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User:Alan R Walker/draft article on Insects of domestic animals

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Insects of domestic animals

Insects that infest and parasitize domestic animals cause direct parasitic damage to their hosts and also transmit many types of pathogenic organisms that cause disease. This article introduces this varied topic from a veterinary perspective about categories of disease caused to livestock and companion animals, illustrated by specific examples. There are many methods of controlling these diseases that farmers, animal health assistants and veterinarians can apply. The variety of insects involved is large and their taxonomy is complex but more taxonomic and epidemiological detail will be found using the list of Further reading. The categories of disease do not correspond closely to the taxonomic categories of the insects; many groups are responsible for several modes of disease. Most of these insects are ectoparasites (feeding at the outer surface of their hosts) but some are endoparasites during their larval stages. The term micro-predator is sometimes used for those biting flies that are not resident on their host.

Cochliomyia hominivorax (Coquerel 1858) New World screw-worm fly. Phylum Arthropoda, Class Insecta, Order Diptera, Family Calliphoridae


Groups of insects causing disease in domestic animals edit

Felicola subrostratus louse of cats, immature stage of louse with egg glued on hair

Insects (class Insecta, sub-phylum Hexapoda, phylum Arthropoda) are defined as invertebrate, segmented, animals with a jointed chitinous exoskeleton, with a body divided into head, thorax and abdomen; the head bears a pair of eyes and a pair of antennae, and the thorax bears three pairs of legs[1]. They are distinct from the ticks and mites of class Acari in the Arthropoda, but which cause many similar diseases in domestic animals. There are three orders of insects causing disease in domestic animals: Diptera – the true flies; Siphonaptera - the fleas; and Phthiraptera - the lice. The taxonomy of lice is complex and the order Phthiraptera is paraphyletic, (comprising groups of separate origin) with the sub-orders Anoplura, Ischnocera and Amblycera important to domestic animals.

Stomoxys calcitrans stable-fly, complete metamorphosis, anti-clockwise - eggs, larvae, pupa, adult

Typical life-cycles edit

Incomplete metamorphosis edit

All lice have a life-cycle as follows[2]. Eggs are laid on the host by the female individually attaching eggs to a hair or feather of its host with a secreted glue. Such eggs are often called nits and are useful in preliminary diagnosis. Larvae hatch from the eggs, feed, and when they reach maximum size allowed by their exoskeleton they molt into a nymph. Several nymphal stages follow. The larvae and nymphs are similar in form to the adults. The final molt will produce an adult as a reproductively functional female or male. These stages (or instars) all occur on a single host. Transfer between hosts is by crawling between hosts in close contact. Although few eggs are laid by a female, they are large, well protected and hatch on the host. Thus survival of eggs and subsequent stages is high and dense infestations of lice can build up if a host is unable to resist them.

Ctenocephalides' flea larva
Ctenocephalides adult flea

Normal complete metamorphosis edit

Most flies and all fleas have the same type life-cycle, and that of fleas is a useful example[3]. Female fleas lay smooth slippery eggs that fall to the ground. Larvae hatch from the eggs and live amongst debris on the ground or resting site of their host such as a dog kennel. The larvae are worm-like, with a form substantially different from the adults. The larvae feed on organic debris and dry pellets of flea-dirt excreted by adult fleas. Flea-dirt is semi-digested blood of the host. When the larva has developed through three molts it then becomes immobile and develops into a pupa. The transformation from larva to adult through the changes within the pupa is a complete metamorphosis. The new adult will seek a host and may spend much of its life their, but can easily crawl and jump between hosts. All dipteran flies have a complete metamorphosis and the commonest pattern is for the blood-feeding female to lay repeated batches of eggs of several hundred each and for the larvae to develop as free-living animals in a habitat separate from that of the adults. In this case the reproductive rate is high but the survival rate of offspring is low. Some blood-sucking flies, such as mosquitoes and biting midges, have a distinct cycle of feeding and laying eggs, called a gonotrophic cycle, in which a single large blood meal is converted into a batch of eggs, then another blood meal is sought to support the next batch of eggs, and so on for as long as the female can survive.

Melophagus ovinus sheep ked female and pupa

Larviparous form of complete metamorphosis edit

Flies within the families Hippoboscidae (louse flies) and Glossinidae (tsetse) have a specialized life-cycle[1][4]. The female permits one egg at a time to be fertilized from the male's spermatozoa that was delivered and stored previously. This egg remains within the female, then the larva hatches and receives nutrition directly from the female. The female supports this by repeated blood-meals from its hosts. The larva slowly gains a mass greater than that of the female and is laid as a soft mobile larva. With louse flies this larva remains on the host and forms into a pupa. With tsetse the larva is laid on sandy soil where it rapidly burrows and forms into a pupa. The adults that develop in and emerge from the pupae have undergone a complete metamorphosis. The reproductive rate is low but the survival rate of the offspring is high with this type of reproduction.

Some species of dipteran flies have adapted to feeding on blood of their hosts[5]. Usually it is only the females that are blood-feeders; the males feed on plant nectar or in other non-parasitic ways. The Glossina and Stomoxys flies are examples of where both sexes take frequent blood meals during their adult lifetime. Blood-feeding by female insects is used primarily to support production of eggs or in special cases, larvae.

Glossina morsitans adult tsetse fly

Types of disease caused by directly by insects as parasites edit

Biting stress and loss of body condition edit

Infestations of dipteran flies can accumulate severely under favorable environmental and seasonal conditions. The larvae of Stomoxys stable flies for example develop in the mixtures of cattle dung and straw typical of where cattle are gathered in building. Bites of adult Stomoxys to obtain blood-meals are painful and reduce gain in cattle weight or milk production[6]. Similar stress is caused, often seasonally, by flies in the families Simuliidae (blackflies) Tabanidae (horseflies), Culicidae (mosquitoes), Ceratopogonidae (biting midges), Hippoboscidae (louse flies) Haematobia (horn flies), and others. The large tabanid flies have complex slicing and piercing mouthparts that create a wound from which blood flows. The blood is then imbibed from the sponge-like labella. The minute Culicoides midges have similar mouthparts – making their bites disproportionately irritating. The loss of blood caused by these flies can be a direct cause of lost production, but the disturbance to normal feeding and resting behavior is more important. Cattle and sheep congregate together tightly to protect themselves from biting flies (known as fly syndrome); doing so they suffer heat stress and do not graze. Infestations of this type tend to be difficult to control because their source relates to habitats of the insect's larvae dispersed in the environment and because usually the adult blood-feeders are individually on the host only for a short time[7].

Haematobia horn fly infesting a cow
Simulium blackfly adults, scale in millimeters

In contrast lice infest their hosts continually. Each species of louse has a close association with one or several similar species of host. Host-specific adaptations include body form and feeding apparatus that physically fits the host, and feeding mechanisms and salivary components that reduce resistance reactions from their hosts[2]. For example the shape and size of the mouthparts of chewing lice fit closely the size and texture of their specific host's hairs or feathers. Healthy and uncrowded livestock animals usually resist high infestations by lice. When confined over winter in housing, or in a state of poor nutrition, or with concomitant infections with parasites, such animals can accumulate numbers of lice that will directly reduce condition by irritation and blood loss[8]. Such lousiness causing clinical disease is known as pediculosis. Similar conditions develop with companion animals that are not cared for adequately. Lice on poultry raised intensively are a particular problem. Birds have numerous species of ischnoceran and amblyceran lice adapted to feed on them, all with a feeding mechanism known as chewing. Their mouthparts are structured for rasping at the dead layers of skin or feather shafts, although some species will feed on blood exuding from small wounds. Heavy infestations of these often large actively crawling lice irritate the birds and depress their productivity.

Culex adult female mosquito
Tabanus adult horsefly

Fleas may cause severe biting stress in some circumstances[9]. The infestation of the host is associated with the habitat of the larvae, situated in the resting site of the host. Populations of fleas can accumulate to such large numbers, where flocks of goats for example, are tightly housed at night, that severe debilitation is caused by biting stress. In less extreme cases dogs and cats kept in poor conditions can suffer greatly from constant high level of irritation from flea bites.

Linognathus sucking lice infestation of a cow

Allergic reactions edit

Flea bite allergy, typically in dogs, is the best studied example of allergy caused by biting insects[10]. The dog flea Ctenocephalides canis is a common cause, and often the cat flea Ctenocephalides felis, which has adapted well to feeding on dogs, are responsible. Another allergy is called sweet-itch in horses, caused the blood-feeding of Culicoides biting midges[11]. Insect saliva contains many proteinacious components to aid the flow of blood. Being foreign to the host, they are antigenic and likely to induce inflammatory and hypersensitive responses in the skin of the host. These cutaneous hypersensitivities are usually type 1 (immediate) and type 4 (delayed). The resulting allergies manifest as inflammation, edema, exudation of serum, induration, and crusting or scabbing of the skin, with associated intense pruritus. These dermatitis reactions are usually confined to the sites of feeding of the insects.

Menacanthus chewing louse of poultry

Skin and hide damage edit

Blood-feeding by insects damages the skin at least slightly, but costly damage is caused in complex ways. Anopluran lice and mosquitoes have blood sucking tubes composed of separate elements that can move independently so that the tube can delicately seek out a capillary with little direct damage to the skin[2]. But the saliva secreted at the feeding site will induce inflammation and immune reactions. The blood-sucking lice such as Linognathus of cattle cause damage to the dermis of their hosts associated with immune reactions in the skin that lead to a natural wound healing with slight scarring. The feeding activity of the chewing lice may also cause reactions in the skin leading to hide damage[12][13]. These scars show up during and after processing of hides for leather, reducing the cash value of the products. (Similar damage is caused by feeding of ticks of domestic animals.) The flesh-eating larvae of myiasis flies damage the skin in large superficial patches or by discrete holes when they emerge through the skin as fully developed larvae prior to pupation (see below).

Culicoides imicola biting midge

Flesh-eating larvae (myiasis) edit

Some species of dipteran flies have larvae that infest the flesh or skin of their hosts, such infestation is called myiasis[1][2]. The adults of these flies are always free-living and cause no direct damage. There are two functional types. The green-bottle flies, Lucilia sericata and L.cuprina, are examples of an optional type, known as facultative myiasis. These types of fly are generally known as blow-flies and the myiasis they cause is called blow-fly strike. The natural life-cycle has the adult female seeking out and laying eggs on carcasses of freshly dead animals (carrion). The larvae feed on the rotting flesh until ready for pupation, when they leave the carcasse. But the females will also lay eggs at bacterially contaminated areas of skin or small wounds on their host and the larvae will feed on this live skin and subcutaneous tissue. Sheep may be fatally poisoned by ammonia produced as an excretory product of the larvae.

The other functional type is known as obligate myiasis, in which the adult female seeks out only a living host to lay eggs on[14]. Less specialized obligate flies, similar to the blowflies above, include the screw-worm fly of South America, Cochliomyia hominivorax, and the equivalent fly in Africa, Chrysomia bezziana. These parasitize cattle as larvae. Screw-worms are named after their similarity to carpenter's screws and the way they burrow superficially into the flesh. The resulting wounds containing densely packed larvae from an entire batch of eggs are severe and may lead to fatal septicemia. More specialized obligate flies are the bot and warble flies, in which the larvae are adapted for deep burrowing whilst the adults have no functional mouthparts and depend of food reserves built up by the larvae for their host seeking and reproduction. The adult flies resemble bumble bees and some species are recognized by cattle, which may then panic and damage themselves. The Hypoderma warble-flies of cattle, and Gasterophilus stomach bots of horses, are important examples. The female lays eggs and glues them to hairs on the host's legs. The larvae of Hypoderma hatch and immediately burrow into the skin of the leg. They burrow through muscles and grow until emergence through the skin of the back of the host a year later. The larvae of Gasterophilus crawl on the skin from where they are groomed by the horse licking. The larvae then penetrate the tissue of the mouth and eventually settle attached to the inner lining of the stomach. When mature they detach and are voided with the feces. In South America the torsalo, Dermatobia hominis, is a serious pest of cattle. As its name shows, it is also a threat to humans. The adult flies lay their eggs on mosquitoes and when the mosquito feeds on a suitable host the larvae emerge rapidly and burrow through the skin. The larvae remain and develop where they initially infested until ready to pupate when they emerge through the skin. Infestation of cattle leads to downgrading of meat and hide products. There are numerous species of fly causing myiasis in domestic and wild animals, with some highly specific host associations. For example Asian elephants (Elephas maximus) have Elephantoloemus indicus myiasis flies specialized to parasitize them[15].

Chrysomya bezziana Old World screw-worm fly and larvae, scale in millemeters

Pathogen transmission and diseases caused edit

Hyoderma warble larvae in skin of host
Dermatobia hominis larval infestation showing as the cluster of lumps on shoulder of a cow

Pathways of transmission edit

The insect that transmits is known as the vector of the pathogen. An insect (or tick or mite) that acts as a vector does so whilst it is parasitizing its host. So a vector is distinct from an intermediate host in the life cycles of many parasites, where the intermediate host is not itself a parasite. By definition, the pathogen is likely to cause disease in its hosts, although an infection may remain sub-clinical. There are two main mechanisms whereby pathogenic organisms are transmitted from one domestic animal to another. Mechanical transmission is the term for a contaminative pathway where the organism is carried between hosts on the mouthparts of the insect. For example the bacterium Moraxella bovis that caused kerato-conjunctivitis or pink-eye of cattle, is transmitted on the sponging mouthparts of various species of Musca flies that feed on lachrymal and other secretions of mammals[16]. Protozoan parasites of the blood of cattle and buffalo, such a Trypanosoma evansi, are transmitted during blood-feeding by tabanid flies[17]. The host's blood remains on the sponging part of the mouthparts. These flies are easily disturbed by their host during feeding and will interrupt their feeding to go to another host, with fresh blood on their mouthparts. In mechanical transmission there is neither development of the pathogen in the tissues of the insect, nor long-term residence of the pathogen in the insect vector.

Tabanus horse-fly mouthparts, left to right: palp, sponging labella, piercing mandibles and maxillae

Biological transmission occurs where the pathogens are adapted to infect the tissues of the insect and develop there. This produces sufficient pathogens for a potent infective dose in the next host. For some pathogens, for example Plasmodium species, this also permits the advantages of sexual reproduction within the vector. However, there is a disadvantage in biological compared to mechanical transmission: if the environment is harsh there may be few gonotrophic cycles and insufficient time for replication of the pathogen to an infective dose. An example is the transmission of bluetongue virus by Culicoides midges (see below and the diagram)[18][19].

It is the pathogens that exploit the insect vectors, by adapting to the insect's physiology, so that the pathogens can maintain and disseminate their populations. In some cases the vectors suffer reduced viability from these pathogens, which can be a significant factor in the epidemiology of the diseases[5].

Trypanosoma evansi protozoa in blood

Viral diseases edit

An example is the virus of bluetongue disease of sheep and cattle transmitted by biting midges such as Culicoides variipennis in the Americas and C.imicola in Africa and Europe[20]. Of the 1000 plus species of Culicoides only six are proven to be used by the virus in its transmission from host to host. The virus particles transfer from the blood freshly imbibed by a female midge into digestive cells of the midge's gut. Then they break free of the gut into the hemocoel (an open blood circulation system) of the midge. There they contact the salivary glands and penetrate the saliva secreting cells. At this site considerable multiplication of the virus occurs. Virus is shed into the saliva and may infect another host during subsequent blood-meals. Midges, being small, only live for several weeks and undergo few gonontrophic cycles. The ability of virus to transmit from one mammal host to another depends on its ability to replicate sufficiently whilst the female midge is capable of seeking new hosts. Eggs and larvae of midges do not become infected by bluetongue virus so there is no transmission of the virus from generation to generation of midge, and in many countries the adult midges are absent during cold or dry seasons. This virus survives for up to six months in cattle, so these hosts can act as overwintering reservoirs of infection even if they are suffering little clinical disease.

Transmission of bluetongue virus by Culicoides. The sequence occurs over several weeks

Bacteria edit

Instructive examples are Anaplasma marginale and A. centrale. These are bacteria that infect red blood cells of cattle, buffalos, sheep and camels and cause considerable loss of production and deaths. They are transmitted biologically by ticks of such as Rhipicephalus decoloratus and R.microplus (see Ticks of domestic animals for photograph). Also they can be transmitted iatrogenically, for example by multiple-use injection needles. However, in many cases tabanid flies are responsible for much transmission, by the mechanical route already described above[21].

Protozoa edit

Trypanosomiasis, in its various forms, is a notorious disease of humans, cattle, buffaloes, camels and horses in most of the tropics[22]. Glossina morsitans transmitting Trypanosoma congolense between cattle in Africa is a used as example. Trypanosomes in a fresh blood-meal are soon passed with the mass of blood into the main digestive and absorptive mid-gut area and initially are confined there by the peritrophic membrane which is continually secreted by the proventriculus of the gut as a sheath protecting the digestive cells. The trypanosomes replicate and differentiate within the space of the peritrophic membrane and they also penetrate through this membrane and develop outside it but still within the gut. By three weeks after initial infection of the tsetse the trypanosomes have migrated up the gut to the inner surfaces of the blood-sucking mouthparts. They continue to replicate there and will be flushed out by salivary secretions into other hosts during subsequent blood meals. This transmission occurs in both sexes of tsetse, but the female flies can survive for up to 15 weeks compared to 6 weeks for males. Trypanosoma brucei, which causes human sleeping sickness has a similar biological cycle, but also including invasion and replication in the salivary glands.

Dirofilaria immitis microfilaria larva in blood. (Scale: grey circles are erythrocytes)

Helminth worms edit

Heartworm disease of dogs, also cats, is the example here[23]. It is caused by Dirofilaria immitis (class Nematoda) and transmitted by mosquitoes in the genera Aedes, Anopheles and Culex. The large adult worms live in the pulmonary arteries, and right atrium and right ventricle of the heart. An infection with many adult worms causes congestion of blood pumping. Reproduction of the worms produces larvae in the form of minute microfilariae which are released by the adult female worms to circulate in the blood of the dog. There is a distinct periodicity of this circulation that coincides with the feeding activity of the mosquitoes at night and in the warm / wet season. When ingested by the mosquito the microfilariae penetrate from the gut into the hemocoele and then directly into the inner parts of the blood-sucking mouthparts from where they are infective to new hosts. Other filarioid worms causing disease in cattle and horses are in genera such as Parafilaria and Stephanofilaria.

Options for control edit

Application of insecticides edit

Methods to control these parasites are numerous and with many variations depending on insect, host and local environment. A few examples follow to demonstrate principles; more detail will be found in Wikipedia on specific pesticide chemicals and in Further reading.

The scope for application of insecticides to the sites where free living larvae live is limited because the sites are usually too diffuse or large for this to be cost-effective. One exception is the larvae and pupae of fleas living in household carpets and furniture, or pet's bedding[24]. Insecticides such as the fenoxycarb (a carbamate) are used for this.

A specialized control method in the insect's environment is the use of targets like cloth flags to attract tsetse adults in their dry savanna habitats in Africa[25]. The targets are colored a specific shade of dark blue, may have an additional odor attractant with them, and are treated with deltamethrin (a synthetic pyrethroid) that is capable of delivering a fatal dose after a momentary contact with a tsetse[26]. Another form of target is cattle sprayed with insecticide specifically against the tsetse attracted to them. The same principle is sometimes used to control tabanid adults. Tsetse are also controlled in large regional schemes. These use a combination of clearing the vegetation types that the adult tsetse need as protective micro-climates, application of insecticide to the same vegetation by hand spraying or use of aircraft, and insecticide treated targets[27].

Usually insecticides are applied to the hair coat of the affected hosts[2][28][29]. Synthetic pyrethroids (such as permethrin and cypermethrin) are typically used for this, either because of their high toxicity specifically to the insects, also because of a repellent effect. The triazine derivative cyromazine is used against blowfly larvae. To reduce costs of repeated applications various self-applicator systems for cattle have been invented to deliver the insecticide. Insecticides are also delivered to specific sites on a host where they will have more effect using hand-held aerosol sprayers or with plastic ear tags for cattle and collars for dogs to apply insecticide for fly control and flea control respectively. Concentrated active ingredient of the insecticide is incorporated into the matrix of the plastic, from where is slowly diffuses onto the host's hair coat.

For the more resident infestations of fleas, and the strictly host resident infestations of lice, the insects can either be contacted directly by topical application of insecticides or by systemic application of chemicals that affect the insects as they feed[30]. When treating cats for ectoparasite infestation it is crucial that only products specifically licensed for cats are used, other products may be dangerously toxic to cats. Topical formulations against fleas include fipronil (a phenylpyrrazole) and lufenuron (a benzoylphenyl urea); and against lice include amitraz (a formamidine) and permethrin (a synthetic pyrethroid).

Systemic application of insecticide has also been used for country-wide eradication of Hypoderma myiasis larvae in cattle. Originally an organophosphate insecticide was applied in an oily formulation along the backline of the cattle so that it penetrated through the skin and spread through the vasculature to other tissues where larvae were situated. Now avermectin systemic insecticides can be used against myiasis larvae.

Biological and management methods edit

The most dramatic example was the eradication from the USA and countries in Central America of the screw-worm fly, Cochliomyia hominovirax, by sterile insect technique[31]. The fly larvae were reared on factory scale by feeding them on meat product from slaughterhouses. The insects were sterilized by gamma radiation then released in massive numbers so that the field population of flies was swamped with males. Since the females are unreceptive after the first mating, so many field females were rendered unable to fertilize their eggs that the populations died out.

Hygiene measures against flea larvae include using vacuum cleaners, general maintenance of clean conditions and a dry atmosphere in human and pet housing. Lice infestations on dogs and cats are detected and reduced by grooming using a special fine-toothed comb, which will destroy eggs glued to hairs as well as the active lice. Self-dusting by birds is a defense against lice and can be aided by provision of diatomaceous earth[32]. The dust abrades the cuticle of lice, caused death by dehydration. The larvae of Stomoxys stable flies live in the mixtures of cattle dung and straw common on dairy farms. If these are removed the fly infestations are reduced.

Drugs and vaccines against transmitted pathogens edit

Administration of drugs, either prophylactically or to treat current infections, and mass vaccination of susceptible livestock, is often the most cost-effective approach when available, rather than vector control. Heartworm in dogs is controlled by daily oral administration of the anthelminthic drug diethylcarbamazine. Clinically obvious infections with Anaplasma bacteria are widely controlled directly in the hosts by administration of tetracycline antibiotic and the drug imidocarb[33]. In some countries vaccines are available that use attenuated live cultures of the Anaplasma, or killed bacteria. Bluetongue disease in sheep and cattle is controlled by prophylactic vaccination using killed virus preparations that are available as mixtures against various serotypes of the virus[34]. Much research effort is directed at inventing synthetic antigen vaccines against various transmitted pathogens. Such vaccines would be easier to store and administer, and avoid possible problems with inducing sub-clinical carrier infections in livestock when live pathogen vaccines are used. However, there are great technical difficulties to be overcome in development and deployment of such vaccines.

References edit

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  31. ^ Krafsur, E.S. (1998). Sterile insect technique for suppressing and eradicating insect populations: 55 years and counting. Journal of Agricultural Entomology 15: 303-317. [11]
  32. ^ Martin, C.D. (2012). Housing and dustbathing effects on northern fowl mites (Ornithonyssus sylviarum) and chicken body lice (Menacanthus stramineus) on hens. Medical and Veterinary Entomology 26: 323-333. doi:10.1111/j.1365-2915.2011.00997.x
  33. ^ Coetzer, J.A.W. (2004) Infectious Diseases of Livestock. Oxford University Press, ISBN 0-19-57820-2X.
  34. ^ Noad, R. (2009). Bluetongue vaccines. Vaccine 27: D86-D89. doi:10.1016/j.vaccine.2009.08.037

External Links edit

Further reading edit

  • Colwell, D.D. (2004) The Oestrid Flies: Biology, Host-parasite Relationships, Impact and Management. Wallingford, CABI Publishing, ISBN 0-85199-6841
  • Drummond, R.O. (1988) Control of arthropod pests of livestock: a review of technology. Boca Raton, CRC Press.
  • Lancaster, J.L. (1986) Arthropods in Livestock and Poultry Production. Chichester, Ellis Horwood Ltd. ISBN 085312-790-5.
  • Mullen, G.R. (2009) Medical and Veterinary Entomology. Burlington, Academic Press, ISBN 978-0-12-372500-4.
  • Taylor, M.A.,(2007) Veterinary Parasitology. Oxford: Blackwell Publishing, ISBN 978-1-4051-1964-1.
  • Walker, A.R. (1994) Arthropods of Humans and Domestic Animals: a guide to preliminary identification. London: Chapman & Hall, ISNB 0-412-57280-X.
  • Wall, R. (2001) Veterinary Ectoparasites: biology, pathology & control. Oxford: Blackwell Science Ltd, ISBN 0-632-05618-5.
  • Zajac, A. (2012) Veterinary Clinical Parasitology. Chichester: Wiley – Blackwell, ISBN 0-8138-2053-8.
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