Mapping of serotonin-immunoreactive neurons of Anastrepha obliqua Macquart larvae

Boleli, Isabel Cristina; Paulino-Simões, Zilá Luz

doi:10.1590/S0101-81751999000400019

Abstract

Serotonin-immunoreactive neurons were identified in the central nervous system (CNS) of Anastrepha obliqua Macquart, 1835 wandering stage larvae. The PAP immunocytochemical method was applied to the entire CNS (whole mounts). About 90 neurons were visualized in the CNS (20 in the brain and 70 in the ventral ganglion). Both somata and axons were strongly stained. These neurons showed a segmental arrangement and bilateral symmetry. All processes presented a basic projection pattern, in which the major fibres travel contralaterally. Comparison of these neurons with serotonergic neurons described in other insects suggests order-specific traits such as cerebral clusters and presence of only one 5-HT immunoreactive neuron in the 8th abdominal neuromere as well.

Anastrepha obliqua; fruit fly; serotonin; immunocytochemistry

Mapping of serotonin-immunoreactive neurons of Anastrepha obliqua Macquart larvae

Isabel Cristina Boleli^I; Zilá Luz Paulino-Simões^II

^IDepartamento de Morfologia e Fisiologia Animal, Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista. Rodovia Paulo Donato Castellani Km 5, 14870-000 Jaboticabal, São Paulo, Brasil

^IIDepartamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo. Rodovia Bandeirantes 3900, 14040-901 Ribeirão Preto, São Paulo, Brasil

ABSTRACT

Serotonin-immunoreactive neurons were identified in the central nervous system (CNS) of Anastrepha obliqua Macquart, 1835 wandering stage larvae. The PAP immunocytochemical method was applied to the entire CNS (whole mounts). About 90 neurons were visualized in the CNS (20 in the brain and 70 in the ventral ganglion). Both somata and axons were strongly stained. These neurons showed a segmental arrangement and bilateral symmetry. All processes presented a basic projection pattern, in which the major fibres travel contralaterally. Comparison of these neurons with serotonergic neurons described in other insects suggests order-specific traits such as cerebral clusters and presence of only one 5-HT immunoreactive neuron in the 8^th abdominal neuromere as well.

Key words: Anastrepha obliqua, fruit fly, serotonin, immunocytochemistry

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Acknowledgements. We thank J. Lauder (University of North Carolina, Chapell Hill) for the kind donation of rabbit antiserotonin serum. We are also grateful to Brazilian Government (CNPq) for financial support for ICB.

Recebido em 18.VI.1998; aceito em 07.X.1999.

Albrecht, C.P. & M. Sherman. 1987. Lethal and sublethal effects of overmectin B1 on three fruit fly species (Diptera: Tephritidae). Jour. Econ. Entomol. 80: 344-347.
Banner, S.E.; R.H Osborne & K.J Catell. 1987. The pharmacology of the isolated foregut of the locust Schistocerca migratoria. I. The effect of a range of putative neurotransmitters. Comp. Biochemic. Physiol. 88 (C): 131-138.
Bate, C.M. 1976. Embryogenesis of an insect nervous system. I. A map of the thoracic and abdominal neuroblasts in Locusta migratoria. Jour. Embryol. Exp. Morphol. 35: 107-123.
Bishop, C.A. & M. O'Shea. 1983. Serotonin-immunoreactive neurons in the central nervous segment-specific of an insect (Periplaneta americana). Jour. Neurobiol. 14: 251-269.
Boleli, I.C.; Z.L Paulino-Simões & M.M. da C. Teles. 1994. Neurosecretory cells of third-instar larvae of Anastrepha obliqua Macquart (Diptera, Tephritidae). Revta bras. Zool. 11 (4): 673-682.
Boleli, I.C.; Z.L. Paulino-Simões & K. Hartfelder. 1995. Serotonin-like immunoreactivity in the central nervous and neuroendocrine system of honey bee (Apis mellifera) larvae and pupae. Zoology 99: 58-67.
Bourne, J.A. 1984. Handbook of immunoperoxidase staining methods. Santa Barbara, Dako corporation, 36p.
Breidbach, O. 1991. Constancies in the neuronal architecture of the suboesophageal ganglion at metamorphosis in the beetle Tenebrio molitor L. Cell Tissue Res. 266: 173-190.
Brusca, R.C. & G.J. Brusca. 1990. Invertebrates. Bundesland, Genauer Associates Inc. Publishers, 922p.
Davey, K.G. & J.E. Treherne. 1963. Studies on crop function in the cokroach (Periplaneta americana L.). II. The nervous control of crop-emptyng. Jour. exp. Biol. 40: 763-773.
Fraenkel, G. & G. Bhaskaran. 1973. Pupariation and pupation in Cyclorrhaphous flies (Diptera): terminology and interpretation. Ann. Ent. Soc. Amer. 66 (2): 418-422.
Homberg, U. & J.G. Hildebrand. 1989. Serotonin-immunoreactive neurons in the medial protocerebrum and suboesophageal ganglion of the sphinx moth Manduca sexta. Cell Tissue Res. 258: 1-24.
Lauder, J.M. 1993. Neurotransmitters as growth regulatory signals: role of receptors and second messengers. Tins 16 (6): 233-239.
Longley, A.J. & R.D. Longley. 1986. Serotonin immunoreactivity in the nervous system of the dragonfly nymph. Jour. Neurobiol. 17 (4): 329-338.
Malavasi, A.; J.S. Morgante & R.A. Zucchi. 1980. Biologia de moscas-das-frutas (Diptera-Tephritidae). I. Lista de hospedeiros e ocorrência. Rev. Brasil. Biol. 40(1): 9-16.
Martinez, A.J. & D.S. Moreno. 1991. Effect of cyromazine on the oviposition of Mexican fruit fly (Diptera: Tephritidae) in the laboratory. Jour. Econ. Entomol. 84: 1540-1543.
Nassel, D.R. & R. Cantera. 1985. Mapping of serotonin-immunoreactive neurons in the larval nervous system of the flies Calliphora erythrocephala and Sarcophaga bullata. A comparison with ventral ganglia in adult animals. Cell Tissue Res. 239: 423-434.
Nassel, D.R. & N. Klemm. 1983. Serotonin-like immunoreactivity in the optic lobes of three insect species. Cell Tissue Res. 232: 129-140.
Rachtnsky, A. 1994. Octopamin and serotonin influence on corpora allata activity in honey bee (Apis mellifera) larvae. Jour. Insect Physiol. 40: 549-554.
Raga, A.; M.E. Sato; D.P. Fonseca Jr.; M.R. Potenza & M.F. Souza Filho. 1993. Respostas de Ceratitis capitata (Diptera: Tephritidae) à ação de ciromazina fornecida a adultos em condições de laboratório. Rev. Brasil. Frut. 15: 205-209.
Raga, A.; M.E. Sato; M.R. Potenza; M.F. Souza Filho & R.B.P. Giordano. 1994. Atividade de ciromazina sobre Ceratitis capitata (Wied.) (Diptera: Tephritidae) em laboratório. An. Soc. Entomol. Brasil 23: 503-510.
Riddiford, L.M. 1994. Cellular and molecular actions of juvenile hormones I. General considerations and premetamorphic actions. Adv. Insect Physiol. 24: 213-274.
Steinbush, H.W.M.; A.A.J. Verhofstad & H.W.J. Joosten. 1983. Antibodies to serotonin for neuroimmunocytochemical studies on the central nervous system. Methodological aspects and applications, p.130-158. In: C. Cuello (Ed.). BRD Handbook: Neuroimmunocytochesmistry. Chichester, Wiley, 256p.
Taghert, P.H. & C.S. Goodman. 1984. Cell determination and differentiation of identified serotonin-immunoreactive neurons in the grasshopper embryo. Jour. Neurosc. 4: 988-1000.
Teles da Silva, M.M. 1978. Algumas espécies de mosca-da-fruta do gênero Anastrepha (Diptera-Tephritidae). In: III Congresso Latino-Americano de Entomologia, p.25.
Truman, W.T. & M. Bate. 1988. Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Dev. Biol. 125: 145-157.
Vallés, A.M. & K. White. 1988. Serotonin-containing neurons in Drosophila melanogaster: development and distribuition. Jour. comp. Neurol. 268: 414-428.
van Haeften, T. & H. Schooneveld. 1992. Serotonin-like immunoreactivity in the ventral nerve cord of the Colorado potato beetle, Leptinotarsa decemlineata: identification of five different neuron classes. Cell Tissue Res. 270: 405-413.
van Haeften, T.; H.M. Smid & H. Schooneveld. 1993. Serotonergic innervation of the alimentary canal of the Colorado potato beetle Leptinotarsa decemlineata: structural and fuctional aspects. Cell Tissue Res. 273: 475-485.
Vieillemaringe, J.; P. Duris; C. Bensch & J. Girardie. 1982. Co-localization of amines and peptides in the same median neurosecretory cells of locusts. Neuroscience 31: 237-240.
Wigglesworth, V.B. 1985. Historical perspectives, p. 1-24. In G.A. Kerkut & L.I Gilbert (eds). Comprehensive Insect Physiology, Biochemistry and Pharmacology. Oxford, Pergamon Press, Vol. 7,457p.

Publication Dates

Publication in this collection
19 June 2009
Date of issue
1999

History

Received
18 June 1998
Accepted
07 Oct 1999

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

[1] Albrecht, C.P. & M. Sherman. 1987. Lethal and sublethal effects of overmectin B1 on three fruit fly species (Diptera: Tephritidae). Jour. Econ. Entomol. 80: 344-347.

[2] Banner, S.E.; R.H Osborne & K.J Catell. 1987. The pharmacology of the isolated foregut of the locust Schistocerca migratoria. I. The effect of a range of putative neurotransmitters. Comp. Biochemic. Physiol. 88 (C): 131-138.

[3] Bate, C.M. 1976. Embryogenesis of an insect nervous system. I. A map of the thoracic and abdominal neuroblasts in Locusta migratoria. Jour. Embryol. Exp. Morphol. 35: 107-123.

[4] Bishop, C.A. & M. O'Shea. 1983. Serotonin-immunoreactive neurons in the central nervous segment-specific of an insect (Periplaneta americana). Jour. Neurobiol. 14: 251-269.

[5] Boleli, I.C.; Z.L Paulino-Simões & M.M. da C. Teles. 1994. Neurosecretory cells of third-instar larvae of Anastrepha obliqua Macquart (Diptera, Tephritidae). Revta bras. Zool. 11 (4): 673-682.

[6] Boleli, I.C.; Z.L. Paulino-Simões & K. Hartfelder. 1995. Serotonin-like immunoreactivity in the central nervous and neuroendocrine system of honey bee (Apis mellifera) larvae and pupae. Zoology 99: 58-67.

[7] Bourne, J.A. 1984. Handbook of immunoperoxidase staining methods. Santa Barbara, Dako corporation, 36p.

[8] Breidbach, O. 1991. Constancies in the neuronal architecture of the suboesophageal ganglion at metamorphosis in the beetle Tenebrio molitor L. Cell Tissue Res. 266: 173-190.

[9] Brusca, R.C. & G.J. Brusca. 1990. Invertebrates. Bundesland, Genauer Associates Inc. Publishers, 922p.

[10] Davey, K.G. & J.E. Treherne. 1963. Studies on crop function in the cokroach (Periplaneta americana L.). II. The nervous control of crop-emptyng. Jour. exp. Biol. 40: 763-773.

[11] Fraenkel, G. & G. Bhaskaran. 1973. Pupariation and pupation in Cyclorrhaphous flies (Diptera): terminology and interpretation. Ann. Ent. Soc. Amer. 66 (2): 418-422.

[12] Homberg, U. & J.G. Hildebrand. 1989. Serotonin-immunoreactive neurons in the medial protocerebrum and suboesophageal ganglion of the sphinx moth Manduca sexta. Cell Tissue Res. 258: 1-24.

[13] Lauder, J.M. 1993. Neurotransmitters as growth regulatory signals: role of receptors and second messengers. Tins 16 (6): 233-239.

[14] Longley, A.J. & R.D. Longley. 1986. Serotonin immunoreactivity in the nervous system of the dragonfly nymph. Jour. Neurobiol. 17 (4): 329-338.

[15] Malavasi, A.; J.S. Morgante & R.A. Zucchi. 1980. Biologia de moscas-das-frutas (Diptera-Tephritidae). I. Lista de hospedeiros e ocorrência. Rev. Brasil. Biol. 40(1): 9-16.

[16] Martinez, A.J. & D.S. Moreno. 1991. Effect of cyromazine on the oviposition of Mexican fruit fly (Diptera: Tephritidae) in the laboratory. Jour. Econ. Entomol. 84: 1540-1543.

[17] Nassel, D.R. & R. Cantera. 1985. Mapping of serotonin-immunoreactive neurons in the larval nervous system of the flies Calliphora erythrocephala and Sarcophaga bullata. A comparison with ventral ganglia in adult animals. Cell Tissue Res. 239: 423-434.

[18] Nassel, D.R. & N. Klemm. 1983. Serotonin-like immunoreactivity in the optic lobes of three insect species. Cell Tissue Res. 232: 129-140.

[19] Rachtnsky, A. 1994. Octopamin and serotonin influence on corpora allata activity in honey bee (Apis mellifera) larvae. Jour. Insect Physiol. 40: 549-554.

[20] Raga, A.; M.E. Sato; D.P. Fonseca Jr.; M.R. Potenza & M.F. Souza Filho. 1993. Respostas de Ceratitis capitata (Diptera: Tephritidae) à ação de ciromazina fornecida a adultos em condições de laboratório. Rev. Brasil. Frut. 15: 205-209.

[21] Raga, A.; M.E. Sato; M.R. Potenza; M.F. Souza Filho & R.B.P. Giordano. 1994. Atividade de ciromazina sobre Ceratitis capitata (Wied.) (Diptera: Tephritidae) em laboratório. An. Soc. Entomol. Brasil 23: 503-510.

[22] Riddiford, L.M. 1994. Cellular and molecular actions of juvenile hormones I. General considerations and premetamorphic actions. Adv. Insect Physiol. 24: 213-274.

[23] Steinbush, H.W.M.; A.A.J. Verhofstad & H.W.J. Joosten. 1983. Antibodies to serotonin for neuroimmunocytochemical studies on the central nervous system. Methodological aspects and applications, p.130-158. In: C. Cuello (Ed.). BRD Handbook: Neuroimmunocytochesmistry. Chichester, Wiley, 256p.

[24] Taghert, P.H. & C.S. Goodman. 1984. Cell determination and differentiation of identified serotonin-immunoreactive neurons in the grasshopper embryo. Jour. Neurosc. 4: 988-1000.

[25] Teles da Silva, M.M. 1978. Algumas espécies de mosca-da-fruta do gênero Anastrepha (Diptera-Tephritidae). In: III Congresso Latino-Americano de Entomologia, p.25.

[26] Truman, W.T. & M. Bate. 1988. Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Dev. Biol. 125: 145-157.

[27] Vallés, A.M. & K. White. 1988. Serotonin-containing neurons in Drosophila melanogaster: development and distribuition. Jour. comp. Neurol. 268: 414-428.

[28] van Haeften, T. & H. Schooneveld. 1992. Serotonin-like immunoreactivity in the ventral nerve cord of the Colorado potato beetle, Leptinotarsa decemlineata: identification of five different neuron classes. Cell Tissue Res. 270: 405-413.

[29] van Haeften, T.; H.M. Smid & H. Schooneveld. 1993. Serotonergic innervation of the alimentary canal of the Colorado potato beetle Leptinotarsa decemlineata: structural and fuctional aspects. Cell Tissue Res. 273: 475-485.

[30] Vieillemaringe, J.; P. Duris; C. Bensch & J. Girardie. 1982. Co-localization of amines and peptides in the same median neurosecretory cells of locusts. Neuroscience 31: 237-240.

[31] Wigglesworth, V.B. 1985. Historical perspectives, p. 1-24. In G.A. Kerkut & L.I Gilbert (eds). Comprehensive Insect Physiology, Biochemistry and Pharmacology. Oxford, Pergamon Press, Vol. 7,457p.