Assessment of Rhyzopertha Dominica (F.) Progeny and Feeding Damage on Rice Dried with Infrared Radiation

Journal of Stored Products Research 81 (2019) 69e75

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Journal of Stored Products Research

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Assessment of Rhyzopertha dominica (F.) progeny and feeding damage on rice dried with infrared radiation

Rachel M. Hampton a, b, Grifﬁths G. Atungulu c, Zephania Odek c, Virginie Rolland a, * Terry J. Siebenmorgen c, Shantae A. Wilson c, Tanja McKay a, b, a Department of Biological Sciences, Arkansas State University, Jonesboro, AR, 72467, United States b Arkansas Agricultural Experiment Station, Arkansas State University Research Unit, Jonesboro, AR, 72467, United States c Department of Food Science, University of Arkansas & Division of Agriculture, Fayetteville, AR, 72704, United States article info abstract

Article history: Infrared radiation (IR) is a method of drying grains that eliminates insect and microbial pests. It is un- Received 21 September 2018 known if IR could cause grains to be more susceptible to insects. Thus, the effects of IR on Rhyzopertha Received in revised form dominica development and feeding damage using long-grain rice varieties, Clearﬁeld XL745 (hybrid) and 4 January 2019 CL152 (pureline), were examined. Rough rice was dried with three IR intensities: 2.15, 2.83, and Accepted 23 January 2019 10.84 kW/m2. The number of progeny developed, feeding damage, and frass weight after IR-drying were compared with air-drying methods for rough rice and rice milled to brown rice after drying. Since R. dominica develop internally, X-ray technology was used to examine internal progeny and feeding Keywords: X-ray damage. Progeny development and kernel damage appeared to be more affected by fraction (brown rice) Rough rice than the cultivar of rice or intensity of IR used, with more progeny produced on brown rice than rough 2 Brown rice rice. An IR intensity of 10.84 kW/m increased the number of overall progeny, the amount of adults, and 2 Lesser grain borer progeny frass produced on CL152 brown rice. An intensity of 10.84 kW/m also increased the amount of larvae Kernel damage observed for both varieties and fractions. The intensity of 10.84 kW/m2, under the conditions of this study, is not recommended for drying rice. © 2019 Elsevier Ltd. All rights reserved.

1. Introduction insects, pesticides, such as phosphine, are generally used. Phos- phine is easy to apply, inexpensive, and easily dissipates leaving no The lesser grain borer, Rhyzopertha dominica (F.) (Coleoptera: residual chemicals on treated grains (Chaudhry, 2000; Benhalima Bostrichidae) is a commonly found stored-product insect that feeds et al., 2004; Pimentel et al., 2009). However, due to its long-term and develops on many different types of grain including rice use (about 50 years) and misuse (i.e., improper application where (Hagstrum and Subramanyam, 2006). Both the adults and imma- a non-lethal dose is applied to grains), many stored-product insect ture stages of R. dominica feed on grain, causing damage. Adult pests are showing resistance to phosphine throughout the world, females lay eggs in clusters (up to 500 eggs in a lifetime) on the including the U.S., China, Asia, Australia, and Central and South exterior of the grain; however, single eggs can also be laid (USDA, America (Zettler and Cuperus, 1990; Rajendran and Narasimhan, 1979). Once the larva emerges, it chews its way into the rough 1994; Chaudhry, 2000; Benhalima et al., 2004; Pimentel et al., rice kernel by eating through the outer hull, where it feeds and 2009; Opit et al., 2012; Afful et al., 2017). Afful et al. (2017) exam- develops internally. After pupation is completed, adults emerge. ined different samples of R. dominica collected from populations The development from egg to adult can be completed in about 30 across the U.S. as well as Canada, and 32 out of 34 populations days (USDA, 1979). To control for the damage caused by these showed some level of phosphine resistance. Rhyzopertha dominica is also showing resistance to many other pesticides, including organophosphorus compounds (Lorini et al., 2007; Edde, 2012; Chen et al., 2015; Nayak et al., 2015). Therefore, alternative treat- Abbreviations: Infrared radiation, IR; Arkansas, AR; Moisture Content, m.c.; Relative humidity, r.h. ments to pesticides are needed. * Corresponding author. Department of Biological Sciences, Arkansas State Uni- One grain-drying technique that eliminates mycotoxin produc- versity, P.O. Box 599, State University, AR, 72467, United States., ing and decomposing fungi often encountered in grain storage (e.g. E-mail address: [email protected] (T. McKay). https://doi.org/10.1016/j.jspr.2019.01.002 0022-474X/© 2019 Elsevier Ltd. All rights reserved. 70 R.M. Hampton et al. / Journal of Stored Products Research 81 (2019) 69e75

Aspergillus flavus (Link)) (Wang et al., 2014) is infrared radiation (IR) content chamber (EMCC) (ESL 4CA Platinous temperature and hu- on grain stored on farms or at mills. In the past this technique was midity chamber, Espec, Hudson, MI, U.S.) with air conditions of not a safe alternative due to open flames (Cogburn, 1967; Faulkner 26 C and 65% relative humidity (r.h.). Control samples were dried and Wratten, 1969; Kirkpatrick, 1974; Kirkpatrick and Cagle, 1978). completely (no IR treatment) in the EMCC with air conditions of However, new flameless infrared emitters have been developed. 26 C and 65% r.h. to a final m.c. of 13% wet basis. For brown rice Current research shows promise in IR also eliminating internal and treatments, hulls were removed from a portion of IR-treated and external stored-product insect pests at various life stages (Pan et al., control rice samples of each cultivar using a laboratory dehuller 2006, 2008; Khamis et al., 2010, 2011a, 2011b). Although these (Satake Rice Machine, Satake Engineering Co., Ltd., Tokyo, Japan). studies looked at the IR treatment's effect on milling quality, po- After drying, the rice samples were placed in zip top plastic bags tential post-IR treatment effects on the grains, and resulting sus- and kept in a cooler with ice packs. The samples were then trans- ceptibility of kernels to insect infestations are unknown. Cracks in ported from Fayetteville to Jonesboro, AR where they were stored in the rice hulls or fissures in the kernel endosperm make the kernel a refrigerator at 5 C for about ten months before being exposed to more easily accessed by R. dominica, which will lay eggs in cracks R. dominica. found in rough rice (Phillips and Throne, 2010; Kavallieratos et al., 2012); therefore, changes in the grain's structure that could 2.2. Rhyzopertha dominica infestation potentially occur when kernels are heated and dried with IR could result in an increase in R. dominica infestation post-drying. For both varieties, treated and control rough and brown rice X-ray imaging is a tool that can be used to detect insects within were placed into 5 dram vials with approx. 4.5 g of rice in each vial. rough rice and brown rice kernels. Brabec et al. (2010) used X-rays Volumetrically, these amounts were equal in the vials for both to detect R. dominica larvae in wheat and examined the accuracy of rough and brown rice; however, rough rice kernels are larger than milling equipment designed to detect grain damage and insect brown rice kernels, so it took fewer rough rice kernels to fill a vial to parts in milled wheat. Also, Neethirajan et al. (2007) determined the desired level than brown rice. Also, the CL152 kernels tended to that X-ray would be an excellent detection method because it can be smaller than the XL745 kernels; therefore, it took more CL152 detect living and dead insects internally and externally of the grain rough rice kernels (251.0 ± 2.00) than XL745 kernels (189.5 ± 2.50) in various life stages, excluding the eggs, without damaging ker- to fill the vials to the desired level. For brown rice, XL745 and CL152 nels. Karunakaran et al. (2004) used X-ray imaging to detect the averaged 275.0 ± 1.00 and 333.5 ± 7.50 kernels per vial, respec- larvae, pupae, and adults of the rice weevil, Sitophilus oryzae (L.), on tively. There were ten replicates per treatment, totaling 160 vials. wheat with nearly 100% accuracy. X-ray is also effective at detecting Once vials were filled with rice kernels, ten unsexed adult fissuring in rough rice that has occurred due to drying (Odek et al., R. dominica were placed in each vial (assuming a 1:1 sex ratio). Each 2017). In this study X-ray images were used to assess feeding vial was covered with a fine mesh lid to allow the beetles air while damage and delineate the number of R. dominica progeny pro- preventing escape. The vials were stored in an incubator at 27 C duced. These variables were then compared among three IR in- and 60% r.h. Beetles were placed in vials on 10 May 2017 and were tensities (2.15, 2.83, and 10.84 kW/m2) and a control (traditional air checked biweekly until the 28th day when daily checks were done drying) using two long grain rice varieties to determine if drying to look for adult emergence (more adults present than the original using IR has the potential to make rice more susceptible to ten). The development period for R. dominica varies depending on R. dominica infestation. temperature and humidity; however, under preferred conditions the expected development time is about 30 d (Rees, 2007). There- 2. Materials and methods fore, after 50 d, when no further signs of adult emergence were seen, vials were placed in a freezer to stop further development and 2.1. Rice varieties and infrared treatment progeny feeding.

Long-grain rice varieties Clearfield XL745 (hybrid) and CL152 2.3. Progeny assessment (pureline) were harvested in northeast Arkansas during fall of 2015 and sent to the University of Arkansas’ Grain Processing and En- The number of additional adults from the ten adults originally gineering Laboratory (Food Science Department, Fayetteville, AR). placed in each vial was counted. Unexpectedly, larval R. dominica The samples were cleaned to remove any material other than grain (N ¼ 65) as well as pupae (N ¼ 8) were found outside of the kernels and stored in sealed tubs at 4 C to maintain a high moisture con- in some of the vials (Tables 1 and 2). This was an unusual finding as tent (m.c.), approx. 20% wet basis, before drying with infrared R. dominica are primary insect pests that should develop internally energy. of the kernel. Since R. dominica normally develop on the inside of Infrared treatments were applied to rough rice at the University the kernel, to accurately identify if there were progeny that had not of Arkansas’ Grain Processing and Engineering Laboratory (Food emerged from the kernels, a subsample of approx. 40 kernels (no Science Department, Fayetteville, AR) using an IR-heating system visible damage from the outside of the kernel) from each vial was with a catalytic IR emitter (Catalytic Infrared Drying Technologies sent to University of Arkansas Department of Food Science (Fayet- LLC, Independence, KS). For each treatment, rice samples were teville, AR) for X-ray analysis. The subsamples were obtained by placed on a conveyor belt which allowed passage of a single layer of pouring the contents of the vial onto a piece of paper from which rice under the IR emitter. The IR-heating system is designed for the the kernels were randomly selected and placed in a different vial conveyer belt shelving to be placed at three specific distances from for shipment. X-ray imaging was completed using a Faxitron the IR emitter. These three distances (43, 24, and 11 cm) dictated UltraFocus 60 (Faxitron Bioptics LLC., Tucson, AZ) at 4X magnifi- the IR intensities (2.15, 2.83, and 10.84 kW/m2) used in this study. cation. For rough rice, 36 kernels were imaged for each treatment The IR intensity at the product-to-emitter-gap was determined sample. For brown rice, the number of kernels imaged for each using a radiometer (Ophir Laser Measurement Group, North Logan, treatment sample ranged from 39 to 41 kernels although most UT). All treated rice was heated to 60 C, a temperature that would samples contained 40 kernels. Since rough rice kernels are larger effectively kill insects without breaking or popping the kernels than brown rice kernels, only 36 kernels could be imaged at a time (2.15: 22 s, 2.83: 13 s, and 10.84 kW/m2: 7 s). The IR-treated rice was for the same magnification to be used for both rough and brown dried to a final m.c. of 13% wet basis in an equilibrium moisture rice samples. From the X-ray images, the number of larvae, pupae, R.M. Hampton et al. / Journal of Stored Products Research 81 (2019) 69e75 71

Table 1 The total number of larval, pupal and adult R. dominica observed through sieving and X-ray imaging for rough rice samples.

Infrared Intensity kW/m2 Rice Cultivar Larvae Pupae Adult Total Progeny Total Means ± SE

0 CL152 23 (2) 5 (1) 3 (2) 36 12.0 ± 6.5 XL745 13 (0) 7 (0) 6 (1) 27 9.0 ± 2.0 2.15 CL152 11 (1) 1 (0) 7 (1) 21 7.0 ± 3.2 XL745 12 (0) 3 (0) 2 (3) 20 6.7 ± 2.8 2.83 CL152 5 (1) 2 (0) 7 (1) 16 5.3 ± 1.8 XL745 17 (0) 6 (0) 2 (1) 26 8.7 ± 4.3 10.84 CL152 6 (0) 0 (0) 8 (0) 14 4.7 ± 2.4 XL745 10 (2) 3 (0) 3 (3) 21 7.0 ± 2.6 Mean ± SE 12.9 ± 2.2 3.5 ± 0.9 6.3 ± 0.7 22.6 ± 2.5

Note: Number in parentheses represents the additional larvae and pupae observed when the frass was sieved. Adult totals are with ten subtracted to account for the initial 10 adults.

Table 2 The total number of larval, pupal and adult R. dominica observed through sieving and X-ray imaging for brown rice samples.

Infrared Intensity kW/m2 Rice Cultivar Larvae Pupae Adult Total Progeny Total Means ± SE

0 CL152 72 (5) 8 (0) 54 (5) 147 48.0 ± 20.7 XL745 120 (4) 23 (0) 23 (1) 150 57.0 ± 33.5 2.15 CL152 74 (8) 23 (2) 35 (9) 151 50.3 ± 16.8 XL745 91 (6) 27 (0) 18 (1) 143 47.7 ± 24.8 2.83 CL152 82 (8) 15 (0) 19 (1) 125 42.7 ± 24.2 XL745 110 (9) 17 (2) 42 (4) 184 61.0 ± 30.1 10.84 CL152 111 (10) 31 (2) 54 (10) 218 72.7 ± 25.8 XL745 135 (9) 21 (1) 17 (0) 183 61.0 ± 41.5 Mean ± SE 106.8 ± 8.4 21.5 ± 2.7 36.6 ± 6.7 162.6 ± 10.6

Note: Number in parentheses represents the additional larvae and pupae observed when the frass was sieved. Adult totals are with ten subtracted to account for the initial 10 adults.

and adults were counted and the percentage of infested kernels pupae. Because the full models were associated with a variance calculated for each sample. inflation factor > 1, we performed the model selection with Quasi- All analyses were performed in the statistical software program AIC (QAIC; Burnham and Anderson, 2002). These analyses included R(R Core Team, 2017). For all analyses of damage and development, only samples having at least one kernel with development. we used an information-theoretic approach using AIC (Akaike In- formation Criterion; Akaike, 1973). The model with the lowest AIC 2.4. Feeding damage assessment was typically the best model, although if two models had a DAIC < 2, we retained the model with the fewest parameters, following the Through the use of the X-ray images, the kernels with and principle of parsimony (Burnham and Anderson, 2002). Using the without damage were counted and the amount of feeding damage total counts of kernels from sieving and X-ray images, progeny data to each kernel was categorized into 5 levels of damage (0 ¼ no were analyzed in three steps. In the first step, logistic regressions damage, 1 ¼1e25%, 2 ¼ 25e50%, 3 ¼ 50e75%, and 4 ¼ 75e100% for proportion data were conducted to determine if the proportion damage; Fig. 1). The number of kernels in each of the category of kernels with development in a sample was influenced by IR in- levels was counted. As an additional assessment of feeding damage, tensity, rice cultivar, and rice fraction. We considered all possible the amount of frass (excrement and any residual dust from the rice) combinations of these three independent variables, including interactions. In the second step, we excluded samples that had no development and analyzed the amount of development in the remaining samples. We created a progeny score by calculating a weighted average of the number of kernels presenting individuals at each developmental stage using the following formula: p.score ¼ (3a þ 2p þ l)/n, where a, p, and l are the number of kernels containing one adult, pupa, and larva, respectively; n is the total number of kernels; and the coefficients 3, 2, and 1 represent each stage of development (3 ¼ adults, 2 ¼ pupae, and 1 ¼ larvae; category 0 was no development, but these kernels were excluded from these analyses). The progeny score, which ranged from 0 to 3 (from lowest to highest stage of development), was not normally distributed; therefore, we tested for an effect of fraction, cultivar, and IR intensity on the amount of progeny using separate Kruskal-Wallis tests and applying a Bonferroni correction (a ¼ 0.016). In the third step, we also used logistic regressions to determine Fig. 1. An X-ray image of brown rice kernels that were dried with an infrared radiation 2 ¼ more specifically if the proportion of adults that developed in a (IR) intensity of 10.84 kW/m highlighting the different damage categories (0 no damage, 1 ¼1e25%, 2 ¼ 25e50%, 3 ¼ 50e75%, and 4 ¼ 75e100% damage). (For inter- sample was affected by fraction, cultivar, and IR intensity. We pretation of the references to colour in this figure legend, the reader is referred to the repeated this developmental stage-specific approach for larvae and Web version of this article.) 72 R.M. Hampton et al. / Journal of Stored Products Research 81 (2019) 69e75 in each vial was weighed to the nearest 0.05 g. We analyzed damage data in two steps. In the first step, we conducted logistic regressions for proportion data to determine if the proportion of damaged kernels in a sample was influenced by IR intensity, rice cultivar, and rice fraction. We considered all possible combinations of these three independent variables, including interactions. In the second step, we excluded samples that had zero damaged kernels to analyze the amount of damage. We created a damage score by calculating the weighted average number of kernels in each damage category. This damage score, which ranges from 0 to 4 (from lowest to highest amount of damage), was not normally distributed. Therefore, we tested for an effect of fraction, cultivar, and IR intensity on the amount of damage using separate Kruskal-Wallis tests and applying a Bonferroni correction (a ¼ 0.017). Frass weight was not normally distributed for any of the factor categories. However, more frass was produced with brown than rough rice (W ¼ 6290, P < 0.001). Thus, we analyzed the effect of cultivar and intensity on frass weight for each fraction separately. Although frass weight was not normally distributed, we used linear models and checked their validity (e.g., normality for the residuals).

3. Results

3.1. Progeny assessment

All life stages of lesser grain borer were observed on both rough rice (Table 1) and brown rice (Table 2). The best model for the probability of overall development included all factors and two interactions involving intensity (Table 3). The probability of development was greatest with CL152 brown rice dried with an IR intensity of 10.84 kW/m2 (Fig. 2). The amount of progeny was higher for brown rice (mean score ¼ 0.62 ± 0.03) than rough rice (0.13 ± 0.01; K2 ¼ 85.754, df ¼ 1, P < 0.001).

Table 3 Top ﬁve models for the proportion of rice kernels with (1) overall progeny, (2) larvae, (3) pupae, and (4) adults. The variables considered were Cultivar (C) and Fraction (F) of rice, and infrared radiation Intensity (I) as well as their interactions (e.g., FI). The chosen model is listed ﬁrst. AIC is the Akaike Information Criterion, DAIC the difference between each model's AIC and the model with the lowest AIC, AICw the relative weight of the model, and K is the number of parameters. Note: For the in- dividual life stages, QAIC was used.

Factors K AIC DAIC AICw Fig. 2. Probability of overall progeny (A), proportion of kernels with larvae (B), and (1) Overall Progeny proportion of kernels with adults (C) determined by the variables of Cultivar (CL152 F þ C þ I þ FI þ CI 13 1033.4 0.0 0.64 and XL745), Fraction (brown rice; BR and rough rice; RR), and infrared radiation In- F þ C þ I þ FC þ FI þ CI 14 1035.0 1.7 0.28 tensity (0, 2.15, 2.83, and 10.84 kW/m2). Pupae were not included because there was no F þ V þ I þ FC þ FI þ CI þ FCI 17 1037.7 4.3 0.07 signiﬁcant difference other than fraction (BR > RR). F þ I þ C þ FI 10 1044.8 11.4 0.00 F þ C þ I þ CI 10 1044.9 11.6 0.00 (2) Larvae The best model predicting the proportion of kernels with larvae þ C F 4 283.8 0.0 0.35 included the factors of cultivar and fraction (Table 3). Proportion- F þ C þ I 7 284.5 0.7 0.24 C þ F þ CF 5 285.6 1.9 0.14 ally, more larvae were produced on brown rice than rough rice F þ C þ I þ FC 8 285.5 2.8 0.09 (Fig. 2) and the proportion of kernels with larvae was higher with F 3 286.7 3.0 0.08 XL745 than CL152 (Fig. 3). For predicting the proportion of kernels (3) Pupae with pupae, the best model included fraction only (Table 3); pupae F 3 332.0 0.0 0.32 were present on brown rice (0.05 ± 0.01) but not on rough rice C þ F þ CF 5 332.8 0.9 0.21 ± C þ F 4 332.8 0.9 0.21 (0.00 0.00), regardless of cultivar or intensity. I þ F 6 335.4 3.5 0.06 The best model for predicting the proportion of kernels with I þ F þ IF 9 335.7 3.7 0.05 adult development included the factors of cultivar and fraction (4) Adults (Table 3). Proportionally, more adult R. dominica development was C þ F 4 262.6 0.0 0.39 F þ C þ I þ CI 10 262.9 0.4 0.32 observed on brown rice (Fig. 2) and with CL152 than on rough rice or C þ F þ CF 5 264.7 2.1 0.13 with XL745 (Fig. 3). More adult development was seen with CL152 F þ C þ I þ FC þ CI 11 265.3 2.7 0.10 brown rice dried with an IR intensity of 10.84 kW/m2; however, this F þ C þ I 7 268.1 5.5 0.02 was not signiﬁcantly different from the control (Fig. 2). R.M. Hampton et al. / Journal of Stored Products Research 81 (2019) 69e75 73

Table 4 Model selection for the proportion of damaged kernels. The variables considered were Cultivar (C) and Fraction (F) of rice, and infrared radiation Intensity (I) as well as their interactions (e.g., FI). The chosen model is listed ﬁrst. AIC is the Akaike In- formation Criterion, DAIC the difference between each model's AIC and the model with the lowest AIC, AICw the relative weight of the model, and K is the number of parameters.

Factors K AIC DAIC AICw

F þ C þ I þ FC þ FI þ CI 13 994.8 0.00 0.69 F þ C þ I þ FI þ CI 12 997.2 2.43 0.20 F þ C þ I þ FC þ FI þ CI þ FCI 16 998.6 3.79 0.10 F þ C þ I þ FC þ FI 10 1006.1 11.25 0.00 F þ C þ I þ FC þ CI 10 1006.1 11.26 0.00 F þ C þ I þ CI 9 1006.9 12.12 0.00 F þ I þ C þ FI 9 1007.7 12.84 0.00 F þ C þ I þ FC 7 1016.2 21.42 0.00 F þ C þ I 6 1017.8 22.99 0.00 I þ F þ IF 8 1024.0 29.16 0.00 I þ F 5 1034.1 39.31 0.00 C þ F þ CF 4 1037.1 42.26 0.00 C þ F 3 1038.6 43.84 0.00 F 2 1055.1 60.32 0.00 C þ I þ CI 8 2791.3 1796.52 0.00 C þ I 5 2797.6 1802.75 0.00 I 4 2810.3 1815.51 0.00 C 2 2813.3 1818.50 0.00 Null 1 2826.2 1831.36 0.00

Fig. 3. The proportion of kernels with larvae (A) and adults (B) based on the best AIC model with the variables of Cultivar (CL152 and XL745) and Fraction (brown rice; BR and rough rice; RR). Pupae were not included because only fraction had a signiﬁcant effect on pupae (BR > RR).

3.2. Feeding damage assessment

The best model explaining the proportion of damaged kernels Fig. 4. Proportion of kernel damage for each Cultivar by Fraction and Intensity. included all factors and two-way interactions (Table 4). The proportion of damaged kernels was the highest with CL152 brown rice dried with an IR intensity of 10.84 kW/m2 (Fig. 4). Interestingly, the Table 5 highest IR intensity for both varieties of brown rice resulted in the Kruskal-Wallis tests results for the kernel damage score for the variable of Cultivar, Fraction, and Intensity. highest proportion of damaged kernels. However, with rough rice for both varieties, the control (0 kW/m2) resulted in the greatest Variable(s) K-value Degrees of Freedom P-value proportion of damaged kernels (Fig. 4). Fraction was the only var- Cultivar 0.112 1 0.738 iable affecting the amount of kernel damage (K2 ¼ 92.147, df ¼ 1, Fraction 92.147 1 <0.0001a P < 0.001; Table 5). Brown rice had kernels with significantly more Intensity 1.974 3 0.578 feeding damage (mean damage score: 1.23 ± 0.06) than rough rice a Indicates significance at a ¼ 0.017. (mean damage score: 0.18 ± 0.01). Brown rice also had a greater amount of frass (0.23 ± 0.01 g) than rough rice (0.02 ± 0.00 g; ¼ < W 6290, P 0.001). The best model for the amount of frass for 4. Discussion both brown and rough rice was the null model; therefore neither cultivar nor intensity affected the amount of frass. Although not Single-layer IR-drying of rice with an initial m.c. of approx. 20% fi signi cantly different from other categories, the greatest amount of wet basis at an intensity of 10.84 kW/m2 for a duration of 7 s frass produced was with brown rice on CL152 dried with 10.84 kW/ reaching a temperature of 60 C potentially increases the kernels’ 2 m (0.961 g). susceptibility to R. dominica infestations. IR drying with 10.84 kW/ 74 R.M. Hampton et al. / Journal of Stored Products Research 81 (2019) 69e75 m2 used on CL152 brown rice caused an increased proportion of unclear. It is also unknown if these pupae would successfully overall progeny, including an increased amount of adults. An IR develop into adults because the pupae were observed during treatment of 10.84 kW/m2 for both varieties and fractions caused sieving which took place after freezing to stop development. Due to an increase in the number of larvae observed. No significant effect these unknowns, further experimentation is needed. involving IR intensity was observed for the amount of pupae. The Infrared radiation is not the only novel agricultural technology greatest amount of frass was also observed with CL152 brown rice explored in this study. X-ray imagery for the purpose of insect dried with an IR intensity of 10.84 kW/m2. Although no noticeable detection as well as grain damage appears to work well. Others differences were seen on the X-ray images between treated and have looked into X-ray as a method of detecting insects in wheat untreated samples, there could be changes in the rice microstruc- samples. Karunakaran et al. (2004) successfully used X-ray to detect ture (i.e., fractures and changes in the number of pubescent hairs damage in wheat caused by the red flour beetle, Tribolium casta- present on the hull) caused by the highest amount of infrared neum (Herbst). Also, Brabec et al. (2010) used X-ray to detect broken tested (10.84 kW/m2). Previous studies have shown that high insects in wheat flour with success as a comparison tool. In a review temperatures can cause fissures in the grain, which can make the of current and future methods of insect detection in grain, kernels more susceptible to insect infestations (Phillips and Throne, Neethirajan et al. (2007) suggested X-ray as a detection method 2010; Kavallieratos et al., 2012). with great promise for detecting insects both internally and There was significantly more development and damage externally of grain. The images taken for this study confirm that X- observed on brown rice than rough rice. This is most likely because ray imaging is a useful tool for detecting internal insects in larval, rough rice kernels are more protected by the presence of the outer pupal, and adult stages in both rough and brown rice and as a non- hull. Since some differences were observed between the two vari- destructive method for assessing damage caused to the kernel. eties, the hull of one cultivar may be harder than for the other, Further exploration of X-ray imaging as an agricultural tool for the giving it more protection. Being a hybrid rice cultivar, XL745 has a detection of insect pests and damage needs to be continued in the pubescent hull; therefore, this could result in greater protection future as it appears to have good potential. X-ray could be used as a from insect infestation. This could help explain why more devel- quick, non-destructive way for facilities such as rice mills to look for opment and damage was observed with CL152 than with XL745. internal insect pests (including immature stages) that could not be Future research should examine the effect of hull characteristics seen by traditional sampling methods. and insect infestation, and how IR drying might affect these Advances with IR have already been made, such as the use of characteristics. flameless catalytic methods over those that used an open flame. What causes the increase seen in development of larvae and These IR methods heat the grain, rather than using ionizing radi- adults in 10.84 kW/m2 IR-treated samples in comparison to control ation (i.e. gamma rays), a method that is unfortunately highly samples, needs to be further explored because this treatment scrutinized by consumers (Phillips and Throne, 2010). Near infrared (although not significantly different than some other treatments) (NIR) hyperspectral imaging and NIR spectroscopy (NIRS) are other resulted in the highest number of larvae and adults. This is technologies that need further exploration. Singh et al. (2009) and important because it can be expected that an increase in insect Perez-Mendoza et al. (2004) have used these methods to detect populations causes an increase in the amount of damage, and kernels of wheat that had been damaged by insect pests and to age damage to the kernels affects the quality of the grain. Infested and insect pests that are used for research, respectively. These are just a especially damaged grain can be difficult if not nearly impossible to few examples of IR's potential and why there needs to be further sell, particularly for human consumption. If the grain is sold, it will research conducted for agricultural use. be at a reduced cost meaning a loss for the rice producer. Rice production losses due to insect and fungi damage are estimated at Acknowledgments over $500 million (Kells et al., 2001). This leads to increased prices for consumers in the long run as well as an overall reduction in the We thank the rice producers who supplied the rice for this amount of grain available for consumption. project. They were very helpful in supplying rice with a high Another finding of interest that needs further exploration, is moisture content that could be dried using the infrared radiation. what causes the difference in the proportion of kernels with We also thank anonymous reviewers who helped us clarify this damage observed between the two fractions. For brown rice, the manuscript. Funding for this study was provided by the Arkansas 2 highest intensity of 10.84 kW/m resulted in the highest proportion Agricultural Experiment Station. of kernels with damage, for both cultivars. However, the exact opposite was observed for both cultivars in their rough rice form. Appendix A. Supplementary data With rough rice, the control had the highest proportion of kernels with damage. This could be because the IR drying changed the hull Supplementary data to this article can be found online at in a way that makes the kernels more protected than the control https://doi.org/10.1016/j.jspr.2019.01.002. kernels. This side effect could mean that a low intensity of IR used to dry the rice kernels could make the kernels more protected from References insect infestations than with natural air drying. In this study, larvae and pupae were observed among the ker- Afful, E., Elliott, B., Nayak, M.K., Phillips, T.W., 2017. Phosphine resistance in North nels in the development vials. Pupae were observed to cluster rice American field populations of the lesser grain borer, Rhyzopertha dominica e kernels around them and “gluing” them together into a pupation (Coleoptera: Bostrichidae). J. Econ. Entomol. 111, 463 469. Akaike, H., 1973. Information theory and an extension of the maximum likelihood chamber. However, these life stages normally develop internally principle. 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