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Type: Article
Published: 2024-03-20
Page range: 107-123
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The dorsal plate is a critical feature in the reassessment of the rotiferan genus Ptygura (Monogononta; Gnesiotrocha; Flosculariidae)

Department of Cell Biology and Histology; Medical School; IMIB-Arrixaca; Regional Campus of International Excellence - Campus Mare Nostrum; University of Murcia; 30100 Murcia (Spain)
Science and Mathematics Program (Biology); Faculty of Science and Technology; Phuket Rajabhat University; Phuket; Thailand
Ripon College; Department of Biology; 300 Seward St.; Ripon; WI; 54971; USA
Rotifera Anatomy loricate morphology Ptygura sessile rotifers taxonomy

Abstract

All species of Flosculariidae (Rotifera; Monogononta; Gnesiotrocha; Flosculariaceae) possess a flexible integument; they are termed illoricate. But species of four genera (Beauchampia, Floscularia, Limnias, and Ptygura) possess a distinctive hardened region on the dorsal side of their anterior end, which unfortunately has received little attention beyond the species level. In our work we study the ultrastructure of these hardened regions. In Beauchampia, Limnias, and some species of Ptygura the hardened zone takes the form of a dorsal plate (hereafter DP) with or without additional protruding processes. The DP has the shape of a ~50 µm diameter disc enfolding the anterior dorsal region of the animal, with a perimetral inward fold, smooth surface, and pores. The DP of Limnias ceratophylli shows three main ultrastructural differences from the rest of the body: (1) type of glycocalyx, (2) absence of small mounds on its surface, and (3) presence of broad cisternae at the base of the pores. In Floscularia and some Ptygura the hardened structures are reduced to a pair of dorsal projections protecting the dorsal antenna: i.e., lacking a full DP. These structures deserve attention because their adaptive importance has not been studied. Here we augment those observations with other characters: i.e., presence/absence of a birefringent body in late-stage embryos and morphology of their trophi and corona. Our goal was to provide information to help develop better taxonomy, as well as advance our understanding of the evolution of sessile taxa in general and of the potentially polyphyletic Ptygura genus in particular.

 

References

  1. Banik, S. (1996) New records of sessile rotifers from freshwater fishponds of Tripura II. Proceedings of the Indian Natural Science Academy, B62, 111–116.
  2. Bielańska-Grajner, I., Ejsmont-Karabin, J. & Radwan, S. (2015) Rotifers (Rotifera): Freshwater Fauna of Poland. Vol. 32. Jagiellonian University Press, Kraków, 580 pp. https://doi.org/10.4467/K9722.1/17.16.6981
  3. Brown, P.D. & Walsh, E.J. (2019) Genome size and lifestyle in gnesiotrochan rotifers. Hydrobiologia, 844, 105–115. https://doi.org/10.1007/s10750-018-3873-8
  4. Butler, N.M. (1983) Substrate selection and larval settlement by Cupelopagis vorax. Hydrobiologia, 104, 317–323. https://doi.org/10.1007/BF00045984
  5. Dartnall, H. & Hollowday, E.D. (1985) Antarctic rotifers. British Antarctic Survey, 100, 1–46. https://doi.org/10.26749/rstpp.129.7
  6. de Beauchamp, P. (1965) Classe des Rotifèrrs. Traité Zoologie, 4, 1225–1379.
  7. De Smet, W.H. (1998) Preparation of rotifer trophi for light and scanning electron microscopy. Hydrobiologia, 387/388, 117–121. https://doi.org/10.1023/A:1017053518665
  8. Dujardin, F. (1841) Histoire naturelle des zoophytes: Infusoires, comprenant la physiologie et la classification de ces animaux, et la manière de les étudier à raide du microscope. Vol. 1. Roret, Paris, 648 pp. https://doi.org/10.5962/bhl.title.51143
  9. Edmondson, W.T. (1940) The sessile Rotatoria of Wisconsin. Transactions of the American Microscopical Society, 59, 433–459. https://doi.org/10.2307/3222991
  10. Edmondson, W.T. (1944) Ecological studies of sessile Rotatoria, Part I. Factors affecting distribution. Ecological Monographs, 14, 32–66. https://doi.org/10.2307/1961631
  11. Edmondson, W.T. (1945) Ecological studies of sessile Rotatoria, Part II. Dynamics of populations and social structure. Ecological Monographs, 15, 141–172. https://doi.org/10.2307/1948601
  12. Edmondson, W.T. (1949) A formula key to the Rotatorian genus Ptygura. Transactions of the American Microscopical Society, 68, 127–135. https://doi.org/10.2307/3223262
  13. Edmondson, W.T. (1959) Rotifera. In: Edmondson, W.T. (Ed.), Freshwater Biology. 2nd Edition. John Wiley & Sons, Inc., New York, New York, pp. 420–494.
  14. Ejsmont-Karabin, J. & Karpowicz, M. (2019) Epizoic rotifers on Dreissena polymorpha in relation to biotic factors. Hydrobiologia, 828, 137–145. https://doi.org/10.1007/s10750-018-3808-4
  15. Fontaneto, D. & De Smet, W.H. (2015) Rotifera. In: Schmidt-Rhaesa, A. (Ed.), Handbook of Zoology: Gastrotricha, Cycloneuralia and Gnathifera. Vol. 3. Gastrotricha and Gnathifera. De Gruyter, Berlin, pp. 217–300. [http://www.degruyter.com/view/product/180465?format=G] https://doi.org/10.1515/9783110274271.217
  16. Fontaneto, D., Iakovenko, N. & De Smet, W.H. (2015) Diversity gradients of rotifer species richness in Antarctica. Hydrobiologia, 761, 235–248. https://doi.org/10.1007/s10750-015-2258-5
  17. Fontaneto, D., Melone, G. & Wallace, R.L. (2003) Morphology of Floscularia ringens (Rotifera, Monogononta) from egg to adult. Invertebrate Biology, 122, 231–240. https://doi.org/10.1111/j.1744-7410.2003.tb00087.x
  18. Franch, V. (2021) First record for the Palearctic region of a rare rotifer from the Ptygura elsteri group (Rotifera: Monogononta: Flosculariaceae: Flosculariidae) with description and biogeography of a new species: Ptygura innominata n. sp. Biogeographia – The Journal of Integrative Biogeography, 36, a012. https://doi.org/10.21426/b636052746
  19. Funch, P., Sørensen, M.V. & Obst, M. (2005) On the phylogenetic position of Rotifera – have we come any further? Hydrobiologia, 546, 11–28. https://doi.org/10.1007/1-4020-4408-9_2
  20. Gilbert, J.J. (2019) Attachment behavior in the rotifer Brachionus rubens: induction by Asplanchna and effect on sexual reproduction. Hydrobiologia, 844, 9–20. https://doi.org/10.1007/s10750-018-3805-7
  21. Gilbert, J.J. (2023) Does the predatory rotifer Asplanchna induce a behavioral response in the prey rotifer Brachionus calyciflorus? Journal of Plankton Research, 45, 255–265. https://doi.org/10.1093/plankt/fbad006
  22. Hagemann, L., Mauer, K.M., Hankeln, T., Schmidt, H. & Herlyn, H. (2023) Nuclear genome annotation of wheel animals and thorny-headed worms: inferences about the last common ancestor of Syndermata (Rotifera s.l.). Hydrobiologia. [in press] https://doi.org/10.1007/s10750-023-05268-6
  23. Hochberg, A. (2014) Comparative myoanatomy of collothecid rotifers (Rotifera: Gnesiotrocha: Collothecaceae) with details on larval metamorphosis and development of the infundibulum in species of Stephanoceros. Masters Thesis, Department of Biological Science, University of Massachusetts at Lowell, Lowell, Massachusetts, 98 pp.
  24. Hochberg, A. & Hochberg, R. (2015) Serotonin immunoreactivity in the nervous system of the free-swimming larvae and sessile adult females of Stephanoceros fimbriatus (Rotifera: Gnesiotrocha). Invertebrate Biology, 134, 261–270. https://doi.org/10.1111/ivb.12102
  25. Hochberg, R., Hochberg, A. & Chan, C. (2015) Ultrastructure of the rotifer integument: peculiarities of Sinantherina socialis (Monogononta: Gnesiotrocha). Invertebrate Biology, 134, 181–188. https://doi.org/10.1111/ivb.12085
  26. Hochberg, R., Walsh, E.J. & Wallace, R.L. (2017) The ultrastructure of the integument and proventriculus in the raptorial rotifer Cupelopagis vorax (Monogononta: Collothecaceae: Atrochidae). Invertebrate Biology, 136, 50–61. https://doi.org/10.1111/ivb.12161
  27. Hochberg, R., Yang, H., Hochberg, A., Walsh, E.J. & Wallace, R.L. (2019) When heads are not homologous: the coronae of larval and adult collothecid rotifers (Rotifera: Monogononta: Collothecaceae). Hydrobiologia, 844, 191–207. https://doi.org/10.1007/s10750-018-3760-3​
  28. Hollowday, E.D. (1948) Introduction to the study of the Rotifera—XII Philodina roseola Ehrenberg (Continued). The Microscope, 7, 2–6.
  29. Hudson, C.T. & Gosse, P.H. (1886) The Rotifera; or wheel-animalcules, both British and foreign. Vols. I & II. Longmans, Green, and Co., London, VI + 128 pp. & 144 pp. https://doi.org/10.5962/bhl.title.10136
  30. Jiménez-Santos, M.A., Sarma, S.S.S. & Nandini, S. (2019a) Temperature-dependent demographic differences in sessile rotifers of the genus Limnias (Rotifera: Gnesiotrocha). Journal of Environmental Biology, 40, 711–718. https://doi.org/10.22438/jeb/40/4/MRN-1046
  31. Jiménez-Santos, M.A., Sarma, S.S.S., Nandini, S. & Wallace, R.L. (2019b) Sessile rotifers (Rotifera) exhibit strong seasonality in a shallow, eutrophic, Ramsar Site in Mexico. Invertebrate Biology, 138, e12270. https://doi.org/10.1111/ivb.12270
  32. Kellicott, D.S. (1888) Partial list of Rotifera of Shiawassee River at Corunna, Michigan. Proceedings of the American Society of Microscopists, 10, 89–96. https://doi.org/10.2307/3220439
  33. Kordbacheh, A., Wallace, R.L. & Walsh, E.J. (2018) Evidence supporting cryptic species within two sessile microinvertebrates, Limnias melicerta and L. ceratophylli (Rotifera, Gnesiotrocha). PLoS ONE, 13, e0205203. https://doi.org/10.1371/journal.pone.0205203
  34. Koste, W. (1972) Über ein sessile Rädertier aus Amazonien, Floscularia noodti sp. n. Archive für Hydrobiologie, 70, 534–540.
  35. Koste, W. (1974) Das Rädertier-Porträt. Ptygura pectififera, die “Kammträgerin”, eine Einwanderin in Warmwasseraquarien. Mikrokosmos, 63, 182–187.
  36. Koste, W. (1975) Über den Rotatorienbestand einer Mikrobiozönose in einem tropischen aquatischen Saumbiotop, der Eichhornica-crassipes-zone im Littoral des Bung-Borapet, einem Strasee in Zentralthailand. Gewässer u. Abwässer, 57/58, 43–58.
  37. Koste, W. (1978) Rotatoria. Die Rädertiere Mitteleuropas. 2 volumes. Stuttgart: Gebrüder Borntraeger.
  38. Koste, W. (1989) Das Rädertierporträt. Die sessile Art Octotrocha speciosa. Mikrokosmos, 78, 115–121.
  39. Koste, W. & Böttger, K. (1989) Rotatorien aus Gewässern Ecudadors. Amazoniana, 10, 407–438.
  40. Koste, W., Janetzky, W. & Vareschi, E. (1995) Zur Kenntnis der limnischen Rotatorienfauna Jamaikas (Rotifera). Teil 11. Osnabrücker Naturwissenschaftliche Mitteilungen, 20/21, 399–433.
  41. Koste, W. & Poltz, J. (1987) Über die Rädertiere (Rotatoria, Phylum Aschelminthes) des Alfsees, eines Hochwasser-Rückhaltebeckens der Hase, NW-Deutschland, FRG. Osnabrücker Naturwissenschaftliche Mitteilungen, 13, 185–220.
  42. Koste, W. & Shiel, R.J. (1986) New Rotifera (Aschelminthes) from Tasmania. Transactions of the Royal Society of South Australia, 109, 93–109.
  43. Koste, W. & Tobias, W. (1990) Zur Kenntnis der Rädertierfauna des Kinda-Stausees in Zentral-Burma (Aschelminthes: Rotatoria). Osnabrücker Naturwissenschaftliche Mitteilungen, 16, 83–110.
  44. Kotikova, E.A. (2013) The somatic musculature of the rotifer Trichotria pocillum (Rotifera: Transversiramida). Doklady Biological Sciences, 451, 225–227. https://doi.org/10.1134/S0012496613040030
  45. Kotikova, E.A., Raikova, O.I. & Flyatchinskaya, L.P. (2006) Study of architectonics of rotifer musculature by the method of fluorescence with use of confocal microscopy. Journal of Evolutionary Biochemistry and Physiology, 42, 89–97. https://doi.org/10.1134/S0022093006010121
  46. Kotikova, E.A., Raikova, O.I., Flyatchinskaya, L.P., Reuter, M. & Gustafsson, M.K.S. (2001) Rotifer muscles as revealed by phalloidin-TRITC staining and confocal scanning laser microscopy. Acta Zoologica, 82, 1–9. https://doi.org/10.1046/j.1463-6395.2001.00060.x
  47. Kutikova, L.A. (1970) n.k. Kolovratki fauny CCCP (Rotatoria) (Keys of the fauna of USSR), 104, 1–744. [in Russian]
  48. Kutikova, L.A. (1995) Larval metamorphosis in sessile rotifers. Hydrobiologia, 313/314, 133–138. https://doi.org/10.1007/BF00025942
  49. Kutikova, L.A. (2007) [Five species of rotifers of the family Flosculariidae (Rotifera), their larvae and metamorphosis]. Зоология беспозвоночных, 4, 161–172. [in Russian] https://doi.org/10.15298/invertzool.04.2.05
  50. Leutbecher, C. & Koste, W. (1998) Die Rotatorienfauna des Dümmers unter besonderer Berücksichtigung der sessilen Arten Teil I. Osnabrücker Naturwissenschaftliche Mitteilungen, 24, 223–255.
  51. Meksuwan, P. (2015) Systematics and phylogeny of sessile rotifers (Rotifera, Monogononta, Gnesiotrocha). PhD dissertation in Biology. Prince of Songkla University, Hat Yai, Thailand, Hat Yai, 140 pp.
  52. Meksuwan, P., Jaturapruek, R. & Maiphae, S. (2018) Two new species of genus Limnias (Rotifera, Gnesiotrocha) from Thailand. ZooKeys, 787, 1–15. https://doi.org/10.3897/zookeys.787.28098
  53. Meksuwan, P., Pholpunthin, P. & Segers, H. (2011) Diversity of sessile rotifers (Gnesiotrocha, Monogononta, Rotifera) in Thale Noi Lake, Thailand. Zootaxa, 2997 (1), 1–18. https://doi.org/10.11646/zootaxa.2997.1.1
  54. Meksuwan, P., Pholpunthin, P. & Segers, H. (2015) Molecular phylogeny confirms Conochilidae as ingroup of Flosculariidae (Rotifera, Gnesiotrocha). Zoologica Scripta, 44, 562–573. https://doi.org/10.1111/zsc.12114
  55. Obertegger, U. & Wallace, R.L. (2023) Trait-based research on Rotifera: The holy grail or just messy? Water, 15, 1459. https://doi.org/10.3390/w15081459
  56. Ruttner-Kolisko, A. (1953) Beauchampia (Cephalosiphon) crucigera, ein vor langer Zeit entdecktes, aber wenig bekanntes Raclertier. Mikrocosmos, 43, 16–19.
  57. Sarma, S.S.S., Jiménez-Santos, M.A., Nandini, S. & Wallace, R.L. (2020) Review on the ecology and taxonomy of sessile rotifers (Rotifera) with special reference to Mexico. Journal of Environmental Biology, 41, 3–12. https://doi.org/10.22438/jeb/41/1/MRN-1344
  58. Segers, H. (1997) Contribution to a revision of Floscularia Cuvier, 1798 (Rotifera: Monogononta): notes on some Neotropical taxa. Hydrobiologia, 354, 165–175. https://doi.org/10.1023/A:1003166911731
  59. Segers, H. (2002) The nomenclature of the Rotifera: annotated checklist of valid family and genus-group names. Journal of Natural History, 36, 631–640. https://doi.org/10.1080/002229302317339707
  60. Segers, H., Meksuwan, P. & Sanoamuang, L. (2010) New records of sessile rotifers (Phylum Rotifera: Flosculariacea, Collothecacea) from Southeast Asia. Belgian Journal of Zoology, 140, 235–240.
  61. Segers, H., Murugan, G. & Dumont, H.J. (1993) On the taxonomy of the Brachionidae: description of Plationus n. gen. (Rotifera, Monogononta). Hydrobiologia, 268, 1–8. https://doi.org/10.1007/BF00005736
  62. Segers, H. & Shiel, R.J. (2008) Diversity of cryptic Metazoa in Australian freshwaters: a new genus and two new species of sessile rotifer (Rotifera, Monogononta, Gnesiotrocha, Flosculariidae). Zootaxa, 1750, 19–31.
  63. Segers, H. & Wallace, R.L. (2001) Phylogeny and classification of the Conochilidae (Rotifera, Monogononta, Flosculariacea). Zoologica Scripta, 30, 37–48. https://doi.org/10.1046/j.1463-6409.2001.00048.x
  64. Sielaff, M., Schmidt, H., Struck, T.H., Rosenkranz, D., Mark Welch, D.B., Hankeln, T. & Herlyn, H. (2015) Phylogeny of Syndermata (syn. Rotifera): Mitochondrial gene order verifies epizoic Seisonidea as sister to endoparasitic Acanthocephala within monophyletic Hemirotifera. Molecular Phylogenetics and Evolution, 96, 79–92. https://doi.org/10.1016/j.ympev.2015.11.017
  65. Sørensen, M.V. & Giribet, G. (2006) A modern approach to rotiferan phylogeny: combining morphological and molecular data. Molecular Phylogenetics and Evolution, 40, 585–608. https://doi.org/10.1016/j.ympev.2006.04.001
  66. Sørensen, M.V., Segers, H. & Funch, P. (2005) On a new Seison Grube, 1861 from coastal waters of Kenya, with a reappraisal of the classification of the Seisonida (Rotifera). Zoological Studies, 44, 34–43.
  67. Tiefenbacher, L. (1972) Beiträge zur Biologie und Ökologie sessiler Rotatorien unter besonder Berücksichtigung des Gehäusebaues und der Regenerationsfähigkeit. Archiv für Hydrobiologie Beiheft, 71, 31–78.
  68. Wallace, R.L. (1977) Substrate discrimination by larvae of the sessile rotifer Ptygura beauchampi Edmondson. Freshwater Biology, 7, 301–309. https://doi.org/10.1111/j.1365-2427.1977.tb01678.x
  69. Wallace, R.L. (1980) Ecology of sessile rotifers. Hydrobiologia, 73, 181–193. https://doi.org/10.1007/978-94-009-9209-2_31
  70. Wallace, R.L. (1993) Presence of anisotropic (birefringent) crystalline structures in embryonic and juvenile monogonont rotifers. Hydrobiologia, 255/256, 71–76. https://doi.org/10.1007/978-94-011-1606-0_9
  71. Wallace, R.L. & Edmondson, W.T. (1986) Mechanism and adaptive significance of substrate selection by a sessile rotifer. Ecology, 67, 314–323. https://doi.org/10.2307/1938575
  72. Wallace, R.L., Korbacheh, A. & Walsh, E.J. (2018) Key to the currently recognized species of Limnias Schrank, 1803 (Rotifera, Monogononta, Gnesiotrocha, Flosculariidae). Zootaxa, 4442 (2), 307–318. https://doi.org/10.11646/zootaxa.4442.2.7
  73. Wallace, R.L. & Snell, T.W. (2010) Rotifera. In: Thorp, J.H. & Covich, A. (Eds.), Ecology and Classification of North American Freshwater Invertebrates. Elsevier Inc, Amsterdam, pp. 173–235. https://doi.org/10.1016/B978-0-12-374855-3.00008-X
  74. Wallace, R.L., Snell, T.W., Ricci, C. & Nogrady, T. (2006) Rotifera. Vol. 1. Biology, Ecology and Systematics. 2nd Edition. Backhuys Publishers, Leiden, 299 pp.
  75. Wallace, R.L., Snell, T.W. & Smith, H.A. (2015) Phylum Rotifera. In: Thorp, J.H. & Rogers, D.C. (Eds.), Thorp and Covich’s Freshwater Invertebrates. Elsevier, Waltham, Massachusetts, pp. 225–271. https://doi.org/10.1016/B978-0-12-385026-3.00013-9
  76. Wei, N., Jersabek, C.D. & Yang, Y. (2019) Rotifers from China (Western Guangdong Province), with description of Lecane zhanjiangensis sp. nov. (Rotifera: Monogononta: Lecanidae). Zootaxa, 4603 (1), 66–80. https://doi.org/10.11646/zootaxa.4603.1.3
  77. Wilke, T., Ahlrichs, W.H. & Bininda‐Emonds, O.R.P. (2020) The evolution of Synchaetidae (Rotifera: Monogononta) with a focus on Synchaeta: An integrative approach combining molecular and morphological data. Journal of Zoological Systematics and Evolutionary Research, 58, 823–857. https://doi.org/10.1111/jzs.12378
  78. Wright, H.G.S. (1957) The rotifer fauna of East Norfork: notes of new species and some rarities among sessile forms. Transactions of the Norfork and Norwich Naturalists' Society, 18, 1–23.
  79. Wulfert, K. (1966) Rotatorien aus dem Stausec Ajwa und der Trinkwasser-Aufbereitung der Stadt Baroda (Indien). Limnologica, 4, 53–93.
  80. Yang, H. & Hochberg, R. (2018) Ultrastructure of the extracorporeal tube and “cement glands” in the sessile rotifer Limnias melicerta (Rotifera: Gnesiotrocha). Zoomorphology, 137, 1–12. https://doi.org/10.1007/s00435-017-0371-x
  81. Yang, H., Hochberg, R., Walsh, E.J. & Wallace, R.L. (2019) Systematic distribution of birefringent bodies in Rotifera and first evidence of their ultrastructure in Acyclus inquietus (Gnesiotrocha: Collothecaceae). Hydrobiologia, 844, 209–219. https://doi.org/10.1007/s10750-018-3784-8
  82. Yang, H., Hochberg, R., Walsh, E.J. & Wallace, R.L. (2021) Ultrastructure of the extracorporeal secretions of four sessile species of Rotifera (Gnesiotrocha) with observations on the chemistry of the gelatinous tube. Invertebrate Biology, 140, e12318. https://doi.org/10.1111/ivb.12318
  83. Young, A., Hochberg, R., Walsh, E.J. & Wallace, R.L. (2019) Modeling the life history of sessile rotifers: larval substratum selection through reproduction. Hydrobiologia, 844, 67–82. https://doi.org/10.1007/s10750-018-3802-x