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Histochemistry and Ultrastructure of Urocytes in the Pupae of the Stingless Bee Melipona quadrifasciata (Hymenoptera: Meliponini)

Published online by Cambridge University Press:  09 September 2013

Waléria C.A. Furtado
Affiliation:
Department of General Biology, Federal University of Viçosa, 36570-000 Viçosa, MG, Brazil
Dihego O. Azevedo
Affiliation:
Department of General Biology, Federal University of Viçosa, 36570-000 Viçosa, MG, Brazil
Gustavo F. Martins
Affiliation:
Department of General Biology, Federal University of Viçosa, 36570-000 Viçosa, MG, Brazil
José C. Zanuncio
Affiliation:
Department of Animal Biology, Federal University of Viçosa, 36570-000 Viçosa, MG, Brazil
José Eduardo Serrão*
Affiliation:
Department of General Biology, Federal University of Viçosa, 36570-000 Viçosa, MG, Brazil
*
*Corresponding author.jeserrao@ufv.br
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Abstract

The main cell types of the adult bee fat body are trophocytes and oenocytes; however, in pupae of some newly emerged bees, trophocytes are modified into cells called urocytes, which possibly function as a substitute for Malpighian tubules during metamorphosis when larval tubules are not functional and/or storage of urate salts is required. This study evaluated the morphology of urocytes in the stingless bee Melipona quadrifasciata and the possibility of maintaining these cells in primary culture. The urocytes M. quadrifasciata are white spherical cells with an irregular surface as observed by stereomicroscopy. They may be found individually or in groups associated with tracheae. Urocytes have a single, small, and spherical nucleus and cytoplasm rich in neutral polysaccharides, lipid droplets, protein, and granules containing calcium and urate salts. Our findings suggest that urocytes play a role in storage of neutral polysaccharides and calcium in M. quadrifasciata pupae and that these cells can be cultured for 72 h.

Type
Biomedical and Biological Applications
Copyright
Copyright © Microscopy Society of America 2013 

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References

Alberts, B., Bray, D., Lewis, J., Raff, M., Roberts, K. & Watson, J.D. (2010). Molecular Biology of the Cell, 5th ed. New York: Garland Science.Google Scholar
Al-Mohanna, S.Y. & Nott, J.A. (1989). Functional cytology of the hepatopancreas of Penaeus semisulcatus (Crustacea: Decapoda) during the moult cycle. Mar Biol 101, 535544.CrossRefGoogle Scholar
Chapman, R.F. (2013). The Insects: Strucuture and Function. Cambridge, New York: Cambridge University Press.Google Scholar
Costa-Leonardo, A.M., Laranjo, L.T., Janei, V. & Haifig, I. (2013). The fat body of termites: Functions and stored materials. J Insect Physiol 59(6), 577587.CrossRefGoogle ScholarPubMed
Cruz-Landim, C. (1985a). Histological and cytological studies on the fat body of the queen honeybee abdomen during the active oviposition phase. Rev Bras Biol 45, 221232.Google Scholar
Cruz-Landim, C. (1985b). Modificações das células do corpo gorduroso de rainhas de Apis mellifera L. (Hymenoptera: Apinae). Cienc & Cult 37, 471474.Google Scholar
Cruz-Landim, C. (2000). Ovarian development in Meliponine bees (Hymenoptera: Apidae): The effect of queen presence and food on worker ovary development and egg production. Genet Mol Biol 23, 8388.CrossRefGoogle Scholar
Cruz-Landim, C. (2008). Abelhas. Morfologia e Função de Sistemas. São Paulo: Editora UNESP.Google Scholar
Cruz-Landim, C. & Serrão, J.E. (1997). Ultrastructure and histochemistry of the mineral concretions in the midgut of bees (Hymenoptera: Apidae). Neth J Zool 47, 2129.Google Scholar
Dean, R.L., Locke, M. & Collins, J.V. (1985). Structure of fat body. In Comprehensive Insect Physiology, Biochemistry and Pharmacology, Kerkut, G.A. & Gilbert, L.I. (Eds.), pp. 155210. Oxford, UK: Pergamon Press.Google Scholar
Easton, C.M. & Horwath, K.L. (1994). Characterization of primary cell cultures derived from fat body of the beetle, Tenebrio molitor, and the immunolocalization of a thermal hysteresis protein in vitro . J Insect Physiol 40, 537557.CrossRefGoogle Scholar
Ehresmann, D.D., Graf, G. & Buckner, J.S. (1990). Uric acid translocation from the fat body of Manduca sexta during the pupal-adult transformation: Effects of 20-hydroxyecdysone. J Insect Physiol 36, 173180.CrossRefGoogle Scholar
Giannini, T.C., Imperatriz-Fonseca, V.L., Acosta, A.L., Alves-dos-Santos, I., Garófalo, C.A. & Saraiva, A.M. (2012). Pollination services at risk: Bee habitats will decrease owing to climate change in Brazil. Ecol Modell 244, 127131.CrossRefGoogle Scholar
Howard, B., Mitchell, P.C., Ritchie, A., Simkiss, K. & Taylor, M. (1981). The composition of intracellular granules from the metal-accumulating cells of the common garden snail (Helix aspersa). Biochem J 194, 507511.CrossRefGoogle ScholarPubMed
Hunter, W.B. (2010). Medium for development of bee cell cultures (Apis mellifera: Hymenoptera: Apidae). In vitro Cell Dev-An 46, 8386.CrossRefGoogle ScholarPubMed
Janssen, H.H. (1985). Some histological findings on the mid-gut gland of the common garden snail. Arion rufus (L.) (Syn. A. after rufus [L.], A. emporicorum Férrussac) Gastropoda: Stylommatophora. Zool Anz 215, 3351.Google Scholar
Junqueira, L.C.U. & Junqueira, L.M.M.S. (1983). Técnicas Básicas de Citologia e Histologia. São Paulo: Editora Santos.Google Scholar
Kerr, W.E., Almeida, G.A. & Nascimento, V.A. (1996). Abelha Uruçu. Biologia, Manejo e Conservação. Belo Horizonte: Fundação Acangú.Google Scholar
Kishimoto, A., Nakato, H., Izumi, S. & Tomino, S. (1999). Biosynthesis of major plasma in the primary culture of fat body cells from the silkworm, Bombyx mori . Cell Tissue Res 297, 329335.CrossRefGoogle ScholarPubMed
Kuterbach, D.A. & Walcott, B. (1986). Iron-containing cells in the honey-bee (Apis mellifera) accumulation during development. J Exp Biol 126, 389401.CrossRefGoogle ScholarPubMed
Lipovsek, S., Letofsky-Papst, I., Hofer, F., Pabst, M.A. & Devetak, D. (2012). Application of analytical electron microscopic methods to investigate the function of spherites in the midgut of the larval antlion Euroleon nostras (Neuroptera: Myrmeleontidae). Microsc Res Techniq 75, 397407.CrossRefGoogle ScholarPubMed
Lipovsek, S., Novak, T., Janzekovic, F. & Pabst, M.A. (2011). Role of the fat body in the cave crickets Troglophilus cavicola and Trolophilus neglectus (Rhaphidophoridae, Saltatoria) during overwintering. Arthropod Struct Dev 40, 5463.CrossRefGoogle ScholarPubMed
Locke, M. (1984). The structure and development of the vacuolar system in the fat body of insects. In Insect Ultrastructure, King, R.C. & Akai, H. (Eds.), vol. 2, pp. 151197. New York: Plenum Press.CrossRefGoogle Scholar
Lynn, D.E. (2001). Novel techniques to establish new insect cell lines. In Vitro Cell Dev-An 37, 319321.CrossRefGoogle ScholarPubMed
Martins, G.F., Guedes, B.A.M., Serrão, J.E., Ramalho-Ortigão, J.M., Pimenta, P.F.P., Silva, L.M. & Fortes-Dias, C.L. (2011a). Isolation, primary culture and morphological characterization of oenocytes from Aedes aegypti pupae. Tissue Cell 43, 8390.CrossRefGoogle ScholarPubMed
Martins, G.F. & Serrão, J.E. (2004). Changes in the reproductive tract of Melipona quadrifasciata anthidioides (Hymenoptera: Apidae: Meliponini) queen after mating. Sociobiology 44, 241254.Google Scholar
Martins, G.F., Serrão, J.E., Ramalho-Ortigão, J.M. & Pimenta, P.F.P. (2011b). A comparative study of fat body morphology in five mosquito species. Mem I Oswaldo Cruz 106, 742747.CrossRefGoogle ScholarPubMed
Martins, G.F., Serrão, J.E., Ramalho-Ortigão, J.M. & Pimenta, P.F.P. (2011c). Histochemical and ultrastructural studies of the mosquito Aedes aegypti fat body. Effects of aging and diet type. Microsc Res Techniq 74, 10321039.CrossRefGoogle ScholarPubMed
Michener, C.D. (2000). The Bees of the World. Baltimore, MD: The John Hopkins University Press.Google Scholar
Moure, J.S., Urban, D. & Melo, G.A.R. (2008). Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region. Curitiba, Brazil: Sociedade Brasileira de Entomologia.Google Scholar
Nelson, D.E. & Cox, M.M. (2008). Lehninger's Principles of Biochemistry. New York: W.H. Freeman and Company.Google Scholar
Paes-de-Oliveira, V.T. & Cruz-Landim, C. (2003). Size of fat body trophocytes and the ovarian development in workers and queens of Melipona quadrifasciata anthidioides . Sociobiology 41, 701709.Google Scholar
Paes-de-Oliveira, V.T. & Cruz-Landim, C. (2006). Histological and ultrastructural aspects of the fat body in virgin and physogastric queens of Melipona quadrifasciata anthidioides Lepeletier, 1836 (Hymenoptera, Apidae, Meliponini). Braz J Morphol Sci 23, 385392.Google Scholar
Pascini, T.V., Martins, G.F., Serrão, J.E., Vilela, E.F., Albeny, D.S. & Ramalho-Ortigão, J.M. (2011). Changes in the fat body during the post-embryonic development of the predator Toxorhynchites theobaldi (Dyar & Knab) (Diptera: Culicidae). Neotrop Ent 40, 456461.CrossRefGoogle ScholarPubMed
Pearse, A.G.E. (1985). Histochemistry Theoretical and Applied, 4th ed. London: Churchill Livingstone.Google Scholar
Rachinsky, A. & Hartfelder, K. (1998). In vitro biosynthesis of juvenile hormone in larval honey bees: Comparison of six media. In Vitro Cell Dev-An 34, 646648.CrossRefGoogle ScholarPubMed
Roma, G.C., Camargo-Mathias, M.I. & Bueno, O.C. (2006). Fat body in some genera of leaf-cutting ants (Hymenoptera: Formicidae). Proteins, lipids and polysaccharides detection. Micron 37, 234242.CrossRefGoogle ScholarPubMed
Roma, G.C., Camargo-Mathias, M.I. & Bueno, O.C. (2010). Morpho-physiological analysis of the insect fat body: A review. Micron 41, 395401.CrossRefGoogle ScholarPubMed
Rossel, R.C. & Wheeler, D.E. (1995). Storage function and ultrastructure of the adult fat body in workers of the ant Camponotus festinatus (Bukley) (Hymenoptera: Formicidae). Int J Insect Morphol Embryol 24, 413426.CrossRefGoogle Scholar
Sadrud-Din, S., Loeb, M.J. & Hakim, R.S. (1996). In vitro differentiation of isolated stern cells from the midgut of Manduca sexta larvae. J Exp Biol 199, 319325.CrossRefGoogle Scholar
Snodgrass, R.E. (1935). Principles of Insect Morphology. New York: McGraw-Hill.Google Scholar
Snodgrass, R.E. (1956). Anatomy of the Honey Bee. Ithaca, NY: Comstock Publishing Associates.Google Scholar
Sobotnik, J., Weyda, F., Hanus, R., Cvacka, J. & Nevbesarova, J. (2006). Fat body of Prorhinotermes simplex (Isoptera: Rhinotermitidae): Ultrastructure, inter-caste differences and lipid composition. Micron 37, 648656.CrossRefGoogle ScholarPubMed
Stefanini, M., Demartino, C. & Zamboni, L. (1967). Fixation of ejaculated spermatozoa for electron microscopy. Nature 216, 173174.CrossRefGoogle ScholarPubMed
Wren, H.N. (1991). TEM evidence of urocytes in the cockroach fat body. Tissue Cell 23, 291292.CrossRefGoogle ScholarPubMed
Zara, F.J. & Caetano, F.H. (2004). Ultramorphology and histochemistry of fat body cells from last instar larval of the Pachycondyla (=Neoponera) villosa (Fabricius) (Formicidae: Ponerinae). Braz J Biol 64, 725735.CrossRefGoogle ScholarPubMed