Impact of Short-Term Atmospheric Heat Transfer on the Survival of Granary Weevil in Stored Winter Wheat

Abstract

The granary weevil Sitophilus granarius L. is a pest causing substantial damage to stored wheat worldwide, against which the elaboration of sustainable control methods has recently been gaining importance. Our objective was to assess the efficacy of a rapid atmospheric convection heat transfer method against S. granarius under laboratory conditions. We examined the changes in adult mortality and progeny survival triggered by heat and the effect of this on the quality parameters of treated wheat items. The insecticidal efficacy, achieved by the treatment of infested grains, was also analyzed at 37, 47, 67, 87, and 107 °C for 5, 6, and 7 min under 40% and 60% rh exposure to atmospheric heating with the progeny production assessed 45 days after the treatment. The quality parameters of the treated wheat were analyzed by a germination test and NIR grain analysis. Our findings showed that adequate eradication of S. granarius was obtained at 107 °C for 5 min of exposure under suboptimal (40% rh) relative humidity values. At 60% relative humidity, mortality averages were more dispersed, and efficacies above the expected 95% occurred over longer exposures. The progeny-suppression effect from short-term heating was affirmed. The atmospheric convection heat transfer method, under the applied temperature and exposure time combinations, did not induce detectable changes in the quality parameters or the germination ability of the treated wheat. Overall, our findings indicated that the use of short-term heating for the post-harvest protection of cereals is feasible, which may contribute to the realization of residuum-free pest management and provide an effective and sustainable technique in integrated pest management.

1. Introduction

The granary weevil Sitophilus granarius L. 1758 (Coleoptera: Curculionidae) is a serious pest of stored products, which can trigger significant damage to stored grains and alter the qualitative and quantitative parameters of a yield. The species is a typical primary stored product pest; its activity in the attacked grains leads to the deterioration of nutrients, a lower percentage germination, reduced weight, and a lowered market value [1].

Residual insecticides are used worldwide as a protectant of stored grain against stored product pests. Regrettably, these pesticides have several negative effects, such as being toxic to vertebrates and having residues that accumulate in treated products. Furthermore, many pest species can develop a special insecticide resistance [2]. Therefore, economical and effective methods that use natural products are increasingly required for the diminution of the damage caused by S. granarius in order to protect stored grain.

One possible method of sustainable control is the heat transmission of stored products [3]. During this treatment, the temperature of a yield is artificially increased by a heat generator until the abiotic parameter reaches the ecological pessimum range of arthropods, causing their mortality. In parallel, and as an accompanying side effect, the quality parameters of the treated yield may decrease [3,4,5]. In the case of chemical combination, further difficulties in using the method arise from finding a range of the applied insecticide that does not damage the qualitative parameters of a crop [4,6]. Several lines of research deal with the heat-transmission possibilities for the protection of stored products, addressing the use of heat stress to exclusively combat arthropods that damage stored products [7,8,9] or in combination with insecticides [10,11] or other potentially viable methods [12,13]. According to previous studies by Pradzynska [14], temperatures between 45 and 60 °C that are applied over proper thermal exposure periods can sterilize or destroy each development stage of S. granarius without having negative side effects on the qualitative and seedling parameters of the treated grains. The mortality effect of some insecticides can be increased via heating regarding S. granarius populations, as pointed out by Kljajić et al. [10]. Deltamethrin and dichlorvos toxicities were higher in the heat-treated group after a 72 h recovery period than in the control population.

The side effects from the application of heat-treatment-based eradication methods against pests can cause changes in the quality of a treated yield. Thermal degradation of raw materials such as grain can impair the quality of the final food product. Grain drying using excessive heat can decrease the grain’s eventual baking quality, resulting in a lower volume of bread produced; therefore, the application of dry heating at high temperatures for longer periods should be avoided [15,16]. Dry heat treatment (DHT) of wheat flour can be used to modify the hydrolysis, and therefore the digestibility, of starch in low-digestible energy products. DHT causes significant changes in the characteristics of flour and bread when the temperature exceeds 100 °C [17]. Vital wheat gluten (WG) can be processed from wheat flour; during this process, wet gluten dries at approximately 100 °C, which can impair gluten functionality [18]. Heat can cause wheat protein denaturation, which leads to changes in the solubility of proteins and the viscoelastic properties of dough [18]. The viscosity (extensibility) and elasticity (strength) of dough are determined by gliadins and glutenins, respectively. These two groups of proteins constitute gluten when dough is developed. The gluten proteins make up approximately 80% of the total proteins of wheat flour [15]. Because the excessive thermal exposure of wheat can impair the final quality of boiled and baked cereal products, an investigation of grain quality is essential when adding heat treatment for the eradication of S. granarius.

Although some results have been obtained in connection with the effects of heating on S. granarius [10,14], the relevant information about mortality and seed viability efficacy in relation to different heating and relative humidity settings is rather scarce. Therefore, the objective of this research was to obtain information about the efficacy of different heat and relative humidity treatments against S. granarius concerning winter wheat, and to evaluate the influence of the different exposure times of applied doses on weevil mortality and progeny production. Moreover, our aim was to study the impairment effect of these treatments on seedling ability and some of the quality parameters in treated grain.

2. Materials and Methods

2.1. Insect Eradication Test

Healthy, one-year-old, infestation-free wheat kernels (cultivar: Genius^®, which originate from the store house of Kaposmérő, GPS: latitude: 46°21′42.01″ N, longitude: 17°42′14.40″ E) were used for the experiment. The moisture content of the grain was 13.5%. As a first step, 100 g of a sample was measured and placed in a glass jar. Simultaneously, 20 healthy S. granarius adults of mixed sexes and ages were added to each sample in the glass jar. The jars were covered with textiles and placed in a climate chamber (Pol-Eco Apartura KK 1450, Wodzislav-Slenski, Poland) at 26 ± 3 °C, 60% ± 5% relative humidity (rh), and a 16/8 h photoperiod, which are the most favorable developmental conditions for S. granarius [19]. Two days elapsed between sample preparation and the experimental treatments in order to allow egg laying to occur.

To assess the effect of high-temperature degrees combined with different rh on insect mortality, a total of five temperature maximums were set up in addition to the untreated samples. The applied temperature values were 37, 47, 67, 87, and 107 °C, starting from the upper tolerance border (37 °C) of the species in 10 °C steps. Moreover, two different relative humidity values of 40 ± 5 and 60 ± 5% rh were applied in combination with the different temperature levels. The exposure time (exposure to heat) was uniformly 5 min for each heat treatment. Then, the experiment was repeated with the application of 6 and 7 min exposure times at 40% rh in order to determine the optimal insect mortality intervals with data extrapolation. A Memmert UN30 Universal Oven (Memmert GmbH & Co. KG, Büchwenbach, Germany) was used for the heat treatments. Each treatment included 4 repetitions. After the heat treatments, the samples were immediately placed into the climate chamber (at 26 ± 3 °C and 40 ± 5% rh, or at 26 ± 3 °C 60 ± 5% rh, see Figure 1). After a period of 48 h, the emerged S. granarius adults were counted, and classified as dead or alive. These adults were observed for survival and progeny as an indication of their reproductive ability. All adults were removed (dead and alive) from the wheat, and experimental jars were placed into the climate chamber at 26 ± 3 °C, 60% ± 5% rh and a 14/8 h photoperiod. For samples originally containing eggs, larvae, and pupae, adult emergence was observed on the 45th day of treatment to assess the effect of heating on progeny survival compared with the same results originating from the control samples.

2.2. Germination Test

As a first step, seed moisture content was determined using a Kramp MM4510 moisture meter (Kramp UK Ltd., Bedfordshire, UK). For the germination testing, four replicates per treatment, containing 20 seeds, were placed in Petri dishes on two germination papers (Herlitz A4/10, 8gM2) and moistened with 4 mL of distilled water. The Petri dishes were covered to prevent water loss during the test and placed in a climate chamber programmed with the following abiotic settings: 25 ± 5 °C, 40 ± 5% rh, and a 16/8 h photoperiod. The germination rate was determined based on radicle emergence (2 mm) on the 7th day after setting.

2.3. Determination of Compositional and Quality Parameters of Wheat

The intact and treated winter wheat samples were analyzed from each treatment in the four replicates in order to determine seed quality by means of an Xgrain near-infrared grain analyzer (Infracont Xgrain™ Grain Analyzer, Pomáz, Hungary). The measured parameters included the total protein content (P), water-insoluble protein content (glutenins and gliadins), Zeleny index (ZI), and the alveograph deformation energy (W). The potential plant tissue destructive effect of different heating degrees was inferred from the potential change in the examined quality parameters.

2.4. Statistical Analysis

To determine mortality values, Abbott’s [20] formula was applied. In order to test the mortality data of granary weevil (n > 50), the Shapiro–Wilk test was employed. The evaluation of the normal distribution of data was effectuated by Ghasemi- and Zahediasl-type methods (p < 0.05). The data were assayed by means of a two-way ANOVA in SPSS 11.5 software(IBM statistics, Chicago, IL, USA) (response variable: adult mortality, main effects: different temperature and relative humidity parameters). The mortality values of different weight samples and progeny numbers were also analyzed statistically by a Student-type T-probe and one-way ANOVA. To determine the optimal mortality efficacy intervals depending on the relative humidity and maximum temperature value settings, a statistical extrapolation was carried out using the data originating from 5, 6, and 7 min exposures.

Moreover, the effects of different levels of heating on the germination rate and quality values were statistically analyzed by one-way ANOVA using SPSS 11.5. Means were uniformly separated by using the Tukey HSD test, at p ≤ 0.05.

3. Results

3.1. Insect Mortalities Triggered by 5 Minutes Heating

Abbot-corrected mortalities for different temperature and relative humidity values can be seen in Figure 2. The mortality values unequivocally increased as a result of applying maximum temperature regimes at 5 min exposure times coupled to both relative humidity values. The effect of temperature increases on the registered mortality change was statistically confirmed in relation to both relative humidity values (p < 0.001). The data registered by different relative humidity settings did not statistically differ (Student t-value: 0.235). Based on the results of the two-way ANOVA, neither the effect of different rh values nor the interaction between temperature and rh on mortality was significant.

The tendencies of the triggered mortalities were linear types in the cases of both relative humidity values. The relationship was especially strong at 40% rh (y = 0.681x + 19.282; R² = 0.9454), but the linearity could also be justified at 60% rh (y = 0.446x + 32.883; R² = 0.6816). Other than the 40% humidity condition, the total mortality of the experimental population was triggered by applying 107 °C over 5 min of exposure (mortality: 96.66%). At 60% relative humidity, mortality averages were more dispersed, and efficacies above the expected 95% occurred at longer exposures.

The mortality percentages achieved by data extrapolation as a function of the interaction of exposures and maximum temperatures can be seen in Figure 3. The mortality rate increased with the exposure time and at the higher pessimum temperatures. Lower temperatures (until 80 °C) did not result in an acceptable efficacy in the case of 7 min of exposure. The mortality value was only 60–70% under the conditions of 9 min exposure time to 60 °C of heating. Mortality above 90% was only expected when heating the samples to 100 °C for 5–6 min. Heating the samples above 100 °C or for longer than 7 min triggered the complete eradication of the pest population.

With an increase in heating temperature, the adult progeny decreased at each exposure time (5, 6 and 7 min) (

Table 1. Progeny production of S. granarius (mean number of dead adults ± SE) in heated wheat 45 days after the removal of exposed S. granarius adults, and the statistical relationships (p ≤ 0.05).

Treatments		No. Progeny
control		7.25 ± 0.75
applied maximum temperatures		37 °C	47 °C	67 °C	87 °C	107 °C	p
exposure times	5 min	4.25 ± 0.47	4.00 ± 1.08	4.00 ± 0.49	2.50 ± 0.50	2.50 ± 0.28	0.317
	6 min	4.00 ± 1.35	2.00 ± 0.71	2.50 ± 0.50	0.50 ± 0.50	0.50 ± 0.28	0.047
	7 min	2.50 ± 0.50	1.50 ± 0.86	2.25 ± 0.69	1.50 ± 0.64	0.75 ± 0.25	0.004
p		0.075	0.429	0.056	0.280	0.068

(Italic characters show the statistically significant correlations).

). This observation was statistically proven for longer exposure times (6 and 7 min). After forty-five days, the adult progeny numbers, in the case of different exposures of the applied maximum temperature, decreased in the majority of cases; yet, this change was not observed in relation to any of the heat treatments. The progeny production of the sample populations dropped to about 30%, lasting for 6 min at 67 °C heating and 5 min at 87 °C heating, compared with the intact weevil populations. A significant progeny decrease was triggered by the longer heating periods at higher temperatures (other than the lasting 6 and 7 min exposures to 107 °C heating). However, a complete suppression of progeny production was not observed in any of the treatments.

3.2. Germination, Compositional, and Quality Parameters of the Treated Wheat

The germination rates were uniformly between 80% and 95% in each case when examined in relation to exposure and the applied maximum temperatures. The obtained values did not reflect statistically significant differences (p > 0.05). Homogenous germination (90 ± 2.5) was observed even after being subjected to the longest exposure and the highest temperature.

The heat treatments, which were applied at different maximum temperatures from 37 to 107 °C for 5 min, did not produce a significant change in the examined quality parameters (p > 0.05) (Figure 4). Moreover, no effects of either the two examined relative humidity degrees or the interaction of the main influencing factors (different temperature and relative humidity parameters) on the quality parameters were observed under two-way ANOVA (p > 0.05).

4. Discussion

Placing organisms under conditions other than their abiotic preference range leads to disturbing their homeostasis [21]. In the case of insects during their commencement, a shift or delay in ontogenetic processes or a slowdown and cessation in life activities (feeding, reproduction, etc.) will also ensue. Eventually, after exceeding a threshold beyond a certain value or exposure, the affected organisms will have already perished due to irreversible physiological processes [21,22].

In stored product research, different methods of environmental heating have been applied as a method of controlling the Sitophilus genus. There are several types of experimental settings that differ from each other regarding the frequency of the waves that a generating source produces, such as radio frequency [23,24], infrared [25,26], and microwave irradiation [27,28]. This approach can be combined with atmospheric CO₂ saturation [29]. These methods mainly differ with regard to the heated target medium because the infrared and microwave irradiation first heat the objects of the affected environment, with the increased temperature transmitted to the living organisms placed in that environment.

Our data confirmed that the short-term temperature increase of a stored product by atmospheric convection heat transfer may provide environmentally friendly protection against S. granarius. The highest efficacy was detected at 107 °C with 5 min exposure at suboptimal relative humidity values (40% rh). Naturally, the short-term efficacy can be enhanced by an increase in the maximum temperature and exposure time, but these conditions are questionable because of the extra effort required over 100% efficiency.

The aim of our investigation was similar to that of Pradzynska [14], in which lower applied temperatures (45–60 °C) were combined with long exposure times (60–810 min) involving the same target organism. In that experiment, the trends in mortality were similar to the ones observed in our experiment, which were generated by exposure to a maximum temperature. In that work, the most effective condition combinations against the adults were 50 °C for 120 min and 60 °C for 90 min. The results of our work supplement these observations and provide important additions, demonstrating the devastating effects of short-term higher heat transfer on S. granarius. The benefits of this combination were highlighted by Tang et al. [30], who reported the possible applications of this method against codling moth (Cydia pomonella). Overall, the importance of our laboratory experiment lies in its potential applicability in plant protection; insect mortality triggered by short-term exposure to a higher maximum temperature appears achievable without compromising the treated wheat’s germination vigor and baking quality.

According to Eastham and McCully [31], the maximum oviposition rate of S. granarius was observed under 25 °C and at 70% rh (1.1–1.2 eggs/female/day). The same experiment showed that egg laying was 0.8 eggs/female/day at 26 °C and 60% rh, which was represented by the progeny number of the control sample (sex ratio 1:1). The suppressive consequence of the treatment on the progeny was confirmed by our experimental observations. Triggered heating has deleterious effects on insects, such as the reduction of reproductive rate, lost bodyweight, and malformation [32].

According to our observations, the total mortality of the S. granarius population was achieved at temperatures around 100 °C. This temperature has been reported to be critical regarding flour and bread characteristics under dry heat treatment (DHT), or when grain is dried after harvesting [15,16,17]. Moreover, the quality of proteins can also be impaired when vital wheat gluten (WG) is produced at this temperature. In our work, we did not observe changes in either the Zeleny index or in the deformation energy of dough. The deformation energy measured by the alveograph strongly correlates with the amount of gluten that can be extracted with salt solution [15]. Based on the measured values, almost all of the samples could be classified within the intermediate wheat flour category. The Zeleny index depends on both gluten quantity and quality; consequently, it has a strong correlation with baking quality [33]. All of the sedimentation values were more than 30 mL, which is a transition value between a medium-s and high-quality final product.

The absence of a detrimental effect on wheat quality, even at elevated temperatures, may be partially explained by the differences in the applied time intervals. The period of heat shock at 107 °C was very short, lasting only five minutes in this experiment, which provided an adequate effect as the pests were mainly on the surface of the grains. Dry heat treatments (DHTs) exerted a negative effect on the flour and bread properties of the wheat if 100 °C heating was applied for 60 min [17]. Irreversible heat-denatured (nonvital) wheat gluten can be obtained by heating wet gluten at 98 °C for 30 min [18]. A much longer exposure time was applied in the cited studies than in our presented work.

The fundamental expectation concerning a control method or agent is that it must be able to eradicate the target insect at an acceptable level during a short period of time. Our study showed that short-term heating exacts insecticidal activity on S. granarius adults and has a suppressive effect on the species’ progeny. Therefore, rapid atmospheric convection heat transfer of a stored product may provide a promising nonchemical and sustainable pest control method. Our results contribute toward the realization of a reliable and practicable method for stored product pest control. In general, short-term atmospheric heating with properly applied settings can be effectively used for S. granarius larvae and adult control. Moreover, the baking quality of the treated wheat items was not impaired under the examined setting parameters. The benefit of this treatment is its combinability with other protection methods which, ultimately could lead to a more effective and sustainable solution in integrated pest management (IPM).