Insect Control: Biological and Synthetic Agents - Index of

404 11: Entomopathogenic Fungi and their Role in Regulation of Insect Populations
Entomopathogenic fungi active in aquatic environments
usually produce fewer spores than those
infecting terrestrial insects. The mosquito pathogen
C. clavisporus produces around 10 4 conidia/cadaver
(Cooper and Sweeney, 1986). Culicinomyces produces
nonmotile, true conidia, as do other Hyphomycetes.
Other aquatic insect pathogenic fungi belong
to fungal groups that can produce both motile and
nonmotile spores. The oomycete L. giganteum
produces both motile, biflagellate zoospores and
sexually produced oospores (Kerwin and Petersen,
1997). The zoospores are released from both zoosporangial
vesicles and oospores. Up to 20 000 sporangia
can develop in a mosquito larval host, each
releasing zoospores (Couch and Romney, 1973).
Oospore production has been demonstrated to require
sterols (Kerwin and Washino, 1983). These
resistant and long-lived spores are produced within
host cadavers. Another group of mosquito pathogens,
Coelomomyces spp. (Chytridiomycetes) also
has two infective stages. Resistant sporangia from
mosquitoes release motile haploid zoospores, while
the biflagellate diploid zygotes form within or after
release from the obligate secondary host, usually a
copepod (Lucarotti et al., 1985). The zygotes and
zoospores are similar. Sporangia in infected mosquitoes
can number from 100 to 15 000, releasing up to
5000 motile zoospores from each sporangium (Pillai
and O’Loughlin, 1972).
Fluctuating conditions of temperature or humidity
interrupt maximum spore production for most fungi.
In addition, light and dark cycle influence the sporulation
of some entomopathogens, but not others.
At least nine entomophthoralean fungi cause host
mortality in diurnal rhythms (Milner et al., 1984;
Mullens, 1985; Tyrrell, 1987; Eilenberg, unpublished
data), triggered by the onset of light (dawn) (Milner
et al., 1984). This timing of host death seems important
to allow the fungus to maximize the early
morning dew period for sporulation. Conidial discharge
of Z. radicans demonstrates circadian rhythms
under alternating light and dark regimes, with more
conidia discharged in the dark (Yamamoto and
Aoki, 1983). Erynia/Pandora neoaphidis produced
around 500 000 primary conidia from infected
aphids under ideal conditions, but changing from
high to lower humidities and back often stopped,
or at least severely reduced, the number of conidia
produced (Glare and Milner, 1991).
Resting stages represent a different strategy for
entomopathogenic fungi. While primary spores are
produced in large quantities by members of the
Entomophthorales, they last for only a few days;
however, resting spores can survive for months to
even years. This allows them to survive periods of
unfavorable conditions and cause infections the next
season through production of germ conidia. Resting
spores are produced within infected cadavers.
Factors that influence the production of resting
spores include developmental stage of the host,
temperature, humidity, and inoculum density
(e.g., Shimazu, 1979; Glare et al., 1989). With
Z. radicans, which infects aphids, there is evidence
of cytoplasmic based genetic elements involved in
resting spore production, with more resting spores
produced when aphids are inoculated with dual
strains (Glare et al., 1989). The ability to produce
resting spores varies with individual isolates. With
E. maimaiga infecting gypsy moth, the primary determinant
of resting spore production was larval
instar, with infections of later instars producing the
most resting spores (Hajek and Shimazu, 1996).
11.3.5. Transmission and Dispersal
Dispersal of infective propagules is a crucial component
of survival, and entomopathogenic fungi use
different strategies to maximize the chances of encountering
new hosts. For Hyphomycetes and some
other groups that produce copious numbers of
spores, wind, rain, and invertebrates play a role in
transmission. Generally, wind is a major aid for the
distribution of conidia. The minimum airspeed required
for dislodgement of N. rileyi was calculated
to be 2.7 km h 1 (Garcia and Ignoffo, 1977).
Entomophthorales generally forcibly discharge
the primary conidia, increasing the distribution of
these short-lived conidia. Distribution can also be
aided by the type of spore formed, with both the
forcibly discharged and sessile capilliconidia produced
by some Entomophthorales. The aphid pathogen
Neozygites fresenii discharges about 3000
primary spores per cadaver, and Steinkraus et al.
(1999) detected up to 90 000 primary conidia per
cubic meter of air during the nighttime in a Louisiana
cotton crop, indicating how successful forcible
dispersal aided by air movement can be. However,
for N. fresenii, most infections come from the capilliconidia,
which are more resistant to the environment
than primary conidia. With Z. phalloides, it
has been demonstrated how aphids collect capilliconidia
on their legs when walking across leaf surfaces,
making this spore type ideal for infecting
low-density mobile hosts (Glare et al., 1985).
Another mechanism to assist dispersal is through
growth of hyphae out of a cadaver. The Cordyceps
spp. and some of their anamorphs produce extensive
stroma, which can grow more than 30 cm (e.g.,
Evans, 1982) and produce sexual and/or asexual
spores at the end. Even common asexual species