Introduction to Fungi, Third Edition

ENTOMOPHTHORALES
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germination (Webster et al., 1978). Type 1 conidia
may show 1 1, 1 2 and 1 3 germination. Of the
16 (i.e. 4 4) possible interconversions, 12 have
been observed so far (Webster, 1987). The only
type of conidium shown to be infective is the
secondary globose, i.e. type 2, conidium (Hywel-
Jones & Webster, 1986b). It is sometimes termed
an invasive conidium. This kind of conidium
only develops from cornute conidia, although
these may be primary or secondary. When a
secondary globose conidium is in contact with an
insect cuticle, a short germ tube develops with
an appressorium at its tip. Penetration of the
cuticle seems to be mainly by enzymatic means
and is followed by the formation of multinucleate,
branched hyphal bodies in the haemocoel.
It is presumed that the other kinds of
conidia function as dispersal rather than infection
units, and they can be found in appreciable
numbers trapped in foam near infected flies. It
appears that only adult flies are infected through
the cuticle. Although all types of conidia are
known to be present in larval guts, there is no
evidence that larvae are infected from ingested
conidia. Survival over winter, when adult insects
are not available, is by globose, thick-walled
zygospores which are formed within the dead
body of an insect, surrounded by a network of
brown hyphae.
The precise physical conditions associated
with the different types of germination in
E. conica are not known and most attention has
been devoted to the germination of the primary
cornute (type 1) and secondary globose (type 2)
conidia (Nadeau et al., 1995, 1996). Germination
of the latter, resulting in appressorium formation
and cuticular penetration on wings of the
susceptible host S. rostratum, occurs over the
temperature range of 15 25°C with an optimum
at 20°C. Germination occurs within 2 h and
penetration within 9 h. The development of
appressoria is related to the presence of a coating
of lipid on the host cuticle. In experiments in
which lipids were removed from susceptible
blackfly wings, there was no discernible appressorium
formation or cuticular penetration. On
the non-susceptible host S. decorum, germination
is delayed and appressorium formation and
cuticular penetration do not occur. Instead, a
high level (26%) germination of the 2 1 type
takes place.
The plasticity of asexual reproduction shown
by E. conica is not unique. Similar versatility
is shown by some other members of the
Entomophthoraceae which grow on insects
with aquatic larval stages such stoneflies
(Plecoptera) and crane flies (Tipulidae) (Descals
& Webster, 1984).
Entomophthora muscae
There are about a dozen species of Entomophthora,
occurring as widespread insect pathogens
(Samson et al., 1988; Humber, 1997). They are
characterized by unbranched conidiophores and
multinucleate primary conidia which are
projected by a squirt mechanism. Secondary
conidia may form on germination of the primary
conidia, but these are discharged by a septal
eversion mechanism similar to that described
above for Erynia and Conidiobolus. Sexual reproduction
is by the formation of zygospores and
azygospores.
The best-known taxon is E. muscae which is, in
fact, a complex of about five species with similar
morphology and spore dimensions (MacLeod
et al., 1976). This fungus is a parasite of houseflies
and other Diptera. Disease is apparent in summer
to autumn and is more frequent in wet weather.
In the field, epizootics occur in places where there
are dense populations of potential hosts, for
example dung flies (Scatophaga spp.) on farms, or
hoverflies (Melanostoma spp.) attracted to the
honeydew secreted by Claviceps (see Fig. 12.26b)
on the moor grass Molinia. Diseased flies can
occasionally be found attached to the glass of a
window pane surrounded by a white halo about
2 cm in diameter made up of discharged conidia
(Plate 3g).
The dead fly shows a distended abdomen with
white bands of conidiophores projecting between
the segments of the exoskeleton. The unbranched
multinucleate conidiophores arise from the
coenocytic mycelium which plugs the body of
the dead fly. The conidia are also multinucleate
(Fig. 7.43b). They are projected by a forwardly
directed jet of cytoplasm from the elastic conidiophores.
On impact, the bitunicate nature of
the wall of the primary conidium becomes