Impact of honey-enriched mulberry diet on the energy metabolism of the silkworm, Bombyx mori
Article Main
Abstract
The present study was taken-up with a view to clearly define the role of oxidative phosphorylation vis-a-vis transdeamination in Bombyx mori metamorphosis, under the influence of honey-enriched mulberry diet. Therefore, the study examined the accumulation and utilization patterns of carbohydrate (glycogen, trehalose, glucose) and non-carbohydrate energy reserves (proteins, amino acids) in its fat body during larval, pupal and adult stages. In accordance with Hutchinson’s investment principle, the energy reserves invested during larval stage are partly used in pupal stage and those invested during larval and pupal stages are used in adult stage. Their utilization patterns are correlated with the activity levels of succinate (SDH) and glutamate (GDH) dehydrogenases and aspartate (AAT) and alanine (ALAT) aminotransferases and changes thereof were interpreted in terms of glycolytic oxidative phosphorylation and non-glycolytic transdeamination. The trends in mass incorporation rates vis-à-vis enzyme activities indicated that the metabolism-related energy needs of all metamorphic events are majorly met through a gluconeogenetic mechanism called transdeamination, while the behavioural-related energy demands of larval and pupal stages are fulfilled through glycolytic-based oxidative phosphorylation. The activity trends further indicated that AAT plays major role in meeting the energy needs of larva and pupa, while GDH predominantly meets the energy requirements of reproduction in adults. The honey-enriched mulberry diet showed stage-specific and pathway-specific impacts on energy metabolism. It positively reinforced the energy metabolism in larval stage, but showed no significant effect in pupal and adult stages. Similarly, it showed more promising effect on glycolytic-oxidative phosphorylation and null or neutral effect on transdeamination.
Article Details
Article Details
Keywords
Aminotransferases, Bombyx mori, Dehydrogenases, Energy metabolism, Energy reserves
References
Aguila, J.R., Suszko, J., Gibbs A.G., and Hoshizaki, D.K. (2007). The role of larval fat cells in adult Drosophila melanogaster. J. Exp.Biol., 210: 956-963.
Anand, A.N., and Lorenz, M.W. (2008). Age-dependent changes of fat body stores and the regulation of fat body lipid synthesis and mobilisation by adipokinetic hormone in the last larval instar of the cricket, Gryllusbimaculatus. J. Insect Physiol., 54: 1404–1412. http://dx.doi.org/10.1016/j.jinsphys.200 8.08.001.
Arrese, E. L., and Soulages, J. L. (2010). Insect fat body: energy, metabolism, and regulation. Annu. Rev. Entomol. 55: 207-225. http://dx.doi.org/10.1146/annurev-ento-112408-085356.
Bolat, I. (2008). The importance of trehalose in brewing yeast survival. Innovative Romanian food Biotechnology, 2: 1-10.
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.
Cheng DJ, Xia QY, Zhao P, Wang ZL., and Xu HF (2006). EST-based profiling and comparison of gene expression in the silkworm fat body during metamorphosis. Arch Insect Biochem Physiol., 61:10–23. http://dx.doi.org/10.1002/arch.20090.
Garrido, D., Rubin, T., Poidevin, M., Maroni, B., Le Rouzic, A., Parvy, J. P. and Montagne, J. (2015). Fatty acid synthase cooperates with glyoxalase 1 to protect against sugar toxicity. PLoS Genet. 11, e1004995.
Han, R. D., Gan, Y. L., Kong, X. H., and Ge, F. (2008). Physiological and endocrine differences between diapauses and non diapausing larvae of the pine caterpillar Dengrolimus tabulaeformis (Lepidoptera: Lasicampidae). Zoological Studies, 47: 96-102.
Hemalatha, A., Bhuvaneswari, E., Sivaprasad, S.,and Yellamma, K. (2014). Metamorphosis-triggered trans-deamination of amino acids in the silkworm, Bombyx mori. Ind.J.Appl. Res.,4(11): 475-478. https://doi.org/10.36106/ijar
Hemalatha, A., Siva Prasad, S., and Murali Mohan, P. (2016). Aspects of protein metabolism in the silkworm, Bombyx mori (L), during larval-pupal metamorphosis. J. Adv. Zool. 2015: 36(2):70-78.
Hemavathi, B. (2001). Effect of thyroxine on growth and metabolic activities of silkworm, Bombyx mori L. Ph. D.Thesis, Sri Padmavati MahilaVisvavidyalayam, Tirupati, A.P, India.
Hou ,Y., Zhao,P., Liu, H.L., Zou,Y., Guan,J.,and Xia,Q.Y.(2007). Proteomics analysis of fat body from silkworm (Bombyx mori). Sheng Wu Gong Cheng Xue Bao, 23 (5): 867-872.
Hou, Y., Zou , Y ; Wang, F., Gong, J., Zhong, X., Xia, Q., and Zhao, P. (2010). Comparative analysis of proteome maps of silkworm haemolymph during different developmental stages. Proteome Sci., 8: 45.
Hutchinson, J.M.C., McNamara, J.M., Houston, A.I.,and Vollrath, F. (1997). Dyar's Rule and the Investment Principle: optimal moulting strategies if feeding rate is size-dependent and growth is discontinuous. Phil. Trans. R. Soc. Lond. B: 114-138.
Inagaki, S., and Yamashita, O. (1986). Metabolic shift from lipogenesis to glycogenesis in the last instar larval fat body of the silkworm, Bombyx mori. Insect Biochem., 16:327–31.
Kasmaei,F.G.,and Mahesha, H.B. (2012).Studies on succinate dehydrogenase and its relationship with economic characters of silkworm Bombyx mori L, Ann. Biol.,Res., 2012, 3(7):3638-51.
Krishnaswami, S. (1986). New technology of silkworm rearing. Central Sericultural Research and Training Institute, Mysore, India.
Kumar, K., and Balasubramaniyan, U.(2013).Studies on the impact of Spirulina plantensison the mulberry silkworm Bombyx mori (L).Int.J. Res. Phytochem. Pharmacol., 3(2): 99102.
Lee and Lardy (1965). Influence of thyroid hormones on phosphate dehydrogenase and other dehydrogenases in various organs of the rat. J. Biol. Chem.240: 1427-32.
Llandres, A.L., Marques, G.M., Maino, J.L., Kooijman, S., Kearney, M.R., and Casas J. (2015). A dynamic energy budget for the whole life-cycle of holometabolous insects. Ecol. Monogr. 85: 353–371. http://dx.doi.org/10.1890/14-0976.1
Lowry, O. H., Rosenbrough, N. J., Farra, L.,and Randall, R. J. (1951). Protein measurement with Folin phenol reagent. J. Biol. chem., 193: 265-275.
Lussey-Lepoutre,C., Kate E.R., Hollinshead., Christian Ludwig., Me´lanie Menara., Aure´lie Morin., Luis-Jaime Castro-Vega1., Seth J. Parker., Maxime Janin., Cosimo Martinelli1., Chris Ottolenghi., Christian Metallo., Anne-Paule Gimenez-Roqueplo., Judith Favier.,and Daniel A. Tennant. (2015). Loss of succinate dehydrogenase activity results in dependency on pyruvate carboxylation for cellular anabolism. Nature Communications; 10.1038/ncomms 9784.
Madhavi, R., Arivoli, S., and Siva Prasad, S. (2018). Determination of minimum effective concentration of honey that optimizes larval growth and silk production in the silkworm, Bombyx mori., Int. J. Green and Herbal Chem., 7 (3): 477-488.
Madhavi, R., Arivoli, S.,and Siva Prasad, S. (2020).Impact of honey-enriched mulberry diet on the digestive metabolism of the silkworm, Bombyx mori. Ind.J. Appl. Res., 10(4):1-8, https://doi.org/10.36106/ijar.
Maino, J.L., and Kearney, M.R. (2015). Testing mechanistic models of growth in insects. Proc.R.Soc.B,282: 20151973. https://doi.org/10.1098/rspb.2015.1973.
Matsuda, H., Yamada, T., Yoshida, M.,and Nishimura, T. (2015). Flies without trehalose. J. Biol. Chem. 290, 1244-1255.
Mendel,B., Kemp, A.,and Myers, D.K. (1954). A colorimetric micro-method for determination of glucose. Biochemical Journal 56(4):639-46.
Merkey, A.B., Wong, C.K., Hoshizaki, D.K.,and Gibbs, A.G. (2011). Energetics of metamorphosis in Drosophila melanogaster. J. Insect Physiol., 57: 1437–1445. http://dx.doi.org/10.1016/j.jinsphys.2011.07.013.
Mirth, C.K., and Riddiford, L. M. (2007). Size assessment and growth control: how adult size is determined in insects. Bio Essays, 29:344–55.
Moore, S., and Stein, W.A. (1954).A modified ninhydrin reagent for the photometric determination of amino acids and related compounds. J. Biol. Chem. 211: 907-913.
Nachlas, M.M., Margulies, S.I., and Seligman, A.M. (1960). A. A Calorimetric Method for the Estimation of Succinic Dehydrogenase Activity. J. Biol. Chem., 236 (2): 499-503.
Oyedotun, K.S.,and Lemire, B.D. (2004). The quaternary structure of the Saccharomyces cerevisiae succinate dehydrogenase. Homology modeling, cofactor docking, and molecular dynamics simulation studies". J. Biol. Chem., 279 (10): 9424–9431. http://dx.doi.org/10.1074/jbc.M311876200.
Ramakrishna, S.,and Bhaskar, M. (2009). Improvement in cocoon parameters of silkworm larvae, Bombyx mori (L) on induction of thyroxin hormone. The Bioscan. 4(1):175-178.
Ravichandran, S., and Rameshkumar, T. (2014). Effect of monocrotophos on the carbohydrate metabolism in the of ovary, fat body and haemolymph of Laccotrephesruber (Linn.) (Heteroptera: Nepidae). Int. J. Modn. Res. Rev., 2 (12): 605-609.
Reitman, S., Frankel, S. (1957). A calorimetric method for the determination of serum glutamic-oxaloacetic and glutamic-pyruvic transaminases.Am.J. Clin. Pathol.28:56.
Roe, R. (1955). The determination of sugar in blood and spinal fluid with anthrone reagent. J. Biol. Chem., 20: 335-343.
Scott, R.C., Schuldiner, O.,and Neufeld, T.P. (2004). Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev. Cell., 7: 167-178. http://dx.doi.org/10.1016/j.devcel.2004.07.009.
Shukla, E., Thorat, L. J., Nath, B. B.,and Gaikwad, S. M. (2015). Insect trehalase: physiological significance and potential applications. Glycobiology,25:357-67. http://dx.doi.org/10.1093/glycob/cwu125.
Sivaprasad, S. (2012). Simple method for calculation periodical growth rates in animals and plants. J. Bio. Innov. (5): 114-119.
Sivaprasad. S. (2015). Metamorphic changes in the profiles of transdeamination parameters in the intersegmental muscle of the silkworm, Bombyx mori. Int .J. Adv. in Pharmacy, Biology and Chemistry 4 (4): 760-766.
Sivaprasad, S., and Bhuvaneswari, E .(2018). Energetics of pupal-adult metamorphosis in the silkworm, Bombyx mori: An analysis of transdeamination parameters in the fat body and haemolymph. J. App.and Na. Sci. 10 (2): 746 – 752. https://doi.org/10.31018/jans.v7i1.603
Thulasi, N., and Sivaprasad, S. (2013). Synergetic effect of ascorbic acid and lemon juice on the growth and protein synthesis in the silkworm, Bombyx mori and its influence on economic traits of sericulture. J. Bio. Innov., 2(4): 168-183.
Thulasi, N., and Sivaprasad, S. (2014). Impact of feeding of lemon juice-enriched mulberry leaves on the larval growth, protein profiles and economic traits in the silkworm, Bombyx mori. Ind .J. Appl. Res., 4(2):36-44. https://doi.org/10.36106/ijar
Thulasi, N., and Sivaprasad, S (2015). Larval growth, silk production and economic traits of Bombyx mori under the influence of honey-enriched mulberry diet. J. Appl and Nat. Science, 7 (1): 286 – 292. https://doi.org/10.31018/jans.
Tibbets, T.M., and Martinez del Rio, C. (2007). Isotopic enrichment without change in diet: An ontogenetic shift in ?15N during insect metamorphosis, Functional Ecology, 22 (1):109 -113. http://dx.doi.org/ 10.1111/j.1365-2435.2007.01342.x
Van der Horst, D.J. (2003). Insect adipokinetic hormones: release and integration of flight energy metabolism. Comp. Biochem. and Physiol., Part B 136: 217–226.
Venugopal Reddy, B.,Divya, P., and Anitha, M. (2015). Quantitative profile Analysis of Mulberry Silkworm, Bombyx mori. L (CSR2XCSR4). Int. Letters Nat. Sci., 34; 34-41.
Yaginuma, T., and Ushizima, M. (2005). Proteolytic activity in the fat body during the pupal – adult metamorphosis of the silkworm, Bombyx mori. Exp. Zool. 259 (2): 145-153. http://dx.doi.org/10.1002/jez.140 2590202.
Yamada, T., Habara, O., Kubo, H., and Nishimura., T (2018).Fat body glycogen serves as a metabolic safeguard for the maintenance of sugar levels in Drosophila. Retrived on April 08 2020 from http://dev.biologists.org/lookup/doi/10.1242/dev.158865.
Yamaoka, K., Hoshino, M.,and Hirai, T. (1971). Role of sensory hairs on the anal papillae in oviposition behaviour of Bombyx mori. J. Insect Physiol., 47: 2327-2336.
Anand, A.N., and Lorenz, M.W. (2008). Age-dependent changes of fat body stores and the regulation of fat body lipid synthesis and mobilisation by adipokinetic hormone in the last larval instar of the cricket, Gryllusbimaculatus. J. Insect Physiol., 54: 1404–1412. http://dx.doi.org/10.1016/j.jinsphys.200 8.08.001.
Arrese, E. L., and Soulages, J. L. (2010). Insect fat body: energy, metabolism, and regulation. Annu. Rev. Entomol. 55: 207-225. http://dx.doi.org/10.1146/annurev-ento-112408-085356.
Bolat, I. (2008). The importance of trehalose in brewing yeast survival. Innovative Romanian food Biotechnology, 2: 1-10.
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.
Cheng DJ, Xia QY, Zhao P, Wang ZL., and Xu HF (2006). EST-based profiling and comparison of gene expression in the silkworm fat body during metamorphosis. Arch Insect Biochem Physiol., 61:10–23. http://dx.doi.org/10.1002/arch.20090.
Garrido, D., Rubin, T., Poidevin, M., Maroni, B., Le Rouzic, A., Parvy, J. P. and Montagne, J. (2015). Fatty acid synthase cooperates with glyoxalase 1 to protect against sugar toxicity. PLoS Genet. 11, e1004995.
Han, R. D., Gan, Y. L., Kong, X. H., and Ge, F. (2008). Physiological and endocrine differences between diapauses and non diapausing larvae of the pine caterpillar Dengrolimus tabulaeformis (Lepidoptera: Lasicampidae). Zoological Studies, 47: 96-102.
Hemalatha, A., Bhuvaneswari, E., Sivaprasad, S.,and Yellamma, K. (2014). Metamorphosis-triggered trans-deamination of amino acids in the silkworm, Bombyx mori. Ind.J.Appl. Res.,4(11): 475-478. https://doi.org/10.36106/ijar
Hemalatha, A., Siva Prasad, S., and Murali Mohan, P. (2016). Aspects of protein metabolism in the silkworm, Bombyx mori (L), during larval-pupal metamorphosis. J. Adv. Zool. 2015: 36(2):70-78.
Hemavathi, B. (2001). Effect of thyroxine on growth and metabolic activities of silkworm, Bombyx mori L. Ph. D.Thesis, Sri Padmavati MahilaVisvavidyalayam, Tirupati, A.P, India.
Hou ,Y., Zhao,P., Liu, H.L., Zou,Y., Guan,J.,and Xia,Q.Y.(2007). Proteomics analysis of fat body from silkworm (Bombyx mori). Sheng Wu Gong Cheng Xue Bao, 23 (5): 867-872.
Hou, Y., Zou , Y ; Wang, F., Gong, J., Zhong, X., Xia, Q., and Zhao, P. (2010). Comparative analysis of proteome maps of silkworm haemolymph during different developmental stages. Proteome Sci., 8: 45.
Hutchinson, J.M.C., McNamara, J.M., Houston, A.I.,and Vollrath, F. (1997). Dyar's Rule and the Investment Principle: optimal moulting strategies if feeding rate is size-dependent and growth is discontinuous. Phil. Trans. R. Soc. Lond. B: 114-138.
Inagaki, S., and Yamashita, O. (1986). Metabolic shift from lipogenesis to glycogenesis in the last instar larval fat body of the silkworm, Bombyx mori. Insect Biochem., 16:327–31.
Kasmaei,F.G.,and Mahesha, H.B. (2012).Studies on succinate dehydrogenase and its relationship with economic characters of silkworm Bombyx mori L, Ann. Biol.,Res., 2012, 3(7):3638-51.
Krishnaswami, S. (1986). New technology of silkworm rearing. Central Sericultural Research and Training Institute, Mysore, India.
Kumar, K., and Balasubramaniyan, U.(2013).Studies on the impact of Spirulina plantensison the mulberry silkworm Bombyx mori (L).Int.J. Res. Phytochem. Pharmacol., 3(2): 99102.
Lee and Lardy (1965). Influence of thyroid hormones on phosphate dehydrogenase and other dehydrogenases in various organs of the rat. J. Biol. Chem.240: 1427-32.
Llandres, A.L., Marques, G.M., Maino, J.L., Kooijman, S., Kearney, M.R., and Casas J. (2015). A dynamic energy budget for the whole life-cycle of holometabolous insects. Ecol. Monogr. 85: 353–371. http://dx.doi.org/10.1890/14-0976.1
Lowry, O. H., Rosenbrough, N. J., Farra, L.,and Randall, R. J. (1951). Protein measurement with Folin phenol reagent. J. Biol. chem., 193: 265-275.
Lussey-Lepoutre,C., Kate E.R., Hollinshead., Christian Ludwig., Me´lanie Menara., Aure´lie Morin., Luis-Jaime Castro-Vega1., Seth J. Parker., Maxime Janin., Cosimo Martinelli1., Chris Ottolenghi., Christian Metallo., Anne-Paule Gimenez-Roqueplo., Judith Favier.,and Daniel A. Tennant. (2015). Loss of succinate dehydrogenase activity results in dependency on pyruvate carboxylation for cellular anabolism. Nature Communications; 10.1038/ncomms 9784.
Madhavi, R., Arivoli, S., and Siva Prasad, S. (2018). Determination of minimum effective concentration of honey that optimizes larval growth and silk production in the silkworm, Bombyx mori., Int. J. Green and Herbal Chem., 7 (3): 477-488.
Madhavi, R., Arivoli, S.,and Siva Prasad, S. (2020).Impact of honey-enriched mulberry diet on the digestive metabolism of the silkworm, Bombyx mori. Ind.J. Appl. Res., 10(4):1-8, https://doi.org/10.36106/ijar.
Maino, J.L., and Kearney, M.R. (2015). Testing mechanistic models of growth in insects. Proc.R.Soc.B,282: 20151973. https://doi.org/10.1098/rspb.2015.1973.
Matsuda, H., Yamada, T., Yoshida, M.,and Nishimura, T. (2015). Flies without trehalose. J. Biol. Chem. 290, 1244-1255.
Mendel,B., Kemp, A.,and Myers, D.K. (1954). A colorimetric micro-method for determination of glucose. Biochemical Journal 56(4):639-46.
Merkey, A.B., Wong, C.K., Hoshizaki, D.K.,and Gibbs, A.G. (2011). Energetics of metamorphosis in Drosophila melanogaster. J. Insect Physiol., 57: 1437–1445. http://dx.doi.org/10.1016/j.jinsphys.2011.07.013.
Mirth, C.K., and Riddiford, L. M. (2007). Size assessment and growth control: how adult size is determined in insects. Bio Essays, 29:344–55.
Moore, S., and Stein, W.A. (1954).A modified ninhydrin reagent for the photometric determination of amino acids and related compounds. J. Biol. Chem. 211: 907-913.
Nachlas, M.M., Margulies, S.I., and Seligman, A.M. (1960). A. A Calorimetric Method for the Estimation of Succinic Dehydrogenase Activity. J. Biol. Chem., 236 (2): 499-503.
Oyedotun, K.S.,and Lemire, B.D. (2004). The quaternary structure of the Saccharomyces cerevisiae succinate dehydrogenase. Homology modeling, cofactor docking, and molecular dynamics simulation studies". J. Biol. Chem., 279 (10): 9424–9431. http://dx.doi.org/10.1074/jbc.M311876200.
Ramakrishna, S.,and Bhaskar, M. (2009). Improvement in cocoon parameters of silkworm larvae, Bombyx mori (L) on induction of thyroxin hormone. The Bioscan. 4(1):175-178.
Ravichandran, S., and Rameshkumar, T. (2014). Effect of monocrotophos on the carbohydrate metabolism in the of ovary, fat body and haemolymph of Laccotrephesruber (Linn.) (Heteroptera: Nepidae). Int. J. Modn. Res. Rev., 2 (12): 605-609.
Reitman, S., Frankel, S. (1957). A calorimetric method for the determination of serum glutamic-oxaloacetic and glutamic-pyruvic transaminases.Am.J. Clin. Pathol.28:56.
Roe, R. (1955). The determination of sugar in blood and spinal fluid with anthrone reagent. J. Biol. Chem., 20: 335-343.
Scott, R.C., Schuldiner, O.,and Neufeld, T.P. (2004). Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev. Cell., 7: 167-178. http://dx.doi.org/10.1016/j.devcel.2004.07.009.
Shukla, E., Thorat, L. J., Nath, B. B.,and Gaikwad, S. M. (2015). Insect trehalase: physiological significance and potential applications. Glycobiology,25:357-67. http://dx.doi.org/10.1093/glycob/cwu125.
Sivaprasad, S. (2012). Simple method for calculation periodical growth rates in animals and plants. J. Bio. Innov. (5): 114-119.
Sivaprasad. S. (2015). Metamorphic changes in the profiles of transdeamination parameters in the intersegmental muscle of the silkworm, Bombyx mori. Int .J. Adv. in Pharmacy, Biology and Chemistry 4 (4): 760-766.
Sivaprasad, S., and Bhuvaneswari, E .(2018). Energetics of pupal-adult metamorphosis in the silkworm, Bombyx mori: An analysis of transdeamination parameters in the fat body and haemolymph. J. App.and Na. Sci. 10 (2): 746 – 752. https://doi.org/10.31018/jans.v7i1.603
Thulasi, N., and Sivaprasad, S. (2013). Synergetic effect of ascorbic acid and lemon juice on the growth and protein synthesis in the silkworm, Bombyx mori and its influence on economic traits of sericulture. J. Bio. Innov., 2(4): 168-183.
Thulasi, N., and Sivaprasad, S. (2014). Impact of feeding of lemon juice-enriched mulberry leaves on the larval growth, protein profiles and economic traits in the silkworm, Bombyx mori. Ind .J. Appl. Res., 4(2):36-44. https://doi.org/10.36106/ijar
Thulasi, N., and Sivaprasad, S (2015). Larval growth, silk production and economic traits of Bombyx mori under the influence of honey-enriched mulberry diet. J. Appl and Nat. Science, 7 (1): 286 – 292. https://doi.org/10.31018/jans.
Tibbets, T.M., and Martinez del Rio, C. (2007). Isotopic enrichment without change in diet: An ontogenetic shift in ?15N during insect metamorphosis, Functional Ecology, 22 (1):109 -113. http://dx.doi.org/ 10.1111/j.1365-2435.2007.01342.x
Van der Horst, D.J. (2003). Insect adipokinetic hormones: release and integration of flight energy metabolism. Comp. Biochem. and Physiol., Part B 136: 217–226.
Venugopal Reddy, B.,Divya, P., and Anitha, M. (2015). Quantitative profile Analysis of Mulberry Silkworm, Bombyx mori. L (CSR2XCSR4). Int. Letters Nat. Sci., 34; 34-41.
Yaginuma, T., and Ushizima, M. (2005). Proteolytic activity in the fat body during the pupal – adult metamorphosis of the silkworm, Bombyx mori. Exp. Zool. 259 (2): 145-153. http://dx.doi.org/10.1002/jez.140 2590202.
Yamada, T., Habara, O., Kubo, H., and Nishimura., T (2018).Fat body glycogen serves as a metabolic safeguard for the maintenance of sugar levels in Drosophila. Retrived on April 08 2020 from http://dev.biologists.org/lookup/doi/10.1242/dev.158865.
Yamaoka, K., Hoshino, M.,and Hirai, T. (1971). Role of sensory hairs on the anal papillae in oviposition behaviour of Bombyx mori. J. Insect Physiol., 47: 2327-2336.
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Impact of honey-enriched mulberry diet on the energy metabolism of the silkworm, Bombyx mori . (2020). Journal of Applied and Natural Science, 12(2), 133-145. https://doi.org/10.31018/jans.vi.2273
