Entomophthorales

The Entomophthorales are fungi with non-cellular mycelium, currently categorized in the class Zygomycetes. However, the exact taxonomic position of some families is uncertain and can vary depending on the authors. They bring together six families, three of which,  Ancylistaceae, Entomophthoraceae and Neozygitaceae mainly contain species pathogenic for insects, 223 in all including 26 that attack aphids. In France a dozen species are frequently encountered on aphids, whereas the others are rare or absent.

The pathogen's development cycle in its host is just about the same, whatever the species considered:

• The mycelium (hyphal body) in dead bodies of insects killed by an entomophthoral sporule when the ambiant relative humidity comes close to 95% for several hours (often at the end of the night): conidiophores (mycelium filaments) develop on the outside of the dead insect, carrying on their end a conidium, a propagule of asexual reproduction that disseminates the pathogen among the host population. In some species, the conidium is multinucleate, which makes it a sporeless sporangium. Depending on the species, the conidia measure between 15 and 50mm.
• As the conidium matures, it establishes an osmotic differential pressure between the conidiophore and the conidium, so the latter is violently ejected several millimetres, even more than 1cm, away from its original position. In some species, the primary conidium forms a secondary one which is the real infectious form.
• When this conidium touches a living aphid and if by chance the ambient relative humidity stays between 90 and 100%, it sprouts, then develops a germinative filament which penetrates the aphid’s cuticle then propagates, first as protoplasts in certain species, then short mycelium filaments lined with walls, forming the hyphal bodies. At the same time the fungi continue to proliferate inside most of the insect’s tissues, beginning with the fat bodies. After about 60 hours at 20°C, the majority of the tissues have been “digested.” All that remains are the embryos, some of which can be expelled, and then the aphid dies after 4 days on average at 20°C.
• The cycle starts again, with the dead aphid body sporulating. First to be contaminated is its own offspring which is generally found huddled around it.

In many species, the infection cycle can be interrupted by resilient spores, formed in the aphid’s body from the hyphal bodies, which in this case produce no or very few conidia. These durable spores are strongly dehydrated and enclosed within a thick protective wall. These features are adaptations giving resistance, factors for preserving the inoculum in the ground. They are formed either by encystment of a mycelium filament (azygospores) or, in other species like the Neozygites, by the combination of two filaments, in which case they are zygospores.

The Entomophthorales are one of the most important factors in regulation of aphid populations when conditions enabling them to be effective are met. Weather or climatic conditions are the most significant, because very high relative humidity is essential for these fungi to accomplish the two key stages of their life cycle: sporulation and infection. For this reason their activity is more regular and generalized in the oceanic regions, where relative humidity is high, not only at night time but continuing throughout the day when rain or drizzle arrives. They can also be strongly and regularly active in irrigated zones.

Biotic factors can also favour the spectacular effects of some epizootics caused by Entomophthorales, like the aggregation response of the aphid populations. The example always taken is the total destruction of colonies of black bean aphid, Aphis fabae, in the west of France, by two principal species of Entomophthorales, Pandora neoaphidis and Neozygites fresenii. These can intervene in the space of a few days, owing to the massive propagation of inoculum within the aphid colonies attached in a dense cluster of several tens of centimetres around the stems.