Effect of three insect growth regulators on certain biological aspects of the lesser grain borer, Rhyzopertha dominica (Coleoptera: Bostrichidae)

Efeito de três reguladores de crescimento de insetos em certos aspectos biológicos da broca-do-grão, Rhyzopertha dominica (Coleoptera: Bostrichidae)

Abstract

The current study was performed to evaluate the efficacy of certain insect growth regulators (IGRs), buprofezin, hexaflumuron, and lufenuron, at different concentrations (0.2, 0.4, and 0.8 ppm) against Rhyzopertha dominica in wheat grains. Our data showed that the three IGRs tested at different concentrations significantly affected the mortality of adults to varying extents. The percentage mortality of adults increased with increasing concentrations and time of exposure. After 21 days of treatment, the highest mortality (80.00%, 78.33%, and 60.00%) was observed at the highest concentration (0.8 ppm) and the lowest mortality (58.33%, 46.66%, and 30.00%) was observed at the lowest concentration (0.2 ppm) of lufenuron, buprofezin, and hexaflumuron, respectively. The tested IGRs reduced fecundity, hatchability, adult emergence, and weight loss in treated wheat grains and increased the developmental period of R. dominica compared with the control.

Keywords:
lesser grain borer; IGR; mortality; fecundity; adult emergence; weight loss

Resumo

O presente estudo foi realizado para avaliar a eficácia de certos Reguladores de Crescimento de Insetos (RCIs), buprofezin, hexaflumuron e lufenuron, em diferentes concentrações (0,2, 0,4 e 0,8 ppm) contra Rhyzopertha dominica em grãos de trigo. Nossos dados mostraram que os três RCIs, testados em diferentes concentrações, afetaram significativamente a mortalidade de adultos em graus variados. A mortalidade percentual de adultos cresceu com o aumento das concentrações e do tempo de exposição. Após 21 dias de tratamento, a maior mortalidade (80,00%, 78,33% e 60,00%) foi observada na maior concentração (0,8 ppm) e a menor mortalidade (58,33%, 46,66% e 30,00%) foi observada na menor concentração (0,2 ppm) de lufenuron, buprofezin e hexaflumuron, respectivamente. Os RCIs testados reduziram a fecundidade, eclodibilidade, emergência de adultos e perda de peso em grãos de trigo tratados, bem como aumentaram o período de desenvolvimento de R. dominica em comparação com o controle.

Palavras-chave:
broca-do-grão; RCI; mortalidade; fecundidade; emergência de adultos; peso

1. Introduction

Wheat (Tritium aestivum L.) is considered the most important cereal crop because of its high production and consumption. It is the leading staple in human foods (Ileke, 2011). Wheat is attacked in the field and in storage by several pests that attack the stored grains and grain produce. Among them, the lesser grain borer, Rhyzopertha dominica (F.) (Coleoptera: Bostrichidae), is one of the major pests of cereals stored in many regions of the world (Edde, 2012). This pest is present both in the field at harvesting time and in granaries (Naseem and Khan, 2011). It is one of the most important pests of stored wheat, and it also attacks other crops (e.g., barley, beans, chickpeas, millet, malt, oats, sorghum, rice, peanuts, and pearl) (Perisic et al., 2018; Chandel et al., 2019). The beetle is especially prevalent in tropical and subtropical regions (Obretenchev et al., 2020). Adults and larvae cause major qualitative and quantitative losses to several crops (Banga et al., 2018). The total grain damage this insect causes annually around the world is estimated to be 10% to 40% (Matthews, 1993). The presence of this pest in stored grain reduces not only the quantity but also the quality of the grains and reduces their nutritional value as well as the market value, making them unfit for human consumption (Astuti et al., 2013).

Chemical pesticides carry health risks and can cause environmental pollution (Grewal et al., 2017) because of their toxicity to humans and wildlife (Paoletti and Pimentel, 2000). The presence of insecticide residues in food (Phillips and Throne, 2010) and the development of insecticide resistance (Boyer et al., 2012) are of major concern around the world. To overcome these problems, safe alternative approaches are required for the management of insect pests of stored products. Insect growth regulators (IGRs) are receiving more attention because of their efficacy against insects in stored grain. In addition, they are environmentally safe, biodegradable, and nontoxic to humans and nontarget organisms (Ishaaya et al., 2007). These features of IGRs increase acceptance of products treated with IGRs by the food industry (Phillips and Throne, 2010). IGRs are effective in suppressing the development of insects for the entire life cycle (Gelbic et al., 2011). IGRs aim to affect mating efficiency and reduce egg production in emerging adults (Segura et al., 2009). Chitin synthesis inhibitors (CSIs), a group of IGRs, are very effective against several pests of stored grain by treating either the commodities that contain eggs or the adults (Mishra et al., 2013; Trostanetsky et al., 2015; Ali et al., 2016). CSIs have been widely used to impair the reproduction and development of insects (Arthur and Hartzer, 2018). CSIs interfere with chitin synthesis in insects and thus prevent molting or cause production of an imperfect cuticle (Abdel Rahman et al., 2007). Buprofezin, hexaflumuron, and lufenuron are some CSIs that affect oviposition, egg hatchability, adult emergence, and development of stored grain insect pests (Sohrabi et al., 2011; Kavallieratos et al., 2012; Ali et al., 2016, 2018, 2019; Fiaz et al., 2018; Yasir et al., 2019). IGRs are considered ecofriendly in the control of insect pests.

This study aimed to evaluate the effects of buprofezin, hexaflumuron, and lufenuron on mortality in adult R. dominica; determine the effects of these IGRs on the fecundity, hatchability, progeny, and developmental period of R. dominica; and determine the effects of these IGRs on weight loss in wheat grains.

2. Materials and methods

2.1. Rearing of insects

Adults of R. dominica were collected from the naturally infested wheat grains from the local market in Assiut Governorate, Egypt. In each glass jar of 1 liter capacity, fifty pairs of adult R. dominica were released into 500 g of disinfected wheat grains. The mouths of the jars were covered with muslin cloth fastened with rubber bands to ensure ventilation while preventing the escape of the insects, and the jars were incubated at 30°C ± 2°C and 70% ± 5% relative humidity. The beetles were left in the culture for about 10 days for egg-laying. Newly emerged adults (0 to 24 hours old) were placed in glass jars containing sterilized grain for oviposition in order to maintain a stock culture for a continuous fresh supply of the insects.

Male and female adults were identified according to the description of Hagstrum and Subramanyam (2006). The last exposed abdominal tergum was usually uniformly brown in males and pale yellow in females.

2.2. IGRs

Three locally available IGRs (buprofezin [Applaud 25% SC] from Nihon Nohyaku Company Japan, hexaflumuron [Dimeuron 10% EC] from the national company for Agrochemicals Productions Egypt, and lufenuron [Match, 5% EC] from Syngenta Agro Company Switzerland) were used at concentrations of 0.0, 0.2, 0.4, and 0.8 ppm.

2.3. Experimental design

To determine the effects of buprofezin, hexaflumuron, and lufenuron on R. dominica, 30 g of sterilized wheat grains were placed in glass jars of 200 ml capacity and sprayed by hand sprayer with 1 ml each of buprofezin, hexaflumuron, and lufenuron at concentrations of 0.2, 0.4, and 0.8 ppm prepared in distilled water. Distilled water was used as the control. The sprayed grain was then left to air-dry. Ten pairs of 1- to 2-day-old adult R. dominica were then placed in each jar. The jars were covered with muslin cloth to prevent the insects from escaping and maintained at 30°C ± 2°C and 70% ± 5% relative humidity. Three replicates were used for each treatment. Mortality of adults was recorded after 7, 14, and 21 days of treatment application. Corrected mortality (PT) was calculated by Abbotts’s (Abbott, 1925) using the Formula 1

$PT=(Po-Pc/100-Pc)\times 100$ (1)

where Po = Observed mortality, Pc = Control mortality.

The numbers of eggs laid and hatched were recorded after 10 days of treatment. The number of days taken by the insects to complete their life cycle from the egg to the adult stage was calculated according to Howe (1971).

After 50 days of treatment, we counted and recorded the number of F1 adults emerged and determined the weight loss of the wheat grains. The percent inhibition rate (% IR) in fecundity, eggs hatched, and adults emerged were calculated according to Silassie and Getu (2009) using the Formula 2

$$\%IR=Cn–Tn/Cn\times 100$$ (2)

where Cn is the number of eggs laid, eggs hatched, and newly emerged insects in the control group, and Tn is the number of eggs laid, eggs hatched, and newly emerged insects in the treatment group.

Percent weight loss (PWL) was calculated according to Odeyemi and Daramola (2000) as (Equation 3)

$$PWL=IW–FW/IW\times 100$$ (3)

where IW is the initial weight and FW is the final weight.

2.4. Statistical analysis

The data were analyzed by two-way analysis of variance using the Statistical Analysis System at a significance level of 5%. The mean differences were separated using the least significant difference and shown as means ± SE.

3. Results

3.1. Effect of IGRs on adult mortality

The results in Table 1 show the effects of different concentrations of IGRs on mortality in adult R. dominica after 7, 14, and 21 days of treatment. The mean percentages of adult mortality after 7, 14, and 21 days of treatment at 0.2 ppm concentration were 26.66%, 40.00%, and 46.66% for buprofezin, 16.66%, 21.66%, and 30.00% for hexaflumuron, and 35.00%, 53.33%, and 58.33% for lufenuron, respectively. Increasing the IGR concentration to 0.8 ppm increased the percentage of adult mortality after 7, 14, and 21 days of treatment to 40.00%, 61.66%, and 78.33% for buprofezin, 41.66%, 46.66%, and 60.00% for hexaflumuron, and 53.33%, 73.33%, and 80.00% for lufenuron, respectively. In general, the percentage of adult mortality increased vertically with increased concentration of IGRs and horizontally with increased time of exposure to IGRs. The highest percentage of adult mortality was 80.00% for lufenuron at 0.8 ppm after 21 days of treatment. The lowest percentage of adult mortality was 16.66% for hexaflumuron at 0.2 ppm after 7 days of treatment. In general, the results showed that lufenuron was the most effective IGR against R. dominica, followed by hexaflumuron and then buprofezin.

Table 1
Mortality of Rhyzopertha dominica adults exposed for 7, 14, and 21 days to wheat grains treated with different concentrations of insect growth regulators (IGRs).

IGR	Concentration (ppm)	Mean ± SE mortality (%)
		7 days	14 days	21 days
Buprofezin	0.2	26.66 ± 1.66e	40.00 ± 2.89e	46.66 ± 3.33d
	0.4	31.66 ± 3.33de	48.33 ± 1.66cde	70.00 ± 5.78ab
	0.8	40.00 ± 0.00bc	61.66 ± 3.33ab	78.33 ± 1.66a
Hexaflumuron	0.2	16.66 ± 1.66f	21.66 ± 4.41f	30.00 ± 2.89e
	0.4	28.33 ± 1.66de	36.66 ± 6.67e	51.66 ± 3.33cd
	0.8	41.66 ± 4.41bc	46.66 ± 3.33de	60.00 ± 2.89bc
Lufenuron	0.2	35.00 ± 2.89cd	53.33 ± 4.41bcd	58.33 ± 3.33c
	0.4	43.33 ± 1.66b	60.00 ± 2.89bc	71.66 ± 2.89a
	0.8	53.33 ± 3.33a	73.33 ± 4.4a	80.00 ± 5.00a
F-value		17.2	14.6	19.5

• Values within a column sharing the same superscript letter are not significantly different at P < 0.05 (df = 8).

3.2. Effect of IGRs on oviposition

Table 2 shows the mean number of R. dominica eggs laid on wheat grains treated with different concentrations of IGRs, compared with control. The number of eggs laid on untreated grains was 163.33 eggs / female. The number of eggs laid on grains treated with buprofezin at 0.2 ppm concentration was 72.00 eggs / female, decreasing with increasing concentration of buprofezin to 16.33 eggs / female at 0.8 ppm. The number of eggs laid on grains treated with hexaflumuron at 0.2 ppm concentration was 100.33 eggs / female, decreasing with increasing concentration of hexaflumuron to 58.66 eggs / female at 0.8 ppm. The number of eggs laid on grains treated with lufenuron at 0.2 ppm concentration was 83.00 eggs / female, decreasing with increasing concentration of lufenuron to 21.66 eggs / female at 0.8 ppm. The highest percentage reduction of the number of eggs laid (90.08%) was recorded for buprofezin at a concentration 0.8 ppm, while the lowest percentage reduction of the number of eggs laid (38.53%) was recorded for hexaflumuron at a concentration of 0.2 ppm.

Table 2
Oviposition of Rhyzopertha dominica on wheat grains treated with different concentrations of insect growth regulators (IGRs).

IGR	Concentration (ppm)	Mean ± SE
		No. of eggs/female	% reduction
Control	0.0	163.33 ± 3.18a	-
Buprofezin	0.2	72.00 ± 3.46c	55.96 ± 1.26
	0.4	57.66 ± 4.63de	64.77 ± 2.14
	0.8	16.33 ± 4.26f	90.08 ± 2.45
Hexaflumuron	0.2	100.33 ± 1.45b	38.53 ± 1.19
	0.4	82.00 ± 3.60c	49.69 ± 3.01
	0.8	58.66 ± 1.85d	64.04 ± 1.42
Lufenuron	0.2	83.00 ± 3.00c	49.13 ± 2.10
	0.4	47.33 ± 2.02e	70.94 ± 1.80
	0.8	21.66 ± 6.96f	86.88 ± 3.02

• Values within a column sharing the same letter are not significantly different at P < 0.05 (F = 125; df = 9).

3.3. Effect of IGRs on hatchability

The results in Table 3 show the mean number of hatched eggs of R. dominica on grain treated with different concentrations of IGRs, compared with control. The mean number of eggs hatched on untreated grains was 160.66. The lowest number of hatched eggs was recorded in grain treated with lufenuron at 0.8 ppm concentration (0.00 eggs); the number increased gradually with decreasing concentrations of lufenuron to 75.00 eggs at a concentration 0.2 ppm. For grain treated with hexaflumuron, 87.33 eggs were hatched at 0.2 ppm, and the number decreased gradually to 40.33 eggs at 0.8 ppm. The mean number of eggs hatched on grains treated with 0.2 ppm of buprofezin was 60.00, decreasing gradually with increased concentration of buprofezin concentration to 3.66 eggs at a concentration of 0.8 ppm. The highest percent reduction in hatchability (100%) was recorded with lufenuron at a concentration of 0.8 ppm, decreasing gradually with decreased concentration of lufenuron to 53.30% at a concentration 0.2 ppm; the lowest percent reduction in hatchability (45.59%) was recorded with hexaflumuron at a concentration of 0.2 ppm. In general, increasing concentration of the tested IGRs resulted in a decrease in the number of eggs hatching.

Table 3
Hatchability of Rhyzopertha dominica eggs on wheat grains treated with different concentrations of insect growth regulators (IGRs).

IGR	Concentration (ppm)	Mean ± SE
		No. of eggs hatched	% reduction
Control	0.0	160.66 ± 3.28a	-
Buprofezin	0.2	60.00 ± 1.52d	62.66 ± 0.19
	0.4	45.00 ± 2.31e	71.92 ± 1.85
	0.8	3.66 ± 3.67g	97.69 ± 2.30
Hexaflumuron	0.2	87.33 ± 3.93b	45.59 ± 2.71
	0.4	65.00 ± 2.00d	59.52 ± 1.33
	0.8	40.33 ± 2.02ef	74.85 ± 1.54
Lufenuron	0.2	75.00 ± 2.08c	53.30 ± 1.18
	0.4	34.66 ± 2.90f	78.33 ± 2.22
	0.8	0.00 ± 0.00g	100 ± 0.00

• Values within a column sharing the same superscript letter are not significantly different at P < 0.05 (F = 311; df = 9).

3.4. Effect of IGRs on adult emergence

The results in Table 4 show the mean number of adults of R. dominica emerging from wheat grain treated with different IGRs compared with untreated grain. The mean number of adults emerging from untreated wheat grain was 150.66. The mean numbers of adults emerging from wheat grain treated with IGRs at a concentration of 0.2 ppm were 63.33, 47.00, and 39.33 for wheat grain treated with hexaflumuron, buprofezin, and lufenuron, respectively. Adult emergence decreased significantly to 11.00, 1.33, and 0.00 for wheat grain treated with hexaflumuron, buprofezin, and lufenuron, respectively, with increase of the concentration of the three IGRs to 0.8 ppm. The highest percentage reduction of adult emergence (100%) was recorded for lufenuron at a concentration of 0.8 ppm. The lowest percentage reduction of adult emergence (57.97%) was recorded for hexaflumuron at a concentration of 0.2 ppm.

Table 4
Adult emergence of Rhyzopertha dominica from wheat grains treated with different concentrations of insect growth regulators (IGRs).

IGR	Concentration (ppm)	Mean ± SE
		No. of adults emerged	% reduction
Control	0.0	150.66 ± 1.20a	-
Buprofezin	0.2	47.00 ± 1.00c	68.65 ± 0.38
	0.4	22.00 ± 3.21e	85.36 ± 2.21
	0.8	1.33 ± 1.33g	99.11 ± 0.89
Hexaflumuron	0.2	63.33 ± 1.85b	57.97 ± 0.92
	0.4	43.66 ± 2.60cd	71.03 ± 1.51
	0.8	11.00 ± 1.15f	92.49 ± 0.
Lufenuron	0.2	39.33 ± 2.60d	73.86 ± 1.92
	0.4	16.00 ± 2.89f	89.38 ± 1.91
	0.8	0.00 ± 0.00g	100 ± 0.00

• Values within a column sharing the same superscript letter are not significantly different at P < 0.05 (F = 477; df = 9).

3.5. Effect of IGRs on developmental period

The mean developmental period of R. dominica on untreated grain was 27.33 days (Figure 1). The mean developmental period was longer on grains treated with IGRs. The mean developmental period was 29.66, 31.00, and 35.00 days for grains treated with hexaflumuron, buprofezin, and lufenuron, respectively, at 0.2 ppm concentration. The developmental period increased significantly to 34.66, 36.33, and 44.66 days, respectively, with increase of the concentrations of hexaflumuron, buprofezin, and lufenuron to 0.8 ppm.

Figure 1
Mean developmental period of Rhyzopertha dominica on wheat grains treated with different concentrations of insect growth regulators (IGRs).

Statistical parameters: buprofezin (F = 27.3; P < 0.05; df = 3); hexaflumuron (F = 9.91; P < 0.05; df = 3); lufenuron (F = 46.6; P < 0.05; df = 3).

3.6. Effect of IGRs on weight loss

Figure 2 shows the mean loss in weight of wheat grain treated with IGRs at three concentrations, compared with untreated grain. The mean loss in weight of untreated grains was 13.36%. In grain treated with 0.2 ppm lufenuron, the loss in weight was 1.68%, decreasing to 0.00% in grain treated with 0.8 ppm lufenuron. Buprofezin at 0.2 ppm was second to lufenuron in its efficacy in reducing grain weight loss; the mean loss was 2.41%, decreasing gradually to 0.09% with increase of buprofezin concentration to 0.8 ppm. Hexaflumuron at 0.2 ppm was the least effective at reducing grain weight loss; the mean loss was 2.87%, decreasing gradually to 0.44% with hexaflumuron at a concentration of 0.8 ppm.

Figure 2
Mean percent weight loss in wheat treated with different concentrations of insect growth regulators (IGRs).

Statistical parameters: buprofezin (F = 2224; P < 0.05; df = 3); hexaflumuron (F = 1997; P < 0.05; df = 3); lufenuron (F = 2303; P < 0.05; df = 3).

4. Discussion

Our findings regarding the effects of IGRs against R. dominica showed that lufenuron had a strong effect, with 80% adult mortality after 21 days exposure to treated grain. Similar results regarding mortality in R. dominica exposed to IGR-treated grain were reported by Kavallieratos et al. (2012). Other studies have also reported an increase in mortality with increased exposure to IGR-treated diets (Sagheer et al., 2012; Yasir et al., 2012; Ali et al., 2016).

The results of this study showed the inhibitory effects of IGRs on fecundity and egg hatchability in R. dominica. The highest percent reductions in fecundity and egg hatchability were recorded for buprofezin and lufenuron at 0.8 ppm, respectively. Other studies also report the ovicidal activity of the CSIs triflumuron, flufenoxuron, and lufenuron against Tribolium castaneum (Parween et al., 2001; Salokhe et al., 2003). Similar results have been reported by Arthur (2004) against the adults of R. dominica by the application of smethoprene. Abo-Elghar et al. (2004) reported the ovicidal and developmental inhibition activity of CSIs against cowpea weevil. Hexaflumuron reduced the fecundity and affected the growth and development of oocytes and egg viability of Callosobruchus maculatus (Kellouche and Soltani, 2006). Egg production in R. dominica was significantly reduced by treatment with methoprene, which simultaneously affected egg hatchability (Chanbang et al., 2008). Our findings are also in line with the results of the studies on the effect of lufenuron against T. castaneum, which found significant reductions in fecundity and hatchability (Ali et al., 2019; Awais et al., 2019; Yasir et al., 2019).

Our results showed that lufenuron was the most effective compound against R. dominica among the three IGRs tested. At 0.8 ppm, it completely inhibited the F1 adult emergence of R. dominica. For example, exposure of adults of R. dominica to pyriproxyfen- and methoprene-treated grains resulted in reduction in F1 adult emergence (Kostyukovsky et al., 2000; Daglish and Wallbank, 2005). Mahanthi (2006), tested lufenuron as a stored-maize protectant and showed that it completely inhibited the adult emergence of Sitophilus oryzae and completely controlled Corcyra cephalonica. Arthur et al. (2009) reported inhibition of adult emergence of stored-product insect pests due to larval exposure to IGRs. Ali et al. (2016) reported reduced adult emergence when adults of T. castaneum, Tribolium confusum, and Ephestia cautella were exposed to methoprene-treated diets. Similar results of inhibition of adult emergence had been reported (Ioni et al., 2011; Kavallieratos et al., 2012; Ali et al., 2018; Fiaz et al., 2018) when stored grain insect pests were exposed to IGR-treated food media.

The effects of the tested IGRs on the developmental period were similar to the findings of Kostyukovsky et al. (2000), who found that methoprene, pyriproxyfen, RH-5849, and tebufenozide affected the development of susceptible and actellic-resistant strains of T. castaneum and susceptible strains of R. dominica and S. oryzae Our results agree with those of Trostanetsky and Kostyukovsky (2008), who also found that the development of progeny was affected when adults of T. castaneum were treated with CSIs. Our findings are also supported by the work of Arora et al. (2012), who reported the effects of sublethal concentrations of lufenuron against different developmental stages of T. castaneum. Lufenuron had very little effect against adults when it was fed in the diet. These results are supported by the findings of Kavallieratos et al. (2012), who investigated the efficacy of seven IGRs as grain protectants in wheat, rice, and maize against Prostephanus truncates and R. dominica.

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Publication Dates

• Publication in this collection
  13 Jan 2023
• Date of issue
  2022

History

• Received
  07 Sept 2022
• Accepted
  16 Oct 2022