Postharvest Biology and Technology 33 (2004) 175180

The influence of pre-storage delayed cooling on quality and

disorder incidence in Honeycrisp apple fruit
John M. DeLong , Robert K. Prange, Peter A. Harrison
Agriculture and Agri-Food Canada, Atlantic Food and Horticulture Research Centre, 32 Main Street, Kentville, NS, Canada B4N 1J5
Received 17 July 2003; accepted 26 February 2004

Abstract
The influence of a pre-storage, 7-day, 20 C warming period on post-harvest apple (Malus xdomestica Borkh.) fruit quality
and disorder expressionsoft scald and low temperature breakdown in particular, were investigated in Honeycrisp fruit grown
in the Annapolis Valley of Nova Scotia. The apples from 7-year old trees were harvested from three commercial sites on Sept
30, 2002 (early) and Oct 10, 2002 (late), after which, half of the fruit was immediately cooled to 5 C (control), while the other
half was held for 7 days at 20 C (delayed cooling treatment). Both the control and delay cooled apples were then stored at either
3 or 5 C in controlled atmosphere (CA) (2.5 kPa O2 ; 11.5 kPa CO2 ) or refrigerated air (RA) storage for 4 and 6 months. Fruit
quality measurements and disorder incidence were recorded following storage removal and a 7-day shelf-life at 20 C. Delayed
cooling had no effect on fruit firmness, soluble solids (%), titratable acidity, epidermal greasiness, senescent breakdown, and
bitter pit (the incidence of these latter disorders was low), while moisture loss from the delay cooled fruit ranged from 1.2 to 1.3%
following the 7-day treatment. Delayed cooling strongly suppressed the development of the storage disorders soft scald and low
temperature breakdown, which in the control fruit reached upwards to 30% of the sample. No CA- or RA-related differences in
these disorders were observed in the fruit receiving the pre-storage delayed cooling treatment. Storage rot was not influenced
by delayed cooling and was present in upwards to 32% of the fruit from the late-harvested apples after 6 months of storage.
In regions where soft scald and low temperature breakdown are serious postharvest problems, it appears that a delayed cooling
period prior to storage will help minimize economic loss.
Crown Copyright 2004 Published by Elsevier B.V. All rights reserved.
Keywords: Malus xdomestica Borkh.; Low temperature breakdown; Low temperature disorders; Postharvest quality; Soft scald; Storage

1. Introduction
The apple (Malus xdomestica Borkh.) cultivar Honeycrisp was developed in Minnesota and
Atlantic Food and Horticulture Research Centre contribution
no. 2274.
Corresponding author. Tel.: +1-902-679-5765;
fax: +1-902-679-2311.
E-mail address: delongj@agr.gc.ca (J.M. DeLong).

released in 1991 (Bedford, 2001). Since then,

Honeycrisp has become very popular in the
fresh fruit market in the northern US and eastern
Canada resulting in premium prices for the growers.
Honeycrisp fruit has shown a tendency to develop
soft scald as well as several other quality-related
problems (e.g., bitter pit, watercore, low temperature
breakdown, skin punctures, and decay), which vary
in severity with the growing region. These problems
threaten the horticultural adoption of this potentially

0925-5214/$ see front matter. Crown Copyright 2004 Published by Elsevier B.V. All rights reserved.
doi:10.1016/j.postharvbio.2004.02.009

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J.M. DeLong et al. / Postharvest Biology and Technology 33 (2004) 175180

profitable cultivar (Clements et al., 2001; Evans, 2001;

Greene and Weis, 2001; Schwallier, 2001; Prange
et al., 2002).
In Nova Scotia, soft scald is the most frequently
observed storage disorder, sometimes reaching 100%
incidence after harvest followed by low temperature breakdown and watercore (Prange et al., 2002;
Prange and DeLong, unpublished data). Meheriuk
et al. (1994) noted that soft scald is a low-temperature
disorder and is likely to occur when highly respiring
susceptible cultivars are cooled rapidly. Since it is
induced by storing fruit at 2.2 C or lower, Meheriuk
et al. (1994) recommend storage at temperatures not
lower than 2.5 C for the first 68 weeks. Although
a number of additional solutions to control soft scald
have been proposed, e.g., early harvest, avoiding delays in cooling, 2030% CO2 for 2 days during the
cooling period, 3842 C for 812 h before cooling
(Meheriuk et al., 1994; Bedford, 2001; Schwallier,
2001); none have been tested on regionally grown
Honeycrisp.
Honeycrisp fruit can develop a cortical browning
which has been called soggy breakdown (Watkins
and Rosenberger, 2002), an uncommon disorder
well-described by Smock (1977), but not recognized by Meheriuk et al. (1994) as being distinct
from low-temperature breakdown. As photographs of
soggy breakdown (Watkins and Rosenberger, 2002)
are identical to those of cortical low temperature
breakdown (Meheriuk et al., 1994), we refer to this
disorder in this report as low temperature breakdown.
Prange et al. (2002) observed that low temperature breakdown, watercore, and soft scald occur in
Honeycrisp fruit harvested early and stored immediately at 3 C in controlled atmosphere (CA), whereas
late-harvested fruit having a 4-week storage period
at >3 C before CA storage at 3 C developed very
few disorders. These observations indicate that there
are one or more significant factors in controlling
Honeycrisp storage disorders including: (1) storage
temperature (i.e., 3 C, may be too cold); (2) timing of harvest (early versus late) and storage regime
[refrigerated air (RA) versus CA]; and (3) a cooling
delay between harvest and CA or RA storage may be
beneficial.
Therefore, the objective of this study was to examine the influence of delayed cooling, timing of
harvest, storage temperature, and CA versus RA

environments on the occurrence of soft scald, low

temperature breakdown, and other quality-related
problems in Nova Scotia-grown Honeycrisp fruit.

2. Materials and methods

2.1. Plant material and storage conditions
Honeycrisp apples from 7-year old trees on M26
rootstock were harvested early (Sept 30, 2002) and
late (Oct 10, 2002) from three commercial orchards in
the Annapolis Valley of NS with each orchard being
treated as an experimental replicate. Half of the fruit
were immediately cooled over 24 h to 5 C and were
then stored at 3 or 5 C in either refrigerated air or
controlled atmosphere (2.5 kPa O2 , 11.5 kPa CO2 ),
while the other half was kept at 20 C for 7 days (delayed cooling) and were then stored at 3 or 5 C with
the control samples for 4 and 6 months in either RA
or CA environments. In both the RA and CA storage
regimes, the fruit were placed in top-loading 0.34 m3
cabinets; those in the CA environment were flushed
with nitrogen gas until O2 levels of 1.5% were obtained. The CA atmosphere was monitored and controlled by a David Bishop Instrument Oxystat 2002
system (Bacharach Europe, Warwickshire, UK).
2.2. Quality and disorder measurements
Apple weight loss (i.e., moisture loss) was determined as the difference in the weight of the apples
before and after the 7-day pre-storage warming period. Following 4 and 6 months of storage, 15 fruits
were removed from each treatment combination: 10
apples were immediately measured after warming at
20 C and five were held for a shelf-life period of 7
days at 20 C. Fruit firmness (N) was measured on the
red and green sides of individual apples with the fruit
quality testor (Geo-Met Instrument, New Minas, NS),
having the time limit window set at >0.1 and <1.0 s
(DeLong et al., 2000). Soluble solids content and titratable acidity were measured on the 10-apple composite
juice sample with a hand-held refractometer (Atago
Co., Tokyo) and by titration of 2 mL apple juice with
0.1 mol L1 sodium hydroxide, respectively. The latter was expressed as mg equivalents of malic acid per
100 mL juice (DeEll and Prange, 1998).

J.M. DeLong et al. / Postharvest Biology and Technology 33 (2004) 175180

After fruit removal from storage and 24 h at 20 C,

ethylene evolution rates (L L1 per 100 g fruit) for
each treatment were measured on five-apple samples
placed in 4 L mason jars with air flow rates across the
fruit of 20 mL min1 . Following equilibration, a 1 mL
gas sample was withdrawn by a syringe from each
jar outlet line and injected into a gas chromatograph
(GC) (Carle Instruments Inc., Anaheim, California)
equipped with a 1.9 m 3.2 mm (o.d.) stainless steel
column packed with activated alumina with helium
carrier flow at 50 mL min1 and a flame ionization
detector. Quantitation was performed by comparison
of the GC response of the sample to that of a certified
standard (DeEll and Prange, 1998).
The incidence of bitter pit, soft scald, low temperature breakdown, senescent breakdown, and rotted fruit
was assessed as percentages of the total fruit on the
10-apple sample following removal from storage and
on the five-apple sample following the 7-day shelf-life.
Epidermal greasiness was evaluated on a 03 scale,
where: 0, none; 1, slight; 2, moderate; and 3, severe
and unmarketable.
2.3. Experimental design and statistics
The experiment was planned as a randomized
complete design with factorial combination of five
treatments: harvest (early and late), pre-storage conditioning [control (none) and 7 days at 20 C], storage
regime (RA and CA), storage temperature (3 and
5 C) and storage duration (4 and 6 months) with each
treatment combination being replicated three times
(grower: rep). Following the 7-day shelf-life, the two
pre-storage conditioning treatments were compared
at the 4- and 6-month removals for each combination
of harvest, storage regime, and storage temperature
by the LSMeans options of SASs PROC GLM (SAS
Institute, 1994).

3. Results and discussion

Delayed cooling did not affect Honeycrisp firmness, soluble solids, and titratable acidity in early- or
late-harvested fruit held for 4 or 6 months in RA or
CA storage (data not shown). The most striking observation in this experiment was that delayed cooling
markedly suppressed not only cortical low tempera-

177

ture breakdown but also soft scald, regardless of the

timing of harvest, storage regime, duration, and temperature (Table 1A and B). Meheriuk et al. (1994)
recommend delayed cooling and fruit moisture loss
for control of low temperature breakdown but not for
soft scald. Both disorders are thought to be induced
by low storage temperatures (Meheriuk et al., 1994;
Watkins and Rosenberger, 2002), although it is unknown how low chilling temperatures stimulate the
cellular triggers that cause disorder expression. Interestingly, periodic fruit warming prior to and during
storage reduces the incidence of superficial scalda
postharvest disorder also described as chilling injury
(Watkins et al., 1995; Alwan and Watkins, 1999).
Watkins et al. (1995, 2000) suggest that fruit warming
ameliorates superficial scald susceptibility through:
(a) catabolism of toxic substances that accumulate at
lower temperatures; (b) an increase in fatty acid unsaturation; and (c) an increase in endogenous antioxidant compounds. Soft scald has been associated with
a low level or loss of the 18:2 polyunsaturated fatty
acid, linoleic acid (Wills, 1973; Hopkirk and Wills,
1981) as well as an increase in the six carbon alcohol,
hexanol (Wills, 1973). Exposure to chilling temperatures can increase phospholipase D activity which
provides free fatty acid substrate for lipoxygenase
(LOX) (Pinhero et al., 1998). In addition, enzymatic
degradation of linoleic acid via the LOX cascade
generates hexanol (Luning et al., 1995; Rowan et al.,
1999), which when applied exogenously, induces soft
scald symptoms (Wills, 1973).
The average water loss from the delayed cooled
fruit immediately following the treatment ranged
from 1.2 to 1.3% (Table 1A and B). Past research
has demonstrated that moisture loss from McIntosh
apples is associated with a reduction in senescent
and low temperature breakdown (Blanpied, 1981)
as well as the brown core (Lidster, 1990). A moisture loss induced reduction of acetate esters is also
associated with a decrease in low temperature breakdown in Jonathan fruit, perhaps due to the carrier effect of evaporating water on certain volatile
compounds (Wills, 1968). The biochemical linkages between water loss, fatty acid oxidation, and
the volatile compound chemistry that specifically affect low temperature-related disorder expression in
Honeycrisp are presently unknown but merit further
investigation.

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J.M. DeLong et al. / Postharvest Biology and Technology 33 (2004) 175180

Table 1
Low temperature breakdown, soft scald, rot, ethylene evolution, and weight loss in Honeyscrisp fruit following 4 and 6 months of (A)
CA and (B) RA storage at 3 and 5 C
Harvest

Storage
(months)

(A) CA storage
Early
4
6

Temperature
( C)

Low temperature
breakdowna (%)

Soft scald (%)

Rot (%)

Ethylene (per 100 g

fruit) (L L1 )

Weight loss
(%)

0b

7b

0b

7b

0b

7b

0b

7b

0b

7b

3
5
3
5

1.11c
7.86**
4.44
1.11

0
0
1.11
0

16.7**
2.3*
19**
3.33**

0
0
0
0

11.1
4.6
13.4
8.84

7.11
6.67
11.4
16.7

9.18*
29.3**
26.5**
38.5

5.18
11.7
15.7
29

0d
0
0
0

1.18
1.18
1.18
1.18

3
5
3
5

4.44
20**
10**
7.78*

0
0
1.11
1.11

16.8*
11.1**
21.6**
15.6**

0
0
0
0

17.9
7.94
21.1
23.3

11.9
11.4
27.8
22.6

9.38*
20.2
33**
45.9**

5.81
14.4
14.4
23.3

0
0
0
0

1.27
1.27
1.28
1.27

3
5
3
5

1.11
1.11
0
0

1.28
0
0
0

13**
1.11
9.94**
3.33*

0
0
2.47
0

7.78
3.33
12
16.2

9.24
7.78
19.3
18.8

40.7
40.6
66.9**
66.1**

39.4
33.4
32.9
27.3

0
0
0
0

1.18
1.18
1.18
1.18

3
5
3
5

1.11
17.1**
6.67
7.57

0
2.22
2.22
2.22

15.6**
11.5
30.1**
14*

0
2.22
2.22
1.04

11.1
8.09
24.7
31.4

13.2
15.7
31.9
23

38.4
46.7
62
63.1

44.2
28.3
39.7
38.6

0
0
0
0

1.27
1.27
1.27
1.27

Late
4
6
(B) RA storage
Early
4
6
Late
4
6
a

Low temperature breakdown: soggy breakdown.

Cooling delay (days) (fruit not delayed cooled were stored at 5 C immediately following harvest).
c Each value was derived from 90 apples and was calculated as an average from measurements taken immediately following storage
removal and after 7 days at 20 C. All values, except ethylene, are in percentages. Control and 7 days means were separated by SASs
LSMeans procedure with statistically significant differences being indicated by (*) 0.05 < P < 0.10 or (**) P 0.05.
d Weight loss was measured following the initial 7-day treatment only. All weight loss percentages in CA and RA-stored fruit were
significant (P 0.05).
e Fruit not delayed cooled were stored at 5 C immediately following harvest.
b

For the fruit that were not delayed cooled, low temperature breakdown tended to be more severe in the
late-harvested apples (Table 1A and B). Honeycrisp
fruit exposed to a pre-storage delayed cooling period
appeared to respond as well in the CA as in the RA
environment (Table 1A and B). Thus, CA storage
appears to be a viable option for this cultivar. The incidence of other disorders such as bitter pit, senescent
breakdown, and fruit greasiness were not severe and
were not influenced by the delayed cooling period
(data not shown). Bitter pit, in particular, is a serious
post-storage disorder in most of the regions where
Honeycrisp is grown; however, it has not been a
problem in Nova Scotia to date.

Although rot incidence was not influenced by

delayed cooling, storage temperature or regime, it
increased in late-picked fruit (Table 1A and B). As
storage rot is a major problem for this cultivar (Greene
and Weis, 2001; Prange et al., unpublished data),
preharvest fungicidal sprays or a pre-storage fungicidal dip may be a necessary procedure for reducing
storage decay.
Ethylene evolution in delayed cooled Honeycrisp
fruit was lower than in non-treated apples following
CA storage in particular (Table 1A and B) suggesting a negative association between moisture loss and
the rate of cellular metabolism. Prange et al. (2001)
also observed a moisture loss associated decrease

J.M. DeLong et al. / Postharvest Biology and Technology 33 (2004) 175180

in respiration in McIntosh fruit following 4 and 8

months of CA storage; in their study, however, water
loss was facilitated by calcium chloride salt solutions
and not by a pre-storage delayed cooling period. Ironically, ethylene exposure has been shown to reduce
chilling injury in other fruits such as tomato (Hong
and Gross, 2000) and muskmelons (Lipton and
Aharoni, 1979), and reduces chilling-induced woolliness in peaches (Palou et al., 2003) and nectarines
by promoting ripening-related changes both during
and after storage (Dong et al., 2001). It may be that
fruit moisture loss concomitant with the potential increase in the ethylene generation that occurred during
the 7-day delayed cooling period synergistically contributed to reducing chilling injury in the Honeycrisp
fruit.
In conclusion, the delayed cooling treatment of 7
days at 20 C prior to storage at 3 or 5 C resulted in
marked or complete suppression of soft scald and low
temperature breakdown in early-and late-harvested
Honeycrisp fruit following 4 or 6 months of CA or
RA storage. Delayed cooling also decreased the rates
of ethylene evolution but did not affect the incidence
of storage rot. For regions in which soft scald and low
temperature breakdown cause significant economic
loss, delaying the cooling of fruit prior to the storage
appears to be a beneficial step in minimizing disorder
incidence.
Acknowledgements
The authors thank Conny Bishop for her technical
assistance and Dr. Nancy Nickerson and Mr. Doug
Nichols for reviewing this manuscript.

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