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Biology and Management of Stink bugs in Southern African Macadamia
Orchards-Current Knowledge and Recommendations
Working Paper · August 2016
DOI: 10.13140/RG.2.2.36497.12644
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University of South Africa
Agricultural Research Council, South Africa
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S A M AC S T I N K BUG
FA C T S H E E T 1
8 A U G U S T 2 016
Biology and Management of Stink bugs in Southern
African Macadamia Orchards - Current Knowledge
and Recommendations
Compiled by Scalk Schoeman (ARC-ITSC)
and Gerhard Nortjé (Subtrop)
CONTENT
•
•
•
•
•
•
•
•
•
•
Introduction and economic importance.
Seasonal occurrence of stinkbugs in macadamia orchards.
Migration patterns and spatial distribution of bugs in
macadamia orchards.
Cultivar susceptibility.
Overwintering behaviour.
Monitoring and scouting.
Chemical communication.
Management strategies.
Recommendations for an IPM management approach.
Way forward.
For more information, call SUBTROP at 015 307 3676, or the ARC (Nelspruit)
at 013 753 7000.
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Worldwide stink bugs became troublesome after
The stink bug working group was
formed in 2009 and since then
valuable scientific information
has become available. The aim
of this publication is to convey a
summary of the most important
findings regarding aspects of the
biology and control of stink bugs
for macadamia growers.
Macadamias were first planted in
South Africa during the 1960’s.
The macadamia industry has
undergone near exponential
growth during the past 25 years
and South Africa is currently the
biggest producer of macadamia
nuts globally.
The coconut bug was recorded for
the first time on subtropical crops
during 1977.
D
COCONUT BUG
certain broad spectrum contact insecticides with long residual
actions were withdrawn. Their relatively long life cycles and low
population numbers linked with their cryptic behaviour has ensured that comparatively little information regarding stinkbugs is
available in scientific literature
uration of development stages of the two spotted and
coconut bugs under controlled temperature regimes
The two spotted bug was first
identified on macadamias in the
Levubu district in August 1984.
Estimated stink bug damage
affecting the macadamia industry
= R400 million during 2015/16
(excluding NIS exports).
BIOLOGY
Life cycle
• Stink bugs undergo an incomplete
metamorphosis which means that
instead of larval and pupal stages, five
nymph stages are present.
• Nymphs are normally wingless
(wing nodules may be present on
the 4th and 5th instars) and the
coloration of these stages are normally
significantly different from that of the
adult stage.
Egg
2nd Stage
3rd Stage
4th Stage
5th Stage
Adult
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Egg 6.85
days
at 25°C
1st Stage
6.75 days
at 25°C
5th Stage
8.3 days
at 25°C
Egg
4th Stage
6.00 days
at 25°C
1st Stage
3rd Stage
7.38 days
at 25°C
2nd Stage
8.3 days
at 25°C
2nd Stage
Adult
3rd Stage
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4th Stage
5th Stage
TWO-SPOTTED STINK BUG
Egg - Adult
6.75 days
at 25°C
• The two spotted bug lays on average 4.2 egg masses (± 59 eggs) during
its lifetime. This is probably a vast underestimation and it is expected that a
female produces significantly more eggs.
• The coconut bug lays on average 80.9 single eggs during her lifetime.
• First stage nymphs cluster on the empty egg casings and presumably ingest
symbionts during this time. This appears to be critical for the long term
survival of the insects, because if they are disturbed during this stage, their
life expectancy is significantly compromised.
• Eggs can be found all over the trees but two spotted bugs prefer to deposit
eggs on the lower extremes of mature macadamia trees. Due to the difficulty
in locating single eggs of the coconut bug in macadamia trees, no specific
oviposition site for this species has been quantified.
Seasonal occurrence of stinkbugs in
macadamia orchards
• 35 stink bug species from 5 different
families have so far been recorded on
macadamias in South Africa.
• The two spotted bug (Bathycoelia
distincta) is by far the most dominant
species when macadamia nuts are
available and represented ± 78% of
all species that were recovered.
• Yes, stink bugs can penetrate hard
macadamia shells during this period
with ease!
• Although this dominance extends
throughout all development stages
of macadamia nuts, B. distincta is
particularly numerous during the
late season after the shell has hardened
(mid-January – June)
• Lesser important stink bugs (green
vegetable, yellow edged and the small
green stink bugs) are more dominant
during the cooler months of the
year when fewer nuts are available.
Mouthparts of these bugs are shorter
than that of the two spotted bug
(approximately 50% of its length)
but thinner shelled cultivars are still
susceptible to damage. Do not spray
for bugs if the crop has already been
harvested and lots of bugs with short
mouthparts are present. They will
move out of the orchards on their
own and pose no danger to the new
crop.
• The coconut bug (Pseudotheraptus
wayi) is more predominant in
macadamias from February – May.
• Only nymphs of P. wayi, B. distincta
and Pseudatelus raptorius have been
recovered in macadamia orchards
indicating that all other bugs possibly
only use macadamias as a temporary
overwintering refuge.
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Migration patterns and spatial distribution
of bugs in macadamia orchards
• When stink bugs move into an empty niche (uninfested orchard), they normally
settle along the edge of an orchard where they mate, lay eggs and feed. If not
disturbed at this stage, a second wave of stink bug infestation will move deeper
into the orchard once nymphs have matured.
• This edge effect is well documented and in macadamias it has been found to
extend ±5 rows into the orchard from the perimeter. Researchers in other parts of
the world mention an edge effect of ± 20 m.
• In tall overgrown trees, the majority of bug damage occurs in the dense inner
part of the orchard. It has been proven that these insects prefer dense, overgrown
dark orchards. This is presumably a parasitoid/predator avoidance strategy.
• Clearly the two extremes of canopy density management (open trees where
sunlight penetrates through to the orchard floor versus dense overcrowded
orchards) affect the dispersal of the bug populations in two very different ways.
Bug dispersal
-
Open trees
well
managed canopy
Majority of the bugs occur
inside the orchards and cannot
be chemically controlled due to
physical limitations of spray rigs.
Very few bugs occur along the
perimeters of the orchard.
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Overgrown orchard
Majority of the bugs occur along
the perimeter of the orchards.
Chemical control and spray
coverage of trees is optimal.
Dispersal of bugs into the centre of
the orchard is relatively slow.
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•
•
•
Stink bugs are fussy feeders and any movement of these insects between
natural host plants and commercial orchards will be influenced by the
presence/absence of food in the desired stage of development.
Limited immigration of stink bugs has been observed during the first part of
the production season. However, during the second part of the production
season immigration into the orchard can be significant.
Stink bugs prefer to feed in the upper portions of the trees. The difference
between nut damage in the upper and lower extremes of trees can be
considerable (damage in the upper parts – 57%; damage in the lower parts of
the same trees 10.4%)
Cultivar susceptibility
•
•
Due to the long mouthparts of the two spotted bug, no cultivar is really
resistant to stink bug feeding. When cv. Beaumont is planted in the same
orchard along with other cultivars (when bugs are presented with a choice),
damage in Beaumont tends to be reduced. Pure stands of Beaumont trees
where the bugs did not have a choice, had high damage levels under unsprayed
or poorly sprayed conditions.
Thicker shelled cultivars did not consistently have lower damage levels when
compared to thinner shelled cultivars.
Overwintering behaviour
• Quantifying the behaviour of these
insects during winter is regarded
as one of the keys for sustainable
management.
• Two spotted bugs change colour
from light green to russet during
winter - a process known as seasonal
polyphenism which indicates that they
are entering a state of quiescence or
diapause.
• Normally large numbers of nymphs
are found in macadamias as late in
the season as June. Numbers decrease
sharply hereafter and up to October/
November only adults are normally
present in the orchards.
• Warmer winters are associated
with the presence of small numbers of
nymphs during the early summer.
• The fate of the large number of
nymphs after June is unknown but two
possibilities exist namely: a) they die
due to the cold winter and some may
survive during milder winters or b)
they go into a state of hibernation and
hide in inaccessible places in winter.
• It is well known that other stink
bugs such as Pseudatelus raptorius
overwinter underneath loose bark.
Hibernaculums constructed of hessian
sacking effectively lured bugs in pecan
orchards in the Nelspruit district.
Similar traps in macadamia orchards
could significantly reduce stink bug
pressure before the start of the new
season and this is currently one of the
research priorities for the stink bug
working group.
Monitoring and scouting
• Aspects of monitoring and scouting are highlighted in a scouting booklet and
DVD series available from Subtrop.
• Edges of the orchards (especially areas adjoining natural bush consisting of
broad leafed trees) should be monitored especially from late December onwards
as this is where the bugs will initially aggregate.
• From December onwards when premature nut drop comes to an end,
moderately damaged nuts do not always abort. Stink bug damage during this
time should therefore be regarded as additive. Low stink bug populations over a
long time could therefore theoretically damage nuts to the same extent as a high
population over a shorter period of time.
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Management strategies
Host plants
• The coconut bug has a very wide host range and it has been recorded on
avocado, guava, litchi, loquat, macadamia, mango, cashew, coconut and pecan.
Elsewhere it has also been recorded on cinnamon, cocoa and various leguminous
crops.
• Low numbers of the two spotted bugs have been found on mango, avocado,
litchi as well as the Kei apple Dovyalis caffra.
• Stink bugs use trees for two reasons namely hiding/overwintering and as a food
source. It is therefore no surprise that dense compact trees such as litchis yielded
by far the most stink bugs. Comparatively large numbers of other indigenous
stink bugs are also generally recorded on various host plants with mature seed.
Chemical communication
• Insects secrete certain chemicals
for mate location and may also use
chemicals secreted by macadamia trees
to locate an ideal food source.
• This sense of smell of stink bugs is
extremely well developed as they can
differentiate between trees and will
only feed on nuts in the desired stage
of development.
• Evidence also indicates that mate
finding may be more complicated
than previously imagined. Stink bugs
do stridulate (sing) and the behaviour
of bugs in the trees is affected when a
recorded stridulation is played back to
them.
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Cultural management
• Reducing tree height and density is one the most important cultural practices
as recent research in avocado orchards indicates that even moderate pruning has a
significant regulating effect on stink bug populations.
• The two spotted bug clearly prefers fully developed nuts after shell hardening
therefore, the longer the nuts hang on the tree the higher the risk of damage. It is
imperative that nuts are harvested as soon as they are physiologically mature.
• Robinson light traps have been tested with various light sources but did not
lure sufficient stink bugs for reliable population estimates.
Chemical control
• Stink bugs also secrete a number of
smelly compounds to warn off possible
predators/parasitoids. They are after all
not called stink bugs for nothing.
• Selecting between all these smells is
not an easy task and to make things
even more complicated, it is very
likely that more than one compound
in a specific ratio relative to the other
compounds may be involved in both
mate or host plant location.
• It is highly unlikely that macadamias will ever be produced in South Africa
without the use of pesticides.
• Although not conclusively proven, synthetic pyrethroids used for stink bug
control is under pressure and the development of resistance is suspected.
• Of the 39 products currently registered for stink bug control, only 5 belong to
alternative (non-pyrethroid) IRAC groups.
• It is believed that resistance is related to poor spray coverage in the tops of
mature trees (preferred habitat for stink bugs). Most sprayers have a vertical
operational limit of 5 - 6m. Tower sprayers can extend this limit somewhat but
are ideally more suited for flat orchards.
• This process is further exacerbated by the recent rapid development of the
macadamia industry. Large monocultures were planted at the same time and have
now simultaneously reached a point where they have grown too big and dense for
effective spraying.
• Worldwide, mostly three groups of pesticides are registered against stink bugs
namely: synthetic pyrethroids, organophosphates and neo nicotinoids. These
products are effective due to their indiscriminate modes of action and relatively
long residual effects.
• The use of some neo nicotinoids (clothianidin, thiamethoxam and
imidachloprid) was provisionally banned in the EU up to December 2015. The
main reason for this was concern regarding the effect of these products on bees.
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The ban in the EU was extended beyond 2015 and these type of products are also
under pressure in the USA and Canada.
• Due to environmental pressure no, or very few, proprietary products with
indiscriminate modes of actions and long acting residue profiles will ever be
considered for development by various agrochemical companies. Few novel
products are therefore in the pipeline for registration in South Africa. It is thus
imperative that the current products be protected by strictly adhering to directions
of usage as stipulated by the various chemical companies as well as Act No. 36 of
1947.
• New pesticides are generally more target specific, have shorter residual actions
and will probably be more expensive. The take home message here is that the use
of these products will require more intensive knowledge regarding the biology and
susceptible life stages of the target pest(s).
• Degree day models are a basic requirement of any Integrated Management
Program (IPM) and are widely used by growers in many parts of the world (http://
ipm.ucanr.edu/WEATHER/index.html).
• A degree day model will only work if spray coverage in the trees is adequate. If
overwintering bug populations are not eradicated after flowering due to tall and
overgrown trees, economic damage will ensue.
• A degree day model cannot function without regular and effective scouting.
Spray decisions should firstly be based on scouting but should also take cognisance
of the degree day model and date of previous spray application. The degree day
model can be used with the assistance of Dr Schalk Schoeman and the Subtrop
technical advisors.
• Use and spray only registered chemicals – lists are supplied by Subtrop and are
updated on an annual basis.
• (http://www.samac.org.za/index.php/technical-info/food-safety-registeredchemicals-mrls,)
Main group and
primary site of action
Acetylcholinesterase
(AChE) inhibitors
Sodium channel
modulators
Chemical subgroup
or exemplifying active
ingredient
1A
Carbamates
Methomyl *
1B Organophosphates
Acephate, chlorpyrifos,
Dichlorvos &
Trichlorfon**
3A Pyrethroids
Alpha-cypermethrin,
Beta-cyfluthrin,
Beta-cypermethrin,
Cypermethrin.
Gamma-cyhalotjhrin,
Lambda-cyhalothrin,
Tau-fluvalinate & Zetacypermethrin
Clothianadin**
Imidachloprid***
Thiamethoxam
Nicotinic acetylcholine 4A
receptor (n AChR)
Neonicotinoids
competitive modulators
Chordotonal organ
TRPV channel
modulators
Active ingredient
4C Sulfoxamines
9B Pyridine azomethine
derivatives
Sulfoxaflor**
Pymetrozine
* Not registered against stinkbugs in South Africa but registered against this group of pests
in other countries
** Products undergoing evaluation and registration in SA is pending
*** Registered on macadamias in South Africa but not against stinkbugs
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Biological control
• Natural enemies consist mostly of a
group of tiny egg parasitoids belonging
to the wasp Order (Hymenoptera)
as well as a group of parasitic flies
(Tachinidae) affecting adult stink bugs.
• The incidence of egg parasitoids
reaches a peak during February each
year. Parasitism of up to 86% of egg
packets have been recorded in the
past. Chemical usage during this
period should be done with extreme
circumspection as broad spectrum,
long acting pesticides could damage
this tenuous balance.
• Parasitic flies (Family Tachinidae)
may kill up to ± 58 % of adult twospotted bugs in an orchard where
no foliar sprays have been applied
(Bruwer 1992).
• Levels of mortality due to various
entomopathogens normally increase
towards the end of the production
season (May).
• It has been proven that some bats
feed on stink bugs and contribute to
the general levels of biological control.
• Ants have also been observed in close
association with egg packets of the
two spotted bug. This relationship is
currently being studied and findings
will be released as soon as they become
available.
Recommendations for an IPM management approach
• True IPM has not yet been achieved in macadamias. The current insect
management programme is more an integrated pesticide management programme
but it is an important step in the right direction.
• Large dense trees make effective spraying impossible and this situation should
be rectified as soon as possible.
• In Nelspruit where an overgrown orchard was pruned, stink bug damage was
reduced from 11.43% to 1.96%. This was achieved with fewer spray applications
than the preceding year (Unpublished results 2016).
• Chemical control should only be used if pest levels warrant control (scouting)
and not as a form of insurance.
• Insect pathogens should form a bigger part of the crop protection scenario.
Goggas.indd 14-15
• Mating disruption, insect pathogens as well as the inundated releases of beneficial
insects are available for other pests in macadamia and should be used instead of
long acting disruptive pesticides where possible.
• Where trees are pruned and where spray coverage is optimal, perimeter spraying
could be considered. If the risk of damage is deemed too big, the perimeter of an
orchard can be sprayed with a long acting product while the inside of the orchard
can be sprayed with a more environmentally sensitive product such as pymetrozine
or Beauveria bassiana.
• Conservation agriculture (http://www.fao.org/ag/ca/) should be considered and
could be used as a tool to increase the marketability of South African macadamia
nuts.
• Use the IRAC classification table (Table 1) and alternate between various
pesticide subgroups where possible.
• If resistance against synthetic pyrethroids is suspected, rather use one of the
alternative products. This will allow for the wild (susceptible) stink bug population
to interbreed with the resistant population and provided that enough time passes
without selection pressure (pyrethroid sprays), it may be possible to use these
products effectively again. Do not increase the rate of the product if resistance is
suspected.
• In younger macadamia trees, the registered systemic product could be considered
as it will have a negligible negative effect on the general orchard ecology. Care
should however be taken with this product as it could negatively affect bees. Do
not apply it during flowering or when flowering weeds are present and stick to
the label instructions regarding application rate, tree age and clay content of the
soil. As part of a resistance management strategy, it is important not to apply this
product year after year. It is suggested to rather use a foliar spray program every
second or third year. The withholding period of this product is long. In order to
avoid residues in the nuts it is imperative that this product be applied as close to
the end of flowering as possible.
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Way forward
T
he problems facing the macadamia industry regarding crop protection include
the following: poor spray coverage due to tall dense trees, insecticide resistance,
and continued immigration of bugs from the field, overuse of a limited group of
pesticides, and inappropriate crop protection techniques.
The SBWG is tackling the stink bug dilemma holistically and the following aspects
are currently receiving attention:
• A project studying the biology and
for various chemical companies via
behaviour of stink bugs.
SUBTROP.
• Chemical communication of the
• Studies on stink bug migration and
two-spotted and coconut bugs as well
aspects influencing migration and
as comparative host plant volatiles
subsequent dispersal.
secreted by various crops during
• Studies on the effect of bats on insect
susceptible and non-susceptible stages.
populations in macadamia orchards.
• Studies on entomopathogenic
• The effect of various ground covers
nematodes, viroids and fungi.
in terms of increased soil health as well
• PhD study on the genetic basis of
as other related ecosystem services such
possible pyrethroid resistance.
as increased parasitism and predation.
• Insect tracking, search for alternative
• Creation of a degree day model for
host plants as well the development
more precise application of pesticides.
work for an insect identification
• Mating disruption trials for moth
application for smartphones.
pests on macadamia.
• Pesticide registration trials and
applications for new registrations
References
1. Bruwer I. J. 1992. The influence of various Hemipteran species on macadamia and some factors
which can limit nut damage. Unpublished Ph.D. thesis, University of Stellenbosch. 184pp
2. Schoeman, P. S. 2011.Integrated management of macadamia pests with emphasis on alternative
pesticides and more effective monitoring. Yearbook of the South African Macadamia Growers
Association. 19: 26 - 32
3. Schoeman, P. S. 2013 Major findings of the stink bug monitoring program. Subtrop Quarterly
Journal 2: 36 – 38
4.
Schoeman, P. S. R. 2013. Stink bug management in macadamia: Practical recommendations and
solutions. Yearbook of the South African Macadamia Growers Association Vol 21 pp 22 – 26
5.
Schoeman, P. S. 2014a. Aspects affecting distribution and dispersal of the indigenous Heteroptera
complex (Heteroptera: Pentatomidae & Coreidae) in South African macadamia orchards. African
Entomology 22 (1): 191 – 196.
6.
Schoeman, P. S. 2014b. Stinkbug IPM on macadamias in South Africa: Current status and the road
ahead. Trends in Entomology10: 87 – 95.
7.
Schoeman, P. S. 2016. Influence of canopy height and density on Tortricidae moths affecting
macadamia in South Africa. African Entomology 24 (2): 1 – 5.
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