Agri. Reviews, 34 (3) : 163-175, 2013
AGRICULTURAL RESEARCH COMMUNICATION CENTRE
www.arccjournals.com / indianjournals.com
DOI- 10.5958/j.0976-0741.34.3.001
ENTOMOPATHOGENIC NEMATODES - A REVIEW
Sumit Vashisth* , Y.S. Chandel and P. K. Sharma
Department of Entomology,
Himachal Pradesh Krishi Vishvavidyalaya, Palampur, 176 062, India
Received: 20-02-2012
Accepted: 19-10-2012
ABSTRACT
The entomopathogenic nematodes possessing balanced biological control attributes belong to
genera Steinernema and Heterorhabditis and are having mutualistic association with bacteria of the
genus Xenorhabdus for Steinernematidae and Photorhabdus for H eterorhabditidae.
Entomopathogenic nematodes being highly lethal to many important insect-pests, are safe to nontarget organisms and working with their symbiotic bacteria kill the insects within 24-28 hours as
compared to days and weeks required for insect killing in other biological control agents. Their
infective juveniles (IJs) have been reported to tolerate short-term exposure to many chemical and
biological insecticides, fungicides, herbicides, fertilizers and growth regulators, hence providing an
opportunity of tank-mixing and application together. Entomopathogenic nematodes are also reported
to be compatible with a number of agrochemicals and their use can offer a cost-effective alternative
to pest control. Only twelve species out of nearly eighty identified Steinernematids and Heterorhabditis
nematode species have been commercialized. The EPNs have the great potential to be used in
integrated pest management systems and work done have been reviewed in this article to facilitate
the students and researchers to have an overview of the work done and proceed further to undertake
the advanced research in different aspects related to entomopathogenic nematodes.
Keywords: Entomopathogenic nematodes (EPN), Heterorhabditis, Photorhabdus,
Steinernema, Xenorhabdus.
Nematodes are simple roundworms,
colorless, unsegmented, and lacking appendages,
may be free-living, predaceous, or parasitic. Many
of the parasitic species cause important diseases of
humans plants and animals. The term ‘Entomophilic
nematodes’includes all relationships of insects and
nematodes ranging from phoresis to parasitism and
pathogenesis. ‘Entomogenous nematodes’are those
that have a facultative or obligate parasitic
associations with insects. Entomogenous nematodes
have several deleterious effects on their hosts
including sterility, reduced fecundity, longevity and
flight activity, delayed development, or other
behavioral, physiological and morphological
aberrations and in some cases, rapid mortality.
Parasitic associations with insects have been
described from 23 nematode families. Seven of these
families contain species that have potential for
biological control of insects (Koppenhofer and Kaya,
2001). A very few cause insect death but these
species are difficult (e.g., tetradomatids) or expensive
(e.g. mermithids) to mass produce, have narrow host
specificity against pests of minor economic
importance, possess modest virulence (e.g.,
sphaeruliids) or are otherwise poorly suited to
exploit for pest control purposes. The only insectparasi tic nematodes possessing an optimal
balance of biological control attri butes are
entomopathogenic or insecticidal nematodes in the
genera Steinernemaand Heterorhabditis because of
their ability to kill hosts quickly (1-4 d depending on
nematode and host species). Mutualistic association
of these nematodes with bacteria of the genus
Xenorhabdus for Steinernematidae and
Photorhabdus for Heterorhabditidae have also been
reported by Boemare et al. (1993) . However,
although both the families belong to the same order,
but are not closely related and have distinctly
different reproductive strategies (Blaxter et al. 1998).
*Corresponding author’s e-mail: [email protected]
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AGRICULTURAL REVIEWS
Advantages:Entomopathogenic nematodes are
extraordinarily lethal to many important insect pests,
yet are safe for non target organisms (Georgis et al.,
1991). This high degree of safety means that unlike
chemicals, or even Bacillus thuringiensis, nematode
applications do not require masks or other safety
equipment; and re-entry time, residues, groundwater
contamination, chemical trespass, and pollinators
are not issues. Most biologicals require days or weeks
to kill, yet nematodes, working with their symbiotic
bacteria, can kill insects within 24-48 hours. Dozens
of different insect pests are susceptible to infection,
yet no adverse effects have been shown against
beneficial insects or other nontargets in field studies
(Georgis et al., 1991; Akhurst and Smith, 2002).
Nematodes are amenable to mass production and
do not require specialized application equipment as
they are compatible with standard agrochemical
equipments, including various sprayers (e.g.,
backpack, pressurized, mist, electrostatic, fan, and
aerial) and irrigation systems.
Life cycle: The entomopathogenic nematodes under
Steinernematids and heterorhabditids have similar
li fe histories. The free-living, non-feedi ng
developmentally arrested infective juveniles of these
nematode species have attributes of both insect
parasitoids or predators, they have chemoreceptors
and are motile, like pathogens, highly virulent, killing
their hosts quickly, and can be cultured easily and
have a high reproductive potential. When a host has
been located, the nematodes penetrate into the insect
body cavity, usually via natural body openings
(mouth, anus, spiracles) or areas of thin cuticle.
Wang and Gaugler (1999) compared the penetration
behavior of S. glaseri and H. bacteriophora into
Popillia japonica larvae and found that S. glaseri
penetrated primarily through the gut. H .
bacteriophora was not efficient at penetrating the
gut, presumably because of the thick peritrophic
membrane, but penetrati on through the
intersegmental membranes of the cuticle. Once in
the body cavity, a symbiotic bacterium (Xenorhabdus
for
steinernematids,
Photorhabdusfor
heterorhabditids), that are motile, Gram-negative,
faculatively anaerobic rods in the fami ly
Enterobacteriaceae released from the nematode gut,
which multiplies rapidly and causes rapid insect
death due to septicemia. Presently, eight species are
recognized but most isolates from recently described
entomopathogenic nematodes species have yet to
be determined (Hazir et al. 2003). The nematodes
feed upon the bacteria and liquefying host, and
mature into adults. Steinernematid infective juveniles
may become males or females, where as
heterorhabditids develop into self-fertilizing
hermaphrodites although subsequent generations
within a host produce males and females as well
(Fig. 1). The life cycle is completed in a few days,
and hundreds and thousands of new infective
juveniles emerge in search of fresh hosts.
Mode of action:Entomopathogenic nematodes are
a nematode-bacterium complex. In this association,
the nematode is dependent upon the bacterium for
quickly killing its insect hosts, creating a suitable
environment for its development by producing
antibiotics that suppress competing secondary
microorganisms and transforming the host tissues
into a food source. The bacterium requires nematode
for protection from the external environment,
penetration into the hosts haemocoel and inhibition
of the host’s antibacterial proteins.
Edaphic factors: Soil texture has an effect on
infective juvenile survival with survival being lowest
in clay soils. The poor survival rate in clay soils is
probably due to lower oxygen levels in the smaller
soil pores. Oxygen may also become a limiting factor
in water-saturated soils and soils with contents of
organic matter. Soil pH does not have a strong effect
on infective juvenile survival. Thus, infective juvenile
survival at pH values between 4 and 8 does not vary,
but survival declines at pH 10. Similarly, soil salinity
has only limited negative effects on
entomopathogenic nematode survival even at
salinity above the tolerance levels of most crop plants
(Thurston et al., 1994). Sea water has no negative
effects on survival of several Heterorhabditis species/
strains (Griffin et al., 1994) and they have been
frequently isolated from soils near the sea shore.
However, high salinity (seawater) reduced the ability
to Heterorhabdistis to infect hosts but did improve
their tolerance to high temperatures (Finnegan et al.,
1999).
Production and storage technology
Entomopathogenic nematodes are mass
produced as biopesticides usinginvivo or invitro
methods (Shapiro-Ilan and Gaugler 2002).
Vol. 34, No. 3, 2013
In vivo production: Production methods for
culturing entomopathogenic nematodes in insect
hosts have been reported by various authors (Dutky
et al., 1964, Poinar 1979 and Kaya and Stock,
1997). These references essentially describe systems
based on the White trap (White, 1927), which takes
advantage of infective juveniles (IJ) natural
migration away from the host cadaver upon
emergence. Yield is affected by choice of nematode
and host species. Among nematode species, yield is
generally proportional to host size (Blinova and
Ivanova, 1987 and Flanders et al., 1996) but yield
per milligram insect (within host species) and
susceptibility to infection is usually inversely
proportional to host size or age (Dutky et al., 1964
and Blinova and Ivanova, 1987). In vivo production
requires the least capital outlay and technical
expertise (Friedman, 1990; Gaugler and Han, 2002).
The most common insect host used for in vivo
laboratory and commercial entomopathogenic
nematode production is the last instar of the greater
wax moth, Galleria mellonella, because of its high
susceptibility to most nematodes, ease of rearing,
wide availability and ability to produce high yields
(Woodring and Kaya, 1988).
165
Formulation of nematodes into a stable
product has played a signi ficant role in
commercialization of these biological-control agents.
Active nematodes must be immobilized to prevent
depletion of their lipid and glycogen reserves. A
variety of formulations have been developed to
facilitate nematode storage and application including
activated charcoal, alginate and polyacrylamide gels,
baits, clay, paste, peat, polyurethane sponge,
vermiculite, and water-dispersible granules.
Depending on the formulation and nematode
species, successful storage under refrigeration ranges
from one to seven months. Low temperature (2-50C)
generally reduce metabolic activity and can therefore
enhance their shelf-life, some warm adapted species
such as H. indica and S. riobrave do not store well
attemperature below 100C (Strauch et al., 2000 and
Grewal 2002)
Relative effectiveness and application
parameters: Entomopathogenic nematodes are
certainly more specific and have no threat to the
environment than chemical insecticides (Ehlers and
Peters, 1995). In some instances, entomopathogenic
nematodes have proven to be safe and effective
alternatives to chemical pesticides, but in numerous
In vitro production: Production of entomo- other cases they have failed to compete successfully
pathogenic nematodes through in vitro requires a (Georgis et al., 2006). Technological advances in
thorough knowledge of biology and behavior of the nematode production, formulation, quality control,
nematode species produced. The only stage that can application timing and delivery, and particularly in
be commercially used is the dauer juvenile (DJ), a selecting optimal target habitats and target pests,
morphologically distinct juvenile, formed as a have narrowed the efficacy gap between chemical
response of depleting food sources and adverse and nematode agents. S. feltiae is an efficacious and
environmental conditions. Mass production of economical replacement for chemical insecticides
entomopathogenic nematodes has evolved from the in the floriculture industry in the Netherlands,
first large scale in vitro soild media production by England and Germany (Jagdale et al., 2004)
Glaser et al. (1940) to the three dimensional solid Entomopathogenic nematodes are remarkably
media in vitro process (Bedding, 1981 and 1984) versatile in being useful against many soil and cryptic
and to the in vitro liquid fermentation production insect pests in diverse cropping systems, yet are
method (Friedman, 1990). Currently, commercial clearly underutilized. Like other biological control
nematodes are produced monoxenically using the agents, nematodes are constrained by being living
solid-media process developed by Bedding (1981 organisms that require specific conditions to be
and 1984) or the liquid-fermentation method. The effective. Desiccation and temperature extremes are
solid media process has successfully produced the most important abiotic factors affecting survival
pathogenic steinernematids and heterorhabditids, of entomopathogenic nematodes (Glazer, 2002) and
but the high labour cost is the main constraint in soilinfective juveniles are subject to attack by a
(Bedding, 1990). The liquid-fermentation process, variety of microbial and invertebrate antagonists
is highly efficient for several steinernematid species (Kaya, 2002). Thus, desiccation or ultraviolet light
but not for heterorhabditids (Gaugler and Georgis, rapidly inactivates nematodes in comparison to
1991).
chemical insecticides. Similarly, nematodes are
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AGRICULTURAL REVIEWS
TABLE 1: List of insect pests targeted with entomopathogenic nematodes.
Order
Scientifi c and/or comm on
nam e
Com modit
y
Country
Nem atode
sp.a
References
Carposina niponensis
Walsingham
Phthorimaea operculella
(Zeller)
Chilo suppressalis (Walker)
Apple
C hi na
Sc
Potato
India
Sb, Hi
Wang (1993), Yang et al.
(2000)
Hussaini (2003)
Rice
Korea
Sc, Sg, H b
C. zonellus Swinhoe
M aize
India
Sc
T ryporyza i ncertulas (W alker)
Spodoptera littorali s
M aize
Rice
Cabbage
India
India
Egypt
Fo liar
crops
Glasshous
e and
nursery
crops
Crucifers
India
Sb, Hi
Sc
Hb, H i, Sc,
Sa, Sr
H i, Sg
India
Hi
Korea
Tobacco
India
Sc, H b, Sm ,
Sl, Sg
Sf
Tobacco
India
India
Sb, Hi
Sf
Corn
Fo liar
crops
Glasshous
e and
nursery
crops
USA
India
S sp.
H i, Sg
India
Hi
India
India
USA
Sg, Sc, St,
Sm , Ss
Hi
Sr
Famil y
Lepidoptera
Carposinid
ae
Gelechiidae
Pyralidae
N octuidae
Spo doptera litura (F.)
Spodoptera furgiperda
Helicoverpa armigera
Heli coverpa zea
Corn
Cnaphalocrosis medinalis
USA
India
S sp.
H i, Sg
Pieris rapae
Fo liar
crops
Cabbage
Egypt
Pieris brassicae L innaeus
Crucifers
India
Hb, H i, Sc,
Sa, Sr
H i, Sc, St
Agrotis ipsilon (Hufnagel)
Potato
A. segtum (Denis et
SchiVermueller)
Potato
India
India
India
India
Sf
Sb, Sc, H i
Sr
Sf
Turfgrass
India
Korea
Vegetables
Korea
Sb, Sc, H i
Sc, Sg, Hb,
Sl,.
Sm, H sp.
Sc, Sg, Sl,
Hb
Palpi ta indi ca (Saunder)
Choo et al. (1991), C hoo et
al. (1995)
Mathur et al . (1966), Rao et
al . (1971)
Hussaini (2003)
Rao et al . (1971)
Salem et al . (2007)
Saravanapriya and
Subramanian (2007)
Divy a et al. (2010)
Park et al. (2001)
Narayanan and
Gopalakrishnan (1987)
Hussaini (2003)
Narayanan and
Gopalakrishnan (1987)
Raulston et al. (1992)
Saravanapriya and
Subramanian (2007)
Divy a et al. (2010)
Ali et al. (2008)
Prabhuraj et al. (2006)
Cabanillas and Raulston
(1995)
Raulston et al. (1992)
Saravanapriya and
Subramanian (2007)
Salem et al. (2007)
Lalramliana and Yadav
(2010)
Singh (1993)
Hussai ni et al. (2000)
M athasoliya et al. (2004)
Singh (1993)
Hussai ni et al. (2000)
Lee et al. (1997)
Kang et al. (2004)
Kim et al. (2001 b)
Sb, Steinernema bicornutum; Sc, S. carpocapsae; Sf, S. feltiae; Sg, S. glaseri; Sl, S. longicaudum; Sm, S. monticolum; St, S.
thermophilum; S sp,. Steinernema species; H sp., Heterorhabditis species; Hb, H. bacteiophora; Hi, H. indica; Hm, H. marelatus
a
Vol. 34, No. 3, 2013
effective within a narrower temperature range
(generally between 20 °C and 30 °C) than chemicals,
and are more impacted by suboptimal soil type,
thatch depth, and irrigation frequency (Georgis and
Gaugler, 1991; Shapiro-Ilan et al., 2006).
Maintenance of high viability and virulence during
production, formulation and storage forms the
backbone of an effective quality control strategy.
Effect of ageing of infecti ve j uveniles on
pathogenicity was evaluated and compared by
Hussaini et al., 2005 with freshly hatched infective
juveniles of the genera Steinernema and
Heterorhabditis. S. tami and S. carpocapsae
survived up to 40 days without mortality and loss of
infectivity and S. abbasi with 2% mortality.
Heterorhabditis spp. survived up to 20 days without
mortality and declined to 60% and 20% after 40
and 60 days of storage, respectively.
167
Appearance: Nematodes are formulated and
applied as infective juveni les as they are
morphologically, physiologically and behaviorally
adapted to act as the active ingradient of a biological
pesticide. Infective juveniles range from 0.4 to 1.5
mm in length. The location of the infective juvenile
within the soil profile is one of the most important
factor (L ewis, 2002). Formulation in waterdispersable granules is very successful with the
ambush forager S. carpocapsae, while the cruise
foraging S. feltiae and S. riobrave rapidly migrate
out of the granules (Grewal, 2002). Disturbed
nematodes move actively, however sedentary
ambusher speci es (e.g. S. carpocapsae, S.
scapterisci) in water soon revert to a characteristic
“J”-shaped resting position. Ambushing nematode
species are usually associated with highly mobile
surface dwelli ng hosts. Entomopathogenic
Therefore, based on the nematodes’biology, nematodes disperse horizontally and vertically after
applications should be made in a manner that application. S. carpocapsae infective juveniles move
avoids direct sunlight, e.g., early morning or evening upwards in soil column (Georgis and Poinar, 1983;
applications are often preferable. Soil in the treated Schroeder and Beavers, 1987) where as S. glaseri
area should be kept moist for at least two weeks and H. bacteriophora move downwards, but they
after applications (Klein, 1993). Application to also disperse throughout the soil column. Low
aboveground target areas is difficult due to the temperature or low oxygen levels will inhibit
nematode’s sensitivity to desiccation and UV movement of even active cruiser species (e.g., S.
radiation; however, improved formulations have glaseri , H . bacteriophora ). In short, lack of
enhanced the efficacy of nematodes against above movement is not always a sign of mortality;
ground target pests (e.g., Shapiro-Ilan et al., 2010). nematodes may have to be stimulated (e.g., probes,
The most commonly used application method for acetic acid, gentle heat) to move before assessing
entomopathogenic nematodes is spraying directly viability. The infective juveniles do not feed, but
on to the soil (or other) surface. Nematodes can be relies on stored energy reserves. Lipids (especially
applied with most commercially available spray triglycerides) constitute up to 40% of the body weight
equipment including hand or ground sprayers, mist (Selvan te al., 1993, Fitters et al., 1999) and are
blowers etc. (Georgis et al., 1995). The infective most important energy reserve, though protein and
juveniles can withstand pressure up to 1068 kPa and the carbohydrates, glycogen and trehalose, also yield
pass through all common nozzle type sprayers with energy (Qiu and Bedding, 2000). Good quality
openings of about 100 µm (screen in nozzles should nematodes tend to possess high lipid levels that
be removed) in diameter. Nematodes can also be provide a dense appearance, whereas nearly
delivered via irrigation systems including microjet, transparent nematodes are often active but possess
drip, sprinkler, etc. (Georgis et al., 1995 and low powers of infection.
Insects killed by most steinernematid
Cabanillas and Raulston, 1996). In all cases, the
nematodes
become brown or tan, whereas insects
nematodes must be applied at a rate that is sufficient
killed
by
heterorhabditids
become red and the tissues
to kill the target pest; generally, 25 infective juveniles
2
per cm of treated area is required (rate can be assume a gummy consistency. A dim luminescence
increased or decreased according to target pest and given off by insects freshly killed by heterorhabditids
conditions) (Shapiro-Ilan et al., 2002). Selectivity is a foolproof diagnostic for the genus
of nematode species should be according to target H eterorhabditis (the symbiotic bacteria
Photorhabdus provide the luminescence). Black
pest.
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AGRICULTURAL REVIEWS
TABLE 2: Commercial products available in international market.
Nematode species
Steinernema carpocapsae
S. feltiae
S. ri obrave
S. scapteri sci
Heterorhabditis bacteriophora
H. megidis
S. carpocapsae
cadavers with associated putrefaction indicate that
the host was not killed by entomopathogenic species.
Nematodes found within such cadavers tend to be
free-living soil saprophages.
Prod uct formulation
Country
ORTHO Biosafe USA
Bio Vector USA
Exhibit USA
Sanoplant
Bod en Nutz;li nge
Helix
X-GNAT
Vector TL
Magent
Nemasys
Stealth
Entonem
Vector MG
Bio Vector
USA
USA
USA
Switzerland
Germany
Canada
USA
USA
USA
UK
UK
USA
USA
USA
USA
USA
UK
India
Otinem
Nemasys
Green commandos
Soil commandos
and target pest are of great importance if nematode
applications are to result in significant pest
reductions. Nonetheless, when considered as a group
of nearly 80 species, entomopathogenic nematodes
H abitat:Steinernematid and heterorhabditid are useful against a large number of insect pests
nematodes are exclusively soil organisms. They are (Grewal et al., 2005). Although in field infections,
ubiquitous, having been isolated from every impact on target populations has been frequently
inhabited continent from a wide range of ecologically judged modest or negligible, even when
diverse soil habitats including cultivated fields, concentrations equivalent to billion of nematodes
forests, grasslands, deserts, and even ocean beaches. per hectare are applied (Finney and Walker, 1979).
When surveyed, entomopathogenic nematodes are It would be premature to conclude that nematodes
recovered from 2% to 45% of sites sampled are safe for non target invertebrates in all habitats
(Hominick, 2002; Lalramliana and Yadav, 2010; (Akhurst, 1990). Nevertheless, considerable evidence
indicates that nematodes possess a restricted host
Khatri-Chhetri et al. 2010).
Host range: Entomopathogenic nematodes have range in natural systems and, therefore, are not nearly
been tested against a large number of insect pest as threatening as their experimental host range might
species with results varying from no effects to suggest (Kaya and Gaugler, 1993). Smitley et al.,
excellent control. Because the symbiotic bacterium (1992) were the fi rst to test the impact of
kills insects so quickly, there is no intimate host- entomopathogenic nematodes on plant parasitic
parasite relationship as is characteristic for other nematodes i n a field trial and presently,
insect-parasiti c nematodes. Consequently, entomopathogenic nematodes have been marketed
entomopathogenic nematodes attacks a far wider for control of certain plant parasitic nematodes,
spectrum of insects in the laboratory where the host though efficacy has been variable depending on
contact is assured, environmental conditions are species (Lewis and Grewal, 2005).
optimal and no ecological or behavioral barriers to Conservation:Reports and studies of natural
infection exists(Gaugler 1981 and 1988) . Field host occurrence and ecology of entomopathogenic
range is considerably more restricted, with some nematodes are relatively uncommon. Information
species being quite narrow in host specificity. from the manipulative experiments, however, can
Matching biology and ecology of both the nematode help to assess the effects of environmental factors,
Vol. 34, No. 3, 2013
169
infecting four scarabaeid species in three adjoining
sugarcane fields (Akhurst et al., 1992). Under
laboratory conditions, the scarabaeid larvae are not
susceptible to the nematodes, but in the field infected
larvae were readily recovered. This is largely
attributable to the mysterious nature of soil insects.
Consequently, research and guidelines for conserving
native entomopathogenic nematodes are in need of
advancement.
Compatibility: EPN infective juveniles (IJs) can
tolerate short-term exposures (2-24 h) to many
chemical and biological insecticides, fungicides,
herbicides, fertilizers and growth regulators, and can
thus be tank-mixed and applied together. This offers
a cost-effective alternative to pest control, and
facilitates the use of nematodes in integrated pest
FIG. 1: Generalized life cycle of steinernematids and
management systems. H owever, the actual
heterorhabditids. IJ = infective juvenile.
concentration of the chemical to which the
point out the gaps in our knowledge and help us to
nematodes will be exposed will vary depending upon
understand how this important group of natural
the application volume and system used (Alumai and
enemies of insects can be conserved (Lewis et al.,
Grewal, 2004). Compatibility has been tested with
1998). The reasons for success or lack of success in
well over 100 different chemical pesticides.
controlling insect pests, particularly in the soil
Entomopathogenic nematodes are compatible (e.g.,
environment, often remain unknown, underscoring
may be tank-mixed) with most chemical herbicides
the need to obtain basic information on the biology,
and fungicides as well as many insecticides (such
behavior, ecology and genetics of these nematodes.
as bacterial or fungal products) (Koppenhöfer and
Research in behavioral ecology has clearly
Grewal, 2005). In fact, in some cases, combinations
demonstrated that these entomopathogenic
nematodes are not generalist pathogens. Although of chemical agents with nematodes results in
most of them have a broad host range in the synergistic levels of insect mortality. Some chemicals
laboratory, in the field they are adapted to hosts in a to be used with care or should be avoided like
particular environment depending on their foraging aldicarb, carbofuran, diazinon, dodine, methomyl,
strategy. Their foraging strategy restricts much of their and various nematicides as they do not have any
activity to certain soil stratum eliminating many compati ble interaction. H owever, specific
insects from infection. Native populations are highly interactions can vary based on the nematode and
prevalent, but, other than scattered reports of host speci es and application rates. The
epizootics, their impact on host populations is organophosphate oxamyl increased S. carpocapsae
generally not well documented (Stuart et al., 2006). efficacy against Agrotis segetum synergistically, but
Epizootics of entomopathogenic nematode diseases only in fumigated soil, probably by enhancing the
probably occur regularly in soil, but they are difficult nematodes nictation behavior (Ishibashi, 1993).
to detect and often go unrecorded (Kaya, 1987). Two Furthermore, even when a specific chemical
epizootics, both from Australia involving undescribed pesticide is not considered compatible, use of both
Heterorhabditis species, have been documented agents (chemical and nematode) can be
(Akhurst et al., 1992; Sexton and Williams 1981). implemented by maintaining an appropriate interval
In the first case, a significant reduction of the between applications (e.g., 1 – 2 weeks). Prior to
whitefringed beetle, Graphagnathus leucoloma, use, compatibility and potential for tank-mixing
larvae and adults was observed in lucerne field should be based on manufacturer recommendations.
(Sexton and Williams 1981). In the second, two Combination of two nematode species may provide
undescribed species of Heterorhabditis were found effective control of two pests (Kaya et al., 1993) and
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AGRICULTURAL REVIEWS
the nematode species may coexist (Koppenhofer and
Kaya, 1996) if the target differs in susceptibility
against the search strategies and/or pathogenicity
of the two nematodes. Similarly, entomopathogenic
nematodes are also compatible with many pathogens
(Koppenhöfer and Grewal, 2005) like combination
of Bacillus thuringiensis (Bt) against several
lepidopterous pests resulted in additive and
antagonistic interactions. Interactions range from
antagonism to additivity or synergism depending on
the specific combination of control agents, target
pest, and rates and timing of appli cati on.
Koppenhofer et al., (2000) documented synergism
between Heterrhabditis spp. and S. glaseri and
neonicotinoid imidacloprid in scarab larvae. As
imidacloprid reduces the grub’s defensive behavior
resulting in increased nematode attachment and
penetration. Nematodes are generally compatible
with chemical fertilizers as well as composted manure
though fresh manure can be detrimental.
Commercial availability: Of the nearly eighty
steinernematid and heterorhabditid nematodes
identified to date, at least twelve species have been
commercialized. A list of some commercially
available entomopathogenic nematode products in
international market are given in table 2 (Siddiqui
et al., 2010 ) . One billion nematodes per acre
(250,000 per m2) is the rule-of-thumb against most
soil insects (greenhouse soils tend to be treated at
higher rates).
Conclusions: Entomopathogenic nematology has
a relatively short history dating back to the pioneering
research of R.W. Glaser and his coworkers in the
1930s and 1940s (Gaugler R and Kaya HK, 1990).
The primary emphasis of their research and of others
following them focused on developing and using
these nematodes as biological insecticides. The
reasons for success or lack of success in controlling
insect pests, particularly in the soil environment, often
remains unknown, underscoring the need to obtain
basic information on the biology, behavior, ecology
and genetics of these nematodes. Recently advances
made in nematode behavior and ecology clearly
demonstrates that they are not generalist pathogens;
their behavior, for example, restricts much of their
activity to certain soil stratum, eliminating many
insects from infection. Understanding these
behavioral patterns and their genetics will enhance
the use and production of the most adapted species
for insect control in the field.
Entomopathogenic nematodes (Rhabditida:
Steinernematidae and Heterorhabditidae) in
particular have emerged as excellent biocontrol
agents of soil-dwelling insect pests and hence
attracted widespread commercial interest. These
biological control agents are endowed with many
advantages including host seeking capability, high
virulence, ease of production, ease of application,
mammalian safety and exception from registration
in many countries. They also possess a broad host
range, are compatible with many other control
agents, are widespread in distribution and can be
formulated and stored for reasonable length of time.
However, the efficacy of these nematodes against
insect pests varied, particularly in soil environment,
are often unknown, emphasizing the need to obtain
basic information on the biology, behavioral ecology
and genetics of these nematodes. Indeed, there has
been a surge in research to obtain more basic
information and in exploration to discover new
nematode isolates. These nematodes are ubiquitous
in nature, but their populations usually are not
sufficiently high to cause epizootic and reduce pest
population. Research is needed to better understand
the factors that regulate their population and on how
their population can be manipulated to initiate
epizootic in insect-pest populations. Finally, these
fascinating animals may contribute more to science
than their use solely as biological control agents. To
begin with, they may be useful tools in understanding
the evolution of parasitism and symbiosis and
mechanisms by insect resistance to infection.
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