Chilling injury and residue uptake in cold-stored ‘Star
Ruby’ grapefruit following thiabendazole and imazalil dip
treatments at 20 and 50°C
M. Schirra
a,*, G. D’hallewin
a,1, P. Cabras
b, A. Angioni
b,
S. Ben-Yehoshua
c, S. Lurie
caC.N.R. Istituto per la Fisiologia della Maturazione e della Conser6azione del Frutto delle Specie Arboree Mediterranee,
Localita` Palloni,09170 Oristano, Italy
bDipartimento di Tossicologia,Uni6ersita` di Cagliari,6iale Diaz 182,09126 Cagliari, Italy cDepartment of Posthar6est Science of Fresh Produce,ARO,The Volcani Center,Bet Dagan 50250, Israel
Received 23 December 1999; accepted 8 May 2000
Abstract
‘Star Ruby’ grapefruit (Citrus paradisi Macf.) were harvested from November through June and subjected to a 3-min dip in water at room temperature (20°C) with or without 1200 or 200 mg/l imazalil (IMZ) or thiabendazole (TBZ) at 50°C. Fruit were then stored at 2°C and 90 – 95% relative humidity (RH) for 6 weeks and 1 additional week at 20°C and approximately 80% RH to simulate a marketing period (SMP). Fruit harvested in April and June and treated with 1200 mg/l TBZ at room temperature or with 200 mg/l at 50°C contained higher levels of TBZ residue than fruit picked in November and January. Fruit uptake of IMZ was not affected by harvest date. Within each date, conventional treatments with IMZ or TBZ fungicides at room temperature and treatment at 50°C produced similar levels of residues in most samples. Susceptibility to chilling injury (CI) was highest in fruit harvested in November and January, lower in April and negligible in June. Water dips at 50°C significantly reduced CI, the extent depending on harvest date and storage duration. The influence of 1200 mg/l IMZ dips at 20°C on CI control was not significant in most samples. Treatments with 200 mg/l IMZ at 50°C produced effects in CI control similar to that of water dips at 50°C. Beneficial effects were also achieved after treatment with 1200 mg/l TBZ at 20°C, although its efficacy in reducing CI was markedly improved with reduced doses (200 mg/l) at 50°C. © 2000 Elsevier Science B.V. All rights reserved.
Keywords:Citrus; Chilling injury; Decay; Heat treatments; Fungicide absorption; Storage; Weight loss
www.elsevier.com/locate/postharvbio
1. Introduction
The harvesting season of cv. ‘Star Ruby’ grape-fruit in Italy opens in November (early season), when most fruit have reached peel colour break-* Corresponding author.
E-mail address:[email protected] (M. Schirra).
1Permanent address: C.N.R. Istituto per la Fisiologia della
Maturazione e della Conservazione del Frutto delle Specie Arboree Mediterranee, Via dei Mille 07100 Sassari, Italy.
age, and closes in May – June (late season), when fruit may be affected by the Mediterranean fruit fly (MFF; Ceratitis capitata). Various citrus-im-porting countries require quarantine security against MFF, and low-temperature quarantine treatment (17 days storage at 52°C) is currently the protocol used as a non-chemical method to control insect infestation (Jatosti, 1997). However, ‘Star Ruby’ grapefruit are susceptible to low stor-age temperature, and quarantine conditions may cause chilling injury (CI). Postharvest heat treat-ments and certain fungicides such as thiabenda-zole (TBZ) and imazalil (IMZ) induce cold tolerance in CI-susceptible citrus fruit and posi-tive synergistic effects may occur in CI control when IMZ or TBZ are used in combination with hot water (McDonald et al., 1991). While treat-ments with 1200 mg/l TBZ at room temperature or 200 mg/l TBZ at 50°C produced similar fungi-cide uptake in ‘Tarocco’ oranges, the heated fun-gicide proved to be more effective in controlling CI (Schirra et al., 1998b).
The present study investigated the potential of IMZ in inducing low-temperature tolerance in ‘Star Ruby’ grapefruit with respect to TBZ when reduced doses (200 mg/l) of fungicides at 50°C were employed in comparison to the standard (1200 mg/l) room temperature treatments. Active-ingredient uptake and degradation rate following treatments were also determined so as to correlate fruit response to chilling temperature.
2. Materials and methods
2.1. Plant material
Red-fleshed grapefruit (Citrus paradisi Macf. cv. Star Ruby) were obtained from a single block of an experimental orchard located in southern Sardinia receiving standard horticultural care. Fruit were harvested at bimonthly intervals, from the last week of November (when fruit had not yet acquired the full orange colour, but were commercially mature), to June (overmature fruit). Each harvest involved a random sampling from 30 trees. Forty fruit were picked from the outside of the canopy of each tree, placed in plastic boxes,
delivered to the laboratory immediately after har-vest, and left overnight.
2.2. Treatments and storage conditions
Defect-free grapefruit were selected, numbered and grouped into six treatment lots (nine boxes containing 40 fruit each), corresponding to the following 3 min dip treatments: (I) water at 20°C (control fruit); (II) 1200 mg/l IMZ at 20°C; (III) 1200 mg/l TBZ at 20°C; (IV) water at 50°C; (V) 200 mg/l IMZ 50°C; (VI) 200 mg/l TBZ 50°C. IMZ and TBZ mixtures in water were prepared with commercially available Deccozil 50 (44.66% a.i., Janssen Pharmaceutica N.V. Belgium) and Tecto 20 S (22 g/l a.i., Merck Sharp and Dohme, Netherlands), respectively. Dip treatments were performed using an apparatus described by Schirra and D’hallewin (1997). Following treat-ment, fruit were left to dry at room temperature for approx. 5 h. Each treatment group was then divided into three subgroups. Fruit of the first subgroup included four replicate fruit boxes were used for assessment. This included: CI, rot inci-dence, treatment damage and external fruit qual-ity. Four replicate fruit boxes of the second subgroup were used for measurement of total soluble solids, titratable juice acidity and for fun-gicide analyses. Fruit in the remaining box were individually weighed for the determination of transpiration rate as fruit mass loss. Finally, fruit were moved to a storage room and kept at 2°C and 90 – 95% relative humidity (RH) for 6 weeks, with a complete air change every hour. These are conditions favourable to CI development in ‘Star Ruby’ grapefruit. At the end of storage, fruit were maintained at 20°C and about 80% RH for 1 week to simulate marketing period.
2.3. Fruit weight loss and 6isual assessment
rind surface, the damage was not objectionable and would not deter purchase by consumers, moderate, when darker brown spots and depres-sions covered up to 25% of the rind sur-face (some consumers might reject these fruit un-less they could be purchased at reduced prices), and severe when injury covered over 25% of the rind surface, and the fruit would therefore be rejected. The percentage of fruit in each rating was calculated. To obtain a weighted average for a CI index, the number of fruit in each CI rating was multiplied by the designated number and a weighted average was calculated using the fol-lowing formula: CIx=[(% of fruit with slight CI×1)+(% of fruit with moderate CI×2)+(% of fruit with severe CI×3)/100]. Decay incidence was assessed as total rots caused by blue mould (Penicillium italicum Wehmer), green mold (P. digitatum Sacc.), brown rot (Phytophtora cit -rophthora), sour rot (Geotrichum candidum) or as miscellaneous rots of unidentified fungi. Over-all visual quality was rated subjectively into one of five categories: 5 (excellent), 4 (good), 3 (fair), 2 (poor) and 1 (very poor), by an in-formal panel of people familiar with this cul-tivar.
2.4. Internal quality characteristics
Before storage and after SMP, three replicates of five healthy fruit were randomly selected for internal quality attributes. The juice was ex-tracted from individual fruit with a small labora-tory hand reamer (type MPZ2 AG, Braun, Frankfurt, Germany) and percentages of soluble solids content (SSC) and titratable acidity (TA) were determined.
2.5. Analysis of IMZ and TBZ
From each treatment group three fruit per replication were weighed; their peel was removed and weighed and its percentage with respect to the whole fruit was calculated. Samples of peel were then triturated with a mincing knife, ho-mogenized and stored in a freezer at −20°C until analysis. Extraction procedures, recovery assays, sample preparation, IMZ and TBZ
deter-mination were performed as described by Schirra et al. (1996, 1998a).
2.6. Statistical analysis
Analysis of variance (ANOVA) was performed by MSTAT-C software (1991). Mean compari-sons were performed by Tukey’s test at P50.05, where appropriate.
3. Results and discussion
The April – June harvested fruit treated with 1200 mg/l TBZ at room temperature contained more (about 2-fold) TBZ than fruit picked in November – January (Table 1). Differences in ac-tive-ingredient (a.i.) uptake vis a vis maturity stage when TBZ is applied at room temperature have been associated with the condition of the cuticular surface at harvest (Schirra et al., 1998b). The IMZ residue levels were less related to maturity stage. Within each harvest date, con-ventional treatments with IMZ or TBZ at room temperature and at 50°C produced similar levels of residues in most measurements, thus support-ing previous findsupport-ings (Cabras et al., 1999). Both fungicides exhibited great persistance during stor-age, especially IMZ, thus supporting previous re-sults (Cabras et al., 1999). The exception was that a hot dip with TBZ had lower residues at the end of storage and SMP than the conven-tional treatment in three out of four trials.
beneficial effects than water dips at 50°C alone. Positive results in CI control were achieved after treatment with 1200 mg/l TBZ at 20°C, support-ing previous results (Schiffman-Nadel et al., 1972, 1975). However, TBZ’s efficacy in reducing the development of CI was markedly improved with reduced doses (200 mg/l) at 50°C. Previous investigations have shown that postharvest treat-ments with TBZ and IMZ at 53°C were more effective in reducing CI in ‘Marsh’ (white-fles-hed) and ‘Redblush’ (red-fles(white-fles-hed) grapefruit dur-ing 6 weeks of storage at 5°C and 2 additional weeks at 20°C, in comparison with fungicides at 24°C or hot water alone (McDonald et al., 1991). However, this investigation was carried out on fruit from a single harvest in late season and comparisons between heated and unheated fungicides were performed by using equal active ingredient concentrations (1000 mg/l). Therefore, the increased efficacy of heated IMZ and TBZ may be explained by the higher residue uptake on fruit, due to the close relationship between treatment temperature and fungicide deposition (Cabras et al., 1999). From a regulatory stand-point, treatments with 1000 mg/l of TBZ and IMZ at 53°C may produce very high levels of
residues in fruit, well over the US limits (10 mg/kg for TBZ and 6 mg/kg for IMZ) as demonstrated by Schirra et al. (1996, 1998a) with lemons.
In the present study IMZ had no effect when applied at 20°C while at 50°C it appeared to be no more beneficial than hot water alone. There-fore, IMZ did not induce cold tolerance in ‘Star Ruby’ grapefruits stored at 2°C. By contrast, TBZ treatment was effective at 20°C, and even more so at 50°C, thus confirming its physiologi-cal effect in CI control, in addition to its anti-fungal activity, as previously reported by Schiffman-Nadel et al. (1972). TBZ’s efficacy in checking CI has been reported to increase with increasing fungicide concentrations and residues in fruit; its physiological effect has been at-tributed to a decreased rate of peel senescence (Schiffman-Nadel et al., 1975). It has also been stated that TBZ improves CI-control by acting indirectly to suppress latent infections that may develop when adverse ambient conditions, such as low-temperature storage, undermine fruit re-sistance to the point of inducing CI (Schiffman-Nadel et al., 1972). Accordingly, Wild and Hood (1989) suggested that the efficacy of hot dip
Table 1
Residues (whole fruit basis), of imazalil (IMZ) and thiabendazole (TBZ) in ‘Star Ruby’ grapefruit as affected by type of treatment, time in storage and picking date
Treatmentsx
Harvest date Storage duration (weeks)y
0 6+1 0 6+1
IMZ residue (mg/kg)z TBZ residue (mg/kg)z
1200 mg/l, 20°C 4.5a(a) 2.6b(b) 1.6a(a) 1.4a(a)
November
200 mg/l, 50°C 4.7a(a) 4.6a(a) 2.0a(a) 0.5b(b)
1.9a(a) 1.1a(b) 3.0b(a)
January 1200 mg/l, 20°C 2.3a(b)
1.2b(a) 0.8b(a)
April 1200 mg/l, 20°C 4.4a(a)
2.5a(b) 200 mg/l, 50°C 3.9a(a) 3.7a(a) 3.8a(a)
1200 mg/l, 20°C 5.0a(a)
June 4.8a(a) 3.5a(a) 3.2a(a)
2.5a(a) 3.9a(a)
4.9a(a)
200 mg/l, 50°C 1.4b(a)
xTreatments were 3 min dips followed by air drying of dipped fruit. y0=following treatment; 6+1=6 weeks at 2°C+1 week at 20°C.
zIn each row or column grouping, means separation by Tukey’s range test, P50.05. Letters without parentheses relate to
Table 2
Influence of harvest date and postharvest dip treatments on chilling injury index in ‘Star Ruby’ grapefruits after 3 and 6 weeks of storage at 2°C and then after an additional week at 20°C
Picking date
1200 mg/l IMZ 20°C 1.5a(a) 1.3b(a) 0.0a(b) 0.0a(b)
0.2d(b) 0.0a(c)
0.3b(a) 0.0a(c)
1200 mg/l TBZ 20°C
H2O 50°C 0.5b(b) 0.7c(a) 0.0a(c) 0.0a(c)
0.3d(b) 0.0a(c)
0.3b(a) 0.0a(c)
200 mg/l IMZ 50°C
200 mg/l TBZ 50°C 0.4b(a) 0.1d(b) 0.0a(c) 0.0a(c)
6weeks at2°Cy
2.5a(a) 1.7a(ab) 0.4a(b)
H2O 20°C 2.6a(a)
2.5a(a) 1.7a(b)
2.7a(a) 0.5a(c)
1200 mg/l IMZ 20°C
0.8c(b) 0.5b(c)
1200 mg/l TBZ 20°C 1.6b(a) 0.1b(d)
1.7b(a) 0.1c(b)
1.9b(a) 0.0b(b)
H2O 50°C
200 mg/l IMZ 50°C 1.7b(a) 1.5b(a) 0.1c(b) 0.0b(b)
0.4c(b) 0.0c(c) 0.0b(c)
1.0c(a) 200 mg/l TBZ 50°C
6weeks at2°C+1week at20°Cy
H2O 20°C 2.7a(a) 2.7a(a) 2.4a(a) 0.4b(b)
2.5a(ab) 2.3a(b)
2.8a(a) 0.8a(c)
1200 mg/l IMZ 20°C
1200 mg/l TBZ 20°C 1.9b(a) 1.0c(b) 1.6b(ab) 0.1cd(c)
2.0ab(a) 0.5c(b)
2.2b(a) 0.2c(c)
H2O 50°C
1.8b(a) 0.2cd(b)
200 mg/l IMZ 50°C 2.1b(a) 0.1cd(b)
0.9c(a) 0.1d(b)
1.2c(a) 0.0d(b)
200 mg/l TBZ 50°C
xTreatments were 3 min dips followed by air drying of dipped fruit.
yIn each row or column grouping, means separation by Tukey’s range test, P
50.05. Letters without parentheses relate to comparisons of the effect of different treatments, within each harvest date. Letters in parentheses relate to comparisons of the influence of different harvest dates, within each treatment.
treatments in CI control of citrus fruit may be the result of physiological changes in the rind or inactivation of latent infections such as Col -letotrichum gloeosporioides which could weaken cell walls and make fruit more prone to CI. Nonetheless, in our environmental growing condi-tions, C. gloeosporioides decay may occur only occasionally, and in the present study no infec-tions due to this fungi were observed, either dur-ing storage or in subsequent SMP. Recent studies have demonstrated that CI susceptibility of har-vested citrus fruit is related to the efficiency of antioxidant enzyme systems in flavedo tissue, which undergo alterations especially in catalase activity (Sala, 1998), and that heat treatment in-duces CI tolerance (Sala and Lafuente, 1999). The present findings suggest that TBZ’s induction of
CI-control in ‘Star Ruby’ grapefruits is not only related to its fungicidal properties, as postulated by Schiffman-Nadel et al. (1975). TBZ’s CI-resis-tance may also be related to its antioxidant prop-erties (Langcake et al., 1983; Zbozinek, 1984) (e.g. via s-oxidation of thiazole ring as sulphoxide as well as sulphone) which, ultimately, may affect the flavedo tissue’s antioxidant enzyme systems, with TBZ inducing in the latter case an action similar to that of heat treatment. Such an effect might also explain the positive synergistic action of the combined hot water – TBZ treatment in checking CI. Specific studies are underway in our laboratories to elucidate this point.
occurred in fruit harvested later. The high rotting in control fruit for the June harvest, mainly brown rot, sour rot and, to a lesser extent Peni -cillium spp., was caused by the prolonged warm, rainy spell in late spring, as well as by the dimin-ished natural resistance to decay of physiologi-cally older fruit (Ben-Yehoshua et al., 1992). Hot water treatment reduced decay in fruit harvested in April but had no significant effect on fruit harvested in June. Fungicide treatments at 20 or 50°C significantly reduced decay development in fruit harvested in April – June. The relatively high incidence of decay in fruit subjected to IMZ dips at 50°C (about 17%) with respect to the other fungicide treatments (3 – 9%) was due to the lack of efficacy of IMZ in suppression of predomi-nant fungi, brown and sour rot which accounted for approximately 80% of total decay (data not shown).
Fruit weight loss was higher in November – February, with a decline at the June harvest (Table 4); differences due to treatment were not significant. Fruit weight loss has been related to the expression of CI in susceptible citrus cul-tivars (Purvis, 1984), and such factors as
treat-ment type and storage condition that reduce fruit water loss also alleviate CI (Purvis, 1985). In the present study, CI-susceptibility was related to fruit weight loss since both decreased through-out the season. Other factors, however, may be involved in the expression of CI since hot water treatments with or without IMZ or TBZ reduced CI development to varying extents but did not reduce the rate of water loss. Previous in-vestigations have shown that hot water dipping reduced CI in ‘Fortune’ mandarins (Schirra and D’hallewin, 1997) and ‘Tarocco’ oranges (Schirra et al., 1998b) while augmenting fruit weight loss.
The external appearance of untreated and treated fruit free of CI and decay after 6 weeks’ storage was judged to be good. Although fruit appearance showed signs of decline at the end of SMP, it remained still good (data not reported). No treatment-dependent differences were found in TA and SSC (data not reported).
4. Conclusions
Data found in the present study provide evi-dence that: (a) fungicide treatments led to no adverse effects on the peel, even when applied at 50°C; (b) the expression of CI in ‘Star Ruby’ grapefruit was maximum when susceptibility to decay was minimum; (c) postharvest treatment with 1200 mg/l IMZ at room temperature nota-bly suppressed decay, but did not alleviate CI; (d) treatments with 200 mg/l IMZ dips produced beneficial effects similar to those of water dips at 50°C in reducing CI, but IMZ was more effective than hot water alone in decay control and (e) treatment with 1200 mg/l TBZ at room tempera-ture or 200 mg/l TBZ at 50°C produced similar residue levels in fruit, but lower doses of heated fungicide proved to be more effective in reducing CI.
Acknowledgements
This research was funded by European Union FAIR CT-4096.
Table 3
Influence of harvest date and postharvest dip treatments on decay percentage in ‘Star Ruby’ grapefruits after 6 weeks of storage at 2°C plus 1 additional week at 20°C
Picking datey
xTreatments were 3 min dips followed by air drying of
dipped fruit.
yIn each column grouping, means separation by Tukey’s
Table 4
Influence of harvest date and postharvest dip treatments on fruit weight loss (%) of ‘Star Ruby’ grapefruits after 2, 4 and 6 weeks at 2°C and subsequent 1 week at 20°C
Treatmentsx Picking datey
February April
1200 mg/l IMZ 20°C 1.4a(b) 1.5ab(a) 0.8a(c)
1.8a(a)
1200 mg/l TBZ 20°C 1.7a(a) 1.3bc(b) 0.9a(c)
1.6a(a) 1.5ab(a)
1.7a(a) 0.9a(b)
H2O 50°C
1.7a(a)
200 mg/l IMZ 50°C 1.6a(a) 1.2c(b) 0.8a(c)
1.4a(a) 1.2c(b) 0.8a(c)
1.7a(a) 200 mg/l TBZ 50°C
4weeks at2°C
H2O 20°C 2.9a(a) 3.1a(a) 2.8a(a) 1.5a(b)
2.5b(a) 2.7a(a)
2.8a(a) 1.3a(b)
1200 mg/l IMZ 20°C
3.1a(a) 2.4ab(b)
1200 mg/l TBZ 20°C 2.8ba(a) 1.5c(a)
3.0a(a) 2.7a(a)
2.6a(a) 1.5a(b)
H2O 50°C
3.1a(a) 2.1b(b) 1.3a(c)
200 mg/l IMZ 50°C 2.8a(a)
2.8ab(a) 2.2b(b) 1.4a(c)
2.7a(a) 200 mg/l TBZ 50°C
6weeks at2°C
H2O 20°C 4.3a(a) 4.3ab(a) 4.0a(a) 2.4a(b)
3.4b(b) 3.8ab(b)
4.2a(a) 1.6c(c)
1200 mg/l IMZ 20°C
4.3a(a)
1200 mg/l TBZ 20°C 4.4a(a) 3.5abc(b) 1.8bc(c)
4.1a(a)
H2O 50°C 4.2ab(a) 3.9a(a) 2.0b(b)
4.3ab(a) 2.9c(b)
4.5a(a) 1.9bc(c)
200 mg/l IMZ 50°C
200 mg/l TBZ 50°C 4.2a(a) 4.0ab(a) 3.2bc(b) 1.9bc(c)
6weeks at2°C+1week at20°C
H2O 20°C 6.7a(a) 6.7a(a) 5.3a(b) 4.7a(b)
1200 mg/l IMZ 20°C 6.9a(a) 5.4b(b) 5.1ab(b) 4.0a(c)
6.9a(a) 4.7abc(b)
6.7a(a) 4.3a(b)
1200 mg/l TBZ 20°C
H2O 50°C 6.7a(a) 6.9a(a) 5.3a(bc) 4.3a(c)
6.9a(a) 4.0c(b)
6.8a(a) 4.0a(b)
200 mg/l IMZ 50°C
6.9a(a)
200 mg/l TBZ 50°C 6.5ab(a) 4.2bc(b) 4.2a(b)
xTreatments were 3 min dips followed by air drying of dipped fruit.
yIn each row or column grouping, means separation by Tukey’s range test, P50.05. Letters without parentheses relate to
comparisons of the effect of different treatments, within each harvest date. Letters in parentheses relate to comparisons of the influence of different harvest dates, within each treatment.
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