Insect Control: Biological and Synthetic Agents - Index of

11: Entomopathogenic Fungi and their Role in Regulation of Insect Populations 405
such as B. bassiana sometimes grow several centimeters
from the infected cadaver in soil. Movement
of spores in the soil environment is much more
limited than distribution in water or air. However,
there is some movement of spores in soil, whether
down the soil profile by water movement, or
through distribution by invertebrates.
Insect behavior can assist dispersal. Some fungus
mediated behavioral changes have been recorded,
such as ‘‘summit disease’’ where infected grasshoppers
climb to the top of plants to die (see Section
11.3.3.2). This may aid spore dispersal, but it has
also been suggested that it is a mechanism by which
the host reduces infection through increased exposure
to UV. Movement of insects such as scavengers
(e.g., collembolans; Dromph, 2001), natural enemies
(e.g., coccinellid predators or parasitoids; Roy
and Pell, 2000; see also Section 11.3.6), and pollinators
(e.g., honeybees; Butt et al., 1998) can act to
disperse fungal inoculum. In some situations, insects
may actually be attracted to diseased cadavers. For
instance, adult Rhagonycha fulva have been observed
to visit cohort cadavers (Figure 16). Use of
insects to disseminate beneficial microbial control
agents is further discussed by Vega et al. (2000).
Insect behavior can also lead to avoidance of
infection. There is evidence that some insects
actively avoid spores of entomopathogenic fungi.
Scarab larvae were found to move away from soil
containing M. anisopliae mycelia, but not from conidia
(Villani et al., 1999). The same species laid eggs
preferentially in areas where mycelia were present,
presumably because the mycelia respiration mimics
plant root growth. Social insects are particularly
adept at behavioral methods to avoid disease. For
instance, termites have been shown to avoid conidia
of M. anisopliae (Milner and Staples, 1996), and the
common vespid wasps and honeybees use hygienic
behavior to eject diseased individuals from the nest
to reduce disease transmission (Gilliam et al., 1983;
Harcourt, unpublished data).
Some fungi use the host to aid dispersal directly.
The fungus S. castrans sporulates from live hosts
(Figure 18), thereby increasing distribution. Transmission
in this species is also assisted by collembola,
which can colonize the abdominal holes where the
conidia are produced (Griffiths, 1985).
The production of resting spores is a major factor
in transmission of many fungi, allowing the fungus
to avoid unfavorable environmental conditions or
lack of host. Resting spores do not synchronically
germinate for most species of the Entomophthorales,
increasing the temporal distribution of inoculum
and the chances the fungus will eventually encounter
new hosts. These spores can be long lived.
Figure 18 Life cycle of Strongwelsea castrans. (1) Pupae of
D. radicum overwinter in the soil. (2) During spring, it is assumed
that infective conidia of S. castrans are produced and discharged
from resting spores in the soil. (3) Adult D. radicum emerge from
pupae during spring and become infected by the conidia; one to
two abdominal holes appear in the insect as a result of infection.
(4) Conidia are forcibly discharged from the abdominal holes up
to approximately 30 mm while the fly is still alive. (5) Discharged
conidia, eventually after replicative conidiation, infect other
adult D. radicum. Several successive infection cycles can take
place during one season in the host population. (6) After midsummer,
some S. castrans infected D. radicum develop resting
spores instead of conidia. Following an incubation period, flies
filled with resting spores die and drop to the soil surface.
(7) Thick-walled resting spores survive in the soil layers during
winter. (8) An alternative dipteran host gets infected. (9) A hole
develops and primary conidia are discharged.
Persistence of E. maimaiga resting spores was found
to be up to 6 years in forest soils (Weseloh and
Andreadis, 1997), while the infection of the 17-year
cicada by Massospora apparently depends upon
resting spore germination over the full time frame
(Soper et al., 1976).
Transmission in many terrestrial fungi is dependent
upon high humidity, with moisture required for
sporulation and germination of conidia. It is not
surprising that fungi have evolved to take advantage
of the early morning dew through timing of host
death. Timing death to occur just prior to dusk
allows many entomophthoraleans to sporulate during
the humidity of early morning. Despite the active
discharge, conidia of Entomophthorales rarely
reach above crop canopies and for Pandora neoaphidis,
did not travel more than 1 m, even with wind
assistance (Glare and Milner, 1991).
The ability to attack multiple life stages is important
in disease transmission. Winged insects can be
responsible for the spread of disease, especially