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Article

Combined Effects of Cold Treatment and Phosphine in Drosophila suzukii (Diptera: Drosophilidae)

by
Seung-Ju Seok
†,
Hyun Kyung Kim
†,
Hyun-Na Koo
and
Gil-Hah Kim
*
Department of Plant Medicine, College of Agriculture, Life and Environment Science, Chungbuk National University, Cheongju 28644, Republic of Korea
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Appl. Sci. 2022, 12(24), 12531; https://doi.org/10.3390/app122412531
Submission received: 13 October 2022 / Revised: 8 November 2022 / Accepted: 28 November 2022 / Published: 7 December 2022
(This article belongs to the Special Issue Advances in Pest Treatment and Plant Protection)
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Abstract

:
This study analyzed the effect of combined phosphine (PH3) fumigation and low-temperature treatment on the control of Drosophila suzukii. In the low-temperature, single-treatment experiment, there was no significant difference in insecticidal activity between 1 °C and 5 °C except in D. suzukii adults. Adults showed 98.0% mortality after exposure to 1 °C for 7 d. Regarding fumigation treatment with PH3 alone, adults were the most susceptible, and pupae had the highest tolerance. Combined low-temperature treatment and fumigation showed a synergistic effect, except in the egg stage, and showed slight synergistic effects in larvae and pupae regardless of the combined treatment order. In pupae, the combination group exposed to 1 °C for 24 h after exposure to PH3 for 4 h had the lowest LCT99 value, at 10.49 mg·h/L. The sorption rate of PH3 on grapes decreased to 85.49% after 4 h of exposure, with a 15% loading ratio (w/v), and there was no significant difference in various criteria of phytotoxicity in exposed grapes compared to control, even after 14 d of combined treatment. Therefore, this study indicates that combined PH3 fumigation and low-temperature treatment could be useful in D. suzukii control.

1. Introduction

Most fruit flies target wounded or rotting fruit, but Drosophila suzukii (spotted wing drosophila) uses their serrated ovipositor to injure and damage fresh fruit [1,2]. This makes the fruit vulnerable to other pests and fungal infection after harvest, causing secondary damage [3]. D. suzukii originate from Southeast Asia but related economic damage has been reported in North America and many countries worldwide [4,5].
Fumigation treatment is a general method for the management of D. suzukii after crop harvesting. However, a high dose of fumigant or a long treatment time are required for effective control [6,7]. The most widely used fumigant is methyl bromide (MB), but the need for an alternative fumigant is increasing due to restrictions on the use of MB. One potential alternative is phosphine (PH3) [8,9,10]. PH3 is a fumigant mainly used for the control of pests of stored products, which has recently been used for the control of fruit and vegetables pests [11,12,13]. Aluminum phosphide (AlP) in tablet form has been used for several decades and is effective at controlling the rice weevil, Sitophilus oryzae, and the grain moth, Sitotroga cerealella [14,15]. AlP produces ammonia, which causes phytotoxicity in products, and requires a temperature of 15 °C or more to produce PH3; however, PH3 in the gaseous form was recently developed for the possible fumigation of fruit and vegetables at a lower temperature [16]. Fumigation effects of PH3 on various pests, such as the western flower thrips, Frankliniella occidentalis, the oleander scale, Aspidiotus nerii, the longtailed mealybug, Pseudococcus longispinus, the greedy scale, Hemiberlesia rapax, the two-spotted spider mite, Tetranychus urticae, the pumpkin fruit fly, Bactrocera tau, and the guava fruit fly, Bactrocera correcta, have been observed, even at a low temperature [17,18,19,20].
Low-temperature treatment is a physical pest-control method. The effects of low-temperature treatment have been researched for the control of quarantine pests such as the Caribbean fruit fly, Anastrepha suspensa, and the oriental fruit fly, Bactrocera dorsalis. This treatment method is used for quarantine pests in Japan [21,22,23,24]. However, increased cold tolerance after cold-temperature exposure has been observed not only in D. suzukii but also in various other insects, such as Drosophila melanogaster, the potato tuber moth, Phthorimaea perculella, and the Asian citrus psyllid, Diaphorina citri [25,26,27,28,29]. The efficacy of many fumigants (MB, carbonyl sulfide, sulfuryl fluoride, and PH3) is reduced when applied in cold-temperature conditions to maintain product freshness [30,31,32]. Recently, it has become necessary to research a new strategy to address the effect of cold treatment on fumigation and solve this problem.
To this end, this study investigated the effects of cold treatment and PH3 fumigation combination on D. suzukii control on grapes.

2. Materials and Methods

2.1. Insects

D. suzukii adults were reared in acryl cages (30 cm × 30 cm × 30 cm) with 20% sugar solution in a bottle with cotton wool, and eggs, larvae, and pupae were reared in insect breeding dishes (100 mm i.d. × 40 mm) with artificial food. The artificial food was modified using the Dalton et al. (2011) method. In brief, distilled water (2 L), agar (16 g), cornmeal (168 g), sugar (75.2 g), dry yeast (48 g), methyl paraben (3.2 g, Samchun chemicals, Pyeongtaek, Republic of Korea), green food coloring (2 mL, Saerohands, Namyangju, Republic of Korea), and propionic acid (22.8 mL, Samchun chemicals, Pyeongtaek, Republic of Korea) were mixed together. The mixture was placed in a breeding dish and stored in the refrigerator.
The rearing conditions were 22 ± 1 °C, with 60 ± 10% relative humidity and a 16:8 h light:dark cycle.

2.2. Fumigant and Grapes

Phosphine (2% PH3 + 98% CO2) was purchased from Dongbu Farm Hannong Co. Ltd. (Vivakill®, Daejeon, Republic of Korea).
The grapes used to measure the sorption rate and phytotoxic effects of PH3 were of the ‘Campbell early’ cultivar, purchased from a local farm in Chungbuk Province, Republic of Korea; the grapes were stored at 5 °C.

2.3. Cold-Temperature Treatment in a 12 L Desiccator

All D. suzukii developmental stages were subjected to cold-temperature exposure at 1 °C and 5 °C. The mortality associated with the cold-temperature treatments was investigated after exposure for 1, 2, 3, 4, 5, 6, and 7 d in a cold-temperature chamber. All tested insects were incubated at 20 ± 1 °C after exposure to the cold-temperature treatment, and adults were supplied with 20% sugar solution. The experiment was conducted using eggs within 6 h of being laid, 6- to 7-d old larvae and 11- to 12-d old pupae produced by adult D. suzukii that were placed in a breeding dish (100 mm i.d. × 40 mm). The mortality of eggs and larvae were calculated using the pupation rate 2 and 1 weeks after cold-temperature treatment, respectively. After 1 week of cold-temperature treatment, the mortality of pupae was recorded based on the emergence rate, and non-emerged individuals were considered dead. Mortality in adults was observed after 24 h of cold-temperature treatment. Mortality was corrected by Abbott’s formula [33] and all experiments were performed with at least 3 replicates.

2.4. Fumigation Experiments in a 12 L Desiccator

The fumigation effects of various concentrations of PH3 on all developmental stages of D. suzukii were tested in a 12 L desiccator at 20 ± 1 °C with an exposure of 4 h.
All insect test conditions for all D. suzukii developmental stages in the fumigation experiment were the same as those in the cold-temperature treatment experiment. Eggs and larvae were treated in dishes containing artificial food, and pupae were treated in dishes containing filter paper soaked in water. All experiments were performed with approximately 30 insects in each developmental stage and replicated at least 3 times. Mortality was confirmed in the same time periods and using the same methods as those in the cold-temperature treatment experiment.

2.5. Combined PH3 Fumigation and Cold-Temperature Treatment

Combined treatment was carried out in two ways in a 12 L desiccator: fumigation treatment after cold-temperature treatment, and cold-temperature treatment after fumigation.
The cold-temperature treatments consisted of exposure to 1 °C and 5 °C for 24 h, and fumigation was performed for 4 h considering the LCT50 value of PH3 for D. suzukii. The lowest LCT50 value (0.33 mg/L) was applied for eggs and larvae but not adults, and the highest LCT50 value (4.32 mg/L) was applied for pupae.
Pupae of D. suzukii showed the highest tolerance, and the LCT values of PH3 at various concentrations in the combined treatment were investigated in a 12 L desiccator. The combined treatment involved fumigation for 4 h, followed by exposure to a low temperature for 24 h. The LCT50 value and LCT99 value according to temperature were compared as synergistic ratio (SR) values.
The combined treatment for all D. suzukii developmental stages was fumigation of grapes at a 15% loading ratio (w/v) for 4 h with PH3 (3 g/m3) in a 0.65 m3 fumigation chamber, followed by cold-temperature treatment at 1 °C for 24 h to confirm insecticidal toxicity. The mortality of D. suzukii according to location (top, middle, bottom) was observed in a 0.65 m3 fumigation chamber.
The mortality in all developmental stages exposed to the combined treatment in the 12 L desiccator and 0.65 m3 fumigation chamber was calculated in the same way as those in the cold-treatment experiment.

2.6. Gas Concentration and Sorption Measurement

Concentration and time (CT) values were calculated by measuring the gas concentration at 30 min, 1 h, 2 h, and 4 h after PH3 treatment in a 12 L desiccator and a 0.65 m3 fumigation chamber [34].
Samples for PH3 concentration measurements were collected using a gastight syringe (100 mL, Hamilton, NV, USA). The concentrations were analyzed using gas chromatography (GC, Agilent Technology 6890 N, NPD, Santa Clara, CA, USA) with the following parameters: the injection temperature of the nitrogen phosphorus detector (NPD) was 250 °C, the oven temperature was 240 °C, the detector temperature was 320 °C, and the column was an HP-5 (0.53 mm × 15 m, Agilent Technology, Santa Clara, CA, USA).
The sorption rate of PH3 on grapes was determined at 30 min, 1 h, 1.5 h, 2 h, 3 h, and 4 h after treatment with a dose of 3 mg/L PH3 and 0%, 15%, 20%, and 25% loading ratios (w/v) in a 12 L desiccator.

2.7. Phytotoxicity Evaluation in Grapes

The phytotoxicity associated with cold-temperature treatment after PH3 fumigation of grapes was evaluated in a 0.65 m3 fumigation chamber. Grapes were fumigated with 3 g/m3 PH3 with a 15% loading ratio for 4 h and then cold treated at 1 °C for 24 h. After the combined treatment, the tested grapes were incubated at 5 °C to maintain freshness. Fifteen grape clusters were randomly selected and 5 quality criteria (weight loss, berry abscission, decay rate, sugar content, and surface color) were evaluated after 3, 7, 10, and 14 d. The weight-loss rate (%) was calculated as the weight change in each grape cluster. The berry abscission rate (%) was calculated using the number of abscised berries after shaking in a shaker (N-Biotec Inc., Bucheon, Korea) at 150 rpm for 1 min. The decay rate (%) was calculated as a percentage by dividing the number of decayed berries by the total number of berries. Measurement of sugar content (%, brix) was performed using a refractometer (Atago Co. Ltd., Tokyo, Japan). Surface color (brightness, redness, and yellowness) was measured using a chromameter (CR-400, Minolta Inc., Osaka, Japan). The control group consisted of grape clusters stored at 5 °C without any treatment.

2.8. Statistical Analysis

The t-test was used to compare insect mortality at 1 °C and 5 °C between the groups that used cold-temperature treatment alone, and to compare and analyze the phytotoxicity of the combined treatment on grapes [35]. The LCT values associated with PH3 fumigation only and the combined treatment for D. suzukii pupae were calculated using probit analysis [35]. The tolerance ratio (TR) was calculated by comparing the LCT50 and LCT99 values for each developmental stage of D. suzukii based on the most susceptible developmental stage to PH3 fumigation in the 12 L desiccator. The SR value was compared to the LCT values among the temperature treatments (room temperature, 1 °C, and 5 °C) using pupal D. suzukii. The mortalities of the combined treatment in a 12 L desiccator and a 0.65 m3 fumigation chamber for all D. suzukii developmental stages were analyzed with Tukey’s test [35].

3. Results

3.1. Effects of Cold-Temperature Treatment

The effects of the cold-temperature (1 °C and 5 °C) treatments in each D. suzukii developmental stage were observed (Figure 1). Cold treatment at 1 °C was associated with higher mortality than cold treatment at 5 °C in all developmental stages except the egg stage. The egg stage did not show a significant difference in the mortality between the 1 °C and 5 °C treatments. The larval stage showed 100% mortality when treated at 1 °C for 5 d, but the larvae were not completely controlled when treated at 5 °C for 7 d (p = 0.0072). The pupal stage showed 100% and 88.6% mortality, respectively, when treated at 1 °C and 5 °C for 7 d. In contrast, the adult stage showed very strong tolerance to cold temperatures. In particular, adults showed 23.3% mortality, even after 7 d at 5 °C, but 98.0% mortality at 1 °C (p = 0.0004).

3.2. Fumigation Activity of PH3 in a 12 L Desiccator

Fumigation activity was confirmed by exposing all D. suzukii developmental stages to PH3 for 4 h in a 12 L desiccator (Table 1).
Adults showed the highest susceptibility to PH3, while the pupal stage showed the highest tolerance, with an LCT99 value 604.55 times higher than that for the adult stage. The egg and larval stages were observed to have similar LCT50 values, but there was a small, approximately 1.54-fold difference in the tolerance ratio according to the LCT99 values.

3.3. Effects of the Combined Treatment

In D. suzukii exposed to combined PH3 fumigation and cold-temperature treatment (1 °C and 5 °C), mortality in all developmental stages except the adult stage was observed (Figure 2). Between the two combined treatment methods, fumigation after cold-temperature treatment showed a stronger insecticidal effect on eggs, with a statistically significant difference. However, cold-temperature treatment after fumigation showed similar insecticidal effect, regardless of the temperature. Compared with fumigation alone, the combined treatment showed synergistic effects in the larval and pupal stages, but there was no statistically significant difference between the treatment methods or temperatures.
The fumigation LCT values for the effective control of D. suzukii exposed to the combination treatment were calculated using the pupal stage LCT value because pupae had the highest tolerance to PH3 (Table 2). There was no significant difference in the SR value of PH3 among room temperature (control) and cold temperatures (1 °C and 5 °C) in the combined treatment groups. However, the LCT99 value of PH3 combined with 1 °C treatment was 4.59 times higher than the LCT99 value of PH3 of the control.
A scale-up experiment was performed in a 0.65 m3 fumigation chamber considering the LCT99 value in pupae exposed to the combined treatment at 1 °C because pupae had the highest tolerance in the experiment in the 12 L desiccator (Table 3). A mortality of 100% was observed in all D. suzukii developmental stages, regardless of insect position at the top, middle, or bottom of the fumigation chamber.

3.4. Evaluation of the PH3 Sorption Rate in Grapes

The sorption of PH3 onto grapes was evaluated in a 12 L desiccator for 4 h (Figure 3). The concentration of PH3 did not change significantly in the desiccator without grapes (0% loading ratio), decreasing to 99.04% after 4 h of PH3 exposure. Meanwhile, the PH3 concentration decreased to 93.90% after 30 min and 85.49% after 4 h of fumigation in the desiccator with grapes, with a 15% loading ratio. The concentration decreased to 81.73% and 74.42% with 20% and 25% loading ratios, respectively, after 4 h of PH3 treatment.

3.5. Effects of the Combined Treatment on Grapes

The effect of the combined treatment on grapes was investigated in a 0.65 m3 fumigation chamber (Table 4). There was no significant difference in the condition of the grapes between the treatment groups and the control. The berry abscission rate was lower in the treatment groups than in the control group. However, there was no statistically significant difference. There was also no significant difference in sugar content between the groups, and there was no relation with time until 14 d after treatment.

4. Discussion

Various management methods (physical, biological, chemical, and behavioral) have been used to control D. suzukii [36,37,38]. In this study, the controlling effects of combined low-temperature treatment and PH3 fumigation were investigated. Some physical methods for the control of D. suzukii, a quarantine pest, including the induction of sterilization through irradiation (such as X-ray and gamma irradiation), and the utilization of the low-temperature thermal tolerance of each developmental stage has been studied [39,40,41,42,43,44,45]. In previous studies, D. suzukii adults were observed to have the highest cold tolerance, and 8 d of treatment at 1 °C was required to control eggs, larvae, and pupae [39,41,43,44,45]. In this study, the adult stage was not completely controlled (98.0%), even after 7 d at 1 °C; however, 100% mortality was shown in the other developmental stages (egg, larva, pupa) of D. suzukii when treated at 1 °C for 7 d.
As a chemical control method of pest control, fumigation with MB, ethyl formate (EF), and PH3 is widely used [36]. However, there is a difference in fumigant susceptibility among insect species and developmental stages within the same species [46,47,48]. Previous studies showed that D. suzukii larvae had the highest tolerance to MB, while eggs had the highest tolerance to EF [38,48,49,50]. In the current study using PH3, D. suzukii pupae showed the highest tolerance.
This experiment was conducted to improve D. suzukii control by combining low-temperature treatment and PH3 fumigation to compensate for the disadvantages associated with single control methods. Previously, it has been shown that the combination of 0 °C treatment and MB fumigation has a synergistic effect on eggs, larvae, and pupae of D. suzukii, and the combination of EF fumigation and low-temperature treatment (1 °C and 5 °C) also showed positive control effects on all developmental stages of D. suzukii [38,48,49]. In this study, the combination of low-temperature treatment and PH3 fumigation had a weak synergistic effect compared to the effects of a single treatment. Regarding the combined treatment method, a relatively slightly higher control effect was observed when PH3 was applied after low-temperature treatment than when low-temperature treatment was applied after fumigation. However, the synergistic effect of the combined treatment on the young egg stage was significant. This is possibly because the egg stage of D. suzukii had a higher susceptibility to low temperatures than the other developmental stages, and older eggs (1–2 d old) had a higher cold tolerance than younger eggs (immediately following infestation) [51,52]. Therefore, it seems that in recently laid eggs (less than 6 h), PH3 fumigation after low-temperature treatment has a synergistic effect due to the influence of low temperature. Conversely, in the group exposed to low-temperature treatment after fumigation, eggs over 10 h old were not affected by the low-temperature treatment. Susceptibility to fumigants and temperatures is different among different insect species and developmental stages, so research on these factors should be continued.
The sorption rate of fumigants is related to the product, the loading ratio, and the fumigant exposure time; in particular, the higher the loading ratio, the higher the sorption rate [53,54]. PH3 has shown a relatively low sorption rate: the concentration decreased by 13% compared to the control in an asparagus experiment with a 20% loading ratio (w/v) at 2 °C [55]. Additionally, when various imported foliage nursery plants were exposed to PH3 at a 2% loading ratio (w/v) for 24 h in an experiment, Heteropanax fragrans showed the highest sorption rate, at 41.5%, whereas Schefflera arboricola showed the lowest sorption rate, at 12.2% [56]. When the exposure time was decreased to 4 h, although there was a difference between plant species, the lowest and highest sorption rates were 12.8% and 24.4%, respectively. However, EF was associated with a maximum sorption rate of 70% or higher [46,56]. In the current study, there was a difference depending on the grape loading ratio, with sorption rates of 14.51% at a 15% loading ratio, and 25.58% at a 25% loading ratio after 4 h of exposure to PH3.
There was no statistically significant difference in phytotoxicity between grapes exposed to combined low-temperature treatment and PH3 fumigation and control grapes.
Therefore, these results suggest that the combined low-temperature treatment and PH3 fumigation might be helpful for D. suzukii control.

5. Conclusions

This research evaluated the effects of combined low-temperature treatment (1 °C and 5 °C) and PH3 fumigation. Similar synergistic effects were confirmed in the larval and pupal stages, regardless of the combined treatment order, but there was a very significant difference associated with fumigation after low-temperature treatment in the egg stage. In this study, complete control of all developmental stages of D. suzukii was observed when exposed to 1 °C for 24 h after PH3 fumigation with 3 g/m3 for 4 h in a 0.65 m3 fumigation chamber. Thus, this combination treatment strategy could be useful for the control of all developmental stages of D. suzukii.

Author Contributions

Investigation, S.-J.S.; formal analysis and writing—original draft, S.-J.S. and H.K.K.; validation, H.-N.K.; supervision, G.-H.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Animal and Plant Quarantine Agency, Korea (grant no. Z-1543086-2021-23-05).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Applsci 12 12531 g001 550
Figure 1. Effects of cold temperatures (1 °C and 5 °C) by exposure time on the control of each D. suzukii developmental stage. (A): eggs; (B): larvae; (C): pupae; (D): adults. * p < 0.001; ** p < 0.0001.
Figure 1. Effects of cold temperatures (1 °C and 5 °C) by exposure time on the control of each D. suzukii developmental stage. (A): eggs; (B): larvae; (C): pupae; (D): adults. * p < 0.001; ** p < 0.0001.
Applsci 12 12531 g001
Applsci 12 12531 g002 550
Figure 2. Effects of single treatments and combined treatments on the control of each D. suzukii developmental stage in a 12 L desiccator. (A): eggs; (B): larvae; (C): pupae. Different letter above the bars indicates significant difference.
Figure 2. Effects of single treatments and combined treatments on the control of each D. suzukii developmental stage in a 12 L desiccator. (A): eggs; (B): larvae; (C): pupae. Different letter above the bars indicates significant difference.
Applsci 12 12531 g002
Applsci 12 12531 g003 550
Figure 3. Concentrations of PH3 at different grape loading ratios (0, 15%, 20%, and 25%) during fumigation in a 12 L desiccator with 3 mg/L PH3 for 4 h.
Figure 3. Concentrations of PH3 at different grape loading ratios (0, 15%, 20%, and 25%) during fumigation in a 12 L desiccator with 3 mg/L PH3 for 4 h.
Applsci 12 12531 g003
Table
Table 1. Fumigation effect of PH3 against all D. suzukii developmental stages in a 12 L desiccator after 4 h of exposure at 20 °C.
Table 1. Fumigation effect of PH3 against all D. suzukii developmental stages in a 12 L desiccator after 4 h of exposure at 20 °C.
StagenLCT50 a (mg·h/L)
(95% CL b)		TR cLCT99 (mg·h/L)
(95% CL)		TRSlope ± SEdfⅹ2
Egg3600.41
(0.37–0.44)		8.911.76
(1.39–2.48)		203.64 ± 0.362104.87
Larva4500.33
(0.31–0.35)		7.171.14
(0.97–1.4)		12.954.34 ± 0.323162.88
Pupa7204.32
(3.90–4.77)		93.9153.20
(37.11–87.48)		604.552.13± 0.186142.16
Adult3780.046
(0.044–0.048)		10.088
(0.081–0.100)		18.22 ± 0.683145.08
a LCT50 and 99; 50% and 99% lethal concentration time. b Confidence limit. c TR (Tolerance ratio) = LCT value of each developmental stages/LCT value of Drosophila suzukii adult.
Table
Table 2. Toxicity of the combined treatment in the D. suzukii pupal stage exposed to the two cold-temperature treatments after PH3 fumigation for 4 h in 12 L desiccator.
Table 2. Toxicity of the combined treatment in the D. suzukii pupal stage exposed to the two cold-temperature treatments after PH3 fumigation for 4 h in 12 L desiccator.
Temp.
(°C)		nLCT50 (mg·h/L)
(95% CL a)		SR bLCT99 (mg·h/L)
(95% CL)		SRSlope ± SEdfⅹ2
RT c5404.80
(4.29–5.40)		148.17
(33.52–79.95)		12.32 ± 0.204130.05
14503.32
(3.06–3.57)		1.4510.49
(8.98–12.99)		4.594.66 ± 0.413128.33
54504.54
(4.20–4.90)		1.0618.02
(14.94–23.16)		2.673.89 ± 0.313161.69
a Confidence limit. b SR (Synergistic ratio) = LCT value of each developmental stages/LCT value of D. suzukii adult. c Room temperature.
Table
Table 3. Mortality of D. suzukii at each location exposed to cold treatment (1 °C, 24 h) after PH3 fumigation (3 g/m3, 4 h) in a 0.65 m3 fumigation chamber containing grape with a 15% loading ratio.
Table 3. Mortality of D. suzukii at each location exposed to cold treatment (1 °C, 24 h) after PH3 fumigation (3 g/m3, 4 h) in a 0.65 m3 fumigation chamber containing grape with a 15% loading ratio.
StageLocationnMortalityCT
(mg·h/L)
(Mean ± SE)
EggTop270   100.0 ± 0.0a a10.58
Middle270100.0 ± 0.0a
Bottom270100.0 ± 0.0a
Control270    8.5 ± 1.0b
LarvaTop369100.0 ± 0.0a
Middle384100.0 ± 0.0a
Bottom393100.0 ± 0.0a
Control394    3.6 ± 0.7b
PupaTop450100.0 ± 0.0a
Middle450100.0 ± 0.0a
Bottom450100.0 ± 0.0a
Control450    4.2 ± 0.8b
AdultTop177100.0 ± 0.0a
Middle195100.0 ± 0.0a
Bottom181100.0 ± 0.0a
Control285    1.8 ± 0.8a
a Means with different letter indicates significant difference.
Table
Table 4. Phytotoxicity of the combined treatment to grapes at a 15% loading ratio in a 0.65 m3 fumigation chamber.
Table 4. Phytotoxicity of the combined treatment to grapes at a 15% loading ratio in a 0.65 m3 fumigation chamber.
DAT aTreatmentWeight Loss (%)Berry Abscission (%)Decay Rate (%)Sugar Content (%, brix)Mean Surface Color b
Lab
3Control1.5 ± 0.1 c0.5 ± 0.30.0 ± 0.015.9 ± 0.121.5 ± 0.6−0.4 ± 0.14.9 ± 0.2
Combination treatment1.8 ± 0.20.0 ± 0.00.0 ± 0.016.0 ± 0.221.7 ± 0.6−0.4 ± 0.14.8 ± 0.1
p  c0.1560.172-0.6620.8040.8250.534
7Control2.4 ± 0.21.4 ± 0.70.3 ± 0.215.5 ± 0.320.9 ± 0.6−0.3 ± 0.24.8 ± 0.3
Combination treatment2.5 ± 0.20.5 ± 0.30.3 ± 0.315.9 ± 0.321.1 ± 0.6−0.5 ± 0.24.7 ± 0.2
p0.4800.3380.8500.3750.7790.4990.813
10Control3.1 ± 0.32.3 ± 0.80.6 ± 0.315.9 ± 0.320.9 ± 0.4−0.6 ± 0.14.9 ± 0.1
Combination treatment3.3 ± 0.21.1 ± 0.60.5 ± 0.316.2 ± 0.221.1 ± 0.3−0.6 ± 0.15.0 ± 0.2
p0.7000.3120.8010.4540.7020.7430.408
14Control3.9 ± 0.32.5 ± 0.80.7 ± 0.315.9 ± 0.222.2 ± 0.4−0.6 ± 0.14.7 ± 0.2
Combination treatment4.0 ± 0.21.1 ± 0.61.0 ± 0.516.0 ± 0.222.1 ± 0.2−0.4 ± 0.14.7 ± 0.1
p0.7150.2740.5340.6200.8240.2550.761
a Day after treatment. b L is lightness; a represents the green-red color opponents; and b represents blue-yellow color opponents (CIELAB color space). c A t-test was used to compare the values (%, mean ± SE) of each quality criterion between the control and combination treatment.
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Seok, S.-J.; Kim, H.K.; Koo, H.-N.; Kim, G.-H. Combined Effects of Cold Treatment and Phosphine in Drosophila suzukii (Diptera: Drosophilidae). Appl. Sci. 2022, 12, 12531. https://doi.org/10.3390/app122412531

AMA Style

Seok S-J, Kim HK, Koo H-N, Kim G-H. Combined Effects of Cold Treatment and Phosphine in Drosophila suzukii (Diptera: Drosophilidae). Applied Sciences. 2022; 12(24):12531. https://doi.org/10.3390/app122412531

Chicago/Turabian Style

Seok, Seung-Ju, Hyun Kyung Kim, Hyun-Na Koo, and Gil-Hah Kim. 2022. "Combined Effects of Cold Treatment and Phosphine in Drosophila suzukii (Diptera: Drosophilidae)" Applied Sciences 12, no. 24: 12531. https://doi.org/10.3390/app122412531

APA Style

Seok, S.-J., Kim, H. K., Koo, H.-N., & Kim, G.-H. (2022). Combined Effects of Cold Treatment and Phosphine in Drosophila suzukii (Diptera: Drosophilidae). Applied Sciences, 12(24), 12531. https://doi.org/10.3390/app122412531

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