The Spherocrystals in the Tubule Epithelial Cells and Ultrastructure of the Malpighian Tubules of Adult Isophya nervosa (Orthoptera, Tettigoniidae)

Year 2020, , 630 - 644, 01.09.2020

Damla Amutkan Mutlu , Zekiye Suludere

https://doi.org/10.35378/gujs.690948

Cited By: 3

Abstract

The excretory system in insects consists of Malpighian tubules (MTs) which are responsible for osmoregulation. The functions of the MTs are the removal of the last products of metabolism and the transfer of the toxic compounds into the hindgut. The MTs of the insects vary structurally. In this study, the MTs of Isophya nervosa Ramme, 1951, which is a species that belongs to Orthoptera order, were investigated by light and electron microscopes. Adult individuals of Isophya nervosa were collected in Kızılcahamam, Ankara in 2017 and 2018. Extracted MTs were fixed in Formaldehyde for light microscopy, in glutaraldehyde for electron microscopes. They were examined and photographed after dehydration, blocking, sectioning and staining processes were completed. This species has a great number of MTs. One end of the MTs in this species is attached to the ileum and the other closed end is free in hemolymph. The outer surface of the cells is surrounded by muscle layers and trachea. There are microvilli on the apical region of cells. The lumen is covered with a monolayer cuboidal epithelium. Numerous concentrically layered spherocrystals in different shapes were observed in the cells. When the chemical compositions of these spherocrystals were analyzed by SEM-EDX system, it was seen that the contents of them were different ions such as iron (Fe), carbon (C), phosphorus (P), magnesium (Mg), sulfur (S), calcium (Ca), and manganese (Mn). 

Keywords

Elemental Analysis, SEM-EDX, Spherocrystal, Excretory System, Histology

Supporting Institution

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Project Number

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Thanks

We express our thanks to Prof. Dr. Mustafa ÜNAL (Bolu Abant İzzet Baysal University, Faculty of Arts and Sciences, Biology Department) for helping the species diagnosis and to Gazi University Academic Writing and Research Center for their help and support in the proofreading of the current study. This study is a part of Damla AMUTKAN MUTLU’s PhD thesis. The Malpighian tubules is presented as an oral presentation in 1st International Eurasian Conference on Biological and Chemical Sciences, 26-27 April 2018 in Ankara, Turkey.

References

• Acar, G., “Morphology and Histology of Malpighian Tubules of Melanogryllus desertus (Pallas, 1771) (Orthoptera: Gryllidae)”, Msc. Thesis, Ege University Institution of Science, İzmir, 1-23, (2009) (in Turkish).
• Savage, A.A., “The development of the Malpighian tubules of Schistocerca gregaria (Orthoptera)”, Querterly Journal of Microscopical Science, 97(4):599-615, (1956).
• Gautam, N.M., Tapadia, M.G., “Overview of Malpighian tubules development and function in Drosophila melanogaster”, Journal of Scientific Research, 58:87-98, (2014).
• Ramsay, J.A., “The excretory system of the stick insect, Dixippus morosus (Orthoptera, Phasmidae)”, Journal of Experimental Biology, 32:183-199, (1955).
• Maddrell, S.H.P., “Secretion by the Malpighian tubules of Rhodnius. The movements of ions and water”, The Journal of Experimental Biology, 51:71-97 (1969).
• Jarial, M.S., “Fine structure of Malpighian tubules Grylloblatta compodeiformis (Orthoptera: Grylloblattidae)”, Transactions of the American Microscopical Society, 109(4):329-341 (1990).
• Gullan, P.J. Cranston, P.S., “Böcekler: Entomolojinin Ana Hatları”. In A. Gök (Ed.). Nobel Yayınevi (2012) (in Turkish).
• Pal, R., Kumar, K., “Ultrastructural features of the larval Malpighian tubules of the flesh fly Sarcophaga ruficornis (Diptera: Sarcophagidae)”, International Journal of Tropical Insect Science, 32(3):166-172, (2012).
• Zhong, H., Zhang, Y., Wei, C., “Morphology and ultrastructure of the Malpighian tubules in Kolla paulula (Hemiptera: Cicadellidae)”, Zoologischer Anzeiger-A Journal of Comparative Zoology, 257:22-28, (2015).
• Polat, I., “The Ultrastructural Features of the Digestive, Excretory, Female and Male Reproductive Systems of Poecilimon cervus Karabag, 1950”, Ph.D Thesis, Gazi University Institution of Science, Ankara, 1-187, (2016) (in Turkish).
• Silva, J.R., Amaral, D.T., Viviani, V.R., “Comparison of the Malpighian tubules and fat body transcriptional profiles of Zophobas morio larvae (Coleoptera: Tenebrionidae)”, Comparative Biochemistry and Physiology-Part D, 29:95-105, (2019).
• Nocelli, R., Cintra-Socolowski, P., Roat, T., Silva-Zacarin, E., Malaspina, O., “Comparative physiology of Malpighian tubules: form and function”, Insect Physiology, 2016:13-23, (2016).
• Delakorda, S.L., Letofsky-Papst, I., Novak, T., Hofer, F., Pabst, M.A., “Structure of the Malpighian tubule cells and annual changes in the structure and chemical composition of their spherites in the cave cricket Troglophilus neglectus Krauss, 1878 (Raphidophoridae, Saltatoria)”, Arthropod Structure and Development, 38:315-327, (2009).
• Gonçalves, W.G., Fialho, M.D.C.Q., Azevedo, D.O., Zanuncio, J.C., Serrão, J.E., “Ultrastructure of the excretory organs of Bombus morio (Hymenoptera: Bombini): bee without rectal pads”, Microscopy and Microanalysis, 20(1):285-295, (2014).
• Lipovšek, S., Letofsky‐Papst, I., Hofer, F., Pabst, M.A., Devetak, D., “Application of analytical electron microscopic methods to investigate the function of spherites in the midgut of the larval antlion Euroleon nostras (Neuroptera: Myrmeleontidae)”, Microscopy Research and Technique, 75(4): 397-407, (2012).
• Ballan‐Dufrançais, C., “Localization of metals in cells of pterygote insects”, Microscopy Research and Technique, 56(6):403-420, (2002).
• Fontanetti, C.S., Tiritan, B., Camargo-Mathias, M.I., “Mineralized bodies in the fat body of Rhinocricus padbergi (Diplopoda)”, Journal of Morphological Sciences, 23(3-4):487-493, (2006).
• Roeder, K.D., College, T., “Insect Physiology”. Chapmen&Hall Ltd, London, 387-407 p, (1953).
• Beams, H.W., Tahmisian, T.N., Devine, R.L., “Electron microscope studies on the cells of the Malpighian tubules of the grasshopper (Orthoptera, Acrididae)”, The Journal of Biophysical and Biochemical Cytology, 1(3):197-212, (1955).
• Maddrell, S.H.P., “Fluid secretion by the Malpighian tubules of insects”, Philosophical Transactions of the Royal Society of London B, 262:197-207, (1971).
• Martini, S.V., Nascimento, S.B., Morales, M.M., “Rhodnius prolixus Malpighian tubules and control of diuresis by neurohormones”, Annals of the Brazilian Academy of Science, 79(1):87-95, (2007).
• Giglio, A., Perrotta, I.D., Brandmayr, P., “Exosomes: Ultrastructural evidence in epithelial cells of Malpighian tubules”, Micron, 100:34-37, (2017).
• Nation, J.L., “Insect Physiology and Biochemistry”, New York, CRC Press, 485 p, (2002).
• Pacheco, C.A., Alevi, K.C.C., Ravazi, A., de Azeredo Oliveira, M.T.V., “Review: Malpighian tubules, an essential organ for insects”, Entomology, Ornithology and Herpetology, 3(2):1-3, (2014).
• Amutkan, D., Suludere, Z., Candan, S., “Ultrastructure of digestive canal of Graphosoma lineatum (Linnaeus, 1758) (Heteroptera: Pentatomidae)”, Journal of the Entomological Research Society, 17(3):75-96, (2015).
• Bradley, T.J., Stuart, A.M., Satir, P., “The ultrastructure of the larval Malpighian tubules of a saline-water mosquito” Tissue and Cell, 14:59-773, (1982).
• Chapman, R.F., “The Insects: Structure and Function” 4th ed., Cambridge University Press, London, 770 p, (1998).
• Denholm, B., Skaer, H., “Development of the Malpighian Tubules in Insects”, In L.I. Gilbert, K. Iatrou, S.S. Gill (Eds.). Comprehensive Molecular Insect Science, UK, University of Cambridge, 291-314 pp, (2005).
• Gillott, C., “Entomology”, Springer Science & Business Media, (2005).
• Wigglesworth, V.B., “The Principles of Insect Physiology”, Methuen and Co, London, 546 p, (1965).
• Bradley, T.J., “The Excretory System, Structure and Physiology” 1st ed., In G.A. Kerkut, L.I. Gilbert (Eds.). Comprehensive Insect Physiology, Biochemistry and Pharmacology, Pergamon Press, London, 421-465 pp, (1985).
• Green, L.F.B., “Cryptonephric Malpighian tubule system in a dipteran larva, the New Zealand glow-worm, Arachnocampa luminosa (Diptera: Mycetophilidae): A structural study”, Tissue and Cell, 12:41-151, (1980).
• Wall, B.J., Oschman, J.L., Schmidt, B.A., “Morphology and function of Malpighian tubules and associated structures in the cockroach, Periplaneta Americana”, Journal of Morphology, 146(2):265-306, (1975).
• Srivastava, U.S., Bahadur, I., “The development of the Malpighian tubules in Dysdercus koenigi (Hemiptera: Pyrrhocoridae)”, Quarterly Journal of Microscopical Science, 3(59):347-360, (1961).
• Mello, M.L.S., Dolder, H., “Fine structure of the Malpighian tubes in the blood-sucking insect, Triatoma infestans Klug”, Protoplasma, 93(2-3):275-288, (1977).
• Arab, A., Caetano, F.H., “Segmental specializations in the Malpighian tubules of the fire ant Solenopsis saevissima Forel 1904 (Myrmicinae): an electron microscopical study”, Arthropod Structure & Development, 30(4):281-292, (2002).
• Liu, L., Hua, B.Z., “Ultrastructure of the larval Malpighian tubules in Terrobittacus implicatus (Mecoptera: Bittacidae)”, Protoplasma, 255(4):1121-1128, (2018).
• Taylor, H.H., “Structure and functional changes in the Malpighian tubules of Carausius morosus during dehydration and starvation”, Zeitschrift für Zellforschung und Mikroskopische Anatomie, 141(4):479-492, (1973).
• Satmary, W.M., Bradley, T.J., “The distribution of cell types in the Malpighian tubules of Aedes taeniorhynchus (Wiedemann) (Diptera: Culicidae)”, International Journal of Insect Morphology and Embryology, 13:209-214, (1984).
• Yu, C.H., “Ultrastructure of the Malpighian tubule cells in the mosquito larvae, Culex pipiens pallens”, Korean Journal of Entomology, 29:141-147, (1999).
• Yu, C.H., “Ultrastructure of the Malpighian tubule cells in the mosquito larvae, Anopheles sinesis”, Entomological Research, 33(3):151-159, (2003).
• Alkassis, W., Schoeller-Raccaud, J., “Ultrastructure of the Malpighian tubules of blowfly larva, Calliphora erythrocephala Meigen (Diptera Calliphoridae)”, International Journal of Insect Morphology and Embryology, 13:215-231, (1984).
• Pinheiro, D.D.O., Conte, H., Gregorio, E.A., “Spherites in the midgut epithelial cells of the sugarcane borer parasitized by Cotesia flavipes”, Biocell, 32(1):61-67, (2008).
• Santos, H.P., Rost-Roszkowska, M., Vilimova, J., Serrão, J.E., “Ultrastructure of the midgut in Heteroptera (Hemiptera) with different feeding habits”, Protoplasma, 254(4):1743-1753, (2017).
• Krueger, R.A., Broce, A.B., Hopkins, T.L., “Dissolution of granules in the Malpighian tubules of Musca autumnalis Degeer, during mineralization of the puparium”, Journal of Insect Physiology, 33(4):255-263, (1987).
• Krueger, R.A., Broce, A.B., Hopkins, T.L., Kramer, K.J., “Calcium transport from Malpighian tubules to puparial cuticle of Musca autumnalis”, Journal of Comparative Physiology B, 158(4):413-419, (1988).
• Lipovšek, S., Letofsky-Papst, I., Hofer, F., Pabst, M.A., “Seasonal-and age-dependent changes of the structure and chemical composition of the spherites in the midgut gland of the harvestmen Gyas annulatus (Opiliones)”, Micron, 33(7-8):647-654, (2002).
• Stewart, A.D., Anand, R.R., Laird, J.S., Verrall, M., Ryan, C.G., de Jonge, M.D., Paterson, D., Howard, D.L., “Distribution of metals in the termite Tumulitermes tumuli (Froggatt): two types of Malpighian tubule concretion host Zn and Ca mutually exclusively”, PLoS One, 6(11):1-7, (2011).
• Tejeda-Guzmán, C., Rosas-Arellano, A., Kroll, T., Webb, S.M., Barajas-Aceves, M., Osorio, B., Missirlis, F., “Zinc storage granules in the Malpighian tubules of Drosophila melanogaster”, BioRxiv, 159558, (2017).
• Tejeda-Guzmán, C., Rosas-Arellano, A., Kroll, T., Webb, S. M., Barajas-Aceves, M., Osorio, B., Missirlis, F., “Biogenesis of zinc storage granules in Drosophila melanogaster”, Journal of Experimental Biology, 221(6):1-13 jeb168419, (2018).
• Wessing A, Zierold K., “Metal-salt feeding causes alterations in concretions in Drosophila larval Malpighian tubules as revealed by x-ray-microanalysis”, Journal of Insect Physiology, 38(8):623-632, (1992).
• Przybyłowicz, W.J., Przybyłowicz, J.M., Migula, P., Głowacka, E., Nakonieczny, M., Augustyniak, M., “Functional analysis of metals distribution in organs of the beetle Chrysolina pardalina exposed to excess of nickel by Micro-PIXE”, Nuclear Instruments & Methods in Physics Research Section B-Beam Interactions with Materials and Atoms, 210:343-348, (2003).
• Tylko, G., Borowska, J., Banach, Z., Pyza, E., Przybyłowicz, W.J., Mesjasz-Przybyłowicz, J. “Co-localization of copper, zinc and lead with calcium in their accumulation sites in the housefly's abdomen by micro-PIXE”, Microchimica Acta. 155:301-304, (2006).
• Dow, J.A., “The essential roles of metal ions in insect homeostasis and physiology”, Current Opinion in Insect Science, 23:43-50, (2017).
• Köhler, H.R., Körtje, K.H., Alberti, G., “Content, absorption quantities and intracellular storage sites of heavy metals in Diplopoda (Arthropoda)”, BioMetals, 8(1):37-46, (1995).
• Llorens, J.V., Metzendorf, C., Missirlis, F., Lind, M.I., “Mitochondrial iron supply is required for the developmental pulse of ecdysone biosynthesis that initiates metamorphosis in Drosophila melanogaster”, JBIC Journal of Biological Inorganic Chemistry, 20(8):1229-1238, (2015).