Tsetse fly

Tsetse are large biting flies which feed on the blood of vertebrate animals. The flies are African, and consist of several species in the genus Glossina, which in turns belongs to the superfamily Glossinidae, of the order Diptera. The Tsetse fly is the only species in its genus, which is in turn the only genus in its superfamily. The genus name is attributed to Christian Wiedemann, who named the type species in 1830.

Tsetse have been extensively studied because they are biological vectors of the African trypanosomiases, deadly diseases which include sleeping sickness in humans and nagana in cattle.

Tsetse fly (Glossina)
Conservation status: Secure
Tsetse fly
Scientific classification
Kingdom:Animalia
Phylum:Arthropoda
Class:Insecta
Order:Diptera
Family:Glossinidae
Genus:Glossina
Subgenera
  • morsitans ('savannah' species)
  • fusca ('forest' species)
  • palpalis ('riverine' species)

The word tsetse comes from Tswana, a language of southern Africa, and, in that language, the word means fly. The British pronunciation of the word uses two different sounds for the two different syllables, generally tee-tsee. Many African languages have an explosive ts sound and so a common pronunciation of the word involves two identical syllables both having this ts sound and a shorter sound of the vowel, as ts-eh-ts-eh. There is no universal authority on the matter and many different pronunciations exist.

Tsetse are usually easy to distinguished from other flies because of two unusual features of their anatomy. Tsetse fold their wings completely when they are resting so that one wing rests directly on top of the other over their abdomen. Tsetse also have a long proboscis which extends directly forward and is attached by a distinct bulb to the bottom of their head.

Tsetse have existed, in more or less the modern morphological form, for at least 34 million years; Tsetse fossil have been recovered from, among other locations, the Florissant Fossil Beds in Colorado.

Contents


Tsetse biology

Tsetse have been extensively studied partially because of their medical and economic importance and partially because of their large size. Entomologists have discovered a great deal about tsetse development, metabolism, and general biology.

Tsetse morphology

Tsetse are large flies with a recognizable shape or bauplan so they can usually be distinguished without trouble from other flies. Tsetse have large heads with distinctly separated eyes and unusual antennae. The tsetse thorax is quite large while the abdomen is wide rather than elongated.

Four characteristics definitively separate tsetse from other kinds of flies.

  • Proboscis — Tsetse have a distinct proboscis, a long thin structure attached to the bottom of the head and pointing forward.
    Missing image
    Tsetse_head-proboscis.jpeg
    A photograph of the head of a tsetse illustrating the forward pointing proboscis.

  • Folded wings — When at rest, tsetse fold their wings completely one on top of the other.
    Missing image
    Tsetse_foldedWings.jpeg
    A photograph of the whole body of a tsetse illustrating the folded wings when at rest.

  • Hatchet cell — The discal medial ("middle") cell of the wing has a characteristic hatchet shape which resembling a meat cleaver or a hatchet.
    Missing image
    Tsetse_hatchetCell.jpeg
    A photograph of the wing of a tsetse illustrating the hatchet shaped central cell.

  • Branched arista hairs — The antennae have arista with hairs which are themselves branched.
    Missing image
    Tsetse_aristaHairs_labeled.jpeg
    A photograph and diagram of the head of a tsetse illustrating the branched hairs of the antenna's arista.

The tsetse life cycle

Tsetse have an unusual life cycle which may be due to the richness of their food source. Technically these insects undergo a standard development process for insects which comprises oocyte formation, ovulation and fertilization, development of the egg, five larval stages, a pupal stage, and then emergence of the adult. However, tsetse are unusual both in having all of the life stages prior to the third larval stage occur within the female parent, and in completing the larval stages and the pupal stage proper within a puparial case. The importance of the richness of blood to this development can be seen since all tsetse development prior to the emergence from the puparial case as a full adult occurs without feeding based only on nutritional resources provided by the female parent.

This life strategy in which an insect species retains the egg within in the uterus and allows development to proceed into the larval stages before parturition of the new offspring is called adenotrophic vivparity.

Tsetse metabolism

The most interesting aspect of tsetse metabolism is the unusual pathway which tsetse use for flight which seems to be responsible for the extremely high energy output and elevated flying speeds which tsetse can achieve.

Most insects, such as honey bees, consume predominantly sugar for metabolic energy. Tsetse, instead, use a pathway which involves the conversion of the amino acids proline and alanine.

The result of this pathway is that tsetse can create large amounts of ATP but can only sustain this metabolic output for short durations. Tsetse therefore fly at very high speeds (they are known to be able to follow a car moving at thirty miles an hour) for short flights of around thirty seconds or so.

General biology

Tsetse have specialized cells that contain bacterial endosymbionts required for survival.

Tsetse systematics

Tsetse include up to thirty four species and sub-species depending on the particular classification used.

Tsetse are sufficiently different in appearance and behavior to have been placed in their own distinct branch of the flies. This placement is controversial. The science of systematics is currently struggling to reconcile the traditional form of biological classification with the modern understanding of genomic evolution and speciation. The controversy surrounding the placement of tsetse is therefore likely to continue into the future.

All current classifications place all the tsetse species in a single genus named Glossina. Most classifications place this genus as the sole member of the family Glossinidae. The Glossinidae are generally placed within the infraorder Cyclorrhapha which includes the housefly and the blowfly due to the similarity of their developmental biology. This infraorder in turn, is part of the sub-order Brachycera, the stubby flies with reduced antenna. Tsetse are evidently part of the order Diptera, the flies.

Tsetse species

The tsetse genus is generally split into three different groups of species based on a combination of distributional, behavioral, and morphological characteristics. The genus includes :

  • The savannah flies: (Sub-genus morsitans, occasionally named glossina):
    • Glossina austeni (Newstead, 1912)
    • Glossina longipalpis (Wiedemann, 1830)
    • Glossina morsitans centralis (Machado, 1970)
    • Glossina morsitans morsitans (Wiedemann, 1850)
    • Glossina morsitans submorsitans (Newstead, 1911)
    • Glossina pallidipes (Austen, 1903)
    • Glossina swynnertoni (Austen, 1923)
  • The forest flies: (Sub-genus fusca, previously named austenia):
    • Glossina brevipalpis (Newstead, 1911)
    • Glossina fusca congolensis (Newstead and Evans, 1921)
    • Glossina fusca fusca (Walker, 1849)
    • Glossina fuscipleuris (Austen, 1911)
    • Glossina frezili (Gouteux, 1987 (http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&list_uids=3629143&dopt=Abstract))
    • Glossina haningtoni (Newstead and Evans, 1922)
    • Glossina longipennis (Corti, 1895)
    • Glossina medicorum (Austen, 1911)
    • Glossina nashi (Potts,1955)
    • Glossina nigrofusca hopkinsi (Van Emden, 1944)
    • Glossina nigrofusca nigrofusca (Newstead, 1911)
    • Glossina severini (Newstead, 1913)
    • Glossina schwetzi (Newstead and Evans, 1921)
    • Glossina tabaniformis (Westwood, 1850)
    • Glossina vanhoofi (Henrard, 1952)
  • The riverine flies: (Sub-genus palpalis, previously named nemorhina):
    • Glossina caliginea (Austen, 1911)
    • Glossina fuscipes fuscipes (Newstead, 1911)
    • Glossina fuscipes martinii (Zumpt, 1935)
    • Glossina fuscipes quanzensis (Pires, 1948)
    • Glossina pallicera pallicera (Bigot, 1891)
    • Glossina pallicera newsteadi (Austen, 1929)
    • Glossina palpalis palpalis (Robineau-Desvoidy, 1830)
    • Glossina palpalis gambiensis (Vanderplank, 1911)
    • Glossina tachinoides (Westwood, 1850)

Sources:

  • J. A. Van Vesten "The Tsetse Fly Glossina fuscipes fuscipes Newstead, 1911, in East Africa; some aspects of its biology and its role in the epidemiology of human and animal trypanosomiasis" Doctoral Thesis, University of Amsterdam, 1971.
  • A. M. Jordan "Tsetse-flies (Glossinidae)" Chapter 9 in Medical Insects and Arachnids R. P. Lane and R. W. Crosskey eds. Chapman & Hall, 1993.


Tsetse as vectors of trypanosomiasis

Tsetse are biological vectors of trypanosomes meaning that tsetse, in the process of feeding, acquire and then transmit small, single-celled organisms called trypanosomes from infected vertebrate hosts to uninfected animals. Some tsetse transmitted trypanosome species cause trypanosomiasis, an infectious disease. In humans, tsetse transmitted trypanosomiasis is called sleeping sickness. In animals, tsetse vectored trypanosomiases include nagana, souma, and relapsing fever according to the animal infected and the trypanosome species involved, although the usage is not strict and nagana is occasionally used for any form of animal trypanosomiasis.

Trypanosomes are animal parasites, specifically protozoa of the genus Trypanosoma. These organisms are approximately the size of red blood cells. Different species of trypanosomes infect different hosts as can be seen in the table attached to this section. Trypanosomes range widely in their effects on the vertebrate hosts. Some species, such as Trypanosoma theileri, do not seem to cause any health problems except perhaps in animals which are already quite sick. Some strains are much more virulent. Tsetse seem to be unaffected by the infection of trypanosomes but it is entirely possible that the parasites alter tsetse behavior or have other effects which improve the chances of transmission and survival. These trypanosomes have become highly evolved and developed a life cycle which requires periods in both the vertebrate and tsetse hosts.

Tsetse transmit trypanosomes in two ways, mechanical and biological transmission.

  • Mechanical transmission involves the direct transmission of the same individual trypanosomes taken from an infected host into an uninfected host. The name mechanical reflects the similarly of this mode of transmission to the transmission which could be caused mechanically with a syringe. Mechanical transmission requires that tsetse feed on an infected host and acquire trypanosomes in the bloodmeal, and then, within in a relatively short period, for tsetse to feed on an uninfected host and regurgitate some of the infected blood from the first bloodmeal into the tissue of the uninfected animal. This type of transmission occurs most frequently when tsetse are interrupted during a bloodmeal and attempt to satiate themselves with another meal. Other flies, such as horse-flies, also can cause mechanical transmission of trypanosomes.
  • Biological transmission requires a period of incubation of the trypanosomes within the tsetse host. The term biological is used because trypanosomes must reproduce through several generations inside the tsetse host during the period of incubation, which requires extreme adaptation of the trypanosomes to their tsetse host. In this mode of transmission, trypanosomes reproduce through several generations, changing in morphology at certain periods. This mode of transmission also includes the sexual phase of the trypanosomes. Tsetse are believed to be more likely to become infected by trypanosomes during their first few bloodmeals. Tsetse infected by trypanosomes are thought to remain infected for the remainder of their lives. Because of the adaptations required for biological transmission, trypanosomes which are transmitted biologically by tsetse cannot be transmitted in this manner by other insects.

The relative importance of these two modes of transmission for the propagation of tsetse-vectored trypanosomiases is not yet well understood. However, since the sexual phase of the trypanosome lifecycle occurs within the tsetse host, biological transmission is a required step in the life cycle of the tsetse vectored trypanosomes.

The cycle of biological transmission of trypanosomiasis involves two phases, one inside the tsetse host and the other inside the vertebrate host. Trypanosomes are not passed between a pregnant tsetse and her offspring so all newly emerged tsetse adults are free of infection. An uninfected fly which feeds upon an infected vertebrate animal may acquire trypanosomes in its proboscis or gut. These trypanosomes, depending on the species, may remain in place, move to a different part of the digestive tract, or migrate through the tsetse body into the salivary glands. When an infected tsetse bites a susceptible host, the fly may regurgitate part of a previous bloodmeal which contains trypanosomes or may inject trypanosomes contained within its saliva. It is believed that the inoculation must contain a minimum of 300 to 450 individual trypanosomes to be successful, and may contain up to 40,000 individuals. The trypanosomes are injected into vertebrate muscle tissue but make their way, first into the lymphatic system, then into the bloodstream, and eventually into the brain. The disease causes the swelling of the lymph glands, emaciation of the body, and eventually leads to death. Uninfected tsetse may bite the infected animal prior to its death and acquire the disease, thereby closing the transmission cycle.

The tsetse vectored trypanosomiases affect various vertebrate species including humans, antelopes, bovine cattle, camels, horses, sheep, goats, and pigs. These diseases are caused by several different trypanosome species which may also survive in wild animals such as crocodiles and monitor lizards. The diseases have different distributions across the african continent and are therefore transmitted by different species of tsetse. The following table summarizes this information:

Disease

Species affected

Trypanosoma Agents

Distribution

Glossina vectors

Sleeping sickness
Chronic form

Humans

T. brucei gambiense

Western Africa

G. palpalis
G. tachinoides
G. fuscipes
G. morsitans

Sleeping sickness
Acute form

Humans

T. brucei rhodesiense

Eastern Africa

G. morsitans
G. swynnertoni
G. pallidipes
G. fuscipes

Nagana
Acute form

Antelope
Bovine cattle
Camels
Horses

T. brucei brucei

Africa

G. morsitans
G. swynnertoni
G. pallidipes
G. palpalis
G. tachinoides
G. fuscipes

Nagana
Chronic form

Bovine cattle
Camels
Horses

T. congolense

Africa

G. palpalis
G. morsitans
G. austeni
G. swynnertoni
G. pallidipes
G. longipalpis
G. tachinoides
G. brevipalpis

Nagana
Acute form

Bovine cattle
Camels
Horses

T. vivax

Africa

G. morsitans
G. palpalis
G. tachinoides
G. swynnertoni
G. pallidipes
G. austeni
G. vanhoofi
G. longipalpis

Nagana
Acute form

Domestic Pigs
Bovine cattle
Camels
Horses

T. simiae

Africa

G. palpalis
G. fuscipes
G. morsitans
G. tachinoides
G. longipalpis
G. fusca
G. tabaniformis
G. brevipalpis
G. vanhoofi
G. austeni

Surra

Domestic Pigs
Warthogs
  (Phacochoerus
  aethiopicus)
Bushpigs
  (Potamochoerus spp.)
Forest Hogs
  (Hylochoerus spp.)

T. suis

Africa

G. palpalis
G. fuscipes
G. morsitans
G. tachinoides
G. longipalpis
G. fusca
G. tabaniformis
G. brevipalpis
G. vanhoofi
G. austeni

Sources:
* C. A. Hoare "Systematic Description of the Mammalian Trypanosomes of Africa" Chapter 2 in Mulligan, H. & Potts, W. (1970) The African Trypanosomiases London, UK: George Allen and Unwin Ltd.
* R. C. Hunt (2004) Trypanosomiasis page (http://www.med.sc.edu:85/trypanosomiasis.htm) "Microbiology and Immunology On-line" University of South Carolina, USA Retrieved 2 April 2005.

Tsetse vectored human trypanosomiases

Human African trypanosomiasis, also called sleeping sickness, is caused by trypanosomes of the Trypanosoma brucei species. This disease is invariably fatal unless treated but can almost always be cured with current medicines, if the disease is caught early enough.

Sleeping sickness begins with a tsetse bite leading to an inoculation in the sub-cutaneous tissue. The infection moves into the lymphatic system leading to a characteristic swelling of the lymph glands which is called Winterbottoms's sign. The infection progresses into the blood stream and eventually crosses into the central nervous system and invades the brain leading to extreme lethargy and eventually to death.

The page on human sleeping sickness has more extensive information about this disease.

The Trypanosoma brucei species, which causes the disease, has often been subdivided into three sub-genera which were identified based either on the vertebrate hosts which the strain could infect or on the virulence of the disease in humans. The trypanosomes infectious to animals and not to humans were named Trypanosoma brucei brucei. The strains which infected humans were divided into two sub-species based on their different virulences: Trypanosoma brucei gambiense was thought to have a slower onset and Trypanosoma brucei rhodesiense refers to strains with a more rapid, virulent onset. This characterization has always been problematic but was the best that could be done given the knowledge of the time and the tools available for identification. A recent molecular study using restriction fragment length polymorphism analysis suggests that the three sub-genera are polyphyletic [Hide:1999], so the elucidation of the strains of T. brucei infective to humans will require a more complex explanation.

Other forms of human trypanosomiasis also exist but are not transmitted by tsetse. The most notable is American trypanosomiasis, known as Chagas disease, which occurs in South America, caused by Trypanosoma cruzi, and transmitted by certain species of the reduviidae, members of the true bugs.

Tsetse vectored animal trypanosomiases

Animal trypanosomiasis , also called nagana when it occurs in bovine cattle or horses or sura when it occurs in domestic pigs, is caused by several trypanosome species. These diseases reduce the growth rate, milk productivity, and strength of farm animals, generally leading to the eventually death of the infected animals. Certain species of cattle are called trypanotolerant because they can survive and grow even when infected with trypanosomes although they also have lower productivity rates when infected.

The course of the disease in animals is similar to the course of sleeping sickness in humans.


Trypanosoma congolense and Trypanosoma vivax are the two most important species infecting bovine cattle in sub-saharan Africa. Trypanosoma simiae causes a virulent disease in swine.

Other forms of animal trypanosomiasis are also known from other areas of the globe, caused by different species of trypanosomes and transmitted without the intervention of tsetse.

Tsetse control

Tsetse control has been undertaken in order to reduce the incidence of the diseases which the flies transmit. Two alternative strategies have been used in the attempts to reduce the African trypanosomiases. One tactic is primarily medical or veterinary and targets the disease directly using monitoring, prophylaxis, treatment, and surveillance to reduce the number of organisms which carry the disease. The second strategy is generally entomological and intends to disrupt the cycle of transmission by reducing the number of flies.

The idea of tsetse control implies a change in the relationship between people and these insects. Prior to the twentieth century, people in Africa had largely adapted to the presence of tsetse. Human settlement patterns and agricultural practices had adapted to the presence of the fly. For example, in Ethiopia draft powered framing was restricted to the highland areas where the flies were absent whereas lowland areas where tsetse are present were more sparsely populated by people living a nomadic, less agriculturally intensive lifestyle. Tsetse control is a response to changing conditions. Tsetse control has been proposed as a way of reducing the incidence of the disease in the populations living in tsetse regions, of allowing the expansion of human settlement and agriculture into new areas, and of helping people previously relocated either in forced transfers or due to migration.

Tsetse control efforts have been undertaken throughout the African continent but long-term, sustainable control has rarely been achieved. Tsetse control efforts invariably are tied to the complex problems of poverty, heath, politics, and violence which have proved such a disaster for the African people.

The reduction of fly numbers has generally been attempted with two different aims, either eradication which intends to completely eliminate tsetse from the area or control which aims simply to reduce the numbers. Eradication is an idea which has often been imagined, has repeatedly been attempted, and is still proposed but many reasons suggest that control is a safer, cheaper, more realistic, and sustainable approach. Eradication refers to the successful killing of every tsetse either in a region or, under more grandiose proposals, from the entire African continent. Local eradication efforts have repeatedly been undertaken and have achieved temporary success only to fail in the long term because tsetse were able to re-invade (Sansibar).

All of the economic, ecological, political, and environmental justifications for eradication have been called into question. The economic justification for eradication offsets the immense costs of the eradication campaign against the medical and veterinary benefits which are considered to accrue in perpetuity.

Tsetse control techniques

Many techniques have been used to reduce tsetse populations with earlier crude methods being replaced in more recent times by methods which are cheaper, more directed, and ecologically better considered.

Slaughter of wild animals

One early technique involved the slaughter of all the wild animals on which tsetse fed. For example, the Island of Principe off the west coast of Africa, was entirely cleared of feral pigs in the 1930's which led to the extirpation of the fly. While the fly eventually re-invaded in the 1950's, the new population of tsetse was free from the disease.

Land clearing

Another early technique involved the complete removal of any brush or woody vegetation from an area. Tsetse tend to rest on the trunks of trees so the removal of woody vegetation made the area inhospitable to the flies. However, the technique has not been widely used and has been abandoned in more recent times. Preventing the regrowth of woody vegetation requires continuous clearing efforts which is only practicable where large human populations are present. The clearing of woody vegetation has come to be seen as an environmental problem more than a benefit.

Pesticide campaigns

Pesticides have been used to control tsetse starting initially during the early part of the twentieth century in localized efforts using the inorganic metal based pesticides, expanding after the Second World war into massive aerial and ground based campaigns using the early organic pesticides such as DDT, and continuing with the targeted use of pour-ons in which advanced organic pesticides are applied directly to the backs of cattle.

Trapping

Tsetse populations can be effectively controlled using simple, inexpensive traps.

Releases of irradiated males

The Sterile Insect Technique has been used to reduce tsetse populations. This technique involves the rearing of large numbers of tsetse, separation of the males, irradiation of these flies with large doses of gamma rays to make them sterile and then release into to the wild. Since females only mate a few times in their life, generally only once, any mating with a sterile male will prevent that female from giving birth to any offspring. See Sterile Atomic Fly for a more detailed discussion of this technique.

The Sterile Insect Technique has recently been used on Zanzibar, an island off the coast of East Africa. Like other eradication efforts, early indications are that the fly numbers have been decimated with the fly possibly extirpated (locally eradicated) from the island. A number of traps are in place to monitor the island and repress any resurgence.

Resources

Tsetse have an extensive literature.

Books

A lively narrative account of the history of tsetse is:

  • McKelvey Jr., J. (1973) Man Against Tsetse: Struggle for Africa. Ithaca, NY, USA: Cornell University Press.
  • One Chapter in: Robert S. Desowitz, New Guinea Tapeworms and Jewish Grandmothers, tales of parasites and people, 1987, Norton Verlag, ISBN 0393304264 with a short history about the situation at the Lake Victoria.

Scientific books on tsetse and trypanosomiasis

  • Buxton, P. (1955) The Natural History of Tsetse Flies: An Account of the Biology of the Genus Glossina (Diptera). London, UK: H.K. Lewis & Co.
  • Glascow, J. (1963) The Distribution and Abundance of Tsetse International Series of Monographs on Pure and Applied Biology, No. 20. Oxford, UK: Pergamon Press.
  • Mulligan, H. & Potts, W. (1970) The Afrian Trypanosomiases London, UK: George Allen and Unwin, Ltd.
  • Ford, J. (1971) The Role of the Trypanosomiases in African Ecology. Oxford, UK: Clarendon Press.
  • Leak, S. (1998) Tsetse Biology and Ecology: Their role in the Epidemiology and Control of Trypanosomiasis. New York, NY, USA: CABI Publishing. book site (http://www.cabi-publishing.org/bookshop/BookDisplay.asp?SubjectArea=Hum&Subject=Public+Health+and+Communicable+Diseases&PID=1406)

Links

  • "Programmes and information to assist in the planning and implementation of tsetse control operations": http://www.tsetse.org

References

  • Buxton, P. (1955) The Natural History of Tsetse Flies: An Account of the Biology of the Genus Glossina (Diptera). London, UK: H.K. Lewis & Co.
  • Ford, J. (1971) The Role of the Trypanosomiases in African Ecology. Oxford, UK: Clarendon Press.
  • Glascow, J. (1963) The Distribution and Abundance of Tsetse International Series of Monographs on Pure and Applied Biology, No. 20. Oxford, UK: Pergamon Press.
  • Hide, G. (1999) "History of Sleeping Sickness in East Africa". Clinical Microbiology Reviews Jan.1999 112-125.
  • Hoare , C. A. (1970) "Systematic Description of the Mammalian Trypanosomes of Africa" Chapter 2 in Mulligan, H. & Potts, W. (1970) The African Trypanosomiases London, UK: George Allen and Unwin Ltd.
  • Leak, S. (1998) Tsetse Biology and Ecology: Their role in the Epidemiology and Control of Trypanosomiasis. New York, NY, USA: CABI Publishing. book site (http://www.cabi-publishing.org/bookshop/BookDisplay.asp?SubjectArea=Hum&Subject=Public+Health+and+Communicable+Diseases&PID=1406)
  • McKelvey Jr., J. (1973) Man Against Tsetse: Struggle for Africa. Ithaca, NY, USA: Cornell University Press.
  • Mulligan, H. & Potts, W. (1970) The Afrian Trypanosomiases London, UK: George Allen and Unwin, Ltd.


Acknowledgments

The photographs are from the collection of the American Museum of Natural History, in New York City, USA curated by Dr. David Grimaldi. The photographs were taken by Mr. Tam Nguyen, a technician in the Museum.de:Tsetsefliegen

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