An explosive epidemic

An explosive epidemic means death for flies. Entomophthora muscae, an important biological control.
by Taylor Sulerud

In the past, epidemics have decimated human populations. These events can directly affect human health, like the bubonic plague or indirect like the Irish potato famine. These diseases are caused by microbes, and epidemics can be just as dangerous to other species. An epidemic in fly populations caused by Entomophthora muscae is called an epizootic (1). E. muscae is a zygomycota fungus (5). This fungus infects a wide variety of fly species like, Delia antiqua, Pollenia rudis, Coenosia tigrina, the house fly (Musca domestica) along with several other hosts (1). This infection is heavily dependent on host and pathogen population densities (2). This common pathogen of flies can cause epizootics, if conditions are right, with a prevalence of 70-90%, so the majority of flies it infects die. This makes it a good biological candidate for controlling multiple fly populations. However there is some host specificity observed, E. muscae transmitted to the same type of host has a higher infection rate than those transmitted to a different type. It is unknown if this is due to genetic variation or phenotypic adaptation. The isolates from different hosts are morphologically very similar (1). Since the infection rate is dependent on fly population density it will be most effective at stopping swarms of onion flies or cabbage root flies from ruining crops. In these cases E. muscae won’t stop the maggots from damaging the plants roots, just diminish the numbers of following generations that will be present over the course of the growing season (2). Of course, the first step in this process is a fly becoming infected.

Infection by E. muscae starts with the conidia, an asexual, non-motile fungal spore, attaching to a fly. Conidia have outer mucilaginous protoplasm that they use to adhere to most substrates (2). The spores can attach and germinate at any time over the course of the day. However temperature and humidity do affect how virulent the fungus is. Higher atmospheric humidity results in more flies succumbing to the infection. Flies that survived an infection at a lower relative humidity would become lethally infected if exposed at a higher humidity (3). It doesn’t seem like the flies that fight off an infection of E. muscae become resistant to further infections. Temperature could also affect the growth rates, as E. muscae would grow slower at lower temperatures and could even be killed off at higher temperatures. Within 24 hours the spores will pierce the exoskeleton with germ tubes (4). One long germ tube arises from the secondary conidium and can branch out inside the insect hemocoel. Fungal cytoplasm will fill the germ tubes before hyphae can start growing at the ends (2, 4). Sphere like hyphae bodies start replicating in the fly within 24-48 hours. After 48 hours the hyphae start consuming the hemolymph and internal organs. Signs of an infection include changes such as swollen abdomen angled high into the air and outstretched wings. The abdomen turns white as conidiophores grow through the intersegmental membranes (6).

Figure 1. A infected female cadaver and male fly (5)

Figure 2. close up of conidiaphores (2)

It is at this point the fungus can develop two different ways each resulting in different behavior in flies. E. muscae can keep perpetuating itself through the growing season by developing conidiaophores. The infected host flies up to someplace high in the late afternoon and die a few hours later, this is know as summit disease (5). The conidiophores continue to grow and penetrate out through the membranous ventral aspect of the abdomen from between the tergites. The conidiophores are finger shaped as they start growing outwards and start resembling a bell as they mature. Only one spore is developed at the apex, which is then forcibly ejected at the onset of night (2, 4).

Figure 3. life cycle of E. muscae (5)

These conidia drift on the winds until they attach to another fly and begin the cycle again. There is another way for the conidia to find a new host. A male house fly will find an infected female cadaver that he comes across irresistible. He will try court and mate with the female and in the process become infected, even to the point of ignoring a healthy female (5, 6, 7). Another reproductive strategy of E. muscae is producing resting spores. These are primarily made in females and are dependent on the photoperiod (7). Resting spores are produced from about 10% of the infections throughout the growing season. On this path the fly is compelled to find soil to land on and perish. After the fly dies, its abdomen becomes blackened and brittle, eventually falling apart to release the resting spores into the soil (2). They will lie dormant throughout the winter and attach themselves to emerging adult flies in the early spring. Production of either spore type is greatest at 16 degrees Celsius, this is also the optimal temperature for infection. Temperature is something that the flies can exploit to increase their survivability.

Infected flies exhibit a behavior fever, where the fly will try to find hotter areas during the first few days of infection. The hosts that are able to stay in hotter areas, temperatures over 40 degrees Celsius, will have a higher survival rate (4, 5). If the flies don’t exhibit this behavior early enough it won’t be able to kill off the fungus. Such behavior is because the flies can’t efficiently regulate their body temperature. As the infection progresses the fly will seek out a cooler area and succumb to the pathogen. Some E. muscae isolates have been observed that are highly resistant to the behavioral fever. So if conditions are right it is very easy for an epizootic to occur within the fly population.

More research is currently being done to see how feasible it is to use biological controls instead of pesticides. It is true that infected flies take much longer to die than those exposed to a pesticide, but they still consume significantly less than healthy flies (5). Unlike pesticides E. muscae can be very specific and only affect a small number of species, without causing detrimental damage to the environment. The possibility of using E. muscae to keep fly populations low, near crops could be a huge boon and is worth looking into implementing.



Works Cited

1. Jensen, Annette, et al. “intraspecific variatio and host specificity of entomophthora muscae sesu stricto isolates revealed be random amplified polymorphic DNA, universal primed PCR, PCR restriction fragment length polymorphism and conidial morphology.” Invertebrate pathology 78, 251-259. January 21 2002.
2. Carruthers, RAymound, et al. “entomophthora muscae (Entomophthorales: Entomophthoracae) Mycosis in the Onion Fly, Delia antiqua (Diptera: Anthomyiidae).” Invertebrate pathology 45, 81-93. 1985.
3. Kramer, John. “THE HOUSE-FLY MYCOSIS CAUSED BY ENTOMOPHTHORA MUSCAE: INFLUENCE OF RELATIVE HUMIDITY ON INFECTIVITY AND CONIDIAL GERMINATION” new york entomological society. 88 p236-240. 1980.
4. Watson, D. et al. “behavioral fever response of musca domestica to infection by entomophthora muscae.” Invertebrate pathology 61 p10-16. 1993.
5. Roy, H. E., Steinkraus, D. C., Eilenberg, J., Hajek, a E., & Pell, J. K. (2006). Bizarre interactions and endgames: entomopathogenic fungi and their arthropod hosts. Annual review of entomology, 51, 331-57. doi:10.1146/annurev.ento.51.110104.150941
6. Zurek, L., Wes Watson, D., Krasnoff, S. B., & Schal, C. (2002). Effect of the entomopathogenic fungus, Entomophthora muscae (Zygomycetes: Entomophthoraceae), on sex pheromone and other cuticular hydrocarbons of the house fly, Musca domestica. Journal of invertebrate pathology, 80(3), 171-6. Retrieved from PubMed
7. Thomsen, L., & Eilenberg, J. (2000). Entomophthora muscae resting spore formation in vivo in the host Delia radicum. Journal of invertebrate pathology, 76(2), 127-30. doi:10.1006/jipa.2000.4961