Abstract
Pests that infest stored food products are an important problem worldwide. In addition to causing loss and consumer rejection of products, these pests can elicit allergic reactions and perhaps spread disease-causing microorganisms. Booklice (Liposcelis spp.), grain mites (Acarus siro), and flour beetles (Tribolium spp.) are common stored-product pests that have previously been identified in our laboratory animal facility. These pests traditionally are described as harmless to our animals, but their presence can be cause for concern in some cases. Here we discuss the biology of these species and their potential effects on human and animal health. Occupational health risks are covered, and common monitoring and control methods are summarized.
Several insect and mite species are termed ‘stored-product pests,’ reflecting the fact that they routinely infest items such as foodstuffs stored for any noteworthy period of time. Some of the most economically important insect pests include beetles of the order Coleoptera and moths and butterflies of the order Lepidoptera.43,50 In addition, arachnid mites, such as those of the families Acaridae and Glycyphagidae, can cause considerable damage.38,50 Global markets and transport have enabled widespread distribution, and some species have even been found in the stored food supplies of remote Antarctic research stations.14,53 Estimates of the amounts of stored grain lost to insect damage are 5% to 10% in developed countries and as much as 35% in developing countries.11 In the developed world, contamination of food resulting in diminished aesthetic value is of greater concern than is direct loss of material due to insect consumption.11 Aside from aesthetic issues, stored-product pests have been described as harmless to humans and animals. These organisms can, however, induce allergic reactions, alter the taste of food, and potentially serve as mechanical vectors for human pathogens.11
Stored-product pests have been identified in laboratory animal facilities but, given that they are regarded as ‘pseudoparasites,’ they are not typically the primary targets of pest management programs or addressed during animal importation quarantine.13,31,42 Even when research integrity and animal health is not likely affected negatively by infestations, the discovery of these pests on animals or food can have undesirable consequences.13 The untrained eye can easily confuse some species such as grain mites with rodent ectoparasites of concern. If mistaken for ectoparasites, costly additional diagnostics may be undertaken, and animals could be culled or treated unnecessarily.13 In addition, there is some concern that these pseudoparasites may be fomites or vectors for adventitious pathogens.3,13,24,53 Furthermore, the presence of these pests in storage and housing areas can lead to food wastage and negative human health consequences such as allergic hypersensitivity.11,52,53 In light of these attributes, these species should perhaps not be summarily disregarded if found in laboratory animal facilities.
In this brief overview, we discuss the general biology of 3 stored-product pests—booklice (Liposcelis spp.), grain mites (Acarus siro), and flour beetles (Tribolium spp.). All have been observed at our institution with some regularity. We also address the potential risk of untoward consequences of these pests to personnel and animals and thoughts regarding their management.
Booklice
Taxonomy and biology.
As with many organisms, details regarding the taxonomy and phylogeny of lice are often the subjects of debate among professionals. It is generally agreed that the parasitic lice comprise more than 4900 species belonging to the order Phthiraptera.4,5,27 Other, more historical classification schemes place lice in 2 orders: the Anoplura (sucking lice) and Mallophaga (chewing lice).5 This rather simplistic organization appears to be losing support over time, and the majority of phylogenists currently suggest the complete abandonment of Mallophaga as an order, with placement of parasitic lice into the following 4 suborders: Anoplura, and the chewing or biting suborders of Amblycera, Ischnocera, and Rhyncophthirina.5 Species contained in these suborders are important parasites of birds and mammals. Of interest in the laboratory animal facility are Polyplax spinulosa and P. serrata, anopluran ectoparasites capable of infesting rats and mice, respectively.3 Polyplax spp. are known vectors for multiple pathogens including Mycoplasma haemomuris and Francisella tularensis.3 The majority of lice are unique in the world of ectoparasites in that they tend to be very host-specific, although not with complete fidelity to the host, and they experience their entire lifecycle on the host species.9,26
Booklice belong to the order Psocoptera, which contains nonparasitic species.4 Members of this order, which also includes barklice, are free-living species with chewing mouthparts and are thought to be ancestors to the sucking, parasitic lice forms.33 Originally described on the basis of specimens harvested from the bark of trees in Africa in 1931, more than 5500 psocid species within 41 families and 3 suborders have been identified.2,7 The term barklice is typically reserved for psocid species that inhabit the bark of trees. Barklice are often considered beneficial scavengers because they consume excess accumulation of fungi, algae, and dead bark on trees. Psocid species known as booklice received their common name due to their inhabitation of old books, where they can feed on the glue used for binding. Although nonparasitic, these insects often interact with mammals and birds by living in nests, burrows, fur, or feathers and feeding on fungi or organic matter.33 Psocids were historically ignored as storage pests due to lack of evidence indicating noteworthy quantitative or qualitative losses associated with their presence.2 They have been found infesting stored grain worldwide and are adapted to live in food-processing facilities and kitchens also.2 Among psocids, members of the genus Liposcelis, including L. bostrycophila, L. decolor, L. entomophila and L. paeta, are the most frequently encountered food pests, and L. bostrychophila is one of the more commonly studied species.36,37 Psocids can thrive on a variety of food sources, including cellulose, book bindings, fabric, glue, any type of grain, mold, mildew, algae, and other plant material.2
Psocids are usually less than 3 mm long, visible without magnification, with white to light-colored soft bodies and long filiform antennae (Figure 1)38. Psocid eggs are usually simple, smooth, elongate ovoids or cylinders without a micropyle.6 The eggs may be bare or covered with fecal material or a layer of silk webbing and can be laid in groups or singly.2 Several psocid species, including L. bostrychophila, are parthenogenetic.62 Parthenogenesis is a form of asexual reproduction that allows rapid colonization of new habitats but restricts genetic variation.62 An ambient temperature of 30 ± 2.5 °C and relative humidity of 70% to 80% are optimal for growth.2 In typical household conditions of approximately 20 °C and greater than 60% relative humidity, L. bostrychophila can survive as long as 2 mo without food, and survival can exceed 100 d at greater than 70% humidity.54 Psocids are unlikely to complete development or reproduce at temperatures below 20 °C or above 40 °C, and they cannot survive when the relative humidity is consistently below 50% to 60%.43,53,58 They have been observed to move out of a bin of low-moisture food at night to rehydrate and return to the bin in the morning.43
Figure 1.
Adult Liposcelis spp. (booklouse); 4x magnification.
The ability to infest rapidly, due to parthenogenesis and a short (21 d) life cycle, along with adult longevity (72 to 144 d) and the capacity for surviving in adverse conditions without food combine to make Liposcelis spp. very difficult to eradicate.2,39 Objects such as pallets can serve as both hiding places and a means of transporting Liposcelis spp. between facilities.2 In addition, standard food-storage facility practices of protection and disinfestation frequently fail to control psocids.39 They do not succumb to practices that have been developed primarily to control beetle pests, and several psocid populations have shown strong resistance to phosphine and other commonly used grain protectants.36
Significance to animal health.
Psocids are the intermediate host for the ruminant tapeworm Thysanosoma actinioides.3 Psocids ingest the tapeworm eggs, which develop and form cysticercoids in the insect's body cavity, and the insect may subsequently be ingested by ruminants while grazing.3 In addition, Liposcelis spp. may be capable of transmitting fungi and bacteria, because these organisms remain viable in the insect's feces after digestion.53 L. bostrychophila was recently shown to harbor Rickettsia felis, the causative agent of flea-borne spotted fever (rickettsiosis) in humans.8 Some insect symbionts including Wolbachia, Cardinium, and another Rickettsia species have been suggested to induce parthenogenesis in their host.8 Antibiotic treatment inhibits L .bostrychophila reproduction, supporting the theory that these rickettsial symbionts play a role in parthenogenesis.8 In addition to potential reproductive effects, the Rickettsia found in Liposcelis have been postulated to supplement host nutrition.8 Although a definitve mammalian host for R. felis has not been identified, naturally seropositive cats, dogs, opossums, and rats have been identified.10,44 Psocids have not been shown to transmit R. felis-induced disease to vertebrates, but genetic sequencing found that the psocid R. felis plasmid is virtually identical to the R. felis that infects cat fleas, which are known to transmit disease.8 Further research is needed to understand the potential pathogenicity of the psocid R. felis for vertebrates. Because of their potential to carry parasites, fungi, and bacteria and reports of infestation of mammals, ideally psocids should be excluded from the animal facility.
Grain Mites
Taxonomy and biology.
More than 30,000 species of arachnid mites and ticks in the subclass Acari have been described, and an estimated half- million species exist in total.49 Mites are distributed worldwide in a variety of habitats, including soil, oceans, deserts, and ice fields, but relatively few are considered parasites.49 There is some disagreement regarding the names and classification of groups within the subclass Acari.49 Acari can be divided into 2 superorders: Parasitiformes (Anactinotrichida), composed of ticks and a variety of mites, and Acariformes (Actinotrichida), the most diverse group of mites.49 The 3 orders within the superorder Acariformes are the Acaridida (Astigmata), the Actinedida (Prostigmata), and the Oribatida (Cryptostigmata).49 The grain mite (Acarus siro), also known as the flour mite, is in the order Acaridida and family Acaridae, which comprises free-living mites broadly referred to as storage or stored-product mites.15,49 More than 50 species of mites have been found in association with stored products, but A. siro is one of the most common and well-known species.11,22 Other storage mites of importance include Tyrophagus putrescentiae of the family Acaridae and Lepidoglyphus destructor and Glycyphagus domesticus of the family Glycyphagidae.38
Grain mites infest a wide range of food products, including grain, flour, cereal, vegetables, cheese, and animal feed.11 These mites can be difficult to identify with certainty, and many mites described in the literature as A. siro might actually be of the species A. farris or A. immobilis.15,61 However, A. farris and A. immobilis occur primarily in outdoor environments, and morphologic distinction from the primarily indoor species A. siro is possible.61 A. siro mites are generally not visible to the naked eye, measuring approximately 0.5 mm long with almost colorless, oval bodies and brown legs (Figure 2).11,51 Interestingly, they are described as having a pungent ‘minty’ smell, especially when crushed.51 Eggs of stored-product mites, including A. siro, are usually shorter than 165 µm, white, glossy, symmetrical, and ellipsoid, with rounded ends and no micropyle.30 A. siro thrives in ambient temperatures and relative humidity—near 25 °C and 90%, respectively.51 At 60% relative humidity and lower, a population will eventually extinguish, but some mites can survive at 62.5% as long as the temperature is not much below 10 °C or above 20 °C.51 Some A. siro stages are resistant to temperature extremes, but a complete lifecycle is unlikely to occur outside a temperature range of 2.5 to 32 °C.18,19
Figure 2.
Grain mites (several possible species) infesting fresh bread in kitchen storage. Note the multiple rounded, glossy organisms near the center of the image (photo courtesy of DWSPL/N.Cattlin).
Significance to animal health.
Mites are well documented as fungal vectors in stored products, with the potential to change fungal populations and indirectly affect mycotoxin content.24 Some laboratory animal species may be susceptible to acariasis, a syndrome described in humans that is caused by mite invasion of various tissues.17,32 Experimental injection of 5 mites species, including A. siro, into the trachea of guinea pigs resulted in lung changes similar to those seen in humans with pulmonary acariasis.17 One study fed A. siro-infested food to pregnant mice and saw a statistically significant increase in fetal mortality and feed intake.59 Litter sizes were reduced as well but not significantly so.59 Grain mites ingested by rodents have been found in feces and mistaken for other, more problematic mite species, such as Myocoptes musculinus, Myobia musculi, and Radfordia spp.13 In a laboratory animal facility, mistaken identification of grain mite adults or eggs detected within rodent feces could lead to inappropriate treatment and control methods. Grain mite infection of various organs, fungal carrying potential, and reproductive effects could negatively affect research and production colonies.24,32,59
Flour beetles
Taxonomy and biology.
The class Insecta and order Coleoptera (beetles) comprises many species that exhibit a fascinating array of characteristics, including chemiluminescence (fireflies), defensive liquid spitting (bombardier beetles), and behavioral or chemical mimicry.16 Flour beetles belong to the family Tenebrionidae and genera Tribolium.12 The most commonly encountered food pests of the genus Tribolium are the red flour beetle (T. castaneum) and the confused flour beetle (T. confusum).12,50 Flour beetles have been found in more than 100 types of foodstuffs including grains, seeds, spices, flour, and cereal products; animal matter; wood; vegetables; and various drugs.21
Tribolium adults are small, reddish-brown beetles that are approximately 3.5 mm long with well-developed but rarely used wings (Figure 3).21 T. castaneum have wing covers called elytra which, as in all beetles, precisely fold over the wings to provide protection when not used in flight.16 Flour beetles are larger than are booklice and grain mites and are therefore less likely to go unnoticed; however, people may tend to dismiss beetles as a common, nonharmful insect. Adult flour beetles can live more than 3 y, with males remaining fertile for the entire lifespan and females laying fertile eggs until 1 y of age.21 Eggs average 0.35 mm wide and 0.6 mm long and are white to colorless, oblong or ovoidal, and nearly transparent.21,40 The egg surface sometimes appears irregular due to the adhesion of food particles to a sticky membrane.40 Infection with the Rickettsial organism Wolbachia has been shown to increase male fertility but decrease female fecundity.56 Optimal developmental conditions for Tribolium are 35.0 °C and greater than 70% relative humidity, but development can occur at 20.0 to 37.5 °C and 10% to 100% relative humidity.23 The red flour beetle possesses a kidney-like cryptonephridial organ, which allows it to survive extremely dry environments.16 T. castaneum is sometimes used as a research model and is considered more representative of the development of other insects than is Drosophila.16
Figure 3.
Adult Tribolium confusum (confused flour beetle); (photo courtesy of Simon Hinkley and Ken Walker, Museum Victoria).
Significance to animal health.
Tribolium have been recovered from bulk and bagged retail pet-food products.47 They possess benzoquinone-secreting defensive glands, which can impart an unpleasant odor to food. A single adult beetle can contain as much as 0.5 mg of these quinones.20,35 Benzoquinone, a potentially toxic derivative of benzene, is readily absorbed from the gastrointestinal tract and subcutaneous tissue.35 Topical application to skin can cause discoloration, papules, and necrosis.35 Vapors reportedly have caused serious eye injury.35 One study found that Swiss albino mice fed Tribolium-infested flour or biscuits made of Tribolium-infested flour had tumor incidences of 35.2% and 29%, respectively.20 These data were in contrast to the control groups, which did not develop any tumors.20 The tumors were mostly lympholeukemias associated with the liver and spleen.20 Multiple studies have shown benzoquinones cause carcinogenic changes in laboratory animals, but additional research is needed to evaluate these effects and the biologic significance of the levels produced by beetles.35 Flour beetles are an intermediate host of the ‘rat tapeworm’ Hymenolepis diminuta.3 H. diminuta can infect mice, rats, other rodents, and humans and other primates, but it is rarely encountered in laboratory populations.3 Infection of the definitive host occurs by ingestion of the infected arthropod.3 Light H. diminuta infections are generally nonpathogenic, but heavy infection can cause weight loss, retarded growth rate, and catarrhal enteritis.3,57 Tapeworm infestation acquired from the consumption of a flour beetle could negatively affect animal welfare, influence research, and lead to zoonotic infections.
Human Occupational Health Risks
The risk of untoward effects on human health from the species discussed herein has not been well studied to date. Although considered free-living species, parasitic psocid infestations of puppies, human fingernails, and a woman's hair have been reported.2,34,53 It is noteworthy that the human nail infestation was associated with hyperkeratotic, dermatophyte-infected nails, thus providing organic debris and crevices that essentially served as harborage for the psocids.34 The hair infestation, initially confused with headlice, occurred in a woman who habitually went to bed with wet hair next to an old bedside table that was infested with psocids.53 In addition, delusory parasitosis, a strong but erroneous belief that oneself is infested with parasites, has been reported in association with psocids.37 A. siro is one of several mites that have been identified as a cause of intestinal, pulmonary, and urinary acariasis in humans.17,32 Depending on which organ system is affected, acariasis can lead to a variety of clinical signs, including pain, diarrhea, coughing and fever.17 In humans, mites have been isolated from both urine and stool samples and have been associated with intestinal ulceration and bladder wall inflammation.32 The risk of these outcomes is seemingly very low in the laboratory animal setting, given the routine use of personal protective equipment.
Of greater concern is the potential for booklice, grain mites, and flour beetles to serve as sources of sensitizing allergens. Liposcelis spp. have been identified as potential allergens found in house dust.41,53 A study in Mumbai found psocids in 25% of house dust samples, and 20% of the studied allergic population had strong skin sensitivity to psocids.41 Studies of atopic European populations found a 7% to 26% prevalence of IgE antibody reaction to Liposcelis spp., suggesting that allergy to psocids occurs in a significant portion of patients. Grain mites and beetles are well-known sources of allergens for bakers and farm workers, but the role that these insects play in laboratory animal worker allergies has not been extensively evaluated and established.45,52,55 In a study examining 2 laboratory animal facilities for storage and house-dust mites, 25% of samples collected contained mites.42 Most were storage mites of Astigmata (Glycyphagidae, Acaridae) or Prostigmata (Tarsonemus spp., Cheuyletus spp.) species.42 Mites were found in samples collected from feed and bedding-storage floors and lounge chairs.42 The house-dust mite species, Dermatophagoides, was found in only a single sample.42 An additional study found mite-derived material in 21 of 22 dust samples taken in the laboratory animal facility.48 Skin prick tests in 40 laboratory animal workers with work-related rhinitis revealed that 14 (35%) were sensitized to storage mite species (A. siro, L. destructor, or T. putrescentiae).48 Nineteen (48%) subjects were positive for laboratory animal sensitization, and only 6 of these subjects were sensitized to both laboratory animals and mites.48 In contrast, only 1.7% of 300 persons in the general population of the same county were sensitized to any of the 3 storage mites.48 The authors concluded that in addition to laboratory animals and house-dust mites, storage mite species may pose an occupational health risk in animal facilities.42,48 Because of the potential for sensitization to mites, the factors of ventilation, cleaning, and personal protective practices are important considerations not only when handling animals but also when working around feed and bedding materials.48 The risk for laboratory animal allergy is well characterized, but the possibility of mite sensitization should also be considered in workers with respiratory complaints, especially when testing for laboratory animal allergy is negative.48
Management
Comprehensive pest management strategies are vital parts of any animal care program and are, in fact, recommended or required by accrediting and regulatory entities. According to the Guide for the Care and Use of Laboratory Animals, programs should implement “a regularly scheduled and documented program of control and monitoring.”25 The Animal Welfare Act Regulations require the establishment of an effective pest control program that addresses insects, ectoparasites, and avian and mammalian pests.1 The target species of such programs are not prescribed but typically include vermin such as feral mice and rats, spiders, cockroaches, and others species dependent on geographic location. It is unlikely that food-storage pests are routinely considered in pest control program design.
Commonly used monitoring techniques in animal facilities, such as light and sticky traps, may not be effective methods to attract and visualize very small and flightless mite and booklice species.60 In addition, these pests can be resistant to routinely used control techniques. For example, permethrin has been used for pest control in laboratory animal facilities, but field trials in Indonesia found that psocid populations can flourish after permethrin treatment, indicating a tolerance to the insecticide and potential benefit of removing permethrin-sensitive predator and competitor species.37,60
Monitoring of insects in food-processing and -storage facilities is often performed by using direct visual sampling or traps.11 Visual inspection can be time-consuming, destructive when packages must be opened, and requires appropriate training.11 However, direct observation has the benefit of not only identifying signs of infestation but also detecting other potential problems, such as spillage and spoilage.11 A variety of traps are available, and most use an attractant of some kind such as pheromones, food odors, or light.11 Lights are often used for fly management but can attract some food-storage insects and allow monitoring of species and number.11 Pheromones allow targeting of a specific species with a highly sensitive detection tool.43 The most commonly used methods for mite detection include sieving with visual inspection, extraction with Tullgren–Berlese funnels, and filth flotation.29 More recently developed methods include immunochemical methods (ELISA), near-infrared detection, and ‘electronic nose’ gas sensors that identify a specific odor profile.28,29,46
A variety of control strategies used in food-processing facilities include housekeeping and exclusion practices, special packaging methods, pesticide and pheromone use, and the use of heat and biologic control.11 Pheromones are mainly considered a monitoring tool but have also been used for mass trapping and mating disruption.11 Pesticide choice is limited by food-safety requirements and known insecticide resistance in some cases.2 Management options may be even more limited for laboratory animal facilities due to potential effects on animal health and research. Because of their potential to induce toxic effects on research animals, the Guide says pesticides should be used only when necessary.25 In addition, investigators should be consulted before their animals are potentially exposed to pesticides.25 Biorational approaches avoid the use of chemical pesticides either by directly using biologically based materials or by taking advantage of key aspects of the pest's biology to manipulate the environment.43
One of the most basic and important management strategies is sanitation of food-storage areas and exclusion of pests from food packages.43 Food bins should be cleaned before refilling with fresh food to remove older products that may harbor pests.43 All food debris should be carefully swept and/or vacuumed in food storage areas. Consideration should be given to pallets and food packaging which can serve as harboring places for pests as well as a means of transport.2 Chemical treatment of bags and pallets, however, is unlikely to penetrate all potentially infested areas or be effective against all pests while maintaining safety for animals. In our experience, grain mites and psocids have been found inside unopened food bags, theoretically making treatment of the packaging largely ineffective. Ideally, potentially infested wooden pallets would not be allowed to enter the facility, and bags should be closely examined for any signs of damage but, as noted previously, visualization of some of these pests is challenging. Many control strategies have been developed but most leave remnants of the dead pests in the food, making a preventative approach to pest control ideal.
To reduce pest burden in food storage areas, maintaining temperature or humidity levels that are incompatible with life or reproduction of the species at hand is another approach. It would be important to ensure that the conditions chosen for treatment do not carry the risk of compromising the nutrient contents or composition of the food. Maximal population growth occurs between 25 and 33 °C for most insects.43 Temperatures of approximately less than or equal to 13 °C and greater than or equal to 35 °C usually slow development and eventually cause death, but these optimal and lethal temperature ranges do not apply to all species, and control strategies should be based on the biology of the target pest.43 The Guide recommends housing rodents at a macroenvironmental temperature range of 20 to 26 °C.25 This recommended temperature range for rodents overlaps the optimal growth temperature for many pests and may provide an environment suitable for infestation. Storage in freezing conditions for 2 to 3 wk often successfully disinfests products but can be costly.43 Heat treatment can be used to treat a contaminated storage area, and the goal is usually to raise the temperature to 50 to 60 °C for 24 h, but this practice may be contraindicated due to facility structure and heat-sensitive equipment.43 Many storage pests thrive at elevated humidity levels and are sensitive to humidity control and desiccation methods. For example, critical relative humidity limits for psocids range between 50% to 60%, and a 5% decrease below these levels may be lethal.2 It can take several days of decreased relative humidity for psocids to die, and if the humidity fluctuates back to higher levels, desiccated lice can recover lost water within a few hours.2 In addition to the recommended temperature range, the generally accepted relative humidity range of 30% to 70% in laboratory animal facilities allows potentially favorable growth conditions for food pests.25 Although these strategies that use alterations in the ambient environmental conditions are often possible, we acknowledge that making significant changes in HVAC parameters can be very challenging and might be impractical in some facilities.
The Guide recommends using nontoxic means, including insect growth regulators and amorphous silica gel (that is, diatomaceous earth).25 Contact with diatomaceous earth absorbs hydrocarbons from insects’ cuticles, causing fatal dehydration.43 Diatomaceous earth is nontoxic to vertebrates and is a common food additive, but high levels of the abrasive dust can bother workers and damage equipment.43 Perhaps the most effective approach to prevent introduction of storage pests into the facility is to treat food products themselves in ways that eliminate pests prior to dispersion to animals. Autoclaving food is likely the most effective method available in animal facilities. Ionizing radiation can kill insects through DNA damage and cell-cycle disruption but does not cause immediate mortality.43 Doses of 0.4 kGy or less typically are effective.43 Controlled and modified atmospheres with target gas concentrations of less than or equal to 3% oxygen or 60% carbon dioxide have been considered as a biorational substitute for chemical fumigation.43 Many other food-pest control strategies have been described, including impact or mechanical destruction, insect natural enemies, microbial insecticides, botanical insecticides, and insect growth regulators.43
Summary
Booklice, grain mites, and flour beetles are just a few of many food storage pests that could potentially be encountered in a laboratory animal facility. Food-storage pests pose a considerable economic threat to food production worldwide, but light infestations are unlikely to cause major food losses. The potential risk to animal health from these pests may be low but warrants consideration and further investigation. Specifically, additional studies investigating the significance and prevalence of these pests in the laboratory animal facility need to be performed. Booklice, grain mites, and flour beetles are known human allergens and should be considered potential occupational health risks. Ideally, food pests should be excluded from the facility to minimize personnel exposure and avoid variables that may complicate research. Developing a monitoring and control strategy that is effective for all target pests and safe for use in the animal facility is a noteworthy challenge. When developing a plan, the biology of each pest should be considered along with the potential secondary effects on animal health and research.
Acknowledgments
We thank the animal care and veterinary technicians in the Emory University Division of Animal Resources for notifying us when these pests have been observed in our facility, the primary impetus behind this work.
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