Submit or Track your Manuscript LOG-IN

Sublethal Doses of Clove Oil Deplete the Energy Reserves and Downregulate the Carbohydrate Metabolizing Enzymes in the 4th Instar Larvae of Trogoderma granarium

PJZ_56_2_561-569

Sublethal Doses of Clove Oil Deplete the Energy Reserves and Downregulate the Carbohydrate Metabolizing Enzymes in the 4th Instar Larvae of Trogoderma granarium

Asma Ilyas1, Tanzeela Riaz 2*, Sammi Rasheed1, Uzma Ramzan1,

Afsheen Munawar Butt1 and Farah Rauf Shakoori1*

1Institute of Zoology, University of the Punjab, Quaid-i-Azam Campus, Lahore 54590, Pakistan

2Departmnet of Zoology, Faculty of Science and Technology, University of Central Punjab, Lahore, Pakistan

ABSTRACT

The main objective was to search for a new chemical insecticide to control the stored grain insect pest Trogoderma granarium particularly when this pest developed resistance against the currently used insecticides. Clove oil has been traditionally considered as an effective pesticide. The present study aimed at determining the efficacy of clove oil against the 4th instar larvae of insecticide resistant populations of T. granarium collected from different regions of Punjab i.e., Layyah, Okara, Gujranwala and Lahore. The Layyah population of Khapra beetle was identified as the most susceptible population (LC50= 0.1%), and the Lahore population as the resistant one (LC50= 0.78%) after exposure to various oil concentrations. The energy reserves and degradation enzymes needed to breakdown these energy stores were the main focus of this study. The alterations in the levels of carbohydrates, proteins and lipids were remarkable after treatment with clove oil at LC20 and LC50 doses. In Layyah population, a considerable loss of total protein (28.93%), glucose (84.1%) and glycogen (55.71%) while an increase in trehalose (4.48%) and lipids (264.22%) were recorded after exposure to LC50 doses compared with unexposed group. In Lahore population, a reduction in lipid contents (45.97%), total protein (67.67%), glucose (50.45%), glycogen (34.36%) and trehalose (31.59%) were observed after treatment with LC50 doses in comparison with untreated group. In case of LC20 doses, a decline in all the tested energy stores of both populations were observed in comparison with their respective unexposed groups. The total activities of degradation enzymes i.e., trehalase, amylase and invertase in Layyah population decreased (56.25, 21.10 and 84.62%, respectively) and in Lahore population reduction in activities were 14.62, 87.45 and 75%, respectively after exposure to their respective LC20 doses as compared to their respective unexposed groups. The activities of all tested enzymes were decreased after exposure to LC50 doses except for invertase activity that increased after exposure to LC50 dose in Lahore population. The trends observed at LC20 doses were milder compared to that of LC50 dose. The clove oil can be used effectively against khapra beetle to control its damage.


Article Information

Received 02 January 2023

Revised 23 February 2023

Accepted 10 March 2023

Available online 08 September 2023

(early access)

Published 16 January 2024

Authors’ Contribution

FRS and TR designed and supervised the study, and prepared final draft. AI performed experimental work. SR, AHB and UR performed statistical analysis. SR prepared the first draft.

Key words

Trogoderma granarium, Amylase, Clove oil, Glycogen, Trehalase, Stored grains

DOI: https://dx.doi.org/10.17582/journal.pjz/20230102141080

* Corresponding author: farah.zool@pu.edu.pk, dr.tanzeela@ucp.edu.pk

0030-9923/2024/0002-0561 $ 9.00/0

Copyright 2024 by the authors. Licensee Zoological Society of Pakistan.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).



INTRODUCTION

Approximately, 1660 insect pest’s species invade the agricultural commodity after harvesting (Hagstrum and Subramanyam, 2009). The losses due to the attack of insect pests might be about 30% in storage phase (Haubruge et al., 1997). Wheat is the most popular cereal crop in the world. Due to the vast variety of species, assortments, and flexibility, wheat is grown both in the winter and the spring in various countries (McKevith, 2004; Kumar et al., 2011). Approximately, 3.72% of the world’s wheat-growing regions are in Pakistan and it’s the eighth-largest producer of wheat, which accounts for roughly 3.17% of global wheat production (Shuaib et al., 2007). Post-harvest wheat loss contributes to its quantitative and qualitative damage mainly caused by insect pests (Riaz et al., 2022). Among these insect pests Trogoderma granarium is reported to be the most dangerous and destructive insect pest of stored commodities across the globe (Lowe et al., 2000). The uncontrollable invasion of khapra beetle cause huge commercial loss and cause enormous damage to bulk commodities (Hafiz et al., 2017). Larval stages have a three-year resilience to deprivation and a limited supply of nutrient moisture. Human health suffers greatly as a result of swallowing larval spiky hairs that are cut off and remain in product piles (Ahmedani et al., 2007).

Synthetic insecticides like organophosphates, pyrethroids and carbamates and fumigants like methyl bromide and phosphine were the most commonly used strategies. Fumigants were considered applicable and economical due to their broad-spectrum activities as well as rapid penetration without leaving any residue on the grains (Varma and Dubey, 2001; Ogendo et al., 2008). Methyl bromide was completely pushed out because it causes ozone depletion (Shaaya and Kostyukovsky, 2006; Tayoub et al., 2012). So, phosphine was the only strategy to control the invasion of insect pests during storage (Varma and Dubey, 2001). With increase in fumigation frequency, certain other problems like to effect non target organism, safety concerns for human health and environment and development of resistance in insect pests were noticed (Ogendo et al., 2008). Now, almost all major pests of stored products have developed resistance against phosphine (Lorini et al., 2007; Nayak et al., 2012).

In this scenario, some biodegradable, viable, safe, environment friendly and effective alternative to these conventional insecticides and fumigants are the dire need of time (Sheng et al., 2020). Several reports are in favor of fumigant/insecticidal potential of various botanical extracts (Tripathi et al., 2000; Isman, 2006, 2008; Ebadollahi et al., 2013; Sagheer et al., 2013; Tarigan and Harahap, 2016). Moreover, a variety of plant essential oils were investigated for their insecticidal efficacy against various insects and these plant essential oils are proved to more effective to control insect pests of storage facilities (Tripathi et al., 2000; Opolot et al., 2006; Ebadollahi et al., 2013; Tarigan and Harahap, 2016; Ramachandran et al., 2022; Wanna and Wongsawas, 2022).

Essential oils are synthesized as secondary metabolites by various families like Myrtaceae, Meliaceae, Asteraceae and Umbelliferae etc., of aromatic plants in their different vegetative organs (Ebadollahi et al., 2013; Koul et al., 2013; Sheng et al., 2020; Kheloul et al., 2020). Essential oils are the mixtures of highly volatile organic lipophilic components that includes terpenes, aromatic and aliphatic compounds with different functional groups (Brito et al., 2021).

Clove (Syzygium aromaticum L.) essential oils with great efficacy against storage facility insect pests like Sitophilus zeamais and Acanthoscelides obtectus are well documented (Huang et al., 2002; Li et al., 2011; Viteri Jumbo et al., 2014; Gonzales Correa et al., 2015). However, no attention is paid to towards alterations induced by clove oil essential oils in energy stores and carbohydrase activities in insects. The estimation of energy stores and carbohydrase activities after sublethal exposure is essential because these parameters play an important role in development of resistance, pest revival with secondary pest outbreak leading to failure in management strategy (Desneux et al., 2007; He et al., 2013; Guedes and Cutler, 2014; Santos et al., 2015).

Keeping in view all these challenges, the current study aimed at determining the efficacy of clove oil against the 4th instar larvae of insecticide resistant populations of T. granarium. Moreover, an effort was made to document the contents of energy reserves and activities of degradation enzymes after exposure to sublethal LC20 and LC50 doses.

MATERIALS AND METHODS

Trogoderma granarium culture and its maintenance

Four populations of the Khapra beetle were collected from the wheat storage godowns located in Layyah, Okara, Gujranwala and Lahore. Each population had already been exposed to phosphine and deltamethrin for decades while in stores. For propagation of culture, an optimum temperature 35±2°C and relative humidity 60±5% (Riaz et al., 2014) was maintained in the insect culture room of Institute of Zoology, University of the Punjab, Lahore. Male and female beetles were allowed to breed in hygienic, microbe-free glass jars of 300 mL capacity. A proper diet comprising of broken wheat and flour were provided. Different growth stages of beetles were developed but 4th instar larvae were chosen in current studies.

Determination of toxicity of clove oil

Clove oil (C7H12ClN3O2) was purchased from a departmental store in Lahore. It was pale yellow in color with spicy odor. Absolute acetone was used as an organic solvent. To determine the toxicity of clove oil, various concentrations (0.06, 0.08, 0.1, 0.3, 0.5, 0.7, 0.9, 1.1, and 1.3%) were prepared by using 0.6, 0.8, 1, 3, 5, 7, 9 and 11µL/mL of clove oil in acetone, respectively. The mixtures were stirred thoroughly in test tubes covered with aluminum foil.

The glass petri plates (90 mm diameter) were labelled according to their doses and were uniformly covered with 1 mL solution of respective concentration of clove oil. Petri plates were set to air dry until only oil remained on the surface and volatile acetone had disappeared. Twenty 4th larval instars were introduced in each petri plate and these were incubated at 35±2°C, 60±5% rh for 24 h. Control was also prepared by spreading 1 mL acetone instead of clove oil and proceeded like treatment. A completely randomized design with three replicates for each concentration were used. After 24 h exposure, the larvae showing any response after touch with camel hair brush was considered alive, in case of no response was assumed dead (Tayoub et al., 2012). The number of dead larvae in each petri plate was recorded and mortality was subjected to correction according to Abbot (1925). Minitab 16 was used to carry out Probit analysis (Finney, 1971) to estimate the LC20 and LC50.

Biochemical assay

About 1000 4th instars larvae of each Layyah and Lahore populations were exposed to their respective LC20 and LC50 doses for 24 h. Control/unexposed groups were also prepared by exposing the larvae with acetone. All analysis were carried out in triplicates. About twenty-eight 4th instar larvae were crushed in 2 mL phosphate-saline buffer using a motor-driven teflon glass homogenizer. The crushed larvae were centrifuged at 13500xg for 15 min at 4°C. The supernatants were used for estimation of contents of glucose according to Hartel et al. (1969), trehalose according to Carroll et al. (1956) and proteins (soluble and total) according to Bradford (1976). While the activities of trehalase, amylase, and invertase were calculated according to Dahlaqvist (1966), Wootton and Freeman (1982), respectively. The 4th instar larvae were homogenized in a 30% potassium hydroxide solution (KOH) for estimation of glycogen contents according to Consolazio and Lacono (1963) and lipid contents according to Zöllner and Kirsch (1962).

Statistical analysis

The statistical analysis was done using Minitab 16. Probit analysis gave insight about toxicity data while the data obtained on effect of LC20 and LC50 doses on energy stores and degrading enzymes was proceeded through un-paired t test to determine the significant differences at p< 0.05.

RESULTS

Toxicity assessment of clove essential oil

The LC50 values of clove oil for Layyah, Okara, Gujranwala and Lahore populations were 0.1, 0.4, 0.58 and 0.78%, respectively. Based on LC50 values, the Lahore population seemed the most resistant and Layyah population least resistant among all the tested populations. Similarly, LC20 values for Layyah, Okara, Gujranwala, and Lahore populations were 0.001, 0.08, 0.24 and 0.42%, respectively.

Effect of LC20 and LC50 on energy reserves

The amount of energy stores (µg/mg) in 4th instar larvae of Lahore and Layyah populations are presented in Table I while the percent change in these tested contents are shown in Figure 1. The total proteins and glucose contents in both populations were downregulated after exposure to both sublethal doses. The glycogen contents were downregulated in Lahore population after exposure to each sub lethal dose but in case of Layyah population glycogen contents were upregulated after exposure to LC20 but downregulated after LC50 exposure. Trehalose contents in Layyah population were down regulated at LC20 but when lethal dose exposure increased up to LC50, these contents were surprisingly increased as compared to LC20 as well as control group. In case of Lahore population, the trehalose and lipid contents downregulated after each sublethal dose as compared to control group but surprisingly the trehalose and lipid contents decreased after LC20 exposure but when exposure increased upto LC50 these contents increased in comparison with LC20. The lipid contents in Layyah population declined after LC20 and when exposure dose increased the decline was more prominent.

 

Table I. Toxic effects of LC20 and LC50 of clove oil on the energy reserves of 4th instar larvae of T. granarium after 24 h exposure.

Energy stores (µg/mg)

Strains

Unexposed control

Exposure to clove oil

LC20

LC50

Total protein contents

Layyah

45.83±1.16A

39.92±0. 2B

32.57±1.31C

Lahore

35.35±1.15A

26.97±1.55B

11.43±0.83C

Glucose contents

Layyah

94.92±2.31A

22.82±0.87B

15.18±0.32C

Lahore

81.45±0.18A

42.12±1.12B

40.36±0.73B

Glycogen contents

Layyah

13.75±9.44A

14.50±0.98A

60.92±9.48B

Lahore

40.84±4.51A

38.49±7.26A

26.81±1.36B

Trehalose contents

Layyah

55.59±1.68A

53.56±2.17A

58.08±3.55A

Lahore

52.09±4.86A

35.64±5.98A

50.35±4.10A

Lipids contents

Layyah

50.22±2.32A

41.98±2.29A

18.29±1.50B

Lahore

26.17±4.65A

98.95±3.46B

14.14±3.28C

 

Mean ± standard error of mean; n = 3 (No. of replicates used in each experiment); Means followed by the same letter in each row for each parameter are not significant from each other at P < 0.05with 95% confidence limit (Dunnett’s Test).

 

Table II. Effect of clove oil at of LC20 and LC50 on the total activity of carbohydrates metabolizing enzymes of 4th instar larvae of T. granarium

Strains

Enzymes

Unexposed control

Exposure to

LC20

LC50

Layyah

Amylase

63.73±8.46A

50.28±2.09B

38.01±1.27C

Trehalase

1.12±2.86A

0.49±10.6B

0.76±87.1B

Invertase

0.01±1.27A

0.002±0.12B

0.001±0.109B

Lahore

Amylase

1.49±3.17A

2.13±6.45B

1.66±358A

Trehalase

1.71±70.8A

1.46±38.3A

1.15±66.4B

Invertase

0.004±0.09A

0.001±0.02B

0.009±0.03B

 

Mean ± standard error of mean; n = 3 (No. of replicates used in each experiment); Means followed by the same letter in each row for each parameter are not significant from each other at P < 0.05 with 95% confidence limit (Dunnett’s Test). Amylase: SU/mg body wt; Trehalase: IU/mg body wt; Invertase: IU/mg body wt.

 

Effect of LC20 and LC50 on carbohydrate degrading enzymes

The amylase and trehalase activities were decreased after both levels of exposure in Layyah and Lahore populations with reference to their respective unexposed group. The percent decrease in these activities was more prominent at LC50 as compared to LC20 doses. The invertase activities decreased in both populations after each exposure except in Lahore population where a significant increase was observed after exposure to LC50, when compared with their control group (Table II and Fig. 2).

 

DISCUSSION

Plant essential oils are considered as the most interesting strategy for safer, cheaper and eco-friendly alternatives of conventional insecticides (Stevenson et al., 2017). The insecticidal potential of several plant oils and their extracts against the khapra beetle has been investigated (Asawalam and Onu, 2014). The current study’s goal was to assess clove essential oil’s efficiency against populations of 4th instar larvae from Layyah, Okara, Gujranwala, and Lahore at 35±2°C and 60±5% R.H. All populations of T. granarium exhibited very low LC20 and LC50 values of clove oil. These findings were supported by Suma et al. (2009) they examined the toxicity of insecticides and a few non-polar plant extracts on the Coccophagus lycimnia, Aphytis melinus, and Leptomastix dactylopii. All populations were said to be sensitive to the lethal and sub-lethal doses of applied treatments.

To suppress the bean weevil, Jumbo et al. (2014) used prescribed dosages of clove and cinnamon oil that had lower LC50 values. These oils contributed to the pest’s eventual repulsing and demise. Clove, eucalyptus, and neem oil extracts were shown to have lower LC50 values for controlling the larvae of C. maculatus, T. castaneum and T. granarium as reported by Mostafa et al. (2019). The significant impact of oil’s LC20 and LC50 was examined in relation to changes in the energy reserves (total protein, glucose, glycogen, trehalose, and lipids) of T. granarium larvae. However, no reports are available on the impact of sub-lethal dosages of clove oil on the energy stores of the Khapra beetle.

Carbohydrates are utilized during metamorphosis and development of insects (Kaufmann and Brown, 2008). They supply energy either to use immediately like glucose, or in the form of reserves like glycogen and trehalose. They may also have some structural role in cuticle synthesis. Protein synthesis play an important role in growth, maintenance, hormonal regulation, reproduction as well as integration in the cell (Cohen, 2010; Sugumaran, 2010). Enzymes, antibodies, and albuminous fractions are referred to as soluble proteins (Shakoori et al., 2016). While both soluble and insoluble proteins are present in total proteins. The lipids are considered as an independent reservoir of energy and their mobilization is done through hemolymph from storage site to the other organs where needed especially the vitellogenesis (Zhou and Miesfeld, 2009) and cuticular synthesis (Dapporto et al., 2008).

The considerable decline in protein levels as observed in current investigation might be attributed to their breakdown for metabolic need or for supply of amino acids to build polypeptide chains or it might be due to downregulation of protein synthesis. The findings of Khosravi et al. (2011) and Valizadeh et al. (2013) are in favor of current investigations. They observed decline in total proteins in Glyphodes pyloalis larvae exposed to Artemisia annua extracts and in elm leaf beetle toxified with neem extract, respectively. Ali and Ibrahim (2018) reported a decline in protein and carbohydrates contents in 4th instar larvae of Spodoptera littoralis after exposure to camphor oil while castor oil only decreased the carbohydrate contents.

Tarigan et al. (2016) investigated the effect of cinnamon, cardamom and nutmeg essential oils on carbohydrates, lipids and protein contents in various developmental stages of T. castaneum and Callosobruchus maculatus. They reported that all essential oils decreased all the above-mentioned nutritional components. Dris et al. (2017) documented protein, carbohydrate and lipids depletion in 4th larval instar of Culex pipiens after exposure with Ocimum basilicum essential oils. The drop in lipid contents were attributed to stimulation of adipokinetic hormone, which is involved in lipid metabolism (Kodrik and Socha, 2005). According to various reports, the conversion of lipids into proteins causes decrease in lipids and they are also involved to provide more energy (Omar et al., 2005; Shakoori et al., 2016).

Amylase, invertase and trehalase are the enzymes responsible for the degradation of carbohydrates to harvest needed energy in insects. The reduction in the total protein contents and reduced activities of degrading enzymes might be due to reduction DNA and RNA synthesis and ultimately leads to inhibition in protein expression are supported by the explanation of El-Barky et al. (2008). The current study indicated that stress induced by clove oil causes the inhibition of carbohydrate degrading enzymes and insect was unable to harvest energy from reservoirs and finally died. Similarly, Sohbi (2020) reported reduced activities of trehalase, invertase and amylase in 4th larval instar of Spodoptera littoralis after exposure to camphor essential oil. The studies of Yousef et al. (2018) also supported the current findings that significant inhibition in the activities of these tested enzymes in S. littoralis were observed after exposure to pepper mint oil. In contrast to these reports, El-Gendy and El-Shafiey (2018) reported a significant elevation in the activities of amylase, invertase and trehalase enzymes in Nezara viridula after exposure to bottle brush essential oil. They proposed that the decrease in protein contents and elevation in carbohydrate degrading enzymes implies mobilization of amino acids to provide energy which is required during detoxification mechanism (Gamil et al., 2011).

CONCLUSION

The clove oil has a great insecticidal potential having very low values of LC50 against all tested populations. It can be used as a biopesticide to kill khapra beetle in godowns. These findings are useful and can be incorporated in insect pest management strategy to control T. granarium.

ACKNOWLEDGEMENTS

FRS is highly grateful to Institute of Zoology, University of the Punjab to provide the facilities to carry-out this research work.

Funding

No funding was available.

Statement of conflict of interest

The authors have declared no conflicts of interest.

REFERENCES

Ahmedani, M.S., Khaliq, A., Tariq, M., Anwar, M. and Naz, S., 2007. Khapra beetle (Trogoderma granarium Everts): A serious threat to food security and safety. Pak. J. agric. Sci44: 481-493.

Ali, A.M. and Ibrahim, A.M., 2018. Castor and camphor essential oils alter hemocyte populations and induce biochemical changes in larvae of Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae). J. Asia Pac. Ent., 21: 631-637. https://doi.org/10.1016/j.aspen.2018.04.005

Asawalam, E.F. and Onu, L., 2014. Evaluation of some plant powders against Khapra beetle (Trogoderma granarium Everts) (Coleoptera: Dermestidae) on stored groundnut. Adv. Med. Pl. Res.2: 27-33.

Bradford, M.M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem.72: 248-254. https://doi.org/10.1016/0003-2697(76)90527-3

Brito, V.D., Achimón, F., Pizzolitto, R.P., Ramírez Sánchez, A., Gómez-Torres, E.A., Zygadlo, J. A. and Zunino, M.P., 2021. An alternative to reduce the use of the synthetic insecticide against the maize weevil Sitophilus zeamais through the synergistic action of Pimenta racemosa and Citrus sinensis essential oils with chlorpyrifos. J. Pest Sci., 94: 409-421.

Carroll, N.V., Longley, R.W. and Roe, J.H., 1956. The determination of glycogen in liver and muscle by use of anthrone reagent. J. biol. Chem.220: 583-593. https://doi.org/10.1016/S0021-9258(18)65284-6

Cohen, E., 2010. Chitin biochemistry: synthesis, hydrolysis and inhibition. Adv. Insect Physiol., 38: 5–74. https://doi.org/10.1016/S0065-2806(10)38005-2

Consolazio, C.F. and Iacono, J.M., 1963. Carbohydrates. In: Newer methods for nutritional biochemistry with applications and interpretations (ed. A.A. Albanese). Academic Press, New York, USA., pp. 317-367. https://doi.org/10.1016/B978-0-12-048001-2.50012-0

Dahlqvist, A., 1966. Intestinal disaccharidases. In: Methods in enzymology. Academic Press, New York, 8: 584-591. https://doi.org/10.1016/0076-6879(66)08105-9

Dapporto, L., Lambardi, D. and Turillazzi, S., 2008. Not only cuticular lipids: First evidence of differences between foundresses and their daughters in polar substances in the paper wasp Polistes dominulus. J. Insect Physiol., 54: 89–95. https://doi.org/10.1016/j.jinsphys.2007.08.005

Desneux, N., Decourtye, A. and Delpuech, J.M., 2007. The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Ent., 52: 81–106. https://doi.org/10.1146/annurev.ento.52.110405.091440

Dris, D., Tine-Djebbar, F. and Soltani, N., 2017. Lavandula dentata essential oils: Chemical composition and larvicidal activity against Culiseta longiareolata and Culex pipiens (Diptera: Culicidae). Afr. Entomol., 25: 387-394.

Ebadollahi, A., Khosravi, R., Sendi, J.J., Honarmand, P. and Amini, R.M., 2013. Toxicity and physiological effects of essential oil from Agastache foeniculum (Pursh) Kuntze against Tribolium castaneum Herbst (Coleoptera: Tenebrionidae) larvae. Annls Res. Rev. Biol., 3: 649-658.

El-barky, N.M., Dahi, H.F. and El-Sayed, Y.A., 2008. Toxicological evaluation and biochemical impacts for radient as a new generation of spinosyn of Spodoptera littoralis (Boisd.), larvae. Egypt. Acad. J. biol. Sci., 1: 85-97. https://doi.org/10.21608/eajbsa.2008.15738

El-Gendy, R.M. and El-Shafiey, S.N., 2018. Eco-friendly control strategies of green stink bug, Nezara viridula L. (Hemiptera: Pentatomidae): Repellency and toxicity effects of Callistemon citrinus, bottle brush essential oil. J. Pl. Prot. Pathol., 9: 807-813. https://doi.org/10.21608/jppp.2018.44071

Gamil, W.E., Mariy, F.M., Youssef, L.A. and Abdel-Halim, S.M., 2011. Effect of Indoxacarb on some biological and biochemical aspects of Spodoptera littoralis (Boisd.) larvae. Annls Agric. Sci., 56: 121-126. https://doi.org/10.1016/j.aoas.2011.07.005

Gonzales-Correa, Y.D.C., Faroni, L.R., Haddi, K., Oliveira, E.E. and Pereira, E.J.G., 2015. Locomotory and physiological responses induced by clove and cinnamon essential oils in the maize weevil Sitophilus zeamais. Pestic. Biochem. Physiol., (in press). https://doi.org/10.1016/j.pestbp.2015.06.005

Guedes, R.N.C. and Cutler, G.C., 2014. Insecticide-induced hormesis and arthropod pest management. Pest Manage. Sci., 70: 690–697. https://doi.org/10.1002/ps.3669

Hafiz, A., Riaz, T. and Shakoori, F.R., 2017. Metabolic profile of a stored grain pest Trogoderma granarium exposed to deltamethrin. Pakistan J. Zool., 49: Pages? https://doi.org/10.17582/journal.pjz/2017.49.1.183.188

Hagstrum, D.W.A. and Subramanyam, B., 2009. Stored-product insect resources. AACC International Inc., St. Paul, MN.

Hartel, A., Helger, R., and Lang, H., 1969. A method for determination of glucose. Z. Klin. Chem. Klin. Biochem., 7: 183-184.

Haubruge, E., Arnaud, L. and Mignon, J., 1997. The impact of sperm precedence in malathion resistance transmission in populations of the red flour beetle Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae). J. Stored Prod. Res., 33: 143-146. https://doi.org/10.1016/S0022-474X(96)00045-8

He, Y., Zhao, J., Zheng, Y., Weng, Q., Biondi, A., Desneux, N. and Wu, K., 2013. Assessment of potential sublethal effects of various insecticides on key biological traits of the tobacco whitefly, Bemisia tabaci. Int. J. biol. Sci., 9: 246–255. https://doi.org/10.7150/ijbs.5762

Huang, Y., Ho, S.H., Lee, H.C. and Yap, Y.L., 2002. Insecticidal properties of eugenol, isoeugenol and methyleugenol and their effects on nutrition of Sitophilus zeamais Motsch. (Coleoptera: Curculionidae) and Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae). J. Stored Prod. Res., 38: 403–412. https://doi.org/10.1016/S0022-474X(01)00042-X

Isman, M.B., 2006. Botanical insecticides, deterrents and repellents in modern agriculture and an increasingly regulated world. Annu. Rev. Ent., 51: 45-66. https://doi.org/10.1146/annurev.ento.51.110104.151146

Isman, M.B., 2008. Botanical insecticides for richer, for poorer. Pest Manage. Sci., 64: 8-11. https://doi.org/10.1002/ps.1470

Jumbo, L.O.V., Faroni, L.R., Oliveira, E.E., Pimentel, M.A. and Silva, G.N., 2014. Potential use of clove and cinnamon essential oils to control the bean weevil, Acanthoscelides obtectus Say, in small storage units. Ind. Crops Prod.56: 27-34. https://doi.org/10.1016/j.indcrop.2014.02.038

Kaufmann, C. and Brown, M.R., 2008. Regulation of carbohydrate metabolism and flight performance by a hypertrehalosaemic hormone in the mosquito Anopheles gambiae. J. Insect Physiol., 54: 367–377. https://doi.org/10.1016/j.jinsphys.2007.10.007

Kheloul, L., Anton, S., Gadenne, C. and Kellouche, A., 2020. Fumigant toxicity of Lavandula spica essential oil and linalool on different life stages of Tribolium confusum (Coleoptera: Tenebrionidae). J. Asia Pac. Ent.23: 320-326. https://doi.org/10.1016/j.aspen.2020.02.008

Khosravi, R., Sendi, J.J., Ghadamyari, M. and Yezdani, E., 2011. Effect of sweet wormwood Artemisia annua crude leaf extracts on some biological and physiological characteristics of the lesser mulberry pyralid, Glyphodes pyloalisJ. Insect Sci.11: 156. https://doi.org/10.1673/031.011.15601

Kodrík, D. and Socha, R., 2005. The effect of insecticide on adipokinetic hormone titre in the insect body. Pest Manage. Sci., 61: 1077-1082.

Koul, O., Singh, R., Kaur, B. and Kanda, D., 2013. Comparative study on the behavioral response and acute toxicity of some essential oil compounds and their binary mixtures to larvae of Helicoverpa armigera, Spodoptera litura and Chilo partellus. Ind. Crops Prod.49: 428-436. https://doi.org/10.1016/j.indcrop.2013.05.032

Kumar, P., Yadava, R.K., Gollen, B., Kumar, S., Verma, R.K. and Yadav, S., 2011. Nutritional contents and medicinal properties of wheat: A review. J. Life Sci. Res., 22: 1-10.

Li, L., Ge, L., Xue, T. and Li, X., 2011. Insecticidal effects of the insecticide based on porous starch and cinnamon oil against Sitophilus zeamais. Adv. Mater. Res., 160-162: 579–584. https://doi.org/10.4028/www.scientific.net/AMR.160-162.579

Lorini, I., Collins, P.J., Daglish, G.J., Nayak, M.K. and Pavic, H., 2007. Detection and characterization of strong resistance to phosphine in Brazilian Rhyzopertha dominica (F.) (Coleoptera: Bostrichidae). Pest Manage. Sci., 63: 358-364. https://doi.org/10.1002/ps.1344

Lowe, S., Browne, M., Boudjelas, S. and De Poorter, M., 2000. 100 of the world’s worst invasive alien species: A selection from the global invasive species database (Vol. 12). Invasive Species Specialist Group, Auckland.

McKevith, B., 2004. Nutritional aspects of cereals. Nutr. Bull., 29: 111-142. https://doi.org/10.1111/j.1467-3010.2004.00418.x

Mostafa, R.M., Essawy, H.S. and Baz, M.M., 2019. Potency of Alhagi maurorum plant extracts as phytoacaricidal against Panonychus citri (Acari: Tetranychidae). Egypt. Acad. J. biol. Sci., 10: 41-53.

Nayak, N.K., Holloway, J.C., Emery, R.N., Pavic, H., Bartlet, J. and Collins, P.J., 2012. Strong resistance to phosphine in the rusty grain beetle, Cryptolestes ferrugineus (Stephens) (Coleoptera: Laemophloeidae): its characterization, a rapid assay for diagnosis and its distribution in Australia. Pest Manage. Sci., 69: 48-53. https://doi.org/10.1002/ps.3360

Ogendo, J., Kostyukovsky, M., Ravid, U., Matasyoh, J., Deng, A., Omolo, E., Kariuki, S. and Shaaya, E., 2008. Bioactivities of Ocimum gratissimum L. oil and two of its constituents against five insect pests attacking stored food products. J. Stored Prod. Res., 44: 328-334. https://doi.org/10.1016/j.jspr.2008.02.009

Omar, N.A.M., Mousa, A., El-Husseini, M.M. and El-Bishry, M.H., 2005. Changes in lipid contents due to infection with Bacillus thuringiensis kurstaki in larvae of the greater wax moth, Galleria mellonella L. (Lepidoptera: Galleridae). Egypt. J. Biol. Pest Cont.15: 41-44.

Ramachandran, M., Baskar, K. and Jayakumar, M., 2022. Essential oil composition of Callistemon citrinus (Curtis) and its protective efficacy against Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae). PLoS One, 17: e0270084. https://doi.org/10.1371/journal.pone.0270084

Riaz, T., Masoom, A., Virk, U.Y., Raza, M. and Shakoori, F.R., 2022. Impacts of Metarhizium anisopliae on mortality, energy reserves, and carbohydrase of Trogoderma granarium. J. Stored Prod. Res., 99: 102013. https://doi.org/10.1016/j.jspr.2022.102013

Riaz, T., Shakoori, F.R. and Ali, S.S., 2014. Effect of temperature on the development, survival, fecundity and longevity of stored grain pest, Trogoderma granarium. Pakistan J. Zool., 46: 1485-1489.

Sagheer, M., Ali, K.,Hasan, M., Rashid, M., Sagheer, U. and Alvi, A., 2013. Repellent and toxicological impact of acetone extracts of Nicotiana tabacum, Pegnum hermala, Saussurea costus and Salsola baryosma against red flour beetle, Tribolium castaneum (Herbst). Pakistan J. Zool., 45: 1735-1739.

Santos, M., Santos, R., Tomé, H., Barbosa, W., Martins, G., Guedes, R. and Oliveira E., 2015. Imidacloprid-mediated effects on survival and fertility of the Neotropical brown stink bug Euschistus heros. J. Pest Sci. 89: 231–240. https://doi.org/10.1007/s10340-015-0666-y

Shaaya, E. and Kostyukovsky, M., 2006. Essential oils: Potency against stored product insects and mode of action. Stewart Posth.,

Shakoori, F.R., Feroz, A. and Riaz, T., 2016. Effect of sub-lethal doses of phosphine on macromolecular concentrations and metabolites of adult beetles of stored grain pest, Trogoderma granarium, previously exposed to phosphine. Pakistan J. Zool.48: 583-588.

Sheng, Z., Jian, R., Xie, F., Chen, B., Zhang, K., Li, D. and Hong, W.D., 2020. Screening of larvicidal activity of 53 essential oils and their synergistic effect for the improvement of deltamethrin efficacy against Aedes albopictusInd. Crops Prod., 145: 112131. https://doi.org/10.1016/j.indcrop.2020.112131

Shuaib, M., Zeb, A., Ali, Z., Ali, W., Ahmad, T. and Khan, I., 2007. Characterization of wheat varieties by seed storage protein electrophoresis. Afr. J. Biotechnol.6: 497-500.

Sobhi, A.S., 2020. Some toxicological and physiological aspects induced by camphor oil, Cinnamomum camphora on the cotton leafworm, Spodoptera littoralis (Boisduval). (Lepidoptera: Noctuidae). Egypt. Acad. J. Biol. Sci. Toxicol. Pest Contr., 12: 63-73.

Stevenson, P.C., Isman, M.B. and Belmain, S.R., 2017. Pesticidal plants in Africa: A global vision of new biological control products from local uses. Ind. Crops Prod., 110: 2-9. https://doi.org/10.1016/j.indcrop.2017.08.034

Sugumaran, M., 2010. Chemistry of cuticular sclerotization. Adv. Insect Physiol., 39: 151–209. https://doi.org/10.1016/B978-0-12-381387-9.00005-1

Suma, P., Zappalà, L., Mazzeo, G. and Siscaro, G., 2009. Lethal and sub-lethal effects of insecticides on natural enemies of citrus scale pests. Biol. Contr.54: 651-661. https://doi.org/10.1007/s10526-009-9215-z

Tarigan, S.I. and Harahap, I.S., 2016. Toxicological and physiological effects of essential oils against Tribolium castaneum (Coleoptera: Tenebrionidae) and Callosobruchus maculatus (Coleoptera: Bruchidae). J. Biopestic., 9: 135. https://doi.org/10.57182/jbiopestic.9.2.135-147

Tarigan, S.I. and Harahap, I.S., 2016. Toxicological and physiological effects of essential oils against Tribolium castaneum (Coleoptera: Tenebrionidae) and Callosobruchus maculatus (Coleoptera: Bruchidae). J. Biopest., 9: 135-147.

Tayoub, G., Abu Alnaser, A. and Ghanem, I., 2012. Fumigant activity of leaf essential oil from Myrtus communis L. against the Khapra beetle. Int. J. med. Arom. Pl.2: 207-213.

Tripathi, A.K., Veena, P., Aggarwal, K.K. and Sushil, K., 2000. Effect of volatile oil constituents of Mentha species against the stored grain pests, Callosobruchus maculatus and Tribolium castaneum. J. med. Aromat. Pl. Sci., 22: 549-556.

Valizadeh, B., Jalali Sendi, J., Zibaee, A. and Oftadeh, M., 2013. Effect of neem based insecticide Achook® on mortality, biological and biochemical parameters of elm leaf beetle Xanthogaleruca luteola (Col.: Chrysomelidae). J. Crop Prot.2: 319-330.

Varma, J. and Dubey, N.K., 2001. Efficacy of essential oils of Caesulia axillaris and Mentha vriensis against some storage pests causing biodeterioration of food commodities. Int. J. Fd. Microbiol., 68: 207-210. https://doi.org/10.1016/S0168-1605(01)00506-2

Viteri-Jumbo, L.O., Faroni, L.R.A., Oliveira, E.E., Pimentel, M.A. and Silva, G.N., 2014. Potential use of clove and cinnamon essential oils to control the bean weevil, Acanthoscelides obtectus Say, in small storage units. Indus. Crops Prod., 56: 27–34. https://doi.org/10.1016/j.indcrop.2014.02.038

Wanna, R. and Wongsawas, M., 2022. Toxicity and bioactivity of essential oil of cilantro (Eryngium foetidum L.) against red flour beetle [Tribolium castaneum (Herbst)]. Aust. J. Crop Sci., 16: 259-265. https://doi.org/10.21475/ajcs.22.16.02.3414

Wootton, I.D.P. and Freeman, H., 1982. Microanalysis in medical biochemistry. Churchill Livingstone, London, pp. 91-114.

Yousef, D.A., Bayoumi, A.E., Dimetry, N.Z., Amin, A.H. and Hoballah, E.M., 2018. Evaluating effect of pepper mint oil (Mentha pipreta) and its nano-formulations on some enzymatic activities and bionomics of cotton leaf worm Spodoptera littoralis (BOISD.). Arab Univ. J. agric. Sci.26: 1977-1991. https://doi.org/10.21608/ajs.2018.31665

Zhou, G. and Miesfeld, R.L., 2009. Energy metabolism during diapause in Culex pipiens mosquitoes. J. Insect Physiol., 55: 40–46. https://doi.org/10.1016/j.jinsphys.2008.10.002

Zöllner, N. and Kirsch, K., 1962. Micro determination of lipids by the sulphophosphovanillin reaction. Z. Ges. Exp. Med.135: 545–561. https://doi.org/10.1007/BF02045455

To share on other social networks, click on any share button. What are these?

Pakistan Journal of Zoology

February

Pakistan J. Zool., Vol. 56, Iss. 1, pp. 01-501

Featuring

Click here for more

Subscribe Today

Receive free updates on new articles, opportunities and benefits


Subscribe Unsubscribe