Paper 137 Disc

Ecology Letters, (2000) 3 : 228±235

REVIEW
Can plants use entomopathogens as bodyguards?

1
Sam L. Elliot, Maurice W.
Sabelis,1 Arne Janssen,1 Leo P. S.
van der Geest,1 Ellen A. M.
Beerling1,2 and Joanne Fransen2
1
Section Population Biology,
University of Amsterdam,
Postbus 94084, 1090 GB
Amsterdam, The Netherlands.
E-mail: elliot@bio.uva.nl
2
Research Station for
Floriculture and Glasshouse
Vegetables, Linnaeuslaan 2a,
1431 JV Aalsmeer, The
Netherlands.
Abstract
For 20 years, ecologists have been gathering evidence in support of the hypothesis that
plants can use insect natural enemies such as predators and parasitoids as bodyguards to
protect themselves from herbivory, but entomopathogens have escaped this
consideration. We extend the bodyguard hypothesis to ask whether plants can use
entomopathogens as bodyguards. We first discuss the evolutionary context of such
tritrophic interactions and then categorize possible mechanisms as: (1) maintaining a
population of bodyguards on the plant surface, (2) increasing contact rates between
insect host and pathogen and (3) increasing the susceptibility of the host. We explore
these mechanisms further, examining published studies for evidence for the hypothesis.
We then discuss potential costs to the plant of promoting pathogens as bodyguards
which may include a reduction in the efficiency of other ``bodyguard'' species, the
incidental promotion of plant pathogens and the risk of entomopathogens developing
phytopathogenicity. Aside from our intention to stimulate the testing of the bodyguard
hypothesis with entompathogens and to provide a conceptual framework for this, we
hope to bring evolutionary ecology and insect pathology closer together.

Keywords
Biological control, bodyguards, epizootiology, insect pathology, mutualisms, plant
defence, tri±trophic interactions.
Ecology Letters (2000) 3 : 228±235
INTRODUCTION
There is something of a gulf between insect pathology and
evolutionary ecology. Insect pathologists have historically
been concerned with description of pathogens and their
application to the resolution of pest problems. Reviews of
the field have mainly been mechanistic syntheses. Mean-
while, many evolutionary ecologists developing theory
have tended to skirt around insect pathogens.
In the area of tri-trophic interactions between plant,
insect herbivore and pathogen of the herbivore, there
have been many experimental studies of an applied bent,
and one review (Duffey et al. 1995), the subject also
receiving brief treatments in other reviews (e.g. Cory et al.
1997; Hajek 1997). Throughout this literature, there is a
modest assumption that observed effects of the plant on
the pathogen are the result of evolved defences to
herbivores or phytopathogens. In the meantime, ento-
mologists working on predators and parasitoids have
spent nearly 20 years following up a suggestion by Price et
al (1980) that natural enemies of herbivores could be
considered part of the battery of defences available to a
plant. This is increasingly yielding evidence that plants
may use natural enemies as bodyguards (a term ascribed to
Ahed
Bhed
Ched
Dhed
Ref marker
Fig marker
the interaction more than a century ago; see Bentley 1977), Table mar-
by providing food or shelter for the enemies (e.g. Jolivet ker
1996; Walter 1996) or by producing herbivore-induced Ref end
volatiles to betray the presence of herbivores (see Sabelis Ref start
et al. 1999a, b). Curiously, the possibility that pathogens
may be involved in similar mutualistic interactions with
plants, whilst implicit throughout the literature, has
largely been overlooked by both sets of scientists.
In this review, we ask whether plants can use entomo-
pathogens as bodyguards. We argue that to understand the
evolution of bodyguard interactions requires a connection to
be made from the plant trait which affects the pathogen,
through direct and indirect effects on the dynamics of the
herbivore on the plant, to fitness consequences for the plant.
We use this approach to recast some empirical studies in the
light of the bodyguard hypothesis. In this, our aim is not to
convince the reader that our explanation is universally
applicable. It is rather to provide an alternative hypothesis,
which at times is inevitably speculative in nature, to those
normally explored. We have avoided a taxonomic treatment
of the pathogens, or any related predictions according to life
history, as the absence of literature specifically testing this
hypothesis would render any such generalities at best
premature and at worst limiting.

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The flip-side of bodyguard interactions is then examined:
costs for the plant to promote the pathogens such as
potentially diminished efficiency of other ``bodyguard''
species, the incidental promotion of plant pathogens and
the risk of entomopathogens developing phytopathogenicity.
It is intended that our arguments will at once stimulate
the critical testing of the bodyguard hypothesis with
pathogens whilst serving to bring food web ecology and
evolutionary theory closer together with insect pathology.
WHAT IS THE BASIS FOR THE EVOLUTION OF
PLANT-ENTOMOPATHOGEN MUTUALISMS?
For mutualisms to have evolved between a plant and
pathogen of its insect herbivores requires that the plant be
able to affect the pathogen so as to counter the loss of plant
fitness arising from herbivory. If there is genetic variation
in plant traits that can effect the herbivore±entomopatho-
gen interaction and there are resulting fitness consequences
to the plant, then there is a basis for natural selection to act,
i.e. plants may evolve to use entomopathogens as body-
guards. Twin assumptions arising from this are that
herbivory in the absence of natural enemies reduces plant
fitness and that pathogens are capable of limiting this loss
of fitness. That the former is commonly (although by no
means universally) the case is clear from the existence of
evolved plant defences to herbivory. The latter is perhaps
less clear so we shall now briefly address this.
An explanation for the anomaly that the world is green
when there are so many extant herbivores has been found in
the control of these herbivores by natural enemies on the
third trophic level (Hairston et al. 1960). This is commonly
taken to mean predators and parasitoids, but of course there
is no reason to exclude pathogens from this explanation.
There is an abundance of evidence that natural epizootics of
pathogenic diseases can cause very high mortalities in
populations of herbivorous insects (see Fuxa & Tanada
1987). This has led to a body of work attributing population
cycles of forest Lepidoptera to baculoviruses (see Anderson
& May 1980) but this view has been challenged (Berryman
1996). A review of life table data from 78 insect herbivore
species from a range of habitats concluded that pathogens do
not on average represent a potent mortality source, but there
remain instances where they do and their impact may often
be underestimated (Hawkins et al. 1997). The impact of this
source of herbivore mortality on plant fitness has not
specifically been assessed and in fact any negative effects on
herbivore population dynamics (through reduced feeding,
birth rates, etc.) should benefit the plant. Successful use of
microbial control in agricultural crops (see Lacey & Goettel
1995) suggests that there may be (or have been in a plant's
evolutionary history) beneficial fitness effects of naturally
occurring insect diseases to the plant.
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Entomopathogens as plant bodyguards 229
As regards the pathogen's fitness, it is worth clarifying
that a bodyguard interaction, in the strictest sense, need
not be mutualistic ± the effect on the pathogen could be
neutral or even detrimental so long as there is a positive
effect on the plant. A conflict of interests may arise when
the optimal strategy for an entomopathogen is slowly to
exploit a patch of hosts, or to allow its hosts to continue
to feed, while the optimal strategy for the plant is to
promote the pathogen's virulence and quickly be free of
herbivory. In this case, a bodyguard trait on the part of
the plant may not be beneficial to the pathogen and one
might expect to see some coevolutionary interplay
between plant and entomopathogen.
HOW MIGHT PLANTS MANIPULATE
ENTOMOPATHOGENS?
Most work on the ecology of entomopathogens has
focused on the direct effects of pathogens on herbivore
numbers. A bodyguard interaction is, by definition, an
indirect one, i.e. between the plant and the herbivore via
the pathogen. A plant may have an indirect effect on
herbivores by affecting pathogen numbers (a numerical
interaction), in essence maintaining a population of
pathogens as bodyguards, or it may enhance the
effectiveness of the pathogen (a functional interaction)
by increasing contact rates with the host or the host's
susceptibility to the pathogen (see Janssen et al. (1998) for
a discussion of direct versus indirect and numerical versus
functional interactions in food webs).
While proposing possible interactions, it is important
to bear in mind the constraints imposed by the biology of
the organisms concerned. The three groups of entomo-
pathogens discussed are fungi, bacteria and viruses. Some
generalities are that fungi and bacteria may combine a
saprophytic lifestyle with insect pathogenesis, whilst
viruses are exclusively pathogenic. There are a variety of
routes by which entomopathogens disperse, but dispersal
in the air or in water is most important for fungi, whilst
dispersal via movement of infected hosts and release from
disintegrating host cadavers to drip down to lower leaves
is most important for viruses and bacteria. To infect new
hosts, fungi actively penetrate the cuticle. Bacteria and
viruses are ingested together with the plant substrate,
whereupon they must pass the hosts' gut lining to infect
it. These characteristics set the stage upon which the plant
may act to increase its fitness by promoting the
effectiveness of the pathogen.
Maintenance of a pathogen population
Where insect natural enemies of herbivores are employed
by plants as bodyguards, the provision of food and shelter
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230 S.L. Elliot et al
seems to be one of the best strategies available to a plant
as it allows for maintenance of a population of body-
guards that can act early against herbivore populations
before they become established. One may therefore expect
a similar strategy to be employed with respect to
pathogens of insect herbivores. In fact, the relative
immobility of pathogens may make this a very feasible
form of bodyguard interaction as the bodyguard is
unlikely to relocate to another plant. Much evidence
exists of fungal endophytes reducing insect and mammal
herbivory via toxins (Carroll 1988; Clay 1988; Saikkonen
et al. 1998) and of microbial populations on the phyllo-
plane and rhizosphere protecting the plant from phyto-
pathogens (Blakeman & Fokkema 1982; Cook 1993; Elad
et al. 1996). It is not then a great intuitive leap to suppose
that a plant may have evolved to exploit pathogens of
herbivores in a similar manner. Indeed, the fungal
pathogen Beauveria bassiana sprayed on to US corn was
found to grow into the plant and provide season-long
control of corn borer larvae (Bing & Lewis 1991).
This type of interaction was in fact proposed by Smith
& Couche (1991) to explain the high population densities
of Bacillus thuringiensis on the phylloplanes of trees and
other plants, and this in fact represents one of the few
formulations of the bodyguard hypothesis we were able to
find in the pathology literature. It has long been
wondered why B. thuringiensis is commonly found in
insects and soil, yet rarely causes epizootics in nature (e.g.
Dulmage & Aizawa 1982). If one casts the bacterium as a
plant mutualist then this begins to make a good deal of
sense: the bacterium may be maintained by the plant on
the phylloplane and in the soil while the plant benefits
from the bacterium killing insects before they reach large
numbers. Furthermore, microbial populations on leaves
can be spatially very heterogeneous (Kinkel 1997); so,
there may be a basis for herbivores to recognise and avoid
plants or critical plant parts that are protected in this
fashion, rendering the defence even more effective. Seeds
may tolerate a certain amount of growth of such
organisms and thereby gain protection, much as they do
with fungal endophytes (Carroll 1988; Clay 1988;
Saikkonen et al. 1998). The fact that fungi that combine
a saprophytic lifestyle with an entomopathogenic one are
able to grow on grains of rice or wheat (albeit boiled)
implies that plant seeds are at least nutritionally adequate.
Many plant traits will influence directly or indirectly the
survival of entomopathogens. Although certainly not the
only selection pressure on these traits, selection may
mould them to improve pathogen persistence. Examples
are canopy architecture, leaf form and leaf colour, which
can greatly diminish the harmful effects of UV on these
pathogen propagules. Other examples include the density
of hairs, waxiness, the veins, size and shape of leaf, angle
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of the leaf to the stem, number of stomata and density of
the canopy, which will influence the microclimate of the
leaf, the thickness of the boundary layer and the effects of
wind and rain (Burrage 1971; Ferro & Southwick 1984).
Finally, the phylloplane pH can affect infectivity of
polyhedra of baculoviruses (Young et al. 1977) and plants
may provide nutrition or other chemical needs. Conidia of
the fungal pathogen Aschersonia aleyrodis were found to
retain infectivity to whitefly much better on some plants
(e.g. cucumber) than others (e.g. poinsettia). Whatever the
reasons, the implication is that there is genetic variation
upon which selection may act. It certainly seems that
further investigation of this area could bear fruit.
Contact rates
The first means by which a plant may have a functional
effect on entomopathogens is by increasing the contact rate
of infective propagules with potential hosts, and this may be
via an effect on the pathogen or alternatively on the host.
Plant growth and form may determine contact not only
with phytopathogenic propagules but also with entomo-
pathogenic ones. Evidence for the latter comes form a
laboratory study by Ignoffo et al. (1977), who demonstrated
that soybean seedlings can pick up spores of the fungus
Nomuraea rileyi from the soil and that these spores can
subsequently infect larvae of Trichoplusia ni (soybean looper).
Inyang et al. (1998) showed that brassica leaf expansion may
reduce the density of spores of the fungus Metarhizium
anisopliae already present on the leaf and so reduce contact
with larvae of Phaedron cochliariae (the mustard beetle). Plants
may also influence the physical, chemical and biological
properties of soil, and in turn the growth and movement of
entomopathogens (Fuxa & Geaghan 1982; Storey &
Gardner 1987; Storey et al. 1989; Studdert & Kaya 1990).
Furthermore, one can imagine an influence of leaf shape,
glabrousness and waxiness on the ability of entomopathogen
propagules to penetrate the leaf boundary layer and then to
adhere. All of these factors influence the contact rate and may
therefore be modified by selection.
When attacked, many plants release herbivore-induced
volatiles which may attract predators or parasitoids. Few
attempts have been made to investigate the effects of these
volatiles on entomopathogens but it is conceivable that a
plant may influence pathogen behaviour by providing
signals, such as volatile chemicals, in order to stimulate
germination of dormant spores, affect arrestment in the
patch or even attract infected insects if the pathogen can
alter its hosts' responsiveness to plant volatiles. Indeed,
the study that comes closest to testing the bodyguard
hypothesis in entomopathogens is by Brown et al. (1995).
The authors found that the germination of conidia of the
entomophthoralean pathogen Pandora ( = Erynia) neoa-

phidis was inhibited by volatiles released by tobacco plants
in response to herbivory by Myzus nicotianae (tobacco
aphids). Germination would in this instance lead to the
production of secondary conidia, which would re-disperse
away from the leaf. Thus, the authors hypothesized that
the conidia ``sit and wait'' until they are picked up,
whereupon they germinate to infect the aphid hosts. This
hypothesis was unfortunately not tested but such arrest-
ment in response to herbivore-induced plant volatiles has
very strong parallels with other systems where plant
volatiles can cause predators or parasitoids to remain in a
patch, thereby acting as bodyguards for the plant (Sabelis
et al. 1999a, b).
A plant may also increase contact rates by manipulating
the insect herbivore distribution rather than that of the
pathogen. Heterogeneity in the concentration of resources
or toxins within a plant is known to affect herbivore
distribution, concentrating them in some areas of the plant
(Hoy et al. 1998). An alternative means to this end is to
limit new growth and expansion of leaves. These would
almost certainly increase transmission rates, which is an
important factor for many microorganisms. Plant form
and defences can also influence the mobility of herbivores
(Kartohardjono & Heinrichs 1984; Hoy et al. 1998) and so
their pick-up of pathogen propagules. With respect to
baculoviruses, the higher an infected herbivore feeds, the
more drip-down of virions will protect leaves from further
damage, so there may be a benefit to both the plant and the
pathogen to concentrate these herbivores higher up (even
at the cost of a higher risk of damage to the more
vulnerable parts of the plant). Alternatively, it may benefit
a plant for a mycosed herbivore to remain lower down or
away from the extremities to provide a more suitable
climate and to gain monopoly of dispersing spores.
Finally, a plant may increase the contact rate by
employing a fourth party. Although pathogens, predators
and parasitoids may compete for a common host or prey
species, there may be instances where the presence of one
enhances the effect of the other. The potential for other
natural enemies and scavengers to effect the dissemination
or horizontal transmission of pathogens has been demon-
strated in the laboratory (Brooks 1993; Fransen & van
Lenteren 1993; Pell et al. 1997), and there is some evidence
that this may lead to increased infection rates in the field
(Hochberg 1991). The presence of parasitoids may
increase transmission due to the increased movement of
the host (Furlong & Pell 1996) and predation pressure in
the field can increase the aggregation of herbivores and
thus make them more susceptible to pathogens (Cappuc-
cino 1988). So, any mechanism whereby a plant increases
the number or foraging activity of these fourth parties
would conceivably have an extra benefit by increasing
contact rate and therefore disease.
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Entomopathogens as plant bodyguards 231
Susceptibility
If a herbivore is diseased or liable to be so, then a plant
defence which somehow increases its susceptibility can be
just as effective as a more direct defence, or more so. One
component of a herbivore's susceptibility may be its
development time, which will in turn affect the length of
time for which it is vulnerable. The attractive hypothesis
that sublethal plant defences (or poor food quality) can
induce slow herbivore growth (perhaps especially of more
vulnerable life stages) and so high natural enemy-induced
mortality, has received mixed support from empirical
studies when tested with insect natural enemies (Clancy &
Price 1987; Benrey & Denno 1997). There is even
evidence that high food quality and herbivore growth
rates can be positively correlated with increased mortality
due to baculoviruses (Hoover et al. 1998). It may be
illuminating to explore this with more entomopathogens.
Different food plant types or species can alter
differentially the susceptibility of herbivores to pathogens
(Hajek et al. 1995; Peng et al. 1997). This leads into the
most obvious and the most studied area of tri-trophic
interactions within insect pathology, which is the effect of
chemical plant products on pathogens. This has been the
subject of a major review in the case of baculoviruses
(Duffey et al. 1995) and there are many examples from
other areas of insect pathology. Throughout the literature,
effects on entomopathogens are seen as a side-effect of
chemical defences against phytopathogens and herbivores.
These effects may be positive or negative; where positive,
fitness benefits to the plant may accrue, so the pathogen
effectively functions as a bodyguard. Where negative, any
fitness losses due to reduced herbivore disease are
presumably outweighed by the advantages accruing from
the direct protection from plant disease or herbivory.
There is variation in the effects of toxins on pathogens:
the toxin tomatine was found to be more toxic in vitro to
B. bassiana than was solanine (Costa & Gaugler 1989).
This may explain a lower natural prevalence of B. bassiana
in Leptinotarsa decemlineata (Colorado beetles) in fields of
tomato than fields of Solanum spp. (Hare & Andreadis
1983). We will probably never be able to test experimen-
tally whether greater fitness costs from this herbivore
have led to a greater selective pressure on Solanum spp.
for its alkaloid to be less toxic to its potential ally, B.
bassiana. However, we do see here a basis for such
selection to occur. Costa & Gaugler (1989) noted that B.
bassiana is relatively tolerant to alkaloids compared with
phytopathogenic fungi, but questioned how selection
pressure could be sufficiently strong on the pathogen to
have led to this. But there is of course every reason to
expect the pathogen to adapt to its chemical environment,
without corresponding coevolution of the plant to
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232 S.L. Elliot et al
counter this (as might be the case with a plant pathogen).
If indeed it does develop tolerance to plant alkaloids then
the production by a plant of a toxin which does not harm
B. bassiana may be selected for.
A particular case may be made for the production of
pathogenesis-related (PR-) proteins as a bodyguard trait.
These are synthesized by a plant in response to attack by
herbivores or phytopathogens and the chitinase activity of
many of these proteins may be able to degrade the insect
peritrophic membrane (Gopalakrishnan et al. 1995; Mayer
et al. 1995). This membrane is the principal barrier to
infection by baculoviruses and the entry of B. thuringiensis
toxins into the host body (see Lehane 1997). Laboratory
and field studies have shown that the activity of
baculoviruses and B. thuringiensis can be enhanced by the
addition of chitinases to the diet of lepidopterous insects or
to aerial spray applications in forestry (Smirnoff 1971, 1973,
1974; Morris 1976; Shapiro et al. 1987). The mechanism
that has been proposed is that the chitinase attacks the
insect's peritrophic membrane, making it more permeable
to virions or B. thuringiensis toxins. It may be that this
indirect effect on the herbivore has been to some degree
responsible for the evolution of this trait in plants. Such a
strategy would combine very well with the maintenance of
a population of bodyguard pathogens on the plant surface.
A parallel with the PR-proteins can be seen in the
piercing of the insect gut by plant trichomes (Wellso
1973). Aside from potentially severe direct effects, this (or
perhaps abrasion by other plant structures) would
probably aid subsequent invasion by pathogens and so
could be a bodyguard mechanism. Another possibility is
that the nutritional quality of the food plant, such as
amino acid concentrations, may diminish the herbivore's
ability to form a cuticle strong enough to resist
penetration by fungi (Mollema & Cole 1996).
SO IS IT WORTH IT?
For an entomopathogen to be employed as a bodyguard by
a plant, it must represent a good return on the investment
(the benefits of the trait must outweigh the costs), it must
complement the plant's other defences, and the investment
should be to some degree secure (i.e. not be overly
exploitable by herbivores or by the pathogen itself).
Costs and benefits of the interaction
For there to be a plant±bodyguard interaction it is the
gain in plant fitness which matters. Any active defence
mechanism on the part of the plant would probably entail
direct energetic costs which would impact on its ability to
invest in other activities, such as growth or reproduction.
In some cases, these costs will be so small as to be difficult
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to detect experimentally (Dicke & Sabelis 1992), in others
this will not be the case. They could also be so tied up in the
costs and benefits of another trait that they become hard to
disentangle. Furthermore, the costs and benefits may vary
in space and time (Bronstein 1994; Saikkonen et al. 1998)
and may not even add up to an overall benefit for a given
individual or local population in a particular environment.
Rather, defence should lead to an overall benefit over a
sufficiently large temporal and spatial scale. It is clearly too
early to discuss the direct costs in detail, but some indirect
costs may be envisaged and are now discussed.
Entomopathogenic bodyguards versus other plant defences
The fostering of an entomopathogen by a plant may lead
to disease in other potential bodyguard species and there
may also be interference between natural enemies redu-
cing the overall effectiveness. Investment in pathogen
bodyguards may limit the investment in other defence
mechanisms or may directly diminish their efficacy;
alternatively, it may act in synergy with other defences.
Whether it is beneficial to promote pathogens as
bodyguards over other defences, including other natural
enemies, will to some degree depend upon the relative
hierarchy of these defences. Modelling by Abrahamson &
Weis (1997) suggests that defences occurring earlier in the
sequence of the plant±herbivore interaction will generally
be subject to greater positive selection because those
acting later will have proportionally less herbivory to
prevent, and so a proportionally diminished fitness
benefit. Plant traits which promote bodyguards will be
among the first in this sequence as they lead to reductions
in herbivory. Where pathogen activity occurs earlier than
that of other natural enemies, the pathogen is more likely
to be utilized by the plant as a bodyguard.
Given that there are also predators and parasitoids
around, does it help the plant to invest in a pathogen as a
bodyguard? That mechanisms for the selective favouring of
different natural enemies may exist is suggested by work on
the effect of wheat plant resistance on the outcome of
within-host competition between the fungus Erynia
(=Pandora) neoaphidis and the parasitoid wasp Aphidius
rhopalosiphi. On a resistant wheat variety the pathogen was
favoured, apparently via an increased parasitoid develop-
ment time during competition within their host Sitobion
avenae (grain aphid) (Fuentes-Contreras et al. 1998). An
advantage of pathogens to the investor is their low
mobility: predators and parasitoids can walk or fly away.
Pathogens often have the means to survive periods of host
scarcity in certain environments, such as within host cada-
vers or the soil, or as resistant spores, as occlusion bodies in
the case of viruses, or as saprophytes. They may take a
while to kill their hosts but can rapidly reduce feeding rates,

in contrast to some parasitoids (see van der Meijden &
Klinkhamer 2000). Although pathogens may require a high
host density to cause an epizootic, once they do the large
number of propagules can lead to horizontal transmission
to a sizeable proportion of the host population, and where
vertical transmission also occurs, this can affect future
generations. Compared with the insect herbivores and
natural enemies, pathogens evolve much more rapidly,
allowing for adaptations to the local situation over an
ecological time scale. Where a plant supports a population
of predators or parasitoids, their growth rates are comp-
aratively low, whereas it may be possible to obtain a sub-
stantial population of a fungus or bacterium quite rapidly if
it is saprophytic. Furthermore, a plant may be able to
transmit a microbial bodyguard to its offspring (Clay 1988).
Risks from pathogens or herbivores
Fostering pathogenic microorganisms could be a risky
business for a plant which may itself be subject to attack
by pathogens. However, if they are able to use insect
predators and parasitoids as bodyguards without falling
foul of insect herbivores then the same may be true of
microorganisms. One means by which a plant may
selectively defend itself against phytopathogens is by
employing defences targeted at infection and subsequent
stages of the interaction, rather than earlier stages where
defences may adversely affect both plant and insect
pathogen. Where a reduction in generalized defences
favours an entomopathogen (e.g. leaf allelochemicals),
one can expect this also to favour herbivores or
phytopathogens, much as the production of herbivore-
induced plant volatiles may be exploited by another
herbivore to locate a vulnerable plant (Sabelis et al.
1999a). Whether the bodyguard trait is selected for will
then depend upon the biotic environment, principally
which species are present and at what levels.
A pathogen of an insect herbivore may well be able also to
exploit other bodyguard species as hosts, although many
pathogens have a host spectrum sufficiently limited for this
not to occur. Where a broad host spectrum is not
maintainable over evolutionary time, switching to third
trophic level hosts should be rare as these generally have a
lower density and so a higher epidemic threshold (Anderson
& May 1998). Of course, if predator or parasitoid levels (or
biomass) are higher or more constant than herbivore levels
because the plant is providing food to keep a population of
bodyguards (Bakker & Klein 1992; van Rijn & Tanigoshi
1999), then these may present a better potential host.
There is the potential risk of an entomopathogen
switching to phytopathogenicity. The fungal genera
Colletotrichum and Verticillium contain both plant and
insect pathogens, implying some flexibility over evolu-
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Entomopathogens as plant bodyguards 233
tionary time, but we know of no species which has a host
range spanning both groups ± this may, however, be
because any which are found are rapidly discarded as
biological control agents. If the plant represents to the
pathogen a large resource whilst the herbivore represents
an ideal means of dispersal, why should it not exploit both,
much as plant pathogens may exploit herbivores via
phoresy? Conversely, if a long-living plant is subject to
risk from a plant pathogen which is also capable of
attacking herbivores, it might benefit the plant to employ
one of the traits described above to increase the herbivore's
susceptibility and so drive specialization of the pathogen
towards an insect-pathogenic lifestyle. The degree to which
these processes can occur will depend upon how much the
specialization necessary to exploit adequately one type of
host renders the other type unsuitable.
PERSPECTIVE
One cannot help but be speculative in proposing an
alternative framework to interpret published results than
that employed by the authors: the hypothesis we present
has simply not been tested for entomopathogens within
tritrophic systems. As we have stated, it is hard to
disentangle the costs and benefits of a trait, and therefore
to ascribe a coevolutionary function. However, this is not
unique to the type of system we discuss.
The assumption throughout the literature is that plants,
herbivores, phytopathogens, predators and parasitoids
share an evolutionary history which may affect interac-
tions with pathogens coincidentally to be found on the
third trophic level. Only once this important group of
natural enemies of insect herbivores is seen as having been
a player in the coevolutionary game will adequate
hypotheses be formed to explore and explain the
ecological interactions being considered in a given system.
Once it is realized that pathogens are very much part of
this game, perhaps evolving faster than any of the other
players and so allowing the plant to keep up with the
more rapidly evolving herbivores (Carroll 1988), will their
true potential be exploited in pest management.
ACKNOWLEDGEMENTS
We thank Martijn Egas, Sara MagalhaÄes, two anonymous
reviewers and the editor J.J. Burdon for their valuable
comments. SLE was supported by the Netherlands Founda-
tion for the Advancement of Tropical Research (WOTRO).
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BIOSKETCH
Sam Elliot's research interest is applying concepts of evolu-
tionary ecology to invertebrate pathology, particularly in the
fields of food web interactions and the evolution of virulence.
Editor, J. Burdon
Manuscript received 24 September 1999
First decision made 23 November 1999
Manuscript accepted 8 February 2000
#2000 Blackwell Science Ltd/CNRS