If you were in the European silkworm business two or three hundred years ago the last thing you wanted to find in your colony were stiff dead caterpillars. Worse still would be if when you picked them up and bent them, they snapped in half and revealed a solid white or green interior, giving them the appearance of a stick of chalk. Horror stricken you realise that your beloved silkworms have been struck down by white or green muscardine disease, or if you were an Italian, calcino; in both cases the name refers to the chalk like appearance of the inside of the stricken larvae. By the middle of the 19th century the combined effects of the industrial revolution, the revival of the Japanese silk industry and an epidemic of viral and fungal diseases had pretty much shut down the European silk industry (Federico, 1997). We now know that the muscardine diseases are caused by the entompathogenic fungi Beauveria bassiana and Metarhizium anisipoliae, although this was not realised until the early part of the 19th Century when the Italian naturalist Agostino Bassi discovered their true nature.
So what about the aphids I hear you asking? I have written earlier about the attacks that aphids have to suffer from predators and parasitoids, but that is not all with which they have to contend. Fungal diseases (Dean &Wilding, 1973; Rabasse et al., 1982; Aqueel & Leather, 2013) also attack aphids in the same way that they attack most other insects. In the case of aphids, it is not one of the muscardines, instead they are attacked by a number of fungi belonging to the Entomophthoraceae. The first member of this family to be recognised as a fungus was named Empusa musca (now Entomophthora muscae) by Charles de Geer in 1782 (Cohn, 1855). As the name suggests, it attacks house flies. There are, however, a number of different entomopathogenic fungi that specialise in attacking aphids, Erynia neoaphidis, and other members of the Entomophtoraceae, being the most commonly seen (Dean & Wilding,
An aphid unfortunate enough to encounter an insect infecting fungal spore and lacking the appropriate symbionts (Parker et al., 2013) is very likely to suffer a slow and lingering death as the fungal mycelia proliferate within its body.
Aphid infected by Pandora (Erynia) neopahidis https://commons.wikimedia.org/wiki/File:Pandora_neoaphidis.jpg
Pandora neoaphidis infected pea aphids (photo Tom Pope)
On landing on a susceptible aphid, the fungal spore germinates and the germ tube penetrates the aphid, either directly through the cuticle or via a nearby spiracle. Unlike those other invidious invaders of aphids, the parasitoids, entomopathogenic fungi need very specific environmental conditions to successfully colonise their aphid hosts. The damper the better, and if the aphid is surrounded by liquid water the more likely the fungus is to be able to effect an entry (Wilding, 1969; Dean & Wilding, 1973). More than a century ago Paul Hayhurst of Harvard University noticed that galls of the Chenopodium aphid, Hayhurstia atriplicis (then known as Aphis atriplicis) that were ruptured and had allowed water in, had a much higher incidence of diseased aphids than the intact galls (Hayhurst, 1909). Another more recent indication of this dependence on damp conditions is a mention of a high incidence of Pandora neoaphidis (described as Empusa aphidis) on Schizolachnus pini-radiatae being associated with higher than average rainfall (Grobler, 1962).
The earliest experiment involving aphid specific entompathogenic fungi that I have been able to find is from the latter half of the 19th Century (Houghton & Phillips, 1885).
“I placed some infected aphides under a glass with healthy specimens from my garden-beans and in a short time these became similarly covered with the same red-coloured fungoid growth. The n*****s took the scarlet fever and died.”
Their conclusion was that it was an Entomopthora species, perhaps related to, if not, E. planchoniana.
Although fungal pathogens have been shown to be able to reduce aphid populations in the field (Fluke*, 1925; Grobler et al., 1962; Plantegenest et al., 2001), their effectiveness as biological control agents on their own is variable and unpredictable (Milner, 1997). Most often, they are used either as biopesticides, or in conjunction with parasitoids and predators (e.g. Milner, 1997; Aqueel & Leather, 2013). One of the problems that entompathogenic fungi have is ‘finding’ their hosts. While it is known that entompathogenic fungi, as with entomopathogenic viruses, affect the behaviour of many insect that they attack (Hughes et al., 2011), by making them move to locations on their host plant where they are more likely to infect their kin, as far as I know, there is only one record of this for aphids (Harper, 1958). Surely a productive avenue of research to follow? That said, these clever fungi have another option up their mycelial sleeves. They are, like other fungi, able to discharge their spores explosively. Erynia neopahidis can project its spores more than 3mm vertically and more than 5 mm horizontally (Hemmati et al., 2001). This may seem a tiny distance to you and me, but the spores only need to get further than 2 mm to get air borne and move on to other plants or plant parts. It might be a leap into the unknown but it seems to work out all right for the fungi 🙂
Aqueel, M.A. & Leather, S.R. (2013) Virulence of Verticillium lecanii (Z.) against cereal aphids; does timing of infection affect the performance of parasitoids and predators? Pest Management Science, 69, 493-498.
Cohn, F. (1855) Empusa muscae und die Krankeit der Stubenfliegen Nova acta Academiae
Caesareae Leopoldino-Carolinae Germanicae Naturae Curiosorum, 25, 301-360
Dean, G.J. & Wilding, N. (1973) Infection of cereal aphids by the fungus Entomophthora. Annals of Applied Biology, 74, 133-138.
Federico, G. (1997 ) An Economic History of the Silk Industry, 1830-1930. Cambridge University Press, Cambridge.
Fluke, C.L. (1925) Natural enemies of the pa aphid (Illinoia pisi Kalt.); their abundance and distribution in Wisconsin. Journal of Economic Entomology, 18, 612-616.
Grobler, J.H., MacLeod, D.M. & Delyzer, A.J. (1962) The fungus Empusa aphidis Hoffman parasitic on the wooly pine needle aphid, Schizolachnus pini-radiatae (Davidson). Canadian Entomologist, 94, 46-49.
Harper, A.M. (1958) Notes on behaviour of Pemphigus betae Doane (Homoptera: Aphididae) Infected with Entomophthora aphidis Hoffm. Canadian Entomologist, 90, 439-440.
Hayhurst, P. (1909) Observations on a gall aphid (Aphis atriplicis L.). Annals of the Entomological Society of America, 2, 88-100.
Hemmati, F., Pell, J.K., McCartney, H.A., Clark, S.J. & Deadman, M.L. (2001) Conidial discharge in the aphid pathogen Erynia neoaphidis. Mycological Research, 105, 715-722.
Hughes, D.P., Andersen, S.B., Hywel-Jones, N.L. , Himaman, W., Billen, J. & Boomsma, J. (2011) Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection. BMC Ecology, 11, 13.
Milner, R.J. (1997) Prospects for biopesticides fro aphid control. Entomophaga, 42, 227-239.
Parker, B.J., Spragg, C.J., Altincicek, B. & Gerardo, N.M. (2013) Symbiont-mediated protection against fungal pathogens in pea aphids: a role for pathogen specificity. Applied & Environmental Microbiology, 79, 2455-2458.
Plantegenest, M., Pierre, J.S., Dedryver, C.A. & Kindlmann, P. (2001) Assessment of the relative impact of different natural enemies on population dynamics of the grain aphid Sitobion avenae in the field. Ecological Entomology, 26, 404-410.
Rabasse, J.M., Dedryver, C.A., Molionari, J. & Lafont, J.P. (1982) Facteurs de limitation des populations d’Aphis fabae dans l’Ouest de la France 4. Nouvelles donnees sur le deroulement des epizooties entomophtoracees sur feverole de printemps. Entomophaga, 27, 39-53.
Roditakis, E., Couzin, J.D., K., B., Franks, N.R. & Charnley, R.K. (2000) Improving secondary pick up of insect fungal pathogen conidia by manipulating host behaviour. Annals of Applied Biology, 137, 329-335.
Wilding, N. (1969) Effect of humidity on the sporulation of Entomophthora aphidis and E. thaxteriana. Transactions of the British Mycological Society, 53, 126-130.
*I had to include this reference as he mentions the aphidozer whatever that is! I can only guess as he doesn’t explain in his methods or cite a reference:-)