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Journal of morphology
02, 2024;285 (2): e21679.

To be a transit link: Similarity in the structure of colonial system of integration and communication pores in autozooids and avicularia of Terminoflustra membranaceotruncata (Bryozoa: Cheilostomata).

Natalia Shunatova
Author Information
  1. Natalia Shunatova: Department of Invertebrate Zoology, Saint-Petersburg State University, St. Petersburg, Russian Federation. ORCID
PMID: 38329427 DOI: 10.1002/jmor.21679

Abstract

Bryozoan colonies consist of zooids, which can differ in structure and function. Most heteromorphic zooids are unable to feed and autozooids supply them with nutrients. The structure of the tissues providing nutrient transfer is poorly investigated. Here, I present a detailed description of the colonial system of integration (CSI) and communication pores in autozooids and avicularia of the cheilosome bryozoan Terminoflustra membranaceotruncata. The CSI is the nutrient transport and distribution system in the colony. In both autozooids and avicularia it consists of a single cell type, that is, elongated cells, and has a variable branching pattern, except for the presence of a peripheral cord. The general similarity in the CSI structure in avicularia and autozooids is probably due to the interzooidal type of the avicularium. Interzooidal avicularia are likely to consume only a part of the nutrients delivered to them by the CSI, and they transit the rest of the nutrients further. The variability and irregularity of branching pattern of the CSI may be explained by the presence of single communication pores and their varying number. The structure of communication pores is similar regardless of their location (in the transverse or lateral wall) and the type of zooid in contact. Rosette complexes include a cincture cell, a few special cells, and a few limiting cells. Along each zooidal wall, there are communication pores with both unidirectional and bidirectional polarity of special cells. However, the total number of nucleus-containing lobes of special cells is approximately the same on each side of any zooidal wall. Supposing the polarity of special cells reflects the direction of nutrient transport, the pattern of special cells polarity is probably related to the need for bidirectional transport through each zooidal wall. The possibility for such transport is important in large perennial colonies with wide zones of autozooids undergoing polypide degeneration.

Keywords

funicular system funiculus rosette complexes storage cells ultrastructure

References

  1. Ameisen, J. C. (2002). On the origin, evolution, and nature of programmed cell death: A timeline of four billion years. Cell Death and Differentiation, 9(4), 367-393. https://doi.org/10.1038/sj.cdd.4400950
  2. Banta, W. C. (1969). The body wall of cheilostome Bryozoa. II. Journal of Morphology, 129(2), 149-169. https://doi.org/10.1002/jmor.1051290203
  3. Bertheloot, D., Latz, E., & Franklin, B. S. (2021). Necroptosis, pyroptosis and apoptosis: An intricate game of cell death. Cellular & Molecular Immunology, 18(5), 1106-1121. https://doi.org/10.1038/s41423-020-00630-3
  4. Best, M. A., & Thorpe, J. P. (1985). Autoradiographic study of feeding and the colonial transport of metabolites in the marine bryozoan Membranipora membranacea. Marine Biology, 84, 295-300. https://doi.org/10.1007/BF00392499
  5. Bobin, G. (1958a). Structure et genèse des diaphragmes autozoéciaux chez Bowerbankia imbricata (Adams) (Bryozoaire Cténostome, Vésicularine) [Structure and genesis of autozooecial diaphragms in Bowerbankia imbricata (Adams) (Bryozoa, Ctenostomata, Vesicularinae)]. Archives de zoologie expérimentale et générale, 96, 59-99.
  6. Bobin, G. (1958b). Histologie des bourgeons autozoéciaux et genèse de leurs diaphragmes chez Vesicularia spinosa (Linné). (Bryozoaire Cténostome) [Histology of autozoeal buds and genesis of their diaphragms in Vesicularia spinosa (Linnaeus) (Bryozoa, Ctenostomata)]. Bulletin de la Société Zoologique de France, 83, 132-144.
  7. Bobin, G. (1962). Histogenése des diaphragmes septaux stoloniaux et valeurs des rosettes chez les vésicularines (Bryozoaires, Cténostomes) [Histogenesis of stolonal septal diaphragms and rosette values in vesicularines (Bryozoans, Ctenostomes)]. Archives de zoologie expérimentale et générale, 101(1), 14-48.
  8. Bobin, G. (1964). Cytologie des rosettes de Bowerbankia imbricate (Adams) (Bryozoaire, Cténostome, vésicularine). Hypothèse sur leur fonctionnement [Cytology of rosettes of Bowerbankia imbricate (Adams) (Bryozoa, Ctenostomata, Vesicularinae). Hypothesis on their functioning]. Archives de zoologie expérimentale et générale, 104(1), 1-44.
  9. Bobin, G. (1965). Introduction à l'histophysiologie des rosettes de Bowerbankia imbricata (Adams) (Bryozoaire Cténostome, Vésicularine). Les Ribonucldines [Introduction to the histophysiology of rosettes of Bowerbankia imbricata (Adams) (Bryozoa, Ctenostomata, Vesicularinae). Ribonucleins]. Archives de zoologie expérimentale et générale, 105, 1-25.
  10. Bobin, G., & Prenant, M. (1968). Sur le calcaire des parois autozoéciales d'Electra verticillata (Ell. et Sol.) Bryozoaire chilostome, Anasca. Notions préliminaires. [On the calcification of the autozoecial walls of Electra verticillata (Ell. et Sol.) cheilostome bryozoan, Anasca. Preliminary ideas]. Archives de zoologie expérimentale et générale, 109, 157-191.
  11. Bobin, G. (1977). Interzooecial communications and the funicular system. In R. M. Woollacott & R. L. Zimmer (Eds.), Biology of bryozoans (pp. 307-333). Academic Press.
  12. Carle, K. J., & Ruppert, E. E. (1983). Comparative ultrastructure of the bryozoan funiculus: A blood vessel homologue. Journal of Zoological Systematics and Evolutionary Research, 21(3), 181-193. https://doi.org/10.1111/j.1439-0469.1983.tb00286.x
  13. Carter, M. C., Gordon, D. P., & Gardner, J. P. (2010a). Polymorphism and vestigiality: Comparative anatomy and morphology of bryozoan avicularia. Zoomorphology, 129(3), 195-211. https://doi.org/10.1007/s00435-010-0113-9
  14. Cook, P. L. (1968). Polyzoa from West Africa. The Malacostega. Part 1. Bulletin of the British Museum (Natural History), Zoology, 16, 115-160.
  15. Decker, S., Wanninger, A., & Schwaha, T. (2020). Morphology and life cycle of an epiphytic pherusellid ctenostome bryozoan from the Mediterranean Sea. Organisms Diversity & Evolution, 20(3), 417-437. https://doi.org/10.1007/s13127-020-00443-2
  16. Dyrynda, P. E. J., & King, P. E. (1983). Gametogenesis in placental and non-placental ovicellate cheilostome Bryozoa. Journal of Zoology, 200(4), 471-492. https://doi.org/10.1111/j.1469-7998.1983.tb02810.x
  17. Gordon, D. P. (1975). Ultrastructure of communication pore areas in two bryozoans. Travaux et Documents des Laboratoires de Géologie de Lyon, 3(1), 187-192.
  18. Hughes, D. J. (1987). Gametogenesis and embryonic brooding in the cheilostome bryozoan Celleporella hyalina. Journal of Zoology, 212(4), 691-711. https://doi.org/10.1111/j.1469-7998.1987.tb05965.x
  19. Hyman, L. H. (1959). The invertebrates: Smaller Coelomate groups (Vol. 5, p. 783). McGraw-Hill.
  20. Kluge, G. A. (1962). Bryozoans of the northern seas of the USSR. Publishing house of the USSR Academy of science. [in Russian]
  21. Lidgard, S., Carter, M. C., Dick, M. H., Gordon, D. P., & Ostrovsky, A. N. (2012). Division of labor and recurrent evolution of polymorphisms in a group of colonial animals. Evolutionary Ecology, 26(2), 233-257. https://doi.org/10.1007/s10682-011-9513-7
  22. Lutaud, G. (1961). Contribution à l'étude du bourgeonnement et de la croissance des colonies chez Membranipora membranacea Linné, Bryozoaire Chilostome [Contribution to the study of budding and colony growth in Membranipora membranacea Linnaeus, cheilostome bryozoan] [Doctoral dissertation]. Impr. médicale et scient if.
  23. Lutaud, G. (1962). Sur la presence d'un muscle du caecum chez les bryozoaires chilostomes [On the presence of a cecum muscle in cheilostome bryozoans]. Bulletin de la Société Zoologique de France, 87, 410-418.
  24. Lutaud, G. (1982a). Étude morphologique et ultrastructurale du funicule lacunaire chez le bryozaire chilostome Electra pilosa (Linné) [Morphological and ultrastructural study of the lacunar funiculus in the cheilostome bryozoan Electra pilosa (Linnaeus)]. Cahiers de Biologie Marine, 23, 71-81.
  25. Lutaud, G. (1982b). La communauté des parois et les voies de l'unité physiologique de la colonie chez les Bryozoaires Eurystomes [The morphogenetical continuity of the parietal tissues and the pathways of the physiological unity of a colony in Eurystome Bryozoan]. Bulletin de la Société Zoologique de France, 107, 251-266.
  26. Lutaud, G. (1983). Autozooid morphogenesis in anascan cheilostomates, In R. A. Robinson (Ed.), Treatise on invertebrates Palaeontology Part G: Bryozoa (revised) (Vol. 1, pp. 208-237). Geological Society of America and University of Kansas, Boulder and Lawrence.
  27. Lutaud, G. (1985). Preliminary experiments on interzooidal metabolic transfer in anascan bryozoans. In C. Nielsen & G. P. Larwood (Eds.), Bryozoa: Ordovician to recent (pp. 183-191). Olsen & Olsen.
  28. Lutaud, G. (1991). The organization of the mesenchymal tissues in a cheilostomate zooecium. Bulletin de la Société des Sciences Naturelles de l'Ouest de la France. Memoire Hors Serie, France, 1, 219-228.
  29. Marcus, E. (1939). Bryozoarios marinhos brasileiros III [Brazilian marine bryozoans III]. Boletins da faculdade de philosophia, sciencias e Letras, Universidade de São Paulo. Zoologia, 3(3), 111-353.
  30. McKinney, F. K., & Jackson, J. B. (1991). Bryozoan evolution (p. 238). University of Chicago Press. https://doi.org/10.1046/j.1420-9101.1993.6010142.x
  31. Miles, J. S., Harvell, C. D., Griggs, C. M., & Eisner, S. (1995). Resource translocation in a marine bryozoan: Quantification and visualization of 14 C and 35 S. Marine Biology, 122, 439-445. https://doi.org/10.1007/BF00350877
  32. Mukai, H., Terakado, K., & Reed, C. G. (1997). Bryozoa. In F. W. Harrison, & R. M. Woollacott (Eds.), Microscopic anatomy of invertebrates (Vol. 13, pp. 45-206). Wiley-Liss.
  33. Nekliudova, U. A., Schwaha, T. F., Kotenko, O. N., Gruber, D., Cyran, N., & Ostrovsky, A. N. (2019). Sexual reproduction of the placental brooder Celleporella hyalina (Bryozoa, Cheilostomata) in the White Sea. Journal of Morphology, 280(2), 278-299. https://doi.org/10.1002/jmor.20943
  34. Nekliudova, U. A., Schwaha, T. F., Kotenko, O. N., Gruber, D., Cyran, N., & Ostrovsky, A. N. (2021). Three in one: Evolution of viviparity, coenocytic placenta and polyembryony in cyclostome bryozoans. BMC Ecology and Evolution, 21, 54. https://doi.org/10.1186/s12862-021-01775-z
  35. Nielsen, C., & Pedersen, K. J. (1979). Cystid structure and protrusion of the polypide in Crisia (Bryozoa, Cyclostomata). Acta Zoologica, 60(2), 65-88. https://doi.org/10.1111/j.1463-6395.1979.tb00599.x
  36. Park, W., Wei, S., Kim, B. S., Kim, B., Bae, S. J., Chae, Y. C., Ryu, D., & Ha, K. T. (2023). Diversity and complexity of cell death: A historical review. Experimental & Molecular Medicine, 55, 1573-1594. https://doi.org/10.1038/s12276-023-01078-x
  37. Parzych, K. R., & Klionsky, D. J. (2014). An overview of autophagy: Morphology, mechanism, and regulation. Antioxidants & Redox Signaling, 20(3), 460-473. https://doi.org/10.1089/ars.2013.5371
  38. Pröts, P., Wanninger, A., & Schwaha, T. (2019). Life in a tube: morphology of the ctenostome bryozoan Hypophorella expansa. Zoological Letters, 5(1), 28. https://doi.org/10.1186/s40851-019-0142-2
  39. Ryland, J. S. (1970). Bryozoans (p. 175). Hutchinson University Library.
  40. Schack, C. R., Gordon, D. P., & Ryan, K. G. (2019). Modularity is the mother of invention: A review of polymorphism in bryozoans. Biological Reviews, 94(3), 773-809. https://doi.org/10.1111/brv.12478
  41. Schwaha, T., & De Blauwe, H. (2020). Morphology of ctenostome bryozoans: 1. Arachnidium fibrosum. Journal of Morphology, 281(12), 1598-1606. https://doi.org/10.1002/jmor.21275
  42. Schwaha, T. (2020a). Morphology of bryozoans. In T. Schwaha (Ed.), Handbook of zoology (pp. 57-100). De Gruyter.
  43. Schwaha, T. (2020b). Ctenostomata. In T. Schwaha (Ed.), Handbook of zoology (pp. 269-316). De Gruyter.
  44. Schwaha, T., Wood, T. S., & Wanninger, A. (2011). Myoanatomy and serotonergic nervous system of the ctenostome Hislopia malayensis: Evolutionary trends in bodyplan patterning of ectoprocta. Frontiers in Zoology, 8(1), 11. https://doi.org/10.1186/1742-9994-8-11
  45. Schwaha, T. F., Ostrovsky, A. N., & Wanninger, A. (2020). Key novelties in the evolution of the aquatic colonial phylum Bryozoa: Evidence from soft body morphology. Biological Reviews, 95(3), 696-729. https://doi.org/10.1111/brv.12583
  46. Schwaha, T. F., & Wanninger, A. (2015). The serotonin-lir nervous system of the Bryozoa (Lophotrochozoa): A general pattern in the Gymnolaemata and implications for lophophore evolution of the phylum. BMC Evolutionary Biology, 15(1), 223. https://doi.org/10.1186/s12862-015-0508-9
  47. Schwaha, T. F., & Wanninger, A. (2018). Unity in diversity: A survey of muscular systems of ctenostome Gymnolaemata (Lophotrochozoa, Bryozoa). Frontiers in Zoology, 15(1), 24. https://doi.org/10.1186/s12983-018-0269-6
  48. Shunatova, N., Denisova, S., & Shchenkov, S. (2021). Ultrastructure of rhizoids in the marine bryozoan Dendrobeania fruticosa (Gymnolaemata: Cheilostomata). Journal of Morphology, 282(6), 847-862. https://doi.org/10.1002/jmor.21351
  49. Shunatova, N., Denisova, S., Shchenkov, S., & Filippov, A. (2023). Colonial system of integration and communication pores in a polymorphic bryozoan Dendrobeania fruticosa (Bryozoa: Cheilostomata). Journal of Morphology, 284(7), e21601. https://doi.org/10.1002/jmor.21601
  50. Shunatova, N., Serova, K., Denisova, S., Shchenkov, S., & Ostrovsky, A. (2022). Small, but smart: Fine structure of an avicularium in Dendrobeania fruticosa (Bryozoa: Cheilostomata). Journal of Morphology, 283(2), 174-206. https://doi.org/10.1002/jmor.21436
  51. Shunatova, N., & Tamberg, Y. (2019). Body cavities in bryozoans: Functional and phylogenetic implications. Journal of Morphology, 280(9), 1332-1358. https://doi.org/10.1002/jmor.21034
  52. Silén, L. (1938). Zur kenntnis des polymorphismus der bryozoen: Die avicularien der cheilostomata anasca [On the knowledge of the polymorphism of the bryozoans: The avicularia of the anascan cheilostomes]. Zoologiska bidrag från Uppsala, 17, 149-366.
  53. Silén, L. (1944). On the formation of the interzoidal communications of the Bryozoa. Zoologiska bidrag från Uppsala, 22, 433-488.
  54. Silén, L. (1977). Polymorphism. In R. Woollacott & R. Zimmer (Eds.), Biology of bryozoans (pp. 184-232). Academic Press.
  55. Simpson, C., Jackson, J. B. C., & Herrera-Cubilla, A. (2017). Evolutionary determinants of morphological polymorphism in colonial animals. The American Naturalist, 190(1), 17-28. https://doi.org/10.1086/691789
  56. Stebbing, A. R. D. (1971). Growth of Flustra foliacea (Bryozoa). Marine Biology, 9, 267-273. https://doi.org/10.1007/BF00351389
  57. Tamberg, Y., Batson, P. B., & Napper, R. (2021). Polypide anatomy of hornerid bryozoans (Stenolaemata: Cyclostomatida). Journal of Morphology, 282(11), 1708-1725. https://doi.org/10.1002/jmor.21415
  58. Tang, D., Kang, R., Berghe, T. V., Vandenabeele, P., & Kroemer, G. (2019). The molecular machinery of regulated cell death. Cell Research, 29(5), 347-364. https://doi.org/10.1038/s41422-019-0164-5
  59. Yamaguchi, H., Hirose, M., Nakamura, M., Udagawa, S., Oguchi, K., Shinji, J., Kohtsuka, H., & Miura, T. (2021). Developmental process of a heterozooid: Avicularium formation in a bryozoan, Bugulina californica. Zoological Science, 38(3), 203-212. https://doi.org/10.2108/zs200143
  60. Zhuang, J., Xie, L., & Zheng, L. (2022). A glimpse of programmed cell death among bacteria, animals, and plants. Frontiers in Cell and Developmental Biology, 9, 790117. https://doi.org/10.3389/fcell.2021.790117

Grants

  1. 23-24-00050/Russian Science Foundation

MeSH Term

Animals
Bryozoa
Journal Article Research Support, Non-U.S. Gov't
Article has an altmetric score of 1

Word Cloud

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