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Suitability and potential of entomopathogenic

microorganisms for forest pest
management—some points for consideration
a b
S. I. Ahmed & S. R. Leather
a
Division of Forest Protection, Arid Forest Research Institute, 16/512 Chopasarry
Housing Board, Jodhpur, 342 008, India
b
Silwood Centre for Pest Management, Department of Biology, Imperial College,
Ascot, Berkshire, SL5 7PY, UK
Published online: 21 Nov 2008.

To cite this article: S. I. Ahmed & S. R. Leather (1994) Suitability and potential of entomopathogenic
microorganisms for forest pest management—some points for consideration, International Journal of Pest
Management, 40:4, 287-292, DOI: 10.1080/09670879409371901

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 INTERNATIONAL JOURNAL OF PEST MANAGEMENT, 1994, 40(4) 287-292

Suitability and potential of entomopathogenic microorganisms for forest pest

management—some points for consideration

(Keywords: entomopathogens, forestry, fungi, viruses, bacteria, nematodes, protozoa)

S. I. AHMED† and S. R. LEATHER‡$

†Division of Forest Protection, Arid Forest Research Institute, 16/512 Chopasarry Housing Board,
Jodhpur 342 008, India.
‡Silwood Centre for Pest Management, Department of Biology, Imperial College, Ascot, Berkshire, SL5 7PY,
UK.
Downloaded by [University of Illinois at Urbana-Champaign] at 12:01 31 August 2013

Abstract. The suitability of entomopathogenic organisms as part of a
suite of control measures in integrated pest management schemes in
forestry is critically reviewed. The use of fungi, viruses, bacteria, protozoa
and nematodes as control agents of forest insect pests is discussed with
particular reference to the contrast between these organisms and chemical
control methods. In general entomopathogenic organisms are environ-
mentally more suitable than the latter and, although currently more
expensive in monetary terms, are in the long run less expensive in terms
of deleterious side effects such as human health hazards and destruction
of non-target organisms. The fact that many of these organisms are able
to persist in the environment, despite their target organisms being at low
levels, also makes them more attractive to use than conventional
insecticides. The considerations that need to be given before using such
organisms, and future developments, are discussed. The use of entomo-
pathogenic fungi and baculoviruses as components of IPM systems is
highly recommended and seen as a real alternative to chemical control
methods in forestry.
1. Introduction
Entomopathogens provide a resource for selection of novel
agents effective in controlling insect pests of forest trees and
agricultural crops. Because of resistance to traditional chemi-
cal insecticides, removal of many chemical products from the
market and the lack of new insecticidal products, the use of
microbial pesticides in forestry, agriculture and public health
is growing rapidly (Starnes et al., 1993). In addition, the use
of chemical insecticides poses several problems such as
environmental contamination (Laskowski et al., 1990), ad-
verse effects on non-target organism (Isensee, 1991),
residues in food and water (Foschi, 1989; Roberts, 1989;
Tooby, 1989), and accumulation of chemicals in the food chain
(Mellanby, 1967). Microbial pesticides form a small part of the
market at present, but they are gaining in importance because
of improvements in their performance and cost competitive-
ness, and to increasing insect resistance to chemical insecti-
cides (Stames et al., 1993). The use of microbial insecticides
is growing at a rapid pace, 10-25% per year, as compared with
chemical insecticides at 1-2% per year. Hence, replacement
of the more environmentally unsuitable chemical pesticides
with safer control methods is now becoming a real possibility.
The development of integrated control systems combining
microbial, biological, chemical, sivicultural and mechanical
control methods may present the best solution for the not too
distant future (Hall, 1964; Katagiri, 1969; Speight and
Wainhouse, 1989).
In forest ecosystems, entomopathogens such as bacteria,
fungi, viruses, protozoa and nematodes may replace some of
the less specific and more dangerous chemical insecticides,
thus enabling naturally occurring beneficial insects (parasites
and predators) to play a greater role in the control and
regulation of insect pest populations. Microbial pest control
agents represent the largest number of recent registrations
obtained by commercial pesticide-manufacturing industries.
Currently there are 20 microbial products registered with the
Environmental Research Agency (USA) (Stames ef a/.,1993).
The general objective of this paper is to compare the relative
merits of entomopathogens and chemical insecticides and to
suggest environmentally acceptable measures to minimize
the hazards involved in forest pest management programmes.
2. General considerations
There are six major points to be considered in arriving at an
assessment of the suitability of any agent, whether chemical
or biological, for insect control. These are:
1. Specificity for the particular insect or range of insects to be
controlled with minimum effect on other species (non-
target organisms) and especially on those -that are
beneficial. The balance between desired specificity and
required target range may be difficult to achieve.'
2. Safety to man and other vertebrates.
3. Persistence of the effects so that the necessity for repeated
application is minimal.
4. No increase in resistance of the insect population.
5. Ease of application.
6. Cost, including all factors such as propagation, formulation
and utilization.
Despite the great and increasing importance of chemical
pesticides, all are deficient in one or more of the foregoing
criteria. Practically none are selective, and parasites and
predators are frequently killed indiscriminately together with

$To whom correspondence should be addressed.

0967-0874/94 $10-00 01994 Taylor & Francis Ltd.

 288 S. I. Ahmed and S. R. Leather
the target species. Many insecticides leave persistent
residues on the treated plants, posing problems in their
acceptability as a food or fodder. They may also be
concentrated in the food chain and become a hazard (Carson,
1962; Rudd, I974).
The forest ecosystem is an ideal environment for microbial
control for several reasons including:
1. The natural enemy complex for forest insects has a high
degree of predictability upon which sophisticated pest
management strategies can be based.
2. Along with their rich complex of natural enemies of
parasites, predators and pathogens, forest communities
often extend uniformly over large areas and these
complexes exhibit only minor regional differences.
3. Forests are usually long lasting ecosystems with a high
. degree of stability, a long evolutionary history and if they
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are not monocultural, possess great diversity of plant and
animal life.
3. Entomopathogenic microorganisms as control
agents and their role in the environment
To be able to estimate the risk of releasing a microorganism
into the environment it is important to understand the way in
which it interacts ecologically. In the case of many entomo-
pathogenic fungi and viruses, there has been extensive study
of their general pathogenicity, toxicity and safety to selected
animals in standard laboratory-based safety test protocol
fulfilment (Dresner, 1949),'but there has been only limited
research on their impact in the enviroment. Hence, extensive
studies of their ecology are increasingly being conducted as
the only sound basis for risk assessment.
3.1. Fungi
The entomopathogenic fungi hold rather a strange position
with regard to forest insect control. Over 500 fungi have been
reported to be associated with insects (Stames etal., 1993)
and some of them do cause serious disease in their host. Yet
very few have been used commercially as control agents.
Fungi infect a broader range of insects than do other
microorganisms and infection of the Lepidoptera, Homoptera
(aphids, plant hoppers, scale insects, etc.), Hymenoptera
(bees, wasps, sawflies), Coleptera (beetles, including wee-
vils), and Diptera (flies and mosquitoes) are quite common
(Brucher, 1964; Burges, 1973; Burke, 1982). Beauveria
bassiana has been recorded from many forest insect species
in both temperate and tropical regions and is used for pest
control on a moderate scale in both eastern Europe and China
(Stames et al., 1993). AF-4, a new B. bassiana-based
biosecticide produced by Mycotech, has been shown to be
highly pathogenic to Coleoptera. This fungus is amenable to
mass production of conidia by semi-solid fermentation and the
product has been found to be highly effective when field tested
against citrus root weevil.
Entomopathogenic fungi can be very effective in forest
nursery pest management when the plants may be attacked
severely by soil insects such as white grubs and by Gryllus
species. Reid trials using Entomophthora grylli against
grasshoppers in western Canada reduced populations by up
to 99% (Pickford and Reigert,1964).
Entomopathogenic fungi in general are less host specific
than viruses or bacteria. One strain of B. bassiana has been
reported as parasitizing more than 100 different insect species
(Cameron, 1977). It is also a possibility that parasites and
predators are as susceptible to entomopathogenic fungi as
their prey (Madelin, 1963). However, despite the wide host
range of some fungi they appear to be less detrimental to
biological control agents than chemical insecticides. This may
be because of differences between natural enemies and
herbivores; predators and parasites may be less exposed
under field conditions.
It has been generally believed that fungal spores germinate
only under conditions of very high relative humidity and
relatively high temperatures (Cameron, 1977) and this fact
has often been given as the reason for the sporadic and
unpredictable occurrence of fungal epizootics. This reason
has also been cited to explain the inadequacy of some fungal
pest control systems. However, attention to formulation can
counteract this problem (Bateman etal., 1993).
Most entomopathogenic fungi have the advantage that they
infect following contact by penetrating the host integument
and do not need to be ingested. Therefore, they can be used
as contact pesticides. In addition, they are not restricted to a
particular host stage of development and seem able to infect
all stages from egg to adult in both sucking and chewing insect
species (Samson et al., 1988). This may account for their
wider host spectrum compared with other insect pathogens.
In Canada, a large-scale screening programme was
established for species of entomopathogenic fungi which can
be mass-produced in the hope that the results would serve as
a basis for well planned field trials in the future (Entomological
Society of Canada, 1986). The use of fungal species with
economic potential to initiate and maintain fungal epizootics
is a very attractive strategy and research programmes should
be directed to overcome the technical problems involved in
their mass propogation. In addition, research should be
undertaken in isolating strains with a narrow host range so as
to produce 'tailor made' biocontrol agents.
It is suggested that future studies should be especially
directed towards the control of forest insects causing damage
to the root and shoot through excavation of tunnels because
soil is perhaps the most suitable environment for biocontrol by
entomopathogenic fungi as it has a generally high moisture
content suitable for fungal spore germination and growth.
3.2. Viruses
Members of more than 11 virus families infect insects.
Amongst these, the baculoviridae (especially nuclear polyhe-
drosis and granulosis viruses) have been the focus of control
strategy and implementation because of their effectiveness,
stability and comprehensive safety. There are many records
of control of forest outbreaks by viruses from Canada (Morris
etal., 1977; Cunningham etal., 1978), the USA (Abrahamson
and Harper, 1973; Steizer etal., 1975; Yendol, 1975), West
Germany (Schonherr, 1969), Japan (Koyama and Katagiri,
1967), Denmark (Zethner, 1976), France (Grison, 1960),
South Africa (Ossowski, 1960) and Yugoslavia (Sidor, 1965).
 Entomopathogenic microorganisms for forest pest management
Conversely, only a few reports on viral control have been
made in India and Britain (Cunningham and Entwistle, 1981;
Ahmed and Sen-Sarma, 1983; Ahmed and Joshi, 1987;
Entwistle and Evans, 1987; Ahmed era/., 1989a,b).
In India, examples of forest insects that are or can be
controlled by artificial dissemination of virus, are the poplar
defoliator Pygaera fulgurite (Ahmed and Sen-Sarma, 1983),
Amaltas defoliator, Catopsilia crocale (Ahmed and Joshi,
1987), the teak defoliator, Hyblaeapuera (Ahmed era/1989a,
b) and a polyphagous defoliator, Achaeajanata (Ahmed etal.,
1988,1989a, b). The control programmes directed against the
above pests have not been extended on a large scale,
because no adequate supply of virus material is currently
available.
The situation in Britain is very similar. Highly successful
large scale trials using nuclear polyhedrosis virus (NPV)
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against the pine beauty moth, Panolis flammea, and the pine
sawfly, Neodiprion sertifer(Cunningham and Entwistle, 1981;
Entwistle and Evans, 1987; Doyle and Entwistle, 1988), have
been carried out; Neodiprion sertifer NPV has been available
in the United Kingdom and Finland as separate commercial
products for several years but Panolis flammea NPV has yet
to complete registration. Several baculoviruses have been
developed and used commercially for crop pest control, e.g.
cotton boll worms (Heliothis spp.) of velvet bean caterpillar
(Anticarsia gemmatalis) on soy bean and of orchard crops
(Young and Yearian, 1989), e.g. codling moth (Cydia
pomonella) granulosis virus (Shieh, 1989).
There are a number of advangates to using an insect virus
as a control agent. Baculoviruses are ideal for IPM because
they do not affect predators and parasites. They are safe for
non-target insects, humans and the environment. One of the
major advantages associated with the use of baculoviruses is
the persistence of the virus infection in an insect population.
This is of great advantage in the control of forest insect pests
where the expected revenue is likely to be low and where the
need for repeated application of pesticides can make control
costs prohibitive. The NPV of the spruce sawfly, Gilplnia
hercyniae, is a good example of persistence in the insect
population both environmentally and by transovarian trans-
mission (Bird and Burk, 1961). The very long term persistence
of baculoviruses in the soil is well known and is, for example,
considered to be the inoculum source from which economi-
cally valuable epizootics of NPV disease originate in Douglas
fir tussock moth (Orgyia pseudotsugata). Some NPVs, e.g.
that of Malacosoma spp. are transmitted not only through the
egg but also by being preserved in the soil or on the host plant
(Clark, 1985)
As with other pathogens and also chemical insecticides, the
effectiveness of baculoviruses is maximized by good spray
coverage, especially where this is targeted to specific regions
of insect feeding. There are also limitations to the use of viral
pesticides. One of these is the slow rate of kill, resulting in
feeding damage. As it is unlikely that substantially more
virulent strains can be found, so reduction of kill time will rely
on improvements to formulation and application (including
accurate timing) in the immediate future (Starnes etal., 1993).
However, the limitation can be managed in the short term by
employing baculoviruses in carefully developed IPM systems.
Stames et al. (1993) also pointed out that the growth and
289
success of baculoviruses as commercial insecticides de-
pends on reducing production costs; developing practical
effective formulations; optimizing field performance, overcom-
ing regulatory obstacles, and educating users and the public.
There are many opportunities in the use of baculoviruses;
hence research and development have accelerated.
3.3. Bacteria
A number of earlier attempts to utilize bacteria in controlling
forest insects pests have been recorded in countries such as
Canada, Japan and the USA (Moms, 1984), but very little work
has been carried out, for example, in India and Britain. More
than 100 bacterial species have been identified as insect
pathogens, but only certain Bacillus species have enjoyed
success (Stames, etal., 1993). Of these Bacillus thuringiensis
(B.t.) has been widely exploited. Because of its environmental
safety, activity in insects resistant to chemical insecticides,
and selectvity, usage is increasing. Bacillus thuringiensis is a
naturally occum'ng pathogen and strains active against
Lepidoptera, Coleoptera and Diptera have been isolated
commercially (Morris, 1983; Keller and Langenbruch, 1993).
B.t. spores can remain viable in the soil apparently for several
years, germinating only when they are ingested by a suitable
host (Morris, 1982). However, infection of hosts is not
essential to control since B.t. produces toxic proteins which,
following ingestion, rapidly derange insect midgut function
leading to death.
It is well known that B.t. lasts only several hours on plant
foliage under typical field conditions because of ultraviolet
(UV) degradation, rain fall, etc. (Stames et al., 1993).
Pioneering work had been done in the forest environment for
control of the gypsy moth, spruce budworm and other forest
caterpillars. Optimization studies of droplet size and distri-
bution in a forest canopy from various aircraft in combination
with undiluted, high potency formulations have greatly im-
proved control of lepidopterous forest pests so that control is
equivalent to that of the most widely used chemical insecti-
cide, the juvenile hormone mimic, Dimilin (diflubenzuron). For
example Foray™ (Novo Nordisk) was optimized for forestry
taking into account all the factors necessary to deliver a high
B.t. dose to the place where the insect feeds (Stames et al.,
1993). The largest use of B.t. in forestry is against the spruce
budworm, Choristoneura fumiferana, in Canada and-fjarts of
the United States, the western spruce budworm C. occidental-
is, in the western United States and the gypsy moth Lymantria
dispar, in Canada and the United States (Roberts etal., 1991).
In forests it has been shown to have virtually no effects on
beneficial arthropods, and the possibility of a synergistic
interaction between B.t. and some of the parasites of the
gypsy moth has been suggested (Weseloh and Andreadis,
1982).
In India, recent attempts to utilize bacterial preparations
have been concentrated on various strains of B.t. These are
at present the only industrially-produced microbe for use in
controlling any lepidopterous forest insect pest. B.t. is now
being produced at the rate of hundreds of tons per year in
several countries and has been certified by the appropriate
licensing authorities for its use on a number of forest insect
pests (Entomological Society of Canada, 1986). In Britain,
 290 S. I. Ahmed and S. R. Leather
although B.t. is used on some agricultural and horticultural
crops (Evans, 1989), its use in forestry has been very limited.
A preparation of B.t. was applied aerially against P. flammea
in northern Scotland in 1977, but proved spectacularly
unsuccessful (Stoakley, 1987) because of the timing and the
method of application. However, the use of B.t. generally in
Britain appears likely to increase dramatically as farmers
move towards more environmentally acceptable pest man-
agement practices (Meadows, 1993). Sales of B.t. products
are estimated to rise by at least 20% per annum over the next
few years (Rigby, 1991).
3.4. Protozoa
There are many records of natural control of forest insect
outbreaks by the action of Protozoa (Henry, 1990), but despite
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the fact that microsporidia of the genera Nosema (Ishihara and
Sohi, 1966), Pleistophora (Wilson, 1981) and Vairimorpha
(Wilson, 1986) cause disease in many forest insect pests,
it cannot generally be said that all protozoa control their
host insects. Only one species of microsporidium, Nosema
fumiferana, which is particularly prevalent in long established
outbreaks of spruce budworm has been reported to reach
a level at which 70% of insects were infected (Wilson,
1982).
Some potential exists, e.g. there is ample evidence that the
presence of microsporidia in insects has a depressing effect
of fecundity (Thomson, 1958) and tests with Pleistophora
schubergi and Vairimorpha necatrix against the forest pest
caterpillars, Malacosoma disstria, and the spruce budworm,
Choristoneura fumiferana, in Canada, showed that high
infection rates and high level mortality could be achieved on
an experimental basis (Wilson, 1981,1986). In India no study
on insect pathogenic protozoa has so far been carried out but
certainly the information now available in other countries
indicates that extensive studies in this group are needed
(Payne, 1987).
3.5. Nematodes
Several nematode families contain species that are para-
sites of insects during at least part of the nematode's
development (Finney and Bennett, 1984). Steinernematid
nematodes can be easily and economically mass-produced
(Bedding, 1981) and are now available in Canada and several
European countries, where they are very effective against
glasshouse pests (Hominick and Reid, 1990). Laboratory
studies have shown that a wide range of forest insect pests
are susceptible to entomopathogenic nematodes and trials
against forest pests have been carried out in British Columbia
and Newfoundland (Entomological Society of Canada, 1986).
In Britain, the possibility of using Steinemematid nematode
species against the large pine weevil, Hylobius abietis, has
been discussed (Collins, 1993) but results so far, suggest that
some time will elapse before this is a feasible option in the field,
if ever.
In India, nematodes, particularly those belonging to the
family Mermithidae, have been reported to have potential
against many forest insect pests (Chatterjee and Singh, 1965;
Muthukrishnan, 1986). Ahmed (1982) reported high infection
by juvenile mermithid nematode during mass-rearing in the
laboratory of Calopepla leayana (Lepidoptera), the Gmelina
defoliator. However, if Mermithids are to have any future in
pest management, the strategy will be different from Stein-
emematids because of production and mode of action. Further
research and development on entomopathogenic nematodes
is necessary and hence should be encouraged.
4. Conclusions
It is now possible to make an assessment of the suitability
and potential of entomopathogenic microorganisms for mi-
crobial control of forest insect pests. Because of changing
attitudes to the employment of traditional chemical insecti-
cides, microbial pesticides are now much favoured, especially
within integrated pest management schemes. The following
major points should be considered:
1. Selectivity. Insect pathogens have a high degree of host
specificity and this makes them highly suitable for utiliza-
tion against one or more closely related host species, with
little or no danger to non-target organsims. The selectivity
of B.t. strains makes it especially effective against
lepidopterous pests without risk to hymenopterous and
dipterous parasites and predators. Entomopathogenic
fungi usually have a broad range but there are a few cases
reported where parasites of the target organism have been
affected by the same species that infects the pest species.
Baculoviruses are environmentally benign and totally
without danger for beneficial insects.
2. Safety. There are no known cases where an insect
pathogen developed for pest control has caused infection
in higher animals.
3. Resistance: Apart from some recent instances of B.t.
resistance in diamondback moth, Plutella xylostella, there
is little evidence to indicate that insects develop resistance
to entomopathogenic microorganisms (Cameron, 1977;
Tabashnik, 1992; Marrone and Macintosh, 1993). In any
case, B.t. achieves its effect by producing a toxin rather
than acting as a pathogen and it is to this toxin that
resistance has developed.
4. Persistence: Insect viruses, once introduced and causing
an epizootic in an outbreak, will generally persists long
as the outbreak lasts, although this is not alwaysthe case
(Payne, 1987). For example, virus epizootics in Achaea
janata (Lepidoptera) have been found \o exerf control
throughout the season (Ahmed, era/., 1989b). On the other
hand, B.f. tends strongly not to create persistent epizootics
and repeated applications may be necessary. Insect
pathogenic protozoa persist and spread by transovarian
transmission so once introduced they may be expected to
exert a continuing effect, although the level at which this
effect will act is unknown.
5. Application: All the microorganisms can be applied by
conventional equipment, but recent findings suggest
benefits are obtained by ulv/cda application methods
(Lisansky and Coombs, 1992; Bateman era/., 1993).
6. Cost So far only B.t. entomopathogenic fungi, nematodes
and baculoviruses have been produced industrially and the
 Entomopathogenlc microorganisms for forest pest management
required propagation work, although labour intensive, does
require investment. B.t. and fungi have the advantage that
they can be produced by fermentation on most media.
Baculoviruses and protozoa, however, are obligate parasites
and so far can be economically produced only in living insects.
Industrialization of insect cultures is possible and has been
done, but many people are sanguine about the eventual mass
production of viruses in insect cell cultures. Several forest
insect viruses have been mass produced in vivo.
Insect pathogens have the capacity to compete with
chemicals for the control of many forest pests. In view of the
hazards involved in the use of chemical pesticides—acute
toxicity, persistence in the environment, creation of new pest
problems by the accumulation of residues in the food chain—it
is hard to understand why conventional chemical insecticides
are still used to their present extent. In view of the pressure
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being put on the use of pesticides in several European
countries (Covarelli etal., 1988), it is extremely likely that the
use of entomopathogenic microorganisms will become in-
creasingly important components of IPM strategies for forest
protection.
Acknowledgements
It is a pleasure to thank Philip Entwistle and Chris Prior for
their detailed and helpful criticism of this paper. This work was
partly funded by the British Council.
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