Phthiraptera (Chewing and Sucking Lice)

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Phthiraptera

(Chewing and sucking lice)

Class Insecta

Order Phthiraptera

Number of families 24

Evolution and systematics

It generally is accepted that lice (Phthiraptera) are derived from the insect order Psocoptera (the so-called book lice or bark lice), and speculative estimates place their origin between the Late Carboniferous and the end of the Cretaceous, 66–320 million years ago. With the exception of a louse egg found in Baltic amber and a louselike insect from the Lower Cretaceous of Transbaikalia in Russia, there are no fossils that might provide direct information on the evolution of lice. The host distribution of lice is, however, analogous in some ways to a fossil record.

The order Phthiraptera comprises four suborders, three of which (the Amblycera, Ischnocera, and Rhynchophthirina) are known as chewing or biting lice and the fourth (the Anoplura) as sucking lice. All species of Anoplura and Rhynchophthirina are restricted to mammals, whereas species of Ischnocera and Amblycera are known from both mammals and birds. Sucking lice and the so-called elephant and warthog lice (suborder Rhynchophthirina) are one another's closest relatives and share more derived morphological features. These have a common ancestor with the Ischnocera and together form a sister taxon to the most basal louse suborder—the Amblycera.

By 1999, 4,384 valid species of chewing lice had been recorded from 3,910 different hosts (3,508 bird and 402 mammal species). The sucking lice are a much smaller group and, as of the year 2002, 543 valid species were described from 812 different species of mammals. These figures are a small fraction of the true species diversity among lice, and many new species await formal description or discovery.

Physical characteristics

Lice are wingless, typically flat-bodied insects with three to five short, segmented antennae, highly modified mouthparts, and six relatively short legs modified for clinging to their host's feathers or pelage. Their size ranges from just 0.01 in (0.3 mm) long for the nymphs of some Hoplopleura (Anoplura) species on rodents, to 0.4 in (11 mm) for the giant adults of Laemobothrion (Amblycera) from birds of prey. Within many host groups there is a strong correlation between the size of the host and the size of their lice. Sexual dimorphism also influences louse size and is evident in many species, with females typically 10–20% larger than males.

The body is dorsoventrally flattened, with a horizontally positioned head. These are adaptations for lying flat against

a hair shaft or between feather barbules, and they reduce the chance of the louse becoming dislodged during grooming or preening by the host. Coloration varies from pale white through shades of yellow and brown to black. Patterns are evident on some species, and cryptic coloration sometimes is employed, allowing the louse to match the coloration of its host's plumage or pelage.

Lice have mandibles that have been variously modified in each of the suborders. Asymmetric opposing mandibles are present in Amblycera and Ischnocera. In Amblycera, the mandibles articulate horizontally from the head, whereas in Ischnocera, the mandibles articulate vertically. These mandibles are involved in feeding and play a vital secondary role in anchoring the louse to the host. Within the Rhynchophthirina, the mandibles are much reduced, occurring at the end of a long rostrum and articulating outward rather than opposing each other. In most Anoplura, the mandibles have been completely lost. However, some species have tiny mandibular vestiges present internally within the anterior section of the head. These vestiges are just one of the many characters that highlight the common ancestry of chewing and sucking lice.

Distribution

As permanent, obligate (host-specific) ectoparasites, lice have distributions that essentially mirror those of their hosts, with very few exceptions. As such, they are found worldwide and are present on every continent and in virtually every habitat occupied by birds and mammals. All orders and most families of birds have records of host-specific lice; of the few groups that do not, it is likely either that their lice are extinct or that the hosts have been searched insufficiently. Similarly, all major groups of mammals have lice, with the exception of species belonging to the orders Chiroptera (bats), Cetacea (whales and dolphins), Microbiotheria (Chilean colocolos), Monotremata (echidna and platypus), Notoryctemorphia (marsupial moles), Pholidota (pangolins), and Sirenia (dugongs and manatees).

Within the range of a host species, louse distribution often is patchy, and not every individual harbors all the lice previously recorded from the host. A true geographic distribution within the range of a host also has been noted for some species of lice. The size of a louse population varies enormously on different individuals, sometimes seasonally. Sick animals and, in particular, birds with damaged bills or feet may have abnormally large numbers, owing to their inability to groom or preen effectively.

Habitat

All lice complete their entire life cycle from egg to adult on the body of the host. The constant temperature and relative humidity that this environment affords lice may account for their success on mammals and birds. This seemingly uniform environment is, in fact, a series of interconnected microhabitats, and different species of lice are morphologically and behaviorally adapted to exploiting these niches on their host. This allows several species of lice to coexist on the same host species. These microhabitats are most evident on birds and are partitioned by the different feather types present on the wings, back, head, and rump. The differential ability of birds and mammals to preen or groom various parts of their bodies also exerts a major selection pressure on louse morphological characteristics and influences the microhabitat occupied by most lice. Extreme examples are the species of Piagetiella (Amblycera), which live inside the throat pouches of pelicans and cormorants, feeding on blood and serum within the pouch, but return to the head feathers to lay their eggs. Some species of Actornithophilus (Amblycera) have adapted to living inside the quills of wing feathers, thus completely escaping the effects of preening by their shorebird hosts.

Most species of lice are highly host specific, restricted to a single host species or a handful of closely related hosts. In several cases, host specificity extends to the host subspecies, and for this reason it often is possible to judge the identity of the host from the assemblage of lice present on its body. There are some notable exceptions to this trend, and a few louse species are recorded from hosts spanning several bird or mammal orders. There are also many anomalies in host-louse associations that can be explained only by accepting that there has been some interchange of lice between major host groups. For example, Trichophilopterus babakotophilus from Madagascan lemurs is a species of ischnoceran louse that belongs to a group otherwise restricted to birds. Similarly, Heterodoxus spiniger (Amblycera) on the domestic dog and other carnivores is a secondary infestation derived from an Australian marsupial. Thus, the axiom of strict host specificity that once was thought to be the rule of host-louse associations is a generalization, for which there are exceptions.

Behavior

Observations on the behavior of lice are limited to generalizations obtained from a few louse species. Amblyceran lice typically are more mobile than the other louse suborders, and some species are known to make short forays away from the host. For the majority of species, however, remaining attached to the host is critical for survival, and lice have a variety of behavioral and morphological adaptations to ensure that they never become parted from their host, except during dispersal. Wing lice of birds escape preening by inserting between feather barbs of the wing feathers, and there is a strong correlation between the size of the interbarb space and the size of the lice for different host and louse species. Similarly, "fluff lice" that occupy the fine feathers close to the abdomen, escape the preening activity of their hosts by burrowing down into the downy basal regions of these feathers. Lice grip feather barbs or hair shafts with the aid of their tightly locking mandibles. Even when dead, the dried exoskeletons of lice can remain fixed firmly to the host's body and frequently are recovered from museum collections of mammal and bird skins, long after the death and preservation of the host.

Successful transmission is perhaps the greatest challenge faced by any parasite, and lice are no exception. Direct physical contact between host individuals remains the principal route of dispersal for lice within a host species. Shared nest holes and nest material, predator-prey interactions, and mixed species use of dust baths all provide opportunities for dispersal to a new host species. Arguably the most unusual means of dispersal between hosts involves hitchhiking on the abdomen of hippoboscid flies, a phenomenon known as "phoresy." Records of phoresy are relatively common for louse species belonging to the ischnoceran louse genera Degeeriella and Brueelia but are rare for other taxa, and this is unlikely to represent a major means of dispersal for most lice.

Feeding ecology and diet

Specializations in the diet of lice underpin their major taxonomic divisions. The Anoplura, or sucking lice, are the only group that feeds exclusively on mammalian blood, drawn up from small vessels located close to the surface of the host's skin. Small buccal teeth are used to pierce the skin's surface, and a bundle of sharp stylets are extruded from the haustellar sheath of the louse into the host. This flexible bundle can be driven in different directions until a suitable blood vessel is located. Once the tip of the bundle enters a vessel, feeding can commence. The other three louse suborders possess a pair of distinct mandibles.

Rhynchophthirina (elephant lice and their relatives) have mandibles located at the end of a long rostrum. They each have been rotated 180 degrees so that they articulate outward, rather than oppose each other. Thus, Rhynchophthirina cannot "bite" or "chew" in the traditional sense of the word, but instead they use the sharply serrated mandibles to rasp at the skin, allowing a pool of blood to form that is sucked up through an opening at the end of the rostrum. These are true pool feeders (telmophages), unlike the vessel-feeding Anoplura (solenophages).

All species of avian Ischnocera are believed to feed exclusively on feather barbules, the remains of which usually can be seen in crops of specimens that have fed recently. These are sheared from feathers by toothed mandibles. Mammalian Ischnocera (family Trichodectidae) feed on skin debris and hair (although this is disputed by some researchers), and at least one species is known to take blood meals. Amblycera have more generalist feeding habits, and in addition to feathers or hair, are known to feed on flakes of dead skin, blood, and skin secretions. Most chewing lice that do not partly blood-feed have an efficient water-vapor uptake system that extracts water from the atmosphere. For this reason, these species are particularly sensitive to the ambient humidity.

Reproductive biology

Lice are difficult to study under natural conditions, and for this reason most information on the bionomics of lice (i.e., their relations with other organisms and the environment) is obtained from in vitro studies, with the attendant disadvantages of applying laboratory results to natural situations. Separate male and female sexes are known for most louse species, but a few species reproduce parthogenetically. Lice eggs are attached to feather barbs; to hairs; or, in the case of the human body louse, to projecting clothing fibers with a drop of glandular cement. This surrounds the substrate and the base of the egg. Eggs, also known as nits, usually are attached close to the host's skin and remain firmly fastened as the feather barb or hair grows outward. Typically whitish in color, the eggs require four to 10 days of incubation before hatching, depending upon species and ambient temperature. When the nymph is ready to hatch, air is drawn in though the mouth and accumulates behind the nymph. When sufficient pressure is reached, the caplike operculum on the noncemented end of the egg is forced open, and the first-stage nymph crawls out. Three nymphal stages follow, each lasting three to 12

days. In some cases the first-stage nymphs, while lacking functional genitalia, may be miniature versions of the adult; in others, the nymphs successively become more adultlike through each instar (developmental stage). Adult lice live for about one month, and a female human body louse may produce 50–150 eggs during her lifetime.

Conservation status

It is seldom appreciated that the extinction of a mammal or bird species also results in the extinction of all associated host-specific parasites. The extreme host specificity of lice, along with other ectoparasite groups, such as feather mites and fleas, leaves them particularly vulnerable to co-extinction. At least eight species of lice were known to be extinct by 1990, and this is almost certainly a gross underestimate of true loss of louse species diversity within the past century. Perhaps as the result of ignorance or the negative human perception of parasites, just one louse species (Haematopinus oliveri—an anopluran whose host species is the pygmy hog, Sus salvanius) is listed on the IUCN Red List of threatened species as of 2002, yet this same list defines 185 bird and 184 mammal species as Extinct in the Wild or Critically Endangered. If we assume that these species have an average rate of host-specific louse infestation, there are at least 50 species of lice that face a significant and immediate threat of extinction within the next 10 years.

Significance to humans

The human body louse (Pediculus humanus "humanus"; quote marks are used to indicate that this is not considered a valid taxonomic species) is the principal vector for Rickettsia prowazekii, which causes louse-borne typhus; Bartonella quintana, which causes trench fever; and Borrelia recurrentis, which causes epidemic or louse-borne relapsing fever. Epidemic and endemic infections can occur in conditions that foster the prevalence of lice, such as among homeless populations, in refugee camps, and during times of war or natural disasters. Humans can be infested with the human head louse (Pediculus humanus "capitis"), which is confined to the scalp and is common among schoolchildren worldwide, or the pubic louse (Pthirus pubis), which normally is transmitted through sexual contact.

Lice are important pests of domesticated mammals and poultry, and while modern insecticides have proved highly effective at controlling louse infestations, concerns over the safety of these chemicals, insecticide resistance, and the difficulty of treating large numbers of animals on a regular basis mean that lice will continue to be a major problem for livestock farmers. In 1994, for example, lice cost the Australian sheep industry an estimated $100 million U.S. dollars through lost production and control costs. Similar losses are likely in other countries where sheep, cattle, or poultry are farmed intensively.

Species accounts

List of Species

Elephant louse
Wandering seabird louse
Human head/body louse
Slender pigeon louse

Elephant louse

Haematomyzus elephantis

family

Haematomyzidae

taxonomy

Haematomyzus elephantis Piaget, 1869. Type host: Loxodonta africana.

other common names

None known.

physical characteristics

Distinct triangular head with the pre-antennal region elongated into a long rostrum bearing a pair of outward-facing mandibles. Short, broad thorax without a sternal plate and long, slender legs with a single serrated claw.

distribution

Restricted to the Indian and African elephant but not recorded throughout the host's range and less common on African elephants.

habitat

Common on the more hairy regions, especially in folds of soft skin of juvenile elephants. They are most common on the ears, groin, or axilla (armpits) or at the base of the tail.

behavior

Nothing is known.

feeding ecology and diet

Sharp, outward-facing mandibles rasp at the surface of the skin, causing blood to flow. The louse sucks the blood up through a median notch at the end of the rostrum.

reproductive biology

Nothing is known.

conservation status

Not listed by the IUCN but should be considered threatened in those areas where the host population is considered endangered.

significance to humans

None known.

Wandering seabird louse

Ancistrona vagelli

family

Menoponidae

taxonomy

Pediculus vagelli Fabricius, 1787. Type host: Fulmarus g. glacialis.

other common names

None known.

physical characteristics

Distinguished by its large size (0.1–0.2 in, or 3–6 mm), large triangular or rectangular postnotum, characteristic gular processes, and the absence of setal brushes on the venter of the third femur and abdominal sternites.

distribution

Recorded from more than 45 species of seabird in the families Procellaridae and Hydrobatidae. These include species of fulmar, petrel, prion, and shearwater, with a combined distribution covering virtually every patch of seawater in the world.

habitat

Restricted to the host's plumage, particularly regions surrounding the head and neck of the bird that are preened infrequently or are difficult to preen.

behavior

Particularly vagile; hence its name. Capable of moving rapidly over the skin between feathers. This behavior may explain why this species has one of the widest host distributions of any louse in the suborder Amblycera.

feeding ecology and diet

Mainly soft feathers, particularly those close to the skin. As with most Amblycera, however, this probably is supplemented with traces of host blood, serum, and skin debris.

reproductive biology

Nothing specific is known. As with most avian lice, the female is considerably larger than the male and always is found in greater numbers on the host. Eggs are cemented onto feather barbules and hatch within five to 10 days.

conservation status

Not threatened. However, some populations of the species are restricted to rare or endangered hosts, such as the magenta petrel (Pterodroma magentae) and as such should be considered vulnerable.

significance to humans

None known.

Human head/body louse

Pediculus humanus

family

Pediculidae

taxonomy

Pediculus humanus Linnaeus, 1758. Type host: Homo sapiens.

other common names

English: Cootie

physical characteristics

Head with distinctive dark eyes. Abdomen elongate and lacking distinct tubercles. The head louse variant is typically 20% smaller than the body louse form.

distribution

Worldwide. Lives as an ectoparasite on humans but also is recorded from gibbons and New World monkeys.

habitat

Two morphological variants exist that were once thought to be separate species or subspecies. The form commonly referred to as "head lice" is restricted to the human scalp, whereas the form referred to as "body lice" is restricted to clothing and the human torso.

behavior

Human head and body lice are ecological variants of the same species, capable of adapting to the different ecological conditions on the human scalp, torso, or clothing. They are inter-mixed genetically, and their behavioral ecology has been studied extensively, as they are the vector for several important human diseases.

feeding ecology and diet

Both forms feed on blood, but their ecology differs between body morphs. Head lice feed at regular intervals every few hours, whereas body lice feed only once or twice per day during periods of host inactivity.

reproductive biology

The head louse variant attaches eggs (nits) to the base of hair shafts, whereas body lice glue their eggs to projecting fibers of clothing on the host. Eggs typically hatch in five to seven days, and the nymphs reach maturity after another 10–12 days.

conservation status

Not threatened. However, populations restricted to isolated human tribes and nonhuman primates should be considered vulnerable.

significance to humans

As the principal vector of epidemic typhus (Rickettsia prowazekii), the body louse variant was responsible for hundreds of millions of deaths up until the early 1900s. Since World War II, large outbreaks of typhus have occurred mainly in Africa, with reported cases coming predominantly from Burundi, Ethiopia, and Rwanda. The head louse variant is common in the Western World, with infection rates exceeding 20% reported from selected primary schools in Australia, the United Kingdom, and the United States. This form is not known to transmit louse-borne diseases in natural circumstances.

Slender pigeon louse

Columbicola columbae

family

Philopteridae

taxonomy

Pediculus columbae Linnaeus, 1758. Type host: Columba livia domestica.

other common names

None known.

physical characteristics

A long, slender louse, readily distinguished from other ischnoceran genera by the presence of two bladelike dorsal setae on the anterior margin of the head.

distribution

This louse is restricted to four species of pigeon (Columba eversmanni, C. guinea, C. livia, and C. oenas), including the widely distributed common rock dove. The latter has been introduced throughout the world and has a cosmopolitan distribution, living commensally with humans in temperate and tropical areas. Louse distribution is assumed to mirror the distribution of the host. The distribution map accompanying this text shows only the host's native distribution.

habitat

Restricted to the wing feathers of their hosts, either on the undersurface of the wing coverts or at the base of secondary feathers.

behavior

Its slender shape allows the louse to live between the feather barbs. The edge of the barb is grasped with the mandibles and legs, protecting it from the preening activities of the host.

feeding ecology and diet

Feeds on the downy part of the feathers and may migrate from the wings to feed on the fluffy basal portions of body feathers.

reproductive biology

Females deposit their eggs on the underside of the wing feathers, next to the pigeon's body. Eggs are attached to a feather in the space between feather barbs and hatch between three and five days at 98.6°F (37°C).

conservation status

Not threatened. However, populations present on Columba eversmanni (the pale-backed pigeon) should be considered vulnerable.

significance to humans

Used as a "model organism" by biologists to address questions on the evolution and ecology of host-parasite interactions.

Resources

Books

Hopkins, G. H. E., and T. Clay. A Checklist of the Genera and Species of Mallophaga. London: British Museum of Natural History, 1952.

Kim, K. C., H. D. Pratt, and C. J. Stojanovich. The Sucking Lice of North America. University Park: Pennsylvania State University Press, 1986.

Ledger, J. A. The Arthropod Parasites of Vertebrates in Africa South of the Sahara Vol. 4, Phthiraptera (Insecta). Johannesburg: South African Institute for Medical Research, 1980.

Palma, R. L., and S. C. Barker. "Phthiraptera." In Psocoptera, Phthiraptera, Thysanoptera, edited by A. Wells. Zoological Catalogue of Australia, vol. 26. Melbourne, Australia: CSIRO Publishing; 1996.

Price, Roger D., Ronald A. Hellenthal, Ricardo L. Palma, Kevin P. Johnson, and Dale H. Clayton. The Chewing Lice: World Checklist and Biological Overview. Illinois Natural History Survey Special Publication no. 24. Champaign-Urbana: Illinois Natural History Survey, 2003.

Periodicals

Clay, T. "Some Problems in the Evolution of a Group of Ectoparasites." Evolution 3 (1949): 279–299.

—— "The Amblycera (Phthiraptera: Insecta)." Bulletin of the British Museum (Natural History) Entomology 25 (1970): 73–98.

Durden, L. A, and G. G. Musser. "The Sucking Lice (Insecta, Anoplura) of the World: A Taxonomic Checklist with Records of Mammalian Hosts and Geographical Distributions." Bulletin of the American Museum of Natural History 218 (1994): 1–90.

Price, M. A., and O. H. Graham. "Chewing and Sucking Lice as Parasites of Mammals and Birds." USDA Agricultural Research Service Technical Bulletin 1849 (1997): 1–309.

Smith, V. S. "Avian Louse Phylogeny (Phthiraptera: Ischnocera): A Cladistic Study Based Morphology." Zoological Journal of the Linnean Society 132 (2001): 81–144.