Biology, habitat and diseases of flies

AILIE ROBINSON: Hi. My name’s Ailie Robinson, and I’m a research fellow at the London School of Hygiene and Tropical Medicine. I study the flies Musca sorbens. Musca sorbens has been shown to be a vector of the eye disease trachoma, which is endemic in 42 countries worldwide and is a progressive eye disease that can eventually cause blindness. Musca sorbens is a species complex containing three members– Musca sorbens, Musca biseta, and Musca vetustissima. This species complex is in the family Muscidae, within the infraorder Muscomorpha. Flies in this infraorder look relatively similar, conforming to the popular idea of a fly, being robust and a bit hairy. The family Muscidae are of medical importance for several reasons.

Some species, like the genus Stomoxys, are bloodsucking. Others cause human myiasis, where the fly larvae burrow in human flesh. And some species, known as “synanthropic flies,” live in close association with humans and have the potential to mechanically transmit pathogens. As well as transmitting trachoma, Musca sorbens is thought to mechanically transmit enteric, or gut, pathogens, and has also been proposed to be a vector of yaws, a skin and bone disease also caused by bacteria. As well as their role in disease transmission, these flies present a huge nuisance problem. Both Musca sorbens and Musca biseta are found in Africa, while Musca vetustissima is found in Australia.

All are known as “face flies” because of their habit of aggressively visiting the face, while the African species are also collectively known as the “bizarre fly.” The three species are difficult to distinguish morphologically, but they can be distinguished genetically. And Musca vetustissima is geographically allopatric to the African species, allowing species identification. Adult Musca sorbens are mainly grey in colour, although females, in particular, appear silver in the light. They have large, pale, and conspicuous calypters, which are membranous lobes on the posterior edge of the wing. Musca sorbens are very variable in size, although generally, they’re similar to their cousins, the housefly, Musca domestica, about 6 to 9 millimetres in length.

Females have a distinctive pattern of black stripes on their thorax that bifurcate, which means to split, towards the head, and anteriorly to the transverse suture. In contrast, the males two stripes do not bifurcate. Males and females are most easily differentiated by the position of the orange eyes. Like many calyptrate dipterans, these are widely separated in females, which is called “dichoptic,” but close together in males, which is called “holoptic.” Female Musca sorbens lay their eggs on excreta, faeces. The eggs then hatch, and the first-stage larvae burrow into the faeces. There are three larval stages which feed on faeces and the microbiota within for about four to five days.

After that, the third-stage larvae stops feeding, moves away from the faeces breeding site to an area that is cooler and drier, the larval skin cataracts, and it becomes a pupa. The pupae are dark brown, and this stage lasts about four days. The speed of development of all of these juvenile stages is dependent on temperature, with slower development occurring in cooler temperatures. The adult female needs to consume protein in order to make eggs, and it is thought that this is why fly’s visit human faeces and feed on ocular and nasal discharge. The lifespan of the adult also depends on temperature. In the lab, they have been known to survive for eight weeks. However, one month is more usual.

We don’t currently know their lifespan in the wild, although could guess it similar. It’s worth noting that this is a very understudied species.

Adult Musca sorbens are opportunistic feeders, requiring protein and carbohydrate. As well as feeding on ocular and nasal discharge, which is rich in protein, they are attracted to and feed on exudate from sores and will also feed on blood from wounds. They’ve been known to scrape sores until the skin is perforated, then feed on the exudate. Other things they have been documented feeding on our fresh, unspoiled meat, fish, milk, fruit, garbage, animal corpses, and human faeces, which the female feeds on after laying their eggs. Musca sorbens particularly attacks children with ocular and nasal discharge, and we’ve recently shown that males, as well as females, exhibit this behaviour in Ethiopia.

The eye-seeking behaviour of males here might be because of a lack of water in the study area, so flies are simply going to the eyes for liquid and hydration. Musca sorbens are very active flyers, with a preference for open spaces with bright sunlight. Their activity most likely depends on the ambient temperature, being most active in Egypt in the cooler a morning before the temperature rises, and in higher-altitude Ethiopia, more active later in the day as it gets warmer. In some locations, including India and China, they’re commonly found inside, while in other locations, including Egypt, Russia, Australia, Morocco, and Ethiopia, they are rarely found indoors. They rest at night on vegetation or on the walls of human habitations.

Musca sorbens is found across the old-world tropics and subtropics, Asia, the Pacific Islands, and Australasian regions. It’s thought they originated in Africa and migrated into other regions alongside humans. The distribution of Musca sorbens closely matches the distribution of active trachoma, with the exception of Latin America, where trachoma is present without Musca sorbens. These flies are not found in the Americas, probably because they could not follow humans across the northern land bridges. The preferred breeding media of Musca sorbens is faeces, and in most places, they show a strong preference for human faeces. Therefore, these flies live in and around human habitations in areas where food and breeding sites are available.

It has been suggested that Musca sorbens are so dependent on man that they are, in fact, euanthropic, meaning they’re totally reliant on humans for their habitat. Musca sorbens have been documented emerging from animal faeces, including dog, cat, chicken, pig, cow, and buffalo. And the relative importance of non-human breeding sites most likely varies according to geographical location and breeding-site availability. They are larger, and “big” means “fit” in fly terms, while small stunted flies emerge from poor breeding media. However, it’s almost always excrement, and it appears that isolated or exposed stools are required for some reason. Musca sorbens does not emerge from pit latrines and not usually from middens or dung heaps either.

Therefore, safe faeces disposal, for example, latrine use will reduce breeding-site availability. From a control perspective, the local relative importance of different faeces types as breeding media will govern how effectively appropriate faeces disposal can reduce Musca sorbens populations. Musca sorbens has been shown to be a vector of trachoma. The latest figures show that 200 million people live at risk of trachoma, often those living in abject poverty. Because of this disease, 1.9 million people are blind worldwide, and a further 3.2 million require surgery to prevent blindness. Trachoma is caused by the bacterium Chlamydia Trachomatis, often referred to as “CT.” This is the same bacterium, but a different strain, that causes a sexually transmitted infection chlamydia.

Trachoma is caused by serovars A to C, while chlamydia is caused by serovars D to K. Chlamydiae are obligate intracellular bacteria, meaning that they must invade host cells inside which they then survive and replicate. Because Chlamydia trachomatis infects cells of the eyelid, the damage caused by this intracellular infection causes inflammation, which, after repeated infection, can cause irreversible scarring and blindness. Trachoma is a Neglected Tropical Disease, or an NTD. NTDs are found in remote resource-poor settings, often in populations living in close proximity to animals or vectors, and therefore, often affecting the world’s poorest and most marginalised people. NTDs do not attract great investment into disease-control measures or research.

Children and women are the worst affected by trachoma, and active disease is common in preschool children. Chlamydial infections are easily treatable with antibiotics if these are available. There is no vaccine. There are multiple routes of transmission of trachoma, and it is likely that the relative importance of these routes varies by location. Classically, three transmission routes are sited– fingers; fomites, which are inanimate objects that can carry infectious particles; and flies, the focus of this piece. When Musca sorbens flies visit the face to feed on ocular or nasal discharge, they can pick up CT and transfer it to another person. This is called “mechanical transmission.”

Sometimes the housefly, Musca domestica, will also display eye-seeking behaviour, but it seems that across most trachoma-endemic regions, the vast majority of fly eye contacts are made by Musca sorbens. Some areas have trachoma and no Musca sorbens, for example, Latin America, indicating the importance of other transmission routes in that setting. In clinical trials, significantly decreasing the Musca sorbens population has led to decreases in trachoma prevalence, while fly-control interventions in other regions were found to have no effect. Multiple transmission routes complicate trachoma epidemiology, and the extent to which flies contribute to transmission must also be dependent on local factors, such as fly seasonality and abundance.

Musca sorbens has also been found to carry enteric pathogens, including the helminths Ascaris, Trichuris, hookworm, Taenia, Strongyloides, and the protozoans– Entamoeba, Cryptosporidium, and Giardia. As with other mechanical vectors, the extent to which carriage of these pathogens by flies contributes to disease transmission remains unknown. Finally, the nuisance burden caused by these insects should not be disregarded. In areas of high-fly density, they can be seen clustered all around the eyes, nose, and mouth of children because for them, swatting the flies away is essentially futile. It’s generally accepted that Musca sorbens are vectors of trachoma. Disease vectors can be biological or mechanical. Biological vectors are intrinsic to the development of the pathogen, while mechanical vectors inadvertently carry the pathogen.

A pathogen with a biological vector cannot exist in the absence of the vector because they require the developmental stages that occur in the vector to complete their lifecycle. For example, the development of Plasmodium gametocytes through to sporozoites in malaria mosquitoes. In mechanical vectors, however, no development and no significant multiplication should occur. But there’s a bit of a question mark around the transmission of trachoma by Musca sorbens, as it’s reasonable to speculate this CT may, indeed, invade the fly tissues, for example, in the gut mucosa. If there was replication in this scenario, they may constitute biological vectors. Multiplication of bacteria within synanthropic flies has been documented.

For example, the excretion of the bacteria species Escherichia, Salmonella, and Shigella by Musca domestica at significantly greater numbers as those which the flies were initially fed, although other investigators fail to repeat these findings. Other studies have documented bacterial multiplication, but only following removal of competition first by sterilising the normal gut flora. Irrespective of possible multiplication within fly tissue, pathogens can be mechanically carried by flies either internally or externally. If we consider the morphology of the synanthropic fly families, Muscidae, Sarcophagagidae, and Calliphoridae, known as “filth flies,” and all with known potential for mechanical transmission, it’s easy to see how carriage of pathogens could happen.

There are cracks, crevices, and sticky areas all over the bodies of these flies, in which microorganisms could easily become lodged on the hairs that are present all over their bodies; on the tarsae with their sticky, tenent hairs; or in grooves on the fleshy proboscis that most of these flies exhibit, which is used to lap, sponge, or scrape up food. If the pathogen is ingested it can be egested at a later time and onto either a different host or the host’s food. Flies have a tendency to regurgitate liquid food, and both fly vomit drops and faecal drops can contain viable pathogens.

The persistence of pathogens either on or in flies most probably depends on a number of factors and most importantly, the fly species, the pathogen species, the amount of pathogen uptaken, and the environment. But even if flies are infected only transiently, they may still be of profound medical importance as pathogen transmitters, especially when you consider that flies may carry a small inoculum pathogen to the food, where the pathogen then multiplies many times. Returning to trachoma transmission by Musca sorbens, with such direct and, often, prolonged contact between the fly and human mucosal membranes– with such direct and, often, prolonged contact between the fly and human mucosal membranes– transient fly infection would be sufficient to transmit CT.

Further, the developmental cycle of Chlamydia bacteria involves two stages– the extracellular and infectious elementary bodies and the intracellular and non-infectious reticulate bodies. CT is transmitted by the elementary bodies, which are small, light, resistant to environmental stress, and which invade mucosal membranes. It is thought that these could easily be carried by flies and transferred between hosts. For vector control, the overall goal here is to reduce or prevent fly eye contact by Musca sorbens to the extent that transmission of CT could not occur. This could be achieved either by reducing the overall fly population or by blocking fly-face contacts. It is highly likely that only a minority of Musca sorbens flies in trachoma-endemic areas carry CT.

Therefore, it may not be necessary to totally prevent all fly-face contact. Despite the incredible propensity of flies for multiplying– i.e., they breed like flies– reducing the overall fly population would probably be the most efficient way to reduce fly-eye contacts. This could be achieved by removal of breeding sites or by killing the adult population with insecticide. Because Musca sorbens prefer to breed in isolated and exposed faeces, installation and high uptake of latrines would eliminate their breeding sites. Only a very few studies have specifically looked at the effect of controlling Musca sorbens populations on rates of trachoma, but a cluster randomised trial in the Gambia found that insecticide spraying with permethrin reduced trachoma by 56%.

And a cluster randomised trial in the Gambia found that insecticide spraying with permethrin reduced trachoma prevalence by 56%, which was a significant reduction, while installation of pit latrines reduced trachoma prevalence by 30%.

Being a neglected tropical disease, there are comparatively few larger-scale trials that look at the effect of any disease-control intervention on trachoma, and there is a good degree of incertitude around which wash interventions– those around water, sanitation, and hygiene– contribute most effectively to trachoma control. Wash interventions which aim to clean faeces to prevent transmission by direct contact will probably also impact fly transmission by removing their food source. , Therefore it is unclear which transmission route is being blocked. Control of breeding sites is the most attractive option, as improving the sanitation and hygiene conditions for the very-poor communities who are affected by trachoma would clearly have multiple benefits.

However, such interventions are costly, and in some areas, uptake is low, indicating further investment and understanding cultural norms around faeces disposal or means to change behaviour are required. Insecticide, while effective, must be reapplied, can have negative environmental impacts, may be unsustainable in the longer term, and perhaps most importantly, the development of insecticide resistance could be problematic. Musca sorbens have almost never been colonised, and so laboratory testing of interventions was not possible. And given their unsanitary breeding preferences, this is an undesirable job. It is possible that other vector-control tools could be applied to Musca sorbens. Indeed, current studies at LSHTM are investigating options, including insect repellents for personal protection and odour-baited traps for population suppression.