Management of Insect Pests by means of Entomopathogenic Nematodes

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35
Management of Insect Pests by means of
Entomopathogenic Nematodes
Muhammad Sarwar and Zahid Mukhtar
35.1 Introduction
Entomogenous microorganisms that arise in insects have the
power in bringing about a certain degree of natural or micro-
bial control of insect pests. Several entomopathogenic agents,
when are inundatively introduced into a variety of habitats,
can provide effective long-term to short-term control (Sarwar,
2015a,d). Nematodes feeding on bacteria, plants, and others can
be parasites of animals. Nematodes are usually considered pests
because of the diseases they cause in humans and animals, and
the economic impact they have on many agricultural products
(Adams and Nguyen, 2008).
They live parasitically inside the infected insect host, hence
they are also termed endoparasites nematodes (Sarwar et al.,
2020). Entomopathogenic nematodes occur naturally in soil
environments and locate their host in response to carbon diox-
ide, vibration, and other chemical cues (Kaya and Gaugler, 1993;
Sarwar, 2015b,c).
Nematode attacks an insect pest, kills or hampers the develop-
ment of the insect host, and is capable of mass production hence
can be used as an effective biological-control agent. In addition
to insects, nematodes can parasitize spiders, leeches, annelids,
crustaceans, and mollusks (Siddiqi, 2000; Sarwar, 2016).
The families Steinernematidae, Neosteinernematidae, and
Heterorhabditidae (Superfamily Rhabditoidea) are unique
because they are the only nematodes, which have developed the
ability to carry and introduce symbiotic bacteria into the body
of insects (Poinar, 1990). Of all nematodes studied for biologi-
cal control of insects, those in the families Steinemernatidae
and Heterorhabditidae have aroused the most interest, and
information about them is growing exponentially. These two
families, mutualistically associated with bacteria in the genus
Xenorhabdus, are similar in their actions. Xenorhabdus species,
which are gram-negative, facultatively anaerobic rods, belong
to the family Enterobacteriaceae. Both groups are in the order
Rhabdita, the bacteria-feeding nematodes (Poinar, 1990; Sarwar
and Sarwar, 2018). They have a broad host range, are safe to ver-
tebrates, plants, and other non-target organisms, easily applied
using standard spray equipment, compatible with many chemi-
cal pesticides, and are amenable to genetic selection (Georgis,
1990a; Zimmerman and Cranshaw, 1990).
The bacterial cells, voided from the nematode’s intestine into
the hemolymph, propagate and kill the host by bacterial septice-
mia within 48 hours. The nematodes feed on the bacterial cells
and host tissues, produce two or three generations, and emerge
from the host as infective juveniles to search for new hosts
(Bednarek and Nowicki, 1991).
Mutualism occurs between the nematode and bacterium
Xenorhabdus species. The bacterium requires the nematode for
protection from the external environment, penetration into the
host’s hemocoel, and possibly inhibition of the host’s antibac-
terial proteins (Akhurst et al., 1990). The nematodes provide
Biopesticides in Organic Farming Insect Pests Control by means of Entomopathogenic Nematodes
CONTENTS
35.1 Introduction ................................................................................................................................................................................ 225
35.2 Population Distribution of Nematodes ....................................................................................................................................... 226
35.3 Life Cycle of Nematodes ............................................................................................................................................................226
35.4 Parasitic Nematodes for Insects Control ....................................................................................................................................227
35.4.1 Steinernema Travassos ..................................................................................................................................................227
35.4.1.1 Steinernema carpocapsae (Weiser) Nematode .............................................................................................227
35.4.1.2 Steinernema feltiae (Filipjev) Nematode ....................................................................................................... 227
35.4.2 Heterorhabditis Poinar ...................................................................................................................................................227
35.4.2.1 Heterorhabditis bacteriophora Poinar Nematode ........................................................................................ 228
35.5 Commercialization .....................................................................................................................................................................228
35.5.1 Collection.......................................................................................................................................................................228
35.5.2 Mass Production ............................................................................................................................................................ 229
35.5.3 Formulation and Storage ...............................................................................................................................................229
35.5.4 Application Considerations ...........................................................................................................................................229
35.6 Conclusion and Future Prospects ............................................................................................................................................... 229
References ............................................................................................................................................................................................230
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226 Biopesticides in Organic Farming
shelter to the bacteria, which, in return, kill the insect host and
provide nutrients to the nematode. Together, the nematodes and
bacteria feed on the liquefying host, and reproduce for several
generations (Figure 35.1) inside the cadaver maturing through
the growth stages of J2-J4 into adults (Boemare, 2002; Gaugler
etal., 1997).
Nematode parasites of insects (also called entomophilic nema-
todes) can be found in the orders Aphelenchida, Ascaridida,
Mermithida, Oxyurida, Rhabditida, Spirurida, and Tylenchida
(Smart and Nguyen, 1994). Several species of Heterorhabditis
and Steinernema are available in multiple commercial formula-
tions, primarily for managing soil insect pests (Table 35.1).
35.2 Population Distribution of Nematodes
Entomopathogenic nematodes have limited dispersal ability and
are typically found in patchy distributions, The founding of new
populations and movement between patches may depend on the
movement of infective juveniles or the movement of infected
hosts (Lewis et al., 1998). Some studies suggest that entomo-
pathogenic nematodes may also use non-host animals, such as
isopods and earthworms for transport (Eng etal., 2005) or can
be scavengers (San-Blas and Gowen, 2008).
35.3 Life Cycle of Nematodes
Insect parasitic nematodes are mobile and move short distances
in search of host insects. The active stage of the nematode
that invades an insect is the juvenile (dauer larva) third stage.
Nematodes use carbon dioxide, vibration, and other chemicals
produced in waste products of insects as cues to nd their hosts.
Steinernema nematodes enter the insect through natural open-
ings, such as the mouth, spiracles, and anus, then penetrate into
the body cavity and enter into the hemocoel. Heterorhabditis
nematodes use natural openings, but also can enter by piercing
the body wall (Bedding and Molyneux, 1982).
Both Heterorhabditis and Steinernema are mutualisti-
cally associated with bacteria of the genera Photorhabdus
(Figure 35.2) and Xenorhabdus (Figure 35.3), respectively
(Ferreira and Malan, 2014). The insect cadaver becomes red if
the insects are killed by Heterorhabditids and brown or tan if
killed by Steinernematids (Kaya and Gaugler, 1993). Associated
color changes may occur, for instance, caterpillars parasitized by
Heterorhabditis may have a reddish-brown color.
Reproduction differs in Heterorhabditid and Steinernematid
nematodes. Infective juveniles of Heterorhabditid nema-
todes become hermaphroditic adults, but individuals of the
next generation produce both male and females, whereas in
Steinernematid nematodes all generations are produced by
males and females (gonochorisism) (Grewal etal., 2005). Insect
parasitic nematodes typically kill their host insect within two to
three days after invading the body cavity and a large number of
infective juveniles are eventually released into the environment
to infect other hosts, and continue their life cycle (Kaya and
Gaugler, 1993).
FIGURE 35.1 Entomopathogenic nematode assaulted insect.
TABLE 35.1
Commercial Use of Entomopathogenic Nematodes Steinernema and Heterorhabditis as Bioinsecticides
Pathogen Species Target Pests
Steinernema
Steinernema glaseri White grubs (scarabs, especially Japanese beetle, Popillia sp.), banana root borers
Steinernema kraussei Black vine weevil, Otiorhynchus sulcatus
Steinernema carpocapsae Turfgrass pests: billbugs, cutworms, armyworms, sod webworms, chinch bugs, crane ies. Orchard,
ornamental and vegetable pests banana moths, codling moths, cranberry girdlers, dogwood borers and
other clearwing borer species, black vine weevils, peachtree borers, shore ies (Scatella spp.)
Steinernema feltiae Fungus gnats (Bradysia spp.), shore ies, western ower thrips, leafminers
Steinernema scapterisci Mole crickets (Scapteriscus spp.)
Steinernema riobrave Citrus root weevils (Diaprepes spp.), mole crickets
Heterorhabditis
Heterorhabditis bacteriophora White grubs (scarabs), cutworms, black vine weevils, ea beetles, corn root worms, citrus root weevils
Heterorhabditis megidis Weevils
Heterorhabditis indica Fungus gnats, root mealy bugs, grubs
Heterorhabditis marelatus White grubs (scarabs), cutworms, black vine weevils
Heterorhabditis zealandica Scarab grubs
Heterorhabditis heliothidis Wide variety of soil-dwelling and boring insect larvae
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227Insect Pests Control by means of Entomopathogenic Nematodes
35.4 Parasitic Nematodes for Insects Control
Entomopathogenic nematodes t nicely into integrated pest
management programs because they are considered non-toxic
to humans, relatively specic to their target pest (s), and can be
applied with standard pesticide equipment (Shapiro-Ilan et al.,
2006). Because the nematodes are susceptible to drying and
ultraviolet light, they are most effective against insects that occur
in moist dark locations (Nickle, 1991).
35.4.1 Steinernema Travassos
Steinernema is the most widely researched species for insect con-
trols. In the insect cadaver, the fertilized eggs hatch as rst larval
juvenile (J1), and these animals molt into J2, J3, J4, and adults.
It is the most readily available for yard and garden use because
it is easier to rear and handle. In eld applications, Steinernema
carpocapsae tends to be most effective against caterpillar larvae.
In laboratory and eld trials, it has controlled sod webworms,
cutworms, and certain borers (raspberry crown borer, carpenter
worm).
35.4.1.1 Steinernema carpocapsae (Weiser) Nematode
Nematode S. carpocapsae (Figure 35.4) is a classic sit-and-wait
ambush attacker near the soil surface and will attach to passing
pest insects. This nematode is most effective against ea larvae
and caterpillars in lawns, garden soil, and under trees where lar-
vae pupate. It tends to be most effective when applied against
highly mobile surface-adapted insects. For managing the branch
and twig borer (Melagus confertus) in grapes, S. carpocapsae is
one of the recommended options (Varela etal., 2015).
Essentially the nematodes serve as mobile vectors for their
insect-pathogenic bacteria cargo. Symbiotic bacteria observed in
the intestinal tract (Figure 35.5) of S. carpocapsae are mutual-
istically grown in the host. Infected insect hosts die quickly, the
bacteria proliferate, the nematodes feed on bacteria and insect
tissues, and reproduce.
35.4.1.2 Steinernema feltiae (Filipjev) Nematode
They are the most effective against larval control of several
y species (Sciaridae, Phoridae, leaf miners, domestic y) and
also of some moth larvae (Sarwar, 2020). The entomopatho-
genic nematode, S. feltiae, has reduced raspberry crown borer
(Pennisetia marginata) populations by 33–67% (Capinera
etal., 1986).
35.4.2 Heterorhabditis Poinar
The Heterorhabditis nematodes are most effective against
Japanese beetles, weevils, and ma ny other target pests i n lawn and
garden. Several species are sold, including Heterorhabditis bac-
teriophora Poinar, H. megadis, and H. indica. Heterorhabditis
also effectively controls many nursery pests that feed in the root
FIGURE 35.2 Photorhabdus.FIGURE 35.3 Xenorhabdus.
FIGURE 35.4 Steinernema carpocapsae and invaded host.
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228 Biopesticides in Organic Farming
zone, such as black vine weevils and citrus-infesting root weevils
(Rasmann etal., 2005). (Figure 35.6)
35.4.2.1 Heterorhabditis bacteriophora
Poinar Nematode
Nematode Heterorhabditis bacteriophora (Figure 35.7) can be as
effective against white grubs as chemical insecticides, but is less
effective against mole crickets. Interactions with other organisms.
H. bacteriophora is an insect parasite used for the biological con-
trol of insects and an obligate host for symbiotic Photorhabdus
luminescens bacteria (Figure 35.8) and reproduces for 2–3 gen-
erations on the host (O’Halloran and Burnell, 2002).
They are highly efcient when the pest is more widely dis-
persed in the soil because they have a “tooth” to rupture the
insect’s skin. The nematodes are effective against grubs and the
larva or grub stage of Japanese beetles, northern masked cha-
fer, European chafer, rose chafer, y larvae, oriental beetles,
June beetles, ea beetles, termites, ants, bill-bugs, cut-worms,
army worms, black vine weevils, strawberry root weevils, fun-
gus gnats, sciarid larvae, sod web-worms, girdler, citrus weevils,
maggots and other Diptera, mole crickets, iris borer, root mag-
got, cabbage root maggot and carrot weevils.
35.5 Commercialization
Nematodes are open to mass production and do not require spe-
cialized application equipment since they are compatible with
standard agrochemical equipment, including various sprayers
(backpack, pressurized, mist, electrostatic, fan, and aerial) and
irrigation systems (Cranshaw and Zimmerman, 2013).
35.5.1 Collection
Steinernema is collected mostly in loamy-sand and sandy-loam
soils with a pH below 6, whereas Heterorhabditis can be com-
monly collected in sandy and loamy-sand soils with pH higher
than 6. After incubation the insects are removed and exam-
ined. Dead insects from each sample are rinsed and placed on
a moist lter paper in a petri dish for 3 to 4 days. The G. mel-
lonella larvae showing signs of parasitism by Steinernematids
or Heterorhabditids (Poinar, 1979) are transferred to a modied
White trap (White, 1929) to collect the infective juveniles (IJ).
Living insects from each site are also rinsed and placed on a lter
paper in a petri dish for 3 to 4 days at 23°C and then observed for
FIGURE 35.5 Symbiotic bacteria in Steinernema carpocapsae intestine.
FIGURE 35.6 Steinernema feltiae and host incursion.
FIGURE 35.7 Heterorhabditis bacteriophora and attacked host.
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229Insect Pests Control by means of Entomopathogenic Nematodes
parasitism. When IJs are recovered, they are rinsed three times
with sterile Ringer solution and nally added into a G. mel-
lonella larvae (Rosa etal., 2000).
35.5.2 Mass Production
Mass production of nematodes is inuenced by the amount of
progeny required, time, resources, the costs of production, as
well as the level of expertise available. The differences in nema-
tode life cycle and bacterial symbiosis play major role in nal
nematodes yields.
Large-scale commercial yields of entomopathogenic nema-
todes require economies of production (decreasing costs in yields
with an increasing scale of operation). Without such economies
of scale, commercial production of nematodes will be conned to
cottage industries. Mass production of entomopathogenic nema-
todes has evolved from the rst large-scale in vitro solid media
production by Glaser etal. (1940) to the in vivo production by
Dutky etal. (1964), to the three-dimensional solid media in vitro
process (Bedding, 1981), and to the in vitro liquid-fermentation
production method (Friedman, 1990). Once upon a time, com-
mercial nematodes have been produced monoxenically using the
solid-media process developed by Bedding (1984) or the liquid-
fermentation method.
Currently, entomopathogenic nematodes are produced by dif-
ferent methods either in vivo or in vitro (solid and liquid culture)
(Shapiro-Ilan and Gaugler, 2012). In vivo production is a simple
process of culturing a specic entomopathogenic nematode in
live insect hosts, which requires minimal technology and involves
the use of a surrogate host (typically larvae of wax moth (Galleria
mellonella), trays, and shelves. However, this method is not cost-
effective for scaled-up productions and may be ideal only for
small markets or laboratory studies (Shapiro-Ilan etal., 2002).
The quality of nematodes produced in vitro solid culture is
similar to that produced in vivo. A high quality of nematodes can
be produced using liquid culture provided good media as well
suitable environmental conditions in the bioreactor.
35.5.3 Formulation and Storage
Formulation of nematodes into a stable product has played a
signicant role in commercialization of these biological-con-
trol agents. Active nematodes must be immobilized to prevent
depletion of their lipid and glycogen reserves. Immobilization
has been accomplished by maintenance in aqueous suspensions
at low temperatures (5–15°C), but this approach is not commer-
cially desirable. Further advancements have been made with the
development of a owable concentrate that will revolutionize
nematode applications and eliminate many of the constraints
associated with current formulations, namely the dissolution
of the carrier or separation of the nematodes from the carrier.
Steinernematids, especially S. carpocapsae, can be maintained
for up to 5 months at room temperatures or up to 12 months
under refrigeration (Georgis, 1990b).
Formulated entomopathogenic nematodes can be stored for
2 to 5 months depending on the nematode species, and storage
media and conditions. The quality of the nematode product can
be determined by nematode virulence and viability assays, age,
and the ratio of viable to non-viable nematodes (Grewal etal.,
2005).
35.5.4 Application Considerations
Entomopathogenic nematodes can be applied with most horti-
cultural equipment including pressurized sprayers, mist blow-
ers, and electrostatic sprayers. In general, large diameter nozzles
(orices) and high volumes (up to 400 gallons per acre) are
recommended. It is also important to ensure an adequate agi-
tation during application because nematodes settle quickly in
suspension, high pressures (> 300 psi) should also be avoided
and nematodes can be kept cool by adding ice packs to the spray
suspension. Entomopathogenic nematodes are compatible with
many (but not all) insecticides, fungicides, and herbicides, but
fresh manure or high rates of chemical fertilizers (urea) can be
detrimental (Shapiro-Ilan etal., 2010).
Insect parasitic nematodes are sold in the infective juvenile
dauer larva stage and are barely visible to the unaided eye. They
typically are used at rates of 250 million to 2 billion per acre
(approximately 6,000 to 46,000 per square foot). To apply, dilute
the nematodes in water and drench the soil or inject them into
plants. Regular spray equipment can be used and nematodes are
quite tolerant of pressures found in many sprayers.
Innovative research has yielded insights into the fundamen-
tals of the genera Steinernema and Heterorhabditis. Substantial
progress in research on biology including major advances in
genomics, nematode-bacterial symbiont interactions, ecological
relationships, and foraging behavior and application has been
made in the past decade, and the numbers of target pests shown
to be susceptible to nematodes have continued to increase (Lacey
etal., 2015).
35.6 Conclusion and Future Prospects
Entomopathogenic nematodes are a group of nematodes (thread-
worms), causing death to insects. While most parasitic nema-
todes might be seen as harmful, entomopathogenic nematodes
are benecial to humans. Entomopathogenic nematodes are a
welcome addition to the natural enemy pool of insects and can
be integrated with various control measures for management of
those target pests where individual tactics alone are inadequate.
Entomopathogenic nematodes play a role underground reminis-
cent of that played by insect parasitoids. Like parasites or preda-
tors they have chemoreceptors and are motile. Like pathogens
FIGURE 35.8. Photorhabdus luminescens in intesti ne of H. bacteriop hora.
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230 Biopesticides in Organic Farming
they are highly virulent, killing their hosts quickly, and can be
cultured easily in vivo or in vitro.
Their eld efcacy could be improved simply by matching
nematode species and strains against those insects for which they
are best adapted. Further understanding of their biology, behav-
ior, ecology, and genetics will enhance the use and production of
the most adapted species for insect control in the eld. Recent
advances made in nematode behavior and ecology clearly dem-
onstrate that they are not generalist pathogens and their behavior
restricts much of activity to a certain soil stratum, thus eliminat-
ing many insects from infection. The occurrence of quiescent
nematodes suggests that they have evolved for effective survival
strategies, and the J2 cuticle on some nematode species seem
to play a signicant role in desiccation tolerance and protection
against fungal antagonists. They can be used effectively and
selectively as inundative agents against numerous insect pests
and have the potential to be used as inoculative agents for classi-
cal biological control. Finally, conservation and augmentation of
natural nematode populations through proper management prac-
tices and periodic nematode releases offer exciting possibilities
for insect pests suppression.
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