Field evaluation of strobilurins and a plant activator for the control of citrus black spot


Miles, A.K.; Willingham, S.L.; Cooke, A.W.

Australasian Plant Pathology 33(3): 371-378

2004


Black spot (caused by Guignardia citricarpa) is a major disease affecting the citrus industry in subtropical Queensland (Australia). A number of chemicals were tested for control of black spot, including the strobilurins (azoxystrobin, trifloxystrobin, pyraclostrobin and methoxycrylate); a plant activator (acibenzolar); copper-based fungicides (copper ammonium acetate, copper oxychloride, copper hydroxide plus ferric chloride, cuprous oxide); mancozeb; phosphorous acid; captan and iprodione. In all experiments, the strobilurins used alone, or incorporated with copper and mancozeb, were as effective, or better than, the industry standard of copper and mancozeb. Acibenzolar used alone significantly reduced the severity and incidence of black spot by up to 50% compared with the untreated control, but was not as effective as the industry standard fungicides. No significant differences in disease control were found between the four different copper types. Phosphorous acid and captan were ineffective, but iprodione was as effective as the industry standard fungicides. The strobilurins induced less rind damage than the industry standard products, and pyraclostrobin was less toxic to the predatory mite Amblyseius victoriensis than the industry standard products.

CSIRO
PUBLISHING
www.publish.csiro.au/journals/app
Australasian
Plant
Pathology,
2004,
33,
371-378
Field
evaluation
of
strobilurins
and
a
plant
activator
for
the
control
of
citrus
black
spot
A.
K
Miles
A
'
B
,
S.
L.
Willingham
A
and
A.
W
Cooke
A
A
Horticulture,
Department
of
Primary
Industries,
80
Meiers
Road,
Indooroopilly,
Qld
4068,
Australia.
B
Corresponding
author;
email:
andrew.miles@dpi.q1d.gov.au
Abstract.
Black
spot
(caused
by
Guignardia
citricarpa)
is
a
major
disease
affecting
the
citrus
industry
in
subtropical
Queensland.
A
number
of
chemicals
were
tested
for
control
of
black
spot,
including
the
strobilurins
(azoxystrobin,
trifloxystrobin,
pyraclostrobin
and
methoxycrylate);
a
plant
activator
(acibenzolar);
copper
-based
fungicides
(copper
ammonium
acetate,
copper
oxychloride,
copper
hydroxide
plus
ferric
chloride,
cuprous
oxide);
mancozeb;
phosphorous
acid;
captan
and
iprodione.
In
all
experiments,
the
strobilurins
used
alone,
or
incorporated
with
copper
and
mancozeb,
were
as
effective,
or
better
than,
the
industry
standard
of
copper
and
mancozeb.
Acibenzolar
used
alone
significantly
reduced
the
severity
and
incidence
of
black
spot
by
up
to
50%
compared
with
the
untreated
control,
but
was
not
as
effective
as
the
industry
standard
fungicides.
No
significant
differences
in
disease
control
were
found
between
the
four
different
copper
types.
Phosphorous
acid
and
captan
were
ineffective,
but
iprodione
was
as
effective
as
the
industry
standard
fungicides.
The
strobilurins
induced
less
rind
damage
than
the
industry
standard
products,
and
pyraclostrobin
was
less
toxic
to
the
predatory
mite
Amblyseius
victoriensis
than
the
industry
standard
products.
Additional
keywords:
induced resistance,
integrated
pest
management,
mandarin,
orange.
Introduction
Citrus
black
spot,
caused
by
the
fungus
Guignardia
citricarpa,
has
been
present
in
several
citrus
growing
regions
of
Australia
since
at
least
1895
(Benson
1895).
In
particular,
northern
areas
of
New
South
Wales
and
the
Central
Burnett
region
of
Queensland
are
known
to
have
black
spot.
Black
spot
is
an
economically
significant
disease
in
most
citrus
producing
countries
of
the
world
(Kiely
1948;
Wager
1952;
Calavan
1960;
McOnie
1964;
Korf
et
al.
2001).
Kiely
(1948)
and
McOnie
(1964)
accurately
describe
disease
symptoms
of
both
fruit
and
leaves.
Fruit
are
susceptible
to
infection
during
the
first
4-6
months
after
fruit
-set
(Calavan
1960;
Kotze
1981),
after
which
time
fruit
become
resistant
(Kotze
1981).
After
infection,
a
latent
period
occurs
before
symptoms
are
observed
(Wager
1952;
McOnie
1967;
Kotze
1981).
During
this
time,
the
fungus
remains
latent
as
a
mass
of
mycelium
beneath
the
fruit
cuticle
(Brodrick
and
Rabie
1970).
When
fruit
reach
full
maturity,
the
majority
of
latent
infections
develop
into
typical
black
spot
lesions
(Calavan
1960).
Control
of
black
spot
greatly
relies
on
preventative
fungicide
sprays
(Schutte
et
al.
1997),
with
copper
-based
products,
mancozeb
or
benomyl
(Garran
1996;
Schutte
et
al.
1997)
applied
during
the
period
of
fruit
susceptibility.
However,
use
of
these
products
has
been
found
to
cause
some
©
Australasian
Plant
Pathology
Society
2004
undesirable
side
effects.
Copper
can
be
toxic
to
soil
and
plants,
and
has
been
reported
to
cause
rind
stippling
and
darkening
of
pre-existing
blemishes
(Schutte
et
al.
1997;
Timmer
et
al.
1998;
Agostini
et
al.
2003).
The
fungicides
mancozeb
and
benomyl
are
highly
toxic
to
the
predatory
mite
Amblyseius
victoriensis,
an
important
species
of
the
integrated
pest
management
(IPM)
system
widely
used
in
citrus
for
control
of
brown
citrus
rust
mite
(Tegolophus
australis)
and
broad
mite
(Phyllocoptruta
oleivora)
(Smith
and
Papacek
1991).
Herbert
and
Grech
(1985)
have
also
reported
the
detection
of
benomyl
resistant
isolates
of
G.
citricarpa
in
South
Africa.
This
paper
reports
on
four
field
experiments
over
three
seasons
where
four
strobilurin
fungicides,
the
plant
activator
acibenzolar,
phosphorous
acid
and
other
fungicides
were
evaluated
for
the
control
of
citrus
black
spot.
The
strobilurin
group
of
commercial
fungicides
are
synthetic
analogues
of
naturally
occurring
fungitoxic
metabolites
produced
by
the
edible
mushroom
Stobilurus
tenacellus
(Godwin
et
al.
1992).
The
mode
of
action
of
these
chemicals
is
to
inhibit
respiration
of
fungal
mitochondria
(Becker
et
al.
1981).
The
result
is
a
severe
reduction
in
aerobic
energy
production
by
fungi
and
inhibition
of
growth
(Godwin
et
al.
1994).
Perhaps
the
greatest
advantages
of
the
strobilurin
fungicides
are
low
10.1071/AP04025
0815-3191/04/030371
372
Australasian
Plant
Pathology
A.
K.
Miles
et
al.
Table
1.
Product
names,
active
ingredients,
manufacturers
and
standard
rates
of
chemicals
used
in
citrus
black
spot
chemical
control
experiments
carried
out
in
Queensland
Product
Name
Active
ingredient
Manufacturer
Standard
rate
(x)
A
AgriFos
600
60%
phosphorus
acid
Agrichem
3.33
mL/L
Amistar
50%
azoxystrobin
Syngenta
0.40
g/L
Bion
50%
acibenzolar
Syngenta
0.05
g/L
Captan
WG
80%
captan
Crop
Care
1.25
g/L
Coppox
50%
copper
oxychloride
Melpat
2.00
g/L
DC
Tron
78.2%
petroleum
oil
Caltex
6.00
mL/L
Ferric
chloride
FeC1
3
.6H
2
0
Sigma
0.02
g/L
Flint
50%
trifloxystrobin
Bayer
0.07
g/L
HEC
5725
methoxycrylate
Bayer
1.60
mL/L
Headline
23.6%
pyraclostrobin
BASF
0.80
g/L
Kocide
40%
copper
hydroxide
Griffin
2.00
g/L
Liquicop
8%
copper
ammonium
acetate
Hygrotech
Oceania
5.00
mL/L
Mancozeb
DF
75%
mancozeb
Crop
Care
2.00
g/L
Norshield
40%
cuprous
oxide
Nipro
Products
2.00
mL/L
Rovral
Aquaflo
50%
iprodione
Bayer
1.00
mL/L
A
Rate
used
throughout
all
experiments
except
where
otherwise
specified
in
text
as
a
factor
of
'x'.
mammalian
toxicity
(Sauter
et
al.
1994)
and
low
toxicity
to
A.
victoriensis
used
in
citrus
IPM
(M.
Bernard,
unpublished
data).
It
should
be
noted
that
the
highly
specific
mode
of
action
of
the
strobilurins
increases
the
potential
for
resistant
pathogen
individuals
to
develop,
and
preventative
measures
need
to
be
taken.
Anti
-resistance
strategies
are
recommended
by
the
Fungicide
Resistance
Action
Committee
(FRAC)
to
reduce
the
possibility
of
resistance
developing,
and
include
such
rules as
limiting
strobilurin
applications
to
one
third
of
the
total
number
of
fungicide
applications.
Such
strategies
are
investigated
in
the
following
experiments.
The
plant
activator
acibenzolar
(Bion,
50%
a.i.
wettable
granule
formulation)
is
a
non
-fungicidal
compound
used
to
combat
plant
pathogens
by
inducing
the
host
plant's
natural
defence
mechanisms
(Tally
et
al.
1999).
This
chemical
is
a
functional
analogue
of
salicylic
acid
(SA),
shown
to
accumulate
in
plants
challenged
with
a
pathogen
(Friedrich
et
al.
1996).
Following
accumulation
of
SA,
plant
defence
genes
are
induced
(Lawton
et
al.
1996),
triggering
the
production
of
defence
compounds.
Phosphorous
acid
has
been
shown
to
have
a
number
of
modes
of
action
including
being
directly
fungistatic
(Grant
et
al.
1990),
as
a
plant
activator
(e.g.
enhancing
production
of
the
defence
compound
scoparone
in
some
citrus
varieties;
Afek
and
Sztejnberg
1989),
and
as
an
inhibitor
of
pathogen
defence
suppressors
(Grant
et
al.
1990).
Methods
The
products
described
in
Table
1
were
applied
in
field
experiments
on
commercial
citrus
orchards
in
Queensland,
Australia.
The
chemicals
were
applied
in
all
experiments
to
individual
trees
until
drip
-off
(-10-25
L
per
tree)
using
a
Hardi
hand-held
lance
fitted
with
dual
hollow
cone
nozzles
and
a
100
L
capacity
tank.
Experiment
1
A
commercial
citrus
orchard
near
Mundubbera,
Queensland
(25'36'S,
151'17'N),
known
to
have
high
black
spot
incidence,
was
selected
for
the
experiment
conducted
during
the
2000/2001
cropping
season.
Twenty
-year
-old
'Imperial'
mandarin
trees
on
'Troyer'
rootstock
were
treated
with
the
following
chemical
treatments,
each
with
a
total
of
three
sprays
per
treatment
[application
dates:
11
October
2000
(3/4
petal
fall),
20
November
2000,
3
January
2001]:
industry
standard
(1
x
Kocide,
2
x
mancozeb);
azoxystrobin
(3
x
Amistar);
methoxycrylate
(3
x
HEC
5725);
iprodione
+
mancozeb
(3
x
Rovral
Aquaflo
+
mancozeb);
trifloxystrobin
(3
x
Flint),
each
of
these
treatments
tank
mixed
with
acibenzolar
e.g.
azoxystrobin
+
acibenzolar
(3
x
Amistar
+
Bion),
acibenzolar
alone
(3
x
Bion)
and
an
untreated
control
(no
chemicals)
giving
a
total
of
12
treatments.
Experiment
2
A
commercial
citrus
orchard,
near
Gayndah,
Queensland
(25'38'S,
151'37'N)
was
selected
for
the
experiment
conducted
during
the
2000/2001
cropping
season.
Twenty
-year
-old
'Navel'
oranges
on
`Troyer'
rootstocks
were
treated
with
the
following
chemical
programs,
each
with
a
total
of
four
sprays
per
treatment
[application
dates:
20
September
2000
(3/4
petal
fall),
18
October
2000,
27
November
2000,
4
January
2001]:
untreated
control
(no
chemicals);
industry
standard
(2
x
Kocide
+
DC
Tron,
2
x
mancozeb);
acibenzolar
(4
x
Bion);
industry
standard
+
acibenzolar
(2
x
Kocide
+
DC
Tron
+
Bion,
2
x
mancozeb
+
Bion),
azoxystrobin
(4
x
Amistar);
azoxystrobin
+
acibenzolar
(4
x
Amistar
+
Bion);
copper
ammonium
acetate
(4
x
Liquicop);
copper
oxychloride
(4
x
Coppox);
copper
hyrdroxide
+
ferric
chloride
(4
x
Kocide
+
ferric
chloride)
and
cuprous
oxide
(4
x
Norshield).
Experiment
3
A
commercial
citrus
orchard,
near
Gayndah,
Queensland
(25'38'S,
151'37'N),
was
selected
for
the
experiment
conducted
over
the
2001/2002
cropping
season.
Twenty
-one
-year
-old
'Navel'
oranges
on
`Troyer'
rootstocks
were
treated
with
the
following
chemical
programs,
each
with
a
total
of
four
sprays
[application
dates
2-3
October
2001
(3/4
petal
fall),
31
October
to
1
November
2001,
29
November
2001,
2-3
January
2002]:
untreated
control
(no
chemicals);
industry
standard
Chemical
control
for
citrus
black
spot
(2
x
1
g/L
Kocide,
2
x
mancozeb);
azoxystrobin
[0.5
x
standard
rate]
(4
x
0.2
g/L
Amistar);
azoxystrobin
(4
x
Amistar);
azoxystrobin
[1.5
x
standard
rate]
(4
x
0.6
g/L
Amistar);
trifloxystrobin
[0.5
x
standard
rate]
(4
x
0.035
Flint);
trifloxystrobin
(4
x
Flint);
trifloxystrobin
[2
x
standard
rate]
(4
x
0.15
g/L
Flint);
azoxystrobin
[0.5
x
standard
rate]
anti
-resistance
(2
x
1
g/L
Kocide,
1
x
0.2
g/L
Amistar,
1
x
mancozeb);
azoxystrobin
anti
-resistance
(2
x
1
g/L
Kocide,
1
x
Amistar,
1
x
mancozeb);
trifloxystrobin
anti
-resistance
(2
x
1
g/L
Kocide,
1
x
Flint,
1
x
mancozeb);
trifloxystrobin
[2
x
standard
rate]
anti
-resistance
(2
x
1
g/L
Kocide,
1
x
0.15
g/L
Flint,
1
x
mancozeb).
Experiment
4
A
commercial
citrus
orchard,
near
Mundubbera,
Queensland
(25'36'S,
151'17'N),
was
selected
for
the
experiment
conducted
over
the
2002/2003
cropping
season.
Fifteen
-year
-old
'Nova'
mandarins
on
`Swingle'
rootstock
for
two
replicates
and
'Sweet
Orange'
rootstock
for
two
replicates
were
treated
with
the
following
chemical
programs,
each
with
a
total
of
four
sprays
(application
dates:
3-4
December
2002,
14
February
2002,
24 February
2003,
7
April
2003):
untreated
control
(no
chemicals);
industry
standard
(4
x
mancozeb);
azoxystrobin
[0.5
x
standard
rate]
anti
-resistance
(1
x
0.2
g/L
Amistar,
3
x
mancozeb);
azoxystrobin
anti
-resistance
(1
x
Amistar,
3
x
mancozeb);
pyraclostrobin
[0.5
x
standard
rate]
anti
-resistance
(1
x
0.4
g/L
Headline,
3
x
mancozeb);
pyraclostrobin
anti
-resistance
(1
x
Headline,
3
x
mancozeb);
pyraclostrobin
[0.5
x
standard
rate]
(4
x
0.4
g/L
Headline);
pyraclostrobin
(4
x
Headline);
pyraclostrobin
[1.5
x
standard
rate]
(4
x
1.2
g/L
Headline);
captan
(4
x
captan)
and
phosphorus
acid
(4
x
AgriFos
600).
All
treatments
received
two
extra
fungicide
treatments
[copper
oxychloride
(Coppox)
tank
mixed
with
zinc
sulphate
(100
g/L),
magnesium
sulphate
(100
g/L)
and
oil
(DC
Tron)
at
petal
fall
(3
October
2002);
and
mancozeb
4
weeks
after
the
first
spray
(8
November
2002)]
applied
commercially
using
an
oscillating
boom
prior
to
implementation
of
the
experimental
treatments.
Twenty-two
days
after
the
final
application
of
treatments
in
experiment
4,
the
number
of
A.
victoriensis
predatory
mites
on
ten
5
-leaf
whorls,
selected
from
random
positions
throughout
the
canopy
of
each
treatment
tree,
were
counted
in
the
field.
The
experimental
design
for
all
four
experiments
was
a
split
-plot
with
four
single
tree
replicates
per
treatment
as
whole
plots
split
for
fruit
position.
One
carton
of
mature
fruit
(-60
fruit)
from
each
of
the
eastern
and
western
sides
of
the
tree
were
randomly
selected
at
commercial
harvest
time
(experiment
1,
10
May
2001;
experiment
2,
9
May
2001;
experiment
3,
9
May
2002;
experiment
4,
13-14
May
2003),
degreened
(10
ppm
ethylene,
22°C,
24
h)
and
placed
at
22°C
for
up
to
3
weeks
before
black
spot
disease
severity
was
visually
assessed
(experiment
1,
3
June
2001;
experiment
2,
15
May
2001;
experiment
3,
4-5
June
2002;
experiment
4,
3-5
June
2003).
The
fruit
from
experiment
4
were
not
degreened.
Results
are
presented
as
incidence
(percentage
of
affected
fruit)
and
severity
[on
a
scale
of
1-4
for
experiment
1
and
2
(where
1
=
no
disease,
2
=
1-25%,
3
=
26-50%,
4
=
51-100%
of
the
fruit
surface
affected);
a
scale
of
1-5
for
experiment
3
(where
1
=
no
disease,
2
=
1-20%,
3
=
21-40%,
4
=
41-60%
and
5
=
61-100%
of
the
fruit
surface
affected),
and
a
visual
assessment
of
percentage
surface
area
affected
was
used
for
experiment
4
due
to
the
low
disease
pressure].
Rind
damage,
i.e.
any
form
of
physical
injury
to
the
fruit
rind
(wind
blemish,
insect
damage,
etc.),
was
measured
similarly
using
a
scale
of
1-4
(where
1
=
no
damage,
2
=
1-25%,
3
=
26-50%,
4
=
51-100%
of
the
fruit
surface
affected).
Statistical
analyses
Statistical
analyses
were
conducted
using
Genstat
5
(release
4.1)
data
analysis
software
(Lawes
Agricultural
Trust,
Rothamsted
Experimental
Station)
for
a
split
plot
design
with
whole
plots
split
for
fruit
position.
Arcsine
angular
transformations
were
made
on
incidence
Australasian
Plant
Pathology
373
(percentage)
data
and
square
root
transformations
were
made
on
severity
data.
However,
examination
of
residual
plots
indicated
transformations
did
not
show
improved
distribution
of
residuals
for
experiments
1,
2
and
3.
Hence,
untransformed
data
are
presented.
However
in
experiment
4,
transformed
and
back
-transformed
data
is
presented.
Pair
-wise
testing
between
means
was
done
using
the
least
significant
difference
(LSD)
procedure
at
P
=
0.05.
The
mean
numbers
of
predatory
mites
in
experiment
4
was
analysed
using
a
one-way
ANOVA
in
randomised
blocks.
A
square
root
transformation
was
performed
on
mean
mite
counts,
resulting
in
an
improved
distribution
of
residuals.
Hence,
transformed
and
back
-transformed
data
are
presented.
Results
Experiment
1
Each
fungicide
treatment
applied
in
experiment
1
significantly
reduced
the
severity
and
incidence
of
black
spot
compared
with
the
untreated control
(Table
2).
All
of
the
fungicides,
except
for
the
iprodione
+
mancozeb
+
acibenzolar
treatment,
provided
comparable control
to
the
current
industry
standard
fungicides.
The
acibenzolar
treatment
also
had
significantly
less
severe
(30%
reduction)
and
a
lower
incidence
(47%
reduction)
of
black
spot
compared
with
the
untreated
control
but not
the
industry
standard
treatment.
Tank
mixing
acibenzolar
with
the
fungicides
did
not
significantly
affect
disease
control,
except
for
increasing
the
severity
of
black
spot
when
mixed
with
the
iprodione
+
mancozeb
treatment
compared
with
the
industry
standard
treatment.
All
of
the
fungicide
treatments
caused
significantly
less
rind
damage
(severity
and
incidence)
compared
with
the
industry
standard
treatment
and
had
damage
levels
similar
to
the
untreated control
fruit.
The
severity
and
incidence
of
rind
damage
observed
on
the
acibenzolar
treated
fruit
was
similar
to
the
industry
standard
treated
fruit
but
significantly
greater
compared
with
the
untreated control
fruit.
Tank
mixing
acibenzolar
with
the
fungicides
did
not
significantly
affect
rind
damage,
except
for
an
observed
significant
increase
in
the
severity
and
incidence
when
mixed
with
the
industry
standard
treatment
(Table
2).
Experiment
2
All
of
the
fungicides
were
as
effective
as
the
current
industry
standard
fungicides
(Table
3).
Again,
the
acibenzolar
treatment
had
significantly
less
severe
(20%
reduction)
and
a
lower
incidence
(20%
reduction)
of
black
spot
compared
with
the
untreated control
but
it
was
not
as
effective
as
the
industry
standard
treatment.
Tank
mixing
acibenzolar
with
the
fungicides
did
not
affect
the
efficacy
of
the
fungicides
against
black
spot.
No
significant
differences
in
black
spot
control
were
observed
between
the
different
copper
types.
Azoxystrobin
(with
or
without
acibenzolar)
had
significantly
less
severe,
and
a
lower
incidence
of,
rind
damage
compared
with
the
industry
standard
treatment
and
all
of
the
different
copper
fungicide
types.
The
copper
374
Australasian
Plant
Pathology
A.
K.
Miles
et
al.
Table
2.
Effects
of
various
chemicals
in
experiment
1
on
citrus
black
spot
(caused
by
Guignardia
citricarpa)
and
rind
damage
of
`Imperial'
mandarin
fruit
harvested
during
the
2000/2001
season
Treatment
Citrus
black
spot
Severity
Incidence
(1-4)
(%)
Rind
damage
Severity
Incidence
(1-4)
(%)
Untreated
control
Industry
standard
B
Acibenzolar
(0.05
g/L)
Industry
standard
+
acibenzolar
(0.05
g/L)
Azoxystrobin
(0.4
g/L)
Azoxystrobin
(0.4
g/L)
+
acibenzolar
(0.05
g/L)
Methoxycrylate
(1.6
mL/L)
Methoxycrylate
(1.6
mL/L)
+
acibenzolar
(0.05
g/L)
Iprodione
(1
mL/L)
+
mancozeb
(2
g/L)
Iprodione
(1mL/L)
+
mancozeb
(2
g/L)
+
acibenzolar
(0.05
g/L)
Trifloxystrobin
(0.07
g/L)
Trifloxystrobin
(0.07
g/L)
+
acibenzolar
(0.05
g/L)
LSD
(P
=
0.05)
East
West
LSD
(P
=
0.05)
2.1
A
a
1.1
d
1.4
b
1.0
d
1.0
cd
1.1
bcd
1.0
cd
1.0
d
1.2
bcd
1.4
bc
1.1
bcd
1.1
cd
0.3
1.1
b
1.3
a
0.1
58.5
a
6.0
cd
31.2
b
1.4
d
2.8
d
7.7
cd
6.2
cd
0.9
d
9.1
cd
22.1
bc
5.8
cd
5.5
d
16.6
10.0
b
16.2
a
4.5
1.14
cde
1.32
b
1.38
b
1.42
a
1.20
cd
1.14
cde
1.09
e
1.07
e
1.10
e
1.11
de
1.22
c
1.12
de
0.10
1.19
1.19
13.3
cde
27.7
b
33.3
ab
38.4
a
19.0
c
15.3
cde
8.2
e
7.8
e
10.4
e
9.8
e
18.2
cd
12.1
cde
7.9
17.8
17.8
A
Mean
values
within
columns
followed
by
the
same
letter
are
not
significantly
different
at
P
=
0.05
(n
=
4).
B
Industry
standard
program
-single
application
of
copper
oxychloride
(Kocide
at
2
g/L)
+
Oil
(DC
Tron
at
6
mL/L)
followed
by
two
applications
of
mancozeb
(2
g/L)
+
Oil
(DC
Tron
at
6
mL/L).
Table
3.
Effects
of
various
chemicals
in
experiment
2
on
citrus
black
spot
(caused
by
Guignardia
citricarpa)
and
rind
damage
of
'Navel'
orange
fruit
harvested
during
the
2000/2001
season
Treatment
Citrus
black
spot
Severity
Incidence
(1-4)
(%)
Rind
damage
Severity
Incidence
(1-4)
(%)
Untreated
control
2.1
A
a
81.3
a
1.9
cd
75.1
ab
Industry
standard
B
1.1
c
11.9
c
1.9
bc
80.8
ab
Acibenzolar
(0.05
g/L)
1.7
b
63.3
b
1.7
cd
69.1
bc
Industry
standard
+
acibenzolar
(0.05
g/L)
1.1
c
15.8
c
1.9
bc
79.3
ab
Azoxystrobin
(0.4
g/)
1.3
c
28.1
c
1.6
d
57.2
c
Azoxystrobin
(0.4
g/L)
+
acibenzolar
(0.05
g/L)
1.2
c
15.9
c
1.6
d
61.1
c
Copper
ammonium
acetate
(5
mL/L)
1.2
c
20.4
c
1.9
bc
78.0
ab
Copper
oxychloride
(2
g/L)
1.1
c
11.7
c
2.2
a
84.3
a
Copper
hydroxide
(2
g/L)
+
ferric
chloride
(0.022
g/L)
1.2
c
19.6
c
1.9
b
79.0
ab
Cuprous
oxide
(2
mL/L)
1.1
c
12.9
c
2.0
b
76.6
ab
LSD
(P
=
0.05)
0.2
16.7
0.2
13.1
East
1.3
b
25.8
b
1.9
74.2
West
1.4
a
30.4
a
1.8
73.9
LSD
(P
=
0.05)
0.1
13.1
A
Mean
values
within
columns
followed
by
the
same
letter
are
not
significantly
different
at
P
=
0.05
(n
=
4).
B
Industry
standard
program
-2
applications
of
copper
oxychloride
(Kocide
at
2
g/L)
+
Oil
(DC
Tron
at
6
mL/L)
followed
by
two
applications
of
mancozeb
(2
g/L)
+
Oil
(DC
Tron
at
6
mL/L).
oxychloride
fungicide
also
had
significantly
more
severe
rind
damage
compared
with
the
industry
standard
treatment
and
the
other
copper
types
tested
(Table
3).
Experiment
3
Increasing
the
concentration
of
azoxystrobin
applied
repeatedly
throughout
the
season
did
not
significantly
improve
black
spot
control
(Table
4).
However,
increasing
the
concentration
of
trifloxystrobin
applied
repeatedly
throughout
the
season,
resulted
in
significantly
less
black
spot
at
the
highest
concentration,
compared
with
the
two
lower
concentrations
tested.
When
azoxystrobin
or
trifloxystrobin
were
applied
repeatedly
throughout
the
season
at
the
highest
tested
rates,
the
severity
of
black
spot
was
significantly
reduced
compared
with
the
industry
standard
treatment.
However,
no
significant
differences
were
Chemical
control
for
citrus
black
spot
Table
4.
Effects
of
various
chemicals
in
experiment
3
on
citrus
black
spot
(caused
by
Guignardia
citricarpa)
of
'Navel'
orange
fruit
harvested
during
the
2001/2002
season
Treatment
Citrus
black
spot
Severity
Incidence
(1-5)
(%)
Untreated
control
Industry
standard
B
Azoxystrobin
(0.2
g/L)
Azoxystrobin
(0.4
g/L)
Azoxystrobin
(0.6
g/L)
Trifloxystrobin
(0.035
g/L)
Trifloxystrobin
(0.07
g/L)
Trifloxystrobin
(0.15
g/L)
Azoxystrobin
(0.2
g/L)
anti-resistance
c
Azoxystrobin
(0.4
g/L)
anti-resistance
c
Trifloxystrobin
(0.07
g/L)
anti-resistance
c
Trifloxystrobin
(0.015
g/L)
anti-resistance
c
LSD
(P
=
0.05)
East
West
LSD
(P
=
0.05)
1.73
A
a
1.21
bc
1.07
cd
1.07
cd
1.03
d
1.24
b
1.21
bc
1.03
d
1.08
bcd
1.23
bcd
1.14
bcd
1.14
bcd
0.16
1.16
b
1.21
a
0.04
50.4
a
15.7
bcd
5.4
cd
5.7
cd
3.0
d
19.2
b
18.6
b
2.9
d
6.8
bcd
17.1
bcd
10.3
bcd
12.0
d
12.9
11.7
b
16.1
a
0.4
A
Mean
values
within
columns
followed
by
the
same
letter
are
not
significantly
different
at
P
=
0.05
(n
=
4).
B
Industry
standard
program
-
two
applications
of
reduced
strength
copper
oxychloride
(Kocide
at
1
g/L)
+
Oil
(DC
Tron
at
6
mL/L)
followed
by
two
applications
of
mancozeb
(2
g/L).
c
Anti-resistance
program
-
two
applications
of
reduced
strength
copper
oxychloride
(Kocide
at
1
g/L)
+
Oil
(DC
Tron
at
6
mL/L),
followed
by
one
application
of
trifloxystrobin
or
azoxystrobin,
followed
by
a
single
application
of
mancozeb
(2
g/L).
detected
between
the
different
concentrations
of
trifloxystrobin
or
azoxystrobin
when
used
in
an
anti
-resistance
strategy
spray
program
and
both
strobilurin
fungicides
were
as
effective
as
the
industry
standard
treatment
against
black
spot
(Table
4).
Experiment
4
The
industry
standard
treatment
significantly
reduced
both
the
incidence
and
severity
of
black
spot
compared
with
the
untreated
control
(Table
5).
The
severity
and
incidence
of
black
spot
in
the
captan
and
phosphorous
acid
treatments
were
significantly
higher
than
the
industry
standard.
Most
other
treatments
were
found
to
be
no
more
effective,
or
no
less
effective
than
the
industry
standard
and
untreated
control.
Mite
populations
were
significantly
reduced
by
the
industry
standard
and
the
high
concentration
strobilurin
anti
-resistance
treatments
compared
with
the
untreated
control
(Table
5).
The
treatments
of
pyraclostrobin
alone
and
captan
alone
maintained
significantly
higher
mite
populations
than
the
untreated
control.
The
phosphorous
acid
treatment
and
low
concentration
strobilurin
anti
-resistance
strategy
treatments
were
not
significantly
different
from
the
untreated
control.
Australasian
Plant
Pathology
375
The
incidence
and
severity
of
black
spot
in
all
experiments
was
found
to
be
significantly
higher
on
the
western
aspect
of
the
tree
canopy
compared
with
the
eastern
aspect.
Canopy
aspect
had
no
effect
on
rind
damage.
Discussion
Azoxystrobin
has
been
shown
in
four
experiments
over
three
seasons
to
be
as
effective
as
the
industry
standard
copper/mancozeb
programs
in
controlling
citrus
black
spot.
Registration
of
this
product
for
control
of
black
spot
is,
therefore,
the
most
likely
candidate
of
all
the
strobilurins
tested.
Whilst
all
the
strobilurins
tested
were
as
efficacious
as
the
industry
standard
treatments,
the
most
data
were
able
to
be
collected
for
azoxystrobin.
The
effectiveness
of
the
strobilurins
has
been
previously
demonstrated
on
other
citrus
diseases
such
as
melanose
(caused
by
Diaporthe
citri),
scab
(caused
by
Elsinoe
fawcettii),
greasy
spot
(caused
by
Mycosphaerella
citri)
and
brown
spot
(caused
by
Alternaria
alternata)
in
the
USA
(McMillan
et
al.
1998;
Raid
et
al.
1999).
However,
strobilurins
are
more
desirable
than
copper
and
mancozeb
for
use
on
citrus,
as
we
found
significantly
reduced
rind
damage
on
fruits.
In
our
investigation,
pyraclostrobin-alone
and
captan
were
beneficial
to
the
IPM
predatory
mite
A.
victoriensis
compared
with
the
industry
standard
fungicides,
and
the
untreated
control.
Unfortunately,
mite
populations
were
not
measured
for
azoxystrobin-alone
treatments,
although
the
low
toxicity
of
azoxystrobin
to
A.
victoriensis
has
been
observed
(M.
Bernard,
unpublished
data).
Mancozeb
is
toxic
to
this
predatory
mite
(Smith
and
Papacek
1991)
so
low
mite
counts
were
expected
for
those
treatments
incorporating
repeated
applications
of
mancozeb
(industry
standard,
anti
-resistance
treatments).
However,
it
is
surprising
that
mite
counts
in
the
pyraclostrobin
alone
and
captan
treatments
were
significantly
higher
than
the
untreated
control.
This is
possibly
due
to
the
very
low
chemical
input
in
the
untreated
control
allowing
a
more
diverse
insect
population
to
develop,
introducing
competition
for
A.
victoriensis.
Further
experiments
examining
insect
populations
would
be
required
to
investigate
the
high
mite
populations
in
the
pyraclostrobin-alone
and
captan
treatments.
IPM
compatibility
and
rind
quality
are
issues
of
great
concern
to
the
citrus
industry,
and
the
strobilurins
address
these
grower
concerns.
Efficacy
of
the
strobilurins
was
not
compromised
when
they
were
integrated
into
an
anti
-resistance
strategy.
The
use
of
an
anti
-resistance
strategy
is
paramount
to
prolonging
the
useful
life
of
the
strobilurins
and
the
FRAC
guidelines
should
be
adhered
to.
Our
data
show
that
growers
will
not
be
disadvantaged
by
using
anti
-resistance
regimes.
Of
great
interest
in
our
investigations
was
the
effectiveness
of
the
plant
activator
Bion
against
black
spot.
Acibenzolar
was
able
to
reduce
black
spot
by
close
to
50%
of
the
untreated
control.
Natural
plant
defence
compounds
in
376
Australasian
Plant
Pathology
A.
K.
Miles
et
al.
Table
5.
Effects
of
various
chemicals
in
experiment
4
on
citrus
black
spot
(caused
by
Guignardia
citricarpa)
of
'Nova'
mandarin
fruit
harvested
during
the
2002/2003
season
and
populations
of
the
predatory
mite
Amblyseius
victoriensis
Treatment
Citrus
black
spot
Square
root
-transformed
Arcsine-transformed
severity
value
incidence
value
Predatory
mite
Square
root
-transformed
mites/5-leaf
whorl
count
Untreated
control
0.05
A
abc
(0.22)
0.03
a
(9.6)
0.8
be
(0.60)
Industry
standard
B
0.02
(0.02)
0.01
c
(1.4)
0.2
(0.02)
Azoxystrobin
(0.2
g/L)
anti-resistance
c
0.03
bcd
(0.06)
0.02
abc
(3.6)
0.4
cd
(0.15)
Azoxystrobin
(0.4
g/L)
anti-resistance
c
0.02
cd
(0.04)
0.02
bc
(2.3)
0.3
(0.11)
Pyraclostrobin
(0.4
g/L)
anti-resistance
c
0.02
cd
(0.04)
0.01
c
(1.7)
0.4
bcd
(0.19)
Pyraclostrobin
(0.8
g/L)
anti-resistance
c
0.02
cd
(0.04)
0.02
bc
(2.3)
0.3
(0.09)
Pyraclostrobin
(0.4
g/L)
0.04
bcd
(0.16)
0.03
ab
(9.0)
1.4
a
(1.96)
Pyraclostrobin
(0.8
g/L)
0.03
bcd
(0.07)
0.02
abc
(3.6)
1.6
a
(2.55)
Pyraclostrobin
(1.2
g/L)
0.02
cd
(0.04)
0.01
c
(2.0)
1.7
a
(2.94)
Captan
(1.25
g/L)
0.07
a
(0.55)
0.03
a
(10.9)
1.3
a
(1.76)
Phosphorous
acid
(3.33
mL/L)
0.05
ab
(0.24)
0.03
ab
(9.0)
0.8
b
(0.69)
LSD
(P
=
0.05)
0.03
0.02
0.4
East
0.02
b
(0.05)
0.02
b
(2.6)
West
0.04
a
(0.17)
0.03
a
(6.7)
LSD
(P
=
0.05)
0.01
0.01
A
Mean
values
within
columns
followed
by
the
same
letter
are
not
significantly
different
at
P
=
0.05
(n
=
4).
Values
in
parentheses
are
back
-transformed
means.
B
Industry
standard
program
-
one
application
of
copper
oxychloride
(Coppox at
2
g/L)
+
Oil
(DC
Tron
at
6
mL/L)
followed
by
five
applications
of
mancozeb
(2
g/L).
c
Anti-resistance
program
-
one
application
of
copper
oxychloride
(Coppox at
2
g/L)
+
Oil
(DC
Tron
at
6
mL/L),
followed
by
one
application
of
mancozeb
(2
g/L),
followed
by
one
application
of
azoxystrobin
or
pyraclostrobin,
followed
by
three
applications
of
mancozeb
(2
g/L).
citrus
that
may
be
activated
by
acibenzolar
include
citral
(Rodov
et
al.
1995),
citrinol,
narigin,
hesperidin
(Arimoto
1986),
osthol,
auraptene,
coumarin,
anoxycoumarin
(Ben-Yehoshua
et
al.
1988)
and
scoparone
(Kim
et
al.
1991).
Stimulation
of
these
compounds
by
acibenzolar
is
likely
to
be
effective
against
G.
citr•icarpa
as
this
fungus
would
be
readily
exposed
to
the
host
biology
during
the
pathogen's
latent
phase.
Acibenzolar
has
been
effective
against
other
pathogens
that
closely
interact
with
the
host
biology,
such
as
Cladosporium
oxysporum
(cause
of
passionfruit
scab),
in
which
the
pathogen
induces
cork
cell
development
in
the
host
(Willingham
et
al.
2002).
Pathogens
not
so
closely
interacting
with
their
host,
for
example
a
necrotrophic
pathogen
such
as
Alternaria
alternata
(cause
of
citrus
brown
spot),
producing
a
host
-specific
toxin
(HST),
may
not
be
as
easily
controlled
through
natural
host
defences
because
host
cells
are
killed
by
the
HST
prior
to
invasion
(Timmer
et
al.
2000).
This
would
allow
little
opportunity
for
host
cells
to
produce
anti
-fungal
compounds,
or
the
pathogen
to
be
exposed
to
them.
Willingham
et
al.
(2002)
suggests
this
as
the
reason
why
acibenzolar
was
less
effective
at
controlling
A.
alternata
leaf
spot
on
passionfruit
than
controlling
the
passionfruit
scab
disease.
Whilst
acibenzolar
alone
significantly
reduced
disease
compared
with
untreated
trees,
the
level
of
control
was
not
as
high
as
that
achieved
by
the
industry
standard
fungicides.
Tank
mixing
acibenzolar
with
different
fungicides
offered
no
significant
improvement
in
disease
control
compared
with
the
industry
standard
fungicides,
or
applying
the
fungicide
alone,
and
thus
further
tests
with
acibenzolar
were
not
pursued.
Of
the
other
products
tested,
methoxycrylate
was
the
most
effective
fungicide,
but
further
testing
was
abandoned
due
to
manufacturer
withdrawal
of
the
product
from
commercial
production.
Currently,
iprodione
is
registered
for
non-
bearing
citrus
only,
and
despite
its
effectiveness
at
controlling
disease,
it
cannot
be
used
on
fruit
-bearing
trees.
No
differences
in
disease
control
were
found
for
the
various
copper
formulations
in
experiment
2,
although
copper
oxychloride
resulted
in
significantly
more
severe
rind
damage
than
the
other
copper
formulations.
This
suggests
that
growers
can
choose
what
copper
type
they
use
based
on
product
characteristics
other
than
efficacy,
such
as
cost
or
ease
of
preparation
at
the
spray
tank.
The
fungicides
captan
and
phosphorous
acid,
whilst
being
non-toxic
to
A.
victoriensis
in
experiment
4,
were
not
effective
in
controlling
black
spot.
In
our
experiments,
black
spot
was
consistently
worse
on
the
western
(warmer)
aspect
of
the
canopy.
Kiely
(1948)
noted
that
the
disease
first
develops
on
the
warmer
side
of
the
tree.
Kiely
(1948)
also
noted
that
fruit
from
the
warmer
side
of
the
tree
mature
faster,
further
encouraging
disease
expression,
as
latency
of
the
disease
is
broken
at
fruit
ripening.
This
may
enable
selective
harvesting
of
fruit
for
export
markets
by
avoiding
higher
disease
areas
of
the
tree
canopy.
Our
experiments
demonstrated
the
effectiveness
of
the
strobilurins,
particularly
azoxystrobin,
as
a
new
IPM
Chemical
control
for
citrus
black
spot
compatible
tool
for
managing
black
spot
in
Australia.
By
using
the
proposed
anti
-resistance
regimes
and
replacing
the
first
mancozeb
application
with
a
strobilurin,
growers
utilising
IPM
systems
will
be
able
to
apply
three
chemical
applications
(2
x
copper,
1
x
strobilurin)
that
are
compatible
with
IPM.
At
present,
typically
only
two
compatible
applications
of
copper
(James
and
Rayner
1995)
are
used,
followed
by
mancozeb.
A
change
to
strobilurins
could
potentially
prolong
the
life
of
beneficial
insect populations
by
up
to
8
weeks,
depending
on
the
timing
of
the
applications.
Reducing
the
use
of
mancozeb
and
copper
also
has
the
potential
to
reduce
fruit
damage,
lower
inputs
of
these
chemicals
into
the
environment,
and
decrease
the
risk
of
resistance
development.
All
of
these
will
contribute
to
the
production
of
higher
quality
citrus
fruit
and
the
sustainability
of
the
industry.
Acknowledgements
The
authors
gratefully
acknowledge
the
financial
support
of
the
Australian
citrus
growers
through
Horticulture
Australia
Limited,
and
of
the
Queensland
Department
of
Primary
Industries
Horticulture.
Further
thanks
go
to
Mark
and
Peter
Trott
of
BJ
JE
Trott
&
Sons,
Murray
and
Avrial
Benham
of
Benyenda
Citrus,
and
Steven
and
Brett
Benham
of
Joey
Citrus
for
use
of
their
orchards
for
our
experiments.
Dan
Papacek,
Phil
Jackson,
Tim
Facy,
Tony
Meredith
and
Ed
Carlton
of
Bugs
For
Bugs
provided
entomological
expertise.
We
also
thank
Vivienne
Doogan
for
advice
on
statistical
analysis,
and
the
members
of
the
Central
Burnett
Horticultural
Committee
for
their
advice
and
encouragement.
Dean
Beasley,
Jan
Dean,
Fiona
Giblin,
Claire
Purcell,
Dominic
Hooghuis
and
Luke
Smith
provided
technical
assistance.
References
Afek
U,
Sztejnberg
A
(1989)
Effects
of
fosetyl-Al
and
phosphorous
acid
on
scoparone,
a
phytoalexin
associated
with
resistance
of
citrus
to
Phytophthora
citrophthora.
Phytopathology
79,
736-739.
Agostini
JP,
Bushong
PM,
Timmer
LW
(2003)
Greenhouse
evaluation
of
products
that
induce
host
resistance
for
control
of
scab, melanose,
and
Alternaria
brown
spot
of
citrus.
Plant
Disease
87,
69-74.
Arimoto
Y,
Homma
Y,
Misato
T
(1986)
Studies
on
citrus
melanose
and
citrus
stem
end
rot
by
Diaporthe
citri
(Faw)
Wolf
Part
4
Antifungal
substance
in
melanose
spot.
Ann.
Phytopathology
Society
of
Japan
52,
39-46.
Becker
WF,
Von
Jagow
G,
Anke
T,
Steglich
W
(1981)
Oudemansin,
strobilurin
A,
strobilurin
B
and
myxothiazol:
new
inhibitors
of
the
bc
1
segment
of
the
respiratory
chain
within
an
E-P-
methoxyacrylate
system
as
common
structural
element.
FEBS
Letters
132,
329-333.
doi:10.1016/0014-5793(81)81190-8
Benson
AH
(1895)
Black
spot
of
the
orange.
Agricultural
Gazette
N.S.W.
6,
249-257.
Ben-Yehoshua
S,
Shapiro
S,
Kim
JJ,
Sharoni
J,
Carmeli
S,
Kashman
Y
(1988)
Resistance
of
fruit
to
pathogens
and
its
enhancement
by
curing.
In
'Proceedings
of
the
6th
international
citrus
congress'.
(Eds
R
Goren,
K
Mendel)
pp.
1371-1379.
(Balaban
Publishers)
Australasian
Plant
Pathology
377
Brodrick
HT,
Rabie
CJ
(1970)
Light
and
temperature
effects
on
symptom
development
and
sporulation
of
Guignardia
citricarpa
Kiely,
on
Citrus
sinensis
(Linn)
Osbeck.
Phytophylactica
2,
157-164.
Calavan
EC
(1960)
Black
spot
of
citrus.
The
California
Citrograph
November,
4-24.
Friedrich
L,
Lawton
K,
Ruess
W,
Masner
P,
Specker
N,
et
al.
(1996)
A
benzothiadiazole
derivative
induces
systemic
acquired
resistance
in
tobacco.
The
Plant
Journal
10,
61-70.
doi:10.1046/J.1365-313X.1996.10010061.X
Garran
SM
(1996)
Citrus
black
spot
in
the
northeast
of
Entre
Rios:
etiology,
epidemiology
and
control.
In
'Proceedings
of
the
International
Society
of
Citriculture'.
pp.
466-471.
(International
Society
of
Citriculture:
Nelspruit,
South
Africa)
Godwin
JR,
Anthony
VM,
Clough
JM,
Godfrey
CRA
(1992)
ICIA5504:
a
novel,
broad
spectrum,
systemic
P-methoxy-acrylate
fungicide.
In
'Proceedings
of
the
Brighton
crop
protection
conference'.
Farnham,
UK.
pp.
435-422.
(British
Crop
Protection
Council)
Godwin
JR,
Young
JE,
Hart
CA
(1994)
ICIA
5504:
Effects
on
development
of
cereal
pathogens.
In
'Proceedings
of
the
Brighton
crop
protection
conference'.
pp.
259-264.
(British
Crop
Protection
Council:
Surrey,
UK)
Grant
BR,
Dunstan
RH,
Griffith
JM,
Niere
JO,
Smillie
RH
(1990)
The
mechanism
of
phosphonic
(phosphorous)
acid
action
in
Phytophthora.
Australasian
Plant
Pathology
19,
115-121.
Herbert
JA,
Grech
NM
(1985)
A
strain
of
Guignardia
citricarpa,
the
citrus
black
spot
pathogen,
resistant
to
benomyl
in
South
Africa.
Plant
Disease
69,
1007.
James
DG,
Rayner
M
(1995)
Toxicity
of
viticultural
pesticides
to
the
predatory
mites
Amblyseius
vitcoriensis
and
Typhlodromus
doreenae.
Plant
Protection
Quarterly
10,
99-143.
Kiely
TB
(1948)
Preliminary
studies
on
Guignardia
citricarpa
N.S.:
the
ascigerous
stage
of
Phoma
citricarpa
McAlp.
and
its
relation
to
black
spot
of
citrus.
Proceedings
of
the
Linnean
Society
of
New
South
Wales
73,
249-292.
Kim
JJ,
Ben-Yehoshua
S,
Shapiro
B,
Henis
Y,
Carmeli
S
(1991)
Accumulation
of
scoparone
in
heat
-treated
lemon
fruit
inoculated
with
Penicillium
digitatum.
Plant
Physiology
97,
880-885.
Korf
HJG,
Schutte
GC,
Kotze
JM
(2001)
Effect
of
packhouse
procedures
on
the
viability
of
Phyllosticta
citricarpa,
anamorph
of
the
citrus
black
spot
pathogen.
African
Plant
Protection
7,
103-109.
Kotze
JM
(1981)
Epidemiology
and
control
of
citrus
black
spot
in
South
Africa.
Plant
Disease
65,
945-955.
Lawton
KA,
Friedrich
L,
Hunt
M,
Weymann
K,
Delaney
T,
Kessmann
H,
Staub
T,
Ryals
J
(1996)
Benzothiadiazole
induces
disease
resistance
in
Arabidopsis
by
activation
of
the
systemic
acquired
resistance
signal
transduction
pathway.
The
Plant
Journal
10,
71-82.
doi:10.1046/J.1365-313X.1996.10010071.X
McOnie
KC
(1964)
Source
of
inoculum
of
Guignardia
citricarpa,
the
citrus
black
spot
pathogen.
Phtyopathology
54,
64-67.
McOnie
KC
(1967)
Germination
and
infection
of
citrus
by
ascospores
of
Guignardia
citricarpa
in
relation
to
control
of
black
spot.
Phytopathology
57,
743-746.
McMillan
RT,
Zitko
SE,
Timmer
LW
(1998)
Citrus,
tropical
and
miscellaneous
crop
reports.
Fungicide
and
Nematicide
Tests
53,
489-494.
Raid
RN,
Timmer
LW,
Zitko
SE
(1999)
Citrus,
tropical
and
miscellaneous
crop
reports.
Fungicide
and
Nematicide
Tests
54,
553-556.
Rodov
V,
Ben-Yehoshua
S,
Fang
DQ,
Jin
Kim
J,
Ashkenazi
R
(1995)
Preformed
antifungal
compounds
of
lemon
fruit:
citral
and
its
relation
to
disease
resistance.
Journal
of
Agricultural
and
Food
Chemistry
43,
1057-1061.
378
Australasian
Plant
Pathology
Sauter
H,
Ammermann
E,
Roehl
F
(1994)
Strobilurins
from
natural
products
to
a
new
class
of
fungicides.
In
'Natural
products
as
a
source
for
new
agrochemicals'.
(Ed.
LG
Copping)
(The
Royal
Society
of
Chemistry:
London,
UK)
Schutte
GC,
Becton
KV,
Kotze
JM
(1997)
Rind
stippling
on
valencia
oranges
by
copper
fungicides
used
for
control
of
citrus
black
spot
in
South
Africa.
Plant
Disease
81,
851-854.
Smith
D,
Papacek
DF
(1991)
Studies
of
the
predatory
mite
Amblyseius
victoriensis
(Acarina:
Phytoseiidae)
in
citrus
orchards
of
south-east
Queensland:
control
of
Tegolophus
australis
and
Phyllocoptruta
oleivora
(Acarina:
Eriophyidae),
effect
of
pesticides,
alternative
host
plants
and
augmentative
release.
Experimental
and
Applied
Acarology
12,
195-217.
Tally
A,
Oostendorp
M,
Lawton
K,
Staub
T,
Bassi
B
(1999)
Commercial
development
of
elicitors
of
induced
resistance
to
pathogens.
In
'Induced
plant
defences
against
pathogens
and
herbivores'.
pp.
357-369.
(Eds
A
Agawal,
Sadik
Tuzun,
E
Bent)
(APS
Press)
A.
K.
Miles
et
al.
Timmer
LW,
Darhower
HM,
Zitko
SE,
Peever
TL,
Ibanez
AM,
Bushong
PM
(2000)
Environmental
factors
affecting
the
severity
of
Alternaria
brown
spot
of
citrus
and
their
potential
use
in
timing
fungicide
applications.
Plant
Disease
84,
638-643.
Timmer
LW,
Zitko
SE,
Albrigo
LG
(1998)
Split
applications
of
copper
fungicides
improves
control
of
melanose
on
grapefruit
in
Florida.
Plant
Disease
82,
983-986.
Wager
VA
(1952)
'The
black
spot
disease
of
citrus
in
South
Africa.'
University
of
South
Africa,
Department
of
Agriculture,
Science
Bulletin
No.
303.
Willingham
SL,
Pegg
KG,
Langdon
PWB,
Cooke
AW,
Peasley
D,
Mclennan
R
(2002)
Combinations
of
strobilurin
and
acibenzolar
(Bion)
to
reduce
scab
on
passionfruit
caused
by
Cladosporium
oxysporum.
Australasian
Plant
Pathology
31,
333-336.
doi:10.1071/AP02036
Received
31
July
2003,
accepted
10
February
2004
http://www.publish.csiro.au/journals/app