Neuromuscular systems in the fifth instar larva of silkworm Bombyx mori (Lepidoptera: Bombycidae): II- Abdominal musculature and its innervation
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Abstract
The gross organisation of abdominal musculature and its innervation by segmental ganglionic nerves were studied in the fifth instar larva of Bombyx mori. The musculature comprises dorsal, ventral and lateral groups of muscles, represented as external and internal layers. The dorsal group includes musculi dorsales interni mediales (DIM), musculi dorsales externi mediales (DEM), musculi dorsales interni laterals (DIL) and musculi dorsales externi laterales (DEL). The ventral group includes musculi ventrales interni mediales (VIM), musculi ventrales
externi mediales (VEM), musculi ventrales interni laterales (VIL) and musculi ventrales externi laterales (VEL). The lateral group is represented by musculi laterales interni (LI) and musculi laterales externi (LE). The abdominal muscles are innervated by the dorsal (DN) and ventral (VN) nerves of abdominal ganglia. The DN innervates ventral internal, lateral internal and both dorsal external and internal muscles, while the VN innervates ventral external and lateral muscles. The sensory branches of DN and VN innervate the bodywall in the dorsal and ventral regions respectively with a sort of overlapping in the lateral region. The neuromuscular integration and intersegmental coordination in the abdominal region is discussed with reference to locomotion in the silkworm larva.
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Keywords
Abdominal musculature, Bombyx mori, Ganglionic nerves, Innervation
References
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Barth, R. (1937). Masculatur und Bewegungsart der Reupen. Zool. Jahrb., 62: 507-566.
Bartos, M. and Honegger, H.W. (1992). Complex innervation of three neck muscles by motor and dorsal unpaired median neurons in crickets. Cell and Tissue Research., 267 (2): 399- 406.
Brunn, D.E. (1998). Cooperative mechanism between leg joints of Carausius morosus I.Non-spiking interneurons that contribute to interjoint coordination. J. Neurophysiol.,79: 2964 – 2976.
Bullaro, M. and Prete, F.R. (1999). Thoracic and prothoracic neuromuscular system of the preying mantid, Sphodromantis lineola (burmeister). J.Comp.Neurol., 409(2): 325 – 338.
Burrows, M. (2007). Anatomy of the hind legs and action of their muscles during jumping in leafhopper insects. J. Exp. Biol., 210: 3590 – 3600.
Chauthani, A. R. and Callahan, P.S. (1966). A dissection technique for studying internal anatomy of different stadia of Noctidae. Ann .Entomol . Soc. Am.,59: 1017- 1018.
Copenhaver, P.F. (2007). How to innervate a simple gut: familiar themes and unique aspects in the formation of the insect enteric nervous system. Dev. Dynamics., 236 (7): 1841-1864.
David, B.V. and Ananthakrishnan, T.N. (2006). General and Applied Entomology New Delhi: Tata McGRaw – Hill Publishing Company Ltd.,89-102.
Davis, N.T. (2005). Serial homologies of the motor neurons of the dorsal intersegmental muscles of the cockroach, Periplaneta Americana(L.). J. Morphol., 176 (92): 197- 210.
Denburg, J.L. and Fulop, Z. (2005). Formation of leg neuromuscular system in embryos of the cockroach, Periplaneta Americana. J.Exp.Zool., 219 (3): 323- 338.
Deshpande, S.B. and Pathan, K.M. (1982). On the pregenital abdominal muscular system in nymphal and adult Heptagenia diabasia, Burks (Ephemeroptera). J. Anim. Morphol. Physiol., 29: 272 – 279.
Duve, H., East, P. D., and Thorpe, A.(1999). Regulation of lepidopteran foregut movement by allostatins and allatotropin from the frontal ganglion. J.Comp. Neurol. , 413(3): 405 – 416.
Eaton, J.L. (1982). Exoskeleton and muscular morphology of the larval thorax of Manduca sexta (Lepidoptera: Sphingidae). Ann.Entomol. Soc. Am.,75: 313 – 322.
Honegger, H.W., Altman, J.S., Klen, J., Muller-Tauz, R., and Pollerberg, E.(2004). A comparative study of neck muscle motor neurons in a cricket and a locust. J.Comp.Neurology., 230 (4): 517 – 535.
Iles, J. F. and Pearson, K.G. (1969) Triple inhibitory innervation of insect muscle. J. Physiol., (Lond.)., 204: 125 - 126.
Kawasaki, F. and Kita, H. (2004). Structure and innervation of longitudinal and transverse abdominal muscles of the cricket, Gryllus bimaculatus. J.Comp.Neurol., 352(1): 134 -146.
Kent, K.S. and Levine, R.B.(2004). Neural control of leg movements in a metamorphosing insect: Persistence of larval leg motor neurons to innervate the adult legs of Manduca sexta. J. Comp. Neurol., 276 (1): 30 -43.
Klass, K.D. (2008). The pregenital abdomen of a mantid and a cockroach: Musculature and nerve topography, with comparative remarks on other neoptera (Insecta: Dictyoptera). Deutsche Entamologische Zeitschrift., 46(1): 3-42.
Kondoh, Y. and Obara, Y. (1982). Anatomy of motor neurons innervating mesothoracic indirect flight muscles in the silkmoth, Bombyx mori. J. Exp. Biol.,98: 23-37.
Kreiss, S., Schulte,C.C., Agricola, H.J. and Rathmayer, W. (1999). A single attatostatin- immunoreactive neuron innervates skeletal muscles of several segments in the locust. J.Comp. Neurol.,413 (4): 507-519.
Krishnaswami, S. (1986). New technology of silkworm rearing. Mysore ,India: Central Sericultural Research and Training Institute..
Libby, J. L. (1959). The nervous system of certain abdominal segments of the Cecropia larva (Lepidoptera: Saturnidae). Ann. Ent. Soc. Amer., 52: 469-480.
Masuko, K. (2005). Motor innervation and proprioceptors of the mouth parts in the worker honey bee Apis mellifera. II. Maxillary and labial nerves. J. Morphol., 201(1): 23 -37.
Owen, W.B.(2006). Morphology of the abdominal skeleton and muscles of the mosquito, Culiseta inormata (Wilson) (Diptera: Culicidae). J. Morphol., 166 (2): 155-178.
Ramirez, J.M. and Pearson,K.G. (1989). Alteration of the respiratory system at the onset of locust flight: I. Abdominal pumping. J.Exp.Biol., 142: 401 – 424.
Randall, W.C. (1968). Anatomical changes in the neuromuscular complex of the proleg of Galleria mellonella.L (Lepidoptera: Pyralididae) during metamorphosis. J. Morphol., 125: 105 – 128.
Ready, N.E. and Josephson, R.K. (2005 a). Flight muscle development in a hemi- metabolous insect. J.Exp.Zool., 220 (1): 49 - 56.
Ready, N.E. and Josephson, R.K. (2005 b). Structural and functional development of cricket wing muscles. J.Exp.Zool., 233 (1): 35 - 50.
Shankland, D.L. (2005). Nerves and muscles of the pregenital abdominal segments of the American cockroach, Periplaneta americana (L.). J. Morphol. 117(3): 353 - 385.
Shepheard, P. (1970). Control of head movement in the locust Schistocerca gregaria. Ph.D Thesis. Univrsity of St. Andrews.
Sink, H. (2006). Muscle Development in Drosophila. Springer Publishers.
Sivaprasad, S. and Muralimohan, P. (1998). Morphological changes in the nervous system of silkworm, Bombyx mori L. (Lepidoptera : Bombycidae) during metamorphosis. Indian J. Seric., 37 (1): 21 – 28.
Snodgrass, R.E. (1935). In Principles of Insect Morphology. McGraw-Hill Book Company Inc. New York.
Snodgrass, R. E. (1958). Evolution of arthropod mechanisms. Smithsonian. Misc. Coll., 138.
Spieb, R., Schoofs, A. and Heinzel, H.G. (2007). Anatomy of the stomatogastric nervous system associated with the foregut in Drosophila melanogaster and Calliphora vicina third instar larvae. J. Morphol. ,269(3): 272 – 282.
Stokes, D.R., Josephson, R.K. and Price, R.B. (2005). Structural and functional heterogeneity in an insect muscle. J. Exp. Zool., 194(2): 379- 407.
Taylor,H.M. and Truman, J.W.(1974). Metamorphosis of the abdominal ganglia of the tobacco hornworm, Manduca sexta: Changes in the populations of identified motoneurons. J. Comp.
Physiol., 90: 367 - 388.
Usherwood, P.N.R. (1967). Insect neuromuscular mechanisms. Am. Zool., 7: 553 - 582.
Usherwood, P.N.R. (1968). A critical study for the evidence for peripheral inhibitory axons in insects. J. Exp. Biol., 49: 201 - 222.
Wolf, H. and Harzsch, S. (2002). Evolution of arthropod neuromuscular system-1. Arrangement of muscles and innervation in the walking legs of a scorpion, Vaejovis spingerus(Wood, 1863),Vaejovidae, Scorpiones, Arachnida. Arthropod Struct. Dev., 31(3): 185 – 202.
Yack, J.E. (2004). The structure and function of auditory chordotonal organs in insects. Microsc.Res.Tech., 63(6): 315- 337.
Yang, Q.Z. (1983). The identification of motor neurons innervating an abdominal ventilatory muscle in the locust. J. Exp. Biol., 107: 115 – 127.
Youssef, N.N.(2005 a). Musculature, nervous system and glands of metasomal abdominal segments of the female of Nomia melanderi CkII.(Hymenoptera, Apoidea). J. Morphol., 125(2): 205 – 217.
Youssef, N.N.(2005 b). Musculature, nervous system and glands of metasomal abdominal segments of the male of Nomia melanderi CkII.(Hymenoptera, Apoidea). J. Morphol., 129(1): 59 – 79.
Barth, R. (1937). Masculatur und Bewegungsart der Reupen. Zool. Jahrb., 62: 507-566.
Bartos, M. and Honegger, H.W. (1992). Complex innervation of three neck muscles by motor and dorsal unpaired median neurons in crickets. Cell and Tissue Research., 267 (2): 399- 406.
Brunn, D.E. (1998). Cooperative mechanism between leg joints of Carausius morosus I.Non-spiking interneurons that contribute to interjoint coordination. J. Neurophysiol.,79: 2964 – 2976.
Bullaro, M. and Prete, F.R. (1999). Thoracic and prothoracic neuromuscular system of the preying mantid, Sphodromantis lineola (burmeister). J.Comp.Neurol., 409(2): 325 – 338.
Burrows, M. (2007). Anatomy of the hind legs and action of their muscles during jumping in leafhopper insects. J. Exp. Biol., 210: 3590 – 3600.
Chauthani, A. R. and Callahan, P.S. (1966). A dissection technique for studying internal anatomy of different stadia of Noctidae. Ann .Entomol . Soc. Am.,59: 1017- 1018.
Copenhaver, P.F. (2007). How to innervate a simple gut: familiar themes and unique aspects in the formation of the insect enteric nervous system. Dev. Dynamics., 236 (7): 1841-1864.
David, B.V. and Ananthakrishnan, T.N. (2006). General and Applied Entomology New Delhi: Tata McGRaw – Hill Publishing Company Ltd.,89-102.
Davis, N.T. (2005). Serial homologies of the motor neurons of the dorsal intersegmental muscles of the cockroach, Periplaneta Americana(L.). J. Morphol., 176 (92): 197- 210.
Denburg, J.L. and Fulop, Z. (2005). Formation of leg neuromuscular system in embryos of the cockroach, Periplaneta Americana. J.Exp.Zool., 219 (3): 323- 338.
Deshpande, S.B. and Pathan, K.M. (1982). On the pregenital abdominal muscular system in nymphal and adult Heptagenia diabasia, Burks (Ephemeroptera). J. Anim. Morphol. Physiol., 29: 272 – 279.
Duve, H., East, P. D., and Thorpe, A.(1999). Regulation of lepidopteran foregut movement by allostatins and allatotropin from the frontal ganglion. J.Comp. Neurol. , 413(3): 405 – 416.
Eaton, J.L. (1982). Exoskeleton and muscular morphology of the larval thorax of Manduca sexta (Lepidoptera: Sphingidae). Ann.Entomol. Soc. Am.,75: 313 – 322.
Honegger, H.W., Altman, J.S., Klen, J., Muller-Tauz, R., and Pollerberg, E.(2004). A comparative study of neck muscle motor neurons in a cricket and a locust. J.Comp.Neurology., 230 (4): 517 – 535.
Iles, J. F. and Pearson, K.G. (1969) Triple inhibitory innervation of insect muscle. J. Physiol., (Lond.)., 204: 125 - 126.
Kawasaki, F. and Kita, H. (2004). Structure and innervation of longitudinal and transverse abdominal muscles of the cricket, Gryllus bimaculatus. J.Comp.Neurol., 352(1): 134 -146.
Kent, K.S. and Levine, R.B.(2004). Neural control of leg movements in a metamorphosing insect: Persistence of larval leg motor neurons to innervate the adult legs of Manduca sexta. J. Comp. Neurol., 276 (1): 30 -43.
Klass, K.D. (2008). The pregenital abdomen of a mantid and a cockroach: Musculature and nerve topography, with comparative remarks on other neoptera (Insecta: Dictyoptera). Deutsche Entamologische Zeitschrift., 46(1): 3-42.
Kondoh, Y. and Obara, Y. (1982). Anatomy of motor neurons innervating mesothoracic indirect flight muscles in the silkmoth, Bombyx mori. J. Exp. Biol.,98: 23-37.
Kreiss, S., Schulte,C.C., Agricola, H.J. and Rathmayer, W. (1999). A single attatostatin- immunoreactive neuron innervates skeletal muscles of several segments in the locust. J.Comp. Neurol.,413 (4): 507-519.
Krishnaswami, S. (1986). New technology of silkworm rearing. Mysore ,India: Central Sericultural Research and Training Institute..
Libby, J. L. (1959). The nervous system of certain abdominal segments of the Cecropia larva (Lepidoptera: Saturnidae). Ann. Ent. Soc. Amer., 52: 469-480.
Masuko, K. (2005). Motor innervation and proprioceptors of the mouth parts in the worker honey bee Apis mellifera. II. Maxillary and labial nerves. J. Morphol., 201(1): 23 -37.
Owen, W.B.(2006). Morphology of the abdominal skeleton and muscles of the mosquito, Culiseta inormata (Wilson) (Diptera: Culicidae). J. Morphol., 166 (2): 155-178.
Ramirez, J.M. and Pearson,K.G. (1989). Alteration of the respiratory system at the onset of locust flight: I. Abdominal pumping. J.Exp.Biol., 142: 401 – 424.
Randall, W.C. (1968). Anatomical changes in the neuromuscular complex of the proleg of Galleria mellonella.L (Lepidoptera: Pyralididae) during metamorphosis. J. Morphol., 125: 105 – 128.
Ready, N.E. and Josephson, R.K. (2005 a). Flight muscle development in a hemi- metabolous insect. J.Exp.Zool., 220 (1): 49 - 56.
Ready, N.E. and Josephson, R.K. (2005 b). Structural and functional development of cricket wing muscles. J.Exp.Zool., 233 (1): 35 - 50.
Shankland, D.L. (2005). Nerves and muscles of the pregenital abdominal segments of the American cockroach, Periplaneta americana (L.). J. Morphol. 117(3): 353 - 385.
Shepheard, P. (1970). Control of head movement in the locust Schistocerca gregaria. Ph.D Thesis. Univrsity of St. Andrews.
Sink, H. (2006). Muscle Development in Drosophila. Springer Publishers.
Sivaprasad, S. and Muralimohan, P. (1998). Morphological changes in the nervous system of silkworm, Bombyx mori L. (Lepidoptera : Bombycidae) during metamorphosis. Indian J. Seric., 37 (1): 21 – 28.
Snodgrass, R.E. (1935). In Principles of Insect Morphology. McGraw-Hill Book Company Inc. New York.
Snodgrass, R. E. (1958). Evolution of arthropod mechanisms. Smithsonian. Misc. Coll., 138.
Spieb, R., Schoofs, A. and Heinzel, H.G. (2007). Anatomy of the stomatogastric nervous system associated with the foregut in Drosophila melanogaster and Calliphora vicina third instar larvae. J. Morphol. ,269(3): 272 – 282.
Stokes, D.R., Josephson, R.K. and Price, R.B. (2005). Structural and functional heterogeneity in an insect muscle. J. Exp. Zool., 194(2): 379- 407.
Taylor,H.M. and Truman, J.W.(1974). Metamorphosis of the abdominal ganglia of the tobacco hornworm, Manduca sexta: Changes in the populations of identified motoneurons. J. Comp.
Physiol., 90: 367 - 388.
Usherwood, P.N.R. (1967). Insect neuromuscular mechanisms. Am. Zool., 7: 553 - 582.
Usherwood, P.N.R. (1968). A critical study for the evidence for peripheral inhibitory axons in insects. J. Exp. Biol., 49: 201 - 222.
Wolf, H. and Harzsch, S. (2002). Evolution of arthropod neuromuscular system-1. Arrangement of muscles and innervation in the walking legs of a scorpion, Vaejovis spingerus(Wood, 1863),Vaejovidae, Scorpiones, Arachnida. Arthropod Struct. Dev., 31(3): 185 – 202.
Yack, J.E. (2004). The structure and function of auditory chordotonal organs in insects. Microsc.Res.Tech., 63(6): 315- 337.
Yang, Q.Z. (1983). The identification of motor neurons innervating an abdominal ventilatory muscle in the locust. J. Exp. Biol., 107: 115 – 127.
Youssef, N.N.(2005 a). Musculature, nervous system and glands of metasomal abdominal segments of the female of Nomia melanderi CkII.(Hymenoptera, Apoidea). J. Morphol., 125(2): 205 – 217.
Youssef, N.N.(2005 b). Musculature, nervous system and glands of metasomal abdominal segments of the male of Nomia melanderi CkII.(Hymenoptera, Apoidea). J. Morphol., 129(1): 59 – 79.
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Neuromuscular systems in the fifth instar larva of silkworm Bombyx mori (Lepidoptera: Bombycidae): II- Abdominal musculature and its innervation. (2009). Journal of Applied and Natural Science, 1(2), 210-226. https://doi.org/10.31018/jans.v1i2.60
