Morphology and Ultrastructure of the Nymphal Malpighian Tubules of Conocephalus fuscus fuscus (Fabricius, 1793) (Orthoptera, Tettigoniidae)

Abstract

Malpighian tubules are the main osmoregulatory structures in insects. The primary task of the insects’ Malpighian tubules is to remove the nitrogenous wastes and other remained of metabolites. In this study, the nymphal Malpighian tubules of Conocephalus fuscus fuscus were studied with optical and transmission electron microscopy. The wall of each Malpighian tubule is comprised of a single layer of cells. The Malpighian tubules in nymphal C. fuscus fuscus have 3 types of epithelial cells. The first group of the cells outnumbers the other groups of cells and they have long microvilli at the apical side of the plasma membrane. The second group of the cells has electron-dense cytoplasm. The microvilli of the second group of the cells are shorter than those of the first group of the cells. The cytoplasm of the epithelial cells of the third group is so electron-lucent. These significant differences in the fine structure of the tubule cells were compared with the other Hexapoda orders. The general composition of the Malpighian tubules of the nymphal C. fuscus fuscus is generally similar, despite some histological differences compared to those of other species.

Keywords

• Excretory system
• Histology
• Optical microscope
• Transmission electron microscope
• Insect

References

1. [1] Ragge, D. R. Grasshoppers, Crickets and Cockroaches of the British Isles, F Warne and Co, London, (1965).
2. [2] Budrys, E., Našlėnienė, A. and Winkler, C., “First records of Conocephalus fuscus and Omocestus rufipes (Orthoptera: Conocephalidae, Acrididae) in Lithuania”, New and Rare for Lithuania Insect Species, 27:12-14, (2015).
3. [3] Sadiq, S., Panhwar, W. A., Sultana, R., Saeed, M., Wagan, S. A. and Ahmed, S., “New record of Conocephalus (Anisoptera) fuscus (Fabricius, 1793) (Conocephalinae: Tettigoniidae: Orthoptera) from Pakistan”, J Entomol Zool Stud, 5(3):1431-1434, (2017).
4. [4] Ruchin, A. B. and Mikhailenko, A. P., “Fauna of mantids and orthopterans (Insecta: Mantodea, Orthoptera) of the Mordovia State Nature Reserve, Russia”, Biodivers J Biol Divers, 19(4):1194-1206, (2018).
5. [5] Arab, A. and Caetano, F. H., “Segmental specializations in the Malpighian tubules of the fire ant Solenopsis saevissima Forel 1904 (Myrmicinae): an electron microscopical study”, Arthropod Struct. Dev., 30:281-292, (2002).
6. [6] Rakitov, R. A., “Structure and function of the Malpighian tubules, and related behaviors in juvenile Cicadas: Evidence of homology with Spittlebugs (Hemiptera: Cicadoidea and Cercopoidea)”, Zool. Anz., 241:117-130, (2002).
7. [7] Cordeiro, B. A., Tibúrcio, V. H. S., Hallwass, M., Paes, H. C., Ribeiro, B. M. and Báo, S. N., “Structural and ultrastructural alterations of Malpighian tubules of Anticarsia gemmatalis (Hübner) (Lepidoptera: Noctuidae) larvae infected with different Anticarsia gemmatalis multiple nucleopolyhedrovirus (AgMNPV) recombinant viruses”, J. Invertebr. Pathol., 98:7-19, (2008).
8. [8] Dow, J. A. T., “Insights into the Malpighian tubule from functional genomics”, J. Exp. Biol., 212:435-445, (2009).

9. [9] Wu, G. X., Gao, X., Ye, G. Y., Li, K., Hu, C. and Cheng, J. A., “Ultrastructural alterations in midgut and Malpighian tubules of Boettcherisca peregrina exposure to cadmium and copper”, Ecotoxicol. Environ. Saf., 72:1137-1147, (2009).
10. [10] King, B. and Denholm, B., “Malpighian tubule development in the red flour beetle (Tribolium castaneum)”, Arthropod Struct. Dev., 43:605-613, (2014).
11. [11] Zhong, H., Zhang, Y. and Wei, C., “Morphology and ultrastructure of the Malpighian tubules in Kolla paulula (Hemiptera: Cicadellidae)”, Zool. Anz., 257:22-28, (2015).
12. [12] Giglio, A., Perrotta, I. D. and Brandmayr, P., “Exosomes: Ultrastructureal evidence in epithelial cells of Malpighian tubules”, Micron, 100:34-37, (2017).
13. [13] Silva, J. R., Amaral, D. T. and Viviani, V. R., “Comparison of the Malpighian tubules and fat body transcriptional profiles of Zophobas morio larvae (Coleoptera: Tenebrionidae)”, Comp. Biochem. Physiol. D., 29:95-105, (2019).
14. [14] Roeder, K. D. and College, T., Insect Physiology, London, UK: Chapman&Hall Ltd., (1953).
15. [15] Martini, S. V., Nascimento, S. B. and Morales, M. M., “Rhodnius prolixus Malpighian tubules and control of diuresis by neurohormones”, An. Acad. Bras. Ciênc., 79(1):87-95, (2007).
16. [16] Lipovšek, S., Janžekovič, F. and Novak, T., “Ultrastructure of fat body cells and Malpighian tubule cells in overwintering Scoliopteryx libatrix (Noctuoidea)”, Protoplasma, 254:2189-2199, (2017).
17. [17] Denholm, B. and Skaer, H., Development of the Malpighian Tubules in Insects, Cambridge, UK: University of Cambridge (2005).
18. [18] Pacheco, C. A., Alevi, K. C. C., Ravazi, A. and Oliveira, M. T. V. A., “Malpighian tubule, an essential organ for insects,” Entomol. Ornithol. Herpetol., 3(122):doi:10.4172/2161-0983.1000122, (2014).
19. [19] Maddrell, S. H. P. and Gardiner, B. O. C., “The passive permeability of insect Malpighian tubules to organic solutes”, J. Exp. Biol., 60:641-652, (1974).
20. [20] Maddrell, S. H. and Gardiner, B. O., “Excretion of alkaloids by Malpighian tubules of insects”, J. Exp. Biol., 64(2):267-281, (1976).
21. [21] Maddrell, S. H. P., “The functional design of the insect excretory system”, J. Exp. Biol., 90:1-15, (1981).
22. [22] Gaertner, L. S., Murray, C. L. and Morris, C. E., “Transepithelial transport of nicotine and vinblastine in isolated Malpighian tubules of the tobacco hornworm (Manduca sexta) suggests a P-glycoprotein-like mechanism”, J. Exp. Biol., 201(18):2637-2645, (1998). [23] Torrie, L. S., Radford, J. C., Southall, T. D., Kean, L., Dinsmore, A. J., Davies, S. A. and Dow, J. A., “Resolution of the insect ouabain paradox”, Proc. Nat. Acad. Sci., 101(37):13689-13693, (2004).
23. [24] Ruiz-Sanchez, E., Van Walderveen, M. C., Livingston, A. and O’Donnell, M. J., “Transepithelial transport of salicylate by the Malpighian tubules of insects from different orders”, J. Insect Physiol, 53(10):1034-1045, (2007).
24. [25] Gautam, N. K. and Tapadia, M. G., “Overview of Malpighian tubules development and function in Drosophila melanogaster”, J. Sci. Res., 58:87-98, (2014).
25. [26] Hazelton, S. R., Felgenhauer, B. E. and Spring, J. H., “Ultrastructural changes in the Malpighian tubules of the house cricket, Acheta domesticus, at the onset of diuresis: a time study”, J. Morphol., 247(1):80-92 (2001).
26. [27] Gillott, C., Entomology, The Netherlands: Springer Science & Business Media (2005).
27. [28] Nocelli, R., Cintra-Socolowski, P., Roat, T., Silva-Zacarin, E. and Malaspina, O., “Comparative physiology of Malpighian tubules: form and function”, Insect. Physiol., 2016(6):13-23, (2016).
28. [29] Polat, I., “The ultrastructural features of the digestive, excretory, female and male reproductive systems of Poecilimon cervus Karabag, 1950”, Phd. thesis, Gazi University Institution of Science, Ankara, 1-187 (2016).
29. [30] Delakorda, S. L., Letofsky-Papst, I., Novak, T., Hofer, F. and 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 Struct. Dev., 38:315-327, (2009).
30. [31] Pal, R. and Kumar, K., “Ultrastructural features of the larval Malpighian tubules of the flesh fly Sarcophaga ruficornis (Diptera: Sarcophagidae)”, Int. J. Trop. Insect Sci., 32(3):166-172, (2012).
31. [32] Jarial, M.S., “Fine structure of Malpighian tubules Grylloblatta compodeiformis (Orthoptera: Grylloblattidae)”, T. Am. Microsc. Soc., 109(4):329-341, (1990).
32. [33] Beams, H. W., Tahmisian, T. N. and Devine, R. L., “Electron microscope studies on the cells of the Malpighian tubules of the grasshopper (Orthoptera, Acrididae)”, J. Biophys. Biochem. Cytol., 1(3):197-212, (1955).
33. [34] Prado, M. A., Montuenga, L. M., Villaro, A. C., Etayo, J. C., Polak, J. M. and Sesma, M. P., “A novel granular cell type of locust malpighian tubules: Ultrastructural and immunocytochemical study”, Cell Tissue Res., 268(1):123-130, (1992).
34. [35] Da Cunha, F. M., Caetano, F. H., Wanderley-Teixeira, V., Torres, J. B., Teixeira, A. A. and Alves, L. C., “Ultra-structure and histochemistry of digestive cells of Podisus nigrispinus (Hemiptera: Pentatomidae) fed with prey reared on bt-cotton”, Micron, 43(2):245-250, (2012).
35. [36] Liu, L. and Hua, B. Z., “Ultrastructure of the larval Malpighian tubules in Terrobittacus implicatus (Mecoptera: Bittacidae)” Protoplasma, 255(4):1121-1128, (2018).
36. [37] Berridge, M. J. and Oschman, J. L., “A structural basis for fluid secretion by Malpighian tubules”, Tissue Cell, 1(2):247-272, (1969).
37. [38] Ruiz-Sanchez, E., O’Donnell, M. J. and Donini, A., “Secretion of Na+, K+ and fluid by the Malpighian (renal) tubule of the larval cabbage looper Trichoplusia ni (Lepidoptera: Noctuidae)”, J. Insect Physiol., 82:92-98, (2015).