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Feeding efficiency and digestive physiology of Trogoderma granarium Everts (Coleoptera: Dermestidae) on different rice cultivars
Journal of Stored Products Research 84 (2019) 101511
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Feeding efficiency and digestive physiology of Trogoderma granarium Everts (Coleoptera: Dermestidae) on different rice cultivars Shervin Barzin, Bahram Naseri*, Seyed Ali Asghar Fathi, Jabraeil Razmjou, Pezhman Aeinehchi Department of Plant Protection, Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran
a r t i c l e i n f o
a b s t r a c t
Article history: Received 28 June 2019 Received in revised form 9 September 2019 Accepted 10 September 2019 Available online xxx
The Khapra beetle, Trogoderma granarium Everts (Coleoptera: Dermestidae), is one of the economic pests infesting many stored cereals in the world. The effects of six commercial rice, Oryza sativa L. cultivars including Hashemi, Shiroodi, Gilane, Khazar, Ali Kazemi and Domsiah were evaluated on nutritional indices and digestive enzymatic activity of fifth instar T. granarium at controlled conditions (33±1 C, relative humidity of 65 ± 5%, and a photoperiod of 14:10 (L:D) h). Fifth instar larvae consumed more food when reared on Gilane, and less food when reared on Khazar and Ali Kazemi. The larvae fed with Khazar had the lowest weight gain, efficiency of conversion of ingested food and growth index. The relative growth rate was the highest when larvae were fed with Gilane and lowest when they were fed with Khazar. The highest midgut proteolytic and amylolytic activities of larvae were on Gilane. However, the lowest proteolytic activity was on Khazar and the lowest amylolytic activity was on Khazar and Ali Khazemi. According to the obtained results, Khazar is an unsuitable cultivar for feeding and growth of T. granarium. © 2019 Elsevier Ltd. All rights reserved.
Keywords: Nutritional performance Plant resistance Rice cultivar Trogoderma granarium
1. Introduction The Khapra beetle, Trogoderma granarium Everts (Coleoptera: Dermestidae), is one of the main pests of stored cereals such as wheat, rice, barley, maize and sorghum in the world (Lindgren et al., 1955; Burges, 2008; Majd-Marani et al., 2017). Although it has an extremely large variety of food preferences, but overall rice is not the preferred diet as compared to other cereals like wheat, barley and rye (Borzoui et al., 2015). The larval stage of this pest has the most feeding capacity on the seed embryo, but its adults are not able to feed (Jood et al., 1996). The feeding of larvae causes economic damage by decrease in nutritional quality of stored cereals especially depletion of protein and carbohydrate (Jood and Kapoor, 1993; Jood et al., 1996; Ahmedani et al., 2009). Subsequently, the market value of stored cereals contaminated by T. granarium larvae can be reduced (Jood and Kapoor, 1993; Weston and Rattlingourd, 2000; Hansen et al., 2004). Synthetic pesticides have been used as a first tool for management of stored-product insects such as T. granarium (Throne et al.,
* Corresponding author. E-mail address: [email protected] (B. Naseri). https://doi.org/10.1016/j.jspr.2019.101511 0022-474X/© 2019 Elsevier Ltd. All rights reserved.
2000; Finkelman et al., 2006; Mohandass et al., 2007), however, there are problems associated with using these compounds with respect to human health and non-target organisms (Hagstrum and Subramanyam, 1996; Han et al., 2016). Therefore, understanding of feeding efficiency and digestive enzymatic activity of T. granarium could be helpful in choosing pest management strategies (Kazzazi et al., 2005). Host plant cultivars that are resistant to insect pests can negatively change their growth, survival and reproductive potential (Ofuya and Credlandt, 1995; Naseri et al., 2009; Ashamo, 2010; Nawrot et al., 2010; Borzoui and Naseri, 2016). Thus, using resistant grains is a suitable method to minimize infestations by stored-grain pests (Panda and Khush, 1995). Plant-insect interactions and the resistance of diverse host plants to herbivorous insects can be evaluated by nutritional indices (Naseri and Borzoui, 2016). Nutritional indices of T. granarium on various wheat (Triticum aestivum L.) cultivars were evaluated by Aheer and Ahmad (1993), who reported that the cultivar 86299 was comparatively an unsuitable host for development of this pest. Resistance of wheat cultivars to T. granarium was studied by Rao et al. (2004), who noted that the size and seed hardness had a significant effect on resistance of wheat cultivars to this insect. Sayed et al. (2006) investigated the resistance of different wheat cultivars to T. granarium and revealed
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that Mehran-89 was the most resistant cultivar. Seifi et al. (2015) evaluated the nutritional indices and digestive physiology of T. granarium fed with various barley (Hordeum vulgare L.) cultivars and detected the highest amylolytic and proteolytic activities on cultivar Bahman. Majd-Marani et al. (2017) studied the effect of nine maize (Zea mays L.) hybrids on biology and life table parameters of T. granarium, and reported that BC 678 was a resistant hybrid for population increase of this insect. The effect of various maize hybrids on nutritional performance and digestive enzymatic activity of T. granarium was studied by Majd-Marani et al. (2018), who expressed that BC 678 was an unsuitable hybrid for feeding of fifth instar larvae. The influence of wheat cultivar on feeding performance of T. granarium was studied by Golizadeh and Abedi (2016), who noted that cultivar Kuhdasht was an unfavorable host. Furthermore, Golizadeh and Abedi (2017) considered the varietal resistance of barley against T. granarium and declared that the highest population growth was on cultivar Makuyi. Two major groups of digestive enzymes in the insects' midgut are proteases and amylases that hydrolyze protein and starch, respectively (Nation, 2001; Dastranj et al., 2013). The selective inhibition of these enzymes can be one of the most critical techniques of the insect's management (Bigham and Hosseininaveh, 2010). Borzoui et al. (2015) measured the digestive physiology of T. granarium larvae on different diets including rice (Oryza sativa L.) wheat, barley, rye (Secale cereale L.) and walnut (Juglans regia L.) and noted that both amylase and protease enzymes had the lowest activities when larvae were reared on the walnut. Mardani-Talaee et al. (2017) studied digestive enzymatic activity of T. granarium fed with various barley cultivars and reported high activities of amylase and protease in larvae fed with Line30. Despite the economic importance of T. granarium on stored cereals (Hosseininaveh et al., 2007) especially on rice, no published articles are available about the nutritional performance and digestive enzymatic activity of this pest on rice cultivars. In the present study, therefore, we evaluated the nutritional indices and digestive enzymatic activity of T. granarium larvae in response to feeding on six commercial rice cultivars. The results of this research would be useful to detect rice cultivar(s) unfavorable to T. granarium for developing pest management techniques. For example, resistant cultivar(s) could be stored at granary for longer periods with reduced economic losses by this insect. 2. Materials and methods 2.1. Origin of seeds and insects We used clean, de-husked white rice (Oryza sativa L.) for the experiments. Six rice cultivars including Hashemi, Gilane, Khazar, Shiroodi, Ali Kazemi and Domsiah were supplied by the Agricultural and Natural Resources Research Center of Guilan, Iran. Before beginning of the experiments, all rice seeds were ground for 30 s using an electric grinder. The colony of T. granarium larvae and adults was obtained from the Department of Plant Protection, University of Mohaghegh Ardabili, Iran. They were fed with wheat seeds and maintained at 33±1 C, relative humidity of 65 ± 5%, and a photoperiod of 14:10 (L:D) h, based on the method described by Karnavar (1967). 2.2. Nutritional indices Food consumption and weight gain of larvae were evaluated gravimetrically following Waldbauer (1968). Nutritional indices were investigated on dry-weight basis. Seven groups of 10 fifth instar larvae were weighed for each cultivar. Then, they were transferred into the Petri dishes (diameter 6 cm, depth 1 cm)
containing 1 g of the ground rice seeds for feeding of larvae. After two weeks, the final weight was measured to determine changes in the weight. To investigate total dry weight, twenty specimens of larvae other than those used in feeding tests were weighed, ovendried at 60 C for 48 h, and thereafter re-weighed. Nutritional indices of T. granarium were calculated by using formulae explained by Waldbauer (1968): Efficiency of conversion of ingested food (ECI) ¼ P/E; relative consumption rate (RCR) ¼ E/W0 T; and relative growth rate (RGR) ¼ P/W0 T; where, W0 ¼ initial dry weight of larvae, E ¼ dry weight of food consumed, P ¼ dry weight gain of larvae, T ¼ feeding period (day). 2.3. Growth index and pupal weight The survival rate of larvae, larval growth index (LGI) and pupal weight of T. granarium were estimated on various rice cultivars (Itoyama et al., 1999): LGI ¼ lx/L; where, lx ¼ survival rate of larvae, L ¼ larval period (day). 2.4. Preparation of midgut enzymes Enzyme specimens were prepared from the midguts of fifth instar larvae of T. granarium fed with different rice cultivars (Hosseininaveh et al., 2007). The number of 150 larvae for each cultivar were selected and dissected on ice and their midguts were gathered into a 1.5 mL of distilled water. Midguts were homogenized on ice using a pre-cooled homogenizer (Teflon pestle). The homogenates were centrifuged at 15,000g at 4 C for 15 min. The collected supernatants were transferred to new microtubes and kept at 20 C for enzymatic assays. 2.5. Amylase activity assay 3-5-Dinitrosalicylic acid (DNSA) procedure (Bernfeld, 1955), with a minor modification, was used to assay digestive amylolytic activity. A quantity of 130 ml of Tris-HCl (pH, 8), and 60 ml of 1% soluble starch (Sigma chemical Co., St Louis, USA, 99% purity) were incubated with 20 ml of the enzyme elicited from larval midgut at 37 C for 30 min. The reaction was stopped by the addition of 100 ml of DNSA and heated (85-95 C) for 10 min in boiling water. After cooling on ice for 5 min, the absorbance was read at 540 nm. One portion of amylase activity was defined as the quantity of enzyme required to produce 1 mg maltose (Sigma chemical Co., St Louis, USA) at 37 C for 30 min. A standard curve of absorbance versus quantity of maltose released was constructed to enable its computation the during amylase assay. All assays were carried out in triplicate with blanks containing no enzyme extract. 2.6. Protease activity assay The azocasein digestion procedure (Gatehouse et al., 1999; Elpidina et al., 2001) was used to determine total proteolytic activity of T. granarium fed with six rice cultivars. To assay the proteolytic activity, the reaction combination included 50 ml of azocasein (1.5%) solution in 50 mM glycine-NaOH buffer (pH 10) (Borzoui et al., 2015) and 50 ml of extracted enzyme from midgut. The mixture was incubated at 37 C for 50 min. Proteolysis was terminated by the addition of 100 ml of 30% trichloroacetic acid (TCA), after cooling at 4 C for 30 min, centrifuged at 15,000g for 10 min. One hundred microliters of supernatant was mixed with 100 ml of 2 M NaOH and the absorbance was read at 440 nm (using ELIZA-Reader, Anthos, 2020; England). Proper blanks were provided for each treatment which TCA had been added prior to the substrate. The increase in optical density per milligram protein per
S. Barzin et al. / Journal of Stored Products Research 84 (2019) 101511
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Table 1 Mean (±SE) nutritional indices of fifth instar Trogoderma granarium fed with different rice cultivars. Cultivar
E (mg/larva)
P (mg)
ECI (%)
RCR (mg/mg/day)
RGR (mg/mg/day)
Gilane Hashemi Domsiah Ali Kazemi Khazar Shiroodi
1.52 ± 0.04a 1.17 ± 0.04c 1.32 ± 0.02bc 0.99 ± 0.03d 0.99 ± 0.05d 1.46 ± 0.04 ab
0.46 ± 0.05a 0.32 ± 0.03 ab 0.32 ± 0.03 ab 0.24 ± 0.03bc 0.17 ± 0.03c 0.46 ± 0.03a
29.97 ± 2.83a 27.21 ± 1.91bc 24.11 ± 1.74bc 23.54 ± 2.93bc 17.37 ± 3.03c 31.56 ± 1.79a
0.065 ± 0.001a 0.049 ± 0.001c 0.056 ± 0.001bc 0.041 ± 0.000d 0.040 ± 0.001d 0.061 ± 0.002 ab
0.019 ± 0.002a 0.013 ± 0.001bc 0.013 ± 0.001bc 0.009 ± 0.001cd 0.007 ± 0.001d 0.019 ± 0.001 ab
Means followed by different letters in the same column are significantly different (Tukey, P < 0.05). E ¼ Food consumption, P ¼ Weight gain, ECI ¼ Efficiency of conversion of ingested food, RCR ¼ Relative consumption rate, RGR ¼ Relative growth rate.
minute was represented by one unit of protease activity. All the tests were done in triplicate. 2.7. Grain characteristics Starch content of tested cultivars was determined according to the method of Bernfeld (1955) using starch as a standard. A quantity of 200 mg of each powdered cultivar was homogenized in 35 ml of distilled water and heated to boiling. One-hundred microliters of each specimen were added in 2.5 ml of iodine reagent (0.02% I2 and 0.2% KI), and thereafter absorbance was read at 580 nm. Protein content of examined cultivars was assayed based on the method of Bradford (1976) applying bovine serum albumin as a standard. Based on standard particle size index [%] method (AACC 55e30, 2000), grain hardness was quantified. Primarily, rice cultivars were powdered for 1 min, and then sieved for 1 min. The weight of powdered seeds that passed from the sieve to the total seed weight was considered as a seed hardness index. To evaluate moisture content of each tested cultivar, 2 g of each powdered cultivar was weighed and placed in an oven set at 100 C for 3 h, then reweighed. 2.8. Statistical analysis Examination of all data for normality was done using Kolmogorov-Smirnov test before the analysis. Nutritional indices, growth index, pupal weight and enzymatic activity of T. granarium were examined according to a completely randomized design, via one-way analysis of variance (ANOVA). Statistical differences among the means were ascertained via the Tukey test at a ¼ 0.05. The correlation of some physicochemical characteristics of tested rice cultivars (amount of protein and starch, moisture content and seed hardness) with nutritional indices and digestive enzymatic activity of T. granarium was investigated by Pearson correlation coefficient using SPSS 16.0. 3. Results 3.1. Nutritional indices The nutritional indices of fifth instar larvae of T. granarium fed with different rice cultivars are presented in Table 1. The highest food consumption (F ¼ 6.951, df ¼ 5, 41, P < 0.05) was observed when larvae were fed with cultivar Gilane and the lowest value was seen when they were fed with cultivars Khazar and Ali Kazemi. The highest larval weight gain (F ¼ 11.601, df ¼ 5, 41, P < 0.05) was on cultivars Gilane and Shiroodi and the lowest weight gain was on cultivar Khazar. Moreover, the larvae fed with cultivar Khazar exhibited the lowest ECI value (F ¼ 163.282, df ¼ 5, 41, P < 0.05) compared with the other cultivars. The RCR value (F ¼ 32.221, df ¼ 5, 41, P < 0.05) was the highest on cultivar Gilane and the lowest on cultivars Khazar and Ali Kazemi. The highest and lowest
Table 2 Survival rate of larvae, and mean (±SE) larval growth index (LGI) and pupal weight of Trogoderma granarium fed with different rice cultivars. Cultivar
Survival rate (%)
LGI
Pupal weight (mg)
Gilane Hashemi Domsiah Ali Kazemi Khazar Shiroodi
98 89 94 92 88 98
2.72 ± 0.04a 2.26 ± 0.02c 2.55 ± 0.04b 2.47 ± 0.03b 2.16 ± 0.02c 2.71 ± 0.04a
3.31 ± 0.10a 3.30 ± 0.04a 3.24 ± 0.02a 3.45 ± 0.13a 3.48 ± 0.11a 3.42 ± 0.13a
Means followed by different letters in the same column are significantly different (Tukey, P < 0.05).
RGR values (F ¼ 12.712, df ¼ 5, 41, P < 0.05) were on cultivars Gilane and Khazar, respectively.
3.2. Growth index and pupal weight Data of survival rate, growth index and pupal weight of T. granarium fed with various rice cultivars are shown in Table 2. The survival rate of larvae ranged from 98% on cultivars Gilane and Shiroodi to 88% on Khazar. Larval growth index (F ¼ 42.15; df ¼ 5, 41; P < 0.05) was the highest on cultivars Gilane and Shiroodi, and lowest on cultivars Hashemi and Khazar. No significant difference was observed for pupal weight (F ¼ 0.94; df ¼ 5, 41; P ¼ 0.47) of T. granarium on tested cultivars.
3.3. Enzymatic activity of larvae Amylolytic (F ¼ 33.211, df ¼ 5, 17, P < 0.05) and total proteolytic (F ¼ 13.849, df ¼ 5, 17, P < 0.05) activity of fifth instar larvae of T. granarium fed with tested rice cultivars is shown in Table 3. The highest amylolytic activity was observed when larvae were fed with cultivar Gilane, whereas the lowest activity was seen when they were fed with cultivars Khazar and Ali Kazemi. The larvae reared on cultivar Gilane showed the highest protease activity, whereas the lowest activity was observed on cultivar Khazar.
Table 3 Mean (±SE) amylolytic and proteolytic activities of midgut extracts from fifth instar larvae of Trogoderma granarium fed with different rice cultivars. Cultivar
Amylolytic activity (mU/mg)
Proteolytic activity (U/mg)
Gilane Hashemi Domsiah Ali Kazemi Khazar Shiroodi
0.644 ± 0.008a 0.539 ± 0.020b 0.560 ± 0.003 ab 0.408 ± 0.044c 0.339 ± 0.009c 0.613 ± 0.001 ab
0.128 ± 0.020a 0.060 ± 0.002bc 0.068 ± 0.003bc 0.051 ± 0.002bc 0.034 ± 0.003c 0.081 ± 0.004b
The means followed by different letters in the same column are significantly different (Tukey P < 0.05).
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Table 4 Mean (±SE) some biochemical and physical characteristics in seeds of tested rice cultivars. Cultivar
Starch content (mg/g)
Protein content (mg/g)
Hardness index (%)
Moisture content (%)
Gilane Hashemi Domsiah Ali Kazemi Khazar Shiroodi
0.25 ± 0.01a 0.08 ± 0.01b 0.11 ± 0.01 ab 0.07 ± 0.01b 0.04 ± 0.01c 0.19 ± 0.09 ab
1.89 ± 0.04a 1.50 ± 0.02bc 1.84 ± 0.03 ab 1.91 ± 0.03a 1.87 ± 0.02a 1.14 ± 0.18c
51.56 ± 0.43a 42.60 ± 0.72c 46.44 ± 0.38b 32.28 ± 0.35d 31.32 ± 0.52d 48.56 ± 0.41b
12.08 ± 0.79a 6.58 ± 0.34cd 7.30 ± 0.55c 4.79 ± 0.09de 4.42 ± 0.31e 10.12 ± 0.43b
The means followed by different letters in the same column are significantly different (Tukey, P < 0.05).
3.4. Grain characteristics Table 4 shows some biochemical and physical characteristics of tested rice cultivars. The highest soluble starch content (F ¼ 679.203; df ¼ 5, 17; P < 0.05) was in cultivar Gilane, while the lowest content was in cultivar Khazar. Among tested cultivars, cultivar Shiroodi showed the lowest amount of protein (F ¼ 15.749; df ¼ 5, 17; P < 0.05). Higher particle size index (F ¼ 306.369; df ¼ 5, 29; P < 0.05) for cultivar Gilane displayed that this cultivar is softer than the others. Also, lower particle size index for cultivars Khazar and Ali Kazmi exhibited that they are harder than the others. The highest and lowest percentage moisture content was seen in cultivars Gilane and Khazar, respectively (F ¼ 40.360; df ¼ 5, 17; P < 0.05). 3.5. Correlation analysis The analysis of correlation coefficients of the nutritional indices and digestive enzymatic activity of T. granarium with some physicochemical traits of tested cultivars are indicated in Table 5. The results of this study demonstrated that positive correlations were seen among food consumption (r ¼ 0.76), RGR (r ¼ 0.53), RCR (r ¼ 0.79), and proteolytic (r ¼ 0.70) and amylolytic (r ¼ 0.79) activities with particle size index. Also, food consumption (r ¼ 0.38), RCR (r ¼ 0.57), and proteolytic (r ¼ 0.91) and amylolytic (r ¼ 0.85) activities showed positive correlations with moisture content of tested seeds. There was no significant correlation among tested characteristics of T. granarium with protein content. 4. Discussion The nutritional performance of the insects is dependent upon quality and quantity of consumed diets and physico-chemical characteristic of host plants (Behmer, 2009; Karasov et al., 2011). Feeding on a low quality diet by herbivorous insects could result in delayed growth, reduced survival and fecundity (Lee, 2007; Borzoui
Table 5 Pearson correlation coefficients (r) of some physiological characteristics of Trogoderma granarium fed with different rice cultivars with protein content, starch content, particle size index and moisture content of tested rice cultivars. Parameter
E RGR RCR ECI PA AA
Protein content
Starch content
Particle size index
Moisture content
r
p
r
p
r
p
r
p
0.21 0.06 0.39 0.08 0.07 0.40
0.406 0.827 0.11 0.746 0.796 0.098
0.41 0.33 0.58 0.14 0.70* 0.66
0.089 0.182 0.013 0.571 0.001 0.300
0.76* 0.53* 0.79* 0.16 0.70* 0.79*
0.000 0.002 0.000 0.412 0.001 0.000
0.38** 0.42 0.57 0.24 0.91* 0.85*
0.020 0.081 0.014 0.328 0.000 0.000
E ¼ Food consumption, RGR ¼ Relative growth rate, RCR ¼ Relative consumption rate, ECI ¼ Efficiency of conversion of ingested food, PA¼ Proteolytic activity, AA ¼ Amylolytic activity. *p < 0.01; **p < 0.05.
and Naseri, 2016). The results of this study showed that the food quality, particularly seed hardness of tested rice cultivars, influenced the nutritional indices and digestive enzymes activity of T. granarium larvae. In this study, there were six larval instars on all the tested rice cultivars. However, fifth instar larvae were used in the experiments, because they had higher feeding potential and weight gain than the sixth instar larvae (personal observations). The number of larval instars in T. granarium differed from 6 instar on wheat to 10 instar on rice and walnut. Moreover, the developmental time of larvae on rice (77.25 days) was longer than that obtained on wheat, barley and rye (Borzoui et al., 2015). Therefore, it would be concluded that rice is relatively unsuitable host commodity for feeding and development of T. granarium as compared to the other cereals. This study demonstrated that T. granarium larvae consumed less seeds when reared on cultivars Khazar and Ali Kazemi, leading to the lowest weight gain and digestive enzymatic activity. Furthermore, a significant correlation between food consumption and particle size index (r ¼ 0.75) indicated that the seed hardness was a main factor responsible for the amount of food eaten and weight gain of larvae. Since the seeds of cultivars Khazar and Ali Kazemi are harder than other cultivars, larvae are not able to feed more seeds when reared on these cultivars. Although cultivar Ali Kazemi has a high amount of protein, lower food consumption and weight gain of larvae on this cultivar could be related to seed hardness of it. The amount of food consumption on cultivar Khazar in this study is higher than that reported for T. granarium fed with wheat cultivars (Golizadeh and Abedi, 2016) and maize hybrids (Majd-Marani et al., 2018). It could be suggested that rice cultivars tested in our study are more suitable diet than the cereals (wheat and maize) examined by above-mentioned authors for feeding of larvae. However, the range of food consumption on various rice cultivars is lower than that noted by Seifi et al. (2015) on barley cultivars. Higher weight gain of larvae in T. granarium fed with seeds of cultivar Gilane can be due to the high protein and starch contents and soft seeds of this cultivar (Table 4). The range of larval weight gain in our study is higher than that reported for T. granarium fed with various wheat cultivars (Golizadeh and Abedi, 2016). Differences in larval instar and host grain used by Golizadeh and Abedi (2016) with those tested in our study could explain this inconsistency. The larvae of T. granarium fed with cultivar Khazar indicated the lowest value of ECI, suggesting a less potential of larvae to convert the eaten diet to body mass. Decrease in the weight gain of larvae on cultivar Khazar can explain lower ECI value obtained on this cultivar. Moreover, higher value of ECI on cultivars Gilane and Shiroodi might be attributed to higher weight gain of larvae fed with these two cultivars. In this research, the highest ECI value is approximately similar to that reported for T. granarium on maize hybrid 704 (Majd-Marani et al., 2018) and wheat cultivar Saysonz (Golizadeh and Abedi, 2016). However, the range of ECI values of T. granarium in our study is higher than that expressed on barley cultivars (Seifi et al., 2015; Golizadeh and Abedi, 2017). It would be suggested that the suitability and nutritional value of rice cultivars
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tested in our study is more than barley cultivars used by abovementioned authors for feeding of larvae. The highest values of RGR and RCR in fifth instar larvae fed with cultivar Gilane are due to softer grain and higher amount of starch and moisture in this cultivar. Furthermore, T. granarium fed with cultivar Gilane spent a shorter time to complete larval and pupal stages than that fed with the others (personal observations). Despite the high nutritional quality of cultivar Khazar in terms of protein content, it is a hard grain with low content of starch and moisture. Thus, the growth rate of larvae was the lowest when fed with this cultivar. The range of RGR value on rice cultivars tested in this study is lower than that reported for T. granarium on maize hybrids (Majd-Marani et al., 2018), wheat (Golizadeh and Abedi, 2016), and barley (Seifi et al., 2015) cultivars. The larval growth index (LGI) is one of the important indicators determining the suitability of a host plant to insects, because both survival and duration of larval stages affect this index. As survival rate of larvae was the lowest on cultivar Khazar, the LGI was obtained lowest when larvae were fed with this cultivar, suggesting its unsuitability as a host for growth of T. granarium. The range of LGI in this study is higher than that reported by Seifi et al. (2015) for T. granarium on different barley cultivars. The results of this study showed no significant difference in pupal weight of T. granarium fed with tested cultivars. One of the possible reasons of this result is the high mortality of larvae fed with cultivar Khazar (as an unsuitable cultivar). On the other hands, fewer larvae are pupated while feeding on the resistant cultivar than those fed with the other cultivars. Quality and quantity of food eaten by T. granarium can influence the digestive physiology of larvae (Bernardi et al., 2012; Borzoui et al., 2015; Naseri and Borzoui, 2016). Results from digestive enzymatic assay indicated that larvae fed with cultivar Gilane had the highest enzymatic activity, whereas cultivar Khazar-fed larvae showed the lowest activity. As seen in Table 4, the protein content between cultivars Gilane and Khazar was not significantly different. Therefore, different levels of digestive enzymatic activity of larvae fed with these two cultivars might be attributed to starch content, seed hardness and moisture content of tested cultivars. Based on the correlation analysis, there was a positive and significant relationship between protease and amylase activity with both hardness index and seed moisture content. The role of seed hardness on the levels of digestive enzyme activity in T. granarium is reported by Majd-Marani et al. (2017). In another study, Naseri and Borzoui (2016) proved that amylolytic activity of Sitotroga cerealella (Olivieri) larvae fed with harder wheat grain was lower than those reared on softer grain. Moreover, Mardani-Talaee et al. (2017) reported that amylolytic and proteolytic activities in T. granarium larvae were the lowest when they were fed with barley varieties with hard grains. In our study, the proteolytic activity of T. granarium on different rice cultivars is lower than that reported for T. granarium fed with various barley cultivars (Seifi et al., 2015). This variation could be due to different host species and larval instar tested by Seifi et al. (2015). Furthermore, it is reported that some anti-nutritional substances such as plant enzyme inhibitors occur in barley seeds, which strongly regulate digestive physiology of insects (Casaretto et al., 2004; Borzoui et al., 2015). The amylolytic activity of larvae on cultivar Khazar is nearly close to the activity reported by Seifi et al. (2015) on barley cultivar Bahman (as a resistant cultivar). The results of this study showed that T. granarium larvae fed with cultivar Khazar (as a hard grain with low starch and moisture content) had the lowest feeding efficiency and midgut enzymatic activity. Thus, Khazar was the least suitable (most resistant) cultivar for feeding and growth of this insect. This cultivar can be stored for longer periods of time at storage conditions with reduced
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management cost of T. granarium. Moreover, it can be suggested to incorporate into the breeding programs to minimize seed losses by this pest. However, susceptible rice cultivars such as Gilane and Shiroodi will require more protection approaches to prevent infestation by T. granarium. To obtain more practical knowledge to control T. granarium, recognition and purification of secondary chemical compounds (such as digestive enzymes inhibitors) of the resistant cultivar would be required. Acknowledgment We thankfully acknowledge the University of Mohaghegh Ardabili, Ardabil, Iran, for collaboration by support for the experiment. References AACC 55e30, 2000. Approved Methods of the American Association of Cereal Chemists, tenth ed. The American Association of Cereal Chemists, St Paul, MN. Aheer, G.M., Ahmad, R., 1993. Response of wheat to Trogoderma granarium (Everts.) and Rhizopertha dominica (F.B.). J. Agric. Res. 31, 319e322. Ahmedani, M.Sh, Haque, M.I., Afzal, S.N., Aslam, M., Naz, S., 2009. Varietal changes in nutritional composition of wheat kernel (Triticum aestivum L.) caused by Khapra beetle infestation. Pak. J. Bot. 41 (3), 1511e1519. Ashamo, M.O., 2010. Relative resistance of paddy varieties to Sitotroga cerealella (Lepidoptera: Gelechiidae). Biologia 65 (2), 333e337. Behmer, S.T., 2009. Insect herbivore nutrient regulation. Annu. Rev. Entomol. 54, 165e187. Bernardi, D.M., Garcia, S., Botton, M., Nava, D.E., 2012. Biology and fertility life table of the green aphid Chaetosiphon fragaefolli on strawberry cultivars. J. Insect Sci. 12, 28 available online. insectscience.org/12.28. Bernfeld, P., 1955. Amylase, a and b. Methods Enzymol. 1, 149e158. Bigham, M., Hosseininaveh, V., 2010. Digestive proteolytic activity in the pistachio green stink bug, Brachynema germari Kolenati (Hemiptera: Pentatomidae). J. Asia Pac. Entomol. 13, 221e227. Borzoui, E., Naseri, B., Namin, F.R., 2015. Different diets affecting biology and digestive physiology of the Khapra beetle, Trogoderma granarium Everts (Coleoptera: Dermestidae). J. Stored Prod. Res. 62, 1e7. Borzoui, E., Naseri, B., 2016. Wheat cultivars affecting life history and digestive amylolytic activity of Sitotroga cerealella Olivier (Lepidoptera: Gelechiidae). Bull. Entomol. Res. 106, 464e473. Bradford, M.M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteinedye binding. Anal. Biochem. 72, 248e254. Burges, H.D., 2008. Development of the Khapra beetle, Trogoderma granarium, in the lower part of its temperature range. J. Stored Prod. Res. 44, 32e35. Casaretto, J.A., Zuniga, G.E., Corcuera, L.J., 2004. Abscisic acid and jasmonic acid affect proteinase inhibitor activities in barley leaves. J. Plant Physiol. 161, 389e396. Dastranj, M., Bandani, A.R., Mehrabadi, M., 2013. Age-specific digestion of Tenebrio molitor (Coleoptera: Tenebrionidae) and inhibition of proteolytic and amylolytic activity by plant proteinaceous seed extracts. J. Asia Pac. Entomol. 16, 309e315. Elpidina, E.N., Vinokurov, K.S., Gromenko, V.A., Rudenshaya, Y.A., Dunaevsky, Y.E., Zhuzhikov, D.P., 2001. Compartmentalization of proteinases and amylases in Nauphoeta cinerea midgut. Arch. Insect Biochem. Physiol. 48, 206e216. Finkelman, S., Navarro, S., Rindner, M., Dias, R., 2006. Effect of low pressure on the survival of Trogoderma granarium Everts, Lasioderma serricorne (F.) and Oryzaephilus surinamensis (L.) at 30ºC. J. Stored Prod. Res. 42, 23e30. Gatehouse, A.M., Norton, E., Davison, G.M., Babbe, S.M., Newell, C.A., Gatehouse, J.A., 1999. Digestive proteolytic activity in larvae of tomato moth, Lacanobia oleracea, effects of plant protease inhibitors in vitro and in vivo. J. Insect Physiol. 45, 545e558. Golizadeh, A., Abedi, Z., 2016. Comparative performance of the Khapra beetle, Trogoderma granarium Everts (Coleoptera: Dermestidae) on various wheat cultivars. J. Stored Prod. Res. 69, 159e165. Golizadeh, A., Abedi, Z., 2017. Feeding performance and life table parameters of Khapra beetle, Trogoderma granarium Everts (Coleoptera: Dermestidae) on various barley cultivars. Bull. Entomol. Res. 14, 1e10. Hagstrum, D.W., Subramanyam, B., 1996. Integrated Management of Insects in Stored Products. Marcel Dekker, Inc, New York. Han, Y., Song, L., An, Q., Pan, C., 2016. Removal of six pesticide residues in cowpea with alkaline electrolysed water. J. Sci. Food Agric. 97 (8), 2333e2338. Hansen, L.S., Skovgard, H., Hell, K., 2004. Life table study of Sitotroga cerealella (Lepidoptera: Gelechiidae), a strain from west Africa. J. Econ. Entomol. 97 (4), 1484e1490. Hosseininaveh, V., Bandani, A.R., Azmayeshfard, P., Hosseinkhani, S., Kazzazi, M., 2007. Digestive proteolytic and amylolytic activities in Trogoderma granarium Everts (Dermestidae: Coleoptera). J. Stored Prod. Res. 43, 515e522. Itoyama, K., Kawahira, Y., Murata, M., Tojo, S., 1999. Fluctuations of some characteristics in the common cutworm, Spodoptera litura (Lepidoptera: Noctuidae)
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reared under different diets. Appl. Entomol. Zool 34, 315e321. Jood, S., Kapoor, A.C., Singh, R., 1996. Chemical composition of cereal grains as affected by storage and insect infestation. J. Trop. Agric. 73, 161e164. Jood, S., Kapoor, A.C., 1993. Protein and uric acid contents of cereal grains as affected by insect infestation. Food Chem. 46, 143e146. Karasov, W.H., Martinez del Rio, C., Caviedes-Vidal, E., 2011. Ecological physiology of diet and digestive systems. Annu. Rev. Physiol. 73, 69e93. Karnavar, G.K., 1967. Studies on the biology of the Khapra beetle, Trogoderma granarium Everts under laboratory conditions, with emphasis on diapause. J. Morphol. Physiol. 14, 205e215. Kazzazi, M., Bandani, A.R., Hosseibkhani, S., 2005. Biochemical characterization of aamylase of Sunn pest Eurygaster integriceps. Entomol. Sci. 8, 371e377. Lee, K.P., 2007. The interactive effects of protein quality and macronutrient imbalance on nutrient balancing in an insect herbivore. J. Exp. Biol. 210, 3236e3244. Lindgren, D.L., Vincent, L.E., Krohne, M.E., 1955. The khapra beetle. Trogoderma granarium. Hilgardia 24, le36. Majd-Marani, S., Naseri, B., Nouri-Ganbalani, G., Borzoui, E., 2017. The effect of maize hybrid on biology and life table parameters of the Khapra beetle, Trogoderma granarium Everts (Coleoptera: Dermestidae). J. Econ. Entomol. 110 (4), 1916e1922. Majd-Marani, S., Naseri, B., Nouri-Ganbalani, G., Borzoui, E., 2018. Maize hybrids affected nutritional physiology of the Khapra beetle, Trogoderma granarium Everts (Coleoptera: Dermestidae). J. Stored Prod. Res. 77, 20e25. Mardani-Talaee, M., Zibaee, A., Abedi, Z., Golizadeh, A., 2017. Digestion and protein metabolism of Trogoderma granarium (Coleoptera: Dermestidae) fed on different barley varieties. J. Stored Prod. Res. 73, 37e41. Mohandass, S., Arthur, F.H., Zhu, K.Y., Throne, J.E., 2007. Biology and management of Plodia interpunctella (Lepidoptera: Pyralidae) in stored products. J. Stored Prod. Res. 43, 302e311. Naseri, B., Borzoui, E., 2016. Life cycle and digestive physiology of Trogoderma granarium (Coleoptera: Dermestidae) on various wheat cultivars. Ann. Entomol. Soc. Am. 109 (6), 831e838. Naseri, B., Fathipour, Y., Moharramipour, S., Hosseininaveh, V., 2009. Comparative
life history and fecundity of Helicoverpa armigera (Lepidoptera: Noctuidae) on different soybean varieties. Entomol. Sci. 12, 147e154. Nation, J.L., 2001. Insect Physiology and Biochemistry. CRC Press, Boca Raton, Fla, p. 485. Nawrot, J., Gawlak, M., Szafranek, J., Szafranek, B., Synak, E., Warchalewski, J.R., Piasecka-Kwiatkowska, D., Blaszczak, W., Jelinski, T., Fornal, J., 2010. The effect of wheat grain composition, cuticular lipids and kernel surface microstructure on feeding, egg-laying, and the development of the granary weevil, Sitophilus granarius (L.). J. Stored Prod. Res. 46, 133e141. Ofuya, T.I., Credlandt, P.F., 1995. Responses of three populations of the seed beetle, Callosobruchus maculatus (F.) (Coleoptera: Bruchidae), to seed resistance in selected varieties of cowpea, Vigna unguiculata (L.) Walp. J. Stored Prod. Res. 31, 17e27. Panda, N., Khush, G.S., 1995. Host Plant Resistance to Insect. CAB International, p. 431. Rao, N.S., Sharma, K., Samyal, A., Tomar, S.M.S., 2004. Wheat grain variability to infestation by Khapra beetle, Trogoderma granarium Everts. Ann. Plant Prot. Sci. 12, 288e291. Sayed, T.S., Hirad, F.Y., Abro, G.H., 2006. Resistance of different stored wheat varieties to Khapra beetle, Trogoderma granarium (Everest) and lesser grain borer, Rhizopertha dominica (Fabricus). Pak. J. Biol. Sci. 9, 1567e1571. Seifi, S., Naseri, B., Razmjou, J., 2015. Nutritional physiology of the Khapra beetle, Trogoderma granarium Everts (Coleoptera: Dermestidae) fed on various barley cultivars. J. Econ. Entomol. 109, 472e477. Throne, J.E., Baker, J.E., Messina, F.J., Kramer, K.J., Howard, J.A., 2000. Varietal resistance, pp. 165e192. In: Subramanyam, B., Hagstrum, D.W. (Eds.), Alternatives to Pesticides in Stored-Product IPM. Kluwer Academic, Boston, FL. Waldbauer, G.P., 1968. The consumption and utilization of food by insects. Adv. Insect Physiol. 5, 229e288. Weston, P.A., Rattlingourd, P.L., 2000. Progeny production by Tribolium castaneum (Coleoptera: Tenebrionidae) and Oryzaephilus surinamensis (Coleoptera: Silvanidae) in maize previously infested by Sitotroga cerealella (Lepidoptera: Gelichiidae). J. Econ. Entomol. 93, 533e536.
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Journal of Stored Products Research journal homepage: www.elsevier.com/locate/jspr
Feeding efficiency and digestive physiology of Trogoderma granarium Everts (Coleoptera: Dermestidae) on different rice cultivars Shervin Barzin, Bahram Naseri*, Seyed Ali Asghar Fathi, Jabraeil Razmjou, Pezhman Aeinehchi Department of Plant Protection, Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran
a r t i c l e i n f o
a b s t r a c t
Article history: Received 28 June 2019 Received in revised form 9 September 2019 Accepted 10 September 2019 Available online xxx
The Khapra beetle, Trogoderma granarium Everts (Coleoptera: Dermestidae), is one of the economic pests infesting many stored cereals in the world. The effects of six commercial rice, Oryza sativa L. cultivars including Hashemi, Shiroodi, Gilane, Khazar, Ali Kazemi and Domsiah were evaluated on nutritional indices and digestive enzymatic activity of fifth instar T. granarium at controlled conditions (33±1 C, relative humidity of 65 ± 5%, and a photoperiod of 14:10 (L:D) h). Fifth instar larvae consumed more food when reared on Gilane, and less food when reared on Khazar and Ali Kazemi. The larvae fed with Khazar had the lowest weight gain, efficiency of conversion of ingested food and growth index. The relative growth rate was the highest when larvae were fed with Gilane and lowest when they were fed with Khazar. The highest midgut proteolytic and amylolytic activities of larvae were on Gilane. However, the lowest proteolytic activity was on Khazar and the lowest amylolytic activity was on Khazar and Ali Khazemi. According to the obtained results, Khazar is an unsuitable cultivar for feeding and growth of T. granarium. © 2019 Elsevier Ltd. All rights reserved.
Keywords: Nutritional performance Plant resistance Rice cultivar Trogoderma granarium
1. Introduction The Khapra beetle, Trogoderma granarium Everts (Coleoptera: Dermestidae), is one of the main pests of stored cereals such as wheat, rice, barley, maize and sorghum in the world (Lindgren et al., 1955; Burges, 2008; Majd-Marani et al., 2017). Although it has an extremely large variety of food preferences, but overall rice is not the preferred diet as compared to other cereals like wheat, barley and rye (Borzoui et al., 2015). The larval stage of this pest has the most feeding capacity on the seed embryo, but its adults are not able to feed (Jood et al., 1996). The feeding of larvae causes economic damage by decrease in nutritional quality of stored cereals especially depletion of protein and carbohydrate (Jood and Kapoor, 1993; Jood et al., 1996; Ahmedani et al., 2009). Subsequently, the market value of stored cereals contaminated by T. granarium larvae can be reduced (Jood and Kapoor, 1993; Weston and Rattlingourd, 2000; Hansen et al., 2004). Synthetic pesticides have been used as a first tool for management of stored-product insects such as T. granarium (Throne et al.,
* Corresponding author. E-mail address: [email protected] (B. Naseri). https://doi.org/10.1016/j.jspr.2019.101511 0022-474X/© 2019 Elsevier Ltd. All rights reserved.
2000; Finkelman et al., 2006; Mohandass et al., 2007), however, there are problems associated with using these compounds with respect to human health and non-target organisms (Hagstrum and Subramanyam, 1996; Han et al., 2016). Therefore, understanding of feeding efficiency and digestive enzymatic activity of T. granarium could be helpful in choosing pest management strategies (Kazzazi et al., 2005). Host plant cultivars that are resistant to insect pests can negatively change their growth, survival and reproductive potential (Ofuya and Credlandt, 1995; Naseri et al., 2009; Ashamo, 2010; Nawrot et al., 2010; Borzoui and Naseri, 2016). Thus, using resistant grains is a suitable method to minimize infestations by stored-grain pests (Panda and Khush, 1995). Plant-insect interactions and the resistance of diverse host plants to herbivorous insects can be evaluated by nutritional indices (Naseri and Borzoui, 2016). Nutritional indices of T. granarium on various wheat (Triticum aestivum L.) cultivars were evaluated by Aheer and Ahmad (1993), who reported that the cultivar 86299 was comparatively an unsuitable host for development of this pest. Resistance of wheat cultivars to T. granarium was studied by Rao et al. (2004), who noted that the size and seed hardness had a significant effect on resistance of wheat cultivars to this insect. Sayed et al. (2006) investigated the resistance of different wheat cultivars to T. granarium and revealed
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that Mehran-89 was the most resistant cultivar. Seifi et al. (2015) evaluated the nutritional indices and digestive physiology of T. granarium fed with various barley (Hordeum vulgare L.) cultivars and detected the highest amylolytic and proteolytic activities on cultivar Bahman. Majd-Marani et al. (2017) studied the effect of nine maize (Zea mays L.) hybrids on biology and life table parameters of T. granarium, and reported that BC 678 was a resistant hybrid for population increase of this insect. The effect of various maize hybrids on nutritional performance and digestive enzymatic activity of T. granarium was studied by Majd-Marani et al. (2018), who expressed that BC 678 was an unsuitable hybrid for feeding of fifth instar larvae. The influence of wheat cultivar on feeding performance of T. granarium was studied by Golizadeh and Abedi (2016), who noted that cultivar Kuhdasht was an unfavorable host. Furthermore, Golizadeh and Abedi (2017) considered the varietal resistance of barley against T. granarium and declared that the highest population growth was on cultivar Makuyi. Two major groups of digestive enzymes in the insects' midgut are proteases and amylases that hydrolyze protein and starch, respectively (Nation, 2001; Dastranj et al., 2013). The selective inhibition of these enzymes can be one of the most critical techniques of the insect's management (Bigham and Hosseininaveh, 2010). Borzoui et al. (2015) measured the digestive physiology of T. granarium larvae on different diets including rice (Oryza sativa L.) wheat, barley, rye (Secale cereale L.) and walnut (Juglans regia L.) and noted that both amylase and protease enzymes had the lowest activities when larvae were reared on the walnut. Mardani-Talaee et al. (2017) studied digestive enzymatic activity of T. granarium fed with various barley cultivars and reported high activities of amylase and protease in larvae fed with Line30. Despite the economic importance of T. granarium on stored cereals (Hosseininaveh et al., 2007) especially on rice, no published articles are available about the nutritional performance and digestive enzymatic activity of this pest on rice cultivars. In the present study, therefore, we evaluated the nutritional indices and digestive enzymatic activity of T. granarium larvae in response to feeding on six commercial rice cultivars. The results of this research would be useful to detect rice cultivar(s) unfavorable to T. granarium for developing pest management techniques. For example, resistant cultivar(s) could be stored at granary for longer periods with reduced economic losses by this insect. 2. Materials and methods 2.1. Origin of seeds and insects We used clean, de-husked white rice (Oryza sativa L.) for the experiments. Six rice cultivars including Hashemi, Gilane, Khazar, Shiroodi, Ali Kazemi and Domsiah were supplied by the Agricultural and Natural Resources Research Center of Guilan, Iran. Before beginning of the experiments, all rice seeds were ground for 30 s using an electric grinder. The colony of T. granarium larvae and adults was obtained from the Department of Plant Protection, University of Mohaghegh Ardabili, Iran. They were fed with wheat seeds and maintained at 33±1 C, relative humidity of 65 ± 5%, and a photoperiod of 14:10 (L:D) h, based on the method described by Karnavar (1967). 2.2. Nutritional indices Food consumption and weight gain of larvae were evaluated gravimetrically following Waldbauer (1968). Nutritional indices were investigated on dry-weight basis. Seven groups of 10 fifth instar larvae were weighed for each cultivar. Then, they were transferred into the Petri dishes (diameter 6 cm, depth 1 cm)
containing 1 g of the ground rice seeds for feeding of larvae. After two weeks, the final weight was measured to determine changes in the weight. To investigate total dry weight, twenty specimens of larvae other than those used in feeding tests were weighed, ovendried at 60 C for 48 h, and thereafter re-weighed. Nutritional indices of T. granarium were calculated by using formulae explained by Waldbauer (1968): Efficiency of conversion of ingested food (ECI) ¼ P/E; relative consumption rate (RCR) ¼ E/W0 T; and relative growth rate (RGR) ¼ P/W0 T; where, W0 ¼ initial dry weight of larvae, E ¼ dry weight of food consumed, P ¼ dry weight gain of larvae, T ¼ feeding period (day). 2.3. Growth index and pupal weight The survival rate of larvae, larval growth index (LGI) and pupal weight of T. granarium were estimated on various rice cultivars (Itoyama et al., 1999): LGI ¼ lx/L; where, lx ¼ survival rate of larvae, L ¼ larval period (day). 2.4. Preparation of midgut enzymes Enzyme specimens were prepared from the midguts of fifth instar larvae of T. granarium fed with different rice cultivars (Hosseininaveh et al., 2007). The number of 150 larvae for each cultivar were selected and dissected on ice and their midguts were gathered into a 1.5 mL of distilled water. Midguts were homogenized on ice using a pre-cooled homogenizer (Teflon pestle). The homogenates were centrifuged at 15,000g at 4 C for 15 min. The collected supernatants were transferred to new microtubes and kept at 20 C for enzymatic assays. 2.5. Amylase activity assay 3-5-Dinitrosalicylic acid (DNSA) procedure (Bernfeld, 1955), with a minor modification, was used to assay digestive amylolytic activity. A quantity of 130 ml of Tris-HCl (pH, 8), and 60 ml of 1% soluble starch (Sigma chemical Co., St Louis, USA, 99% purity) were incubated with 20 ml of the enzyme elicited from larval midgut at 37 C for 30 min. The reaction was stopped by the addition of 100 ml of DNSA and heated (85-95 C) for 10 min in boiling water. After cooling on ice for 5 min, the absorbance was read at 540 nm. One portion of amylase activity was defined as the quantity of enzyme required to produce 1 mg maltose (Sigma chemical Co., St Louis, USA) at 37 C for 30 min. A standard curve of absorbance versus quantity of maltose released was constructed to enable its computation the during amylase assay. All assays were carried out in triplicate with blanks containing no enzyme extract. 2.6. Protease activity assay The azocasein digestion procedure (Gatehouse et al., 1999; Elpidina et al., 2001) was used to determine total proteolytic activity of T. granarium fed with six rice cultivars. To assay the proteolytic activity, the reaction combination included 50 ml of azocasein (1.5%) solution in 50 mM glycine-NaOH buffer (pH 10) (Borzoui et al., 2015) and 50 ml of extracted enzyme from midgut. The mixture was incubated at 37 C for 50 min. Proteolysis was terminated by the addition of 100 ml of 30% trichloroacetic acid (TCA), after cooling at 4 C for 30 min, centrifuged at 15,000g for 10 min. One hundred microliters of supernatant was mixed with 100 ml of 2 M NaOH and the absorbance was read at 440 nm (using ELIZA-Reader, Anthos, 2020; England). Proper blanks were provided for each treatment which TCA had been added prior to the substrate. The increase in optical density per milligram protein per
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Table 1 Mean (±SE) nutritional indices of fifth instar Trogoderma granarium fed with different rice cultivars. Cultivar
E (mg/larva)
P (mg)
ECI (%)
RCR (mg/mg/day)
RGR (mg/mg/day)
Gilane Hashemi Domsiah Ali Kazemi Khazar Shiroodi
1.52 ± 0.04a 1.17 ± 0.04c 1.32 ± 0.02bc 0.99 ± 0.03d 0.99 ± 0.05d 1.46 ± 0.04 ab
0.46 ± 0.05a 0.32 ± 0.03 ab 0.32 ± 0.03 ab 0.24 ± 0.03bc 0.17 ± 0.03c 0.46 ± 0.03a
29.97 ± 2.83a 27.21 ± 1.91bc 24.11 ± 1.74bc 23.54 ± 2.93bc 17.37 ± 3.03c 31.56 ± 1.79a
0.065 ± 0.001a 0.049 ± 0.001c 0.056 ± 0.001bc 0.041 ± 0.000d 0.040 ± 0.001d 0.061 ± 0.002 ab
0.019 ± 0.002a 0.013 ± 0.001bc 0.013 ± 0.001bc 0.009 ± 0.001cd 0.007 ± 0.001d 0.019 ± 0.001 ab
Means followed by different letters in the same column are significantly different (Tukey, P < 0.05). E ¼ Food consumption, P ¼ Weight gain, ECI ¼ Efficiency of conversion of ingested food, RCR ¼ Relative consumption rate, RGR ¼ Relative growth rate.
minute was represented by one unit of protease activity. All the tests were done in triplicate. 2.7. Grain characteristics Starch content of tested cultivars was determined according to the method of Bernfeld (1955) using starch as a standard. A quantity of 200 mg of each powdered cultivar was homogenized in 35 ml of distilled water and heated to boiling. One-hundred microliters of each specimen were added in 2.5 ml of iodine reagent (0.02% I2 and 0.2% KI), and thereafter absorbance was read at 580 nm. Protein content of examined cultivars was assayed based on the method of Bradford (1976) applying bovine serum albumin as a standard. Based on standard particle size index [%] method (AACC 55e30, 2000), grain hardness was quantified. Primarily, rice cultivars were powdered for 1 min, and then sieved for 1 min. The weight of powdered seeds that passed from the sieve to the total seed weight was considered as a seed hardness index. To evaluate moisture content of each tested cultivar, 2 g of each powdered cultivar was weighed and placed in an oven set at 100 C for 3 h, then reweighed. 2.8. Statistical analysis Examination of all data for normality was done using Kolmogorov-Smirnov test before the analysis. Nutritional indices, growth index, pupal weight and enzymatic activity of T. granarium were examined according to a completely randomized design, via one-way analysis of variance (ANOVA). Statistical differences among the means were ascertained via the Tukey test at a ¼ 0.05. The correlation of some physicochemical characteristics of tested rice cultivars (amount of protein and starch, moisture content and seed hardness) with nutritional indices and digestive enzymatic activity of T. granarium was investigated by Pearson correlation coefficient using SPSS 16.0. 3. Results 3.1. Nutritional indices The nutritional indices of fifth instar larvae of T. granarium fed with different rice cultivars are presented in Table 1. The highest food consumption (F ¼ 6.951, df ¼ 5, 41, P < 0.05) was observed when larvae were fed with cultivar Gilane and the lowest value was seen when they were fed with cultivars Khazar and Ali Kazemi. The highest larval weight gain (F ¼ 11.601, df ¼ 5, 41, P < 0.05) was on cultivars Gilane and Shiroodi and the lowest weight gain was on cultivar Khazar. Moreover, the larvae fed with cultivar Khazar exhibited the lowest ECI value (F ¼ 163.282, df ¼ 5, 41, P < 0.05) compared with the other cultivars. The RCR value (F ¼ 32.221, df ¼ 5, 41, P < 0.05) was the highest on cultivar Gilane and the lowest on cultivars Khazar and Ali Kazemi. The highest and lowest
Table 2 Survival rate of larvae, and mean (±SE) larval growth index (LGI) and pupal weight of Trogoderma granarium fed with different rice cultivars. Cultivar
Survival rate (%)
LGI
Pupal weight (mg)
Gilane Hashemi Domsiah Ali Kazemi Khazar Shiroodi
98 89 94 92 88 98
2.72 ± 0.04a 2.26 ± 0.02c 2.55 ± 0.04b 2.47 ± 0.03b 2.16 ± 0.02c 2.71 ± 0.04a
3.31 ± 0.10a 3.30 ± 0.04a 3.24 ± 0.02a 3.45 ± 0.13a 3.48 ± 0.11a 3.42 ± 0.13a
Means followed by different letters in the same column are significantly different (Tukey, P < 0.05).
RGR values (F ¼ 12.712, df ¼ 5, 41, P < 0.05) were on cultivars Gilane and Khazar, respectively.
3.2. Growth index and pupal weight Data of survival rate, growth index and pupal weight of T. granarium fed with various rice cultivars are shown in Table 2. The survival rate of larvae ranged from 98% on cultivars Gilane and Shiroodi to 88% on Khazar. Larval growth index (F ¼ 42.15; df ¼ 5, 41; P < 0.05) was the highest on cultivars Gilane and Shiroodi, and lowest on cultivars Hashemi and Khazar. No significant difference was observed for pupal weight (F ¼ 0.94; df ¼ 5, 41; P ¼ 0.47) of T. granarium on tested cultivars.
3.3. Enzymatic activity of larvae Amylolytic (F ¼ 33.211, df ¼ 5, 17, P < 0.05) and total proteolytic (F ¼ 13.849, df ¼ 5, 17, P < 0.05) activity of fifth instar larvae of T. granarium fed with tested rice cultivars is shown in Table 3. The highest amylolytic activity was observed when larvae were fed with cultivar Gilane, whereas the lowest activity was seen when they were fed with cultivars Khazar and Ali Kazemi. The larvae reared on cultivar Gilane showed the highest protease activity, whereas the lowest activity was observed on cultivar Khazar.
Table 3 Mean (±SE) amylolytic and proteolytic activities of midgut extracts from fifth instar larvae of Trogoderma granarium fed with different rice cultivars. Cultivar
Amylolytic activity (mU/mg)
Proteolytic activity (U/mg)
Gilane Hashemi Domsiah Ali Kazemi Khazar Shiroodi
0.644 ± 0.008a 0.539 ± 0.020b 0.560 ± 0.003 ab 0.408 ± 0.044c 0.339 ± 0.009c 0.613 ± 0.001 ab
0.128 ± 0.020a 0.060 ± 0.002bc 0.068 ± 0.003bc 0.051 ± 0.002bc 0.034 ± 0.003c 0.081 ± 0.004b
The means followed by different letters in the same column are significantly different (Tukey P < 0.05).
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Table 4 Mean (±SE) some biochemical and physical characteristics in seeds of tested rice cultivars. Cultivar
Starch content (mg/g)
Protein content (mg/g)
Hardness index (%)
Moisture content (%)
Gilane Hashemi Domsiah Ali Kazemi Khazar Shiroodi
0.25 ± 0.01a 0.08 ± 0.01b 0.11 ± 0.01 ab 0.07 ± 0.01b 0.04 ± 0.01c 0.19 ± 0.09 ab
1.89 ± 0.04a 1.50 ± 0.02bc 1.84 ± 0.03 ab 1.91 ± 0.03a 1.87 ± 0.02a 1.14 ± 0.18c
51.56 ± 0.43a 42.60 ± 0.72c 46.44 ± 0.38b 32.28 ± 0.35d 31.32 ± 0.52d 48.56 ± 0.41b
12.08 ± 0.79a 6.58 ± 0.34cd 7.30 ± 0.55c 4.79 ± 0.09de 4.42 ± 0.31e 10.12 ± 0.43b
The means followed by different letters in the same column are significantly different (Tukey, P < 0.05).
3.4. Grain characteristics Table 4 shows some biochemical and physical characteristics of tested rice cultivars. The highest soluble starch content (F ¼ 679.203; df ¼ 5, 17; P < 0.05) was in cultivar Gilane, while the lowest content was in cultivar Khazar. Among tested cultivars, cultivar Shiroodi showed the lowest amount of protein (F ¼ 15.749; df ¼ 5, 17; P < 0.05). Higher particle size index (F ¼ 306.369; df ¼ 5, 29; P < 0.05) for cultivar Gilane displayed that this cultivar is softer than the others. Also, lower particle size index for cultivars Khazar and Ali Kazmi exhibited that they are harder than the others. The highest and lowest percentage moisture content was seen in cultivars Gilane and Khazar, respectively (F ¼ 40.360; df ¼ 5, 17; P < 0.05). 3.5. Correlation analysis The analysis of correlation coefficients of the nutritional indices and digestive enzymatic activity of T. granarium with some physicochemical traits of tested cultivars are indicated in Table 5. The results of this study demonstrated that positive correlations were seen among food consumption (r ¼ 0.76), RGR (r ¼ 0.53), RCR (r ¼ 0.79), and proteolytic (r ¼ 0.70) and amylolytic (r ¼ 0.79) activities with particle size index. Also, food consumption (r ¼ 0.38), RCR (r ¼ 0.57), and proteolytic (r ¼ 0.91) and amylolytic (r ¼ 0.85) activities showed positive correlations with moisture content of tested seeds. There was no significant correlation among tested characteristics of T. granarium with protein content. 4. Discussion The nutritional performance of the insects is dependent upon quality and quantity of consumed diets and physico-chemical characteristic of host plants (Behmer, 2009; Karasov et al., 2011). Feeding on a low quality diet by herbivorous insects could result in delayed growth, reduced survival and fecundity (Lee, 2007; Borzoui
Table 5 Pearson correlation coefficients (r) of some physiological characteristics of Trogoderma granarium fed with different rice cultivars with protein content, starch content, particle size index and moisture content of tested rice cultivars. Parameter
E RGR RCR ECI PA AA
Protein content
Starch content
Particle size index
Moisture content
r
p
r
p
r
p
r
p
0.21 0.06 0.39 0.08 0.07 0.40
0.406 0.827 0.11 0.746 0.796 0.098
0.41 0.33 0.58 0.14 0.70* 0.66
0.089 0.182 0.013 0.571 0.001 0.300
0.76* 0.53* 0.79* 0.16 0.70* 0.79*
0.000 0.002 0.000 0.412 0.001 0.000
0.38** 0.42 0.57 0.24 0.91* 0.85*
0.020 0.081 0.014 0.328 0.000 0.000
E ¼ Food consumption, RGR ¼ Relative growth rate, RCR ¼ Relative consumption rate, ECI ¼ Efficiency of conversion of ingested food, PA¼ Proteolytic activity, AA ¼ Amylolytic activity. *p < 0.01; **p < 0.05.
and Naseri, 2016). The results of this study showed that the food quality, particularly seed hardness of tested rice cultivars, influenced the nutritional indices and digestive enzymes activity of T. granarium larvae. In this study, there were six larval instars on all the tested rice cultivars. However, fifth instar larvae were used in the experiments, because they had higher feeding potential and weight gain than the sixth instar larvae (personal observations). The number of larval instars in T. granarium differed from 6 instar on wheat to 10 instar on rice and walnut. Moreover, the developmental time of larvae on rice (77.25 days) was longer than that obtained on wheat, barley and rye (Borzoui et al., 2015). Therefore, it would be concluded that rice is relatively unsuitable host commodity for feeding and development of T. granarium as compared to the other cereals. This study demonstrated that T. granarium larvae consumed less seeds when reared on cultivars Khazar and Ali Kazemi, leading to the lowest weight gain and digestive enzymatic activity. Furthermore, a significant correlation between food consumption and particle size index (r ¼ 0.75) indicated that the seed hardness was a main factor responsible for the amount of food eaten and weight gain of larvae. Since the seeds of cultivars Khazar and Ali Kazemi are harder than other cultivars, larvae are not able to feed more seeds when reared on these cultivars. Although cultivar Ali Kazemi has a high amount of protein, lower food consumption and weight gain of larvae on this cultivar could be related to seed hardness of it. The amount of food consumption on cultivar Khazar in this study is higher than that reported for T. granarium fed with wheat cultivars (Golizadeh and Abedi, 2016) and maize hybrids (Majd-Marani et al., 2018). It could be suggested that rice cultivars tested in our study are more suitable diet than the cereals (wheat and maize) examined by above-mentioned authors for feeding of larvae. However, the range of food consumption on various rice cultivars is lower than that noted by Seifi et al. (2015) on barley cultivars. Higher weight gain of larvae in T. granarium fed with seeds of cultivar Gilane can be due to the high protein and starch contents and soft seeds of this cultivar (Table 4). The range of larval weight gain in our study is higher than that reported for T. granarium fed with various wheat cultivars (Golizadeh and Abedi, 2016). Differences in larval instar and host grain used by Golizadeh and Abedi (2016) with those tested in our study could explain this inconsistency. The larvae of T. granarium fed with cultivar Khazar indicated the lowest value of ECI, suggesting a less potential of larvae to convert the eaten diet to body mass. Decrease in the weight gain of larvae on cultivar Khazar can explain lower ECI value obtained on this cultivar. Moreover, higher value of ECI on cultivars Gilane and Shiroodi might be attributed to higher weight gain of larvae fed with these two cultivars. In this research, the highest ECI value is approximately similar to that reported for T. granarium on maize hybrid 704 (Majd-Marani et al., 2018) and wheat cultivar Saysonz (Golizadeh and Abedi, 2016). However, the range of ECI values of T. granarium in our study is higher than that expressed on barley cultivars (Seifi et al., 2015; Golizadeh and Abedi, 2017). It would be suggested that the suitability and nutritional value of rice cultivars
S. Barzin et al. / Journal of Stored Products Research 84 (2019) 101511
tested in our study is more than barley cultivars used by abovementioned authors for feeding of larvae. The highest values of RGR and RCR in fifth instar larvae fed with cultivar Gilane are due to softer grain and higher amount of starch and moisture in this cultivar. Furthermore, T. granarium fed with cultivar Gilane spent a shorter time to complete larval and pupal stages than that fed with the others (personal observations). Despite the high nutritional quality of cultivar Khazar in terms of protein content, it is a hard grain with low content of starch and moisture. Thus, the growth rate of larvae was the lowest when fed with this cultivar. The range of RGR value on rice cultivars tested in this study is lower than that reported for T. granarium on maize hybrids (Majd-Marani et al., 2018), wheat (Golizadeh and Abedi, 2016), and barley (Seifi et al., 2015) cultivars. The larval growth index (LGI) is one of the important indicators determining the suitability of a host plant to insects, because both survival and duration of larval stages affect this index. As survival rate of larvae was the lowest on cultivar Khazar, the LGI was obtained lowest when larvae were fed with this cultivar, suggesting its unsuitability as a host for growth of T. granarium. The range of LGI in this study is higher than that reported by Seifi et al. (2015) for T. granarium on different barley cultivars. The results of this study showed no significant difference in pupal weight of T. granarium fed with tested cultivars. One of the possible reasons of this result is the high mortality of larvae fed with cultivar Khazar (as an unsuitable cultivar). On the other hands, fewer larvae are pupated while feeding on the resistant cultivar than those fed with the other cultivars. Quality and quantity of food eaten by T. granarium can influence the digestive physiology of larvae (Bernardi et al., 2012; Borzoui et al., 2015; Naseri and Borzoui, 2016). Results from digestive enzymatic assay indicated that larvae fed with cultivar Gilane had the highest enzymatic activity, whereas cultivar Khazar-fed larvae showed the lowest activity. As seen in Table 4, the protein content between cultivars Gilane and Khazar was not significantly different. Therefore, different levels of digestive enzymatic activity of larvae fed with these two cultivars might be attributed to starch content, seed hardness and moisture content of tested cultivars. Based on the correlation analysis, there was a positive and significant relationship between protease and amylase activity with both hardness index and seed moisture content. The role of seed hardness on the levels of digestive enzyme activity in T. granarium is reported by Majd-Marani et al. (2017). In another study, Naseri and Borzoui (2016) proved that amylolytic activity of Sitotroga cerealella (Olivieri) larvae fed with harder wheat grain was lower than those reared on softer grain. Moreover, Mardani-Talaee et al. (2017) reported that amylolytic and proteolytic activities in T. granarium larvae were the lowest when they were fed with barley varieties with hard grains. In our study, the proteolytic activity of T. granarium on different rice cultivars is lower than that reported for T. granarium fed with various barley cultivars (Seifi et al., 2015). This variation could be due to different host species and larval instar tested by Seifi et al. (2015). Furthermore, it is reported that some anti-nutritional substances such as plant enzyme inhibitors occur in barley seeds, which strongly regulate digestive physiology of insects (Casaretto et al., 2004; Borzoui et al., 2015). The amylolytic activity of larvae on cultivar Khazar is nearly close to the activity reported by Seifi et al. (2015) on barley cultivar Bahman (as a resistant cultivar). The results of this study showed that T. granarium larvae fed with cultivar Khazar (as a hard grain with low starch and moisture content) had the lowest feeding efficiency and midgut enzymatic activity. Thus, Khazar was the least suitable (most resistant) cultivar for feeding and growth of this insect. This cultivar can be stored for longer periods of time at storage conditions with reduced
5
management cost of T. granarium. Moreover, it can be suggested to incorporate into the breeding programs to minimize seed losses by this pest. However, susceptible rice cultivars such as Gilane and Shiroodi will require more protection approaches to prevent infestation by T. granarium. To obtain more practical knowledge to control T. granarium, recognition and purification of secondary chemical compounds (such as digestive enzymes inhibitors) of the resistant cultivar would be required. Acknowledgment We thankfully acknowledge the University of Mohaghegh Ardabili, Ardabil, Iran, for collaboration by support for the experiment. References AACC 55e30, 2000. Approved Methods of the American Association of Cereal Chemists, tenth ed. The American Association of Cereal Chemists, St Paul, MN. Aheer, G.M., Ahmad, R., 1993. Response of wheat to Trogoderma granarium (Everts.) and Rhizopertha dominica (F.B.). J. Agric. Res. 31, 319e322. 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