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Systematic distribution of birefringent bodies in Rotifera and first evidence of their ultrastructure in Acyclus inquietus (Gnesiotrocha: Collothecaceae)

  • ROTIFERA XV
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Abstract

Small birefringent concretions have been reported in rotifers for over a century and often hypothesized as energy sources. Here, we provide an update on their distribution in superorder Gnesiotrocha and the first data on their ultrastructure. Within Gnesiotrocha, these birefringent bodies (BRB) are known from at least ten species of Collothecaceae and 14 species of Flosculariaceae, both of which include planktonic and sessile species. Among sessile species, the predator Acyclus inquietus contains a single BRB that has been described as starch-like. We examined larvae of A. inquietus with transmission electron microscopy and revealed the BRB to have an irregular, electron-dense margin that surrounds a speckled core. The core appears mostly amorphous, but contains numerous, very small electron-dense spots and thin electron-dense fibers; there is no evidence of any crystalline lattice. The intestinal lumen contains smaller concretions that are probably the result of BRB metabolism. The thin epithelium contains abundant electron-dense granules but relatively few organelles. We hypothesize that the BRB is a unique form of extracellular glycogen that functions as an energy source in larvae for their dispersal and metamorphosis. In adult A. inquietus, the BRB may provide energy permitting reproduction when prey are no longer available.

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References

  • Buchner, H., L. Tiefenbacher, R. Kling & K. Preissler, 1970. Über die physiologische Bedeutung des Magen–Darm– Rudimentes der Männchen von Asplanchna sieboldi (Rotatoria, Monogononta). Journal of Comparative Physiology A 67: 453–454.

    Google Scholar 

  • de Beauchamp, P., 1909. Recherches sur les Rotifères: les formations tegumentaires et l’appareil digestif. Archives Zoologie Experimental et General, series 4(10): 1–410.

    Google Scholar 

  • de Beauchamp, P., 1912. Rotifères communiqués par H. K. Harring et C. F. Rousselet: contributions a l’étude des Atrochidés. Bulletin de la Société zoologique de France 37: 242–254.

    Article  Google Scholar 

  • Donner, P. J., 1964. Die Rotatorien-Synusien submerser Makrophyten der Donau bei Wien und mehrerer Alpenbäche. Veröffentlichungen der Arbeitsgemeinschaft Donauforschung 1(3): 227–324.

    Article  Google Scholar 

  • Hochberg, R., S. O’Brien & A. Puleo, 2010. Behavior, metamorphosis and muscular organization of the predatory rotifer, Acyclus inquietus (Rotifera, Monogononta). Invertebrate Biology 129(3): 210–219.

    Article  Google Scholar 

  • Hochberg, A. & R. Hochberg, 2017. Musculature of the sessile rotifer Stephanoceros fimbriatus (Rotifera: Gnesiotrocha: Collothecaceae) with details on larval metamorphosis and development of the infundibulum. Zoologischer Anzeiger 268: 8495.

    Article  Google Scholar 

  • Hudson, C. T., 1883. Five new Floscules; with a note on Prof. Leidy’s genera of Acyclus and Dictyophora. Journal of the Royal Microscopical Society Series II 3: 161–171.

    Article  Google Scholar 

  • Hudson, C. T. & P. H. Gosse, 1886. The Rotifera; or Wheel-Animalcules, Both British and Foreign. Longmans, Green, and Co., London.

    Book  Google Scholar 

  • Hünerhoff, E., 1931. Ober ein bisher unbekanntes Larvenorgan and die Regeneration bei dem Radertier Apsilus vorax. Zoolgicher Anzeiger 92: 327–332.

    Google Scholar 

  • Joliet, L., 1883. Monographie des Melicertes. Archives de Zoologie Expérimentale et Générale 2(131–122): 11–13.

    Google Scholar 

  • Koste, W., 1974. Zur Kenntnis der Rotatorienfauna der “Schwimmenden Wiese” einer Uferlagune in der Varzea Amazoniens, Brasilien. Amazoniana 5: 25–60.

    Google Scholar 

  • Koste, W., 1978. Rotatoria. Die Rädertiere Mitteleuropas, Vol. 2. Gebrüder Borntraeger, Stuttgart.

    Google Scholar 

  • Kutikova, L. A., 1995. Larval metamorphosis in sessile rotifers. Hydrobiologia 313(314): 133–138.

    Article  Google Scholar 

  • Leidy, J., 1882. Rotifera without rotary organs. Proceedings of the Academy of Natural Science of Philadelphia 34: 243–250.

    Google Scholar 

  • Milne, W., 1905. On the function of the water vascular system in Rotifera, with notes on some South African Floscularia. Royal Philosophical Society of Glasgow 36: 127–188.

    Google Scholar 

  • Noma, K., A. Goncharova, M. H. Ellisman & J. Yishi, 2017. Micritubule-dependent ribosome localization in C. elegans neurons. eLIFE 6: e26376.

    Article  Google Scholar 

  • Penard, E., 1914. A propos rotifères. Revue Suisse de Zoologie 22: 1–25.

    Article  Google Scholar 

  • Prats, C., T. E. Graham & J. Shearer, 2018. The dynamic life of the glycogen granule. Journal of Biological Chemistry 293: 7089–7098.

    Article  CAS  Google Scholar 

  • Revel, J. P., 1964. Electron microscopy of glycogen. Journal of Histochemistry and Cytochemistry 12(2): 104–114.

    Article  CAS  Google Scholar 

  • Revel, J. P., L. Napolitano, & D. W. Fawcett, 1960. Identification of glycogen in electron micrographs of thin tissue sections. The Journal of Biophysical and Biochemical Cytology 8: 575–589.

    Article  CAS  Google Scholar 

  • Rousselet, C. F., 1892. On Conochilus unicornis and Euchlanis parva—two new rotifers. Journal of the Quekett Microscopical Club 4: 367–370.

    Google Scholar 

  • Sullivan, M. A., F. Vilaplana, R. A. Cave, D. Stepleton, A. A. Gray-Weale & R. G. Gilbert, 2010. Nature of & #x03B1; and ß particles of glycogen using molecular size distributions. Biomacromolecules 11: 1094–1100.

    Article  CAS  Google Scholar 

  • Suprenant, K. A., 1993. Microtubules, ribosomes, and RNA: evidence for cytoplasmic localization and translational regulation. Cell Motility and the Cytoskeleton 25: 1–9.

    Article  CAS  Google Scholar 

  • Vournakis, J. & A. Rich, 1971. Size changes in eukaryotic ribosomes. Proceedings of the National Academy of Science USA 68: 3021–3025.

    Article  CAS  Google Scholar 

  • Wallace, R. L., 1975. Larval behavior of the sessile rotifer Ptygura beauchampi (Edmondson). Verhandlungen Internationale Vereinigung Limnologie 19: 2811–2815.

    Google Scholar 

  • Wallace, R. L., 1993. Presence of anisotropic (birefringent) crystalline structures in embryonic and juvenile monogonont rotifers. Hydrobiologia 255(256): 71–76.

    Article  Google Scholar 

  • Weber, E.-F., 1888. Notes sur quelques Rotateurs des environs de Genève. Archive de Biologie 8(647–722): 26–36.

    Google Scholar 

  • Williamson, W. C., 1853. On the anatomy of Melicerta ringens. Quarterly Journal of Microscopical Science 1(3–8): 64–71.

    Google Scholar 

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Acknowledgements

We thank the editor and two anonymous reviewers for critical comments that dramatically improved this manuscript. We also thank the participants of the Rotifera XV Symposium for their ideas on the topic of birefringent bodies. We acknowledge the staff at the Core Electron Microscope Facility (UMM) for their assistance in the use of their TEM. Collections at Hueco Tanks State Park and Historic Site were made under Texas Parks and Wildlife permit TPWD 2016-03 (E.J. Walsh). Kevin Bixby facilitated sampling at La Mancha Wetland. Funding was provided from the National Science Foundation (NSF), DEB Grants 1257110 (R. Hochberg), 1257068 (E.J. Walsh), and 1257116 (R.L. Wallace), and by Grant 5G12MD007592 (E.J. Walsh) from the National Institutes on Minority Health and Health Disparities (NIMHD), a component of the National Institutes of Health (NIH). Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the NSF or NIH.

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Correspondence to Rick Hochberg.

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Guest editors: Steven A. J. Declerck, Diego Fontaneto, Rick Hochberg & Terry W. Snell / Crossing Disciplinary Borders in Rotifer Research

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Yang, H., Hochberg, R., Walsh, E.J. et al. Systematic distribution of birefringent bodies in Rotifera and first evidence of their ultrastructure in Acyclus inquietus (Gnesiotrocha: Collothecaceae). Hydrobiologia 844, 209–219 (2019). https://doi.org/10.1007/s10750-018-3784-8

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