ARTICLE IN PRESS

Crop Protection 26 (2007) 1–10

www.elsevier.com/locate/cropro

Review

Review of Nezara viridula (L.) management strategies and potential for

IPM in field crops with emphasis on Australia
Kristen M.M. Knighta, Geoff M. Gurrb,
a
Biopesticides Unit, Plant Science, Department of Primary Industries & Fisheries, 80 Meiers Road, Indooroopilly, QLD 4068, Australia
b
Pest Biology and Management Group, Charles Sturt University, Orange, PO Box 883, NSW 2800, Australia
Accepted 13 March 2006

Abstract

Nezara viridula (L.) is a cosmopolitan, polyphagous heteropteran that causes economic damage to many crop species. At present,
control of N. viridula in Australia and other countries relies heavily upon insecticides, most of which are disruptive to beneficial insects,
constituting a constraint on integrated pest management (IPM). Much research has been conducted into non-chemical control methods
for N. viridula. This paper reviews the potential for and limitations of sterile insect technique, classical, inundative and conservation
biological control, and trap cropping. None of these techniques appear to be adequate for control of N. viridula when used alone but
there is scope for these non-chemical approaches to be adopted for use in integrated management of this pest. A proposal is given for one
such integrated approach for future development. It includes biopesticides, trap crops and carefully targeted habitat manipulation to
enhance arthropod natural enemies as well as area-wide management and grower education.
r 2006 Elsevier Ltd. All rights reserved.

Keywords: Nezara viridula; IPM; Soybeans

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2. Biology of Nezara viridula . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2.1. Origin and distribution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2.2. Life cycle. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2.3. Behaviour . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2.4. Plant hosts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2.5. Host plant factors affecting survival and development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
2.6. Pest status . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3. Management options for Nezara viridula . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3.1. Sterile-insect technique . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3.2. Biological control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
3.2.1. Classical and inundative biological control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
3.2.2. Conservation biological control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
3.2.3. Biopesticides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
3.2.4. Conservation biological control to enhance entomopathogens . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
3.3. Trap crops. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
4. Integrated pest management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
5. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

Corresponding author. Tel.: +63 60 551; fax: +63 60 5590.

E-mail address: ggurr@csu.edu.au (G.M. Gurr).

0261-2194/$ - see front matter r 2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.cropro.2006.03.007
 ARTICLE IN PRESS
2 K.M.M. Knight, G.M. Gurr / Crop Protection 26 (2007) 1–10
1. Introduction
The pentatomid Nezara viridula (L.) is a major pest of
soybeans (Glycine max L. Merr) other grain legumes and
many other crops in Australia and throughout the world
(Clarke, 1992; Waterhouse, 1998). In most soybean
growing areas of the world including Australia, control
measures for N. viridula rely on chemical insecticides
(Cheyn et al., 1992; McPherson et al., 1994; Todd et al.,
1994). As a result of increasing restrictions on the use of
endosulfan in Australia, the most commonly used insecti-
cide in soybeans and other pulse crops is the synthetic
pyrethroid, deltamethrin (Brier and Lucy, 1999). Although
deltamethrin gives control of N. viridula it is harmful to
natural enemies, making it incompatible with integrated
pest management (IPM) strategies for soybeans or pulse
crops. This constrains the extent to which industry is able
to manage the risk of pesticide resistance and address
environmental impact and food safety concerns.
This review examines the literature on non-chemical
management methods for N. viridula and considers the
scope to develop a more integrated management approach.
Key aspects of pest status and biology are reviewed before
prospects for development of IPM for soybeans is
specifically considered.
2. Biology of Nezara viridula
2.1. Origin and distribution
N. viridula is the most important widespread polypha-
gous heteropteran in the world (Todd, 1989). It is found
throughout the tropical and subtropical regions of the
world including the Americas, Asia, Australasia, and
Europe (Waterhouse, 1998). These authors suggest that
human activity spread the pest from Africa. However, N.
viridula is a strong flier and may have arrived due to
weather systems as well as human means of transport.
In Australia, N. viridula is a pest of many horticultural and
field crops. It established in the Sydney area as early as 1911,
and by 1938 was recorded in all mainland states (Clarke,
1992). While N. viridula is rare over large areas of Australia,
it is considered a major pest in cropping areas throughout
Australia. For instance, it is a major pest in the Northern
Territory (Ward, 2005) and tropical Queensland (H. Brier,
2001 pers. comm.). At present, N. viridula is distributed from
north Queensland to southern Victoria. Its greatest abun-
dance is in a broad belt stretching from southeast Queensland
to central Victoria (Clarke, 1992). In southern Queensland
and northern New South Wales (NSW), N. viridula is most
commonly associated with soybean. Nevertheless, it is not
restricted to that crop and occurs regularly on other hosts.
2.2. Life cycle
Barrel-shaped eggs are laid in rafts consisting of between
80 and 120 or more eggs (Waterhouse, 1998). The eggs are
cemented firmly to one another and usually hatch in 4–9
days. As eggs mature they become deep yellow, then pinkish-
yellow, and finally bright orange at eclosion (Todd, 1989). N.
viridula develops through five instars before reaching
maturity, 24–60 days after hatching. Instar duration depends
on temperature and on host food supplies. First instars
cluster on or near the egg mass and apparently do not feed
(Velasco and Walter, 1992; Waterhouse, 1998).
Adults live for up to 3 weeks in hot summer weather,
longer over winter. Four generations per year have been
observed in Florida and Louisiana, and a fifth generation
has been known to occur in southern Florida (Todd, 1989;
Velasco et al., 1995). However, Velasco et al. (1995)
reported only two principal generations in southeast
Queensland. Coombs and Sands (2000) found three
generations in northern NSW. In regions with a cold
winter the autumn generation may live much longer,
overwintering or diapausing in debris, under bark, or in
buildings (Waterhouse and Norris, 1987; Todd, 1989).
While most diapausing N. viridula turn a reddish brown
colour, this is not the case for all individuals (Seymour and
Bowman, 1994). Diapause is controlled by a long-day
photoperiodic response with the critical day-length for
diapause falling into a narrow range close to 12.5 h
(Musolin and Numata, 2003). Musolin and Numata
(2004) suggest that the environmental conditions required
for colour change do not always coincide with those
required for diapause induction and that the colour of the
adults is not always a reliable indicator of diapause.
Although reproduction ceases during overwintering, survi-
val is improved by feeding and adults often feed during
mild periods on mustard (Brassica spp.) and wild radish
(Raphanus spp.) (Todd, 1989).
Eggs are deposited in the upper regions of crops on the
undersurface of leaves or pods (Todd, 1989). Egg hatch is
temperature dependent and the synchronization of hatching
of an egg mass is due to the emergence of nymphs stimulating
hatching in neighbouring eggs (Lockwood and Story, 1986).
2.3. Behaviour
First instars initially aggregate using tactile cues from
both the egg mass and their siblings (Lockwood and Story,
1985) but by 2 days after emergence they develop an
aggregation pheromone. Nymphs at this stage do not feed
and remain on the egg mass unless disturbed (Todd, 1989).
When nymphs moult to second instar, they begin to feed
but remain aggregated near the egg mass. Third instar
nymphs also remain aggregated; however, they move from
the egg mass. At fourth instar, the clustering behaviour
ends as the nymphs disperse and by the fifth instar the
siblings are widely distributed.
2.4. Plant hosts
The host range of N. viridula includes over 30 families
of dicotyledonous plants and a number of monocots
 ARTICLE IN PRESS
K.M.M. Knight, G.M. Gurr / Crop Protection 26 (2007) 1–10
(Todd, 1989). Velasco et al. (1995) found N. viridula on 34
plant species belonging to 11 families in southeast Queens-
land. Legumes seem to be the favoured hosts for this insect
however it is also a significant pest of cotton. Panizzi (1997)
states that knowing the effect of the various wild host
plants on nymphal or adult performance will help in the
management of selected certain favourable hosts to
mitigate their role in the build-up of pest populations.
2.5. Host plant factors affecting survival and development
In southeast Queensland N. viridula numbers increase in
spring (September–November), and decline through sum-
mer until early autumn when N. viridula become common
on soybeans. Host plants have a significant impact on
nymphal development and adult reproduction. Velasco and
Walter (1992) reported that survival of nymphs to adults is
greatest on soybean (74%) and sorghum (70%) whilst on
thornapple and wild crucifer it was less than 50%. Clover,
lucerne, and sunflower allowed less than 5% of nymphs to
reach adulthood. Over 70% of adults survived on soybean,
sunflower, sorghum, castor bean, and corn. However, less
than 20% were alive after 6 weeks on clover and wild
crucifers. Host plant significantly affected reproductive
performance as soybean produced the highest number of
nymphs (125/female), followed by wild crucifer (94/
female), castor bean (95/female) and corn (3/female).
It can be concluded from these results that only soybean
is highly suitable for both nymphal development and adult
reproduction. There is either a difference in the nutritional
requirements of nymphs and adults or the ability to deal
with toxic secondary chemicals is not similar (Velasco and
Walter, 1992). In the same experiment, there was no
indication that any particular host plant was more attractive
than others to adult N. viridula and that no host species was
especially attractive to adult females for oviposition
(Velasco and Walter, 1992). However, the species of host
plant has a significant effect on the reproductive success of
N. viridula and thus on its population dynamics (Velasco
and Walter, 1992). The seasonal pattern of host availability
is expected to generate a changing pattern of N. viridula
distribution and abundance.
The seasonal peak in N. viridula numbers in southeast
Queensland coincides with the availability of hosts suitable
for both nymphal survival and adult reproduction. In
spring, wild crucifers are available when adults emerge
from diapause. In summer N. viridula numbers (both adult
and nymphs) decrease as the only hosts available at this
time are not suitable for egg production or nymphal
survival (Velasco and Walter, 1992). The increase in
N. viridula numbers during late summer and autumn seems
to be the result of availability of soybean. Once on
soybeans, populations may rapidly increase because of
high reproductive success on this host. It can be concluded
that the availability of suitable host plant species therefore
influences to a large degree the changing abundance of
N. viridula in southeast Queensland.
3
Velasco (1989) found that it is possible for four
generations of N. viridula to occur in a season in southeast
Queensland. As temperature is not a limiting factor, the
lack of nutritious food sources during the early part of the
season may in the past have limited the number of
generations of N. viridula. Since Velasco and Walter
(1992) conducted their research, cropping patterns in
southeast Queensland have changed. Spring plantings of
mungbeans and earlier maturing varieties of soybean such
as cv. Melrose may cause an increase in the number of
generations of N. viridula.
2.6. Pest status
The importance of N. viridula is increasing in Australia
and is thought to be due to the widespread planting of
genetically modified (GM) cotton, the use of IPM for
Helicoverpa spp., the popularity of early season soybeans
and the expansion of spring and summer planted mung-
beans. N. viridula were not regarded as economically
important pests in cotton prior to the release of GM
varieties as the populations were previously suppressed by
multiple applications of broad-spectrum insecticides for
control of Helicoverpa spp. (Greene et al., 2001; Willrich et
al., 2004).
There have been many attempts by researchers to
develop more sustainable practices to control N. viridula
including: partial sterilisation of insects, biological control,
biopesticides and trap cropping. However, use of these
methods individually has rarely succeeded in providing
acceptable control of N. viridula. The following sections
describe and evaluate a number of control strategies for N.
viridula, which do not rely solely on synthetic chemical
control.
3. Management options for Nezara viridula
At present in Australia, N. viridula is controlled with
relatively non-selective insecticides such as deltamethrin or
endosulfan. Whilst endosulfan is increasingly restricted for
environmental reasons (Brier and Lucy, 1999), deltame-
thrin may cause outbreaks of secondary pests such as two-
spotted spider mite, Tetranychus urticae (Koch) (Knight
and Brier, 2000). Currently other products are being tested
to ascertain efficacy and selectivity, but new products as
effective and as selective as endosulfan have not yet been
identified (Brier, Knight and Khan, unpublished data).
Many potential new products are likely to be more
expensive and thus uneconomic for pulse or soybean
growers with small gross margins.
3.1. Sterile-insect technique
The principle of sterile-insect technique is that the
number of sterile males released must be great enough to
prevent reproduction, so starting a downward trend in the
population. The higher the initial ratio of sterilised to
 ARTICLE IN PRESS
4 K.M.M. Knight, G.M. Gurr / Crop Protection 26 (2007) 1–10
fertile individuals, the quicker the pest is brought under
control (Pedigo, 1992). Dyby and Sailer (1999) exposed
N. viridula to ionizing radiation of o10 Gy. This level of
radiation rendered fourth instar nymphs (when testes and
ovaries begin maturation) partially sterile. Irradiated
female N. viridula laid mostly non-viable eggs and had
significantly lower fecundity than the control insects. The
surviving progeny of partially sterilised N. viridula were,
however, capable of reproductive recovery. There are two
other possible strategies for autocidal management of this
pest: release of nymphs sterilised at 15–20 Gy, or use of
irradiation for breeding for translocations or other
chromosomal defects promoting lethality in heterozygous
individuals. In winter or spring, sterile insects could be
released in order to create a less fit population (Dyby and
Sailer, 1999). Using this diversified approach may decrease
the likelihood of N. viridula reaching economic thresholds
in the summer months.
Ultimately, however, the high cost of rearing N. viridula,
($4000 per 1000 insects) (H. Brier, pers. comm.) will
preclude use of this method unless cheaper rearing methods
can be developed. For example, assuming a crop with as
few as 0.1 adults/m2 and a release rate of 10 sterilised adults
per unsterilised adult, the cost of one release is $40,000/ha.
A release of 10,000 adults would also cause significant
damage in most crops. In the case of N. viridula, adults as
well as nymphal stages can cause crop damage in contrast
to well-known examples of success in sterile-insect techni-
que, such as screw worm, Chrysomya bezziana (Villeneuve),
where adults are released but it is the larval life stage that
causes damage (Spradbery, 1994).
3.2. Biological control
3.2.1. Classical and inundative biological control
There are many examples of the use of classical
biological control agents for N. viridula throughout the
world. Waterhouse (1998) gives a comprehensive coverage
of these, the majority of which are hymenopterous egg
parasitoids including Trissolcus basalis (Wollaston) and
tachinid parasitoids that attack adult or late nymphal stage
N. viridula, such as Trichopoda giacomellii (Blanchard)
(Waterhouse, 1998).
Trissolcus basalis was released in Western Australia in
1933 and is now distributed throughout all mainland states
(Clarke, 1992). Loch and Walter (1999) consider it difficult
to assess the degree to which N. viridula populations are
suppressed by T. basalis in Australia, so biological control
could not be considered completely successful, especially in
southeast Queensland where N. viridula remains a sig-
nificant pest despite sometimes-high parasitism rates by
T. basalis. In NSW and Queensland, N. viridula remains a
major pest of soybeans and other pulses (Clarke, 1992;
H. Brier and M. Lucy, 2000, pers. comm.). Currently, it is
regarded as the chief impediment to organic production of
soybeans in NSW (R. Neeson, 2001, pers. com.) and a
major pest that requires control each season in many major
field and horticultural crops in subtropical and tropical
Australia (I Crosthwaite, 2001, pers. comm.). T. basalis is
known to parasitise the eggs of native predatory bugs, such
as Oechalia schellenbergii (Guérin-Méneville) (Loch and
Walter, 1999) thus constituting an example of a non-target
effect of biological control (Howarth, 2000). Other than the
direct consequence of this attack it may also have a
deleterious effect by reducing the impact of these predatory
bugs on other pests such as Helicoverpa spp.
In contrast to the Australian experience, Brazil has
had more success from releases of T. basalis. Corrêa-
Ferreira and Moscardi (1996) estimate that over 4 million
litres of chemical insecticides were used annually to
control stinkbugs on soybean, increasing production
costs and decreasing beneficial insects. Inundative
releases of T. basalis (15,000/ha) were made in soybean
trap crops, and the population density of N. viridula
consequently decreased by 54% in trap crops and 58% in
the main crop (Corrêa-Ferreira and Moscardi, 1996).
Parasitoid releases on early-maturing cultivars decreased
N. viridula population during the entire soybean season.
Releases of T. basalis into early maturing soybean
trap crops when N. viridula start colonising fields
may constitute an important tactic in soybean fields in
lieu of chemical insecticides, depending on whether
soybeans are grown for crushing or edible trade (Corrêa-
Ferreira and Moscardi, 1996).
Another parasitoid of N. viridula that has been released
and established in Australia is the Argentinean tachinid
T. giacomellii. Other Trichopoda species have been released
in West Australia but did not establish (Coombs and
Sands, 2000). T. giacomellii has established in the South
Burnett, Bundaberg, and the Darling Downs (Queensland)
and in northwest NSW near Moree but has also not yet
brought about successful biological control of N. viridula
although there have been reports of parasitism rates as high
as 50% (Coombs and Sands, 2000).
3.2.2. Conservation biological control
Conservation of natural enemies, whether native, natur-
alised or mass released is an important factor in biological
control (Gurr and Wratten, 1999). Adoption of within-field
monocultures of annual crops in modern farming systems
is known to discriminate against and reduce activity of
predatory insects (Gurr et al., 1998; Landis et al., 2000).
Many generalist predators including spiders, ants, frogs,
crickets, beetles, grasshoppers and predatory bugs prey
upon N. viridula and there are also important parasitoids
(Stam et al., 1987; Van den Berg et al., 1995). Natural
enemies in soybean have a variable but major impact on
young stages of N. viridula especially on the egg stage (Van
den Berg et al., 1995). Spraying during the R2–R6 growth
stages of soybean development with broad-spectrum
insecticides may cause a major reduction in predation
and, hence, will increase the dependency on insecticides to
control the pest (Van den Berg et al., 1995).
 ARTICLE IN PRESS
K.M.M. Knight, G.M. Gurr / Crop Protection 26 (2007) 1–10
Many parasitoids such as T. giacomellii require nectar in
order to survive. Fecundity and longevity of T. giacomellii
is reduced when only fed water (Coombs, 1997). Females
fed only water had significantly reduced ovarioles and were
unable to mature any eggs other than those that were
present in the abdomen at the time of emergence (Coombs,
1997). It is obvious then that the availability of adult food
(nectar and other sugar sources) has a significant influence
on the effectiveness of T. giacomellii as a biological control
agent. Thus after the flowering period of the host crop, the
parasitoid needs to forage further afield. In many cases this
may be in areas where there are no host insects, thus
decreasing the probability of T. giacomellii finding N.
viridula.
Equivalent work on the effects of food sources on adult
T. basalis is not well represented in the literature. Recent
laboratory studies show that adult female longevity is
increased several-fold by access to flowers of species such
as French marigold (Tagetes patula), basil (Ocimum
basilicum) and buckwheat (Fagopyrum esculentum) (Rahat
et al., 2005). Dependence of parasitoids on nectar suggests
that maintenance of food flowers may support conserva-
tion of those important natural enemies in farming
landscapes. Australian and many other nations’ farming
landscapes are characterised by homogenous planting,
frequent disruptions due to harvest and fallow cycles, and
lack of shelter from insecticides harmful to natural enemies
(Letourneau, 1998). These disturbances occur with greater
intensity and frequency in monocultures than in diverse
habitats. This means that monocultures favour those
species that can survive high levels of disturbance, which
are often pest species. The patterns of cropping, harvest,
and fallow remove the food sources and habitat for
alternate hosts of natural enemies thus decreasing the
impact that natural enemies can have on pests such as
N. viridula. Small areas left uncultivated, such as field
margins and wildlife corridors between large paddocks can
increase diversity in the landscape, giving natural enemies a
source of food, hosts and refuge throughout the year
(Letourneau, 1998). Many other examples of similar
strategies are reviewed by Landis et al. (2000) and Gurr
et al. (2004).
The crop plant’s life cycle to a large extent dictates the
nature of the pest habitat (Barbosa, 1998). Monocultures
of annual and perennial agroecosystem crop phenology
may cause asynchrony between resource availability and
natural enemy requirements. For instance, most soybeans
planted in northern Australia are determinate in growth
habit and flower over a short period of time. To conserve
natural enemies effectively, growers must ameliorate and/
or compensate for the elimination, reduction, or disruption
of needed resources and conditions that result from
patterns of cropping phenology in agroecosystems (Barbo-
sa, 1998). Natural habitats in the vicinity of croplands are
important in providing alternative foods and refugia for
natural enemy populations (Tscharntke et al, 2005). At
present, the loss and degradation of habitat creates serious
5
impediments to the conservation of natural enemies that
rely on resources not provided in modern agricultural
systems.
Increased vegetational diversity may theoretically: (1)
make crop plants more difficult for N. viridula to locate,
thereby reducing pest infestation, and (2) attract more
natural enemies resulting in better pest control (Buntin et
al., 1995). Though there is little published information
explicitly examining the effect of plant diversity on
N. viridula, it is known that the populations of herbivorous
arthropods only tend (149 species of 287) to be lower in
polycultures rather than monocultures (Andow, 1991).
Importantly, for polyphagous herbivores (such as N.
viridula) this effect was far weaker with only 28.4% of
such species exhibiting lowered densities in polycultures.
The most common response of such herbivores was an
increase in density (40.35% of species) (Andow, 1991).
Jones et al. (2001) showed that a diverse weed flora in
macadamia nut plantations was associated with higher
levels of damage, an effect assumed to be because of higher
N. viridula densities. This case illustrates the potential for
vegetational diversity to be counterproductive to pest
suppression and that rather than adopt a ‘shotgun’
approach to diversification there is a need for ‘directed’
approaches (Gurr et al., 2005), using plants that do not
favour the target pest, an approach dubbed ‘ecological
engineering’ (Gurr et al., 2004).
Nentwig et al. (1998) sowed weeds in strips to increase
biodiversity in agricultural fields and recommended
‘‘weed’’ strips cover at least 5–10% of cropping areas.
Ecological engineering dictates that these species should
undergo prior testing to determine their effects on pests
and natural enemies. While manipulation of wild vegeta-
tion may be practical in small crops areas, it remains to be
determined whether such a method would be accepted on
broadacre farms; though the widespread adoption in
western European cereal farms of a similar habitat method,
‘beetle banks’ (MacLeod et al., 2005), suggests significant
scope. Contamination of seed would be a potential
problem in crops such as edible soybean and mungbeans
but this could be minimised by confining weeds to a
discrete area or by allowing the presence only of species
with small seeds that are readily screened from harvested
beans.
3.2.3. Biopesticides
Populations of N. viridula are naturally infected by
entomopathogenic fungi, especially Metarhizium anisopliae
(Metschnikoff) Sorokin and Beauveria bassiana (Balsamo)
Vuillemin (Sosa-Gómez and Moscardi, 1998). While
natural infections are typically low in incidence, these
fungi can be used as biopesticides. Because N. viridula is a
sucking pest and feeds by penetrating the plant, and
entomopathogenic fungi infect through contact, these
fungi have greater potential as biopesticides for sucking
pests than do bacteria, viruses, and protozoans which
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6 K.M.M. Knight, G.M. Gurr / Crop Protection 26 (2007) 1–10
must be ingested to infect the host (Sosa-Gómez and
Moscardi, 1998).
Time to death is a critical factor where N. viridula
are present in low tolerance crops such as mungbeans
and edible soybeans or where high pest densities are
present. Work in Brazil found that M. anisopliae takes
approximately 14 days to kill adult N. viridula, with
infection incidence in the pest population increasing for up
to 20 days after treatment (Sosa-Gómez and Moscardi,
1998). This may prevent the use of biopesticides in such
crops if the insect keeps feeding and reproducing once
infected. The use of oil formulations in biopesticides
decreases the influence of abiotic conditions on the success
rate of infection of fungal pathogens in insects, thus
increasing the possibility that a mycopesticide based on this
formulation being successful against N. viridula in soy-
beans. This is an attractive prospect because a major
advantage of microbial control over use of conventional
insecticides is minimisation of adverse effects on natural
enemies.
Stinkbugs are naturally resistant to fungal infection by
both of these fungi because aldehydes, that are part of the
stinkbug’s defence secretions, serve as antimycotic agents
against certain entomopathogenic fungi (Sosa-Gómez et
al., 1997). The use of these entomopathogenic fungi might
be enhanced if nymphs are targeted (Sosa-Gómez and
Moscardi, 1998) and recent Australian research suggests
that nymphs rapidly succumb to infection (Knight and
Hauxwell, unpublished).
3.2.4. Conservation biological control to enhance
entomopathogens
As with other natural enemies of pests, entomopatho-
gens can be enhanced through conservation biological
control measures (Fuxa, 1998). This is a tractable
option because most entomopathogens are greatly influ-
enced by their environment and attractive because it
is potentially cheaper. The life cycle of entomopathogens
is generally weakest during transfer from one host
to another. Neither M. anisopliae nor B. bassiana are
transovarially transmitted thus the pathogen must
survive adverse environmental conditions, be transported
from the old host to the new, and penetrate the defenses of
the new host.
If a pathogen is naturally occurring in an agroecosystem,
a slight change in cultural practices could potentially
enhance survival or transmission to the new host (Fuxa,
1998). There are several areas that environmental manip-
ulation could aid the survival and enhancement of
naturally occurring populations of fungal pathogens. First,
improved transport from the pathogen reservoir, usually
soil or cadavers, to a site where the entomopathogen can
come into contact with the insect host. Second, improved
persistence of the pathogen at the site where it contacts the
host insect may also be required because sunlight, low
moisture, or chemical pesticides damage many entomo-
pathogens. Third, ensuring factors are present in order to
promote growth of the entomopathogen population, such
as high relative humidity that promotes the production of
fungal conidia (Fuxa, 1998).
Populations of the fungi M. anisopliae and B. bassiana
are more prevalent in no till than in tilled plots in a
soybean–wheat double cropping system (Sosa-Gómez and
Moscardi, 1994). This may be due to the retention of
sporulating cadavers above the soil which are otherwise
buried by tilling. In no till, the surface temperature
amplitudes are not as great as they are in tilled soil. Other
factors such as the soil’s capacity to retain water, higher
organic matter, and lower temperature of soils under
minimum tillage increase the survival of these entomo-
pathogenic fungi.
Other fungi have been promoted through the use of
irrigation. Such manipulation in soybean crops could
increase humidity and therefore enhance fungal activity.
Finally, the use of selective fungicides needs to be
evaluated, as Nomuraea rileyi (Farlow) is significantly
affected by the use of several fungicides in soybean crops
(Fuxa, 1998).
Environmental manipulation, as well as enhancing
naturally occurring populations of entomopathogens, can
increase the likelihood of outbreaks of fungi that are
released or applied as a biopesticide. Manipulation of crops
such as soybeans by, for instance, using narrower row
spacings creating canopy cover can raise relative humidity
and hence increase the likelihood of control once applied as
a biopesticide.
Environmental manipulation is more likely to succeed
against indirect pests than direct pests because most
entomopathogens act relatively slowly and will not prevent
damage to the part of a crop plant that is used directly by
humans (Fuxa, 1998). It is not, therefore, likely to be
adequate when used alone against N. viridula in crops such
as mungbeans and soybeans. However, such manipulation
would be warranted to increase the likelihood of naturally
occurring outbreaks and enhance applications of biopesti-
cides as part of an IPM strategy. Current research suggests
that some isolates may be faster acting and can be targeted
at nymphs pre-flowering to avoid significant damage
(Knight and Hauxwell, unpublished).
Natural enemies can aid in the local dispersal of
pathogens. The presence of a foraging adult coccinellid
coming into contact with a pathogen can result in a
substantial increase in the local transmission of the
aphid pathogen Erynia neoaphidis within a population
of pea aphids, Acyrthosiphon pisum (Roy and Pell, 2000).
The ability of natural enemies to vector pathogens
between infected and uninfected host populations
could be manipulated for IPM if the vector can be
artificially contaminated with inoculum (Roy and Pell,
2000). Furthermore, beneficial insects other than natural
enemies may provide an alternative means of pathogen
dissemination, for instance, the use of honey bees to
effectively vector M. anisopliae to pollen beetles (Roy and
Pell, 2000).
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K.M.M. Knight, G.M. Gurr / Crop Protection 26 (2007) 1–10
3.3. Trap crops
Trap crops are used either to prevent the pest from
reaching the crop or to concentrate it in a certain part of
the field where it can be economically destroyed mechani-
cally or by strategic pesticide use. Thus, trap crops are
advantageous because they delay the development of
pesticide resistance, are economical, and minimise adverse
impact on natural enemies, and pollution.
The principle of trap crops is that virtually all pests show
a distinct preference to certain plant species, cultivars, or a
certain crop stage (Newsom and Herzog, 1977). Though
the work of Velasco and Walter (1992) suggested
no difference between plant species in attractiveness to
N. viridula, adults of this species are known to be strongly
attracted to podding soybeans in preference to plants in
earlier stages of development so are attracted to plantings
of earlier maturing soybean cultivars (Todd and Schu-
mann, 1988). McPherson and Newsom (1984) reported
70–85% of all N. viridula in a soybean crop were attracted
to trap crop strips covering only 1–10% of the total crop
area. Early in the season there were 0.1 N. viridula per
metre in the trap crop and 0.03 N. viridula per metre in the
main crop. At the end of the season N. viridula numbers
were 1.1 per metre and 0.12 per metre in the trap crop and
main crop, respectively (McPherson and Newsom, 1984).
Similarly successful work was reported by Newsom and
Herzog (1977).
As trap crops can also act as a source of pest populations
they must be selected and managed in such a way as to
minimise the risk of increasing the pest problem. Trap
crops are effective only if N. viridula are controlled in the
trap crop to prevent them spreading into adjacent or main
crops (McPherson and Newsom, 1984). Adult N. viridula
will quickly move out of trap crops into adjacent crops if
they are at a more attractive stage (e.g. early pod-fill in
soybeans) or once the trap crop becomes unattractive (e.g.
during dry down prior to harvest). Regular scouting of trap
crops is essential to ascertain population numbers and
insect life stage to determine when control is necessary.
Chemical control of early instar N. viridula in trap crops
will prevent movement into main crop (McPherson and
Newsom, 1984). Todd and Schumann (1988) reinforce this
argument stating that control measures should be applied
to trap crops before the main crop reaches late podset (R4,
when most oviposition occurs) and before fifth instar
nymphs moult to the adult stage.
Bundy and McPherson (2000) found that when
planted in close proximity, pentatomids show a preference
for soybean and led them to propose that there should
be a large-scale evaluation of soybean as a trap crop
for managing stink bugs in cotton. Soybean trap
crops adjacent to a cotton crop were studied in
the South Burnett region of Australia in 2000–2001
(P Enkleman, 2001, pers. com.,). Results suggest that
small areas of soybean trap crop contain N. viridula for the
whole season indicating that soybean is a far more
7
attractive host than cotton (Khan and Bauer, 2001,
unpublished data).
Trap crops not only have potential for the effective
control of N. viridula in soybean and cotton fields.
A border planting of white mustard (Sinapsis albus) was
used as a trap crop with organic sweet corn in New
Zealand (Rea et al., 2002). The mustard flowered around
three to 4 weeks earlier than the sweet corn. N. viridula
numbers were much higher in the mustard plots (8–12/m2)
than in the sweet corn (o1/m2). As with soybean crops, the
timing of planting the trap crop is crucial. The trap crop
must be more attractive to the pest at a time when pest
damage can be detrimental to the main crop.
Trap crops are a potentially useful tactic in any IPM
program. However, on a regional basis, farmers tend to
stagger crop plantings. Thus, the fields planted earliest
become natural traps attracting the early flux of insects
(Kogan and Turnipseed, 1987). Regional IPM systems
need to be put into practice to alleviate the occurrence of
these natural traps. Although the above results for trap
crops in soybean and cotton systems look promising there
are drawbacks such as the opportunity cost of sacrificing
between 1% and 10% of land area to trap crops. The
viability of trap crops in other systems such as mungbeans
remains to be investigated and in that case there are no
early maturing varieties of mungbean available so alter-
native trap crop species need to be identified.
4. Integrated pest management
In this review we have presented components that can be
utilised to create an IPM system for N. viridula. Kogan
(1988) states that IPM has three levels: (i) integration of
methods for the control of a single species (population
control), (ii) integration of impacts of multiple pest
categories (insects, weeds, and pathogens) and the methods
for their control (community level control), and (iii)
integration of multiple pest impacts and the methods for
their control within the context of the total cropping
system (ecosystem level control). This begs the question:
what IPM strategies are currently being used to control N.
viridula and at what level of IPM are they functioning?
Coombs (2000) manipulated ground cover in a pecan
farming system that resulted in increased control of
N. viridula while enhancing the action of natural enemies.
This is an example of level one IPM strategy. In contrast,
McPherson et al. (2003) examined whether herbicide
tolerant soybean varieties were less attractive to N. viridula
due to less weedy crops. However, they found that the only
difference in pest numbers was due to soybean maturity
groups. Although the herbicide tolerant varieties did not
have decreased numbers of N. viridula this study was
extending to the second level of IPM as it investigated
control at a community level.
The early soybean production system (ESPS) in the mid-
south of the USA allows growers to escape high popula-
tions of late season defoliators and late season drought
 ARTICLE IN PRESS
8 K.M.M. Knight, G.M. Gurr / Crop Protection 26 (2007) 1–10
stress (Baur et al., 2000; McPherson et al., 2001). The early
season soybeans act as a trap crop for all the remaining
soybeans in the area. Stink bugs (including N. viridula)
colonise the ESPS several weeks before the conventional
crop begins to bloom. The potential benefits of this trap
crop effect are lost, however, if the pest population is left
untreated and the stink bugs move out of the senescing
early maturing soybeans to adjacent later maturing
soybeans where they continue to increase (McPherson et
al., 2001). Baur et al. (2000) state that although yields have
increased in ESPS, the cost of insect control is comparable
to conventional crops because of consistent stink bug
pressure in ESPS. Although the ESPS attempts to use
earlier maturing cultivars to enhance the IPM system
for defoliators it is unfortunately acting as a sink for
N. viridula for later planted varieties. Often when attempt-
ing to solve the problem of one group of pests we are still
faced with another pest that needs to be controlled. One
possibility that may improve this system is an area wide
management group that worked together to ensure that the
soybeans in an area were all planted at a similar time.
Integrated soybean pest management has been imple-
mented in micro-river basins in Brazil (Corrêa-Ferreira et
al., 2000). This soybean IPM system was developed in
large, continuous river basin areas and involved: (i) pest
monitoring, (ii) management decisions based on estab-
lished economic injury levels, (iii) use of highly selective
products for Anticarsia gemmatalis (Hübner) to preserve
the whole natural enemy complex, (iv) mass releases of
T. basalis and (v) insecticidal applications on field borders
or at reduced doses mixed with cooking salt to control the
stink bug complex including N. viridula wherever necessary
(Corrêa-Ferreira et al., 2000). This integrated soybean pest
management system resulted in a reduction of insecticide
applications for stink bug control from a mean of 0.81 to
0.09 applications per season after only two seasons
(Corrêa-Ferreira et al., 2000).
5. Conclusion
We propose that an effective management program for
N. viridula should use a variety of preventive and
therapeutic methods. In the case of soybeans, an IPM
program may include trap crops, strip cropping of weeds or
another crop such as lucerne as a source of nectar and
shelter for parasitoids and predators, inundative biological
control, biopesticides, and discriminate use of synthetic
insecticides. Such an IPM strategy would reduce N. viridula
numbers throughout the season to keep populations below
economic thresholds and hence decrease dependence on
broad-spectrum insecticides. A regime may include the
following components.
 Trap crops that are monitored throughout the season
and sprayed with chemical or biological insecticides (as
they become more available) whenever the majority of
the N. viridula population is younger than fifth instar.
Because the sprayed area is only a trap crop, costs are
minimised. Trap crops could also be mechanically
destroyed, killing the pest whilst still at a nymphal stage
though the area of trap crops, as well as optimal species,
needs to be investigated.
 Area-wide management similar to that undertaken for
Helicoverpa spp. in the Darling Downs region of
Queensland Duffield (2004) so that growers do not
create pest sources as in the ESPS (McPherson et al.,
2001) that exacerbate damage at the regional scale.
Growers that participate in area wide management
groups are encouraged to experiment on farm in order
to create strategies that suit individual farming systems
and regions. Area wide management of N. viridula will
make growers aware of the strategies that their
neighbours are using to control this pest by increasing
communication and consequently creating a unified
approach to IPM strategies for N. viridula in soybean
growing areas.
 Education for growers and consultants on therapeutic
measures such as scouting, sampling methods, thresh-
olds, decision making, and beneficial insect identifica-
tion.
 Ecological engineering using carefully selected floral
resources or refuges for beneficial insects. This will
require experimentation with crops such as lucerne, or
weed mixes for sown weed strips that are suitable for
different regions and soybean crops. Potentially, trap
crop species could constitute such refuges, so having
dual utility and using space efficiently.
 Releases of biological control agents such as Trissolcus
basalis, Pristhesancus plagipennis, and Trichopoda gia-
comellii, especially in trap crops and beneficial refuge
areas. If trap crops act also to provide resources to
attract natural enemies (or if such resources can be
provided by other plant species sown immediately
against trap crop species) pests would be attracted to
areas where natural enemy density is optimised, leading
to maximum pest mortality.
 Experimentation with cultural control methods such as
row spacing, no till, and reduced herbicide regimes that
may decrease the crop’s attractiveness to N. viridula or
increase beneficial insect populations and naturally
occurring entomopathogens.
 Monitoring of main crops; plant health, pest numbers,
and beneficial numbers.
 Spraying main crop with synthetic insecticides only
when absolutely necessary.
IPM in general is an important tool in making a farming
system sustainable but current control of N. viridula relies
heavily on broad-spectrum insecticides that are detrimental
to natural enemy species and, indirectly, to IPM of other
pests such as Helicoverpa armigera (Hubner). This review
has illustrated that the non-chemical options available for
use against this serious pest have significant potential but
their widespread use, especially in broadacre crops, is
 ARTICLE IN PRESS
K.M.M. Knight, G.M. Gurr / Crop Protection 26 (2007) 1–10
constrained. The priorities for further research identified in
this review, including the development (and registration) of
narrow-spectrum insecticides, need to be addressed for
IPM based on natural enemies to realise its potential.
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