 December 2006 WHO Regional Office for Europe 2006. LARES: Large Analysis and Review of European housing and health Status. Copenhagen, WH O Regional Office for Europe http:www.euro.who.intDocumentHOHLARES_results.pdf, accessed 9 August 2006. Winpisinger KA et al. 2005. Spread of Musca domestica Diptera: Muscidae, from two caged layer facilities to neighboring residences in rural Ohio. Journal of Medical Entomology , 42:732–738. Zumpt F 1973. The Stomoxyine biting flies of the world. Stuttgart, Gustav Fischer Verlag. Flies 236 Root TL et al. 2003. Fingerprints of global warming on wild animals and plants. Nature, 421:57–60. Rosef O, Kapperud G 1983. H ouse flies Musca domestica as possible vectors of Campylobacter fetus subsp. jejuni. Applied and Environmental Microbiology, 45:381–383. Rugg D 1982. Effectiveness of Williams traps in reducing the numbers of stable flies Diptera: Muscidae. Journal of Economic Entomology, 75:857–859. Sasaki T, Kobayashi M, Agui N 2000. Epidemiological potential of excretion and regur- gitation by Musca domestica Diptera: Muscidae in the dissemination of Escherichia coli 0157:H7 to food. Journal of Medical Entomology, 37:945–949. Scudder HL 1947. A new technique for sampling the density of house fly Musca domes- tica populations. Public Health Reports, 62:681–686. Scudder HL 1949. Some principles of fly control for the sanitarian. The American Journal of Tropical Medicine and Hygiene , 29:609–623. Sherman RA 2000. Wound myiasis in urban and suburban United States. Archives of International Medicine , 160:2004–2014. Skidmore P 1985. The biology of the Muscidae of the world. Dordrecht, Netherlands, Dr. W. Junk Publishers. Sømme L 1961. On the overwintering of house flies Musca domestica L. and stable flies Stomoxys calcitrans L. in Norway. Norsk Entomologisk Tidsskrift, 11:191–223. Soós Á, Papp L, ed. 1986. Catalogue of palaearctic Diptera. Vol. 11. Scathophagidae- Hypodermatidae . Budapest, Akadémiai Kiadó, Sramova H et al. 1992. Epidemiological role of arthropods detectable in health facilities. The Journal of Hospital Infection , 20:281–292. Srinivasan R et al. 2006. Muscoid fly populations in tsunami-devastated villages of sou- thern India. Journal of Medical Entomology, 43:631–633. Steinbrink H 1989. Zur Verbreitung von Stomoxys calcitrans Diptera: Muscidae in Ställen. Angewandte Parasitologie, 30:57–61. Stenseth NC et al. 2002. Ecological effects of climate fluctuations. Science, 297:1292–1296. Szalanski AL et al. 2004. Detection of Campylobacter and Escherichia coli O157:H7 from filth flies by polymerase chain reaction. Medical and Veterinary Entomology, 18:241–246. Public Health Significance of Urban Pests 239

8. Birds

Zdenek Hubálek Summary Beside the harm some wild urban bird species mostly feral pigeons cause to buildings by their activity and droppings, their nesting sites can be the source of abundant ectopa- rasites such as argasid ticks, mites, bugs and fleas that produce allergic reactions in peo- ple. Also, certain microorganisms pathogenic to people have been found to be associated with wild urban birds: • some arboviruses the agent of diseases such as St. Louis encephalitis virus and West Nile virus; • Chlamydophila psittaci the etiological agent of ornithosis; • Borrelia burgdorferi sensu lato the agent of Lyme disease; • Campylobacter jejuni the agent of campylobacterosis; • Salmonella enterica serovars Enteritidis and Typhimurium the agents of salmonello- sis; • Histoplasma capsulatum the agent of histoplasmosis; and • Cryptococcus neoformans the agent of cryptococcosis. Cases of human disease acquired directly from urban birds or from their habitats have been reported for ornithosis, histoplasmosis, salmonellosis, campylobacterosis, mycobac- teriosis, cryptococcosis, and toxoplasmosis. Monitoring zoonotic and sapronotic diseases associated with birds in urban areas is the first essential step in controlling these diseases. In circumstances of established risk, managing urban bird populations includes: • restricting their feeding at public sites; • controlling scavenging birds on landfill sites and at harbours if bird numbers create hygienic problems; and • controlling and sanitizing large communal roosts of birds in city parks and suburban habitats. Also, proactive and reactive control measures can be implemented, such as: • dispersing birds – for example, by acoustic or light signal methods, predation by trai- ned raptors or water-mist sprayers; • modifying habitats – for example, by thinning or clearing vegetation; • inhibiting birds from breeding on buildings by blocking the loft orifices and perch sites in, on, and below the roofs, using netting, spike systems, repellent gels or electroshock