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Biocontrol Science and Technology (2000) 10, 737 ± 752
Interactions Between Entomopathogenic Fungi and Other
Natural Enemies: Implications for Biological Control
HELEN E. ROY1 ,2 and JUDITH K. PELL1
1
Department of Entomology and Nematology, IACR-Rothamsted, Harpenden,
Hertfordshire, AL5 2JQ, UK; 2 Department of Life Sciences, Anglia Polytechnic
University, Cambridge CB1 1PT, UK
(Received for publication 11 Januar y 2000; revised manuscript accepted 30 July 2000)
Pathogens and arthropod natural enemies may contribute to the suppression of insect pest
population s either as individua l species or as species complexes. However, because natural
enemies of insects have evolved and function in a multitrophic context it is important to assess
interactions within complexes of natural enemies if they are to be exploited eVectively in pest
management. Natural enemies can interact either synergistically/additively (e.g. enhanced
transmission and dispersal of insect pathogens) or antagonisticall y (e.g. parasitism/infection,
predation and competition). In this paper, studies assessing the potential interactions between
insect and fungal natural enemies are reviewed. In general, these studies indicate the positive
nature of the interactions between arthropod natural enemies and fungal pathogens with respect
to the control of insect populations . More work is required to investigate further the many
ways in which the natural enemy community interacts in the agroecosystem
Keywords: entomopathogeni c fungi, insect natural enemies, interactions, ecological susceptibility, physiologica l susceptibility, biologica l control
INTRODUCTION
Natural enemies of insects have evolved and function in a complex multitrophi c environment
(Vet & Dicke, 1992; Poppy, 1997). Organisms are in¯ uenced by a range of abiotic and biotic
factors which aVect their physiology, ecology and behaviour. Interactions between organism s
within and between trophic levels are important factors aVecting the structure of population s
and communities. In this paper we review the possible eVects of such interactions in relation
to biologica l control strategies which incorporate the use of multiple species of natural
enemies. We largely focus on the interactions between fungal and insect natural enemies.
Multiple biological control species may act synergistically, additively or antagonisticall y
(Ferguson & Stiling, 1996). Synergistic interactions would result in a higher mortality than
the combined individua l mortalities of the pest population . Additive mortality occurs if the
natural enemies do not interact and, thus, the total level of mortality is equivalen t to the
Correspondence to: H. E. Roy. Tel:
+ 44 1223 363 271; Fax: + 44 1223 352 979; E-mail: [email protected]
ISSN 0958-3157 (print)/ISSN 1360-047 8 (online)/00/060737-16
DOI: 10.1080 /0958315002001170 8
€ 2000 Taylor & Francis Ltd
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H. E. ROY & J. K. PELL
combined individua l mortalities caused by each agent. Ferguson and Stiling (1996) recognized three possible antagonistic eVects. First the natural enemies could interact, resulting
in the total pest mortality being less than the additive mortality. Second, the total mortality
might be less than that caused by one natural enemy but not the other. Finally the total
mortality could be less than when either natural enemy acted alone. Thus, an increase in
the richness of natural enemy species could result in an increase in the host populatio n if
interference between the natural enemies is suYcient. Alternatively, a pest populatio n may
be reduced to a greater extent by multiple rather than single natural enemies if interference
between species is minimal or advantageou s to either species (Chang, 1996).
ADDITIVE/SYNERGISTIC INTERACTIONS
Enhanced Fungal Pathogen Transmission and Dispersal
The development of an epizootic (sudden increase in disease incidence within a population )
is dependent on properties of both the host population , the pathogen populatio n and an
eVective mechanism of transmission between the two. The transmission of a fungal pathogen
is dependent on a number of processes: conidia production, discharge, dispersal, survival
and germination (Hajek & St. Leger, 1994). The large number of conidia produced by
infected cadavers partially compensates for the high probabilit y that many conidia will not
actually infect a host (Shimazu & Soper, 1986). Indeed, the density and distribution of a
pathogen population is one of the most important factors determining whether a disease
becomes epizootic (Fuxa & Tanada, 1987; Carruthers et al., 1991). In an unmanaged host/
pathogen system, epizootics are usually host-density dependent, developin g as the host
populatio n increases. However, an epizootic may develop at low host densities if the pathogen
is widely distributed within the host habitat (Fuxa & Tanada, 1987). Pathogen population s
are often distributed at low densities or discontinuousl y in the host habitat and, therefore,
pathogen dispersal is essential (Fuxa & Tanada, 1987; Richards et al., 1994). Pathogens can
be dispersed in several ways: active discharge of infective spores (local dispersal), weather
factors (wind and rain) or by host and non-host dispersal (long distance dispersal) (Fuxa &
Tanada, 1987; Roy, 1997).
The presence of insect natural enemies may have an impact on local transmission of a
fungal pathogen. The presence of a foraging adult coccinellid, for example, resulted in a
substantial increase in the local transmission of the aphid pathoge n Erynia neoaphidis within
a populatio n of pea aphids, Acyrthosiphon pisum on individua l bean plants in the laborator y
(Roy et al., 1998). Foraging ladybird s cause an increase in aphid movement (Clegg & Barlow,
1982), although the degree to which this occurs depends on the aphid species and host plant
(MuÈller, 1983; Hajek & Dahlsten, 1987). The increase in movement of aphids in the presence
of foraging predators such as coccinellids would increase the probabilit y of the aphid coming
into contact with the sporulating cadaver, and therefore receiving more inoculum.
Increased transmission of fungal entomopathogen s between host insects at a local scale
has also been observed in systems where parasitoids forage. In a laborator y study by Furlong
and Pell (1996) the presence of the foraging parasitoid Diadegma semiclausum increased
the movement of Plutella xylostella larvae and consequently the transmission of the
entomopathogen Zoophthora radicans. In this study, larval movement was quanti® ed using
video techniques; larvae foraged on by D. semiclausum moved signi® cantly further and into
signi® cantly more new areas of leaf than control larvae. Interestingly, larvae foraged on by
a diVerent parasitoid, Cotesia plutellae, were intermediate in their movement and were not
more likely to become infected by the entomopathoge n than control larvae. This suggests
that there is a threshold of movement necessary for fungal transmission to be encouraged
and that this threshold was exceeded by larvae foraged on by D. semiclausum but not by
larvae foraged on by C. plutellae. Clearly, these interactions are complex and diYcult to
predict because they vary between insect natural enemies. In a similar study, the transmission
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INTERACTIONS BETWEEN ENTOMOPATHOGENIC FUNGI AND OTHER NATURAL ENEMIES
739
of E. neoaphidis was increased in the presence of the parasitoid Aphidius rhopalosiph i
(Fuentes-Contreras et al., 1998).
For transmission to occur over a larger spatial scale, pathoge n dispersal is essential
particularly if host population s are discontinuou s in the environment. Most pathogens
have a limited capacity for active dispersal; however, entomophthoralea n fungi (except
Massospora), produce conidiophore s that forcibly discharge primary conidia across the leaf
boundar y layer (Ingold, 1971; Steinkraus et al., 1996; Hemmati, 1999). Dispersal of conidia
over a greater distance requires physical factors such as rain and wind or dispersal by hosts
and non-hosts. Rain can remove pathogens in splash droplets or by vibration caused by the
impact of rain drops. Many studies have shown the importance of rain in the dispersal of
plant pathogens (Fitt et al., 1989; McCartney, 1990; Pedersen et al., 1994; McCartney,
1994), though this may be less important for some entomopathogen s such as E. neoaphidis
(Pell et al., 1997a). Wind is undoubtedly important in the long distance dispersal of many
fungal entomopathogen s (Wilding, 1970; Steinkraus et al., 1996; Hemmati, 1999) with most
fungal conidia being small (for example, E. neoaphidis primary conidia are approximately
25 l m in length and the conidia of Hyphomycetes are less than 10 l m) and capable of being
carried by wind currents. Dispersal of entomopathogen s by weather factors, however, is
random in contrast to dispersal by hosts and non-host vectors which is targeted.
The movement of infected hosts is considered to be one of the most important ways in
which a pathoge n is transmitted and dispersed to new habitats (Fuxa & Tanada, 1987).
Pathogens can also be dispersed by non-hosts such as invertebrate natural enemies of the
host which have become contaminated with the pathogen during foraging . Insect vectors
are important dispersal agents of many plant pathogens (Agrios, 1988; Nemeye et al., 1990;
Peng et al., 1992; Gillespie & Menzies, 1993). It has long been recognized that predators and
parasitoids contribute to the dissemination of viral entomopathogen s and the development of
epizootics (Smith et al., 1956; Stairs, 1965; Capinera & Barbosa, 1975; Reardon & Podgwaite,
1976; Andreadis, 1981; Levin et al., 1983), however, only a few more recent studies have
assessed the transmission of fungal entomopathogen s by non-host vectors (Schabel, 1982;
Poprawski et al., 1992; Pell et al., 1997b; Butt et al., 1998).
In a laborator y study, Roy (1997) demonstrated that adult coccinellids (Coccinella
septempunctata) which had foraged on plants with diVerent densities of sporulating cadavers
became contaminated with E. neoaphidis conidia and carried these conidia to uninfected
aphid populations , thereby initiatin g infection. Transmission was greatest when coccinellid
adults had previously foraged on plants with high densities of infected aphids (30 cadavers
per plant). However, even coccinellids which had foraged on plants with only one cadaver
became contaminate d with suYcient conidia to vector to a small proportion of the uninfected
aphids. Therefore, coccinellids may contribute to pathogen dispersal from aphid population s
even when the pathoge n density is low. In contrast, the number of conidia produced by an
individua l sporulating cadaver may not be suYcient for aerial dispersal because of its
random nature. The ability of coccinellids to aggregate in areas with large aphid densities
(Kareiva & Odell, 1987) would contribute to their role in pathogen dispersal by targeting
the pathogen to aphid population s.
This ability to vector pathogens between infected and uninfected host population s could
also be manipulate d for integrated pest management (IPM) if the vector can be arti® cially
contaminated with inoculum, perhaps using semiochemicals and contaminatio n stations as
has been done in other systems (for example Pell et al., 1993a; Furlong et al., 1995). Pell
et al. (1997b) demonstrated the potential of coccinellid adults to vector E. neoaphidis
passively to uninfected pea aphid population s after arti® cial contamination . Direct exposure
of aphids to adult coccinellids inoculate d with E. neoaphidis resulted in 10 per cent
E. neoaphidis infection. Furthermore, a similar proportion of aphids which were placed on
the plants previously foraged on by inoculated adult and larval coccinellids also succumbed
to E. neoaphidis infection (Pell et al., 1997b; Roy, 1997). The potential of coccinellid adults
to vector E. neoaphidis in a caged ® eld study has also been demonstrated (Roy, 1997).
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H. E. ROY & J. K. PELL
Inoculated coccinellids caused approximatel y ® ve per cent of the aphid population to become
infected by E. neoaphidis. Although this may appear to be a low percentage of infection,
under suitable conditions an epizootic could be initiated by such a level of infection (Pell
et al., 1997b; Roy et al., 1998).
Only a few other studies have examined the potential of arthropod natural enemies to
vector fungal entomopathogen s. In the study of Furlong and Pell (1996), although the
presence of a foraging parasitoid, D. semiclausum, increased the movement of P. xylostella
larvae and consequently the transmission of Z. radicans, there was no evidence that the
parasitoid vectored the pathogen to new P. xylostella populations. Similarly, the aphid
parasitoid A. rhopalosiphi did not vector E. neoaphidis between population s of aphids
(Fuentes-Contreras et al., 1998). Bene® cial insects, other than natural enemies, may provide
an alternative means of pathogen dissemination . For example, the ability of honey bees
(Apis mellifera) to eVectively vector the Hyphomycete fungus Metarhizium anisoplia e to
pollen beetles (Meligethes aeneus) has been demonstrated (Butt et al., 1998). Although
honey bees are susceptible to M. anisopliae (Ball et al., 1994), no detrimental eVects to the
honey bees were observed (Butt et al., 1998).
ANTAGONISTIC INTERACTIONS
An increase in the richness of natural enemy species could result in an increase of the host
if interference between the natural enemies is suYcient (Hochberg & Lawton, 1990).
Parasitism/infection, predation, and competition are three potentially antagonisti c interactions which would result in interference between insect and fungal natural enemy species.
Direct Infection of Non-target Insects by Entomopathogeni c Fungi
Entomopathogeni c fungi may reduce non-target insect population s by directly infecting
them. However, many entomopathogeni c fungi appear to have a limited host range and are
speci® c to single orders of arthropod hosts. In general, fungi from the order Entomophthorales commonly cause epizootics in insect population s (often foliar insects) and these
epizootics can eradicate population s at a local scale (Wilding & Brady, 1984; Glare &
Milner, 1989). Species of fungi within this order are generally considered to be highly host
speci® c (Lacey et al., 1997). For example, E. neoaphidis is the most common fungal species
infecting aphids in temperate regions (Wilding & Brady, 1984; Glare & Milner, 1989) and is
aphid-speci® c. Therefore, Entomophthoralea n fungi considered for pest management are
unlikely to constitute a risk to bene® cial insects and other non-target organisms unless those
organisms are very closely related to the target pest (Lacey et al., 1997). This was highlighte d
by the concerns raised on the release of Entomophaga grylli (pathotype 3) as a classical
biologica l control agent of grasshopper pests in the rangelands of the western USA
(Carruthers & Onsager, 1993). This fungus, while limited to Orthoptera, has a wide host
range with respect to North American grasshopper s with the potential that non-pest
grasshoppers may become infected (Lockwood, 1993). However, in the ® eld, only 8 out of
20 grasshopper species were infected and these were all pest species (Carruthers et al., 1997).
Although this limited host range makes them valuable potential biological control agents,
most entomophthoralea n fungi are quite diYcult to mass-produce and store, therefore, use
as inundativ e mycoinsecticides is currently limited.
In contrast, Hyphomycete fungi are only infrequently recorded causing substantial
epizootics (for example, Keller, 1986) and are generally considered to have wide host ranges
(Feng et al., 1994; Lacey et al., 1997). However, they can be mass produced commercially and
are, therefore, often augmented within pest insect population s as inundativ e mycoinsecticides
(Vinson, 1990; Lacey et al., 1997; Jaronski et al., 1998). Due to their perceived wide host
range, for example, Beauveria bassiana has been recorded infecting over 200 species of
insects in nine orders (Li, 1988; Feng et al., 1994) these fungi could potentially pose a threat
INTERACTIONS BETWEEN ENTOMOPATHOGENIC FUNGI AND OTHER NATURAL ENEMIES
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to non-targets. However, the pathogenicit y of fungal isolates from the same species towards
diVerent insect groups varies signi® cantly (Yeo et al., 1998). There is a tendency for fungal
isolates to have higher virulence to their original hosts or to closely related species than
more distant relatives (Xu, 1988; Goettel et al., 1990; Hajek & Butler, 1999). Examples of
host range studies of isolates from species in the Entomophthorale s and Hyphomycetes
against insect natural enemies speci® cally are described below.
Direct Infection of Insect Natural Enemies by Entomophthorale s
Zoophthora radicans is an entomophthoralea n fungus which is considered to have a relatively
broad host range because it has been recorded from a number of diVerent insect orders
(Hajek & Butler, 1999). This fungus is an important natural enemy of the diamondbac k
moth (P. xylostella) a crucifer pest. The parasitoids D. semiclausum and C. plutellae are also
common natural enemies of this moth and could therefore be at risk from infection by
Z. radicans. Laborator y studies demonstrated that C. plutellae never became infected with
Z. radicans; however, D. semiclausum was susceptible to Z. radicans but only at extremely
high doses of the fungus (Furlong & Pell, 1996). Diadegma semiclausum foraging in the
presence of infected larvae in the laborator y did not succumb to Z. radicans infection and
infected individual s were never observed in the ® eld, even during epizootics in diamondbac k
moth populations. For these reasons Furlong and Pell (1996) concluded that although the
parasitoid was clearly physiologicall y susceptible to Z. radicans, it was unlikely to be
ecologically susceptible in the ® eld. These ® ndings are consistent with other studies on
Z. radicans which have demonstrated that isolates are often unable to infect species from
orders other than the one from which they were isolated (Papierok et al., 1984; McGuire
et al., 1987; Magalhae s et al., 1988) and sometimes even from diVerent families within an
order (Mietkiewski et al., 1986; Pell et al., 1993b).
Direct Infection of Natural Enemies by Hyphomycetes
As already described, fungi within the class Hyphomycetes are generally considered to have
much wider host ranges than entomophthoralean fungi (Goettel & Inglis, 1997) and may
infect both the target pest species and their insect natural enemies (for example Magalhaes
et al., 1988). However, although many species of these fungi have been recorded from
numerous diVerent insect orders, isolates or strains within a species are frequently only
virulent to a few arthropod species (Feng et al., 1994; Yeo et al., 1998). Exposure of two
parasitoid species (Bracon hebetor and Apoanagyru s lopezi) to eleven isolates of M. anisopliae
and one isolate of B. bassiana, under development for control of grasshoppers and locusts,
resulted in 100% mortality of the parasitoids. However, no infection was observed in two
other non-target species, the tenebrionids Pimelia senegalensis and Trachyderma hispida,
exposed to high doses of the same isolates (Danfa & Van der Valk, 1999). A commerciallyformulated isolate of B. bassiana (Naturalis ) is reported to be extremely eYcient at
controlling a number of greenhouse pests, such as white¯ ies, thrips and mites but with no
impact on bene® cial insects (Wright & Kennedy, 1996). In a laborator y study, Poprawski
et al. (1998) assessed the pathogenicit y of B. bassiana and Paecilomyce s fumosoroseus to the
coccinellid Serangium parcesetosum, an important white¯ y predator. Serangium parcesetosum
were highly susceptible to B. bassiana but not to P. fumosoroseus (Poprawski et al., 1998).
As a species, Verticillium lecanii has been recorded from a number of insect and mite
hosts, but in glasshouse trials using target-derived isolates against aphids and white¯ y it did
not infect Tetranychus urticae (red spider mite), Phytoseiulus persimilis (spider mite predator)
or Encarsia formosa (white¯ y parasitoid) (Hall, 1981). Askary and Brodeur (1999) have
demonstrated that V. lecanii is pathogeni c to the aphid parasitoid Aphidius nigripes but only
when aphid population s are heavily infected by the fungus. Similarily P. fumosoroseus infects
the aphid parasitoid, Aphelinus asychis, but only at high pathoge n doses and at high humidity
(Lacey et al., 1997).
Another species of Hyphomycete, Nomuraea rileyi, primarily infects lepidopteran pests
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H. E. ROY & J. K. PELL
but natural epizootics of this fungus have also been observed in two species of Coleoptera
(Hypera punctata and Leptinotarsa decemlineata) (IgnoVo, 1981). However, various natural
enemies (predators (Hippodamia convergens, Chrysoperla carnea and Podisus maculiventris)
and parasitoids (Voria ruralis, Apanteles marginiventris, Campoletis sonorensis and Telenomus
proditor)) did not succumb to N. rileyi infection when exposed to high concentrations of
conidia (25 times higher than used in ® eld experiments to induce epizootics) in laborator y
bioassays (IgnoVo, 1981).
Ecological vs Physiological Susceptibility
Overall, many studies have shown that entomopathogeni c fungi with broad host ranges can
interact antagonisticall y with arthropod natural enemies but only under environmental
conditions that are optimal for the fungus (James & Lighthart, 1994; Lacey et al., 1997;
Askary & Brodeur, 1999). In these cases, `physiologica l susceptibility’ is demonstrated.
However, this may not represent `ecological susceptibility’ under more realistic conditions
in the ® eld which are likely to be suboptimal for the fungus. It is important to distinguish
between physiologica l and ecological susceptibility of predators and parasitoids to pathogens
when considering complexes of these natural enemies as biological control agents.
It is recognized that laborator y bioassays do not always re¯ ect infection levels that are
likely to occur in the ® eld (Goettel et al., 1990; Jaronski et al., 1998). A laborator y bioassay
on one particular isolate (strain GHA) of B. bassiana demonstrated that some predators
and parasitoids were susceptible, but in the ® eld the impact on the natural enemy complex
was minimal (Jaronski et al., 1998). The importance of conducting realistic ® eld experiments,
in addition to preliminary laborator y bioassays, has been further demonstrated through a
series of studies on the interactions between B. bassiana and the convergent ladybird,
H. convergens. Hippodamia convergens is a widespread, abundan t predator of aphids in the
USA. Laboratory studies demonstrated that H. convergens was susceptible to three fungal
pathogens currently being considered as biologica l control agents in the USA, B. bassiana,
M. anisopliae and P. fumosoroseus (James & Lighthart, 1994), which are all known to have
broad host ranges (Goettel et al., 1990). Field studies demonstrated that B. bassiana caused
75± 93% mortality of H. convergens early in the season but that late season application s had
little impact (James et al., 1995). Late season environmenta l conditions may not favour
B. bassiana mycosis in H. convergens. James et al. (1998) showed that, although fastest
germination and growth rates of B. bassiana occurred at temperatures in excess of 25ë C,
levels of mycosis in H. convergens decreased as temperature increased above this temperature.
It appears that temperature may be signi® cantly aVecting the defence of H. convergens
against B. bassiana. Indeed, some metabolic compounds induced by heat stress are known
to play a role in defending an insect against pathogen invasio n (James et al., 1998).
Interestingly, starvation and nutrition stresses increase the susceptibility of C. carnea to
B. bassiana (Donegan and Lighthart, 1989). Prevailin g environmenta l conditions will
undoubtedly aVect the physiology of the host and, hence, its susceptibility to a pathogen.
A further example demonstrating the diVerence between physiologica l and ecological
susceptibility comes from Entomophaga maimaga, an entomophthoralea n fungus associated
with many North American and Japanese lepidopteran species. The host speci® city of
E. maimaiga has been extensively studied because it is a potential biologica l control agent
of the gypsy moth (Lymantria dispar), a lepidopteran pest of forests. Laboratory studies
indicated that 35.6 % of the 78 lepidopteran species exposed to E. maimaiga were susceptible
(Hajek et al., 1995). However, in ® eld trials only two lepidopteran non-target individual s
were infected (Hajek et al., 1996). This highlight s the signi® cance of considering both
physiological and ecological susceptibility of non-target insects to pathogens.
Laborator y practices, such as repeated subculturing , long term storage and in vitro
culturing, can result in changes in virulence which would also aVect the proportion of
insects infected during bioassays (St. Leger et al., 1991; Hajek & Butler, 1999). Furthermore,
there are many potential diVerences between insect hosts in the laborator y and in the ® eld
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INTERACTIONS BETWEEN ENTOMOPATHOGENIC FUNGI AND OTHER NATURAL ENEMIES
743
(Hajek & Butler, 1999). Insects reared on arti® cial diet in the laborator y are more susceptible
to fungal pathogens than insects fed on natural diets (Hajek & Butler, 1999). Insects in the
® eld can exhibit behaviours which are not possible in the laborator y and which can aVect
the pathogen, for example, some insects actively manipulat e thermoregulatio n to impede
development of fungal infections (Watson et al., 1993; Inglis et al., 1996; Blanford et al.,
1998). The spatial and temporal separation of insects and fungi in the ® eld further
contributes to the discrepancy between infection rates observed in the laborator y compared
to those in the ® eld (Hajek & Butler, 1999).
Therefore, when considering the potential risk to insect natural enemies of releasing a
fungal pathogen, susceptibility assays should be carried out beginning with maximum
challenge laborator y studies to identify isolates that have no pathogenicit y to non-targets
even under optimal conditions for the fungus. Such isolates present minimal to no direct
risk. Isolates that are able to infect non-targets should then pass through semi-® eld and ® eld
studies under more realistic conditions to determine whether they are likely to represent an
ecological risk.
Interaction Between Predation and Fungal Infection
Intra-guild predation is a dramatic example of interference between natural enemies, which
could result in antagonism , and reduced mortality of the host. It occurs if competing
predators also engage in a trophic interaction (predation or parasitism) with one another
(Polis & Holt, 1992), and is prevalent within many communities of biologica l control agents
(Rosenheim et al., 1995). Many studies have illustrated the occurrence of asymmetric
(unidirectional ) and symmetric (bi-directional ) intra-guild predation between: (a) predators
and parasitoids (Wheeler, 1977; Colfer & Rosenheim, 1995; Evans & England, 1996); (b)
diVerent parasitoid species attacking the same arthropod pests (Briggs, 1993); (c) diVerent
predator species (Sengonca & Frings, 1985); and (d) entomopathogen s and arthropod
natural enemies (Flexner et al., 1986; Goettel et al., 1990). Studies on the interactions
between entomopathogen s and arthropod natural enemies have generally concentrated on
the pathogen as the `intra-guild predator’, i.e. directly able to infect insect natural enemies
in the guild (Flexner et al., 1986; Goettel et al., 1990). However, the pathoge n can also be
preyed upon. In non-choice laborator y experiments, adult C. septempunctata and the
carabid, Pterostichus madidus, have been shown to consume aphids at a late stage of
E. neoaphidis infection (Pell et al., 1997b; Roy et al., 1998) and can, therefore, be considered
as intra-guild predators of the pathogen. Fourth instar C. septempunctata larvae partially
consumed sporulatin g infected aphids. However, other common aphid predators (larval
stages of the syrphid, Episyrphus balteatus, and the chrysopid, C. carnea) never consumed
infected aphids. Therefore, it is unlikely that syrphid, chrysopid and early instar coccinellid
larvae will negatively aVect the biological control potential of E. neoaphidis.
Adult and fourth instar larvae of C. septempunctata and adults of P. madidus could be
considered as intra-guild predators of E. neoaphidis and have the potential to have a negative
impact on E. neoaphidis. However, the biology of these two predatory beetles suggest that
this interaction may not be important. First, in the absence of uninfected aphids, fourth
instar C. septempunctata larvae predated on aphids infected with E. neoaphidis, but often
only partially consumed the cadavers. Although coccinellid larvae have an increased
motivation to feed than adults (Ferran & Dixon, 1993), even fourth instar larvae starved for
24 h did not entirely consume sporulating E. neoaphidis infected A. pisum. By comparison,
uninfected A. pisum were readily consumed. Hence C. septempunctata has the potential to
reduce E. neoaphidis population density, but uninfected aphids are more likely to be
consumed than infected aphids. Indeed, from ® eld observations it was apparent that no
visibly-infecte d aphids were consumed by either adult or larval C. septempunctata (Roy,
1997). Partially-consume d cadavers produced signi® cantly fewer conidia but this did not
aVect transmission rates in laborator y experiments. The same proportion of aphids became
infected regardless of whether the source of inoculum was a damaged or an intact cadaver
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H. E. ROY & J. K. PELL
(Roy et al., 1998). Furthermore, the presence of a foraging predator greatly increased withinpopulatio n transmission, as already described, which would more than compensate for the
small reduction in inoculum caused by feeding damage.
Infected aphids were entirely consumed more quickly by carabids than uninfected aphids
and, therefore, more infected, than uninfected, aphids were consumed over the study period.
This generalist predator forages on the ground and consumes cadavers that become dislodged
from the plant. These cadavers are already lost from the arena of fungal transmission on
the plant and so may not contribute to the development of a local epizootic. Morgan (1994)
demonstrated that E. neoaphidis conidia could persist on soil where they may be important
in the survival of the fungus over short periods when conditions are unfavourable for
infection. Therefore, P. madidus may not have an eVect on immediate transmission of
E. neoaphidis but may have an eVect on its persistence in soil.
Living infected aphids are able to produce alarm pheromone but are less able to respond
to it (Roy et al., 1999), which may increase the probabilit y of them not surviving attack by
a predator and thus may result in a reduction in pathogen density. Predators feed less on
infected aphids and this, combined with their reduced response to alarm pheromone, may
result in a greater proportion of infected aphids remaining on the plant which would bene® t
local transmission of the pathogen. The reduced abilit y of late-stage infected aphids to recolonize a plant after dislodgement may increase their vulnerabilit y to ground predators,
such as the carabid, P. madidus. However, of the infected aphids that responded to alarm
pheromone, walking was a more common response than dislodging .
A limited number of other laborator y studies have examined the predation of insects
infected with fungal pathogens. Pell and Vandenberg (1998) demonstrated that the convergent
ladybird, H. convergens, avoided feeding on Russian wheat aphids, Diuraphis noxia, infected
with P. fumosoroseus. Sahelian grasshoppers (Acrotylus blondeli and Pyrgomorpha cognata)
infected with M. anisopliae were less likely to be predated on than uninfected individual s
(Arthurs, 1999). Therefore, cadavers of all these insects are likely to persist in the environment. This was in contrast to brown locusts, Locustana pardalina infected with M. anisopliae,
which are more susceptible to predation than uninfected individual s and, therefore, less
likely to contribute to secondary cycling (Arthurs, 1999).
Polis et al. (1989) concluded that intra-guild predation incorporates aspects of exploitation ,
apparent and classical competition: a tendency for exclusion (either because of direct
competition or because the intra-guild predator can be sustained by the intra-guild prey),
possibilitie s for co-existence (if the intra-guild prey species is superior to the intra-guild
predator at resource exploitation ) or an increase in the resource (as a consequence of
removal of predator species by intra-guild predators). Intra-guild predation is widespread
amongst communities of biological control agents and is an important consideration in the
use of multiple species for biologica l control. However, the signi® cance of intra-guild
predation varies in diVerent community contexts (Polis et al., 1989) and, consequently, its
impact on biologica l control programmes will be variable as indicated by the studies outlined
above.
Competition Between Entomopathogeni c Fungi and Other Natural Enemies
A pathoge n may interfere with the natural enemy complex indirectly by reducing the host
population s of predators and parasitoids or by rendering the host unsuitabl e for other
natural enemies (Rosenheim et al., 1995). Most interactions between parasitoids and
entomopathogeni c fungi are asymmetrical in favour of the pathogen (Hochberg & Lawton,
1990), however, the relative timing of parasitism and fungal infection is often crucial to the
® nal competitive outcome.
The interaction between the aphid parasitoid, A. nigripes, and the fungus, V. lecanii, is
dependent on the relative timing of parasitism/infection. Development of the aphid parasitoid, A. nigripes, is impeded by V. lecanii infection; however, a high proportion of parasitoids
developed successfully when aphids were exposed to V. lecanii 4 days after parasitizatio n
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INTERACTIONS BETWEEN ENTOMOPATHOGENIC FUNGI AND OTHER NATURAL ENEMIES
745
(Askary & Brodeur, 1999). Similarily the entomopathogeni c fungus, N. rileyi, inhibits
development of the braconid parasitoid, Microplitis croceipes, if larvae of the bollwor m host
(Heliothis zea) are infected one day after parasitizatio n (King & Bell, 1978). The successful
augmentation of these natural enemies may be impeded by this antagonism , however, careful
management ensuring temporal separation of the interacting natural enemies could result in
eVective biologica l control (King & Bell, 1978). The eVective introduction of antagonisticall y
interacting natural enemies has also been achieved in other systems with careful management.
Some parasitoids can discriminate between hosts infected with a fungal pathoge n and noninfected hosts (Brobyn et al., 1988; Fransen & van Lenteren, 1993). Greenhouse white¯ y,
Trialeurode s vaporariorum, infected with the entomopathogeni c fungus, Aschersonia
aleyrodis, are unsuitabl e hosts for the parasitoid, Encarsia formosa (Fransen & van Lenteren,
1993). However, the parasitoid can discriminate between infected and non-infected hosts
after seven days of fungal infection. Thus, the introduction of the fungus followed seven
days later by the parasitoid may result in eVective white¯ y control (Fransen & van Lenteren,
1993). Similarily the aphid parasitoid, A. rhopalosiphi, avoids ovipositin g in aphid hosts at
late stages of infection (Brobyn et al., 1988).
Increased mortality of pest species can result even when interference between pathogens
and parasitoids is evident. The fungal pathogen Hirsutella cryptosclerotiu m and the parasitoid Gyranussoidea tebygi are both natural enemies of the mealybug Rastrococcus invadens.
The pathogen reduced levels of parasitism by the parasitoid, but the overall mortality of the
mealybug was still greater when both natural enemies acted together (Akalach et al., 1992).
Similarly there were additive eVects with regard to aphid control, with no detrimental eVects
on the percentage parasitism nor parasitoid emergence when P. fumosoroseus and the
parasitoid Aphelinus asychis were used together for control of the Russian wheat aphid
D. noxia under ® eld conditions (Mesquita et al., 1997).
The observation of competitive interactions in the laborator y may not re¯ ect the ® eld
situation. Competition has been demonstrated between two cereal aphid natural enemies:
the entomopathogeni c fungus, E. neoaphidis, and the parasitoid, A. rhopalosiphi (Powell
et al., 1986). The development of the parasitoid was prevented when the aphids were infected
by the fungus less than four days after parasitation. Conversely, fungus development was
impeded when infection occurred more than four days after parasitization . However, in the
® eld, parasitoids are often more abundant early in the season when hyperparasitoid s are
scarce (Powell, 1982) and at this time fungal pathogens are usually at low levels. Thus,
interference between the parasitoid and fungus is likely to be minimal.
Antagonistic interactions between natural enemies may be reduced or prevented by such
temporal or spatial separation. Many of the studies demonstrating natural enemy interactions
are laboratory-base d with behavioural experiments being conducted in simple arenas, for
example, Petri dishes. Although such arenas provide environment s in which preliminary
observation s on invertebrate behaviour can be made, conclusions from such studies are
limited by the context in which they were collected. The interactions between natural
enemies are undoubtedly aVected by the complexitie s of the environment in which they
forage (Sengonca & Frings, 1985; Chang, 1996; Fuentes-Contreras et al., 1998). The
competitive interactions between A. rhopalosiphi and E. neoaphidis are aVected by host plant
resistance (Fuentes-Contreras et al., 1998). Host plants which are partially-resistan t to aphid
attack result in an increase in the developmental times of aphids and their parasitoids.
Consequently, this aVects the third trophic level but appears to be more detrimental to the
parasitoid than the fungus.
Situations where insects are susceptible to more than one pathoge n are very common
(Wilding, 1975; Wilding & Perry, 1980; Sivcev, 1992) and, therefore, there is also potential
for mixed infection and competition between pathogens. The fungal pathogens N. fresenii
and E. neoaphidis both commonly infect aphids. Dual infection of aphids by these two
pathogens has been observed during epizootics in the ® eld (Sivcev, 1992). In laborator y
studies, aphids infected simultaneously with both pathogen s died from N. fresenii at high
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746
H. E. ROY & J. K. PELL
temperatures (30ë C) and E. neoaphidis at low temperatures (10ë C) (Villacarlos, unpublishe d
data). Therefore, these two pathogens may be spatially and temporally isolated from one
another due to their diVerent temperature optima. A similar eVect was observed when
B. bassiana and M. Xavoviride co-infected the migratory grasshopper Melanoplu s sanguinipe s
under constant and oscillatin g temperatures. Proliferatio n of the fungi in the haemocoel was
measured in diVerent environment s with the same mean daily temperature, (25ë C), but
diVering in the degree to which they oscillated daily (constant 25ë C, 20± 30ë C, 15± 35ë C, or
10± 40ë C). More B. bassiana than M. anisopliae was recovered from coinfected nymphs at
constant 25ë C but as the amplitude of temperature increased, more M. anisopliae than
B. bassiana was recovered suggesting that temperature in¯ uenced their competitiveness
(Inglis et al., 1999).
SPATIAL AND TEMPORAL OCCURRENCE
The importance of predators, parasitoids and pathogens in the suppression of pest populations has been the motivation for many studies to quantify ® eld population s of natural
enemies. These studies have generally concentrated on either predators (Edwards et al., 1979;
Coombes & Sotherton, 1986; Booij & Noorlander, 1992; Ekbom, 1994), parasitoids (Powell,
1982; MuÈller et al., 1999) or pathogens (Wilding, 1975; Ekbom & Pickering, 1990) in
isolation . Assessments of the temporal and spatial occurrence of diVerent natural enemies
have largely been neglected. Chambers et al. (1986) monitored population s of predators,
parasitoids and pathogeni c fungi in winter wheat and concluded that the presence of multiple
natural enemies impeded development of the aphid population . However, the contribution
of the diVerent natural enemies varied from year to year. Aphid-speci® c predators were the
major factor limiting cereal aphid population s in the ® rst year studied but parasitoids and
pathogens also contributed to the decline of aphids in the following year. The importance
of natural enemies acting concurrently was implicated in this study.
In a recent study, Roy (1997) assessed the spatial and temporal occurrence of
E. neoaphidis and C. septempunctata in ® eld crops (spring wheat and spring bean) and
in a nettle patch. Monitoring of insect and fungus population s began at the beginning
of May 1995 and continue d until the crops were harvested (August). Although the ® eld
study represents observation s from only one year, C. septempunctata and E. neoaphidis
co-occurred both spatially and temporally in crops and in the weed patch. The ® rst observations of both C. septempunctata and E. neoaphidis were in the nettle patch which provided
an early source of aphids for both the pathogen and the predator. Nettle patches situated
adjacent to crop ® elds may act as reservoirs for parasitoids, predators and pathogens
(Perrin, 1975). However, the concept of using reservoirs (alternative hosts) to maintain
and increase natural enemy population s depends on the ability of the natural enemies to
transfer between diVerent host species. Some aphid parasitoids are capable of transferring
between certain hosts without any apparent loss of ® tness (Wratten & Powell, 1990), but
others are unable to transfer (Cameron et al., 1984). In addition, the virulence of isolates
of the same fungal pathoge n can vary depending on the host species or clone (Sitch &
Jackson, 1997); thus aphid species and clones are diVerentially susceptible to diVerent
isolates of E. neoaphidis (Milner, 1982; Milner, 1985; Pickering & Gutierrez, 1991). Therefore, even generalists may exist as discrete population s associated with particular hosts or
habitats. The potential of natural enemy reservoirs would be impeded by the evolution
of distinct host biotypes. Roy (1997) collected samples of infected nettle aphids and used
these to infect both A. pisum and Sitobion avenae in the laborator y, providin g evidence
that the isolate of E. neoaphidis that infected the nettle aphids was infective to crop aphid
species. The importance of nettles as a reservoir for both E. neoaphidis and C. septempunctata has been implicated and the movement of these natural enemies between noncrop and crop habitats is currently under investigation .
INTERACTIONS BETWEEN ENTOMOPATHOGENIC FUNGI AND OTHER NATURAL ENEMIES
747
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IMPLICATIONS FOR BIOLOGICAL CONTROL
Manipulativ e strategies
The use of entomopathogen s to control pest insects could be enhanced by manipulatin g
pest populations. The process of autodisseminatio n involve s the use of host insects to
introduce and disperse entomopathogen s (IgnoVo, 1978). A sex pheromone trap has been
developed for the autodisseminatio n of Z. radicans by the diamond back moth, P. xylostella
(Pell et al., 1993; Furlong et al., 1995). Synthetic sex pheromone is used to attract adult
male P. xylostella into traps positioned throughout a cabbage crop where they are inoculated
with Z. radicans conidia from a sporulatin g mycelial mat. After habituatio n to the pheromone, the moths leave the trap and disperse into the cabbage crop where they consequently
die of infection releasing infective conidia into the host populatio n on the crop. Attractant
traps have also been developed for the autodisseminatio n of other fungal and viral pathogens
to target pests (Klein & Lacey, 1999; Vega et al., 2000). Similar approaches could be used
for developin g traps for the transmission of pathogens by insect natural enemies.
Conservation Strategies
The potential of arthropod natural enemies to vector entomopathogen s to pest population s
could be encouraged within the agroecosystem. Reservoirs (distinct patches of pathogen
such as cadavers on trees or resting spores in the soil) are important in the population
dynamics of many entomopathogens. For example, the overwintering resting spores of
Entomophaga maimaiga have applied to form a reservoir of the pathoge n for the biological
control of gypsy moth, Lymantria dispar (Hajek & Roberts, 1991).
Erynia neoaphidis does not produce resting spores, but reservoirs of the pathogen could
be established in the form of conidia or cadavers. Nettle aphids are often an early source of
E. neoaphidis inoculum and may act as a pathogen reservoir. The movement of E. neoaphidis
from such a reservoir could be increased by C. septempunctata which disperse from woodland
habitats to nettle patches early in spring (Zhou & Carter, 1992; Zhou et al., 1994).
Coccinellids foraging in nettle patches may become contaminate d with E. neoaphidis conidia
which they may subsequently vector to crop aphids. Therefore, nettle patches within an
agroecosystem may conserve both E. neoaphidis and insect natural enemies and enhance
transmission to crop species. The provision of reservoirs which conserve complementary
insect and fungal natural enemies have potential in other pest/ crop systems.
CONCLUSIONS
The importance of assessing interactions within potential complexes of natural enemies
being considered for use in biologica l control is unquestionabl e (Ferguson & Stiling, 1996).
Intra-guild predation among biologica l control agents could reduce the mortality of the
target pest populatio n (Rosenheim et al., 1995) and it could be argued that intra-guild
predators should be excluded from multi-species assemblages used for the biologica l control
of pests (Polis & Holt, 1992). However, intra-guild predators are likely to be generalists
(Polis & Strong, 1996) and, so, in the presence of multiple prey species, the diets of intraguild predators may only partially overlap.
It is important to assess the interactions between biologica l control agents in a realistic
environment. The interactions between natural enemies are often studied in simpli® ed
laborator y arenas (Chang, 1996). Although such arenas indicate the potential for natural
enemies to interact, they do not re¯ ect the complexities of the multidimensiona l environment
of the ® eld situation. Furthermore, such studies are often limited to the examinatio n of
trophic interactions, ignoring other aspects of the relationships between species, such as
behaviour. From studies described in this paper, it is evident that there are many positive
interactions between natural enemies of pest insects and these interactions could be
manipulate d or encouraged within the agroecosytem .
748
H. E. ROY & J. K. PELL
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ACKNOWLEDGEMENTS
H.E.R. was supported by a Lawes Trust studentship (1994± 1997) and is currently supported
by Anglia Polytechni c University. J.K.P. is supported by the Ministry for Agriculture,
Fisheries and Food, UK. IACR receives grant-aided support from the Biotechnolog y and
Biological Sciences Research Council of the UK. This work was presented at the International Symposium `Biological Control Agents in Crop and Animal Protection’ , University
of Wales, Swansea, 24± 28 August 1999.
REFERENCES
Agrios, G.N. (1988) Plant Pathology. Academic Press, London.
Akalach, M., Fernandez-Garcia, E. & Moore, D. (1992) Interaction between Rastrococcus invadens
(Hom.: Pseudococcidae) and two natural enemies. Entomophaga 37, 99± 106.
Andreadis, T.G. (1987) Transmission, in Epizootiology of Insect Diseases (Fuxa, J.R. & Tanada, Y., Eds).
Wiley-Interscience, New York, pp. 159± 176.
Arthurs, S. (1999) Evaluating the impact of a mycoinsecticide for control of locusts and grasshoppers.
Antenna 23, 256± 258.
Askary, H. & Brodeur, J. (1999) Susceptibility of larval stages of the aphid parasitoid Aphidius nigripes to
the entomopathogenic fungus Verticillium lecanii. Journa l of Invertebrate Pathology 73, 129± 132.
Ball, B.V., Pye, B.J., Carreck, N.L., Moore, D. & Bateman, R.P. (1994) Laboratory testing of the
mycoinsecticide on non-target organisms: the eVects of an oil formulation of Metarhizium anisoplia e
applied to Apis mellifera. Biocontrol Science and Technology 4, 289± 296.
Blanford, S., Thomas, M.B. & Langewald, J. (1998) Behavioural fever in the Senegalese grasshopper,
Oedaleus senegalensis, and its implications for biological control using pathogens. Ecological Entomology
23, 9± 14.
Booij, C.J.H. & Noorlander, J. (1992) Farming systems and insect predators. Agriculture, Ecosystems and
Environment 40, 125± 135.
Briggs, C.J. (1993) Competition among parasitoid species on a stage-structured host and its eVect on host
suppression. American Naturalist 141, 372± 397.
Brobyn, P.J., Clark, S.J. & Wilding, N. (1988) The eVect of fungus infection of Metopolophiu m dirhodu m
(Hom.: Aphididae) on the oviposition behaviour of the aphid parasitoid Aphidius rhopalosiph i (Hym.:
Aphidiidae). Entomophaga 33, 333± 338.
Butt, T.M., Carreck, N.L., Ibrahim, L. & Williams, I.H. (1998) Honey-bee-mediated infection of pollen
beetles (Meligethes aeneus Fab.) by the insect-pathogenic fungus, Metarhizium anisopliae. Biocontrol
Science and Technology 8, 533± 538.
Cameron, P.J., Powell, W. & Loxdale, H.D. (1984) Reservoirs for Aphidius ervi Haliday (Hymenoptera,
Aphidiidae), a polyphagous parasitoid of cereal aphids (Hemiptera, Aphididae). Bulletin of Entomological
Research 74, 647± 656.
Capinera, J.L. & Barbosa, P. (1975) Transmission of nuclear-polyhedrosis virus to gypsy moth larvae by
Calosoma sycophant a. Annals of the Entomological Society of America 68, 593.
Carruthers, R.I., Sawyer, A.J. & Hural, K. (1991) Use of fungal pathogens for biological control of
insect pests, in Sustainabl e Agriculture Research and Education in the Field. National Academy Press,
Washington, pp. 336± 372.
Carruthers, R.L. & Onsager, J.A. (1993) Perspective on the use of exotic natural enemies for biological
control of pest grasshoppers. Environmental Entomology 22, 885± 903.
Carruthers, R.L., Ramos, M.E., Larkin, T.S., Hostetter, D.L. & Soper, R.S. (1997) The Entomphaga
grylli (Fresenius) Batko species complex: Its biology, ecology and use for biological control of pest
grasshoppers. Memoirs of the Entomological Society of Canada 171, 329± 353.
Chambers, R.J., Sunderland, K.D., Stacey, D.L. & Wyatt, I.J. (1986) Control of cereal aphids in winter
wheat by natural enemies: aphid-speci® c predators, parasitoids and pathogenic fungi. Annals of Applied
Biology 108, 219± 231.
Chang, G.C. (1996) Comparison of single versus multiple species of generalist predators for biological
control. Environmental Entomology 25, 207± 212.
Clegg, J.M. & Barlow, C.A. (1982) Escape behaviour of the pea aphid Acyrthosiphon pisum (Harris) in
response to alarm pheromone and vibration. Canadia n Journal of Zoology 60, 2245± 2252.
Colfer, R.G. & Rosenheim, J.A. (1995) Intra-guild predation by coccinellid beetles on an aphid parasitoid,
Lysiphlebus testaceipes. Proceedings of the Beltwide Cotton Conference, pp. 1033± 1036.
Coombes, D.S. & Sotherton, N.W. (1986) The dispersal and distribution of polyphagous predatory
Coleoptera in cereals. Annals of Applied Biology 108, 461± 474.
Danfa, A. & Van der Valk, H.C.H.G. (1999) Laboratory testing of Metarhizium spp. and Beauveria
bassiana on Sahelian non-target arthropods. Biocontrol Science and Technology 9, 187± 198.
Downloaded by [CIMMYT -International Maize and Wheat Improvement Center ] at 07:45 05 September 2012
INTERACTIONS BETWEEN ENTOMOPATHOGENIC FUNGI AND OTHER NATURAL ENEMIES
749
Donegan, K. & Lighthart, B. (1989) EVect of several stress factors on the susceptibility of the predatory
insect, Chrysoperla carnea (Neuroptera: Chrysopidae), to the fungal pathogen Beauveria bassiana. Journal
of Invertebrate Pathology 54, 79± 84.
Edwards, C.A., Sunderland, K.D. & George, K.S. (1979) Studies on polyphagous predators of cereal
aphids. Journa l of Applied Ecology 16, 811± 823.
Ekbom, B. & Pickering, J. (1990) Pathogenic fungal dynamics in a fall population of the blackmargined
aphid (Monellia caryella). Entomologia Experimentalis et Applicata 57, 29± 37.
Ekbom, B. (1994) Arthropod predators of the pea aphid, Acyrthosiphon pisum Harr. in peas, clover and
alfalfa. Journal of Applied Ecology 117, 469± 476.
Evans, E.W. & England, S. (1996) Indirect interactions in biological control of insects: pests and natural
enemies in alfalfa. Ecological Applications 6, 920± 930.
Feng, M.G., Poprawski, T.J. & Khachatourians, G.G. (1994) Production, formulation and application of
the entomopathogenic fungus Beauveria bassiana for insect control: current status. Biocontrol Science
and Technology 4, 3± 34.
Ferguson, K.I & Stiling, P. (1996) Non-additive eVects of multiple natural enemies on aphid populations.
Oecologia 108, 375± 379.
Ferran, A. & Dixon, A.F.G. (1993) Foraging behaviour of ladybird larvae. European Journa l of Entomology
90, 383± 402.
Fitt, B.D.L., McCartney, H.A. & Walklate, P.J. (1989) Role of rain in the dispersal of pathogen
inoculum. Annual Review of Phytopatholog y 27, 241± 270.
Flexner, J.L., Lighthart, B. & Croft, B.A. (1986) The eVects of microbial pesticides on non-target,
bene® cial arthropods. Agricultural Ecosystems and Environment 16, 203± 254.
Fransen, J.J. & Van Lenteren, J.C. (1993) Host selection and survival of the parasitoid Encarsia formosa
on greenhouse white¯ y, Trialeurodes vaporariorium, in the presence of hosts infected with the fungus
Aschersonia aleyrodis. Entomologia Experimentalis et Applicata 69, 239± 249.
Fuentes-Contreras, E., Pell, J.K. & Niemeyer, H.M. (1998) In¯ uence of host plant resistance at the third
trophic level: interactions between parasitoids and entomopathogenic fungi of cereal aphids. Oecologia
117, 426± 432.
Furlong, M.J., Pell, J.K., Choo, O.P. & Rahman, S.A. (1995) Field and laboratory evaluation of a
sex pheromone trap for the autodissemination of the fungal entomopathogen Zoophthor a radicans
(Entomophthorales) by the diamond-back moth, Plutella xylostella (Lepidoptera: Yponomeutidae).
Bulletin of Entomological Research 85, 331± 337.
Furlong, M.J. & Pell, J.K. (1996) Interactions between the fungal entomopathogen Zoophthor a radicans
Brefeld (Entomophthorales) and two hymenopteran parasitoids attacking the diamondback moth,
Plutella xylostella L. Journal of Invertebrate Pathology 68, 15± 21.
Fuxa, J.R. & Tanada, Y. (1987) Epizootiology of Insect Diseases. Wiley-Interscience, New York.
Gillespie, D.R. & Menzies, J.G. (1993) Fungus gnats vector Fusarium oxysporu m f.sp. radicis-lycopersica.
Annals of Applied Biology 123, 539± 544.
Glare, T.R. & Milner, R.J. (1989) Ecology of entomopathogenic fungi, in Handbook of Applied Mycology,
Humans, Animals and Insects, Vol. 2 (Arora, D.K., Ajello, L. & Mukerji, K.G., Eds). Marcel Dekker,
New York.
Goettel, M.S., Poprawski, T.J., Vandenberg, J.D., Li, Z. & Roberts, D.W. (1990) Safety to nontarget
invertebrates of fungal biocontrol agents, in Safety of Microbial Insecticides (Lard, M., Lacey, L.A. &
Davidson, E.W. Eds). CRC Press, Boca Raton, FL, USA, pp. 209± 231.
Goettel, M.S. & Inglis, G.D. (1997) Fungi: Hyphomycetes, in Manual of Techniques in Insect Pathology
(Lacey, L., Ed.). Academic Press, San Diego, pp. 213± 247.
Hajek, A.E. & Dahlsten, D.L. (1987) Behavioural interactions between three birch aphid species and Adalia
bipunctata larvae. Entomologia Experimentalis et Applicata 45, 81± 87.
Hajek, A.E. & Roberts, D.W. (1991) Pathogen reservoirs as a biological control resource: introduction of
Entomophag a maimaiga to North American gypsy moth, Lymantria dispar, populations. Biological
Control 1, 29± 34.
Hajek, A.E. & St. Leger, R.J. (1994) Interactions between fungal pathogens and insect hosts. Annual Review
of Entomology 39, 293± 322.
Hajek, A.E., Butler, L. & Wheeler, M.W. (1995) Laboratory bioassays testing the host range of the gypsy
moth fungal pathogen Entomophag a maimaiga. Biological Control 5, 530± 544.
Hajek, A.E., Butler, L., Walsh, S.R.A., Silver, J.C., Hain, F.P., Hastings, F.L., Odell, T.M. & Smitley,
D.R. (1996) Host range of the gypsy moth (Lepidoptera: Lymantriidae) pathogen Entomophag a maimaiga
(Zygomycetes: Entomophthorales) in the ® eld versus laboratory. Environmental Entomology 25, 709± 721.
Hajek, A.E. & Butler, L. (1999) Predicting the host range of entomopathogenic fungi, in Nontarget EVects
of Biological Control (Follett, P.A. & Duan, J.J., Eds). Kluwer Academic, Netherlands.
Hall, R.A. (1981) The fungus Verticillium lecanii as a microbial insecticide against aphids and scales, in
Microbial Control of Pests and Plant Diseases 1970± 1980 (Burges, H.D., Ed.). Academic Press,
San Diego.
Hemmati, F. (1999) Aerial dispersal of the entomopathogenic fungus Erynia neoaphidis. PhD Thesis,
University of Reading, UK.
Downloaded by [CIMMYT -International Maize and Wheat Improvement Center ] at 07:45 05 September 2012
750
H. E. ROY & J. K. PELL
Hochberg, M.E. & Lawton, J.H. (1990) Competition between kingdoms. Trends in Evolution and Ecology
5, 367± 371.
Ignoffo, C.M. (1978) Strategies to increase the use of entomopathogens. Journa l of Invertebrate Pathology
31, 1± 3.
Ignoffo, C.M. (1981) The fungus Nomuraea rileyi as a microbial insecticide, in Microbial Control of Pests
and Plant Diseases 1970± 1980 (Burges, H.D., Ed.). Academic Press, San Diego.
Inglis, G.D., Johnson, D.L. & Goettel, M.S. (1996) EVects of temperature and thermoregulation on
mycosis by Beauveria bassiana in grasshoppers. Biological Control 7, 131± 139.
Inglis, G.D., Duke, G.M., Kawchuk, L.M. & Goettel, M.S. (1999) In¯ uence of oscillating temperature
on the competitive infection and colonisation of the migratory grasshopper by Beauveria bassiana and
Metarhizium Xavoviride. Biological Control 14, 111± 120.
Ingold, C.T. (1971) Fungal Spores: Their Liberation and Dispersal. Clarendon, Oxford.
James, R.R. & Lighthart, B. (1994) Susceptibility of the convergent lady beetle (Coleoptera: Coccinellidae)
to four entomogenous fungi. Environmental Entomology 23, 190± 192
James, R.R., Shaffer, B.T., Croft, B. & Lighthart, B. (1995) Field evaluation of Beauveria bassiana: its
persistence and eVects on the pea aphid and a non-target coccinellid in alfalfa. Biocontrol Science and
Technology 5, 425± 437.
James, R.R., Croft, B.A., Shaffer, B.T. & Lighthart, B. (1998) Impact of temperature and humidity on
host-pathogen interactions between Beauveria bassiana and a coccinellid. Environmental Entomology 27,
1506± 1513.
Jaronski, S.T., Lord, J., Rosinska, J., Bradley, C., Hoelmer, K., Simmons, G., Osterlind, R., Brown,
C., Staten, R. & Antilla, L. (1998) EVect of Beauveria bassiana-based mycoinsecticide on bene® cial
insects under ® eld conditions. The 1998 Brighton ConferenceÐ pests and diseases, 651± 656.
Kareiva, P. & Odell, G. (1987) Swarms of predators exhibit `preytaxis’ if individual predators use arearestricted search. American Naturalist 130, 233± 270.
Keller, S. (1986) Quantitative ecological evaluation of the May beetle pathogen, Beauveria brongniarti i, and
its practical application, in Fundamental and Applied Aspects of Invertebrate Pathology (Samson, R.A.,
Vlak, J.M. & Peters, D., Eds). Foundation of the Fourth International Colloquium of Invertebrate
Pathology, Wageningen, pp. 178± 181.
King, E.G. & Bell, J.V. (1978) Interactions between a Braconid, Microplitis croceipes, and a fungus,
Nomuraea rileyi, in laboratory-reared bollworm larvae. Journal of Invertebrate Pathology 31, 337± 340.
Klein, M.G. & Lacey, L.A. (1999) An attractant trap for autodissemination of entomopathogenic fungi
into populations of the Japanese beetle Popillia japonica (Coleoptera: Scarabaeidae). Biocontrol Science
and Technology 9, 151± 158.
Lacey, L.A., Mesquita, L.M., Mercadier, G., Debire, R., Kazmer, D.J. & Leclant, F. (1997) Acute
and sublethal activity of the entomopathogenic fungus Paecilomyces fumosoroseus (Deuteromycotina:
Hyphomycetes) on adult Aphelinus asychis (Hymenoptera: Aphelinidae). Environmental Entomology 26,
1452± 1460.
Levin, D.B., Lang, J.E., Jaques, R.P. & Corigan, J.E. (1983) Transmission of the granulosis virus of Pieris
rapae (Lepidopteran: Pieridae) by the parasitoid Apanteles glomeratus (Hymenopteran: Braconidae).
Environmental Entomology 12, 166.
Li, Z.Z. (1988) A list of insect hosts of Beauveria bassiana, in Study and Application of Entomogenous Fungi
in China Vol. 1 (Li, Y.W., Li, Z.Z., Liang, Z.Q., Wu, J.W., Wu, Z.K. & Xu, Q.F., Eds). Academic
Periodical Press, Beijing, pp. 241± 255.
Lockwood, J.A. (1993) Environmental issues involved in biological control of rangeland grasshoppers with
exotic agents. Environmental Entomology 22, 503± 518.
Magalhaes, B.P., Lord, J.C., Wraight, S.P., Daoust, R.A. & Roberts, D.W. (1988) Pathogenicity of
Beauveria bassiana and Zoophthor a radicans to the coccinellid predators Coleomegilla maculata and
Eriopsis connexa. Journa l of Invertebrate Pathology 52, 471± 473.
McCartney, H.A. (1990) The dispersal of plant pathogen spores and pollen from oilseed rape crops.
Aeriobiology 6, 147± 151.
McCartney, H.A. (1994) Dispersal of spores and pollen from crops. Grana 33, 76± 80.
McGuire, M.R., Maddox, J.V. & Armbrust, E.J. (1987) Host range studies of an Erynia radicans strain
(Zygomycetes: Entomophthorales) isolated from Empoasca fabae (Homoptera: Cicadellidae). Journal of
Invertebrate Pathology 50, 75± 77.
Mesquita, A.L.M., Lacey, L.A. & Leclant, F. (1997) Individual and combined eVects of the fungus
Paecilomyces fumosoroseus and parasitoid, Aphelinus asychis Walker (Hym., Aphelinidae) on con® ned
populations of Russian wheat aphid, Diuraphis noxia (Mordvilko) (Hom., Aphididae) under ® eld
conditions. Journal of Applied Entomology 121, 155± 163.
Mietkiewski, R., Van der Geest, L.P.S. & Balazy, S. (1986) Preliminary notes on the pathogenicity of
some Erynia strains (Mycophyta: Entomophthoraceae) towards larvae of Pieris brassicae. Journal of
Applied Entomology 102, 499± 504.
Milner, R.J. (1982) On the occurrence of pea aphids, Acyrthosipho n pisum, resistant to isolates of the fungal
pathogen, Erynia neoaphidis. Entomologia Experimentalis and Applicata 32, 23± 27.
Downloaded by [CIMMYT -International Maize and Wheat Improvement Center ] at 07:45 05 September 2012
INTERACTIONS BETWEEN ENTOMOPATHOGENIC FUNGI AND OTHER NATURAL ENEMIES
751
Milner, R.J. (1985) Distribution in time and space of resistance to the pathogenic fungus Erynia neoaphidis
in the pea aphid Acyrthosiphon pisum. Entomologia Experimentalis and Applicata 37, 235± 240.
Morgan, L.W. (1994) Survival, germination responses and infectivity of conidia of Erynia neoaphidis. PhD
Thesis, University of CardiV, UK.
MuÈ ller, F.P. (1983) DiVerential alarm pheromone responses between strains of the aphid Acyrthosiphon
pisum. Entomologia Experimentalis et Applicata 34, 347± 348.
MuÈ ller, C.B., Adriaanse, I.C.T., Belshaw, R. & Godfray, H.C.J. (1999) The structure of an aphidparasitoid community. Journa l of Animal Ecology 68, 346± 370.
Nemeye, P.S., Moore, D. & Prior, C. (1990) Potential of the parasitoid Heterospilus prosophidi s (Hymenoptera: Braconidae) as a vector of plant pathogenic Colletotrichum spp. Annals of Applied Biology 116,
11± 19.
Papierok, B., Valada o, B., Torres, L. & Arnault, M. (1984). Contribution to the study of the speci® city
of the entomopathogenic fungus Zoophthor a radicans (Zygomycetes: Entomophthorales) (in French).
Entomophaga 29, 109± 119.
Pedersen, E.A., Morrall, R.A.A., McCartney, H.A. & Fitt, B.D.L. (1994) Dispersal of conidia of
Ascochyta fabae f. sp. lentis from infected lentil plants by simulated wind and rain. Plant Pathology 43,
50± 55.
Pell, J.K., Macaulay, E.D.M. & Wilding, N. (1993a) A pheromone trap for the dispersal of the
pathogen Zoophthor a radicans Brefeld. (Zygomycetes: Entomophthorales) amongst populations of
the diamondback moth, Plutella xylostella L. (Lepidoptera: Yponomeutidae). Biocontrol Science and
Technology 3, 315± 320.
Pell, J.K., Wilding, N., Player, A.L. & Clark, S.J. (1993b) Selection of an isolate of Zoophthora
radicans (Zygomycetes: Entomophthorales) for biocontrol of the diamondback moth Plutella xylostella
(Lepidoptera: Yponomeutidae). Journa l of Invertebrate Pathology 61, 75± 80.
Pell, J.K., Tydeman, C. & McCartney, H.A. (1997a) Impact of rainfall on the persistence and transmission
of Erynia neoaphidis. Bulletin of the IOBC Insect Pathogens and Insect Parasitic Nematodes Special
Interest Group Meeting 21, 49.
Pell, J.K., Pluke, R., Clark, S.J., Kenward, M.G. & Alderson, P.G. (1997b ) Interactions between two
aphid natural enemies, the entomopathogenic fungus Erynia neoaphidis RemaudieÁre & Hennebert
(Zygomycetes: Entomophthorales) and the predatory beetle Coccinella septempunctata L. (Coleoptera:
Coccinellidae). Journa l of Invertebrate Pathology 69, 261± 268.
Pell, J.K. & Vandenberg, J.D. (1998) Paecilomyces fumosoroseus, convergent ladybirds and the Russian
wheat aphid: potential interactions. Insect Pathogens and Insect Parasitic Nematodes IOBC Bulletin
21, 133.
Peng, G., Sutton, J.C. & Kevan, P.G. (1992) EVectiveness of honey bees for applying the biocontrol agent
Gliocladium roseum to strawberry ¯ owers to suppress Botrytis cinerea. Canadia n Journa l of Plant
Pathology 14, 117± 129.
Perrin, R.M. (1975) The role of the perennial stinging nettle, Urtica dioica, as a reservoir of bene® cial
natural enemies. Annals of Applied Biology 81, 289± 297.
Pickering, J. & Gutierrez, A.P. (1991) DiVerential impact of the pathogen Pandora neoaphidis (R. & H.)
Humber (Zygomycetes: Entomophthorales) on the species composition of Acyrthosipho n pisum aphids
in alfalfa. Canadia n Entomologist 123, 315± 320.
Polis, G.A., Myers, C.A. & Holt, R.D. (1989) The ecology and evolution of intra-guild predation: potential
competitors that eat each other. Annual Review of Ecological Systematics 20, 297± 330.
Polis, G.A. & Holt, R.D. (1992) Intra-guild predation: the dynamics of complex trophic interactions.
Trends in Ecology and Evolution 7, 151± 154.
Polis, G.A. & Strong, D.R. (1996) Food web complexity and community dynamics. American Naturalist
147, 813± 846.
Poppy, G.M. (1997) Tritrophic interactions: improving ecological understanding and biological control?
Endeavour 21, 61± 64.
Poprawski, T.J., Mercadier, G. & Wraight, S.P. (1992) Interactions between Diuraphis noxia, Zoophthora
radicans and Aphelinus asychis: Preliminary results of laboratory studies. Proceedings of the 5th Annual
Russian Wheat Aphid Conference, Texas.
Poprawski, T.J., Crisostomo Legaspi, J. & Parker, P.E. (1998) In¯ uence of entomopathogenic fungi on
Serangium parcesetosum (Coleoptera: occinellidae), an important predator of white¯ ies (Homoptera:
Aleyrodidae). Environmental Entomology 27, 785± 795.
Powell, W. (1982) The identi® cation of hymenopterous parasitoids attacking cereal aphids in Britain.
Systematic Entomology 7, 465± 473.
Powell, W., Wilding, N., Brobyn, P.J. & Clark, S.J. (1986) Interference between parasitoids (Hym.:
Aphididae) and fungi (Entomophthorales) attacking cereal aphids. Entomophaga 31, 293± 302.
Reardon, R.C. & Podgwaite, J.D. (1976) Disease-parasitoid relationships in natural populations of
Lymantria dispar (Lepidopteran: Lymantriidae) in the Northeastern United States. Entomophaga 21, 333.
Richards, A.R., Speight, M.R. & Cory, J.S. (1994) The interaction of host movement and baculovirus
reservoirs. Proceedings of the 27th Annual Meeting of the Society for Invertebrate Pathology , Montpellier.
Downloaded by [CIMMYT -International Maize and Wheat Improvement Center ] at 07:45 05 September 2012
752
H. E. ROY & J. K. PELL
Rosenheim, J.A., Kaya, H.K., Ehler, L.E., Marois, J.J. & Jaffee, B.A. (1995) Intra-guild predation among
biological control agents: theory and evidence. Biological Control 5, 303± 335.
Roy, H.E. (1997) Interactions between aphid predators and the entomopathogenic fungus Erynia neoaphidis.
PhD Thesis, Nottingham University, UK.
Roy, H.E., Pell, J.K., Clark, S.J. & Alderson, P.G. (1998) Implications of predator foraging on aphid
pathogen dynamics. Journa l of Invertebrate Pathology 71, 236± 247.
Roy, H.E., Pell, J.K. & Alderson, P.G. (1999) EVects of fungal infection on the alarm response of pea
aphids. Journa l of Invertebrate Pathology 74, 69± 75.
Schabel, H.G. (1982) Phoretic mites as carriers of entomopathogenic fungi. Journa l of Invertebrate Pathology
39, 410± 412.
Sengonca, C. & Frings, B. (1985) Interference and competitive behaviour of the aphid predators, Chrysoperla
carnea and Coccinella septempunctata in the laboratory. Entomophaga 30, 245± 251.
Shimazu, M.S. & Soper, R.S. (1986) Pathogenicity and sporulation of Entomophthor a maimaiga Humber,
Shimazu, Soper and Hajek (Entomophthorales: Entomophthoraceae) on larvae of the gypsy moth,
Lymantria dispar L. (Lepidoptera: Lymantriidae). Applied Entomology and Zoology 21, 589± 596.
Sitch, J.C. & Jackson, C.W. (1997) Pre-penetration events aVecting host speci® city of Verticillium lecanii.
Mycological Research 101, 535± 541.
Sivcev, I. (1992) Seasonal dynamics and density of cabbage aphid’s (Brevicoryne brassicae L.) entomopathogenic fungi. Zastita bilja 43, 181± 195.
Smith, O.J., Hughes, K.M., Dunn, P.H. & Hall, I.M. (1956) A granulosis virus disease of the western
grape leaf skeletonizer and its transmission. Canadian Entomologist 88, 507.
Stairs, G.R. (1965) Arti® cial initiation of virus epizootics in forest tent caterpillar populations. Canadian
Entomologist 97, 1059.
Steinkraus, D.C., Hollingsworth, R.G. & Boys, G.O. (1996) Aerial spores of Neozygites fresenii
(Entomophthorales: Neozygitaceae): density, periodicity and potential role in cotton aphid (Homoptera:
Aphididae) epizootics. Environmental Entomology 25, 48± 57.
St. Leger, R.J. (1991) Integument as a barrier to microbial infections, in Physiolog y of the Insect Epidermis
(Binnington, K. & Retnakaran, A., Eds). CSIRO, Australia, pp. 184± 306.
Vega, F.E., Dowd, P.F., Lacey, L.A., Pell, J.K., Jackson, D.M. & Klein, M.G. (2000) Dissemination of
bene® cial microbial agents by insects, in Field Manual Techniques in Invertebrate Pathology: application
and evaluation of pathogens for control of insects and other invertebrate pests (Lacey, L.A. & Kaya,
H.K., Eds). Kluwer, Netherlands.
Vet, L.E.M. & Dicke, M. (1992) Ecology of infochemical use by natural enemies in a tritrophic context.
Annual Review of Entomology 37, 141± 172.
Vinson, S.B. (1990) Potential impact of microbial insecticides on bene® cial arthropods in the terrestrial
environment, in: Safety of Microbial Insecticides (Laird, M., Lacey, L.A. & Davidson, E.W., Eds).
CRC Press, Boca Raton, FL, USA, pp. 43± 64.
Watson, D.W., Mullens, B.A. & Petersen, J.J. (1993) Behavioural fever response of Musca domestica
(Diptera: Muscidae) to infection by Entomophthor a muscae (Zygomycetes: Entomophthorales). Journal
of Invertebrate Pathology 61, 10± 16.
Wheeler, A.G. (1977) Studies on the arthropod fauna of alfalfa. VII. Predaceous insects. Canadian
Entomologist 109, 423± 427.
Wilding, N. (1970) Entomophthora conidia in the air-spora. Journal of General Microbiolog y 62, 149± 157.
Wilding, N. (1975) Entomophthora species infecting pea aphid. Transactions of the Royal Entomological
Society 127, 171± 183.
Wilding, N. & Perry, J.N. (1980) Studies on Entomophthora in populations of Aphis fabae on ® eld beans.
Annals of Applied Biology 94, 367± 378.
Wilding, N. & Brady, B.L. (1984) CMI description of Erynia neoaphidis no. 815, in Commonwealth
Mycological Institute Descriptions of Pathogenic Fungi and Bacteria.
Wratten, S.D. & Powell, W. (1990) Cereal aphids and their natural enemies, in The Ecology of Temperate
Cereal Fields (Firbank L.G., Carter, N., Darbyshire, J.F. & Potts, G.R., Eds). Blackwell Science,
Oxford, pp. 233± 257.
Wright, J.E. & Kennedy, F.G. (1996) A new biological product for control of major greenhouse pests. The
1996 Brighton ConferenceÐ pests and diseases, 885± 892.
Xu, Q.F. (1988) Some problems about study and application of Beauveria bassiana against agricultural and
forest pests in China, in Study and Application of Entomogenous Fungi in China Vol. 1 (Li, Y.W., Li,
Z.Z., Liang, Z.Q., Wu, J.W., Wu, Z.K. & Xu, Q.F., Eds). Academic Periodical Press, Beijing,
pp. 241± 255.
Yeo, H., Pell, J.K. & Pye, B.J. (1998) A biorational approach to selecting mycoinsecticides for aphid
management. The 1998 Brighton ConferenceÐ pests and diseases, 307± 308.
Zhou, X. & Carter, N. (1992) The ecology of coccinellids on farmland. Aspects of Applied Biology 31,
133± 138.
Zhou, X., Carter, N. & Powell, W. (1994) Seasonal distribution and aerial movement of adult coccinellids
on farmland. Biocontrol Science and Technology 4, 167± 175.