Subscriber access provided by UNIVERSITY OF TOLEDO LIBRARIES
Agricultural and Environmental Chemistry
Sensory quality, physicochemical attributes, polyphenol profiles and residual fungicides in strawberries from different disease control treatments Marvin Abountiolas, Katrina Kelly, Yavuz Yagiz, Zheng Li, Gail Mahnken, Wlodzimierz BorejszaWysocki, Maurice R. Marshall, Charles Sims, Natalia Peres, and Maria Cecilia Do Nascimento Nunes J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.8b02153 • Publication Date (Web): 21 Jun 2018 Downloaded from http://pubs.acs.org on June 22, 2018
Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.
is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.
Page 1 of 47
Journal of Agricultural and Food Chemistry
1
Sensory quality, physicochemical attributes, polyphenol profiles and residual
2
fungicides in strawberries from different disease control treatments
3 4
Marvin Abountiolasa, Katrina Kellya, Yavuz Yagizb, Zheng Lib, Gail Mahnkenb, Wlodzimierz
5
Borejsza-Wysockib, Maurice Marshallb, Charles A. Simsb, Natalia Peresc, and Maria Cecilia do
6
Nascimento Nunes*, a
7 8
a
9
University of South Florida, 4202 E. Fowler Avenue, Tampa, Florida 33620, USA.
Food Quality Laboratory, Department of Cell Biology, Microbiology and Molecular Biology,
10
b
11
Gainesville, FL 32611, USA
12
c
13
672, Wimauma, FL 33598, USA.
Department of Food Science and Human Nutrition, University of Florida, 520 Newell Drive,
Gulf Coast Research and Education Center, University of University of Florida, 14625 Co. Rd.
14 15 16 17 18 19
*Corresponding author: Tel: 1-813- 974-9307; fax: 1-813-905-9919
20
E-mail address:
[email protected] (C.N. Nunes).
21 22
1 ACS Paragon Plus Environment
Journal of Agricultural and Food Chemistry
Page 2 of 47
23
ABSTRACT: Using alternative agricultural practices in combination with proper postharvest
24
handling has become a major goal to improve fresh produce quality. Here, two different
25
strawberry (Fragaria × ananassa) genotypes were used as a model to study the impact of
26
repeated, reduced-fungicide or no-fungicide applications on the sensory quality, physicochemical
27
attributes, polyphenol profiles and residual fungicide in strawberries. Strawberries grown under
28
reduced-fungicide applications had similar or better physicochemical quality than conventionally
29
and organically-grown fruit and lower levels of fungicide residues than conventional fruit.
30
Overall, flavor- and health-related attributes of strawberries from reduced-fungicide applications
31
were intermediate between conventional and organic fruit. Thus, growing strawberries with
32
reduced-fungicide applications can be an alternative to conventional or organic agricultural
33
practices.
34 35
KEYWORDS: Fragaria×ananassa, storage, sensory quality, bioactive compounds, sugars,
36
fungicides
37 38 39 40 41 42 43 44 45
2 ACS Paragon Plus Environment
Page 3 of 47
Journal of Agricultural and Food Chemistry
46 47
INTRODUCTION
48
Strawberries are amongst the most popular fruits consumed worldwide and are recognized for
49
their exceptional nutritional qualities. Strawberries have been the focus of many studies for their
50
health benefits due to high levels of bioactive compounds, including phenolic acids, flavonoids,
51
and vitamin C.1-4 However, overall strawberry quality and, the levels of bioactive compounds, is
52
greatly influenced by genotype5-12, agricultural practices13-16 and by postharvest conditions.17 In
53
order to control strawberry diseases, current control measures involve repeated fungicide
54
applications which may impact strawberry quality. Indeed, several studies showed that organic
55
strawberries, in general, have similar or higher levels of polyphenols and vitamin C compared to
56
fruit grown under conventional agricultural practices.18-24 Some have suggested that eliminating
57
or limiting the use of synthetic pesticides results in increased pest pressure and thus organic
58
production methods induce plants to develop more robust defense mechanisms such as
59
increasing the synthesis of polyphenols.13-14, 20, 24-26
60
There is a critical need to provide alternative agricultural practices that in combination with
61
proper postharvest practices will produce “healthier” strawberries. Hence, production will be less
62
harmful to the environment while resulting in lower costs for growers and consumers. From
63
previous work on the impact of different agricultural practices on disease control and yield, and
64
produce quality, it is apparent that much potential exists for reducing the amount of fungicides
65
used and offer the consumer a strawberry with lower fungicide residues and, with equal or
66
superior sensory and nutritional quality as an alternative to organic fruit. While few studies have
67
shown that quality of organic strawberries may be superior compared to that of fruit organically-
68
grown or from integrated pest management18,
21-22, 24
there are no studies that document how
3 ACS Paragon Plus Environment
Journal of Agricultural and Food Chemistry
Page 4 of 47
69
strawberries grow under a reduced-fungicide application regime perform comparatively to fruit
70
gown under conventional or organic disease control measures. Also, only one study reported
71
comparative changes in color, polyphenols and ascorbic acid content in organic as opposed to
72
conventional strawberries during cold storage.19 Thus, the rationale for conducting this work was
73
that by reducing the amount of fungicides used to control strawberry diseases through accurately
74
targeting the right application time the overall postharvest quality of strawberries can be
75
maintained or enhanced providing an alternative to health-aware consumers. The overall
76
objective of this study was to determine the impact of repeated, reduced-fungicide or no-
77
fungicide applications on the sensory quality, physicochemical attributes, polyphenol profiles
78
and residual fungicides in strawberries.
79 80
MATERIAL AND METHODS
81
Plant Material and Disease Control Treatments. ‘Florida Radiance’ and ‘Strawberry
82
Festival’ strawberries were obtained from commercial fields in Florida, USA, and grown under
83
the following disease management conditions: conventional, reduced-fungicide using a disease
84
forecasting system27 and organic. Conventional and reduced-fungicide ‘Florida Radiance’ and
85
‘Strawberry Festival’ strawberries were harvested from commercial fields in Plant City and
86
Floral City, respectively. Organic ‘Strawberry Festival’ was obtained from a commercial field in
87
Duette. Organic ‘Florida Radiance’ strawberries were not available in same geographical area,
88
therefore only organic ‘Strawberry Festival’ strawberries were tested against conventional and
89
reduced-fungicide disease control treatments. Tables 1 and 2 show the types of fungicides and
90
application dates for conventional and reduced-fungicide strawberries grown in Plant City and
4 ACS Paragon Plus Environment
Page 5 of 47
Journal of Agricultural and Food Chemistry
91
Floral City, respectively. Organic strawberries were grown according to the United States
92
Department of Agriculture National Organic Program (NOP) guidelines.28
93
Postharvest Treatments. Strawberries were harvested twice during the 2014 production
94
season: conventional and reduced-fungicide ‘Florida Radiance’ were harvested on January 21
95
(Harvest 1) and on February 18 (Harvest 2). Conventional, reduced-fungicide and organic
96
‘Strawberry Festival’ were harvested on February 7 (Harvest 1) and March 7 (Harvest 2). Fruit
97
were brought to the laboratory, selected for uniformity of size, color and freedom of defects,
98
carefully packed into 0.453 kg-clamshells and stored at 1.5 °C and 85% RH inside a temperature
99
and RH-controlled chamber (Forma Environmental Chambers Model 3940 Series, Thermo
100
Electron Corporation, OH, USA). These conditions simulated the lowest temperature and highest
101
RH measured during strawberry handling.29-31 Strawberry samples (3 clamshells containing 15
102
fruit each per treatment) were evaluated for physicochemical quality at harvest and daily during a
103
7-day storage period. Sensory quality was evaluated after 3 days of storage, and fungicide
104
analysis was performed at harvest and after 3 and 7 days of storage.
105
Sensory Analysis. Fungicide treatments for each cultivar and harvest were subjected to
106
acceptability testing by a panel of 100 strawberry consumers. The panelists were selected based
107
on their consumption frequency of strawberries and availability for all panels. Two strawberries
108
from each treatment were presented to panelists for evaluation. Each treatment was coded by a
109
three-digit random number, and all possible orders of presentation were presented approximately
110
an equal number of times. Panelists rated their level of acceptability for overall, appearance,
111
texture, and flavor using the 9-point hedonic scale where 1 = dislike extremely, 5 = neither like
112
nor dislike, and 9 = like extremely. Evaluations were conducted in a sensory testing lab, with 10
113
individual booths and a computer data entry system using Compusense®.
5 ACS Paragon Plus Environment
Journal of Agricultural and Food Chemistry
Page 6 of 47
114
Instrumental Color and Texture Analysis. A total of two color measurements were taken
115
on the opposite sides of the fruit in the equatorial region. A hand-held tristimulus reflectance
116
colorimeter (Model CR-400, Minolta Co., Ltd., Osaka, Japan) was used following the procedure
117
described by Kelly et al.8 Firmness of each strawberry was measured using a TA.XT Plus
118
Texture Analyzer (Texture Technologies Corp., NY, USA) as described by Whitaker et al.32
119
Weight loss and Dry Weight. Weight loss of three replicated samples of 15 strawberries
120
each was calculated from the initial weight of the fruit and every day during a 7-day storage
121
period. Concentrations of chemical constituents were expressed in dry weight to show the
122
differences between treatments that might be obscured by differences in water content.8 To
123
compensate for water loss during storage, chemical compounds were expressed in g kg-1 on a dry
124
weight basis.
125
Acidity and Soluble Solids Content (SSC). Three replicates of fifteen individual fruit per
126
treatment were homogenized in a laboratory blender at high speed for 2 min and the resulting
127
puree immediately frozen and kept at -30 °C until used. Titratable acidity and SSC were
128
determined according to Nunes et al.33
129
Ascorbic Acid Analysis. The ascorbic acid analysis was conducted using a Hitachi
130
LaChromUltra UHPLC system with a diode array detector and a LaChromUltra C18 2µm
131
column (2 × 50 mm) (Hitachi, Ltd., Tokyo, Japan) as described by Nunes.34
132
Total Phenolics and Anthocyanins. Total phenolic compounds were measured using the
133
Folin-Ciocalteau reagent as described by Nunes et al.35 Anthocyanins were extracted in 0.5%
134
(v/v) HCl in methanol and measured using the procedure described by Nunes et al.35
135
Extraction of Polyphenols. Triplicates of 5 mL of strawberry puree from each treatment
136
were mixed with 15 mL of acetone, sonicated for 10 minutes and filtered through Whatman
6 ACS Paragon Plus Environment
Page 7 of 47
Journal of Agricultural and Food Chemistry
137
paper No.4. The filtrate was concentrated to 5 mL in a rotary evaporator (Buchi Rotavapor R-
138
114, Birkmann Instruments, Inc., USA) and passed through a classic C18 Sep-Pack cartridge
139
(Waters Technologies Corp., USA) previously activated with methanol, followed by water and
140
3% formic acid. Anthocyanins and other phenolics were absorbed onto the column whereas
141
sugars, acids, and other water-soluble compounds were eluted with acidified water. The
142
polyphenols were then recovered by passing 2.0 mL of methanol containing 3% formic acid
143
through the cartridge. The extract was filtered through a 0.20 µm syringe filter into 2 mL
144
autosampler vials and stored at -30 °C until used.
145
Identification and Quantification of Polyphenols. Individual polyphenol compounds
146
were identified and quantified using the extracts prepared as described above. Analysis of
147
phenolic compounds was conducted using a Hitachi LaChroma Ultra HPLC system coupled with
148
a photodiode array detector (Hitachi, Japan).36 Samples were injected at 40°C onto a reverse-
149
phase Hypersil Gold C18 column (100 × 2.1 mm; particle size, 1.9 µm) (Thermo Fisher Scientific
150
Inc., USA). The mobile phase was acidified water containing 0.5% formic acid (mobile phase A)
151
and 0.1% formic acid in acetonitrile (mobile phase B) in an isocratic mixture. The flow rate was
152
0.3 µL/min, and the wavelength detection was set at 250, 280, 360 and 520 nm. Sample injection
153
volume was 10 µL. Retention times and spectra were compared with pure standards of 16
154
compounds from different polyphenol classes: flavonoids (anthocyanidins: cyanidin and
155
pelargonidin; anthocyanins: cyanidin 3-glucoside and pelargonidin 3-glucoside; flavonols:
156
quercetin, kaempferol, quercetin 3-glucoside, kaempferol 3-glucoside and myricetin; flavanols:
157
catechin and epicatechin), phenolic acids (p-coumaric acid, ferulic acid, caffeic acid and
158
chlorogenic acid) and hydrolysable tannins (ellagic acid). Afterwards a mixture containing all 16
159
polyphenol standards was analyzed to obtain the retention times. The retention times from the
7 ACS Paragon Plus Environment
Journal of Agricultural and Food Chemistry
Page 8 of 47
160
mixture were used to analyze strawberry samples instead of the individual standards to account
161
for shifts in retention times by polyphenolic interaction. The optimum wavelength absorbency
162
was determined by comparing the chromatograms of each sample and using the strongest peak
163
wavelength. Quantification of individual polyphenols was based on surface area (%) of each
164
peak.
165
Sugar Analysis. Quantification of sucrose, fructose and glucose was conducted using a
166
Hitachi HPLC with an refractive index detector and a 300 mm × 8 mm Shodex SP0810 column
167
(Shodex, Colorado Springs, CO) with an SP-G guard column (2 mm x 4 mm) as described by
168
Kelly et al.8
169
Fungicide Analysis. Strawberry samples were extracted for multiresidue determination of
170
fungicides based on the QuEChERS method developed by Lehotay et al.37 and slightly modified
171
by Lesueur et al.38 Captan was analyzed using a GC/MS system (6890N GC coupled with a
172
MSD 5973, Agilent Technologies, USA) with a ZB-5MSi (30 m x 0.32 mm x 0.25µm,
173
Phenomenex, USA) capillary column under the following conditions: constant helium flow of
174
1.3 mL/min; inlet temperature starting at 100 °C and after one min, ramped at 15.2 °C min-1 to a
175
temperature of 235 °C, held 5 min, and ramped at 15 °C min-1 to a final temperature of 300 °C
176
with holding time of 5 min. Injection volume of 1 µL in splitless mode, ion source temperature
177
(230 °C) and MS Quad temperature (150 °C). Captan was quantified at 149 m/z (quantification
178
ion) and 79 m/z (confirmation ion) with selected ion monitoring mode.
179
validated at 0.025 and 0.25 ppm captan fortification levels. An HPLC with mass spectrometry
180
(TSQ Quantum Ultra LC/MS/MS, Thermo Finnigan, USA) was used to quantify fludioxonil,
181
penthiopyrad, cyprodinil, cyflufenamid, azoxystrobin and pyraclostrobin.37-38 The method was
182
first validated at 0.025 and 0.25 ppm fortification levels on strawberry matrix before sample
The method was
8 ACS Paragon Plus Environment
Page 9 of 47
Journal of Agricultural and Food Chemistry
183
analysis. Spike recoveries should fall in the acceptable range of 70 to 120%. Both fortified and
184
unfortified control samples were analyzed concurrently with each sample set to demonstrate the
185
absence of significant interferences and adequate recoveries. Organic ‘Strawberry Festival’ was
186
used as a control.
187
Statistical Analysis. The Statistical Analysis System computer package (SAS Institute, Inc.,
188
2004) was used for the analysis of the data. Although there was a significant difference between
189
harvests for several of the physicochemical attributes measured, the trend for the different
190
treatments was the same within cultivar and harvest. Therefore, for ease of interpretation,
191
physicochemical data from the two harvests were combined. The data was treated by two-way
192
analysis of variance (ANOVA) with harvest, cultivar and disease control treatment as main
193
effects. Significant differences between cultivars and disease control treatments were detected
194
using the least significant difference (LSD) at the 5% level of significance. Data from sensory
195
quality and residual fungicides from the two different harvests were analyzed separately.
196
Acceptability data from sensory analysis were subjected to a two-way analysis of variance to
197
determine whether significant differences exist between the fungicide treatments. If significant
198
differences were indicated, means were separated by Tukey’s HSD (p>0.05).
199 200
RESULTS AND DISCUSSION
201
Sensory Quality. In the first harvest, the appearance of organic ‘Strawberry Festival’
202
received higher scores than that of fruit from the reduced-fungicide treatment and similar scores
203
to that of conventional strawberries (Table 3). However, the appearance of conventional
204
strawberries was not significantly different from that of reduced-fungicide or organic fruit.
205
‘Strawberry Festival’ scores for texture, flavor and overall liking were not significantly different
9 ACS Paragon Plus Environment
Journal of Agricultural and Food Chemistry
Page 10 of 47
206
between treatments. Conventional ‘Florida Radiance’ received higher scores for texture and
207
flavor and similar scores for appearance and overall liking compared to fruit from the reduced-
208
fungicide treatment. Overall, fruit from the first harvest was not significantly different for overall
209
liking. Results from the second harvest showed that there were no significant differences
210
between the disease control treatments for any of the sensory attributes evaluated. A previous
211
study showed that consumer preference for organic, as opposed to conventional strawberries, is
212
cultivar dependent.39 That is, overall acceptance, flavor, sweetness, and appearance of organic
213
strawberries ‘Lanai’ and ‘San Juan’ were not different than conventional fruit whereas organic
214
‘Diamante’ strawberries received higher scores for the same sensory attributes compared to
215
conventional fruit.18
216
Color and Texture. ‘Strawberry Festival’ were lighter (higher L*) and less red (higher hue)
217
than ‘Florida Radiance’, regardless of the disease control treatment (Figure 1). At harvest,
218
organic ‘Strawberry Festival’ was slightly lighter (higher L*) but redder (lower hue) compared to
219
fruit from the other treatments whereas no significant difference was found between the color of
220
conventional and reduced-fungicide ‘Florida Radiance’. In a previous study, external color
221
intensity was similar between organic and conventional ‘Diamante’, ‘Lanai’ and ‘San Juan’
222
strawberries however organic fruit was darker red compared to conventional strawberries.18
223
Others have also reported that surface color of ‘Selva’ organic strawberries was darker, less vivid
224
and tended to be redder than conventional fruit but no significant differences were found in the
225
color of the flesh between organic and conventional fruit.20 In a study conducted at the retail
226
level, conventional strawberries tended to have higher L* (less dark) and lower or similar hue
227
(redder) than organic fruit. Unlike reported by Crecente-Campo et al.20, the internal color of
228
organic ‘Strawberry Festival’ was redder than that of fruit from conventional or reduced-
10 ACS Paragon Plus Environment
Page 11 of 47
Journal of Agricultural and Food Chemistry
229
fungicide treatments (data not shown). During storage, L* of both strawberry cultivars declined,
230
as the fruit became darker, but after 7 days no difference was found in the L* of Strawberry
231
Festival’ from the different disease control treatments (Figure 1). On the other hand, after
232
storage, ‘Florida Radiance’ from the reduced-fungicide treatment was significantly lighter and
233
less red (higher L* and hue) than conventional fruit. After storage, organic ‘Strawberry Festival’
234
were redder (lower hue) than conventional fruit but less red (higher hue) than reduced-fungicide
235
treatments. Overall, differences in color of strawberries did not result in appearance preferences
236
by consumer-sensory panels between organic and conventional fruit (Table 3).
237
‘Florida Radiance’ was slightly firmer at harvest compared to ‘Strawberry Festival’ (Figure
238
2). At harvest, organic ‘Strawberry Festival’ was softer than fruit from other treatments. Also,
239
when compared to conventional fruit, reduced-fungicide strawberries also tended to be softer at
240
harvest. A previous study showed no significant difference between firmness of organic and
241
conventional strawberries.18 Such differences may be related to genotype variability and possibly
242
to maturity of the fruit at harvest. The firmness of strawberries decreased during storage,
243
regardless of cultivar or treatment. However, compared to initial values at harvest, ‘Strawberry
244
Festival’ and ‘Florida Radiance’ from the reduced-fungicide treatment softened less during
245
storage (10.7 and 12.3% decrease, respectively) than fruit from the conventional treatment (14.5
246
and 20.5% decrease, respectively). The least decrease in firmness during storage was measured
247
for organic ‘Strawberry Festival’ (9.7%). Overall, differences in texture did not result in a
248
preference for the texture of organic versus conventional and reduced-fungicide strawberries by
249
consumer-sensory panels except for conventional ‘Florida Radiance’ that were preferred for
250
texture over fruit from the reduced-fungicide treatment (Table 3).
11 ACS Paragon Plus Environment
Journal of Agricultural and Food Chemistry
Page 12 of 47
251
Weight Loss. Although after storage there was no significant difference in the weight loss of
252
‘Strawberry Festival’ from all treatments, organic and reduced-fungicide strawberries lost
253
slightly less weight (8.5 and 8.9%, respectively) than conventional fruit (9.1%) (Figure 2).
254
Reduced-fungicide ‘Florida Radiance’ lost significantly less weight than conventional fruit. In a
255
previous study, Reganold et al.18 also reported lower weight loss in organic strawberries
256
compared to conventional fruit and suggested that slower dehydration in organic fruit may result
257
from a thicker cuticle and expansion of epidermal cell walls.
258
Overall, there was a decline in strawberry chemical compounds during storage regardless of
259
the treatment (Figures 1-5). The decrease in chemical compounds during storage is likely related
260
to water loss that results in reduced turgor pressure of the cells leading to membrane breakdown.
261
For example, collapse of cellular membranes allows for the interaction of degrading enzymes,
262
such as polyphenol oxidase and ascorbate oxidase, to come into contact with polyphenols and
263
ascorbic acid, respectively.34,35
264
Acidity and Soluble Solids Content. At harvest, the acidity of organic ‘Strawberry Festival’
265
was higher compared to fruit from the conventional or reduced-fungicide treatments whereas
266
acidity of conventional ‘Florida Radiance’ was higher than that of fruit from the reduced-
267
fungicide treatment (Figure 3). Reganold et al.18 reported no consistent trend in the acidity of
268
organic versus conventional strawberries. That is, organic ‘Diamante’, ‘Lanai’ and ‘San Juan’
269
strawberries had higher, similar or lower acidity, respectively, than their conventional
270
counterparts. Acidity declined during storage, regardless of the treatment or cultivar but after 7
271
days, there was no significant difference in the acidity of ‘Strawberry Festival’ whereas
272
conventional ‘Florida Radiance’ had lower acidity compared to reduced-fungicide strawberries.
12 ACS Paragon Plus Environment
Page 13 of 47
Journal of Agricultural and Food Chemistry
273
Initial values for SSC were significantly different between cultivars and between disease
274
control treatments and (Figure 3). ‘Strawberry Festival’ from reduced-fungicide had higher SSC,
275
followed by organic and conventional fruit while conventional ‘Florida Radiance’ had, at
276
harvest, higher SSC compared to fruit from the reduced-fungicide treatment. Reganold et al18
277
reported higher SSC for organic ‘Diamante’ strawberries but similar SSC for organic and
278
conventional ‘Lanai’ and ‘San Juan’ strawberries. During cold storage, SSC of ‘Strawberry
279
Festival’ and ‘Florida Radiance’ declined significantly. Within each cultivar, the highest
280
decrease in SSC was for reduced-fungicide ‘Strawberry Festival’ (58.0%) and conventional
281
‘Florida Radiance’ (52.1%). Though, after storage there was no significant difference between
282
SSC of organic and reduced-fungicide ‘Strawberry Festival’, SSC of conventional strawberries
283
was significantly lower compared to other treatments. After 7 days, there was no significant
284
difference in the SSC of ‘Florida Radiance’ from both treatments. Results from this and other
285
studies suggest that cultivar variability might have a greater impact on fruit acidity and SCC than
286
disease control treatments.
287
Ascorbic Acid Content. At harvest, ascorbic acid (AA) content of organic ‘Strawberry
288
Festival’ was significantly higher compared to fruit from the conventional or reduced-pesticide
289
treatments (Figure 4). Initial AA contents of ‘Florida Radiance’ from conventional and reduced-
290
pesticide treatments were not significantly different. Others reported that the difference in the
291
levels of AA between conventional and organic strawberries is cultivar dependent and that
292
genotype and environmental conditions may have a greater impact on AA levels than cultivation
293
methods. Therefore, controversial reports have been published with some showing no difference
294
or significantly higher levels of AA in organic compared to conventional strawberries.22-23, 40 For
295
example, Hakala et al.40 showed no significant difference in the levels of vitamin C of organic
13 ACS Paragon Plus Environment
Journal of Agricultural and Food Chemistry
Page 14 of 47
296
‘Jonsok’, ‘Polka’ and ‘Honeoye’ strawberries compared to conventionally-grown fruit. Olsson et
297
al.22 reported that AA and vitamin C contents of organic ‘Cavendish’ strawberries were similar
298
to conventional fruit, but AA levels of organic ‘Honeoye’ were higher compared to
299
conventionally-grown fruit. Several recent studies showed that organic strawberries tend to have
300
higher levels of AA compared to conventional fruit.18,
301
‘Diamante’, ’Lanai’ and ‘San Juan’ organic strawberries was on average 9.7% higher compared
302
to conventional fruit.18
20, 41
For example, AA content of
303
After cold storage, AA content of ‘Strawberry Festival’ from the conventional and reduced-
304
fungicide treatments declined by approximately 47.9 and 51.3%, respectively whereas a decrease
305
in AA content of organic fruit was approximately 49.1%. Although after storage AA content
306
remained significantly higher in organic ‘Strawberry Festival’, AA content of fruit from other
307
treatments was not significantly different. Similarly, AA content of conventional and reduced-
308
fungicide ‘Florida Radiance’ was not significantly different after storage. One previous study
309
also showed that organic ‘Earligow’ and ‘Allstar’ strawberries had higher levels of AA
310
compared to conventional strawberries at harvest and after 7 days at 0, 5 or 10 °C.19 Unlike in the
311
present study, Jin et al.19 reported that AA levels increase during storage, regardless of the
312
cultivation method, and that AA levels were higher in fruit exposed to 5 or 10 °C compared to 0
313
°C. However, AA was reported on fresh weight, and it is possible that the increase reported by
314
Jin et al.19 was caused by a concentration effect due to loss of water rather than to an actual
315
increase.
316
Total Phenolic and Anthocyanin Contents. Total polyphenol (TPC) and anthocyanin
317
(ANC) contents of ‘Strawberry Festival and ‘Florida Radiance’ showed similar patterns (Figure
318
4). At harvest, TPC was significantly higher in organic ‘Strawberry Festival’ (25.6 g kg-1),
14 ACS Paragon Plus Environment
Page 15 of 47
Journal of Agricultural and Food Chemistry
319
followed by reduced-fungicide and conventional strawberries (21.1 and 20.2 g kg-1,
320
respectively). Anthocyanin content (ANC) was also higher in organic ‘Strawberry Festival’
321
compared to other treatments, yet there was a less marked difference in ANC between organic
322
and reduced-fungicide fruit (Figure 4). The levels of ANC in conventional ‘Strawberry Festival’
323
were 21% lower compared to fruit from both organic of reduced-fungicide treatments. At
324
harvest, TPC and ANC of ‘Florida Radiance’, from conventional and reduced-fungicide
325
treatments were similar (17.4 and 16.5 g TPC kg-1; 1.8 and 1.7 g ANC kg-1, respectively). One
326
single study reported that strawberry cultivars from integrated pest management had lower TPC
327
and ANC compared to organic fruit
328
higher TPC and ANC than conventional fruit.18-20, 22
21
. Others have also shown organic strawberries having
329
After cold storage, there was a significant decline in TPC of ‘Strawberry Festival’, yet TPC
330
of organic fruit remained the highest compared to the other treatments. After 7 days, there was
331
no significant difference between the TPC of conventional and reduced-fungicide ‘Strawberry
332
Festival or ‘Florida Radiance’ (Figure 4). A significant decline in ANC was also observed during
333
storage, with organic ‘Strawberry Festival’ having the lowest decline (38.7%) compared to fruit
334
from conventional and reduced-fungicide treatments (48.6 and 60.8%). ANC of ‘Florida
335
Radiance’ from conventional and reduced-fungicide also declined during storage, but the levels
336
remained comparable. Jin et al.19 reported that TPC and ANC levels increase during storage,
337
regardless of the cultivation method, and were higher in fruit exposed to 5 or 10 °C compared to
338
0 °C. However, like for AA, TPC and ANC were reported on fresh weight, and it is possible that
339
the increase reported by Jin et al.19 was caused by a concentration effect due to loss of water
340
during storage, rather than to an actual increase. In fact, Shin et al.42 reported that the marked
341
decline in total flavonoid and phenolic concentrations in strawberries after 12 days of storage at
15 ACS Paragon Plus Environment
Journal of Agricultural and Food Chemistry
Page 16 of 47
342
10 °C paralleled the increase in water loss and a decrease in anthocyanin concentration. Thus, in
343
shelf life studies to determine the actual changes in chemical compounds, and to show the
344
differences between treatments that might be obscured by differences in water content,
345
concentrations of chemical constituents should be expressed in dry weight.
346
Polyphenol Profiles of ‘Strawberry Festival’ from Different Disease Control
347
Treatments. Polyphenol profiles were only obtained for ‘Strawberry Festival’ due to
348
unavailability of ‘Florida Radiance’ organic strawberries. Regardless of the disease control
349
treatment or storage period, pelargonidin 3-glucoside was the major polyphenol measured in
350
conventional, reduced and organic fruit (9.8, 16.7 and 19.8%, respectively), followed by
351
quercetin (4.0, 3.5 and 3.2%, respectively), quercetin 3-glucoside (3.6, 4.5 and 2.9%,
352
respectively), kaempferol 3-glucoside (2.3, 1.9 and 2.4%, respectively) and coumaric acid (1.0,
353
1.8 and 2.0%, respectively) (Figure 6). Other polyphenols were also detected but at levels lower
354
than 2%. Overall, there were significant differences in the levels of each polyphenol measured
355
between disease control treatments. At harvest, organic strawberries had significantly higher
356
levels of pelargonidin 3-glucoside, catechin and coumaric acid compared to fruit from
357
conventional or reduced-fungicide treatments (Figure 6A). Crecente-Campo et al.20 also reported
358
higher levels of pelargonidin 3-glucoside and cyanidin 3-glucoside in organic strawberries than
359
in conventional fruit. In this study, compared to conventional ‘Strawberry Festival’, strawberries
360
from the reduced-fungicide treatment had significantly higher levels of cyanidin 3-glucoside,
361
pelargonidin 3-glucoside, coumaric, chlorogenic and ellagic acids. A previous study reported that
362
organic ‘Cavendish’ strawberries had higher levels of cyanidin and pelargonidin but lower levels
363
of flavonols compared to conventionally-grown fruit whereas organic ‘Honeoye’ had lower
364
levels or ellagic acid, cyanidin and pelargonidin than conventional fruit.22 Others have reported
16 ACS Paragon Plus Environment
Page 17 of 47
Journal of Agricultural and Food Chemistry
365
mixed or no differences in kaempferol, quercetin, ellagic and p-coumaric acids between organic
366
and conventional strawberry cultivars18-19, 24. It appears that the levels of specific polyphenols,
367
other than the major anthocyanins, are more influenced by cultivar than by cultivation method.
368
However, there seems to be an agreement among published data that pelargonidin 3-glucoside
369
and cyanidin 3-glucoside are higher in organic than in conventional fruit.19-20,
370
strawberry cultivars from integrated pest management cultivation also showed lower levels
371
pelargonidin 3-glucoside and cyanidin 3-glucoside than organic fruit.21 Some have suggested that
372
in organic agriculture, the limited use of pesticides contributes to increased pest pressure and
373
induces plants to develop more robust defense mechanisms such as increasing the synthesis of
374
polyphenols.
375
may affect plant growth, nutritional composition an synthesis of polyphenols.13
13-14, 20, 24-26
22
Different
In addition, soil composition, particularly the availability of nitrogen,
376
After cold storage, the major differences in the polyphenol profiles were the increase in
377
levels of epicatechin and ellagic acid in organic fruit compared to other treatments and
378
significantly higher levels of quercetin in conventional fruit compared to other treatments (Figure
379
6B). Some other individual polyphenols also increased or decreased during storage depending on
380
the treatment. For example, in conventional strawberries, pelargonidin 3-glucoside increased
381
during storage whereas it decreased in reduced-fungicide and organic fruit. Jin et al.19 showed
382
that cyanidin 3-glucoside increased in organic and conventional ‘Allstar’ after storage at 0 °C but
383
no significant increase in cyanidin 3-glucoside or pelargonidin 3-glucoside was reported for
384
organic or conventional ‘Earliglow’ strawberries. In addition, no significant increases were
385
reported for ellagic acid, quercetin 3-glucoside and kaempferol 3-glucoside in organic and
386
conventional ‘Allstar’ and Earliglow’ strawberries after 7 days of storage at 0 °C.19 On average,
387
at harvest, and based on the sum of individual polyphenols measured, there was no significant
17 ACS Paragon Plus Environment
Journal of Agricultural and Food Chemistry
Page 18 of 47
388
difference between organic and reduced-fungicide fruit whereas conventional fruit had
389
significantly lower percentage of polyphenol compounds (Figure 6C). Compared to data
390
obtained from TPC (Figure 4) the results agree as the levels of TPC were significantly lower in
391
conventional fruit and similar between reduced-fungicide and organic fruit. However, after 7
392
days there was an increase in the sum of individual polyphenols measured in conventional fruit
393
whereas there was no change in other treatments compared to initial values (Figure 6C). These
394
results are not in agreement with those from TPC where there was a significant decreased in TPC
395
during storage, regardless of the treatment (Figure 4). This discrepancy may be due to a
396
concentration effect resulting from the loss of moisture during storage rather than an increase or
397
no change in the polyphenol profiles. In fact, to compensate from water loss, TPC was expressed
398
in dry weight while the data (Area %) for individual polyphenols were based on fruit fresh
399
weight. Because area percentage was used to estimate the levels of individual polyphenols
400
detected in strawberries, it did not seem accurate to calculate these values in dry weight.
401
Sugar Profiles. Although there is quite some variability in sugar content amongst strawberry
402
cultivars, in general sucrose has the lowest contribution to the total sugar content whereas
403
concentrations of glucose and fructose are approximately on 1:1 ratio.43 At harvest, sucrose
404
levels of conventional ‘Florida Radiance’ were approximately 3-fold higher than in conventional
405
‘Strawberry Festival’ (Figure 5). However, sucrose contents of ‘Strawberry Festival’ and
406
‘Florida Radiance’ from the reduced treatment were not significantly different. Within cultivars,
407
conventional ‘Strawberry Festival’ had significantly lower sucrose levels at harvest compared to
408
fruit from the reduced or organic treatments (Figure 5). Reduced and organic ‘Strawberry
409
Festival’ had similar sucrose levels at harvest. Conversely, at harvest, sucrose content was
410
significantly higher in conventional ‘Florida Radiance’ compared to the fruit from the reduced
18 ACS Paragon Plus Environment
Page 19 of 47
Journal of Agricultural and Food Chemistry
411
treatment. After 7 days, sucrose levels decreased significantly, regardless of the cultivar or
412
treatment. Conventional ‘Strawberry Festival’ showed the highest decrease in sucrose content
413
(91%) followed by fruit from the reduced and organic treatments (80 and 74% %, respectively).
414
Sucrose levels of ‘Florida Radiance’ also decreased after storage. However, the decrease was
415
significantly higher in fruit from the reduced-fungicide treatment compared to the conventional
416
(68 and 61%, respectively).
417
Although in a previous study Reganold et al.18 reported no difference in reducing (glucose
418
and fructose) or total sugars between conventional and organic strawberries, in this study glucose
419
and fructose were higher in ‘Strawberry Festival’ from the conventional or reduced treatments
420
and lower in fruit from organic treatments (Figure 5). ‘Florida Radiance’ from the reduced-
421
fungicide treatment had higher glucose and fructose contents than conventional fruit. Within
422
cultivars, there was no significant difference in glucose and fructose contents of conventional
423
and reduced ‘Strawberry Festival’ both at harvest and after storage. Although organic fruit had
424
lower glucose and fructose levels at harvest compared to the other treatments, there was no
425
significant difference between treatments after storage. Nonetheless, after cold storage, organic
426
‘Strawberry Festival’ had the lowest decrease in glucose and fructose contents (45 and 48%,
427
respectively) compared to fruit from the conventional (52 and 55%, respectively) and reduced
428
treatments (57 and 60%, respectively). A similar trend was observed for ‘Florida Radiance’
429
where fruit from the reduced treatment had significantly higher glucose and fructose levels at
430
harvest but no difference after cold storage.
431
Residual Fungicides. Organic ‘Strawberry Festival’ was used as a control as no detectable
432
levels for any of the fungicides were measured in the fruit (data not shown). Eight different
433
active fungicide compounds namely, captan, fludioxonil, penthiopyrad, fenhexamid, cyprodinil,
19 ACS Paragon Plus Environment
Journal of Agricultural and Food Chemistry
Page 20 of 47
434
cyflufenamid, azoxystrobin, and pyraclostrobin, were measured (Tables 4 and 5). There was
435
significant variability between harvests and cultivars regarding the presence and levels of these
436
compounds in the fruit but pyraclostrobin was never detected in the fruit. In the first harvest,
437
only fludioxonil and cyprodinil were detected in conventional and reduced-fungicide ‘Strawberry
438
Festival’ (Table 4). On average, cyprodinil was detected at higher levels (0.398 and 0.260 ppm
439
in conventional and reduced fruit, respectively) than fludioxonil (0.143 and 0.113 ppm in
440
conventional and reduced fruit, respectively). There was no trend observed in the levels of
441
fludioxonil and cyprodinil between the day of harvest and after 3 and 7 days of storage most
442
likely due to sample variability. Even so, levels of these two fungicides were on average higher
443
in conventional fruit than in fruit from reduced-fungicide treatment. In ‘Florida Radiance’
444
strawberries from the first harvest other than fludioxonil and cyprodinil, fungicides captan,
445
fenhexamid and cyflufenamid were also detected (Table 5). However, only cyflufenamid was
446
measured on both fruit from the conventional and reduced-fungicide treatments, but the levels
447
were not significantly different between treatments. Conventional strawberries had higher levels
448
of captan and fenhexamid compared to fruit from the reduced-fungicide treatment, which
449
showed no detectable levels. In contrast, strawberries from the reduced-fungicide treatment had
450
higher levels of fludioxonil and cyprodinil compared to conventional fruit, which showed no
451
detectable levels. In the second harvest, captan, fludioxonil, penthiopyrad and cyprodinil were
452
measure in ‘Strawberry Festival’ (Table 4). Captan was higher in conventional strawberries
453
compared to the reduced-fungicide fruit, which showed no detectable levels. Unlike in the first
454
harvest, levels of fludioxonil and cyprodinil were slightly higher in ‘Strawberry Festival’ from
455
the reduced-fungicide compared to the conventional treatment. Levels of penthiopyrad were not
456
significantly different between disease control treatments. Although there was no trend in the
20 ACS Paragon Plus Environment
Page 21 of 47
Journal of Agricultural and Food Chemistry
457
levels of these compounds during storage, captan tended to be higher in conventional
458
‘Strawberry Festival’ at harvest than after 7 days of storage (Table 4). In ‘Florida Radiance’ from
459
the second harvest, captan, fludioxonil, penthiopyrad, fenhexamid, cyprodinil cyflufenamid and
460
azoxystrobin were measured in the fruit (Table 5). On average, conventional strawberries had
461
higher levels of captan, fludioxonil, cyprodinil, and azoxystrobin compared to the reduced-
462
fungicide fruit which had higher levels of penthiopyrad, fenhexamid and cyflufenamid. In an
463
earlier analysis of pesticide residue data from organic and non-organic fresh fruits and
464
vegetables, Baker et al.44 also found higher levels of captan in conventional strawberries (1.1084
465
ppm) compared to fruit from integrated pest management (0.1200 ppm). In the second harvest,
466
the residual levels of fenhexamid and cyflufenamid in conventional ‘Florida Radiance’ were
467
slightly lower than that measured in fruit from the reduced-fungicide treatment most likely
468
because in conventional strawberries Elevate was applied on February 4 (14 days before harvest)
469
whereas in the reduced-fungicide treatment Elevate was applied on February 10 (8 days before
470
harvest). Thus, it seems that the levels of fungicides in the fruit were more influenced by when
471
the fungicide was applied, relative to the sampling date, than to how much or how many times it
472
was applied. The United States Environmental Protection Agency (USEPA) establishes 20 ppm
473
for captan, 3 ppm for fludioxonil, penthiopyrad and fenhexamid, 5 ppm for cyprodinil, 0.2 ppm
474
for cyflufenamid, 10 ppm for azoxystrobin, and 1.2 ppm for pyraclostrobin.45 Therefore, the
475
levels of fungicides found in all strawberry cultivars from any disease control treatments used in
476
this study were well below the tolerances established by the USEPA. Others have suggested that
477
the benefits or reducing human exposure to pesticides by substituting conventional by organic
478
produce is insignificant because the exposure to pesticide residues from consuming a standard
479
diet poses minimal risk to humans.46
21 ACS Paragon Plus Environment
Journal of Agricultural and Food Chemistry
Page 22 of 47
480
In summary, ‘Strawberry Festival’ and ‘Florida Radiance’ strawberries grown under
481
reduced-fungicide applications had at harvest similar or better physicochemical quality than
482
conventionally-grown fruit. Organic ‘Strawberry Festival’ had higher phenolics, anthocyanins
483
and ascorbic acid contents but lower levels of glucose and fructose compared to conventional or
484
reduced-fungicide strawberries. After cold storage, consumer-sensory panels did not show liking
485
preference between organic, reduced-fungicide and conventional fruit. Physicochemical quality
486
of reduced-fungicide ‘Strawberry Festival’ and ‘Florida Radiance’ was comparable to that of
487
conventional and organic fruit. Organic strawberries were softer after storage but maintained its
488
higher levels of phenolics, anthocyanins and ascorbic acid. On average, strawberries from the
489
reduced-fungicide treatment had lower levels of fungicides than conventional fruit. Overall,
490
results showed that flavor- and health-related attributes of strawberries from the reduced-
491
fungicide treatment were intermediate between conventional and organic fruit. Thus, growing
492
strawberries with reduced-fungicide applications can be an alternative to conventional disease
493
control or organic practices.
494
22 ACS Paragon Plus Environment
Page 23 of 47
495
Journal of Agricultural and Food Chemistry
REFERENCES
496
(1) Zafra-Stone, S.; Yasmin, T.; Bagchi, M.; Chatterjee, A.; Vinson, J. A.; Bagchi, D. Berry
497
anthocyanins as novel antioxidants in human health and disease prevention. Mol. Nutr. Food
498
Res. 2007, 51, 675-683.
499 500 501 502
(2) Giampieri, F.; Alvarez-Suarez, J. M.; Battino, M.. Strawberry and human health: effects beyond antioxidant activity. J. Agric. Food Chem. 2014, 62, 3867-3876. (3) Nile, S.H.; Park, S.W. Edible berries: bioactive components and their effect on human health. Nutrition 2014, 30, 134-144.
503
(4) Afrin, S.; Gasparrini, M.; Forbes-Hernandez, T.Y.; Rebodero-Rodriguez, P.; Mezzetti,
504
B.; Varela-López, A.; Giampieri, F.; Battino, M. Promissing health benefits of the strawberry: a
505
focus on clinical studies. J. Agric. Food Chem. 2016, 64, 4435-4449.
506 507
(5) Capocasa, F.; Scalzo, J.; Mezzetti, B.; Battino, M. Combining quality and antioxidant attributes in the strawberry: The role of genotype. Food Chem. 2008, 111, 872-878.
508
(6) Singh, A.; Singh, B. K.; Deka, B. C.; Sanwal, S. K.; Patel, R. K.; Verma, M. R. The
509
genetic variability, inheritance and inter-relationships of ascorbic acid, β-carotene, phenol and
510
anthocyanin content in strawberry (Fragaria×ananassa Duch.). Scientia Hort. 2011, 129, 86-90.
511
(7) Tulipani, S.; Marzban, G.; Herndl, A.; Laimer, M.; Mezzetti, B.; Battino, M. Influence of
512
environmental and genetic factors on health-related compounds in strawberry. Food Chem. 2011,
513
124, 906-913.
514
(8) Kelly, K.; Whitaker, V. M.; Nunes, M. C. N. Physicochemical characterization and
515
postharvest performance of the new Sensation ® ‘Florida127’ strawberry compared to
516
commercial standards. Scientia Hort. 2016, 211, 283-294.
23 ACS Paragon Plus Environment
Journal of Agricultural and Food Chemistry
Page 24 of 47
517
(9) Kelly, K.; Nunes, M. C.N. ; Whitaker, V. M. A comparison of physical and chemical
518
attributes of strawberry cultivars and advanced breeding selections from the University of
519
Florida. Proc. Fla. State Hort. Sco. 2016, 129, 185-189.
520
(10)
Fredericks, C. H.; Fanning, K. J.; Gidley, M. J.; Netzel, G.; Zabaras, D.;
521
Herrington, M.; Netzel, M. High-anthocyanin strawberries through cultivar selection. J. Sci.
522
Food Agric. 2013, 93, 846-852.
523
(11)
Aaby, K.; Mazur, S.; Nes, A.; Skrede, G. Phenolic compounds in strawberry
524
(Fragaria x ananassa Duch.) fruits: Composition in 27 cultivars and changes during ripening.
525
Food Chem. 2012, 132, 86-97.
526
(12)
Cayo, Y. P.; Sargent, S.; Nunes, C. d. N.; Whitaker, V. Composition of
527
Commercial Strawberry Cultivars and Advanced Selections as Affected by Season, Harvest, and
528
Postharvest Storage. HortScience 2016, 51, 1134-1143.
529
(13)
Mitchell, A. E.; Hong, Y.-J.; Koh, E.; Barrett, D. M.; Bryant, D.; Denison, R. F.;
530
Kaffka, S. Ten-year comparison of the influence of organic and conventional crop management
531
practices on the content of flavonoids in tomatoes. J. Agric. Food Chem. 2007, 55, 6154-6159.
532
(14)
Martí, R.; Leiva-Brondo, M.; Lahoz, I.; Campillo, C.; Cebolla-Cornejo, J.;
533
Roselló, S. Polyphenol and L-ascorbic acid content in tomato as influenced by high lycopene
534
genotypes and organic farming at different environments. Food Chem. 2018, 239, 148-156.
535
(15)
Ren, F.; Reilly, K.; Kerry, J. P.; Gaffney, M.; Hossain, M.; Rai, D. K. Higher
536
Antioxidant Activity, Total Flavonols, and Specific Quercetin Glucosides in Two Different
537
Onion (Allium cepa L.) Varieties Grown under Organic Production: Results from a 6-Year Field
538
Study. J. Agric. Food. Chem. 2017, 65, 5122-5132.
24 ACS Paragon Plus Environment
Page 25 of 47
539
Journal of Agricultural and Food Chemistry
(16)
Wang, S. Y.; Chen, C.-T.; Sciarappa, W.; Wang, C. Y.; Camp, M. J. Fruit quality,
540
antioxidant capacity, and flavonoid content of organically and conventionally grown blueberries.
541
J. Agric. Food Chem. 2008, 56, 5788-5794.
542
(17)
Nunes, M. C. N. Chapter 3. Soft Berries. In Color Atlas of Postharvest Quality of
543
Fruits and vegetables; Nunes, M.C.N., Ed.; John Wiley & Sons: Ames, Iowa, USA, 2008, pp.
544
175-184 .
545
(18)
Reganold, J. P.; Andrews, P. K.; Reeve, J. R.; Carpenter-Boggs, L.; Schadt, C.
546
W.; Alldredge, J. R.; Ross, C. F.; Davies, N. M.; Zhou, J. Fruit and soil quality of organic and
547
conventional strawberry agroecosystems. PLoS One 2010, 5, 1-14.
548
(19)
Jin, P.; Wang, S. Y.; Wang, C. Y.; Zheng, Y. Effect of cultural system and storage
549
temperature on antioxidant capacity and phenolic compounds in strawberries. Food Chem. 2011,
550
124, 262-270.
551
(20)
Crecente-Campo, J.; Nunes-Damaceno, M.; Romero-Rodríguez, M. A.; Vázquez-
552
Odériz, M. L. Color, anthocyanin pigment, ascorbic acid and total phenolic compound
553
determination in organic versus conventional strawberries (Fragaria×ananassa Duch, cv Selva).
554
J. Food Compos. Anal. 2012, 28, 23-30.
555
(21)
Fernandes, V. C.; Domingues, V. F.; de Freitas, V.; Delerue-Matos, C.; Mateus,
556
N. Strawberries from integrated pest management and organic farming: phenolic composition
557
and antioxidant properties. Food Chem. 2012, 134, 1926-1931.
558
(22)
Olsson, M. E.; Andersson, C. S.; Oredsson, S.; Berglund, R. H.; Gustavsson, K.-
559
E. Antioxidant levels and inhibition of cancer cell proliferation in vitro by extracts from
560
organically and conventionally cultivated strawberries. J. Agric. Food Chem. 2006, 54, 1248-
561
1255.
25 ACS Paragon Plus Environment
Journal of Agricultural and Food Chemistry
562
(23)
Page 26 of 47
Cardoso, P. C.; Tomazini, A. P. B.; Stringheta, P. C.; Ribeiro, S. M. R.; Pinheiro-
563
Sant’Ana, H. M. Vitamin C and carotenoids in organic and conventional fruits grown in Brazil.
564
Food Chem. 2011, 126, 411-416.
565
(24)
Häkkinen, S. H.; Törrönen, A. R. Content of flavonols and selected phenolic acids
566
in strawberries and Vaccinium species: influence of cultivar, cultivation site and technique. Food
567
Res. Int. 2000, 33, 517-524.
568
(25)
Young, J. E.; Zhao, X.; Carey, E. E.; Welti, R.; Yang, S. S.; Wang, W.
569
Phytochemical phenolics in organically grown vegetables. Mol. Nutr. Food Res. 2005, 49, 1136-
570
1142.
571
(26)
Winter, C. K.; Davis, S. F. Organic Foods. J. Food Sci. 2006, 71, R117-R124.
572
(27)
Peres, N.; MacKenzie, S. In Development of a Forecast System for Control of
573
Strawberry Anthracnose, Proc. of the Colletotrichum Diseases of Fruit Crops Workshop at
574
International Congress of Plant Pathology, 2009; pp 47-48.
575 576 577
(28)
USDA United States department of Agriculture National Organic Program.
http://www.ams.usda.gov/AMSv1.0/nop (accessed March 18, 2018). (29)
Nunes, M. C. N.; Emond, J. P.; Rauth, M.; Dea, S.; Chau, K. V. Environmental
578
conditions encountered during typical consumer retail display affect fruit and vegetable quality
579
and waste. Postharvest. Biol. Technol. 2009, 51, 232-241.
580
(30)
Pelletier, W.; Brecht, J. K.; Nunes, M. C. N.; Emond, J.-P. Quality of strawberries
581
shipped by truck from California to Florida as influenced by postharvest temperature
582
management practices. HortTechnology 2011, 21, 482-493.
26 ACS Paragon Plus Environment
Page 27 of 47
583
Journal of Agricultural and Food Chemistry
(31)
Lai, Y.; Emond, J.-P.; Nunes, M.C.N. Environmental conditions encountered
584
during distribution from the field to the store affect the quality of strawberry (‘Albion’). Proc.
585
Fla. State Hort. Soc. 2011, 124, 213-220.
586 587 588
(32)
Whitaker, V. M.; Chandler, C. K.; Santos, B. M.; Peres, N.; Nunes, M. C. N.;
Plotto, A.; Sims, C. A. Winterstar™(‘FL 05-107’) strawberry. HortScience 2012, 47, 296-298. (33)
Nunes, M. C.N.; Brecht, J.; Morais, A.; Sargent, S. Physical and chemical quality
589
characteristics of strawberries after storage are reduced by a short delay to cooling. Postharvest
590
Biol. Technol. 1995, 6, 17-28.
591 592 593
(34)
Nunes, M. C. N. Correlations between subjective quality and physicochemical
attributes of fresh fruits and vegetables. Postharvest Biol. Technol. 2015, 107, 43-54. (35)
Nunes, M. C. N.; Brecht, J. K.; Morais, A.; Sargent, S. A. Possible influences of
594
water loss and polyphenol oxidase activity on anthocyanin content and discoloration in fresh ripe
595
strawberry (cv. Oso Grande) during storage at 1 C. J. Food Sci. 2005, 70, S79-S84.
596
(36)
Abountiolas, M.; Nunes, M.C.N. Polyphenols, ascorbic acid and antioxidant
597
capacity of commercial nutritional drinks, fruit juices, smoothies and teas. Int. J. Food Sci.
598
Technol. 2018, 188-198.
599
(37)
Lehotay, S. J.; Kok, A. d.; Hiemstra, M.; Bodegraven, P. V. Validation of a fast
600
and easy method for the determination of residues from 229 pesticides in fruits and vegetables
601
using gas and liquid chromatography and mass spectrometric detection. J. AOAC Int. 2005, 88,
602
595-614.
603
(38)
Lesueur, C.; Knittl, P.; Gartner, M.; Mentler, A.; Fuerhacker, M. Analysis of 140
604
pesticides from conventional farming foodstuff samples after extraction with the modified
605
QuECheRS method. Food Control 2008, 19, 906-914.
27 ACS Paragon Plus Environment
Journal of Agricultural and Food Chemistry
606
(39)
Page 28 of 47
Reganold, J. P.; Andrews, P. K.; Reeve, J. R.; Carpenter-Boggs, L.; Schadt, C.
607
W.; Alldredge, J. R.; Ross, C. F.; Davies, N. M.; Zhou, J. Fruit and soil quality of organic and
608
conventional strawberry agroecosystems. PloS one 2010, 5, e12346.
609
(40)
Hakala, M.; Lapveteläinen, A.; Huopalahti, R.; Kallio, H.; Tahvonen, R. Effects
610
of varieties and cultivation conditions on the composition of strawberries. J. Food Compos. Anal.
611
2003, 16, 67-80.
612 613 614
(41)
Nunes, M.C.N.; Delgado, A. Quality of organic compared to conventionally
grown strawberries at the retail level. Acta Hort. 2012, 1049 (723-730). (42)
Shin, Y.; Ryu, J.-A.; Liu, R. H.; Nock, J. F.; Watkins, C. B. Harvest maturity,
615
storage temperature and relative humidity affect fruit quality, antioxidant contents and activity,
616
and inhibition of cell proliferation of strawberry fruit. Postharvest Biol. Technol. 2008, 49, 201-
617
209.
618
(43)
Cordenunsi, B. R.; Oliveira do Nascimento, J. R.; Genovese, M. I.; Lajolo, F. M.
619
Influence of cultivar on quality parameters and chemical composition of strawberry fruits grown
620
in Brazil. J. Agric. Food Chem. 2002, 50, 2581-2586.
621
(44)
Baker, B. P.; Benbrook, C. M.; III, E. G.; Benbrook, K. L. Pesticide residues in
622
conventional, integrated pest management (IPM)-grown and organic foods: insights from three
623
US data sets. Food Addit. Contam. 2002, 19, 427-446.
624
(45)
625
Federal
626
idx?tpl=/ecfrbrowse/Title40/40cfr180_main_02.tpl (accessed March 18, 2018).
627
(46)
USEPA United States Environmental Protection Agency, Electronic Code of Regulations
40
CFR
Part
180.
https://www.ecfr.gov/cgi-bin/text-
Winter, C. K.; Davis, S. F. Organic foods. J. Food Sci. 2006, 71, 117-124.
628 629 28 ACS Paragon Plus Environment
Page 29 of 47
Journal of Agricultural and Food Chemistry
630
FUNDING SOURCES
631
This work was supported by the Specialty Crop Block Grant Program at the U.S. Department of
632
Agriculture (USDA) through grant 12-25-B-1663. Its contents are solely the responsibility of the
633
authors and do not necessarily represent the official views of the USDA. The authors would like
634
to thank Mr. Carl Grooms from Fancy Farms and Mr. Dudley Calfee from Ferris Farms, Inc. for
635
conducting the different disease control treatments and by providing the strawberry samples.
636
29 ACS Paragon Plus Environment
Journal of Agricultural and Food Chemistry
Page 30 of 47
637
Figure 1. Color attributes of ‘Strawberry Festival’ and ‘Florida Radiance’ strawberries from
638
different disease control treatments during storage at 1.5°C and 85% RH. Letters next to data
639
points denote significant differences between disease control treatments based on Fisher’s LSD
640
test at p ≤ 0.05. Data points are averages of two harvests; average data points with the same letter
641
are not significantly different.
642 643
Figure 2. Firmness and weight loss of ‘Strawberry Festival’ and ‘Florida Radiance’ strawberries
644
from different disease control treatments during storage at 1.5°C and 85% RH. Letters next to
645
data points denote significant differences between disease control treatments based on Fisher’s
646
LSD test at p ≤ 0.05. Data points are averages of two harvests; average data points with the same
647
letter are not significantly different.
648 649
Figure 3. Titratable acidity and soluble solids content (SSC) of ‘Strawberry Festival’ and ‘Florida
650
Radiance’ strawberries from different disease control treatments during storage at 1.5°C and 85%
651
RH. Letters next to data points denote significant differences between disease control treatments
652
based on Fisher’s LSD test at p ≤ 0.05. Data points are averages of two harvests; average data
653
points with the same letter are not significantly different.
654 655
Figure 4. Levels of bioactive compounds (total polyphenols, anthocyanins, and ascorbic acid
656
contents) of ‘Strawberry Festival’ and ‘Florida Radiance’ strawberries from different disease
657
control treatments during storage at 1.5°C and 85% RH. Letters next to data points denote
658
significant differences between disease control treatments based on Fisher’s LSD test at p ≤ 0.05;
30 ACS Paragon Plus Environment
Page 31 of 47
Journal of Agricultural and Food Chemistry
659
average data points with the same letter are not significantly different. Data points are averages of
660
two harvests; average data points with the same letter are not significantly different.
661 662
Figure 5. Sucrose, glucose and fructose contents of ‘Strawberry Festival’ and ‘Florida Radiance’
663
strawberries from different disease control treatments during storage at 1.5°C and 85% RH.
664
Letters next to data points denote significant differences between disease control treatments based
665
on Fisher’s LSD test at p ≤ 0.05. Data points are averages of two harvests; average data points
666
with the same letter are not significantly different.
667 668
Figure 6. Polyphenol profiles of ‘Strawberry Festival’ strawberries from conventional, reduced
669
and organic disease control treatments at harvest (A), after a 7-day storage period (B), and (C)
670
total polyphenols at harvest and after 7 days at 1.5°C and 85% RH. Letters above each bar denote
671
significant differences between disease control treatments based on Fisher’s LSD test at p ≤ 0.05.
672
Data are averages of two harvests; bars with the same letter within each polyphenolic compound
673
are statistically non-significant (ns).
674 675
31 ACS Paragon Plus Environment
Journal of Agricultural and Food Chemistry
Page 32 of 47
Table 1. Fungicides applied to ‘Florida Radiance’ strawberries grown in Plant City, Florida, USA, under conventional and reduced-fungicide disease control treatments. Date
Conventional
Reduced
10/29/2013
Quilt Xcel (a.ia azoxystrobin, propiconazole)
11/19/2013
11/29/2013
Captan + Thiram (a.i. captan,
Thiram (a.i. tetramethylthiuram
tetramethylthiuram disulfide)
disulfide)
Captan + Elevate (a.i. captan, fenhexamid)
12/07/2013
Switch (a.i. cyprodinil, fludioxonil)
12/19/2013
Captan (a.i. captan)
12/22/2013 12/26/2013
Switch (a.i. cyprodinil, fludioxonil)
Captan (a.i. captan) Captan (a.i. captan)
12/30/2013
Switch (a.i. cyprodinil, fludioxonil)
1/04/2014
Captan (a.i. captan)
1/08/2014
Captan + Thiram (a.i. captan,
Thiram (a.i. tetramethylthiuram
tetramethylthiuram disulfide)
disulfide)
Captan + Elevate + Torino (a.i. captan,
Torino (a.i. cyflufenamid)
1/15/2014
fenhexamid, cyflufenamid)
1/21/2014
Harvest 1
1/25/2014
Switch (a.i. cyprodinil, fludioxonil)
1/27/2014
Fontelis (a.i. penthiopyrad)
2/01/2014
Switch (a.i. cyprodinil, fludioxonil)
2/02/2014
Captan + Quilt Xcel (a.i. captan, azoxystrobin, propiconazole)
2/04/2014
Captan + Elevate (a.i. captan, fenhexamid)
2/10/2014
Captan (a.i. captan)
Captan + Elevate (a.i. captan,
32 ACS Paragon Plus Environment
Page 33 of 47
Journal of Agricultural and Food Chemistry
fenhexamid) 2/15/2014
Switch (a.i. cyprodinil, fludioxonil)
2/18/2014
Harvest 2
a
a.i = active ingredient.
33 ACS Paragon Plus Environment
Journal of Agricultural and Food Chemistry
Page 34 of 47
Table 2. Fungicides applied to ‘Strawberry Festival’ strawberries grown in Floral City, Florida, USA, under conventional and reduced-fungicide disease control treatments. Date
Conventional
Reduced
10/31/2013
Captec (a.ia captan)
Captec (a.i. captan)
11/8/2013
Captec (a.i. captan)
Captec (a.i. captan)
11/14/2013
Captec (a.i. captan)
11/18/2013
Captec (a.i. captan)
Captec (a.i. captan)
11/21/2013
Thiram (a.i. tetramethylthiuram
Thiram (a.i. tetramethylthiuram
disulfide)
disulfide)
11/29/2013
Captevate (a.i. captan, fenhexamid)
12/11/2013
Captec (a.i. captan)
12/19/2013
Captec (a.i. captan)
12/24/2013
Captec (a.i. captan)
Captec (a.i. captan)
1/2/2014
Switch (a.i. cyprodinil, fludioxonil)
Switch (a.i. cyprodinil, fludioxonil)
1/3/2014
Captec (a.i. captan)
Captec (a.i. captan)
1/10/2014
Fontellis (a.i. penthiopyrad)
Fontellis (a.i. penthiopyrad)
2/1/2014
Switch (a.i. cyprodinil, fludioxonil)
Switch (a.i. cyprodinil, fludioxonil)
2/7/2014
Harvest 1
2/11/2014
Fontellis (a.i. penthiopyrad)
2/19/2014
Captec (a.i. captan)
2/25/2014
Fontellis (a.i. penthiopyrad)
Fontellis (a.i. penthiopyrad)
3/7/2014
Captec (a.i. captan)
Captec (a.i. captan)
3/7/2014
Harvest 2
a
Captec (a.i. captan)
Fontellis (a.i. penthiopyrad)
a.i = active ingredient.
34 ACS Paragon Plus Environment
Page 35 of 47
Journal of Agricultural and Food Chemistry
Table 3. Sensory quality of ‘Strawberry Festival’ and ‘Florida Radiance’ strawberries from conventional and reduced-fungicide disease control treatments after 3 days storage at 1.5°C and 85% RH. Appearancea
Texturea
Flavora
Overall likinga
Conventional
6.71 abb
6.90 a
6.36 a
6.49 a
Reduced
6.39 b
6.83 a
6.19 a
6.30 a
Organic
6.93 a
6.63 a
6.19 a
6.44 a
Conventional
7.29 a
7.38 a
7.30 a
7.34 a
Reduced
7.15 a
6.90 b
7.00 b
7.02 a
Conventional
6.46 a
6.83 a
6.21 a
6.42 a
Reduced
6.62 a
6.85 a
6.29 a
6.41 a
Organic
6.73 a
6.65 a
5.93 a
6.14 a
Conventional
6.75 a
6.54 a
6.10 a
6.34 a
Reduced
6.38 a
6.46 a
5.99 a
6.22 a
Cultivar/Treatment Harvest 1 ‘Strawberry Festival’
‘Florida Radiance’
Harvest 2 ‘Strawberry Festival’
‘Florida Radiance’
a
1 = dislike extremely; 5 = neither like nor dislike; 9 = like extremely.
b
Letters after averages denote significant differences (p < 0.05) between disease control
treatments based on Tukey’s HSD test; averages followed by the same letter are not significantly different.
35 ACS Paragon Plus Environment
Journal of Agricultural and Food Chemistry
Page 36 of 47
36 ACS Paragon Plus Environment
Page 37 of 47
Journal of Agricultural and Food Chemistry
Table 4. Residual fungicides on ‘Strawberry Festival’ from conventional and reduced-fungicide disease control treatments at harvest (day 0) and after 3 and 7 days of storage at 1.5°C and 85% RH. Captan
Fludioxonil
Penthiopyrad
Fenhexamid
Cyprodinil
Cyflufenamid
Azoxystrobin
Pyraclostrobin
(ppm)
(ppm)
(ppm)
(ppm)
(ppm)
(ppm)
(ppm)
(ppm)
Harvest 1 Conventional 0
N.D.
0.152 ab
N.D.
N.D.
0.340 b
N.D.
N.D.
N.D.
3
N.D.
0.119 b
N.D.
N.D.
0.367 ab
N.D.
N.D.
N.D.
7
N.D.
0.159 a
N.D.
N.D.
0.488 a
N.D.
N.D.
N.D.
-
-
0.398 A
-
-
-
Average
a
c
-
0.143 A
0
N.D.
0.099 b
N.D.
N.D.
0.204 b
N.D.
N.D.
N.D.
3
N.D.
0.129 a
N.D.
N.D.
0.293 a
N.D.
N.D.
N.D.
7
N.D.
0.112 b
N.D.
N.D.
0.285 a
N.D.
N.D.
N.D.
Average
-
0.113 B
-
-
0.260 B
-
-
-
0
4.023 a
0.002 a
0.021 a
N.D.
0.006 a
N.D.
N.D.
N.D.
3
3.937 a
0.002 a
0.018 a
N.D.
0.005 a
N.D.
N.D.
N.D.
7
3.476 b
0.002 a
0.026 a
N.D.
0.006 a
N.D.
N.D.
N.D.
Average
3.812
0.002 B
0.022 A
-
0.006 B
-
-
-
Reduced
Harvest 2 Conventional
Reduced
37 ACS Paragon Plus Environment
Journal of Agricultural and Food Chemistry
Page 38 of 47
0
N.D.
0.004 a
0.026 a
N.D.
0.006 b
N.D.
N.D.
N.D.
3
N.D.
0.005 a
0.023 a
N.D.
0.008 a
N.D.
N.D.
N.D.
7
N.D.
0.004 a
0.021 a
N.D.
0.006 b
N.D.
N.D.
N.D.
Average
-
0.004 A
0.023 A
-
0.007 A
-
-
-
a
N.D. = Not detected.
b
c
Means separations are within disease control treatments and days of storage and within columns by the Fisher’s LSD test at P ≤ 0.05.
Means separations are within harvests and within columns by the Fisher’s LSD test at P ≤ 0.05.
38 ACS Paragon Plus Environment
Page 39 of 47
Journal of Agricultural and Food Chemistry
Table 5. Residual fungicides on ‘Florida Radiance’ from conventional and reduced-fungicide disease control treatments at harvest (day 0) and after 3 and 7 days of storage at 1.5°C and 85% RH. Captan
Fludioxonil
Penthiopyrad
Fenhexamid
Cyprodinil
Cyflufenamid
Azoxystrobin
Pyraclostrobin
(ppm)
(ppm)
(ppm)
(ppm)
(ppm)
(ppm)
(ppm)
(ppm)
Harvest 1 Conventional 0
3.144 ba
N.D.b
N.D.
0.224 b
N.D.
0.015 b
N.D.
N.D.
3
4.596 a
N.D.
N.D.
0.320 a
N.D.
0.025 a
N.D.
N.D.
7
3.638 b
N.D.
N.D.
0.220 b
N.D.
0.019 b
N.D.
N.D.
-
-
0.254
-
0.020 A
-
-
Average
3.792
c
Reduced 0
N.D.
0.027 a
N.D.
N.D.
0.018 ab
0.016 a
N.D.
N.D.
3
N.D.
0.025 a
N.D.
N.D.
0.016 b
0.016 a
N.D.
N.D.
7
N.D.
0.026 a
N.D.
N.D.
0.019 a
0.015 a
N.D.
N.D.
Average
-
0.026
-
-
0.017
0.016 A
-
-
0
3.008 a
0.388 a
N.D.
0.105 b
0.474 a
N.D.
0.019 a
N.D.
3
2.066 b
0.162 c
N.D.
0.194 a
0.282 c
N.D.
0.011 b
N.D.
7
2.175 b
0.232 b
N.D.
0.090 b
0.397 b
N.D.
0.018 b
N.D.
Average
2.416 A
0.261 A
-
0.130 B
0.384 A
-
0.016
-
Harvest 2 Conventional
Reduced
39 ACS Paragon Plus Environment
Journal of Agricultural and Food Chemistry
Page 40 of 47
0
1.493 a
0.125 a
0.010 a
0.204 b
0.110 b
0.009 a
N.D.
N.D.
3
1.796 a
0.135 a
0.009 a
0.271 a
0.138 a
0.001 b
N.D.
N.D.
7
1.360 a
0.084 b
0.010 a
0.113 c
0.099 b
0.007 a
N.D.
N.D.
Average
1.550 B
0.115 B
0.010
0.196 A
0.116 B
0.006
-
-
a
Means separations are within disease control treatments and days of storage and within columns by the Fisher’s LSD test at P ≤ 0.05.
b
N.D. = Not detected.
c
Means separations are within harvests and within columns by the Fisher’s LSD test at P ≤ 0.05.
40 ACS Paragon Plus Environment
Page 41 of 47
Journal of Agricultural and Food Chemistry
'Strawberry Festival'
'Florida Radiance'
40 38
Conventional Reduced
[
a
L* value
36
]
b
34
[
a
32
b Conventional Reduced Organic
30
p