Control of postharvest decay of citrus fruit with calcium polysulfide
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1 Postharvest Biology and Technology 21 (2001) Control of postharvest decay of citrus fruit with calcium polysulfide J.L. Smilanick a, *, D. Sorenson b a USDA-ARS, Horticultural Crops Research Laboratory, 2021 South Peach A enue, Fresno, CA 93727, USA b Sunkist Growers, Technical Ser ices, 222 W. Lindmore Street, Lindsay, CA 93247, USA Received 3 April 2000; accepted 24 June 2000 Abstract Incidence of green mold of citrus, caused by Penicillium digitatum, was reduced by 80% or more by the immersion of lemons or oranges for 1 4 min in warm ( C) liquid lime-sulfur (LLS) solution that contained 0.75% (wt vol 1 ) calcium polysulfide. The incidence of sour rot, caused by Geotrichum citri-aurantii, was reduced 35 70% by this treatment. LLS was similar in effectiveness to other treatments employed to control postharvest decay. Effectiveness was higher on lemons than oranges, and on green compared to yellow lemons. LLS did not stop sporulation, a benefit now obtained with some fungicides. The sulfide content of oranges, lemons, and grapefruit after LLS treatment was 31.9, 33.1, and 36.3 g g 1, respectively. Rigorous cleaning of fruit with water applied at high pressure after LLS treatment slightly improved LLS efficacy; conversely, similar cleaning reduces the efficacy of sodium carbonate or borax boric acid solutions now in use. The risk of injury to fruit by LLS was low. Fruit of one lemon and five navel orange cultivars were not visibly injured after LLS treatment for 3 min at 40.6 C followed by storage for 7 weeks at 10 C. After LLS treatment at 48.9 C, 5 C higher than needed for effective LLS use, only Lisbon lemons and Bonanza navel oranges were slightly injured. Sulfide concentration in LLS solution declined at a rate of about 7% every 24 h, this rate was similar between 25 and 65 C, and it was accompanied by the appearance of resistant deposits on the equipment. Additional losses would occur when some LLS solution is carried on fruit out of the tank. Although H 2 S in the air above LLS solution in pilot tests was less than 1 l l 1 and below the worker safety threshold of 10 l l 1, LLS solution has an odor of H 2 S that can be a nuisance to workers. The disposal of used LLS solutions is more readily accomplished than other tank treatments whose disposal can be difficult because they contain synthetic fungicides, are caustic, or have a high salt concentration. Because LLS improves water penetration in soils and is commonly used for this purpose, in many locations it can be disposed of by application to agricultural soils. Published by Elsevier Science B.V. Keywords: Penicillium digitatum; Green mold; Geotrichum citri-auranti; Geotrichum candidum; Sour rot; Liquid lime sulfur 1. Introduction * Corresponding author: Tel.: ; fax: address: jsmilanick@aol.com (J.L. Smilanick). Green mold of citrus, caused by Penicillium digitatum (Pers.: Fr.) Sacc, and sour rot, caused /01/$ - see front matter Published by Elsevier Science B.V. PII: S (00)
2 158 J.L. Smilanick, D. Sorenson / Posthar est Biology and Technology 21 (2001) by Geotrichum citri-auranti (Ferraris) R. Cif. and F. Cif. (syn=geotrichum candidum Link), are the most economically important postharvest diseases of citrus in arid growing regions of the world. The primary infection courts of both pathogens are wounds on fruit inflicted during harvest and subsequent handling, and these infections must be eradicated to achieve acceptable levels of control (Powell, 1908; Eckert and Brown, 1986). Currently, measures employed to manage postharvest decay of citrus include treatments usually incorporated into fruit waxes, such as the fungicides orthophenyl phenate (SOPP), imazalil, and thiabendazole, or biological control formulations containing Candida oleophila or Pseudomonas syringae. Fruit are also immersed in tanks containing sodium bicarbonate at ambient temperatures (Smilanick et al., 1999), or heated solutions of SOPP, sodium carbonate, or a mixture of borax and boric acid (Eckert and Eaks, 1989). Several issues make the development of new treatments important, including concerns about human health risks associated with fungicide residues, particularly in the diets of children (National Research Council, 1993), the widespread occurrence of fungicide-resistant isolates of P. digitatum (Eckert et al., 1994), environmental problems associated with the disposal of water used in packing operations, and a lack of approved fungicides for the control of sour rot (Eckert and Eaks, 1989). To facilitate their regulatory approval and commercial acceptance, we evaluated compounds that have known environmental and animal toxicological properties and extensive precedents as additives or natural components in foods (Smilanick et al., 1995, 1997, 1999). Calcium polysulfide, formulated as liquid limesulfur (LLS) solution, was first described early in the nineteenth century and is one of the oldest fungicides (McCallan, 1967). LLS solution is a yellow-orange liquid, ph 11.5, with a density of 1.26 g ml 1. The formulation we used is typical (Tweedy, 1967), it contained a mixture of 29% (wt/vol) calcium polysulfide and small amount of calcium thiosulfate. It is prepared by combining hydrated lime (CaO H 2 O) and elemental sulfur with water. When diluted to 3% (wt vol 1 ) LLS solution, a common rate recommended in foliar fungicide applications, it has a ph of 10.0 and constantly releases small amount of hydrogen sulfide (H 2 S) gas. More H 2 S is released if the solution is acidified. At concentrations less than 1.5% (wt vol 1 ) or at low ph, yellow precipitates, which are primarily composed of elemental sulfur, form rapidly. In addition to its use as a fungicide, LLS solution is used to open sewer lines, immobilize metals in mine tailings, acidify soil, and improve water penetration into soil. As a pesticide, LLS was first described in 1802 in England, by 1850, the present lime sulfur formula was standardized, and it was in common use by 1900 in California for apple scab, powdery mildew, San Jose scale, aphids, mites, brown rot of peaches, and other pests and diseases (Tweedy, 1967). It is certified as an acceptable pesticide by most organic grower organizations and the USDA. Reports of its use to control postharvest diseases are few. Haller (1952) reviewed its use on stone fruit, where applications before harvest substantially reduced the postharvest incidence of brown rot of peaches, caused by Monilinia fructicola. Poulos (1949) reported postharvest applications to peaches of LLS reduced postharvest brown rot incidence about 60% without injury to the fruit. LLS has moderate acute toxicity (oral LD 50 for rats is 820 mg kg 1 ) but no chronic dietary toxicity hazard or carcinogenicity has been identified (Anon, 1997). The primary safety hazards it poses are burns from skin or eye contact with the concentrated solution, or from exposure to H 2 S gas that can evolve from LLS. Occupational Health and Safety Administration workplace limits for H 2 S are 10 l l 1 for 8 h and 15 l l 1 for brief exposures of 15 min (Anon, 1997). Our objectives were to assess the value of LLS for citrus fruit postharvest applications, by evaluating variables associated with its practical use, such as the influence of temperature, fruit contact time, and lime-sulfur solution concentration on its effectiveness, the risk of LLS injury to fruit, the in vitro toxicity of LLS to spores of P. digitatum, and quantification of H 2 S evolution in air during semi-commercial tests to estimate worker safety hazards. LLS was compared to treatments already in commercial use whose efficacy for the control
3 J.L. Smilanick, D. Sorenson / Posthar est Biology and Technology 21 (2001) of postharvest decay has been well-investigated (Eckert and Eaks, 1989). We also quantified sulfur residues in the LLS-treated fruit. 2. Materials and methods 2.1. Fruit Commercially harvested lemons (Citrus lemon [L.] N.L. Burm) or oranges (Citrus sinensis [L.] Osbeck) were randomized and inoculated within 2 days of harvest. Oranges were of typical commercial maturity. Lemons in most tests were lightgreen in color Liquid lime sulfur solution The LLS solution was donated by Best Sulfur Products, 5427 E. Central Avenue, Fresno, CA It contained by weight 29% wt wt 1 calcium polysulfide. The treatment solutions were prepared by dispensing LLS solution, usually at 3%, by weight to water into stainless steel tanks. The active concentration of calcium polysulfide in a 3% LLS solution was 0.85% wt vol Culture of pathogens P. digitatum isolate M6R (from J. W. Eckert, University of California, Riverside, CA) was cultured 1 2 wk on potato dextrose agar (PDA). Spores were harvested by adding 5 ml of water containing 0.05% Triton X-100 to the Petri dish, rubbing the surface with a sterile glass rod, and passing the suspension through two layers of cheese cloth. The suspension was diluted with water to an absorbance of 0.1 at 425 nm determined with a spectrophotometer; this density contains about 10 6 spores per ml (Eckert and Brown, 1986). Geotrichum citri-aurantii isolate 99-3 (isolated from lemon) was similarly cultured and prepared, except the arthrospores from 2-week-old cultures were suspended in 10 mg l 1 cyclohexamide to facilitate infection (Eckert and Brown, 1986) and 100 mg l 1 thiabendazole to minimize interference from P. digitatum In itro toxicity of LLS solution to spores To determine the germinability of spores of P. digitatum after immersion in LLS solution, 1 ml containing spores of P. digitatum, cultured and prepared as previously described, was added to 30 ml of water alone or LLS solution (3% wt vol 1 ). The solutions were either 25 or 40.6 C. Initially, and after 0.5, 2, 3.5, 5, and 6 h, 3 ml aliquots of each solution were removed and placed on a 2.4 cm diameter glass fiber filter in a glass support in a vacuum apparatus. To remove the original solution and thoroughly rinse the spores, the solution was removed by vacuum followed by the addition of two, 30 ml volumes of deionized water, each of which was removed by vacuum. The filter was removed from the support, inverted, placed on PDA and removed, where most of the spores were deposited. After 18 h at 15 C, the proportion of germinated spores was determined by examination of spores by light microscopy at 100. The experiment was repeated twice Inoculation methods Standard methods used to evaluate citrus postharvest fungicides were used. Lemons and oranges used in all experiments were selected by hand from field bins soon after harvest. The day before each experiment, the fruit were washed with water on commercial processing equipment, randomized, and inoculated with P. digitatum or G. citri-aurantii by briefly immersing a stainless steel tool with a1mmwide and 2 mm long tip in the solution and wounding each fruit once Laboratory tests to control green mold and sour rot Fruit were dipped into the treatment solutions contained in stainless- steel, computer-controlled heated tank system with l capacity tanks and stored 1 or 2 weeks at C before the incidence of green mold infected fruit was counted. The influence of lime-sulfur concentration, length of treatment, and solution temperature was evaluated. The effectiveness of
4 160 J.L. Smilanick, D. Sorenson / Posthar est Biology and Technology 21 (2001) lime-sulfur solution was compared to solutions now in commercial use (expressed as wt vol 1 ): 3% sodium carbonate (ph 11.5), 3% sodium bicarbonate (ph 8.3), and a mixture of 4% borax and 2% boric acid (ph 10.5) Impact of lemon maturity on LLS and sodium bicarbonate effecti eness Fruit from field bins were segregated into two color classes: (1) green, where 50% or more of the lemon surface was green in color; or (2) yellow, where none of the fruit surface had any green color. These fruit were from coastal groves in California where fruit of all maturity stages occur simultaneously. Fruit surface color was quantifed by recording CIELab chroma values (McGuire, 1992) of a 20 fruit sample of each class with a tristimulus colorimeter with an 8 mm aperture (Minolta Model DP301). The soluble solids and titratable acid content of a 10 ml aliquot of the juice of each of four replicates (each replicate a composite of the juice of five fruit) from fruit of each maturity class was determined with a refractometer and titration with 1.0 N NaOH. The fruit were inoculated 24 h before treatment in 3% (wt vol 1 ) LLS or sodium bicarbonate at 40.6 C for 2 min, followed by a brief rinse in 2-ml dih 2 O per fruit, then the fruit were stored 1 week at 20 C before examination. The experiment was repeated three times Semi-commercial tests to control green mold and sour rot Tests to assess the impact of temperature, LLS concentration, immersion period, and post-treatment fruit cleaning on LLS solution effectiveness and to compare it to other treatments were conducted with commercial fruit processing equipment at the University of California Lindcove Research and Extension Center (CREC) Fruit Quality Evaluation facility in Lindcove, CA. LLS solution was compared to treatments that are already in commercial use and their efficacy for the control of green mold have been well-characterized (Eckert and Eaks, 1989). These tests employed commercial harvest crews, large numbers of fruit per replicate, and processing equipment typical of commercial packing operations, such as a large tank with an overhead submerger/advancer that forced the fruit under the solution surface during immersion, a high-pressure water fruit washer, an overhead wax applicator with rotating brushes, and a dryer with high-velocity heated air. In the first test to assess control of green mold, four replicates, each of of oranges cv. Valencia or lemons cv. Eureka, were immersed for 90 s in a 2250 l tank containing LLS solution (3% wt vol 1 ) at 26.5 or 43.3 C ( 0.5 C). After treatment, the fruit were rinsed briefly using a low-pressure overhead spray of 10 ml water alone per fruit, or washed for 45 s at high pressure (200 psi or 1350 kpa) with water containing 50 mg l 1 free chlorine applied at 2400 l min 1. The highpressure water washer was 61 cm wide, 3 m long, and contained 15 rows of three 45 angle flat-fan nozzles per row. After rinsing or washing with water at high pressure, the fruit were waxed with a finishing wax (Britex 505, Brogdex) and dried at 50 C for 3 min. Other treatments included: (1) fruit that were inoculated but not treated or waxed; (2) fruit that were immersed for 3 min in 2250 l of sodium carbonate (3% wt vol 1 ) at 43.3 C, washed with water at high pressure as previously described, waxed, and dried; and (3) fruit that were immersed for 3 min in 2250 l of sodium carbonate (3% wt vol 1 ) at 43.3 C, washed with water at high pressure as previously described, coated with wax that contained 2000 mg l 1 imazalil, and dried. The test was conducted once with Valencia oranges and once with Eureka lemons. After treatment, the fruit were stored at 10 C for 15 days and the incidence of green mold was determined. In second test to assess control of sour rot and green mold, four replicates of 100 lemons cv. Eureka. each were immersed for 90 s in a 100 l of each test solution in tanks suspended in a temperature controlled-tank containing 2250 l of water. Solution temperatures were either 16.0 ( 2 C) or 40.6 C ( 2 C). Fruit were immersed in: (1) water alone at 16.0 C; (2) water alone at 40.6 C; (3) LLS (3% wt vol 1, ph 10.0) at 40.6 C; (4) sodium carbonate (3% wt vol 1, ph 11.5) at
5 J.L. Smilanick, D. Sorenson / Posthar est Biology and Technology 21 (2001) C; (5) a mixture of borax and boric acid (4 and 2% wt vol 1, respectively, ph 8.4) at 40.6 C; or (6) SOPP (0.5% wt vol 1, ph 8.6, Freshgard 20, 23% a.i.; FMC Corp., Riverside, CA) at 40.6 C. SOPP was also applied by passage of fruit for 15 s over eight rotating brushes where an overhead spray of SOPP (1.9% wt vol 1, ph 11.9) was constantly applied at 16.0 C Assessment of phytotoxicity of LLS to citrus fruit Three replicates of fruit each were immersed in LLS solution (3% wt vol 1 ) at 40.6, 48.9, or 54.4 C for 3 min followed by pressure washing with water as previously described. Fruit were randomized, treated, waxed with a finishing wax (Britex 505, Brogdex Co., Pomona, CA), dried at 49 C, and stored at 10 C for 7 weeks. The treatments were applied to five navel orange cultivars (Atwood, Thomsom Improved, Fisher, New Hall, Bonanza, USA) and Lisbon lemons. After storage, fruit were sorted visually into four classes: (1) perfect; (2) slight but not significant rind blemish present; (3) modest rind blemish present; or (4) scald injury present. Fruit of the first two classes would typically be ranked as USDA No. 1, those in the last two classes would be of lower value and classified as choice, standard, or juice-grade fruit. Because lime-sulfur solution has a sulfide odor, H 2 S and sulfur dioxide (SO 2 ) concentrations in air were monitored during semi-commercial tests to determine if these gases were present at levels hazardous to workers. The National Institute of Occupational Safety and Health workplace exposure limits for H 2 S and SO 2 are 10 and 2 l l 1, respectively, for 8 h (Anon, 1997). For brief exposures of 15 min, H 2 S and SO 2 are limited to 15 and 5 l l 1, respectively. Two models of colorimetric dosimeters for H 2 S (Drager Model 10/a- D and Synsidyne Model 4D) and one for SO 2 (Synsidyne Model 5D) were used. When activated, each could detect a minimum of 1 l l 1 of their respective gases for the next 8 h. They were placed at four locations cm above LLS tank and along packingline at Lindcove CREC during 5 h of operation of the heated 2000-l tank Impact of temperature on life of lime-sulfur solution sulfide content Lime-sulfur solution (3% wt vol 1 ) was distributed in 22 l aliquots to temperature-controlled stainless-steel tanks at 25, 40, 45, 50, 55, 60, or 65 C and the sulfide concentration was determined initially and after 24 and 48 h. Sulfide content was determined by the addition of standardized I 2 in excess of the sulfide content, followed by titration of the solution with stardardized thiosulfate to determine the I 2 remaining (Skoog and West, 1980). To a 10 ml aliquot of lime sulfur solution, 20 ml of 0.1 N I 2 was added, followed by additions of 1 ml of starch indicator and 50 ml of distilled water. The solution was titrated with 0.1 N calcium thiosulfate until it was colorless. The molarity of sulfide was calculated stochiometrically from the moles of 0.1 N thiosulfate titrant consumed Sulfur residues Sulfur residues were determined by distillation of a macerated sample of the whole fruit tissue followed by titration or liquid chromatography of the distillate to determine the content of sulfite or sulfide. Ten lemons, oranges, and grapefruit were immersed for 2 min in 3% wt vol 1 LLS at 40.6 C, then rinsed for 5 s in deionized water applied in a low pressure spray at 50 ml s 1, then stored for 5 days at 5 C before analysis. A distillation method was employed to determine the total volatile sulfite/sulfide content of the fruit, the aeration oxidation procedure, that is typically employed to estimate the total sulfur dioxide content in foods ( Modified Monier Williams procedure ; Zoecklein et al., 1990). A 1 l capacity distillation flask containing 400 ml of water and 5 ml of ethanol was purged with nitrogen at a flow rate of 20 ml min 1. After 15 min had passed for the system to de-oxygenate, a sample of 100 g (a composite of 20 g from each of 5 fruit) was added and promptly followed by the addition of 90 ml of 4.0 N HCl. The flask was heated to boiling and produced drops/min 1 from the condenser and continued for 105 min. The condenser was cooled to 6.0 C with circulating chilled ethyl-
6 162 J.L. Smilanick, D. Sorenson / Posthar est Biology and Technology 21 (2001) ene glycol. The receiver contained 30 ml of 2.0 mm Na 2 CO 3 plus 15 mm NaHCO 3. To determine the sulfide/sulfite content, the receiver contained 10 ml of 0.3% H 2 O 2 and after distillation its contents were titrated with 0.01 N NaOH with methyl red as an indicator. Recovery efficiency was determined by spiking the fruit sample with 10 g sulfite per gram fresh sample weight. In a second test, the receiver contents were not oxidized with H 2 O 2 and ion chromatography was applied to determine the nature of the sulfur content of the distillate. A 7.5 l-aliquot of the distillate was injected into a Dionex model DX- 120 with a Ionpac Fast Ion column (10 32) with a 2.0 mm Na 2 CO mm NaHCO 3 eluent at a flow rate of 2 ml min 1. A conductivity detector was employed. Sodium sulfite standards of 5, 10, 20, 50, and 100 mg l 1 were injected using the same conditions. The detection limit was 0.73 mg l 1. Recovery efficiency of both the distillation and ion chromatography procedures together was determined by spiking the fruit sample with 30 g sulfite/g fresh sample weight Statistical analysis A one- to three-way analysis of variance was applied to the square root of the arcsin of the proportion of infected or injured fruit, followed by Fisher s Protected LSD to separate means. Orthogonal analysis and paired-t tests were applied in some tests. Actual values are shown. 3. Results 3.2. Impact of concentration and duration of treatment on LLS effecti eness The incidence of green mold was equally reduced by the immersion of inoculated lemons in 2, 3, 4, or 6% wt vol 1 LLS solution at 40.6 C for 1.5 min (Fig. 2A). No injury to the lemons was observed after storage of the lemons after any treatment. The incidence of green mold was progressively reduced by the immersion of inoculated lemons in 3% wt vol 1 LLS at 40.6 C for 0.25, 1, 2, or 4 min (Fig. 2B). injury to the lemons was observed after storage of the lemons after any of the treatments Comparison of LLS to sodium carbonate and borax boric acid The effectiveness of LLS treatment for the control of citrus green mold was not significantly different from sodium carbonate or borax boric treatments (Table 1). Water alone at 40.6 C did not reduce green mold significantly. Lime-sulfur treatment reduced green mold incidence by 93, 88, and 81%, respectively, in tests one, two, and three. No injury to the lemons was observed after storage of the lemons after any treatment. In a laboratory test, LLS treatment reduced sour rot of lemons was significantly, from 64% incidence among inoculated control fruit to a mean of 35% among treated fruit (data not shown). However, increasing the LLS concentration (from 2 to 4.5% wt vol 1 ) or treatment time (from 1.5 to 3 min) did not significantly improve 3.1. In itro toxicity of LLS solution to spores The germinability of spores of P. digitatum was only slightly diminished after exposures as long as 6 h (Fig. 1) in either water or lime-sulfur solution at 25 C. At 40.6 C, however, spore germinability declined rapidly, particularly in LLS solution, where it decreased from 80 to 14% after 30 min exposure, and none could germinate after 2 h exposure. In water at 40.6 C, spore germinability declined from 80 to 59% after 30 min exposure, to 2.5% after 2 h exposure, and none survived 3.5 h exposure. Fig. 1. Germinability of spores of P. digitatum on potato dextrose agar after immersion in water or lime-sulfur solution (3% wt vol 1 ).
7 J.L. Smilanick, D. Sorenson / Posthar est Biology and Technology 21 (2001) Fig. 2. Influence of (A) lime-sulfur solution concentration during 1.5 min of treatment, and (B) the period of fruit immersion in 3% (wt vol 1 ) lime-sulfur solution on the subsequent incidence of green mold on lemons. The fruit were inoculated 24 h before treatment, the solution temperature during treatment was 40.6 C, and after treatment the fruit were stored for 2 weeks at 20 C before examination. control of sour rot. Treatment at 43.3 C was slightly but significantly superior to treatment at 21.1 or 32.2 C. These results are of one successful test, two other trials were inconclusive because sour rot did not develop among the inoculated control fruit. In all three tests, no injury to the lemons was observed after any treatment immediately or after 2 wk storage at 20 C Impact of fruit maturity Green lemons had lower chromicity values and higher soluble solid and acid contents than yellow lemons. Among the green lemons, the L, a, and b chromicity values were 67.4, 14.8, and 47.6, respectively, and the soluble solids content was 7.5% and 5.7 g acid per 100 ml of juice. Among the yellow lemons, the L, a, and b chromicity values were 75.7, 3.3, and 58.4, respectively, and the soluble solids content was 6.8% and 4.9 g acid per 100 ml of juice. The differences in chromicity, soluble solids, and acid content were all significant (P 0.05). Lemon maturity significantly influenced LLS efficacy. Control of green mold by LLS was superior to sodium bicarbonate on green lemons (Fig. 3). Conversely, the control of green mold on yellow lemons by LLS was significantly inferior to its control on green lemons, and the efficacy of LLS and sodium bicarbonate was not significantly different Semi-commercial tests In the first semi-commercial test, LLS significantly reduced the incidence of green mold on both oranges and lemons (Table 2). Heating the LLS solution, increasing the length of time the fruit were in the LLS solution, and pressure washing the fruit after LLS treatment all significantly (P 0.05) improved its effectiveness. On oranges, this LLS treatment was significantly superior to the sodium carbonate and imazalil combination (P=0.0138, paired t-test). On lemons, the most Table 1 Incidence of green mold (%) after the treatment of lemons inoculated 24 h before treatment with spores of P. digitatum a Test number b Treatment Inoculated, untreated control 99 a 99 a 97 a Inoculated, 40.6 C water- treated 91 b 99 a 97 a Lime-sulfur solution 3% c 7c 12 b 19 b Sodium carbonate 3% 20 c 14 b 14 b Borax 4% boric acid 2% ND d 9b 13 b a The temperature of all solutions was 40.6 C. The fruit were immersed for min, rinsed briefly with 2 ml per fruit of deionized water, and stored 2 wk. b Means in columns followed by the same letter are not significantly different (Fisher s Protected LSD; P 0.05). c Concentration is percentage wt vol 1. d ND=not done.
8 164 J.L. Smilanick, D. Sorenson / Posthar est Biology and Technology 21 (2001) Fig. 3. Influence of lemon maturity on the effectiveness of LLS and sodium bicarbonate. The fruit were inoculated, 24 h later immersed in 3% wt vol 1 of each solution at 40.6 C for 2 min duration, then stored for 1 week at 20 C before examination. effective LLS treatment was not significantly different (P=0.2152, orthogonal comparison) in effectiveness than sodium carbonate followed by imazalil. No visible injury to the lemons or oranges occurred in this test. In a second semi-commercial test, LLS significantly reduced the incidence of green mold and sour rot on lemons (Table 3). For the control of green mold, LLS was significantly superior to immersion in borax/boric acid, sodium carbonate, or sodium ortho-phenyl phenate applied over rotating brushes. LLS was inferior only to immersion in sodium ortho-phenyl phenate for green mold control. For the control of sour rot, LLS was not significantly different than immersion in borax/boric acid, sodium carbonate, or sodium ortho-phenyl phenate. It was superior to sodium ortho-phenyl phenate applied over rotating brushes. No visible injury to the lemons occurred in this test Assessment of phytotoxicity of LLS to citrus fruit The percentage of fruit marketable as USDA No. 1 of six citrus fruit cultivars was not influenced by 3% wt vol 1 LLS treatment at 40.6 C, and only two cultivars had a reduction in USDA No. 1 ratings at 48.9 C (Fig. 4). Even at 54.4 C, the quality of two cultivars (Fisher and Atwood navel oranges) was not reduced. The 7 week storage period used in this test was long and a normal and high incidence of rind breakdown occurred, particularly among navel oranges. Most of the Table 2 Incidence of green mold among lemons and oranges after treatment with lime sulfur, sodium carbonate, or soda ash (each at 3% wt-vol 1) followed by 2000 g/ml imazalil in finishing wax followed by 15 days storage at 10 C a Green mold incidence (% S.D.) Treatment Temp ( C) Contact time Pressure washer Lemons (min) Oranges Inoculated, untreated NA NA NA Lime sulfur No Lime sulfur No Lime sulfur Yes Lime sulfur Yes Lime sulfur No Lime sulfur No Lime sulfur Yes Lime sulfur Yes Sodium carbonate Yes Sodium carbonate+2000 ppm imazalil Statistical comparisons Yes Did pressure washing improve LLS effectiveness? Yes (P=0.0247) Yes (P=0.0001) Did heating improve LLS effectiveness? Yes (P=0.0001) Yes (P=0.0001) Was control of green mold after 3 min contact in LLS superior to contact for 1.5 min? Yes (P=0.0343) Yes (P=0.0008) a Treatments were applied 24 h after inoculation with spores of P. digitatum.
9 J.L. Smilanick, D. Sorenson / Posthar est Biology and Technology 21 (2001) Table 3 Incidence of green mold and sour rot among lemons inoculated with spores of P. digitatum or G. citri-auranttii 24 h before treatment a Treatment Green mold b Sour rot Water immersion, 16.0 C 99.6 a 58.1 a Water immersion, 40.6 C 92.4 b 39.7 b SOPP c (1.9%) d over rotating brushes, 16.0 C, 15 s 85.1 c 26.9 c Borax (4%) plus boric acid 34.0 d 13.8 d (2%) immersion, 40.6 C Sodium carbonate (3%) 30.6 d 10.1 d immersion 40.6 C Lime-sulfur solution (3%) immersion 40.6 C 17.8 e 17.8 d SOPP (0.5%) immersion, 40.6 C 9.2 f 15.2 d a The fruit were treated by immersion in the solutions for 90 s or by an overhead spray for 15 s, then stored at 13 C for 3 or 4 weeks when the incidence of green mold or sour rot was determined, respectively. b Means followed by unlike letters differ significantly by Fisher s Protected LSD (P 0.05) applied after a one-way ANOVA of the arcsin transformed incidence data. Actual percentages shown. c SOPP=sodium ortho-phenyl phenate. d Concentrations in wt vol 1. quality defects observed were rind pitting associated with senescent fruit. Gray-colored rind injuries, presumably caused by LLS solution scalding, were observed on a few fruit treated at 54.4 C. H 2 S and SO 2 were not detectable by the dosimeters in the air above the treatment tank during a 5 h-period of continuous operation of the semi-commercial tests, and therefore was below the 1 l l 1 detection limit of the dosimeters Impact of temperature on life of LLS solution sulfide content Freshly prepared LLS solution (3% wt vol 1 ) contained ( 2) mm sulfide. After 24 and 48 h, the mean sulfide contents in the tanks at 25, 40, 45, 50, 55, 60, or 65 C were similar and not significantly different (P 0.05). The sulfide content ( S.D.) among all the tanks after 24 and 48 h was 92.8 ( 0.9) mm and 87.6 ( 1.5) mm, respectively, representing losses of 93.1 and 84.9% from the original sulfide content. Yellow-colored scale deposits accumulated within the tanks during this period Sulfur residues in LLS-treated fruit The presence of sulfur residues in LLS-treated fruit was indicated after application of the Modified-Monier Williams distillation procedure, while none were detected in untreated fruit. The Fig. 4. Influence of liquid lime-sulfur solution temperature during treatment on the quality of lemons and oranges. The fruit were immersed for 3 min in 3% wt vol 1 LLS solution at 20.0, 40.6, 48.9, or 54.0 C, stored for 7 weeks at 10 C, and the visual quality of the fruit determined.
10 166 J.L. Smilanick, D. Sorenson / Posthar est Biology and Technology 21 (2001) recovery of a 10.2 g g 1 sodium sulfite spike added to untreated oranges, lemons, and grapefruit was 93.7, 87.8, and 108.0%, respectively. The volatile sulfur content, calculated either as sulfite or sulfide, was 31.9, 33.1, and 36.3 g g 1 of oranges, lemons, and grapefruit. In the second experiment, the distillation was repeated and the receiver contents were not oxidized by H 2 O 2 but analyzed by ion chromatography. The recovery of a30 g g 1 sodium sulfite added to orange and lemon samples followed by distillation and by ion chromatography was 87.3 and 23.3% respectively. No sulfite was detected when untreated fruit were analyzed. When LLS-treated oranges and lemons were analyzed, no sulfite was detected by ion chromatography, suggesting the volatile sulfur present was sulfide and not sulfite. Therefore, the sulfur content of the LLS-treated fruit from the initial distillation procedure was not sulfite and should be calculated as sulfide. 4. Discussion Used LLS can be safely disposed of by many routes, and this is its most compelling advantage over other methods to control postharvest decay. Because LLS is frequently applied to sewers or agricultural soils, it can be used in locations where the disposal of other fungicides, particularly those used in large tanks (whose capacity can exceed l) has become difficult due to environmental concerns. LLS can be an effective and inexpensive treatment for the control of postharvest green mold and provide some control of sour rot. There was little risk of injury to citrus fruit. The treatment was more effective on lemons than oranges, and on less mature lemons than on more mature lemons. Therefore, LLS is a good candidate for applications to fruit soon after harvest, rather than to fruit that are reprocessed after long storage. LSS effectiveness was similar when it was applied before or after fruit cleaning operations, therefore it can be used in processing lines either before or after the fruit are cleaned. Cleaning alone, even when done with water at high pressure, does not reduce postharvest decay after the inoculation of wounds with pathogens (Smilanick et al., 1999). Like other tank treatments such as borax boric acid or sodium carbonate, it is very important that attention be paid to sanitation of the fruit after treatment, because LLS treatment probably does not leave residues capable of providing persistent protection of the fruit. Therefore, spores from the air or surfaces of packing equipment could inoculate the fruit through wounds made during handling after LLS treatment. Opportunities for re-contamination are minimized if LLS treatment is applied at the end of the packing process, after sorting and grading, and just before waxing. This way, exposure of the treated fruit to contamination is minimized. In this work we quantified sulfur residues in the LLS-treated fruit and showed they were probably sulfides and not sulfites. This is important because sulfite residues are under regulatory control and typically cannot exceed 10 g g 1 without a consumer warning label attached (Zoecklein et al., 1990). The mode of action of LLS is incompletely known. Two toxic components of LLS are H 2 S, produced by the decomposition of LLS, and elemental sulfur, which comprises part of the yellow scale deposits on equipment that accumulated after prolong use of LLS. Elemental sulfur oxidizes cytochrome b to cytochrome c, with a concomitant production of H 2 S, itself an inhibitor of cytochrome oxidase (Smith et al., 1977), and a fungistatic, not fungicidal, inhibition results (Tweedy, 1967). LLS did not kill P. digitatum spores immediately, but caused a persistent inhibition of their growth. P. digitatum spores germinated very slowly after LLS treatment, even when they have been rinsed repeatedly with fresh water, which suggests the LLS deposits a very persistent residue on them. Gadoury et al. (1994) reported 1 h of exposure to LLS was required before the viability of ascospores within cleistothecia of Uncinula necator was significantly reduced, while formaldehyde killed most all of them within 5 min. LLS forms irreversible and insoluble sulfide salts with zinc and copper, and could conceivably solve water contamination problems associated with these metals (Salvato, 1992). Zinc, a micronutrient, and copper, a fungicide, are applied
11 J.L. Smilanick, D. Sorenson / Posthar est Biology and Technology 21 (2001) to citrus trees in many parts of the world. In some areas, residuals of these metals from field applications represent water quality problems when treated fruit are cleaned in packinghouses, because the wash water zinc and copper content can exceed water quality standards when it is discharged into sewers or ponds. Insoluble zinc and copper sulfides would accumulate in the bottom of LLS tanks, and disposal of these solids would occur when the tank scale is removed. An important practical consideration is that the sulfide content of LLS solution declined slowly as the solution aged. Additional losses would occur when some LLS is carried away as fruit pass out of commercial processing tanks. Because the volume of fruit processed and the size of the tanks differs considerably among packinghouses, the life of the LLS solution and the intervals at which it must be recharged in a commercial packingline needs to be determined empirically at each facility. Sulfide concentration can be determined by titration or with a sulfide selective electrode (Papp, 1971). If the LLS concentration falls below 1.5% wt vol 1 it will decompose rapidly to elemental sulfur, which precipitates in the tank. The solution concentration can be routinely approximated with a salt refractometer or a hydrometer calibrated for LLS solution. The odor of H 2 S was present and could conceivably be a significant nuisance, although it was below safety thresholds. Placement of the tank in an isolated and well-ventilated area is recommended. Another issue of concern is the corrosiveness of the solution. The tank, heat exchanger, rollers, and other components should be plastic or stainless steel; mild steel, iron, and non-ferrous metals are not compatible with LLS. Scale is also deposited on equipment, and the capability to dismantle and mechanically remove scale should be accommodated in the design of this equipment. We presume most of the scale is calcium carbonate and elemental sulfur. In other tests, we evaluated the effectiveness and stability of potassium polysulfide solution. Unlike calcium polysulfide, the potassium polysulfide solution deposited little scale on equipment, and its effectiveness for the control of green mold was equal to LLS (data not shown). However, the amount of potassium polysulfide available for commercial use was small and its price was higher than LLS, so we did not evaluate its use further. Acknowledgements We are thankful for the financial support of the California Citrus Research Board, the formulation and donation of lime-sulfur solution by Best Sulfur Products and the assistance of Faith Potter, Don Holbrook, and Alex Holman of that company, John Maze, Walter Stutzman, and Louis Whitendale of University of California Lindcove Citrus Research and Extension Center are gratefully acknowledged, we thank D.A. Margosan, D.J. Henson, Jim Sievert for technical support and Paul Nelson of FMC regarding commercial tests in Yuma AZ. We appreciate the donation by Sunkist Growers of much of the labor to conduct these tests, and we thank Husain Ajwa, Monir Monsour, and Dennis Margosan for review of the manuscript. References Anonymous, National Institute for Occupational Safety and Health Pocket Guide to Chemical Hazards. US Department of Human Health Services (NIOSH) Publication No US Government Printing Office, Washington, DC. Eckert, J.W., Brown, G.E., Evaluation of postharvest treatments for citrus fruits. In: Hickey, K.D. (Ed.), Methods for Evaluating Pesticides for Control of Plant Pathogens. American Phytopathological Society, St Paul, MN, pp Eckert, J.W., Eaks, I.L., Postharvest disorders and diseases of citrus fruits. In: Reuther, W., Calavan, E.C., Carman, G.E. (Eds.), The Citrus Industry, vol. 4. University of California Press, Berkeley, CA, pp Eckert, J.W., Sievert, J.R., Ratnayake, M., Reduction of imazalil effectiveness against citrus green mold in California packinghouses by resistant biotypes of Penicillium digitatum. Plant Dis. 78, Gadoury, D.M., Pearson, R.C., Riegel, D.G., Seem, R.C., Becker, C.M., Pscheidt, J.W., Reduction of powdery mildew and other diseases by over-the-trellis applications of lime sulfur to dormant grapevines. Plant Dis. 78, Haller, M.H., Handling, transportation, storage, and marketing of peaches. USDA Biograph. Bull. 21,
12 168 J.L. Smilanick, D. Sorenson / Posthar est Biology and Technology 21 (2001) McCallan, S.E.A., History of fungicides. In: Torgeson, D.C. (Ed.), Fungicides: An Advanced Treatise, vol. 1. Academic Press, New York, pp McGuire, R.G., Reporting of objective color measurements. HortScience 27, National Research Council, Pesticides in the Diets of Infants and Children. National Academy Press, Washington, DC. Papp, J., Potentiometric determination of sulphur compounds in white, green and black liquors with sulphide ion-selective electrode. Cellul. Chem. Technol. 5, Poulos, P.L., The use of sodium hypochlorite for the control of the brown rot disease of peach in Delaware. Plant Dis. Rep. 33, Powell, G.H., The decay of oranges while in transit from California. Bulletin No. 123, Bureau of Plant Industry. United States Department of Agriculture, Washington, DC. Salvato, J.A., Environmental Engineering and Sanitation, 4th edn. Wiley-Interscience, New York. Skoog, D.A., West, D.M., Analytical Chemistry, 3rd edn. Saunders College, Philadelphia, PA. Smilanick, J.L., Mackey, B.E., Reese, R., Usall, J., Margosan, D.A., Influence of the concentration of soda ash, temperature, and immersion period on the control of postharvest green mold of oranges. Plant Dis. 81, Smilanick, J.L., Margosan, D.A., Henson, D.J., Evaluation of heated solutions of sulfur dioxide, ethanol, and hydrogen peroxide to control postharvest green mold of lemons. Plant Dis. 79, Smilanick, J.L., Margosan, D.A., Mlikota, F., Usall, J., Michael, I.F., Control of citrus green mold by carbonate and bicarbonate salts and the influence of commercial postharvest practices on their efficacy. Plant Dis. 83, Smith, L., Kruszyna, H., Smith, R.P., The effect of methemoglobin on the inhibition of cytochrome c oxidase by cyanide, sulfide and azide. Biochem. Pharmacol. 26, Tweedy, B.G., Elemental sulfur. In: Torgeson, D.C. (Ed.), Fungicides: An Advanced Treatise, vol. 2. Academic Press, New York, pp Zoecklein, B.W., Fugelsang, K.C., Gump, B.H., Nury, F.S., Production Wine Analysis. Van Nostrand Reinhold, New York..
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