Skip to main content
Log in

Ultrastructure of fat body cells and Malpighian tubule cells in overwintering Scoliopteryx libatrix (Noctuoidea)

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

The herald moths, Scoliopteryx libatrix, overwinter in hypogean habitats. The ultrastructure of their fat body (FB) cells and Malpighian tubule (MT) epithelial cells was studied by light microscopy and transmission electron microscopy, and essential biometric and biochemical measurements were performed. The FB was composed of adipocytes and sparse urocytes. The ultrastructure of both cells did not change considerably during this natural starvation period, except for rough endoplasmic reticulum (rER) which became more abundant in March females. In the cells, the reserve material consisted of numerous lipid droplets, glycogen rosettes, and protein granula. During overwintering, the lipid droplets diminished, and protein granula became laminated. The MTs consisted of a monolayer epithelium and individual muscle cells. The epithelial cells were attached to the basal lamina by numerous hemidesmosomes. The apical plasma membrane was differentiated into numerous microvilli, many of them containing mitochondria. Nuclei were surrounded by an abundant rER. There were numerous spherites in the perinuclear part of the cells. The basal plasma membrane formed infoldings with mitochondria in between. Nuclei were located either in the basal or in the central part of the cells. During overwintering, spherites were gradually exploited, and autophagic structures appeared: autophagosomes, autolysosomes, and residual bodies. There were no statistical differences between the sexes in any measured biometric and biochemical variables in the same time frames. The energy-supplying lipids and glycogen, and spherite stores were gradually spent during overwintering. In March, the augmented rER signified the intensification of synthetic processes prior to the epigean ecophase.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Arrese EL, Soulages JL (2010) Insect fat body: energy, metabolism, and regulation. Annu Rev Entomol 55:207–225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arrese EL, Canavoso LE, Jouni ZE, Pennington JE, Tsuchida K, Wells MA (2001) Lipid storage and mobilization in insects: current status and future directions. Insect Biochem Mol Biol 31:7–17

    Article  CAS  PubMed  Google Scholar 

  • Ballan-Dufrancais C (2002) Localization of metals in cells of pterygote insects. Microsc Res Techniq 56:403–420

    Article  CAS  Google Scholar 

  • Beyenbach KW, Skaer H, Dow JAT (2010) The developmental, molecular, and transport biology of Malpighian tubules. Annu Rev Entomol 55:351–374

    Article  CAS  PubMed  Google Scholar 

  • Bourne JD, Cherix D (1978) Note sur l'écophase souterraine de Triphosa dubitata L.(Lep., Geometridae) et Scoliopteryx libatrix L. (Lep., Noctuiidae). Bull Soc Vaudoise Sc Nat 354(74):147–156

    Google Scholar 

  • Bouvet Y, Turquin M-J, Bornard C, Desvignes S, Notteghem P (1974) Étude des déclencheurs visuels intervenant lors de la pénétration souterraine de Scoliopteryx libatrix L. et Triphosa dubitata L. (Lépidoptères trogloxènes). Ann Spéléol 29(2):229–236

    Google Scholar 

  • Bradle TJ (1985) The excretory system: structure and physiology. In: Kerkut GA, Chopard L (eds) La biologie des Orthoptères. Lechevalier, Paris, p 541

    Google Scholar 

  • Bradley TJ (2003) Excretion. In: Resh VH, Cardé RT (eds) Encyclopaedia of insects. Academic Press, Elsevier Science, San Diego, pp 380–386

    Google Scholar 

  • Chapman RF (2008) The insects: structure and function. Cambridge University Press, New York, pp 478–508

    Google Scholar 

  • Christian E, Moog O (1982) Zur Frage der ökologischen Klassifikazion der Kavernikolen am Beispiel der Höhlen-Schmetterlinge Österreichs. Zool Anz 5(6):382–392

    Google Scholar 

  • Cohen E (2003) Fat body. In: Resh VH, Cardé RT (eds) Encyclopedia of insects. Academic, Amsterdam, pp 407–409

    Google Scholar 

  • Dow JAT (2009) Insights into the Malpighian tubule from functional genomics. J Exp Biol 212:435–445

    Article  CAS  PubMed  Google Scholar 

  • Fibiger M, Hacker HH (2005) Systematic list of Noctuoidea of Europe. Esperiana Schwanfeld Bucherei zur Entomologie 11:93–205

    Google Scholar 

  • Furtado WCA, Azevedo DO, Martins GF, Zanuncio JC (2013) Histochemistry and ultrastructure of urocytes in the pupae of the stingless bee Melipona quadrifasciata (Hymenoptera: Meliponini). Microsc Microanal 19:1502–1510

    Article  CAS  PubMed  Google Scholar 

  • Hahn DA, Denlinger DL (2011) Energetics of insect diapause. Annu Rev Entomol 56:103–121

    Article  CAS  PubMed  Google Scholar 

  • Hazelton SR, Felgenhauer BE, Spring JH (2001) Ultrastructural changes in the Malpighian tubules of the house cricket, Acheta domesticus, at the onset of diuresis: a time study. J Morphol 247:80–92

    Article  CAS  PubMed  Google Scholar 

  • Kalender Y, Kalender S, Candan S (2002) Fine structure of Malpighian tubules in the Agrotis segetum (Lepidoptera: Noctuidae) pupae. Acta Zool Bulg 54:87–96

    Google Scholar 

  • Kates M (1991) Techniques in Lipidology. Elsevier, Amsterdam

    Google Scholar 

  • Keeley LL (1985) Physiology and biochemistry of the fat body. Structure of the fat body. In: Kerkut, GA, Gilbert LI (Eds.), Comprehensive insect physiology and pharmacology. Integument, respiration and circulation 3. Pergamon Press, Oxford, pp. 211–248

  • Klionsky DJ, Abdalla FC, Zuckerbraun B (2012) Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8(4):445–544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lipovšek S, Novak (2016) Autophagy in the fat body cells of the cave cricket Troglophilus neglectus Krauss, 1878 (Rhaphidophoridae, Saltatoria) during overwintering. Protoplasma 253:457–466

    Article  PubMed  Google Scholar 

  • Lipovšek S, Letofsky-Pabst I, Novak T, Hofer F, Pabst MA (2009) 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 (Rhaphidophoridae, Saltatoria). Arthropod Struct Dev 38:315–327. doi:10.1016/j.asd.2009.02.001

    Article  Google Scholar 

  • Lipovšek S, Novak T, Janžekovič F, Pabst MA (2011) Role of the fat body in the cave crickets Troglophilus cavicola and Troglophilus neglectus (Rhaphidophoridae, Saltatoria) during overwintering. Arthropod Struct Dev 40(1):54–63

    Article  PubMed  Google Scholar 

  • Lipovšek S, Novak T, Janžekovič F, Leitinger G (2015) Changes in the midgut diverticula in the harvestmen Amilenus aurantiacus (Phalangiidae, Opiliones) during winter diapause. Arthropod Struct Dev. doi:10.1016/j.asd.2014.12.002

  • Martoja R, Ballan-Dufrançais C (1984) The ultrastructure of the digestive and excretory organs. In: King RC, Akai H (eds) Insect ultrastructure. Plenum, New York, pp 199–268

    Chapter  Google Scholar 

  • Mizushima N (2007) Autophagy: process and function. Genes Dev 21:2861–2873

    Article  CAS  PubMed  Google Scholar 

  • Mizushima N, Klionsky DJ (2007) Protein turnover via autophagy: implications for metabolism. Annu Rev Nutr 27:19–40

    Article  CAS  PubMed  Google Scholar 

  • Motas C, Decou V, Burghele A (1967) Sur l’association pariétale des grottes d’Oltenie (Roumanie). Ann Spéléol 22(3):475–522

    Google Scholar 

  • Novak T, Perc M, Lipovšek S, Janžekovič F (2012) Duality of terrestrial subterranean fauna. Int J Speleol 41(2):181–188

    Article  Google Scholar 

  • Novak T, Janžekovič F, Lipovšek S (2013) Contribution of non-troglobiotic terrestrial invertebrates to carbon input in hypogean habitats. Acta Carsologica 42:301–309

    Article  Google Scholar 

  • Paes de Oliveira VT, Cruz-Landim C (2003) Morphology and function of insect fat body cells: a review. Biociências, Porto Alegre 11:195–205

    Google Scholar 

  • Pal R, Kumar K (2013) Malpighian tubules of adult flesh fly, Sarcophaga ruficornis fab. (Diptera: Sarcophagidae): an ultrastructural study. Tissue Cell 45(5):312–317

    Article  PubMed  Google Scholar 

  • Pigino G, Migliorini M, Paccagnini E, Bernini F, Leonzio C (2005) Fine structure of the midgut and Malpighian papillae in Campodea (Monocampa) quilisi Silvestri, 1932 (Hexapoda, Diplura) with special reference to the metal composition and physiological significance of midgut intracellular electron-dense granules. Tissue Cell 37:223–232

    Article  CAS  PubMed  Google Scholar 

  • Plummer DT (1987) An introduction to practical biochemistry. McGraw-Hill, London

  • Polver PD, Sacchi L, Grigolo A, Laudani U (1986) Fine structure of the fat body and its bacteroids in Blattella germanica (Blattodea). Acta Zool 67:63–71

    Article  Google Scholar 

  • Roeder KD, Fenton MB (1973) Acoustic responsiveness of Scoliopteryx libatrix (Lepidoptera, Noctuidae), a moth that shares hibernacula with some insectivorous bats. Canad J Zool 51(7):681–685

    Article  Google Scholar 

  • Scott RC, Schuldiner O, Neufeld TP (2004) Role and regulation of starvation-induced autophagy in the Drosophila fat body. Develop Cell 7:167–178

    Article  CAS  Google Scholar 

  • Šobotnik J, Weyda F, Hanus R, Cvačka J, Nebesáŕová J (2006) Fat body of Prorhinotermes simplex (Isoptera: Rhinotermitidae): ultrastructure, inter-caste differences and lipid composition. Micron 37:648–656

    Article  PubMed  Google Scholar 

  • Sohal RS (1974) Fine structure of the Malpighian tubules in the housefly, Musca domestica. Tissue Cell 6:719–728

    Article  CAS  PubMed  Google Scholar 

  • Turqiun M-J (1994) Lepidoptera. In: Encyclopaedia biospeologica I. Société de Biospéologie. Moulis (CNRS) and Bucarest (Academie Roumaine), pp. 333–339

  • Yang Z, Klionsky DJ (2010) Eaten alive: a history of macroautophagy. Nature Cell Biol 12(9):814–822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu CH (1999) Ultrastructure of the Malpighian tubule cells in the mosquito larvae, Culex pipiens pallens. Korean J Entomol 29:141–147

    Google Scholar 

  • Yu CH (2003) Ultrastructure of the Malpighian tubule cells in the mosquito larvae, Anopheles sinesis. Korean J Entomol 33:151–159

    Article  Google Scholar 

  • Ziegler H (2016) Scoliopteryx libatrix (Linnaeus, 1767). In: Ziegler. H., Schmetterlinge der Paläarktischen Region. http://www.euroleps.ch/index.php Accessed 27.11.2016

Download references

Acknowledgements

We would like to thank Elisabeth Bock und Rudi Schmied (Medical University Graz) for their excellent technical assistance. Michelle Gadpaille valuably improved the English of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Saška Lipovšek.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Handling Editor: Douglas Chandler

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lipovšek, S., Janžekovič, F. & Novak, T. Ultrastructure of fat body cells and Malpighian tubule cells in overwintering Scoliopteryx libatrix (Noctuoidea). Protoplasma 254, 2189–2199 (2017). https://doi.org/10.1007/s00709-017-1110-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-017-1110-3

Keywords

Navigation