Siphonaptera (Fleas)

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Siphonaptera

(Fleas)

Class Insecta

Order Siphonaptera

Number of families 16

Evolution and systematics

Fleas may have evolved as early as 140 million years ago (mya), along with their mammalian hosts. Only five flea species are known from fossil records: three from Baltic amber (35–40 mya: Palaeopsylla baltica, Palaeopsylla dissimilis, and Palaeopsylla klebsiana) and two from Dominican amber (15–20 mya: Pulex larimerius and an undescribed species of Rhopalopsyllus). The specialized combs, setae, and appendages of these relics are very similar to those of their modern relatives. Molecular and morphological data suggest the small Mecopteran family of snow scorpionflies, or (Boreidae), snow fleas is a sister group of Siphonaptera. Snow fleas are not actually fleas and are not parasitic, as are all members of the Siphonaptera.

Based on empirical evidence, some workers have divided the superfamily Pulicoidea into two subfamilies (Pulicinae and Tunginae), whereas others have considered them as two separate families (Pulicidae and Tungidae). DNA analyses conducted from 2000 to 2003 of taxa assigned to these subfamilies indicate that they are two distinct families. The family placement of many of the 244 genera remains to be defined by molecular studies. Until molecular studies redefine the genetic phylogeny, 16 families belonging to five superfamilies are recognized: Ceratophylloidea (Ancistropsyllidae, Ceratophyllidae, Ischnopsyllidae, Leptopsyllidae, and Xiphiopsyllidae), Hystrichopsylloidea (Chimaeropsyllidae, Coptopsyllidae, Ctenophthalmidae, Hystrichopsyllidae, Pygiopsyllidae, and Stephanocircidae), Malacopsylloidea (Malacopsyllidae and Rhopalopsyllidae), Pulicoidea (Pulicidae and Tungidae), and Vermipsylloidea (Vermipsyllidae). Of about 2,575 species (including subspecies), some 5% occur on birds, while the remaining 95% parasitize mammals. DNA analyses indicate that fleas originated on mammals, with some crossing over later to avian hosts. Fleas typically do not parasitize amphibians and reptiles.

Physical characteristics

Fleas are wingless, laterally compressed, holometabolous insects, and the adults are adapted to a parasitic mode of life. Their eggs are small, elongated spheres, varying in color from pearly white to dark brown to black; they are about 0.02–0.06 in (0.5–1.4 mm) in diameter. Larvae are wormlike and range from 0.02 to 0.4 in (0.5–10 mm) in length, with well-sclerotized head capsules, three thoracic segments without appendages, and ten abdominal segments. There usually are three larval stadia (intervals between molts), although some species of Tunga have only two. A silk pupal case contains an exarate (having the appendages not "glued" to the body) pupa that is 0.008–0.4 (0.2–10 mm) long. Fine debris, which blends with the surroundings, often adheres to the pupal case.

In general, adult fleas range from 0.04 to 0.3 in (1.0–8 mm), excluding engorged Tungidae and Vermipsyllidae. Female adult fleas typically are larger than males, and those of

a few species may achieve lengths of 0.6 in (16 mm) when they are engorged or gravid. Their mouthparts are modified for piercing avian or mammalian hosts and sucking their blood. Adults have evolved highly modified combs and setae on their body and legs. These features provide protection for intersegmental membranes and spiracle openings and are used for grasping hairs and feathers and for preventing dislodgment during the host's preening activities. Legs are specialized to promote mobility through the fur and feathers of the host and for jumping to facilitate host acquisition. Fleas that have adapted to a parasitic life on birds (bird fleas) tend to have more setae that are longer and more slender than those of fleas that parasitize mammals (mammal fleas).

The internal anatomy of fleas may be as important in flea phylogeny as the external morphological features. Females possess either one or two spermathecae. Two are considered a primitive condition, because a blind duct exists in most species with a single spermatheca. Most families have six rectal pads, a proventriculus with spines, and a ventral nerve cord. Tungidae are exceptional in possessing only two rectal pads and no proventricular spines; moreover, the nerve cord is displaced dorsally. The variety of morphological specialization (such as head, thoracic, and abdominal combs; the degree of sclerotization of the exoskeleton; the length and number of setae; the development of mouthparts, tarsal claws, and associated bristles on appendages; spiracle characteristics; development of complex genitalia, particularly in males; diversification of internal anatomy; and display of neosomatic growth) is reflective of the corresponding diversity of the respective host species.

Male and female fleas are sexually dimorphic. In addition to size differences, the eighth sternum, ninth tergum, and aedeagus of males are highly specialized, whereas only the seventh sternum of females is particularly modified. The dorsal area of the male head frequently is grooved longitudinally, and the anterior portion of the head is divided from the posterior portion by a distinct suture or groove. The female head may or may not be divided. Antennae generally are longer in males than in females.

Distribution

The Ceratophyllidae, Hystrichopsyllidae, Leptopsyllidae, Vermipsyllidae, Coptopsyllidae, and Ancistropsyllidae occur predominantly in the boreal continents of North America, Europe, or Asia. Those families restricted to the southern continents of Africa, Antarctica, Australia, or South America include Malacopsyllidae, Rhopalopsyllidae, Stephanocircidae, Pygiopsyllidae, Xiphiopsyllidae, and Chimaeropsyllidae. The remaining three families, Ctenophthalmidae, Ischnopsyllidae and Pulicidae, occur in both the Northern and Southern Hemispheres.

Habitat

Fleas parasitize hosts in virtually every conceivable terrestrial habitat, adapting to the microclimate of the nests, burrows, and body conditions. Such adaptations enable fleas to live in the most extreme environmental conditions. For example, Glaciopsyllus antarcticus occurs only in the frigid, sub-zero conditions of the Antarctic. They proliferate in the microclimate of the nest and in the down of their avian host, the southern fulmar (Fulmarus glacialoides). Many species (Xenopsylla and Nosopsyllus) thrive in the dry conditions of deserts, living in the burrows of their rodent hosts, where the temperature and humidity are optimal for their development. Adult fleas are found on mammalian hosts more frequently and in greater numbers than those species parasitizing birds. Fleas have adapted only to birds that use their nests over and over (swallows, seabirds, and some ground-dwelling birds and cavity dwellers). A few species (Pulex and Ctenocephalides), especially those inhabiting coastal, semitropical, and tropical regions, are free living, jumping on and off their hosts and proliferating in open environmental conditions, such as floors of homes, pathways, barnyards, animal pens, and pet beds.

Behavior

Perpetuation of each species is dependent on the success of finding a host. Some fleas remain in a quiescent pupal state for an extended time, to survive cold periods or to wait until a host approaches. Vibrations produced by an approaching host may stimulate adults to emerge immediately from their pupal cases. Although the visual acuity of fleas is poor, shadows of approaching hosts illicit a jump response. They also are attracted to the warmth and carbon dioxide emitted by potential hosts. A few species, particularly bat fleas, are negatively geotrophic (moving against gravity), crawling up cave walls to locate bats roosting on the cave ceiling.

Feeding ecology and diet

With the exception of Uropsylla tasmanica, the larvae of most fleas are free living, scavenging on dried blood, animal dandruff, and animal excreta in the host's nest or the environment. Larval cat fleas (Ctenocephalides felis felis) feed on partially digested blood excreted from the anus of adult fleas. The larvae of Hoplopsyllus, Tunga, and Dasypsyllus are documented facultative ectoparasites, feeding either on host tissues or on organic debris in the nest substrate. Uropsylla tasmanica larvae burrow into the skin of their host and are the only known true obligate larval flea parasites. A few species are predaceous on other nest-dwelling organisms.

Depending on the species, adult fleas ingest blood by either tapping into a capillary, or by cutting the tissue and causing

a pool of blood from which to feed. A few species have been observed to imbibe water. The vast majority of fleas are intermittent feeders, among them, C. f. felis, and some attach to their hosts permanently, for example, Echidnophaga gallinacea and species of Tunga. The nutritional requirements of adults are understood only partly. Male and female fleas require a blood meal as a prerequisite for spermatogenesis or oogenesis. Females feed more rapidly than males and require larger volumes of blood to facilitate egg production. The chemistry of host blood is known to affect the host specificity of some species and is suspected to influence many others.

Reproductive biology

Males assume a position directly beneath the female, each facing the same direction. The occipital groove in the dorsal portion of the male head frequently is developed to accommodate the keel-shaped surface of forward sternites of the female abdomen. The male clasps the sides of the female sternites with suckerlike structures on the inner surface of the antennae. He also may clasp the hind legs of the female between a notch in the hind coxa and the retracted femur. The highly modified ninth tergite (basimere and telomere) attaches to the terminal segments of the female in a "clasping" manner. The posterior margin of the seventh sternum of many females is modified with various lobes and sinuses that facilitate attachment during copulation. The vaginal canal also is modified to accommodate partial insertion of the highly modified apical portion of the aedeagus. Sperm transfer is accomplished during insertion of long penis rods through the vaginal canal, into the bursa copulatrix, through the duct of the spermatheca, and into the spermatheca. This process varies from species to species.

Copulation is vastly different in Tunga. The female attaches to the skin of the host and soon becomes enveloped by the host tissues, exposing only the caudal disc (the last four abdominal spiracles, the anus, and the vaginal opening). A darkly sclerotic ring made up of host tissues surrounds the caudal disc. Males locate the female and copulate in situ with a highly modified aedeagal apparatus. After copulation, the female develops massive numbers of eggs that are expelled into the environment wherever the host travels. The breeding cycles of Cediopsylla and Spilopsyllus are bound to the estrus cycle of their hosts, hares and rabbits. Other genera probably are influenced by the breeding cycle of the host, but studies are lacking.

Neosomy is the expansion of pregenital abdominal segments by secretion of new cuticle without molting. This process takes place in females of Hectopsylla, Neotunga, Tunga (Tungidae), Chaetopsylla, Dorcadia, Vermipsylla (Vermipsyllidae), and Malacopsylla (Malacopsyllidae), as a way to accommodate growth up to 1,000x normal size. Neosomatic growth is especially pronounced in Tunga, Neotunga, and Dorcadia. Males do not undergo neosomatic growth, because their principal function is to mate. Females expand primarily to accomodate egg production.

Some species lay eggs on their host, others do so indiscriminately in the environment, and still others place them in the lair or nest of the host. The duration of each stage of the life cycle varies for each species. An example is the common cat flea C. f. felis. Eggs are laid on the host within 48 hours of a blood meal. The eggs drop to the ground (most often in the lair of a cat or dog), hatch, and pass through three larval stadia. The mature larva spins a silken cocoon and molts within, ultimately emerging as an adult. The developmental cycle is completed in two to three weeks under optimal conditions of temperature and humidity but may take as long as three to four months. Across the order, sex ratios are approximately 1:1, and longevity of adults may range from only a few weeks to more than three years.

Conservation status

There are no flea taxa specifically listed as threatened by the IUCN; however, species that are very host specific (that is, they depend on a single host for their existence) are in danger of perishing if their host is endangered. Attempts to identify such combinations have never been undertaken.

Significance to humans

The bite of the dog, cat, and human flea (Pulex complex) may cause annoyance, irritation, extreme itching, hypersensitivity, and secondary infections. Many species of flea transmit diseases to humans and their pets directly through their bite, through rubbing or scratching infected feces into an open wound, or by ingesting infected fleas. These include plague (Yersinia pestis), murine typhus (Rickettsia typhi), and cat scratch fever (Bartonella henslae). Fleas also have the potential to transmit Q-fever (Coxiella burnetti), tularemia (Francisella tularensis), listeriosis (Listeria monocytogenes), salmonellosis (Salmonella species), and Carrion's disease (Bartonella bacilliformis). Fleas also are efficient vectors of myxomatosis, a viral disease of rabbits. Some serve as the intermediate host of the double-pored tapeworm (Dipylidium caninum) of humans and several tapeworms of sylvatic (wild) and commensal rodents (Hymenolepis diminuta and H. nana). The filarial worm, Dipetalonema reconditum, and the protozoan blood parasite, Trypanosoma lewisi, may be transmitted to dogs and rats, respectively.

Species accounts

List of Species

Bat flea
Oriental rat flea
Helmet flea
Chigoe
Sheep and goat flea

Bat flea

Ischnopsyllus octactenus

family

Ischnopsyllidae

taxonomy

Ischnopsyllus octactenus Kolenati, 1856. Type locality not specified.

other common names

None known.

physical characteristics

Yellowish-brown in color. Males reach 0.09 in (2.4 mm), and females grow to 0.1 in (2.5 mm). Head, thorax, abdomen, and legs are exceptionally long and slender. The front of the head has two posteriorly directed spatulate ctenidia. Pronotum has a comb of 28 pointed ctenidia. Metanotum and abdominal terga I–VI have ctenidial combs.

distribution

Europe, southern British Isles and Scandinavia, Canary Islands, North Africa and the northern Middle East to Pakistan.

habitat

The bat known as Kuhl's pipistrelle (Pipistrellus kuhli) rests under the leaves and in the attics of houses, often providing close access for adult fleas.

behavior

Bat fleas parasitize bats that roost in areas that bring them into close association with adult fleas. Immature stages develop on the substrate below roosting bats, requiring adult fleas to climb to access the bats or to crawl up on them when baby bats fall from the ceiling and are retrieved by their mothers.

feeding ecology and diet

Host preferences include bats of the family Vespertilionidae, particularly Pipistrellus kuhli.

reproductive biology

Nothing is known.

conservation status

Not threatened.

significance to humans

None known.

Oriental rat flea

Xenopsylla cheopis cheopis

family

Pulicidae

taxonomy

Xenopsylla cheopis cheopis (Rothschild, 1903), Shendi, Sudan.

other common names

English: Asiatic rat flea, common rat flea, tropical rat flea, Egyptian rat flea.

physical characteristics

Golden brown in color. Males grow to 0.06 in (1.6 mm) and females to 0.09 in (2.4 mm). Combs are absent. Single row of setae on each abdominal tergite. Oblique row of spiniform setae on the inner aspect of hind coxa.

distribution

Cosmopolitan. Present wherever Norway rats (Rattus norvegicus) and roof rats (Rattus rattus) are found.

habitat

Seaports and unsanitary situations associated with humans that provide food and harborage for rats.

behavior

Larvae and fed adults avoid light, whereas unfed adults are attracted to light. Adults can jump 100 times their length.

feeding ecology and diet

Prefers commensal rodents of the genus Rattus but bites humans readily and is the most efficient vector of plague. The presence of blood and plague bacilli in the proventriculus creates a clot matrix, blocking the gut at temperatures below 80.6°F (27°C). While the proventriculus is blocked, the flea repeatedly attempts to feed, injecting the deadly plague organisms into the host (human or rat). At ambient temperatures of 80.6°F (27°C) or greater, the blockage clears by a combination of enzymes present in the plague bacillus and in the flea's gut. For this reason urban plague epidemics caused by X. c. cheopis do not occur during warm seasons.

reproductive biology

Males cannot mate until they have fed. Feeding triggers the dissolution of the testicular plug, allowing spermatozoa to pass during copulation. Copulation takes about 10 minutes. Eggs are 0.01–0.02 in (0.3–0.5 mm) in diameter, oval, and white, with a sticky surface. They are laid off the host. Eggs hatch in 2–21 days; three larval stages require about 9–15 days to pupation. Adults may emerge from pupae after a week or more. The life cycle can be completed at a temperature range of 64.4–95°F (18–35°C) but optimally at 80.6°F (27°C), with relative humidity above 60% (optimally 80%).

conservation status

Not threatened.

significance to humans

X. c. cheopis was responsible for the plague pandemic of Europe in the fourteenth century, which is estimated to have killed 25 million people.

Helmet flea

Stephanocircus dasyuri

family

Stephanocircidae

taxonomy

Stephanocircus dasyuri Skuse, 1893, New South Wales, Australia.

other common names

None known.

physical characteristics

Dark reddish-brown color. Males reach 0.114 in (2.9 mm), and females reach 0.118 in (3.0 mm). The head is divided into a forward plate of 14 pointed ctenidia, referred to as a "helmet" or a "crown of thorns," and a rear plate on each side of the head bearing the antenna and genal combs of seven pointed ctenidia. The pronotum has a comb of 22 pointed ctenidia. There are two rows of setae on each abdominal tergite. The dorsal margin of each hind tibia is adorned with a row of setae resembling the teeth of a comb. Three antesensilial bristles occur on each side of the seventh tergite.

distribution

Coastal areas of southern and eastern continental Australia and Tasmania.

habitat

Foothill habitats of New South Wales, Queensland, and Tasmania.

behavior

Nothing is known.

feeding ecology and diet

Wide range in host preferences but found most frequently on quolls (Dasyuridae), potoroos (Macropodidae), and long- and short-nosed bandicoots (Peramelidae).

reproductive biology

Nothing is known.

conservation status

Not threatened.

significance to humans

None known.

Chigoe

Tunga penetrans

family

Tungidae

taxonomy

Tunga penetrans Linnaeus, 1758, America.

other common names

English: Jigger, chigger (not to be confused with the six-legged larval "chigger" mite belonging to the family Trombiculidae), sand flea; Spanish: Chique.

physical characteristics

Yellow color, similar to straw. Males and females are about 0.04 in (1.0 mm) long, but gravid females may attain 0.16 in (4.0 mm). Front of head acutely pointed upward. No combs or spinelike setae. Single row of setae on each tergite. Posterior four pairs of spiracles greatly enlarged. Distinct tooth on apex of hind coxa.

distribution

Southern United States, Central and South America, West Indies, and tropical Africa.

habitat

Unsanitary situations.

behavior

Adults will pass through clothing to feed.

feeding ecology and diet

Male and female fleas bite humans intermittently. They prefer the feet, but other areas of the body are not exempt. Only impregnated females permanently attach to the host. They usually select tender areas between the toes, under the nail beds, and along the soles of the feet.

reproductive biology

After insemination, the female seeks a host and permanently attaches, is enveloped by the swelling host tissues, and becomes replete with eggs. Eggs are released into the environment and hatch; larvae require about 10–14 days to pupation. Under optimal conditions, adults emerge after about 10–14 days.

conservation status

Not threatened.

significance to humans

Bites cause extreme irritation. Embedded females may form pustules and cause secondary infections resulting in the sloughing away of toes. Gangrene may ensue and require surgical amputation. Removal of embedded females facilitates healing.

Sheep and goat flea

Dorcadia ioffi

family

Vermipsyllidae

taxonomy

Dorcadia ioffi Smit, 1953, Issyk-Kul, Tien Shan, Turkestan.

other common names

None known.

physical characteristics

Distinctly intermixed pale and dark brown markings. Males grow to 0.13 in (3.3 mm), and females reach 0.18 in (4.5 mm); gravid females may attain 0.6 in (16 mm) by neosomatic growth. Combs are absent. Exceedingly long and multisegmented labial palpus.

distribution

Mongolia, Russia, and the Chinese provinces of Qinghai, Xinjiang, Gansu, and Xizang.

habitat

Pastures and agricultural areas suitable for domestic sheep, cattle, goats, and wild ungulates.

behavior

The legs of engorged females are of little use because of the enormous size of the abdomen. Such females often are seen moving through the host's hair by wormlike contractions.

feeding ecology and diet

Although males feed less than females, they both imbibe blood. Males attach to the skin along the sides of the neck, and gravid females have been noted to attach to the inside of the nostrils of wild and domestic even-toed ungulates.

reproductive biology

Winter months occur from November to March in the range of this flea. From December through February, animals may have 100–200 adult fleas. The ratio of male to female occurring on hosts is 1:10. Eggs are expelled into the environment in about March. Eggs are oval and darkly pigmented. As spring temperatures increase, eggs hatch. Larval development progresses until pupation in August, and adults emerge in November. The life cycle requires about nine months.

conservation status

Not threatened.

significance to humans

Parasites of domestic animals; not known to bite humans.

Resources

Books

Hopkins, George Henry Evans, and Miriam Rothschild. An Illustrated Catalogue of the Rothschild Collection of Fleas (Siphonaptera) in the British Museum (Natural History). Vols. 1–5. London: British Museum (Natural History), 1953–1971.

Mardon, D. K. An Illustrated Catalogue of the Rothschild Collection of Fleas (Siphonaptera) in the British Museum (Natural History). Vol. 6. London: British Museum (Natural History), 1981.

Rothschild, Miriam, and Robert Traub. A Revised Glossary of Terms Used in the Taxonomy and Morphology of Fleas. London: British Museum (Natural History), 1971.

Smit, F. G. A. M. An Illustrated Catalogue of the Rothschild Collection of Fleas (Siphonaptera) in the British Museum (Natural History). Vol. 7. London: British Museum (Natural History), 1987.

——. "Key to the Genera and Subgenera of Ceratophyllidae." In The Rothschild Collection of Fleas. The Ceratophyllidae: Key to the Genera and Host Relationships, edited by Robert Traub, Miriam Rothschild and John F. Haddow. Cambridge, U.K.: Cambridge University Press, 1983.

Traub, Robert, Miriam Rothschild, and John F. Haddow. The Rothschild Collection of Fleas. The Ceratophyllidae: Key to the Genera and Host Relationships. Cambridge, U.K.: Cambridge University Press, 1983.

Periodicals

Audy, J. R., F. J. Radovsky, and P. H. Vercammen-Grandjean. "Neosomy: Radical Intrastadial Metamorphosis Associated with Arthropod Symbioses." Journal of Medical Entomology 9 (1972): 487–494.

Cavanaugh, D. C.. "Specific Effect of Temperature upon Transmission of the Plague Bacillus by the Oriental Rat Flea, Xenopsylla cheopis." American Journal of Tropical Medicine and Hygiene 20 (1971): 264–273.

Humphries, D. A. "The Mating Behavior of the Hen Flea Ceratophyllus gallinae (Schrank) (Siphonaptera: Insecta)." Animal Behavior 15 (1967): 82–90.

Lewis, Robert E. "Résumé of the Siphonaptera (Insecta) of the World." Journal of Medical Entomology 35 (1998): 377–389.

Lewis, Robert E., and David Grimaldi. "A Pulicid Flea in Miocene Amber from the Dominican Republic (Insecta: Siphonaptera: Pulicidae)." Novitates 3205 (1997): 1–9.

Rothschild, Miriam. "Fleas." Scientific American 213 (1965): 44–53.

——. "Neosomy in Fleas, and the Sessile Life-Style." Journal of the Zoological Society of London 226 (1992): 613–629.

——. "Recent Advances in Our Knowledge of the Order Siphonaptera." Annual Review of Entomology 20 (1975): 241–259.

Whiting, M. F. "Mecoptera Is Paraphyletic: Multiple Genes and a Phylogeny for Mecoptera and Siphonaptera." Zoologica Scripta 31 (2002): 93–104.