Tsetse

Tsetse ( , or ) (sometimes spelled tzetze; also known as tik-tik flies), are large, biting flies that inhabit much of tropical Africa. Tsetse flies include all the species in the genus ''Glossina'', which are placed in their own family, Glossinidae. The tsetse are obligate parasites, which live by feeding on the blood of vertebrate animals. Tsetse have been extensively studied, because of their role in transmitting disease. They have a prominent economic impact in sub-Saharan Africa, as the biological vectors of trypanosomes, causing human and animal trypanosomiasis. Tsetse are multivoltine and long-lived, typically producing about four broods per year, with up to 31 broods over their lifespans.

Tsetse can be distinguished from other large flies by two easily-observed features: Primarily, tsetse fold their wings over their abdomens completely when they are resting (so that one wing rests directly on top of the other); Secondly, tsetse also have a long proboscis, extending directly forward, which is attached by a distinct bulb to the bottom of their heads.

Fossilized tsetse have been recovered from Paleogene-aged rocks in the United States and Germany. Twenty-three extant species of tsetse flies are known from the African continent as well as the Arabian Peninsula.

Etymology

The word ''tsetse'' means "fly" in Tswana, a Bantu language of southern Africa. Recently, ''tsetse'' without the fly has become more common in English, particularly in the scientific and development communities.

The word is pronounced ''tseh-tseh'' in the Sotho languages and is easily rendered in other African languages. During World War II, a British de Havilland antisubmarine aircraft was known as the 'Tsetse' Mosquito.

Biology

The biology of tsetse is relatively well understood by entomologists. They have been extensively studied because of their medical, veterinary, and economic importances, because the flies can be raised in a laboratory, and because they are relatively large, facilitating their analysis.

Morphology

Tsetse flies can be seen as independent individuals in three forms: as third- instar larvae, pupae, and adults.

Tsetse first become separate from their mothers during the third larval instar, during which they have the typical appearance of maggots. However, this life stage is short, lasting at most a few hours, and is almost never observed outside of the laboratory.

Tsetse next develop a hard external case, the puparium, and become pupae - small, hard-shelled oblongs with two distinctively small, dark lobes at the tail (breathing) end. Tsetse pupae are under long. Within the puparial shell, tsetse complete the last two larval instars and the pupal stage.

At the end of the pupal stage, tsetse emerge as adult flies. The adults are relatively large flies, with lengths of , and have a recognizable shape, or bauplan, which makes them easy to distinguish from other flies. Tsetse have large heads, distinctly separated eyes, and unusual antennae. The thorax is quite large, while the abdomen is wider, rather than elongated, and shorter than the wings.

Four characteristics collectively separate adult tsetse from other kinds of flies:

Anatomy

Like all other insects, tsetse flies have an adult body comprising three visibly distinct parts: the head, the thorax and the abdomen.

The head has large eyes, distinctly separated on each side, and a distinct, forward-pointing proboscis attached underneath by a large bulb. The thorax is large, made of three fused segments. Three pairs of legs are attached to the thorax, as are two wings and two halteres. The abdomen is short but wide and changes dramatically in volume during feeding.

The internal anatomy of the tsetse is fairly typical of the insects; the crop is large enough to accommodate a huge increase in size during feeding, as tsetse can take a bloodmeal equal in weight to themselves. The dipteran crop is heavily understudied, with ''Glossina'' being one of the few genera having relatively reliable information available: Moloo and Kutuza 1970 for ''G. brevipalpis'' (including its innervation) and Langley 1965 for ''G. morsitans''. The reproductive tract of adult females includes a uterus, which can become large enough to hold the third-instar larva at the end of each pregnancy. The article “'' Parasitic flies of domestic animals''” has a diagram of the anatomy of dipteran flies.

Most tsetse flies are, physically, very tough. Houseflies, and even horseflies, are easily killed with a flyswatter, for example; a great deal of effort is needed to crush a tsetse fly.

Life cycle

Tsetse have an unusual life cycle, which may be due to the richness of their blood food source. A female fertilizes only one egg at a time; she will retain each egg within her uterus, the offspring developing internally (during the first three larval stages), in an adaptation called adenotrophic viviparity. During this time, the female feeds the developing offspring with a milky substance (secreted by a modified gland) in the uterus.
In the third larval stage, the tsetse larvae leave the uterus and begin independent life. The newly-birthed larvae crawl into the ground, and develop a hard outer shell (called the puparial case), within which they complete their morphological transformations into adult flies.

The larval life stage has a variable duration, generally 20 to 30 days, and the larvae must rely on stored resources during this time. The importance of the richness and quality of blood to this stage can be seen; all tsetse development (prior to emerging from the puparial case as a full adult) occurs without feeding, with only the nutrition provided by the mother fly. She must get enough energy for her own survival (in addition to the needs of her developing offspring), as well as for the stored resources which her offspring will require until they emerge as adults.

Technically, these insects undergo the standard development process of insects, beginning with oocyte formation, ovulation, fertilization, and development of the egg; following egg development and birth are the three larval stages, a pupal stage, and the emergence and maturation of the adult.

Hosts

Overall Suidae are the most important hosts. By species, bloodmeals are derived from:
*'' G. swynnertoni'' 6070% from warthog, ~8% from giraffe
*'' G. austeni'' 5060% from bushpig, ~33% from Bovidae, possibly 10% from various duiker
*'' G. fuscipleuris'' 65% from bushpig and giant forest hog, up to 20% from hippopotamus
*'' G. tabaniformis'' 70% from red river hog, >7% from porcupines
*'' G. morsitans'' 3045% from warthog, 2540% from various Bovidae, especially kudu, buffalo, bushbuck, and eland, most especially domestic cattle, ~2% from hartebeest
*'' G. fusca'' 5590% from bushbuck, 15% from red river hog, ~12% from aardvark
*'' G. brevipalpis'' up to 40% (high variability with geography) from bushpig, up to 36% from hippopotamus, ~25% from Bovidae, especially buffalo and bushbuck
*'' G. palpalis'' ~3% from wild Suidae, more substantial amounts from domestic Suidae when available, ~2040% from Bovidae (including domestic cattle) depending on geography, ~10% from waterside birds including cormorants, 2530% from '' Varanus'' and crocodile (possibly higher in natural settings, 50% from crocodile in particular locations)
*'' G. fuscipes'' ~3% from wild Suidae, ~2040% from Bovidae (including domestic cattle) depending on geography, ~10% from waterside birds including cormorants, 2530% from '' Varanus'' and crocodile (possibly higher in natural settings)
*'' G. tachinoides'' ~3% from wild Suidae, more substantial amounts from domestic Suidae when available, ~2040% from Bovidae (including domestic cattle) depending on geography, >7% from porcupines
*'' G. pallidipes'' 5590% from bushbuck
*'' G. longipalpis'' 5590% from bushbuck
*'' G. longipennis'' unusually dependant (~60%) on rhinoceros, also ~20% from Bovidae, variably up to 12% from elephant, up to 7% from ostrich
*'' G. m. submorsitans'' ~6% from various birds excluding ostrich
Waterbuck (''Kobus ellipsiprymnus'') are unmolested by ''Glossina'' because they produce volatiles which act as repellents. Waterbuck odor volatiles are under testing and development as repellents to protect livestock.

Genetics

The genome of ''Glossina morsitans'' was sequenced in 2014.

Symbionts

Tsetse flies have at least three known bacterial symbionts. The primary symbiont is ''Wigglesworthia'' ('' Wigglesworthia glossinidia'') within the fly's bacteriocytes, the secondary symbiont is ''Sodalis'' (''Sodalis glossinidius'') intercellularly or intracellularly, and the third is some kind of '' Wolbachia''.

Diseases

The salivary gland hypertrophy virus causes abnormal bleeding in the lobes of the crop of '' G. m. centralis'' and '' G. m. morsitans''.

Systematics

Tsetse are in the order Diptera, the true flies. They belong to the superfamily Hippoboscoidea, in which the tsetse's family, the Glossinidae, is one of four families of blood-feeding obligate parasites.

Up to 34 species and subspecies of tsetse flies are recognized, depending on the particular classification used.

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 superfamily Hippoboscoidea, which contains other hematophagous families.

Species

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

* The 'savannah' flies: (subgenus ''Morsitans'', occasionally named ''Glossina''):
** '' Glossina austeni'' ( Newstead, 1912) patr. of Austen
** '' Glossina morsitans'' (Westwood, 1851)
*** ''Glossina morsitans submorsitans''
** '' Glossina pallidipes'' ( Austen, 1903)
** ''Glossina swynnertoni'' ( Austen, 1922) GBIF: 5055987 patr. of Swynnerton

* The 'forest' flies: (subgenus ''Fusca'', previously named ''Austenia''):

** ''Glossina fusca fusca'' (Walker, 1849)
** ''Glossina fuscipleuris'' ( Austen, 1911)
** ''Glossina frezili'' (Gouteux, 1987)
** '' Glossina haningtoni'' ( Newstead and Evans, 1922)
** '' Glossina longipennis'' (Corti, 1895)
** ''Glossina medicorum'' ( Austen, 1911)
** ''Glossina nashi'' (Potts, 1955)
** ''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' and 'lacustrine' flies: (subgenus ''Palpalis'', previously named ''Nemorhina''):
** ''Glossina caliginea'' ( Austen, 1911)
** ''Glossina fuscipes'' ( Newstead, 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) patr. of Newstead
** ''Glossina palpalis palpalis'' (Robineau-Desvoidy, 1830)
** '' Glossina palpalis gambiensis'' (Vanderplank, 1911)
** '' Glossina tachinoides'' (Westwood, 1850)

Evolutionary history

Fossil glossinids are known from the Florissant Formation in North America and the Enspel Lagerstätte of Germany, dating to the late Eocene and late Oligocene respectively.

Range

''Glossina'' is almost entirely restricted to grassland and forested areas of the Afrotropics. Only two subspecies - '' G. f. fuscipes'' and '' G. m. submorsitans'' - are definitely present in the very southwest of Saudi Arabia. Although Carter found '' G. tachiniodes'' in 1903 nearby, near Aden in southern Yemen, there have been no confirmations since.

Trypanosomiasis

Tsetse are biological vectors of trypanosomes, meaning that in the process of feeding, they acquire and then transmit small, single-celled 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'' (a French term which may not be a distinct condition), and ''surra'' according to the animal infected and the trypanosome species involved. The usage is not strict and while ''nagana'' generally refers to the disease in cattle and horses it is commonly used for any of the animal trypanosomiases.

Trypanosomes are animal parasites, specifically protozoans of the genus ''Trypanosoma''. These organisms are about the size of red blood cells. Different species of trypanosomes infect different hosts. They range widely in their effects on the vertebrate hosts. Some species, such as ''T. theileri'', do not seem to cause any health problems except perhaps in animals that are already sick.

Some strains are much more virulent. Infected flies have an altered salivary composition which lowers feeding efficiency and consequently increases the feeding time, promoting trypanosome transmission to the vertebrate host. These trypanosomes are highly evolved and have developed a life cycle that 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 similarity of this mode of transmission to mechanical injection with a syringe. Mechanical transmission requires the tsetse to feed on an infected host and acquire trypanosomes in the blood meal, and then, within a relatively short period, to feed on an uninfected host and regurgitate some of the infected blood from the first blood meal into the tissue of the uninfected animal. This type of transmission occurs most frequently when tsetse are interrupted during a blood meal and attempt to satiate themselves with another meal. Other flies, such as horse-flies, can also 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 (development within the fly is known as the extrinsic incubation period), 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 blood meals. Tsetse infected by trypanosomes are thought to remain infected for the remainder of their lives. Because of the adaptations required for biological transmission, trypanosomes that can be 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 life cycle 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 that feeds on 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 blood meal that contains trypanosomes, or may inject trypanosomes in its saliva. Inoculation must contain a minimum of 300 to 450 individual trypanosomes to be successful, and may contain up to 40,000 cells.

In the case of ''T. b. brucei'' infecting ''G. p. gambiensis'', during this time the parasite changes the proteome contents of the fly's head. This may be the reason/a reason for the behavioral changes seen, especially the unnecessarily increased feeding frequency, which increases transmission opportunities. This may be due in part to the altered glucose metabolism observed, causing a perceived need for more calories. (The metabolic change, in turn, being due to complete absence of glucose-6-phosphate 1-dehydrogenase in infected flies.) Monoamine neurotransmitter synthesis is also altered: Production of aromatic L-amino acid decarboxylase - involved in dopamine and serotonin synthesis - and α-methyldopa hypersensitive protein was induced. This is very similar to the alterations in ''other'' dipteran vectors' head proteomes under infection by ''other'' eukaryotic parasites of mammals, found in another study by the same team in the same year.

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.

Disease hosts and vectors

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 that may also survive in wild animals such as crocodiles and monitor lizards. The diseases have different distributions across the African continent, so are transmitted by different species. This table summarizes this information:

In humans

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

Sleeping sickness begins with a tsetse bite leading to an inoculation in the subcutaneous tissue. The infection moves into the lymphatic system, leading to a characteristic swelling of the lymph glands called ''Winterbottom'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 species ''Trypanosoma brucei'', which causes the disease, has often been subdivided into three subspecies that 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''. Strains that infected humans were divided into two subspecies 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 subspecies are polyphyletic, so the elucidation of the strains of ''T. brucei'' infective to humans requires a more complex explanation. Procyclins are proteins developed in the surface coating of trypanosomes whilst in their tsetse fly vector.

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 insects of the Reduviidae, members of the Hemiptera.

In domestic animals

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 eventual 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 the tsetse fly.

The tsetse fly vector ranges mostly in the central part of Africa.

Trypanosomiasis poses a considerable constraint on livestock agricultural development in Tsetse fly infested areas of sub Saharan Africa, especially in west and central Africa. International research conducted by ILRI in Nigeria, the Democratic Republic of the Congo and Kenya has shown that the N'Dama is the most resistant breed.

Control

The conquest of sleeping sickness and nagana would be of immense benefit to rural development and contribute to poverty alleviation and improved food security in sub-Saharan Africa. Human African trypanosomosis (HAT) and animal African trypanosomosis (AAT) are sufficiently important to make virtually any intervention against these diseases beneficial.

The disease can be managed by controlling the vector and thus reducing the incidence of the disease by disrupting the transmission cycle. Another tactic to manage the disease is to target the disease directly using surveillance and curative or prophylactic treatments to reduce the number of hosts that carry the disease.

Economic analysis indicates that the cost of managing trypanosomosis through the elimination of important populations of major tsetse vectors will be covered several times by the benefits of tsetse-free status. Area-wide interventions against the tsetse and trypanosomosis problem appear more efficient and profitable if sufficiently large areas, with high numbers of cattle, can be covered.

Vector control strategies can aim at either continuous suppression or eradication of target populations. Tsetse fly eradication programmes are complex and logistically demanding activities and usually involve the integration of different control tactics, such as trypanocidal drugs, impregnated treated targets (ITT), insecticide-treated cattle (ITC), aerial spraying (Sequential Aerosol Technique - SAT) and in some situations the release of sterile males ( sterile insect technique – SIT). To ensure sustainability of the results, it is critical to apply the control tactics on an area-wide basis, i.e. targeting an entire tsetse population that is preferably genetically isolated.

Control techniques

Many techniques have reduced tsetse populations, with earlier, crude methods recently replaced by methods that are cheaper, more directed, and ecologically better.

Slaughter of wild animals

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

Land clearing

Another early technique involved complete removal of brush and woody vegetation from an area. However, the technique was not widely used and has been abandoned. Tsetse tend to rest on the trunks of trees so removing woody vegetation made the area inhospitable to the flies. Until about 1959 this was done by hand and so was quite time consuming. Glover et al 1959 describes the technique which they call "chain clearing". Chain clearing drags a chain forward between two heavy vehicles and thereby does the same job much more quickly - but still at some expense. Preventing regrowth of woody vegetation requires continuous clearing efforts which is even more expensive, and only practical where large human populations are present. Also, 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 with organochlorine pesticides such as DDT applied as aerosol sprays at Ultra-Low Volume rates. Later, more targeted techniques used ''pour-on'' formulations in which advanced organic pesticides were applied directly to the backs of cattle.

Trapping

Tsetse populations can be monitored and effectively controlled using simple, inexpensive traps. These often use electric blue cloth, either in sheet or biconical form, since this color attracts the flies. The traps work by channeling the flies into a collection chamber, or by exposing the flies to insecticide sprayed on the cloth. Early traps mimicked the form of cattle, as tsetse are also attracted to large dark colors like the hides of cows and buffaloes. Some scientists put forward the idea that zebra have stripes, not as a camouflage in long grass, but because the black and white bands tend to confuse tsetse and prevent attack.

The use of chemicals as attractants to lure tsetse to the traps has been studied extensively in the late 20th century, but this has mostly been of interest to scientists rather than as an economically reasonable solution. Attractants studied have been those tsetse might use to find food, like carbon dioxide, octenol, and acetone—which are given off in animals' breath and distributed downwind in an ''odor plume.'' Synthetic versions of these chemicals can create artificial odor plumes. A cheaper approach is to place cattle urine in a half gourd near the trap. For large trapping efforts, additional traps are generally cheaper than expensive artificial attractants.

A special trapping method is applied in Ethiopia, where the BioFarm Consortium ( ICIPE, BioVision Foundation, BEA, Helvetas, DLCO-EA

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