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New Zealand Journal of Experimental Agriculture
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Fungal fruit rots of Actinidia deliciosa (kiwifruit)
S. R. Pennycook
To cite this article:S. R. Pennycook (1985) Fungal fruit rots of Actinidia deliciosa
(kiwifruit), New Zealand Journal of Experimental Agriculture, 13:4, 289-299, DOI:10.1080/03015521.1985.10426097
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New Zealand Journal o Experimental Agriculture 1985,
Vol
13:
289-299 289
0301-5521/85/1304-0289 2.50/0 Crown copyright 1985
Review
Fungal fruit rots o
ctinidia deliciosa
(kiwifruit)
S. R. PENNYCOOK
Plant Diseases Division, DSIR
Private Bag, Auckland, New Zealand
Abstract Current knowledge
of
the symptoms,
etiology, and control
of
the three main fungal fruit
rots
of
kiwifruit in New Zealand
is
reviewed. Field
rot, caused by Sclerotinia sclerotiorum affects
immature fruits on the vines. Storage rot, caused
by Botrytis cinerea affects harvested fruits during
cold storage. Ripe rot, caused by Botryosphaeria
doth idea affects harvested fruits during post-stor
age ripening.
Keywords plant diseases; fruit rots; post-har
vest diseases; kiwifruit; Sclerotinia sclerotiorum;
Botrytis cinerea; Botryosphaeria dothidea;
field rot;
storage rot; ripe rot
INTRODUCTION
The kiwifruit, Actinidia deliciosa (Chevalier) Liang
& Ferguson (1984; syn. A chinensis Planchon var.
hispida Liang),
is
now established as New Zealand's
major horticultural export crop (Weston & Bollard
1984). During the early years of its commercial
development, the crop was regarded as virtually
disease-free (Bailey 1950, 1961; Bailey Topping
1951;
Schroeder
&
Fletcher
1967),
but, with the
increasing duration
of
kiwifruit monoculture and
the rapid expansion of production, disease prob
lems have become more numerous and important
(Sale 1980). However, in comprehensive publica
tions dealing with the crop, information on kiwi
fruit diseases and their control has remained sparse
This paper was first presented on 23 November 1983
at
a seminar in honour of Professor F.
J.
Newhook on his
retirement from the
Chair
of
Plant
Pathology, Depart
ment of Botany, University of Auckland, Auckland, New
Zealand.
Received 30 May
1985;
revision
29
July 1985
and rudimentary (Fletcher 1971; Ford 1971; Sale
1981, 1983, 1984).
This paper reviews our current knowledge in New
Zealand of field rot, storage rot, and ripe rot, the
three main fungal diseases that directly affect the
marketable product - the fruit.
FIELD ROT
The major rot that affects immature fruits while
they are growing on the vines is caused by Scler-
otinia sclerotiorum (Libert) de Bary (Pennycook
1982; for pathogen description and illustrations, see
Kohn
1979).
Field rot has often in the past been
mistakenly attributed to infection by Botrytis
cinerea Persoon : Fries (Fletcher 1971; Ford 1971;
Sale 1981). Isolations from lesions on fruits that
had dropped from the vines during a field rot epi
demic in late January 1980 yielded 80%
S. sclero-
tiorum
and
20%
B
cinerea
(D. J. Beever
unpublished data). The presence of Botrytis in these
esions may have resulted from secondary infec
tion, possibly after the fruits had fallen to the
ground; over several years, I have isolated no fun
gus other than S. sclerotiorum from numerous field
rot lesions on fruits that had not yet fallen from
the vines. Seasonal incidence of field rot is depend
ent on the frequency and duration of periods of
summer rain conducive to the establishment
of
infection by
Sclerotinia
ascospores.
An
estimated
5
loss
of
immature fruits was reported from the
Te Puke district after a severe
Sclerotinia
infection
period in late December 1980.
Symptoms
The earliest symptom
of
Sclerotinia field rot is a
blossom blight during late November and Decem
ber. Blossoms and their pedicels tum pale brown
and wither. The symptoms are common on male
vines, and entire clusters of male blossoms degen
erate into a tangled mass (Fig. I); female buds and
blossoms are less frequently affected. Bud symp
toms could be confused with those
of
bacterial bud
rot (Young 1984), from which they differ in two
conspicuous ways: the characteristic bacterial slim
ing and darkening of the anthers is absent, and the
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290
New Zealand Journal of Experimental Agriculture, 1985, Vol. 13
withered brown tissues are not confined to the bud
but usually include the full length of the pedicel as
well.
In a dry season, the withered blossoms become
dry and crisp with little or no mycelium apparent.
No secondary spread of infection occurs.
In a wet season, the rotting blossoms remain soft
and mushy, and become covered with copious white
mycelium. The mycelium often aggregates into
dense knots c. 1-3 mm in diameter, which may
darken and harden to form sclerotia. The rot lesions
frequently progress from the pedicels into the shoots
(Fig.
1),
and destructive secondary spread is com
mon where rain-sodden infected blossoms adhere
to shoots, leaves, and petioles.
Fruit rot symptoms can develop at any time from
fruit set onwards, but occur most commonly during
December and January. Fruit lesions are watery,
sunken, and more
or less whitish (depending on the
degree
of
superficial mycelial growth); black scler
otia often develop amongst the mycelium on the
surface of the lesions (Fig.
2).
Lesions rarely occur
on clean, exposed fruit surfaces, but are usually
centred on sites t which either infected buds or
blossom debris (particularly senescing stamens nd
petals) are in contact with the fruit surface, or adja
cent fruits are in contact with each other so that
they retain a water droplet between them.
Fruits affected by large, deeply penetrating lesions
usually drop from the vines within a week or two
of infection. However, if dry weather intervenes,
Fig. 1 clerotinia sclerotiorum
blight
of
male kiwifruit blossoms.
Shoot lesions are arrowed.
lesions may dry out leaving the fruits badly scarred
Fig.
3) but otherwise unimpaired.
Etiology
clerotinia sclerotiorum
overwinters in kiwifruit
orchards as sclerotia in the soil. Some of the scler
otia will have developed on diseased kiwifruit blos
soms and fruits during the previous summer, but
probably their major source is saprophytic growth
of the fungus on grass and weed debris and other
ground litter.
After a period
of
winter dormancy, sclerotia ger
minate during spring and summer in response to
moisture and rising soil temperatures (Willetts
Wong
1980).
Apothecia (sexual fructifications) grow
from the sclerotia up through the soil and litter,
and flare out just above ground level into a trum
pet-shaped, off-white to fawnish-brown disc, usu
ally c. 5-6 mm in diameter
Fig.
4). In the Te Puke
district, the earliest apothecia have been found in
kiwifruit orchards in late September; they become
plentiful during late October, November,
nd
December. Apothecial production usually termi
nates in mid summer as the soil dries out or as the
supply of overwintered sclerotia is depleted. How
ever, in some years nd in some
10ca1ities,
apothe
cial production may continue throughout the
summer.
There is frequent spore dispersal from the apoth
ecia. Changes in atmospheric humidity
or
pressure
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Pennycook Fungal
fruit rots
of
kiwifruit
Fig. 2
Sclerotinia sclerotiorum field
rot
of
immature
kiwifruit. Sclerotium left) and adhering anthers right) are
arrowed.
trigger 'puffing', the simultaneous discharge of
thousands ofascospores from the upper, fertile sur
face of an apothecium (Hartill Underhill 1976).
This phenomenon can sometimes be observed as
a transient, cigarette smoke-like wisp rising a few
centimetres from the orchard floor as the litter is
disturbed. Discharged ascospores are dispersed by
wind and deposited on the vines as ascospore
'showers'.
Fruit infections result only if ascospores are
deposited at infection sites that are in direct con
tact with an adequate food base
e
.g., senescing sta
mens and petals,
or
water droplets containing pollen
grains
or
pollen exudates) for saprophytic growth,
and
if
those infection sites subsequently remain wet
291
for several hours (Willetts Wong 1980). There is
no secondary spread from fruit lesions because the
pathogen does not produce conidia (asexual spores).
Control
The risk
of
Sclerotinia
infection can be reduced by
removal of senescent blossom tissues from the
vines. A vigorous air-blast spray application
at
petal
falI
will help dislodge the senescent petals and sta
mens
ofthe
female
flowers
from the newly set fruits.
Male vines should be pruned as soon as possible
after pollination, to eliminate the senescent male
blossoms. General pruning for a relatively open
canopy
will
also reduce the risk of infection by
allowing the vines to dry more quickly after rain.
The dicarboximide fungicides registered for use
on kiwifruit, iprodione (Rovral) and vinclozolin
(Ronilan), are extremely effective against
S.
scler-
otiorum
if their application is timed to coincide with
the deposition
of
ascospore showers. In some
seasons, a single, thorough application at late blos
som-early petal fall to prevent saprophytic colon
isation of senescing blossom tissues may be
sufficient. However, in a wet season, additional
applications may be necessary during blossom and
after petal
fall
.
Ground applications of fungicides, herbicides,
fumigants, and hyperparasitic fungi have been used
to destroy either sclerotia
or
apothecia of S.
scler-
otiorum
in susceptible field crops (Hartill Camp
bell
1973;
KrUger 1973; Trutmann et al.
1980).
However, their efficacy has not been demonstrated
in kiwifruit orchards.
STORAGE R T
Harvested fruits that have been graded and packed
as healthy and unblemished will often develop rot
symptoms while being held in commercial cold
storage at Oe During the normal storage life of
the fruits, these symptoms consist
of
strikingly uni
form stem-end rots caused by the grey mould fun
gus,
Botrytis cinerea
Persoon : Fries (Scapin et al.
1983; Beever et al.
1984;
Pennycook
1984;
for
pathogen description
and
illustration, see Ellis
1971). Later, when the storage life of the fruits is
coming to an end, more variable symptoms
develop, associated with a number of fungal path
ogens including
B. cinerea, Fusarium cumin tum
Ellis Everhart,
Cryptosporiopsis
spp., and
Phom-
opsis
spp. The
Botrytis
rot
of
kiwifruit reported from
California (Opgenorth 1983; Sommer et al.
1983)
appears to belong in this category
of
late-storage
diseases; the symptoms
and
etiology described for
the Californian disease differ from those of
Botrytis
stem-end rot in New Zealand.
Botrytis
stem-end
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292 New Zealand Journal o Experimental Agriculture 1985 Vol. 3
Fig. 3 Scarring
o
immature
kiwifruits resulting from dried out
lesions o
clerotinia sclerotiorum
field rot.
Fig. 4
clerotinia sclerotiorum
apothecia protruding above the
ground
in
a kiwifruit orchard.
Scale
is
indicated by a ballpoint
pen tip.
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Pennycook-Fungal fruit rots
of
kiwifruit
Fig. 5 External symptoms
of
Botrytis cinerea stem-end
rot
of
cold-stored kiwifruit.
rot first became a problem in New Zealand in
1978
(Beever et
al. 1984),
when the overall loss to the
industry was estimated
as
c. 2-3 . Incidence
is
unpredictable and highly variable, not only from
year to year and from orchard to orchard, but even
between fruits picked from the same vines on dif
ferent days.
Up
to
32
incidence
of
primary
Botry-
tis
stem-end rots has been recorded in New Zealand
kiwifruit
(S. R
Pennycook unpublished data), and
an incidence
of> 50
has been reported from Italy
(Bisiach et al. 1984; Bisiach Minervini 1984).
Symptoms
The symptoms
of
Botrytis
stem-end rot first begin
to appear after
c.
4 weeks
of
cold storage. A con
spicuous external darkening commences at the stem
end
of
the fruit, and advances with a straight,
sharply defined front (Fig. 5). The affected area
retains the normal shape
of
the fruit, and
feels
soft
but resilient. The unaffected area remains
firm
and
does not differ from healthy fruits. The rot advances
more or less evenly through all the internal tissues
of
the fruit
(Fig. 6);
after several weeks it may have
spread throughout the fruit, but often the distal end
remains unaffected. The affected
flesh is
glassy and
293
Fig. 6 Internal symptoms of Botrytis cinerea stem-end
rot
of
cold-stored kiwifruit.
water-soaked, and often has a faint pinkish-fawn
discoloration.
Initially, there
is
little or no visible fungal growth
on the outside
of
the rotting fruit. Later, however,
an uneven, fluffy, dull white layer
of
Botrytis myce
lium may develop on the skin
of
the affected por
tion
of
the fruit. This white mycelium usually
resembles the typical 'white mould'
of Sc/erotinia
sc/erotiorum
rather than the 'grey mould' usually
associated with
Batrytis
infections. After prolonged
cold storage, the mycelium may assume a grey,
fuzzy appearance, because of the growth
of
tufts of
dark conidiophores bearing numerous, powdery,
grey conidia; in other instances, the mycelium may
aggregate to form small, flat, irregularly shaped,
black sclerotia, closely appressed to the fruit sur
face
. External mycelium frequently spreads to adja
cent fruits within the tray, ultimately causing
secondary infections ('nesting').
At
1C, Botrytis
lesions on kiwifruit produce only a small amount
of
ethylene (an hourly rate
of c.
0.2
J-lgjkg
fruit),
although they are capable
of
prolific production (an
hourly rate
of
up to 135 J-lg/kg) at ambient tem
peratures
(M. J.
Muir &
S.
R. Pennycook unpub
lished data).
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294
New Zealand Journal
of
Experimental Agriculture, 1985 , Vol. 13
Fig. 7 Sporulation arrowed)
of
Botrytis cinerea on
senescent petal of a kiwifruit blossom at fruit set.
Etiology
Botrytis cinerea often becomes conspicuous in
kiwifruit orchards during late blossom and petal
fall late November-December). On unsprayed
vines, profuse sporulation may
be
visible on 80
90
of
blossoms that have senescing petals Fig.
7).
During wet weather, leaf lesions may develop
from secondary spread via adhering debris from
infected blossoms Fig. 8). t was initially assumed
by analogy with the etiology
of
Botrytis fruit rot
in strawberry) that Botrytis stem-end rots in kiwi
fruit were the result of latent infections established
on the fruits during the blossom period Beever
1979). Subsequent experimental data Pennycook
1984 and unpublished data) have indicated that this
assumption was incorrect, and that kiwifruit blos
som infections have only an indirect influence on
stem-end rots by increasing the amount
of
Botrytis
inoculum present in the orchards.
Through the remainder
of
the growing season
January-May), Botrytis sporulation
is
rarely
observed on kiwifruit vines, except on wounded
tissues. However, the fungus can be readily cul
tured from apparently healthy, undamaged sepals
and fruits; the nature of this Botrytis population is
unclear, but it appears to be predominantly
epiphytic.
Fruit infection occurs during harvesting, grading,
and packing operations, by direct Botrytis contam
ination
of
the picking wound that is formed where
the fruit
is
snapped from its pedicel Pennycook
1984 and unpublished data). Symptoms first begin
to appear after
c.
4 weeks
of
cold storage. After
c.
12 weeks, the remaining healthy fruits are unlikely
to develop primary Botrytis stem-end rots during
continued cold storage, although secondary infec
tions nesting) may continue to develop.
The
low
concentrations
of
ethylene produced by
Botrytis rots during cold storage may reduce the
storage life
of
healthy fruits within the same tray.
Such fruits also tend to have a reduced post-storage
shelf-life and a more rapid onset
of
ripe rots see
below) compared with similar fruits from trays
unaffected by
Botrytis
storage rots.
Control
Because Botrytis infection occurs via the picking
wound that is created as the fruit is detached from
its pedicel during harvest, orchard fungicide appli
cations cannot directly control the disease. How
ever, they can contribute indirectly, by reducing the
level of Botrytis inoculum present at harvest. The
two critical periods for this purpose are: a) late
blossom-early petal fall, to prevent the build up
of
heavy
Botrytis
sporulation on senescing petals; and
b) pre-harvest, to minimise the risk
of Botrytis
contamination
of
the picking wounds during har
vesting and post-harvest handling
of
the fruits. The
dicarboximide fungicides iprodione and vinclozo
lin are currently recommended for both these
applications. The pre-harvest application should be
a thorough wetting with a high volume, dilute spray,
to achieve maximum fungicide penetration to the
specific target area, the stem end of the fruits,
including the sepals. The residues from the pre-har
vest application also prevent the growth
of
external
mycelium on infected fruits during storage, thus
eliminating nesting and confining losses to those
fruits with primary, picking wound infections.
Incidence
of
Botrytis stem-end rot in unsprayed
fruits has been significantly decreased by the use
of
techniques which reduce the opportunities for
Botrytis
contamination
of
the picking wounds
Pennycook 1984 and unpublished data). However,
such techniques have not yet been translated into
practical, commercial methods.
Incidence
of
Botrytis stem-end rot in unsprayed
fruits has also been decreased to a very low level
by experimental applications
of
dicarboximide
fungicide immediately post-harvest, either specifi
cally to the picking wounds, or as a general fruit
dip (S. R. Pennycook unpublished data). A delay
of
24 h between harvest
and
fungicide application
significantly reduced the efficacy
of
such treat
ments. Bulk methods
of
post-harvest fungicidal
treatment have not yet been tested, and commer
cial use
of
such methods would conflict with the
pesticide regulations of some importing countries.
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Pennycook Fungal fruit rots of kiwifruit
295
Fig. 8 Secondary infection of kiwifruit leaf by otrytis cinerea growing from adhering, infected blossom debris.
RIP ROT
Kiwifruits develop ripe rots as they are ripening at
ambient temperatures, either immediately after
harvest or after removal from cold storage. The
presence of ripe rots reduces the crop's shelf-life
directly,
by
the deterioration of
flesh
Quality and
the development of unpleasant odours and fla-
vours in affected fruits, and indirectly, by the accel
erated ripening ofadjacent fruits because of ethylene
evolution. However, it is not clear to what extent
either the onset of the rots is a result of the ripening
process,
or
the developing rots are themselves a
primary cause of accelerated ripening. Several fun
gal pathogens have been isolated from various ripe
rot symptoms (Beraha
1970;
Sommer
&
Beraha
1975; Pennycook
1981 a;
Hawthorne et al. 1982;
Hawthorne Reid 1982), but most of these path
ogens produce lesions only after the fruits have
already reached an advanced state of ripeness or
become disagreeably overripe.
Of
more commer
cial significance is a distinctive type of lesion,
caused by
otryosphaeria doth idea
(Mougeot ex
Fries) Cesati & de Notaris (anamorph:
Fusicoccum
aesculi
Corda), that develops at a relatively early
stage in the ripening process (Pennvcook 1981b; for
pathogen description and illustrations, see Penny
cook Samuels 1985). In samples of kiwifruits
from the Te Puke district, up to
15
of fruits have
been affected with the distinctive, early symptoms
of B doth idea ripe rot, while the total incidence of
this fungus (including later developing, more var
iable symptoms) has been up to
32
(Pennycook
1981 b).
B
dothidea
ripe rot is also a major disease
affecting kiwifruits grown in Japan
(S.
Takaya pers.
comm.).
Symptoms
An occasional early symptom
of
B
dothidea
ripe
rot is the development of shallow, brown dimples,
c. 2 5 mm in diameter, on the surface
of
the fruits;
the skin within each dimple is unbroken, with a
thin layer of dry, yellowish flesh beneath. Some,
but not all, of these dimples develop into expand
ing rot lesions as the fruits ripen, whereas, in other
instances, identical rot lesions develop without a
preliminary dimple having been observed.
Lesions of B
dothidea
ripe rot expand rapidly
into large, pale brown ovals up to c. 30 mm long
with a narrow, glassy, dark green margin (Fig. 9).
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296
New Zealand Journal
of
Experimental Agriculture,
1985,
Vol.
13
Fig. 9 External symptoms of Botryosphaeria doth idea
ripe rot of kiwifruit.
There
is
usually only one lesion per fruit, but occa
sionally up to three may develop simultaneously.
In some years the lesions occur mainly on the side
of the fruits, but in other years mainly at the distal
end, centred on the senescent styles. The lesion sur
face
is soft and squashy; it usually conforms to the
normal outline
of
the fruit, but is slightly depressed
in some instances; the skin is unbroken. Internally,
the fruit tissues are macerated
so
that the skin peels
back easily to expose a zonate lesion (Fig.
10)
con
sisting
of
a narrow, water-soaked, green margin
surrounding a water-soaked, gas-suffused, whitish
oval, often with a small, hard, yellowish, central
core corresponding to the tissues underlying the
dimple symptom (see above). The macerated tis
sues extend deep into the fruit in a cone or lens
sharply delimited from the unaffected flesh
Fig.
II).
Lesions of
B doth idea
developing in fully ripe
overripe fruits are smaller and more variable than
the earlier developing lesions. On each fruit there
are usually numerous, sometimes confluent, lesions,
most
of
which yield fungi other than
B doth idea;
lesions caused
by
the various pathogens cannot be
distinguished reliably on the basis of their
appearance.
Etiology
Botryosphaeria dothidea is a cosmopolitan fungus
with a wide host range (Punithalingam Holliday
1973 ; as
B ribis
Grossenbacher Duggar). In
kiwifruit orchards, the most abundant source of
inoculum is in the numerous dead twigs and
branches in poplar shelterbelt trees. The bark
of
these twigs and branches is often riddled with black,
asexual and sexual fructifications (pycnidia and
ascomata) of
B dothidea
Fig. 12). Ascomata and
pycnidia have also been found occasionally in the
bark
of
kiwifruit prunings that have been left to lie
on the ground in the orchard.
In samples of kiwifruits picked from a block
sheltered
by
heavily infected poplars, incidence of
B doth idea ripe rot decreased with increasing dis
tance from the trees S.
R
Pennycook unpublished
data). This distribution pattern suggests that infec
tions are caused by wind-borne ascospores which
are discharged into the air during warm, wet
weather (Sutton 1981). (The conidia, an alternative
potential source of inoculum, are produced n slimy
masses that are distributed over only relatively short
distances by rain splash.) There is no unequivocal
evidence
of
when the fruits become infected; warm,
wet weather, conducive to ascospore dispersal and
infection, can occur t any period of the growing
season, but some experimental data suggest that
infections become established as early as blossom
or fruit set see below).
Whenever they may occur, the infections remain
completely latent until the fruits begin to ripen.
Factors which accelerate the ripening process not
only accelerate the onset
of
ripe rot symptoms but
also appear to increase their severity. However, the
development of ripe rot lesions may itself be a
cause, rather than an effect, of accelerated ripening.
Control
Fungicide applications to shelterbelt trees, and
elimination
of
kiwifruit prunings (either by removal
or by mulching) could be used to reduce the amount
of
inoculum of B doth idea present in the orchard.
Because the time of
infection of the kiwifruits is
unknown, it is difficult to design an effective pro
tectant fungicide programme. In one fungicide trial
in 1981-82, the greatest reduction in incidence of
B doth idea
ripe rot was achieved with a pro
gramme that included blossom, petal
fall,
and pre
harvest applications of dicarboximide fungicides;
programmes that lacked the blossom applications
gave smaller, but significant, reductions S. R. Pen
nycook unpublished data). However, the
1981
sur
vey data reported by Pennycook (198Ib) suggested
that pre-harvest dicarboximide sprays might be the
most effective. All these results may be measuring
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Pennycook-Fungal fruit rots o kiwifruit
Fig. 1 upper) Surface view
skin peeled off o internal symp
toms
o
Botryosphaeria doth idea
ripe rot o kiwifruit.
Fig. lower) Internal symp
toms
o
Botryosphaeria doth idea
ripe rot
o
kiwifruit.
Fig. 2 far right) Numerous
black pycnidia and ascomata o
Botryosphaeria dothidea develop
ing beneath the bark o a dead
twig in a poplar shelterbelt tree.
indirect effects. For example, a fungicide pro
gramme which reduces the incidence
o
Botrytis
stem-end rot will thus decrease ethylene produc
tion during cold storage see above), resulting in a
longer storage life and post-storage shelf-life for the
297
crop; the slower ripening o such fruits win delay
the development
o
ripe rot symptoms, resulting in
an apparent decrease in ripe rot incidence. Trays
repacked after removal
o
Botrytis-infected fruits
are probably at greatest risk
o
developing ripe rots
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298
New Zealand Journal of Experimental Agriculture, 1985, Vol. 13
in the market place, together with late-picked crops,
and trays that include some damaged fruits or fruits
of
more advanced maturity at picking. Conse
quently, the best method
of
avoiding the potential
economic damage from B. doth idea infections may
be a combination of effective control of Botrytis
storage rot, scrupulous quality control during grad
ing and packing to improve the general storage
quality of the crop, and careful handling through
out the distribution chain to ensure that ripening
is not accelerated at too early a stage.
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