My head was turned by this scene of high fungal drama at Sheffield Park, East Sussex, last Saturday. A fly, clinging on tightly atop a patch of nettles, wings outstretched. Dead.
Looking closer, I spotted the fungus, consuming and growing out of its host.
The amateur entomologist in my life tells me this is a Yellow Dung Fly Scathophaga stercoraria. It's been infected by an Entomophthora fungus; I guessed that much as Sussex naturalist Jamie Burston had posted similar images on Twitter a few days before, here.
In idle Googling of this species, I was intrigued to find an account from Pevensey, East Sussex, from 11 June 1933 when a Mr H. M. Edelsten found "a large patch of nettle, every shoot of which was covered with dead dung-flies. There must have been many thousands in this one patch..." The specimens collected by Mr. Edelsten were identified as S. stercoraria (Hobby & Elton, 1935).
What is this fungus that stalks the nettle patches of Sussex, killing flies one by one, or in their thousands? I had to know.
Spooner & Roberts give a brief introduction to the Entomophthoraceus fungi (Entomophthorales) in their book 'Fungi' (2005). Taking Entomophthora muscae as an example, they explain that the fungus can affect host flies' behaviour in different ways, depending on whether conidia or resting spores are produced. Infected flies producing conidia die above ground in the late afternoon, adopting a position which is favourable to the dispersal of the spores, and the spores are then discharged at night when conditions are ideal for germination.
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| Life cycle of Entomophthora muscae infecting a muscoid fly. From Gryganskyi et al (2017) (CC-0) |
I came across this illustration of the Entomophthora muscae lifecycle over on ResearchGate and it features in an open access article: 'Hijacked: Co-option of host behavior by entomophthoralean fungi' by Gryganskyi et al (2017), well worth a read for its dramatised introduction (conidia – the asexual spores of the fungus – are described as "biological bullets of death", which is one way of looking at it; a mycologist might point out they are also, quite literally, biological bullets of life...).
The authors encourage the reader to "note lifelike stance". This appearance of life in death is part of the fungus's game. A study by Møller (1993) found that, "Males especially were attracted to and behaved sexually towards dead, infected flies even when a choice was available between a dead, infected fly and a dead, uninfected individual. The abdomen of infected flies swelled considerably as a consequence of infection, and uninfected female flies with larger abdomens are more fecund than the average female and maybe more attractive."
What I think Møller is saying here is, FLIES LIKE BIG BUTTS (maybe) and Entomophthora muscae is perhaps exploiting this prediliction to spread its spores. The results of Møller's study are, however, not entirely conclusive on the question of what it is about fungus-infected female flies that makes them so darn sexually attractive (to male flies).
Anyway, all this biology stuff is fascinating. But this blog is about IDENTIFYING fungi.
Spooner & Roberts (2005) explain that identification of the Entomophthorales often presents problems but mention that Waterhouse & Brady's 'Key to the species of Entomophthora sensu lato' (1982) is still useful, and they also reference Keller's work on this group.
I managed to track down Waterhouse & Brady's key and found it includes some nice illustrations of the microscopic features of the various species. This, for example, is what conidia from species in the Entomophthora muscae complex look like:
This was motivation enough for me to spend the rest of the morning scraping stuff off the dead fly I'd collected, so that I could get a look at it under the microscope.
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| Stuff I'd scraped off a dead fly, mounted in water at 400x magnification. |
I reckon I've found me some conidia there, and they look about right for Entomophthora muscae sensu lato. That doesn't help much with identifying my collection to species though, since I read that "E. muscae sensu stricto and E. scatophagae are virtually indistinguishable using conidial characteristics" (Jensen et al, 2006).
In Keller's treatment of the genus Entomophthora (2002), he talks about how to separate E. muscae sensu stricto from other closely related species, including E. scatophagae, noting that, "So far only a single species of Entomophthora was found to attack the [Yellow Dung Fly Scathophaga stercoraria] which can, therefore, be considered as E. scatophagae."
On that basis, I think I can reasonably determine my collection as Entomophthora scataphagae Giard. Having delved this far into the depths of the internet, I thought I'd have a go at tracking down Giard's original description. With a bit of help from MycoBank, I managed to find it in the Biodiversity Heritage Library. Giard (1888) talks about E. scataphagæ [sic] differing from E. muscae in having spores which are "d'une couleur jaune" ~ of a yellow colour ~ and I reckon I could convince myself that the spores in my collection have a touch of yellow about them.
More recently, Jensen et al (2006) have been using molecular data to re-assess the Entomophthora muscae species complex, looking at host range, morphological and genetic characteristics to reach "an operational species definition", i.e. a reliable way of telling these cryptic species apart. They find that E. scataphagae is genetically distinct from, albeit closely related to E. muscae sensu stricto and note that, "The high host specificity of these fungi emphasizes the importance of identifying the host taxon at species level in the recognition of Entomophthora species."
So I guess a take-home message for mycologists wanting to get into Entomophthora is 'find a friendly dipterist' to help you with those fly IDs.
A note on names
Entomophthora scataphagæ / scataphagae / scataphaga ? I have followed Keller and other authors in using scataphagae, although I note this species is listed on MycoBank and the NBN Atlas as scatophaga.
References
Giard, A. (1888). Fragments biologiques. XI. Sur quelques Entomophthorèes. Bulletin Scientifique de la France et de la Belgique. 19:298-309. URL: https://biodiversitylibrary.org/page/10723150
Gryganskyi, A.P., Mullens, B.A., Gajdeczka, M.T., Rehner, S.A., Vilgalys, R. & Hajek, A.E. (2017). Hijacked: Co-option of host behavior by entomophthoralean fungi. PLoS pathogens, 13(5). URL: https://doi.org/10.1371/journal.ppat.1006274
Hobby, B.M. & Elton, C. (1935). Mortality in the Dung-fly, Scatophaga stercoraria. Journal of the Society for British Entomology 1935 Vol.1 Part 3 pp.71-72. URL: https://www.biodiversitylibrary.org/item/224780#page/87/mode/1up
Jensen, A.B., Thomsen, L. & Eilenberg, J. (2006). Value of host range, morphological, and genetic characteristics within the Entomophthora muscae species complex. Mycological Research Vol. 110 Issue 8 pp.941-950. URL: https://doi.org/10.1016/j.mycres.2006.06.003
Keller, S. (2002). The genus Entomophthora (Zygomycetes, Entomophthorales) with a description of five new species. Sydowia. 54:157-197. URL: https://www.zobodat.at/pdf/Sydowia_54_0157-0197.pdf
Møller, A.P. (1993). A fungus infecting domestic flies manipulates sexual behaviour of its host. Behav Ecol Sociobiol 33: 403. URL: https://doi.org/10.1007/BF00170255
MycoBank. (2019). Search for "Entomophthora scatophaga". URL: http://www.mycobank.org/BioloMICSDetails.aspx?Rec=321312 [accessed 19/05/2019]
NBN Atlas (2019). Search for "Entomophthora scatophaga". URL: https://species.nbnatlas.org/species/BMSSYS0000045310 [accessed 19/05/2019]
Spooner, B. & Roberts, P. (2005). Fungi. The New Naturalist Library, Collins. pp. 175-178.
Waterhouse, G.N. & Brady, B.L (1982). Key to the species of Entomophthora sensu lato. Bulletin of the British Mycological Society Vol. 16 Issue 2. pp. 113-143. URL: https://doi.org/10.1016/S0007-1528(82)80006-0
For the record
Date: 11/05/2019
Location: Sheffield Park, East Sussex
Grid reference: TQ412235
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