Postharvest Biology and Technology 25 (2002) 15 24 www.elsevier.

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Effect of post-ripening nitrogen atmosphere storage on banana shelf life, visual appearance and aroma
A. Klieber *, N. Bagnato, R. Barrett, M. Sedgley
Department of Horticulture, Viticulture and Oenology, Adelaide Uni6ersity, Waite Campus, Plant Research Centre, PMB 1, Glen Osmond, SA 5064, Australia Received 21 February 2001; accepted 21 August 2001

Abstract Bananas (Musa acuminata Colla, Cavendish cv. Williams) were stored in nitrogen at 22 C for 6, 12 and 24 h at a more green than yellow (stage 3) or more yellow than green (stage 4) ripening stage. Shelf life in nitrogen at 22 C, that is the time taken from a more yellow than green colour stage 4 to yellow with slight brown ecking stage 7, was not extended when compared to air-stored bananas. However, areas of brown discolouration appeared on bananas placed in nitrogen-storage. The aroma of ripe bananas was assessed with a mass spectrometry-based chemical nose. Bananas stored in nitrogen generally had a riper aroma prole compared with air-storage. An ion with a mass to charge ratio of 61 was strongly associated with nitrogen-treated bananas; this ion is a decomposition product of a known banana aroma compound, ethyl acetate that produces an over-ripe banana note. An ion with a mass to charge ratio of 55 was associated with air-stored bananas; this ion is a decomposition product of ripe bananas (3-methylbutyl ester and 1-butanol). Post-climacteric nitrogen storage is not a suitable method for increasing shelf life, as it causes skin browning. 2002 Elsevier Science B.V. All rights reserved.
Keywords: Nitrogen storage; Bananas; Shelf life; Chemical nose; Aroma

1. Introduction A consumer product survey prepared for the Australian Banana Growers Council (1999) found that if bananas had a longer shelf life than the current 3 days, Australians would be likely to purchase more of these fruit. Currently, Aus* Corresponding author. Tel.: + 61-8-8303-6653; fax: + 618-8303-7116. E -mail address: andreas.klieber@adelaide.edu.au (A. Klieber).

tralians consume over 15 kg of bananas per capita per annum (Australian Banana Growers Council, 1999). The short shelf life is due to a rapid senescence process that causes the visual appearances of the fruit peel to degrade from yellow to a muddy brown colour terminating banana shelf life. Wholesalers want to extend the banana shelf life between ripening stage 4 (more yellow than green) and 7 (yellow with light brown ecks) (CSIRO, 1972) to increase appeal to consumers to gain higher purchase quantities at one shopping occasion.

0925-5214/02/$ - see front matter 2002 Elsevier Science B.V. All rights reserved. PII: S 0 9 2 5 - 5 2 1 4 ( 0 1 ) 0 0 1 6 3 - 6

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Currently, ripened bananas are pre-cooled to 13 C before their distribution to supermarkets (T. Johnson, Chiquita Brands South Pacic, pers. commun., 2000), to slow down fruit metabolism and therefore prolong senescence (Rippon and Trochoulias, 1976). However, this is costly, and fruit rewarm rapidly on the display shelves, thereby reducing shelf life. Most research has focused on ways to extend the green life of unripe fruit. Modied atmosphere packaging has been suggested as a substitute for low temperature storage (Scott et al., 1970); however, this storage is costly as it involves labour as well as ethylene absorbent packaging and also requires careful handling to prevent damage to bags and loss of the modied atmosphere. Wills et al. (1990) successfully used short-term nitrogen treatments to increase the green life (from harvest to yellow with green tips) of bananas, with nitrogen atmospheres of 3-day duration applied immediately after harvest increasing their green life by 42%. Nitrogen atmospheres are inexpensive and easy to apply to large quantities of fruit. A nitrogen atmosphere will reduce the level of oxygen available to the fruit, which in turn will inhibit ethylene production and ripening (Thompson, 1998). A method is required for slowing the rate of senescence of ripening bananas to extend their shelf life from the point of sale to consumption. The aim of this study was to examine whether storing fruit temporarily in nitrogen atmospheres after partial ripening could extend the shelf life of bananas without affecting their appearance or aroma.

vest. All hands were harvested from plants within a single block. Only hands from the middle of the bunch were used, to ensure an even maturity of fruit. At arrival all fruit were still green and hard. Once delivered, the bananas were dehanded and dipped for 1 min in fungicide (0.55 ml/l Sportak, Hoechst Schering AgrEvo, Glen Iris, Vic.) and allowed to air dry. Matched ngers were then randomly allocated to treatment groups. A treatment unit consisted of 12 fruit, six of which were used to assess external characteristics of the fruit and the remaining six were used to assess internal properties of the bananas. Bananas were ripened in 10-l plastic containers in the presence of a CO2 scavenger (160 g of Ca(OH)2) ensuring a 0% CO2 level, and a 95% relative humidity was maintained using a saturated KNO3 solution. All fruit were ripened according to common industry practice to ripening stage 3 (more green than yellow) or 4 (more yellow than green) at 16 C with 300 ml/l ethylene gas on the rst two consecutive days of ripening (T. Johnson, Chiquita Brands South Pacic, pers. commun., 2000).

2.2. Nitrogen application for 6arious periods of time at different ripening stages
After initiation of ripening, bananas were stored in a nitrogen atmosphere at ripening stage 3 or 4. Storage periods were 0, 6, 12 or 24 h. The two control (no nitrogen) treatments were stored in vented polyethylene bags at 22 C once the appropriate ripening stage had been reached at 16 C. Treated bananas were placed in containers that were ushed with high purity nitrogen (BOC gases, Adelaide) for 5 min, before being sealed for the allotted treatment periods of 6, 12 or 24 h. Atmosphere samples were taken from sealed containers and analysed using a thermal conductivity detector gas chromatograph (Varian 3300, Walnut Creek, CA) to ensure O2 and CO2 levels were B 1 and 0%, respectively (Wills et al., 1990). On completion of treatments, fruit were placed in vented polyethylene bags at 22 C to complete ripening under simulated retail marketing conditions.

2. Materials and methods

2.1. Plant material and preparation

Chiquita Brands South Pacic Ltd. Pty. supplied Cavendish bananas cv. Williams used for this study. Fruit were harvested during the months of June and July 2000 in the Cairns region of north Queensland and transported at 13 C to the Plant Research Centre (Waite Campus, Adelaide University) within 3 days of har-

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2.3. Nitrogen atmosphere storage in the presence of low or high relati6e humidity
A second nitrogen atmosphere experiment was performed to observe whether humidity stress was a factor in the results obtained from the previous experiment. Bananas were ripened to stage 4 as above and held in nitrogen for 0 or 24 h without humidity control. In addition, a similar lot of bananas was held in nitrogen for 24 h in the presence of a saturated KNO3 solution (95% RH). The atmospheric composition was again monitored. After nitrogen treatment, bananas were removed from storage containers and placed in polyethylene bags. To regulate humidity, fruit were held in the presence or absence of a beaker of water in the unsealed bags. Airstored fruit were stored in closed bags that were folded under the bananas without a beaker of water. The relative humidity inside polyethylene bags was measured using a hand-held humidity probe (HM34C, Vaisala, Helsinki) as ] 95% RH for high (beakers of water present) or 5 75% RH for low humidity treatments.

DI =

(a 0) + (b 1) + (c 2) + (d 3) n

(1)

where a is the number of fruit with no discolouration, b the number of fruit with slight discolouration, c the number of fruit with mild discolouration, d the number of fruit with severe discolouration, and n the total number of fruit observed.

2.4. Assessments of bananas 2.4.1. External assessments All bananas were weighed at ripening stage 1 and at ripening stage 6 to determine the percent weight loss. In addition, shelf life was determined by observing banana peel colour changes as determined by the CSIRO Banana Ripening Chart (CSIRO, 1972) and calculating the number of days it took for the peel to change from ripening stage 4 (more yellow than green) to ripening stage 7 (yellow with light brown ecks), excluding treatment periods. Discolouration of the banana peel was observed at ripening stage 6 (fully yellow). The discolouration severity scale used consisted of 0, no discolouration; 1, slightly discoloured; 2, mildly discoloured; 3, severely discoloured. As fruit from a given treatment displayed similar symptoms, scores were weighted and averaged into an O2 injury discolouration index (DI) for each treatment, using a formula modied from Schirra et al. (1999):

2.4.2. Internal fruit assessments Pulp rmness is a measure of the crushing strength of pulp tissue and was measured using a twist tester (Department of Agricultural Engineering Massey University, NZ) as described by Harker et al. (1996). This method is destructive to fruit tissue; however, it is very easy to use and gives reliable results when used on soft tissue, unlike a hand-held penetrometer (Studman and Yuwana, 1992). The penetrometers action compresses the esh against esh within the fruit, whereas the twist tester rotates the esh within a single tissue layer allowing for differences in textural characteristics within that layer to be measured (Griessel and Crouch, 1996). Soluble solid concentrations (SSC) were also measured on pulp tissue using a conventional refractometer (0 30% sugar w/w, Bellingham and Stanley Ltd., UK). A sample from the middle of the banana was squeezed through muslin cloth onto the refractometer glass, and the SSC (%) recorded after calibration to room temperature. Aroma was measured using a mass spectrometry-based chemical nose, to determine whether there were any characteristic aroma differences. Pulp (20 30 g) from each of the internal assessment bananas from a single treatment was combined and pureed for 6 s in a blender. For each treatment 10 20-ml headspace vials were then lled with 5 g of the puree and 5 ml of heptadecane (an internal standard) was added to the vial. The vials were immediately sealed and randomly allocated to the Hewlett Packard Chemical Sensor (HP440, Wilmington, DE), which consists of a modied HP 7694 headspace auto sampler and a mass sensor based on a HP 5973 MSD. Parameters for the chemical sensor were set as by Muchui (2000).

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2.5. Statistical analysis

The rst experiment was designed as a 4 2 factorial randomised complete block with three replicates. Treatments included the effect of 0 (air-storage), 6, 12 or 24 h of nitrogen storage when applied to bananas at ripening stage 3 (more green than yellow) or 4 (more yellow than green). Harvests on three consecutive weeks were replicates and bananas were randomly allocated to all treatments. The second experiment was established in a randomised complete block design with three replicates and a single treatment factor. Each replicate consisted of the following nitrogen-storage treatments, 0 (air-storage), 24 h with a high humidity or 24 h with a low humidity during shelf life assessment. All experimental units were randomly distributed to treatments. Analysis of most data (shelf life, SSC, rmness and discolouration) was conducted using the General ANOVA directive in Genstat 5 (Release 4.1, 4th edn., 1998, Lawes Agricultural Trust, Rothamsted Experimental Station, UK). Shelf life data for the rst experiment were transformed for statistical analysis by squaring, but were converted to the original units for presentation in Table 1. Treatment effects were examined for signicance using a least signicant difference test (LSD) at the 5% level.

Finally, data on aroma were analysed using standard principal component analysis (PCA) (Wirthensohn et al., 1999) using the Pirouette analysis package (Infometrix Inc., Woodenville, WA, USA). Each model was validated using a cross-validation method, which indicated the principal components that accounted for more than 80% of the variation. Fruit with similar volatile compounds were grouped and separated on plots from fruit with different volatile patterns.

3. Results

3.1. Nitrogen application for 6arious periods of time at different ripening stages
Shelf life and SSC readings were similar in bananas stored in nitrogen atmospheres at ripening stages 3 or 4 for 6, 12 or 24 h and in bananas stored in air (Table 1). The amount of surface discolouration observed on banana peels varied signicantly among nitrogen atmosphere treatments applied, but increased in severity with longer exposure. No surface discolouration was observed on air-stored bananas; however, brown streaking developed along the vascular tissues in the peel of air-stored fruit. This discolouration is a symptom of mild in-eld or postharvest chilling injury. The injury from nitrogen treatments was

Table 1 Assessment of Cavendish bananas cv. Williams at ripening stage 6, after being stored in a nitrogen atmosphere for 0, 6, 12 or 24 h at ripening stage 3 or 4 at 22 C Banana assessment Ripening stage and period of time (h) for which bananas were stored in nitrogen atmosphere Ripening stage 3 0 Shelf life (days)a Firmness (kPa)b SSC (%) Weight loss (%) Discolour. index 7.4a 23.6a 2.0a 0.0a 6 7.4a 101a 23.0a 2.0ab 1.4b 23.2a 2.1bc 2.0c 23.3a 2.2c 2.7d 23.2a 2.1ab 0.0a 12 6.7a 24 7.3a Ripening stage 4 0 7.3a 6 7.6a 12 24 7.6a 23.1a 2.1bc 2.8d

7.2a 104b 23.5a 23.3a 2.1ab 2.0ab 1.4b 1.9c

Data are averages of three replicates and different letters within a row denote signicant differences at PB0.05 using a LSD test. a Average shelf life (days) data have been back-transformed from squared analysis data. b Only ripening stages are signicant at the 5% level, therefore the average rmness of bananas stored at ripening stages 3 or 4 were the only averages given.

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Fig. 1. The score plot of bananas stored in nitrogen for 0 h (air) at stage 3 or 4 (A, B) at stage 3 for 6, 12, 24 h (C, D, E) or at stage 4 for 6, 12 or 24 h (F, G, H).

different, resulting in large patches of brown discolouration similar to that found on fruit affected by low O2 injury (Wills et al., 1990; Thompson, 1998). The pulp of bananas removed from fruit at ripening stage 3 was softer than pulp of fruit at ripening stage 4. Nitrogen storage also had a signicant effect on weight loss of bananas stored at stage 3, with longer periods of nitrogen storage resulting in higher weight loss. However, this was not observed in fruit removed at colour stage 4 (Table 1). Fruit analysed at ripening stage 6 after storage in air or nitrogen for various periods had different aroma characteristics. The PCA models built to compare mass spectrometric chemical nose data of all nitrogen-stored as well as air-stored bananas explained 91% of the total variance present with two factors, of which 85% was related to Factor 1 only. Score plots with the two factor components showed discrimination between most nitrogen-stored samples and air-stored fruit (Fig. 1). However, some nitrogen-treated fruit, particularly those stored for 6 or 12 h, were found to

have a mixed aroma. Comparing the plot of the mass to charge ratios of the ions (variables) that contributed to this discrimination (Fig. 2) to the score plot (Fig. 1), it is clear that ion 55 strongly correlated to air-stored bananas, while nitrogenstored fruit mainly correlated to ion 61.

3.2. Nitrogen atmosphere storage in the presence of low or high relati6e humidity
Nitrogen storage with high or low humidity did not have a signicant effect on banana shelf life, pulp rmness, SSC or weight loss. Air-stored bananas did not develop skin browning, but were a dull yellow peel colour at stage 6. Skin discolouration was similar in bananas stored in low or high relative humidity (Table 2). The PCA model explained 87% of the total variance among treatments with two factors (Fig. 3). Factor 1 consists of 57% of the total variance with distinct discriminating aroma groupings, with one cluster containing bananas stored in air as well as those stored in nitrogen with a low humidity, and the other cluster consisting of ba-

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nanas stored in nitrogen with a high humidity. The clusters containing air-stored bananas and nitrogen-stored bananas in a low humidity were closely associated with ion 56 (Fig. 4). Aromas from nitrogen-stored bananas in a high humidity clustered around ions 70 and 55. Factor 2 consisted of 30% of the total variance. Bananas stored in nitrogen in a high or low humidity were related to ion 61 and 55, whereas air-stored bananas were generally only associated with ion 55 (Fig. 4).

4. Discussion Post-climacteric, short-term nitrogen storage did not extend banana shelf life and therefore further research into post-ripening treatments to extend shelf life is required. Liu (1976a,b) also found that bananas that were initiated with ethylene and then stored in a 1% O2 atmosphere at 14 C ripened soon after being transferred to air at 21 C. This means that any reduced O2 atmosphere effect is only transient once ripening of bananas has been initiated. In contrast, the green

life of bananas could be extended by short-term low O2 treatments (Wills et al., 1990). Increased ethanol and acetaldehyde contents were found in bananas after exposure to ethylene, and during subsequent continuous low O2 exposure, fruit accumulated more ethanol and ripening ceased (Imahori et al., 1998). Transient changes were also found after short-term low O2 exposure of ripening tomatoes (Klieber et al., 1996), where it induced transient increases in ethanol and acetaldehyde content; however, in that case the ripening period was extended. Therefore, there appear to be differences in response to low O2 stress based on species, severity of low O2 stress and ripeness during application. However, increasing the severity of short-term low O2 treatments is not an option, as nitrogen treatment in this study caused dark discolouration on the peel of fruit. Similar discolouration has previously been observed by Wei and Thompson (1993) on bananas stored between 5 and 14% CO2. Thompson (1998) reported that exposure of bananas to B 1% O2 for an unspecied period causes low O2 injury in the form of a dull yellow or brown peel discolouration, failure to ripen and

Fig. 2. The loadings plot of ions (value = mass to charge ratio) stored in nitrogen at stage 3 or 4 for 0, 6, 12 or 24 h. Extreme positions correlate with similar positioning of treatments on the score plot (Fig. 1).

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Table 2 Assessment of Cavendish bananas cv. Williams at ripening stage 6, after being stored in air, nitrogen atmosphere for 24 h with a beaker of water or without a beaker of water at 22 C Banana assessment at ripening stage 6 Storage of bananas at ripening stage 4 Control (air) 24 h N2 storage+water (95% RH) 8.0a 103.0a 23.4a 2.0a 1.1b 24 h N2 storagewater (575% RH) 7.4a 102.0a 24.0a 1.8a 1.4b

Shelf life (days) Firmness (kPa) SSC (%) Weight loss (%) Discolour. index

7.0a 104.0a 24.2a 1.7a 0.0a

Data are averages of three replicates and different letters within a row denote signicant differences at PB0.05 using a LSD test.

off aromas. Wills et al. (1990) also found some discolouration in nitrogen-treated green fruit. This brown peel discolouration was observed during assessment of bananas that had been stored in nitrogen for 6 h, and severity increased progressively as the storage period in nitrogen increased. A dull peel colour was also observed in the controls in the second experiment that was conducted during winter. The injury is related to slight in-eld chilling injury (Marriott, 1980; Turner, 1997), since fruit were not chilled after harvest. Even though there were statistically signicant differences in pulp rmness among bananas stored in nitrogen atmospheres at ripening stage 3 and 4, these differences would probably not be detected by consumers. The largest difference observed was less than 2% of readings, with all bananas being eating soft. The chemical nose was a simple and reliable method for repeated aroma analyses as opposed to human nose detection, which tends to be tedious for human judges (Muchui, 2000). The aroma of most of the bananas exposed to nitrogen atmospheres for the various periods of time was different to the aroma of control bananas stored in air (Fig. 1). The mass to charge ratios of the ions (variables) that were most important in the discrimination between banana aromas had high absolute loading values, and these relate to more extreme positions of groups on score plots (Fig. 2). Therefore, bananas stored in

air were strongly correlated with an ion with a mass to charge ratio of 55, which arise from the known banana aroma compounds 3-methylbutyl ester and 1-butanol that relate to the aroma of fully ripe bananas (Marriott, 1980). Pulp from bananas that were stored in nitrogen were mainly correlated with an ion with a mass to charge ratio of 61, which arises from ethyl acetate, a banana aroma compound that has an over-ripe aroma character. Therefore, the treatments in Fig. 1 that clustered in between the extremes of ion 55 and ion 61 had a mixed aroma of over-ripe and ripe tones. The presence of ethyl acetate in nitrogen-stored bananas at colour stage 6 may have been due to anaerobic conditions, because production of ethyl acetate in bananas generally only occurs in late senescence or when bananas are considered inedible (Macku and Jennings, 1987). The initiation of anaerobic respiration in tissues and the triggering of fermentation reactions, leads to the production of off-odours in fruit (Wills et al., 1998), like the over-ripe aroma identied in this study. Storage time in anaerobic conditions would have inuenced the production of over-ripe aromas, and this would account for the mixed aromas produced by some nitrogen-stored fruit. Even though the aroma results were obtained for bananas at colour stage 6, the nitrogen atmosphere treatment may have triggered a stress response resulting in an increased production of over-ripe aroma compounds.

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The second experiment had more variable aroma results. The clusters containing air-stored bananas and nitrogen-stored bananas in a low humidity were closely associated with the ion with a mass to charge ratio of 56 (Figs. 3 and 4), which is the known banana compound 1-hexanol that gives an unripe green tone. Aromas from nitrogen-stored bananas in a high humidity clustered around the ion with a mass to charge of 70 that is largely associated with ripe aroma proles and compounds like 3-methylbutyl ester, 1-butanol and propanoic acid; these volatile compounds are also strongly correlated with ion 55. Losses in aroma volatiles have been reported in climacteric fruit when stored in low relative humidity (Grierson and Wardowski, 1978), so unripe aromas mentioned previously are likely to be due to water stress preventing the total production of ripe aromas expected for fully ripe fruit. Over-ripe volatiles were associated with bananas stored in nitrogen in a high or low humidity and this was related to anaerobic respiration

inducing the production of alternative aroma compounds. The production of over-ripe volatiles by fruit at colour stage 6, instead of by fruit at colour stage 7 when these volatiles are generally expected, suggests that an off-odour may have formed as a result of nitrogen-storage and the stress it caused.

5. Conclusion Post-ripening storage in a nitrogen atmosphere prior to commercial marketing of bananas did not extend shelf life. This treatment caused skin browning without delaying ripening or senescence. Although differences in aroma compounds were found among air-stored and nitrogen-stored bananas when fully ripe, these differences did not necessarily have an adverse effect on avour. It was concluded that storage in a nitrogen atmosphere is not an effective method for extending the shelf life of ripening bananas.

Fig. 3. The score plot of bananas stored in (A) nitrogen for 0 h (air), (B) 24 h with a low humidity or for (C) 24 h with a high humidity.

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Fig. 4. The loadings plot of ions (value = mass to charge ratio) stored in nitrogen for 0 h (air), 24 h with a low humidity or for 24 h with a high humidity. Extreme positions correlate with similar positioning of treatments on the score plot (Fig. 3).

Acknowledgements The authors wish to thank Chiquita Brands South Pacic and afliates for their constant support and supply of produce. Thanks also to the Postharvest Department of the South Australian Research and Development Institute for the use of their twist tester.

References
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