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Medical Entomology

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GENERAL ENTOMOLOGY

Basic concepts of entomology, such as morphology, taxonomy and systematics, developmental biology, and ecology, provide important background information for medical and veterinary entomologists. General entomology books which the reader will find helpful in this regard include Borror et al. (1989), Gullan and Cranston (1994), Oillot (1995), Elzinga (1997), Chapman (1998), and Romoser and Stoffolano (1998). References that provide a more taxonomic or biodiversity-oriented approach to general entomology include works by Arnett (1993), Richards and Davies (1994), Bosik (1997), and Daly et al. (1998). General insect morphology is detailed in Snodgrass (1993), whereas a useful glossary of general entomology is Torre-Bueno (1962). Texts on urban entomology, the study of insect pests in houses, buildings, and urban areas, which also has relevance to medical-veterinary entomology, have been prepared by Ebeling (1975), Hickin (1985), MaUis (1997), and Robinson (1996). General texts on acarology include works by Krantz (1978), Woolley (1987), Evans (1992) and Walter and Proctor (1999).

MEDICAL-VETERINARY ENTOMOLOGY LITERATURE

Textbooks or monographs pertaining to medical entomology, veterinary entomology, or the combined discipline of medical-veterinary entomology are listed under these headings at the end of this chapter. Most of these publications emphasize arthropod morphology, biology, systematics, and disease relationships, whereas some of the more recent texts, such as Beaty and Marquardt (1996) and Crampton et al. (1997), emphasize molecular aspects of medical-veterinary entomology. Other works are helpful regarding common names of arthropods of medicalveterinary importance (Pittaway 1992), surveillance techniques (Bram 1978), control measures (Drummond et al. 1988), or ectoparasites (Andrews 1977, Marshall 1981, Kim 1985, Uilenberg 1994, Barnard and Durden 1999). Publications that devote substantial sections to arthropods associated with wildlife and the pathogens they transmit include Davis and Anderson (1971), Davidson et al. (1981), Fowler (1986) and Davidson and Nettles (1997).

Several journals and periodicals are devoted primarily to medical and/or veterinary entomology. These include the Journal of Medical Entomology, published by the Entomological Society of America (Lanham, MD); Medical and Veterinary Entomology, published by the Royal Entomological Society of London (UK); Journal of Vector Ecology, published by the Society of Vector Ecologists (Corona, CA); Vector Borne and Zoonotic Diseases, published by Mary Ann Liebert, Inc., Larchmont, New York; and Review of Medical and Veterinary Entomology, published by CAB International (Wallingford, UK). Journals specializing in parasitology, tropical medicine, or wildlife diseases that also include articles on medical-veterinary entomology include Parasitology, published by the British Society for Parasitology; Journal of Parasitology, published by the American Society of Parasitologists (Lawrence, KS); Parasite-Journal de la Societe Franfaise de Parasitologie, published by PRINCEPS Editions (Paris, France); Advances in Disease Vector Research, published by Springer-Verlag (New York); Bulletin of the World Health Organization, published by the World Health Organization (Geneva, Switzerland); Journal of Wildlife Diseases, published by the Wildlife Disease Association (Lawrence, KS); Emerging Infectious Diseases, published by the Centers for Disease Control and Prevention (Atlanta, GA); the American Journal of Tropical Medicine and Hygiene, published by the American Society of Tropical Medicine and Hygiene (Northbrook, IL); and Memorias Do Instituto Oswaldo Cruz; published by the Instituto Oswaldo Cruz (Rio de Janeiro, Brazil). Various Internet Web sites pertaining to medical-veterinary entomology can also be accessed for useful information.

HISTORY OF MEDICALVETERINARY ENTOMOLOGY

Problems caused by biting and annoying arthropods and the pathogens they transmit have been the subject of writers since antiquity (Service 1978). Homer (mid-8th century BC), Aristophanes (ca. 448-380 BC), Aristotle (384-322 BC), Plautus (ca. 254-184 BC), Columella (5 BC to AD 65), and Pliny (AD 23-79) all wrote about the nuisance caused by flies, mosquitoes, lice, and/or bedbugs. However, the study of modern medicalveterinary entomology is usually recognized as beginning in the late 19th century, when blood-sucking arthropods were first proven to be vectors of human and animal pathogens.

Englishman Patrick Manson ( 1844-1922 ) was the first to demonstrate pathogen transmission by a blood-feeding arthropod. Working in China in 1877, he showed that the mosquito Culex pipiensfatigans is a vector of Wuchereria bancrofti, the causative agent of Bancroftian filariasis. Following this landmark discovery, the role of various blood-feeding arthropods in transmitting pathogens was recognized in relatively rapid succession.

In 1891, Americans Theobald Smith (1859-1934) and F. L. Kilbourne (1858-1936) implicated the cattle tick, Boophilus annulatus, as a vector of Babesia bigemina, the causative agent of Texas cattle fever (bovine babesiosis/piroplasmosis). This paved the way for a highly successful B. annulatus-eradication program in the United States directed by the US Department of Agriculture. The eradication of this tick resulted in the projected goal: the elimination of indigenous cases of Texas cattle fever throughout the southern United States.

In 1898, Englishman Sir Ronald Ross (1857-1932), working in India, demonstrated the role of mosquitoes as vectors of avian malarial parasites from diseased to healthy sparrows. Also in 1898, the cyclical development of malarial parasites in anopheline mosquitoes was described by Italian Giovani Grassi (1854-1925). In the same year, Frenchman Paul Louis Simond (1858-1947), working in Pakistan (then part of India), showed that fleas are vectors of the bacterium that causes plague.

In 1848, American physician Josiah Nott (1804- 1873) of Mobile, AL, had published circumstantial evidence that led him to believe that mosquitoes were involved in the transmission of yellow fever virus to humans. In 1881, Cuban-born Scottish physician Carlos Finlay (1833-1915) presented persuasive evidence for his theory that what we know today as the mosquito Aedes aegypti was the vector of this virus. However, it was not until 1900 that American Walter Reed (1851-1902) led the US Yellow Fever Commission at Havanna, Cuba, which proved A. aegypti to be the principal vector of yellow fever virus.

In 1903, Englishman David Bruce (1855-1931) demonstrated the ability of the tsetse fly Glossina palpalis to transmit, during blood-feeding, the trypanosomes that cause African trypanosomiasis.

Other important discoveries continued well into the 20th century. In 1906, American Howard Taylor Ricketts (1871-1910) proved that the Rocky Mountain wood tick, Dermacentor andersoni, is a vector of Rickettsia rickettsii, the causative agent of Rocky Mountain spotted fever. In 1907, F. P. Mackie (1875-1944) showed that human body lice are vectors of Borrelia recurrentis, the spirochete that causes louse-borne (epidemic) relapsing fever. In 1908, Brazilian Carlos Chagas (1879-1934) demonstrated transmission of the agent that causes American trypanosomiasis, later named Chagas disease in his honor, by the cone-nose bug Panstrongylus megistus.

In 1909, Frenchman Charles Nicolle (1866-1936), working in Tunis, showed that human body lice are vectors of Rickettsia prowazekii, the agent of louse-borne (epidemic) typhus.

These important discoveries, as well as others of historical relevance to medical-veterinary entomology, are discussed in more detail in the references listed at the end of this chapter. Because of the chronology of many major discoveries relevant to this topic in the 50-year period starting in 1877, this time has been called the “golden age of medical-veterinary entomology” (Philip and Rozeboom 1973).

IDENTIFICATION AND ….. SYSTEMATICS OF ARTHROPODS OF MEDICAL-VETERINARY IMPORTANCE

Table I provides a list of the eight orders of insects and four orders of arachnids that are of particular interest to medical-veterinary entomologists. Accurate identification of these arthropods is an important first step in determining the types of problems they can cause and, subsequently, in implementing control programs.

Although taxonomy and identification are discussed in more detail with respect to arthropod groups treated in the chapters that follow, some publications provide a broader perspective on the classification, taxonomy,

Principle Orders of Insects and Arachnids of Medical-Veterinary Interest

and/or identification of a range of arthropods of medical-veterinary importance. These include two works published by the US Centers for Disease Control and Prevention (1979, 1994), as well as citations by Service (1988), Hopla et al. (1994), Lago and Goddard (1994), and Davis (1995). Mso, some medical-veterinary entomology books are very taxonomically oriented, with emphasis on identification, e.g., Baker et al. (1956), Smith (1973), Lane and Crosskey (1993), Walker (1995) and Baker (1999).

TYPES OF PROBLEMS CAUSED BY ARTHROPODS

ANNOYANCE

Irrespective of their role as blood-feeders (hematophages), parasites, or vectors of pathogens, certain arthropods cause severe annoyance to humans or other animals because of their biting behavior. These include lice, bedbugs, fleas, deer flies, horse flies, tsetse flies, stable flies, mosquitoes, black flies, biting midges, sand flies, chiggers, and ticks. Some, however, do not bite but instead are annoying because of their abundance, small size, or habit of flying into or around the eyes, ears, and nose. Nonbiting arthropods that cause annoyance include the house fl); chironomid midges, and eye gnats. Large populations of household or filth-associated arthropods, such as houseflies and cockroaches, can also be annoying. Nuisance arthropods are commonly problems for humans at outdoor recreational areas, including parks, lakes, and beaches.

ENVENOMATION

Members of several groups of arthropods can inject venom when they bite or sting. Most notable are bees, wasps, ants, spiders, and scorpions. Others, such as blister beetles and certain caterpillars, produce toxins that can cause problems when they are touched or ingested. Envenomation by these arthropods is discussed in more detail in the respective chapters that follow.

In general, envenomation results in medical or veterinary conditions ranging from mild itching to intense debilitating pain or even to life-threatening encounters due to allergic reactions. Envenomation sites on the skin usually appear as reddened, painful, more or less circular lesions surrounding the bite, sting, or point of venom contact. These areas may become raised and can persist for several days, often causing inflammation of adjacent tissues. Caterpillars that cause envenomation typically secrete toxins from specialized setae that penetrate the skin, causing contact dermatitis. Blisters can also develop at arthropod envenomation sites on contact of the skin with blister beetles (family Meloidae), false blister beetles (family Oedemeridae), and certain rove beetles (family Staphylinidae) which secrete toxins in their body fluids. If meloid beetles are accidentally ingested with fodder by livestock, the resulting systemic reaction can be life threatening.

ALLERGIC REACTIONS

A relatively wide spectrum of allergic reactions can occur in humans or animals exposed to certain arthropods. Many of the species involved also cause envenomation by biting or stinging, with the allergic reaction resulting from an overresponsive host immune system. Bites or stings from arthropods such as lice, bedbugs, fleas, bees, ants, wasps, mosquitoes, and chiggers all can result in allergic host reactions. Contact allergies can occur when certain beetles or caterpillars touch the skin. Respiratory allergies can result from inhaling allergenic air-borne particles from cockroaches, fleas, or other arthropods. The recirculation of air by modern air-handling systems in buildings tends to exacerbate inhalation of insect allergens.

Humans and animals usually react to repeated exposure to bites or stings from the same or antigenically related arthropods in two possible ways, depending on the nature of the antigen or venom inoculated and the sensitivity of the host: (1) desensitization to the bites or stings with repeated exposure and (2) allergic reactions which, in extreme cases, can develop into life-threatening anaphylactic shock. However, a distinct five-stage sequence of reactions typically occurs in most humans when they are repeatedly bitten or stung by the same, or related, species of arthropod over time. Stage 1 involves no skin reaction but leads to development of hypersensitivity. Stage 2 is a delayed-hypersensitivity reaction. Stage 3 is an immediate-sensitivity reaction followed by a delayedhypersensitivity reaction. Stage 4 is immediate reaction only, whereas Stage 5 again involves no reaction (i.e., the victim becomes desensitized). These changes reflect the changing host immune response to prolonged and frequent exposure to the same arthropod or to cross-reactive allergens or venoms.

INVASION OF HOST TISSUES

Some arthropods invade the body tissues of their host. Various degrees of invasion occur, ranging from subcutaneous infestations to invasion of organs such as the lungs and intestine. Invasion of tissues allows arthropods to exploit different host niches and usually involves the immature stages of parasitic arthropods.

The invasion of host tissues by fly larvae, called myiasis, is the most widespread form of host invasion by arthropods. Larvae of many myiasis-causing flies move extensively through the host tissues. As they mature, they select characteristic host sites (e.g., stomach, throat, nasal passages, or various subdermal sites) in which to complete the parasitic phase of their development.

Certain mites also invade the sldn or associated hair follicles and dermal glands. Others infest nasal passages, lungs, and air sacs or stomach, intestines, and other parts of the alimentary tract of their hosts. Examples include scabies mites, follicle mites, nasal mites, lung mites, and a variety of other mites that infest both domestic and wild birds and mammals.

ARTHROPOD-BORNE DISEASES

Table II lists the principle groups of insects and arachnids involved in arthropod-borne diseases and the associated types of pathogens. Among the wide variety ofarthropods that transmit pathogens to humans and other animals, mosquitoes are the most important, followed by ticks. Viruses and bacteria (including rickettsiae) are the most diverse groups of pathogens transmitted by arthropods, followed by protozoa and filarial nematodes.

All of the viruses listed in Table II are arthropodborne viruses, usually referred to as arboviruses, indicating that they are typically transmitted by insects or other arthropod hosts. The study of arboviruses is termed arbovirology.

Pathogens are transmitted by arthropods in two basic ways, either biologically or mechanically. In biological transmission, pathogens undergo development or reproduction in the arthropod host. Examples of diseases that involve biological transmission are malaria, African trypanosomiasis, Chagas disease, leishmaniasis, and lymphatic filariasis. In mechanical transmission, pathogens are transmitted by arthropods via contaminated appendages (usually mouthparts) or regurgitation of an infectious blood meal. Examples of diseases that involve mechanical transmission are equine infectious anemia and myxomatosis. Biological transmission is by far the more common and efficient mechanism for pathogen maintenance and transmission.

A wide range of life-cycle patterns and degrees of host associations is characterized by arthropod vectors. Some ectoparasites, such as sucldng lice, remain on their host for life. Others, such as mosquitoes and most biting flies, have a more fleeting association with the host, with some being associated with it only during the brief acts of host

Examples of Arthropod-Borne Diseases of Medical-Veterinary Importance

location and blood-fEeding. Between these two extremes is a wide range of host associations exhibited by different arthropod groups.

FOOD CONTAMINANTS

Many arthropods can contaminate or spoil food materials. In addition to causing direct damage to food resources, arthropods or their parts (e.g., setae, scales, shed cuticles, or body fragments) may be accidentally ingested. This can lead to toxic or allergic reactions, gastrointestinal myiasis, and other disorders.

Insects such as the house fly may alight on food and regurgitate pathogen-contaminated fluids prior to, or during, feeding. While feeding they also may defecate, contaminating the food with potential pathogens. Because the alimentary tract of arthropods may harbor pathogenic microorganisms, subsequent consumption of the contaminated food can lead to the transmission of these pathogens to humans or other animals. Similarly, the integument of household pests such as flies and cockroaches (particularly their legs and tarsi) can serve as a contact source of pathogens which may be readily transferred to food items. Some of these arthropods previously may have visited fecal matter, garbage heaps, animal secretions, or other potential sources of pathogens, thereby further contributing to health risks.

Additional information on insects and other arthropods that can contaminate food is provided by Olsen et al. (1996) and in reviews by Terbush (1972), Hughes (1976), and Gorham (1975, 1991a,b).

FEAR OF ARTHROPODS

Some people detest arthropods, or infestation by them, to such a degree that they suffer from entomophobia, the fear of insects; arachnophobia, the fear of spiders and other arachnids; or acarophobia, the fear of mites (including ticks). Showing concern or disapproval towards the presence of potentially injurious arthropods is probably a prudent and healthy reaction, but phobic behaviors reflect an unusually severe psychological response. Such persons exhibit more-than-normal fear when they encounter an arthropod, often resorting to excessive or obsessive measures to control the problem (e.g., overtreatment of themselves or their homes with insecticides and other chemical compounds).

DELUSORY PARASITOSIS

A relatively common psychological state occurs in which an individual mistakenly believes that he or she is being bitten by, or infested with, parasites. This is called delusory parasitosis, also referred to as delusionalparasitosis or delusions ofparasitosis. This condition is distinct from simply a fear, or phobia, of insects or other arthropods and represents a more deeply rooted psychological problem. This delusory condition is most frequently experienced by middle-aged or elderly persons, particularly women, and is one of the most difficult situations for entomologists to approach.

Remarkable behavioral traits are sometimes attributed to the parasites by victims. These include descriptions of tiny animals jumping into the eyes when a room is entered or when a lamp is switched on. Some victims have failing eyesight; others may have real symptoms from other conditions such as psoriasis that they may attribute to the imagined parasites. Victims become convinced that the parasites are real, and they often consult a succession of physicians in a futile attempt to secure a diagnosis and satisfactory treatment to resolve the problem. Patients typically produce skin scrapings or samples of such materials as vacuumed debris from carpets, draperies, and window sills, which they believe contain the illusive parasites.

Victims of delusory parasitosis often turn to extension entomologists or medical entomologists as a last resort out of frustration with being unable to resolve their condition through family physicians, allergists, and other medical specialists. Because patients are convinced that arthropods are present, they are usually reluctant to seek counseling or other psychiatric help. Dealing with cases of delusory parasitosis requires careful examination of submitted specimens, tact, and professional discretion on the part of the entomologist. Additional information on delusory parasitosis is provided by Driscoll et al. (1993), Koblenzer (1993), Kushon et al. (1993), Poorbaugh (1993), Webb (1993a,b), Goddard (1995), and Hinkle (2000).

TOXINS AND VENOMS

Many arthropods of medical-veterinary importance produce toxins. Notable among these are scorpions, spiders, bees, wasps, ants, and velvet ants; certain beetles (e.g., blister beetles, some rove beetles, and darkling beetles); and caterpillars, cocoons, and adults of various moths. Additionally, antigenic components in saliva released during blood-feeding by arthropods (e.g., certain fleas, ticks, mosquitoes, and chiggers) cause local or systemic reactions in their hosts.

Toxins produced by arthropods represent a wide range of chemical substances from simple inorganic or organic compounds to complex alkaloids and heterocyclic compounds. The term venom refers to toxins that are injected into animal tissues via specialized structures such as stings, chelicerae (fangs), and spines. Venoms are often complex mixtures of toxins and various pharmacologically active compounds that facilitate the spread and effectiveness of the toxic components. They commonly include amines (e.g., histamine, catecholamines, serotonin), peptides, polypeptides (e.g., kinins), specific proteins, and enzymes (e.g., phospholipase, hyaluronidase, esterases) that vary significantly among different arthropod taxa. Depending on what types of cells or tissues they affect, toxins and venoms can be characterized, for example, as neurotoxins, cytotoxins, or hemotoxins. Frequently they cause such symptoms as pain, itching, swelling, redness, hemorrhaging, or blisters, the severity of which is largely dependent on the particular types and amounts of toxin involved.

Further information on arthropod toxins and venoms is provided by Beard (1960), Roth and Eisner (1962), B/icherl and Buckley (1971), Bettini (1978), Schmidt (1982), Tu (1984), and Meier and White (1995).

HOST DEFENSES

Humans and other animals have developed elaborate means to defend themselves against infestation by arthropods and infection by pathogens they may transmit. Both behavioral and immunological responses are used to resist infestation by arthropods. Behavioral defenses include evasive, offensive, or defensive action against biting flies such as mosquitoes, black flies, ceratopogonids, stable flies, and horse flies. Grooming and preening by animals (e.g., biting, scratching, or licldng) are defensive behaviors used to reduce or prevent infestations by ectoparasites and other potentially harmful arthropods. Host immunological defenses against arthropods vary with different arthropods and with respect to previous exposure to the same or antigenically related taxa. Details concerning such host immune responses are beyond the scope of this book, but some general trends are noteworthy. Repeated feeding attempts by the same or antigenically cross-reactive arthropods often lead to fewer arthropods being able to feed successfully, reduced engorgement weights, greater mortality, and decreased fecundity of female arthropods. Widespread arthropod mortality rarely results. For more information concerning the types of host immune responses and cell types involved against various ectoparasites, see Wikel (1996b)

Many blood-feeding arthropods partially or completely counteract the host immune response by inoculating immunomodulators or immunosuppressive compounds into the bite site. In fact, a wide range of pharmacologically active compounds is known to be released at the bite site by various arthropods (Ribeiro 1995). These compounds range from anticoagulants to prevent the blood from clotting, local analgesics to reduce host pain, apyrase to prevent platelet aggregation and promote capillary location, and various enzymes and other factors for promoting blood or tissue digestion. Some of these compounds are perceived by the host as antigens and may elicit an immune response, whereas others can cause localized or systemic toxic responses and itching.

FORENSIC ENTOMOLOGY

Forensic entomology is the study of arthropods, especially insects, associated with crimes and other aspccts of the courts and judicial system. Forensic cntomology usually involves the identification of insects and other arthropods associated with human remains as an aid to detcrmining the time and place of death.

Time of death can often be ascertained based on the ambient temperature and other weather conditions over the preceding days at the crime site and by correlating this information with the developmental rates of key arthropod species present on, or in, the corpse. These arthropods are typically fly larvae, some of which are important primary and secondary decomposers of animal remains. By knowing developmental times and related information for decomposer species at different temperatures, it often is possible to quite accurately estimate the time of death.

The location where a crime took place, if different from the discovery site, also sometimes can be determined based on the presence of unique arthropods with known distributions that do not include the area where the body was found. Similarly, examination of carefully collected insect evidence can aid in solving other crimes (e.g., the origin of drug shipments and sources of vehicles and other accessories used in crimes) in which there is arthropod evidence involving taxa with characteristic geographical distributions.

Further details on the science of forensic entomology are provided by Vincent et al. (1985), Smith (1986), Erzinclioglu (1989), Carts and Haskell (1990), Catts and Goff ( 1992 ), and Golf (2000).

MINOR ARTHROPOD PROBLEMS OF MEDICAL-VETERINARY INTEREST

In addition to arthropod groups detailed in the chapters that follow, a few arthropods in other groups may have minor, incidental, or occasional significance to human and animal health. These include springtails (order Collembola), bark lice (order Pscoptera), walking sticks (order Phasmida), mayflies (order Ephemeroptera), earwigs (order Dermaptera), thrips (order Thysanoptera), caddisflies (order Trichoptera), centipedes (class Chilopoda), and millipedes (class Diplopoda).

On rare occasions, springtails have been recorded infesting human skin (Scott et al. 1962, Scott 1966). Similarly, some bark lice (psocids) are known to cause allergies or dermatitis in humans (Li and Li 1995, Baz and Monserrat 1999). Certain adult mayflies and caddisflies can cause inhalational allergies, especially when they emerge in large numbers from lakes, rivers, or streams (Seshadri 1955 ).

In addition to various hymenopterans, arachnids, and other venomous arthropods detailed in the following chapters, a few miscellaneous arthropods produce venoms that can cause medical-veterinary problems. These include walking sticks (stick insects) and millipedes, some of which utilize venomous defensive secretions or sprays. Defensive sprays of certain walking sticks can cause conjunctivitis (Stewart 1937), whereas defensive sprays of some millipedes contain hydrochloric acid that can chemically burn the skin and can cause long-term skin discoloration (Radford 1975). Centipedes, especially some of the larger tropical species, can cause envenomation when they “bite” with their poison claws (maxillipeds), which are equipped with poison ducts and glands (Remington 1950).

Thrips, which have tubular mouthparts adapted for sucking plant fluids, occasionally pierce the skin and have been known to imbibe blood (Williams 1921, Hood 1927, Bailey 1936, Arnaud 1970). On rare occasions, earwigs also have been recorded as imbibing blood (Bishopp 1961). Bishopp further noted that earwigs have been known to pierce human skin with their pair of caudal pincers (cerci) and may stay attached for an extended period.

Some miscellaneous arthropods inhabit the feathers of birds or the fur of mammals. The exact nutritional requirements of some of these arthropods remain unknown; most of them, however, do not appear to be true ectoparasites. Representatives of two of the three subordcrs of earwigs (suborders Arixeniina and Hemimerina) live in mammal fur. The Arixeniina are associated with Old World bats, whereas the Hemimerina are found on African cricetomyine rodents (Nakata and Maa 1974). These earwigs may feed on skin secretions or sloughed cells, but their effect on the health of their hosts is poorly understood. Other occasional inhabitants of host pelage, such as various beetles, cheyletid mites, and pseudoscorpions, are predators of ectoparasites and are therefore beneficial to their hosts (Durden 1987).

A few arthropods that are not mentioned in the following chapters can occasionally serve as intermediate hosts of parasites that adversely affect domestic and wild animals. These include certain springtails andpsocids (bark lice) as intermediate hosts of tapeworms (Baz and Monserrat 1999).

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