ecological barriers can minimize the exposure to fungus (James and Lighthart 1994;
Lacey et al. 1997; Askary and Brodeur 1999; Jaronski et al., 2004). Also, deleterious
effects of insect pathogenic fungi have various effect on predators and parasitoids
(Ashouri et al. 2004; Danfa and Van der Valk 1999; Hall 1981). For example,
exposure of parasitic wasp, Bracon hebetor (Hymenoptera: Braconidae) and
Apoanagyrus lopezi (Hymenoptera: Encyrtidae) to Metarhizium anisopliae
(Ascomycota: Hypocreales) and B. bassiana, resulted in 100% mortality of the
parasitoids. However, no infection was observed in the tenebrionid, Pimelia
senegalensis (Coleoptera: Tenebrionidae) and Trachyderma hispida (Coleoptera:
Tenebrionidae), exposed to high doses of the same isolates (Danfa and Van der
Valk 1999). There are a number of papers since the mid-2000s that indicate
behavioral barriers, whereby a parasitoid can detect mycosis and not oviposit.
Deleterious effect of EPFs on natural enemies especially on parasitoids depends
strongly to fungal isolate and its concentration, inoculation time of host and parasitoid, life stage of host and parasitoid and their behaviors (Askary and Brodeur
1999). Brooks (1993) listed parasitoids that are unable to complete their development due to premature deaths by fungus-infection.
The studies of Askary and Ajam Hassani (2009) on A. muscarius (¼ V. lecanii
isolate DAOM 198499) and Aphidius nigripes (Hymenoptera: Aphidiidae) on potato
aphid, M. euphorbiae clarified some of these host-parasitoid-pathogen relations.
They showed that both A. nigripes males and females were infected by high
concentrations of A. muscarius, however, females were three times less susceptible
than males. Adult wasps were also infected by fungus spores of inoculated plants;
however, the mortality of parasitoid was less than that of direct infection (sprayed on
adults). However, development of fungus mycelium was observed on mummies, but
mortality of parasitoid pupae was significantly lower than its larval stages (Askary
et al. 2007; Askary and Ajam Hassani 2009).
Results demonstrated that there was no transmission of fungus from infected to
healthy individuals during mating. Also, survival of healthy females, parasitism rate
and sex ratio of progeny are same of control, when infected males mated with
healthy females. Whereas, survival, the ability to mating and parasitism rate of
infected females decrease when a heavy concentration of fungi infects them. The
sex ratio and other biological traits of progeny were normal (Askary and Ajam
Hassani 2009).
In order to determine the possible role of Myzus persicae (Homoptera:
Aphididae) treated with B. bassiana on patch time allocation of the parasitoid
wasp, Aphidius matricariae (Hymenoptera: Aphidiidae), Rashki et al. (2009)
found that there was no significant difference in patch leaving time of the parasitoid,
either in presence or absence of fungus. Interaction between presence of eggplant
volatile and fungus did not have effect on patch time allocation. Moreover, they
observed A. matricariae has significant effect on transmission of B. bassiana from
M. persicae sporulating cadavers to non-treated aphids.
Fazeli-Dinan et al. (2016b) investigated virulence of three isolates of
A. dipterigenus (LRC190, LRC216 and LRC229) on third-instar nymphs of greenhouse whitefly, Trialeurodes vaporariorum (Hemiptera: Aleyrodidae), as well the
448
H. Askary et al.
Lacey et al. 1997; Askary and Brodeur 1999; Jaronski et al., 2004). Also, deleterious
effects of insect pathogenic fungi have various effect on predators and parasitoids
(Ashouri et al. 2004; Danfa and Van der Valk 1999; Hall 1981). For example,
exposure of parasitic wasp, Bracon hebetor (Hymenoptera: Braconidae) and
Apoanagyrus lopezi (Hymenoptera: Encyrtidae) to Metarhizium anisopliae
(Ascomycota: Hypocreales) and B. bassiana, resulted in 100% mortality of the
parasitoids. However, no infection was observed in the tenebrionid, Pimelia
senegalensis (Coleoptera: Tenebrionidae) and Trachyderma hispida (Coleoptera:
Tenebrionidae), exposed to high doses of the same isolates (Danfa and Van der
Valk 1999). There are a number of papers since the mid-2000s that indicate
behavioral barriers, whereby a parasitoid can detect mycosis and not oviposit.
Deleterious effect of EPFs on natural enemies especially on parasitoids depends
strongly to fungal isolate and its concentration, inoculation time of host and parasitoid, life stage of host and parasitoid and their behaviors (Askary and Brodeur
1999). Brooks (1993) listed parasitoids that are unable to complete their development due to premature deaths by fungus-infection.
The studies of Askary and Ajam Hassani (2009) on A. muscarius (¼ V. lecanii
isolate DAOM 198499) and Aphidius nigripes (Hymenoptera: Aphidiidae) on potato
aphid, M. euphorbiae clarified some of these host-parasitoid-pathogen relations.
They showed that both A. nigripes males and females were infected by high
concentrations of A. muscarius, however, females were three times less susceptible
than males. Adult wasps were also infected by fungus spores of inoculated plants;
however, the mortality of parasitoid was less than that of direct infection (sprayed on
adults). However, development of fungus mycelium was observed on mummies, but
mortality of parasitoid pupae was significantly lower than its larval stages (Askary
et al. 2007; Askary and Ajam Hassani 2009).
Results demonstrated that there was no transmission of fungus from infected to
healthy individuals during mating. Also, survival of healthy females, parasitism rate
and sex ratio of progeny are same of control, when infected males mated with
healthy females. Whereas, survival, the ability to mating and parasitism rate of
infected females decrease when a heavy concentration of fungi infects them. The
sex ratio and other biological traits of progeny were normal (Askary and Ajam
Hassani 2009).
In order to determine the possible role of Myzus persicae (Homoptera:
Aphididae) treated with B. bassiana on patch time allocation of the parasitoid
wasp, Aphidius matricariae (Hymenoptera: Aphidiidae), Rashki et al. (2009)
found that there was no significant difference in patch leaving time of the parasitoid,
either in presence or absence of fungus. Interaction between presence of eggplant
volatile and fungus did not have effect on patch time allocation. Moreover, they
observed A. matricariae has significant effect on transmission of B. bassiana from
M. persicae sporulating cadavers to non-treated aphids.
Fazeli-Dinan et al. (2016b) investigated virulence of three isolates of
A. dipterigenus (LRC190, LRC216 and LRC229) on third-instar nymphs of greenhouse whitefly, Trialeurodes vaporariorum (Hemiptera: Aleyrodidae), as well the
448
H. Askary et al.