Zoomorphology

, Volume 130, Issue 1, pp 1–15 | Cite as

Pattern of occurrence of supraneural coelomopores and intertentacular organs in Gymnolaemata (Bryozoa) and its evolutionary implications

Review Article

Abstract

The evolution of bryozoan female gonopores (the supraneural coelomopore (SNP) and the intertentacular organ (ITO)) is considered in the light of two alternative hypotheses. In the first hypothesis it is proposed that the ITO originated from the shortening and fusion of two tentacles possessing terminal pore(s), with further transformation into a simple pore. In the alternative hypothesis it is suggested that the ITO evolved from a coelomopore with a contribution from the basal parts of two disto-medial tentacles in an ancestor. Favouring the second hypothesis, in this paper we present a hypothetical scenario, according to which the earliest gymnolaemate bryozoans with uniserial growth and a broadcasting reproductive pattern possessed the supraneural coelomopore (SNP). This could serve both as a female gonopore and as a conduit for sperm entry. Evolution of large colonies of closely packed zooids led to development of the tube-like intertentacular organ (ITO) that is formed by epithelial proliferation of the basal parts of two dorso-medial tentacles. This prevented egg swallowing in the situation when water exchange was hampered within the large colony. The ITO independently evolved in both ctenostome and cheilostome gymnolaemates when multiserial colonies appeared. Evolution of brooding in species with colonies of closely packed zooids led to reduction of the ITO, except for the cheilostomes Tendra and Thalamoporella that acquired brooding independently. A rudimentary ITO also “survived” in two ctenostomes with the “mixed” type of brooding. An alternative, analogous organ—the ovipositor—has evolved in the cheilostome taxon Schizoporella.

Keywords

Gonopore Fertilization Spawning Evolution Bryozoa 

References

  1. Ax P (2001) Multicellular animals. Order in nature—system made by man. Springer, Heidelberg, pp 1–317Google Scholar
  2. Banta WC (1967) A new species of Victorella from Southern California (Bryozoa, Ctenostomata). Proc US Nat Mus 122(3593):1–18Google Scholar
  3. Banta WC (1975) Origin and early evolution of cheilostome Bryozoa. In: Pouyet S (ed) Bryozoa 1974. Doc Lab Géol Fac Sci Lyon HS 3(2):565–582Google Scholar
  4. Bishop JDD, Pemberton AJ (2006) The third way: spermcast mating in sessile marine invertebrates. Int Comp Biol 46(4):398–406CrossRefGoogle Scholar
  5. Boardman RS, Cheetham AH, Blake DB, Utgaard J, Karklins OL, Cook PL, Sandberg PA, Lutaud G, Wood TS (1983) Bryozoa (Part G, revised). In: Robinson RA (ed) Treatise on Invertebrate Paleontology. Geological Society of America, Boulder, Colorado; University of Kansas, Lawrence, 1:1–625Google Scholar
  6. Borg F (1926) Studies on recent cyclostomatous Bryozoa. Zool Bidr Uppsala 10:181–507Google Scholar
  7. Borg F (1947) Zur Kenntnis der Ökologie und des Lebenszyklus von Electra crustulenta. Zool Bidr Uppsala 25:344–377Google Scholar
  8. Braem F (1890) Untersuchungen über die Bryozoen des süssen Wassers. Biobl Zool Stuttg 6:1–134Google Scholar
  9. Braem F (1896) Die geschlechtliche Entwicklung von Paludicella Ehrenbergii. Zool Anz 19(493):54–57Google Scholar
  10. Braem F (1951) Über Victorella und einige ihrer nächsten Vermandten, sowie über die Bryozoenfauna des Ryck bei Greifswald. Zoologica 102(37):1–59Google Scholar
  11. Braiko VB (1967) Biology of reproduction of Membranipora zostericola Nordm. (Bryozoa). Zool Zhurn 46:1119–1121 (in Russian)Google Scholar
  12. Brien P (1953) Etude sur les Phylactolemates. Ann Soc R Zool Belgique 84:301–440Google Scholar
  13. Bullivant JS (1967) Release of sperm by Bryozoa. Ophelia 4:139–142Google Scholar
  14. Cadman PS, Ryland JS (1996) The characters, reproduction, and growth of Alcyonidium mytili Dalyell, 1848 (Ctenostomatida). In: Gordon DP, Smith AM, Grant-Mackie JA (eds) Bryozoans in space and time. National Institute of Water and Atmospheric Research Ltd, Wellington, pp 237–242Google Scholar
  15. Calvet L (1900) Contribution a l’histoire naturelle des Bryozoaires Ectoproctes marins. Trav Inst Zool Un Montpellier, NS 8:1–488Google Scholar
  16. Castric-Fey A (1971) Sur quelques bryozoaires de l’archipel de Glénan (Sud-Finistère). Vie Millieu 22:69–86Google Scholar
  17. Cook PL (1960) The development of Electra crustulenta (Pallas) (Polyzoa, Ectoprocta). Essex Nat 30(4):258–266Google Scholar
  18. Cook PL (1962) The early larval development of Membranipora seurati (Canu) and Electra crustulenta (Pallas), Polyzoa. Cah Biol Mar 3(1):57–60Google Scholar
  19. Cook PL (1964) The development of Electra monostachys (Busk) and Conopeum reticulum (Linnaeus), Polyzoa, Anasca. Cah Biol Mar 5:391–397Google Scholar
  20. Cook PL (1985) Bryozoa from Ghana. Zool Wetens Mus R Afr Centr Tervuren Belgique 238:1–315Google Scholar
  21. Cori CJ (1941) Bryozoa. Ordnung der Tentaculata. Handb Zool III 2(5):263–374, 375–502Google Scholar
  22. Corrêa DD (1948) A embryologia de Bugula flabellata (J. V. Thompson) Bryozoa Ectoprocta. Bol Fac Fil Ci Letr Univ S Paulo Zool 13:7–71Google Scholar
  23. De Blauwe H (2009) Mosdiertjes van de Zuidelijke Bocht van de Noordzee. Determinatiewerk voor België en Nederland, Uitgave Vlaams Instituut voor de Zee, OostendeGoogle Scholar
  24. Dick MH (1987) A proposed mechanism for chimney formation in encrusting bryozoan colonies. In: Ross JRP (ed) Bryozoa: present and past. Western Washington University, Bellingham, WA, pp 73–80Google Scholar
  25. Dudley JW (1973) Observations on the reproduction, early larval development, and colony astogeny of Conopeum tenuissimum (Canu). Chesapeake Sci 14(4):270–278CrossRefGoogle Scholar
  26. Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sørensen MV, Haddock SHD, Schmidt-Rhaesa A, Okusu A, Kristensen RM, Wheeler WC, Martindale MQ, Giribet G (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745–749PubMedCrossRefGoogle Scholar
  27. Ehlers E (1876) Hypophorella expansa. Ein Beitrag zur Kenntniss der minirenden Bryozoen. Abh Physik Class Königl Gesells Wiss Göttingen 21:3–157Google Scholar
  28. Emig CC (1982) Biology of Phoronida. In: Russell FS, Yonge CM (eds) Advances in marine biology. Academic Press, London 14:1–89Google Scholar
  29. Farmer JD (1977) An adaptive model for the evolution of the ectoproct life cycle. In: Woollacott RM, Zimmer RL (eds) Biology of bryozoans. Academic Press, New York, pp 487–517Google Scholar
  30. Farmer JD, Valentine JW, Cowen R (1973) Adaptive strategies leading to the ectoproct ground-plan. Syst Zool 22:233–239CrossRefGoogle Scholar
  31. Farre MB (1837) Observations on the minute structure of some of the higher forms of polypi, with views of a more natural arrangement of the class. Phil Trans R Soc Lond 1:387–426Google Scholar
  32. Fuchs J, Obst M, Sundberg P (2009) The first comprehensive molecular phylogeny of Bryozoa (Ectoprocta) based on combined analyses of nuclear and mitochondrial genes. Mol Phyl Evol 52:225–233CrossRefGoogle Scholar
  33. Gerwerzhagen A (1913) Untersuchungen an Bryozoen. Sitzungsber Heidelb Akad Wiss Math-nat Kl B 9:1–16Google Scholar
  34. Grünbaum D (1995) A model of feeding currents in encrusting bryozoans shows interference between zooids within a colony. J Theor Biol 174:409–425CrossRefGoogle Scholar
  35. Hageman GS (1981) Accessory reproductive structures in Membranipora serrilamella: a fine structural study. In: Larwood GP, Nielsen C (eds) Recent and Fossil Bryozoa. Olsen and Olsen, Fredensborg, p 311Google Scholar
  36. Harmer SF (1892) On the nature of the excretory processes in marine Polyzoa. Quart J Micr Sci 33:123–167Google Scholar
  37. Harmer SF (1926) The Polyzoa of the Siboga expedition. II. Cheilostomata Anasca. Rep Siboga Exp, EJ Brill. Leiden 28b:181–501Google Scholar
  38. Hausdorf B, Helmkampf M, Nesnidal MP, Bruchhaus I (2009) Phylogenetic relationships within the lophophorate lineages (Ectoprocta, Brachiopoda and Phoronida). Mol Phyl Evol 55:1121–1127Google Scholar
  39. Havenhand JN (1995) Evolutionary ecology of larval types. In: McEdwards L (ed) Ecology of marine invertebrate larvae. CRC Press, Boca Raton, pp 9–121Google Scholar
  40. Hayward PJ (1985) Ctenostome bryozoans. Syn Brit Fauna 33:1–169Google Scholar
  41. Helmkampf M, Bruchhaus I, Hausdorf B (2008a) Phylogenomic analyses of lophophorates (brachiopods, phoronids and bryozoans) confirm the Lophotrochozoa concept. Proc R Soc B 275:1927–1933PubMedCrossRefGoogle Scholar
  42. Helmkampf M, Bruchhaus I, Hausdorf B (2008b) Multigene analysis of lophophorate and chaetognath phylogenetic relationships. Mol Phyl Evol 46:206–214CrossRefGoogle Scholar
  43. Hincks T (1851) Notes on British zoophytes, with descriptions of some new species. Ann Mag Nat Hist 2 Ser 8(47):353–362Google Scholar
  44. Hincks T (1880) A history of the British marine Polyzoa. Van Voorst, LondonGoogle Scholar
  45. Hyatt A (1866–1868) Observations on Polyzoa. Suborder Phylactolaemata. Proc Essex Inst 4–5:1–103Google Scholar
  46. Hyman LH (1959) The invertebrates: smaller coelomate groups. McGraw-Hill Book Company, New YorkGoogle Scholar
  47. Jägersten G (1972) Evolution of the metazoan life cycle. Academic Press, New YorkGoogle Scholar
  48. Jebram D (1973a) The importance of different growth directions in the Phylactolaemata and Gymnolaemata for reconstructing the phylogeny of the Bryozoa. In: Larwood GP (ed) Living and Fossil Bryozoa: recent advances in research. Academic Press, London, pp 565–576Google Scholar
  49. Jebram D (1973b) Preliminary observations of the influences of food and other factors on the growth of Bryozoa with the description of a new apparatus for cultivation of sessile plankton feeders. Kiel Meeresf 29:50–57Google Scholar
  50. Jebram D (1975) Effects of different foods on Conopeum seurati (Canu) (Bryozoa Cheilostomata) and Bowerbankia gracilis Leidy (Bryozoa Ctenostomata). In: Pouyet S (ed) Bryozoa 1974. Doc Lab Géol Fac Sci Lyon HS 3(2):97–108Google Scholar
  51. Jebram D (1985) Panolicella nutans, gen. et sp. n., its description, development, and laboratory cultivation. Zool Scr 14:11–18CrossRefGoogle Scholar
  52. Jebram D (1992) The polyphyletic origin of the Cheilostomata (Bryozoa). Z Zool Syst Evol 30:46–52CrossRefGoogle Scholar
  53. Jebram D, Everitt B (1982) New victorellids (Bryozoa, Ctenostomata) from North America: the use of parallel cultures in bryozoan taxonomy. Biol Bull 163:172–187CrossRefGoogle Scholar
  54. Joyeux-Laffuie J (1888) Description du Delagia chaetopteri (J. J.-L.), type d’un nouveau genre de Bryozoaires. Arch Zool Exp Gén 6:135–154Google Scholar
  55. Kluge GA (1975) Bryozoa of the northern seas of the USSR. Fauna USSR Publ Zool Inst Acad Sci USSR, Amerind Publishing Co, New Delhi 76:1–711Google Scholar
  56. Kuklinski P, Porter JS (2004) Alcyonidium disciforme: an exceptional Arctic bryozoan. J Mar Biol Assoc UK 84:267–275CrossRefGoogle Scholar
  57. Levin LF, Bridges TS (1995) Pattern and diversity in reproduction and development. In: McEdwards L (ed) Ecology of marine invertebrate larvae. CRC Press, Boca Raton, pp 1–48Google Scholar
  58. Lidgard S (1981) Water flow, feeding and colony form in an encrusting cheilostome. In: Larwood GP, Nielsen C (eds) Recent and Fossil Bryozoa. Olsen and Olsen, Fredensborg, pp 175–182Google Scholar
  59. Lutaud G (1961) Contribution à l’étude de bourgeonnement et de la croissance des colonies chez Membranipora membranacea (L), Bryozoaire Chilostome. Ann Soc R Zool Belgique 91:157–300Google Scholar
  60. Lützen J, Jespersen Å, Nielsen C (2009) Ultrastructure of spermiogenesis in Cristatella mucedo Cuvier (Bryozoa: Phylactolaemata: Cristatellidae). Zoomorphology 128(4):275–283CrossRefGoogle Scholar
  61. Marcus E (1922) Bryozoen von den Aru Inseln. Abh Senckenberg Natur Ges 35:421–446Google Scholar
  62. Marcus E (1926) Beobachtungen und Versuche an lebenden Meersbryozoen. Zool Jahrb Abt Syst Ökol Geogr Tier 52:1–102Google Scholar
  63. Marcus E (1934) Über Lophopus crystallinus (Pall.). Zool Jahr Abt Anat Ont Tier 58:501–606Google Scholar
  64. Marcus E (1938a) Bryozoarios marinhos brasileiros, II. Bol Fac Philos Sci Letr Univ S Paulo IV Zool 2:1–196Google Scholar
  65. Marcus E (1938b) Bryozoen von St. Helena. Videns Med Dan Natur For København 101:183–252Google Scholar
  66. Marcus E (1941) Sobre Bryozoa do Brasil. Bol Fac Philos Sci Letr Univ S Paulo XXII Zool 5:3–208Google Scholar
  67. Marcus E (1942) Sobre Bryozoa do Brasil. II. Bol Fac Philos Sci Letr Univ S Paulo XXV Zool 6:57–106Google Scholar
  68. Matricon I (1963) Dégénérescence du polypide femelle et formation d’une poche incubatrice chez Alcyonidium polyoum (Hassall) (Bryozoaire Cténostome). Arc Zool Exp Gén 102:79–93Google Scholar
  69. Maturo FJS (1991) A new bryozoan structure: an ovipositor. In: Bigey FP (ed) Bryozoaires Actuels et Fossiels: Bryozoa Living and Fossil. Bull Soc Sci Nat Oues France, Mém HS 1:572–573Google Scholar
  70. Mawatari SF (1975) The life history of Membranipora serrilamella Osburn (Bryozoa, Cheilostomata). Bull Libr Art Sci Cour Sc Med Nihon Univ 3:19–57Google Scholar
  71. Mawatari S, Mawatari SF (1975) Development and metamorphosis of the cyphonautes of Membranipora serrilamella Osburn. In: Pouyet S (ed) Bryozoa 1974. Doc Lab Géol Fac Sci Lyon HS 3(1):13–18Google Scholar
  72. McKinney FK, Jackson JDC (1989) Bryozoan evolution. Unwin Hyman, BostonGoogle Scholar
  73. Mukai H, Terakado K, Reed CG (1997) Bryozoa. In: Harrison FW (ed) Microscopic anatomy of invertebrates, 13. Wiley-Liss, New York, pp 45–206Google Scholar
  74. Nielsen C (2001) Animal evolution: interrelationships of the living phyla, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  75. Nitsche H (1868) Beiträge zur Anatomie und Entwickelungsgeschichte der phylactolaemen Süsswasserbryozoen. insbesondere von Alcyonella fungosa Pall. Akadem.-Dissertation, Berlin, pp 1–57Google Scholar
  76. Osburn RC (1950) Bryozoa of the Pacific coast of America. Part 1, Cheilostomata-Anasca. Allan Hancock. Pacific Exp 14(1):1–269Google Scholar
  77. Ostrovsky AN (2008a) External versus internal and self- versus cross-fertilization in Bryozoa: transformation of the view and evolutionary considerations. In: Wyse Jackson PN, Spencer Jones ME (eds) Annals of Bryozoology 2: aspects of the history of research on Bryozoans. International Bryozoology Association, Dublin, pp 103–115Google Scholar
  78. Ostrovsky AN (2008b) Brood chambers in cheilostome Bryozoa: diversity and revised terminology. In: Hageman SJ, Key MM, Winston JE (eds) Bryozoan Studies 2007. Proceedings of the 14th international bryozoology association conference, Boone, North Carolina. Virg Mus Nat Hist Spec Publ, vol 15, pp 195–204Google Scholar
  79. Ostrovsky AN (2008c) The parental care in cheilostome bryozoans: a historical review. In: Wyse Jackson PN, Spencer Jones ME (eds) Annals of Bryozoology 2: aspects of the history of research on Bryozoans. International Bryozoology Association, Dublin, pp 211–245Google Scholar
  80. Ostrovsky AN (2009) Evolution of the sexual reproduction in the bryozoan order Cheilostomata (Gymnolaemata). St Petersburg State University [in Russian with English Summary]Google Scholar
  81. Ostrovsky AN, Taylor PD (2004) Systematics of Upper Cretaceous calloporid bryozoans with primitive spinose ovicells. Palaeontology 47(3):775–793CrossRefGoogle Scholar
  82. Ostrovsky AN, Taylor PD (2005) Brood chambers constructed from spines in fossil and Recent cheilostome bryozoans. Zool J Linn Soc 144:317–361CrossRefGoogle Scholar
  83. Ostrovsky AN, Vávra N, Porter JS (2008) Sexual reproduction in gymnolaemate Bryozoa: history and perspectives of the research. In: Wyse Jackson PN, Spencer Jones ME (eds) Annals of Bryozoology 2: aspects of the history of research on Bryozoans. International Bryozoology Association, Dublin, pp 117–210Google Scholar
  84. Ostrovsky AN, Gordon D, Lidgard S (2009) Independent evolution of matrotrophy in the major classes of Bryozoa: transitions among reproductive patterns and their ecological background. Mar Ecol Progr Ser 378:113–124CrossRefGoogle Scholar
  85. Owrid GMA, Ryland JS (1991) Sexual reproduction in Alcyonidium hirsutum (Bryozoa: Ctenostomata). In: Bigey FP (ed) Bryozoaires Actuels et Fossiels: Bryozoa Living and Fossil. Bull Soc Sci Nat Oues France, Mém HS, vol 1, pp 317–326Google Scholar
  86. Paltschikowa-Ostroumowa MW (1926) Kurze Bemerkung über den Ovidukt bei den Bryozoen. Zool Anz 65:100–102Google Scholar
  87. Passamaneck Y, Halanych KM (2006) Lophotrochozoan phylogeny assessed with LSU and SSU data: evidence of lophophorate polyphyly. Mol Phyl Evol 40:20–28CrossRefGoogle Scholar
  88. Pohowski RA (1978) The boring ctenostomate Bryozoa: taxonomy and paleobiology based on cavities in calcareous substrata. Bull Amer Paleont 73(301):1–192Google Scholar
  89. Pohowsky RA (1973) A Jurassic cheilostome from England. In: Larwood GP (ed) Living and fossil Bryozoa. Academic Press, London, pp 447–461Google Scholar
  90. Porter JS (2004) Morphological and genetic characteristics of erect subtidal species of Alcyonidium (Ctenostomata: Bryozoa). J Mar Biol Assoc UK 84:243–252CrossRefGoogle Scholar
  91. Porter JS, Hayward PJ (2004) Species of Alcyonidium (Bryozoa: Ctenostomata) from Antarctica and Magellan Strait, defined by morphological, reproductive and molecular characters. J Mar Biol Assoc UK 84:253–265CrossRefGoogle Scholar
  92. Porter JS, Hayward PJ, Spencer Jones ME (2001) The identity of Alcyonidium diaphanum (Bryozoa: Ctenostomatida). J Mar Biol Assoc UK 81:1001–1008Google Scholar
  93. Prenant M, Bobin G (1956) Bryozoaires. 1. Entoproctes, Phylactolèmes, Cténostomes. Faune France 60:1–398Google Scholar
  94. Prenant M, Bobin G (1966) Bryozoaires. 2. Chilostomes Anasca. Faune France 68:1–647Google Scholar
  95. Prouho H (1889) Sur la reproduction de quelques Bryozoaires cténostomes. Comp Rend Hebd Séan Ácad Sci Paris 109:197–198Google Scholar
  96. Prouho H (1892) Contribution à l’histoire des Bryozoaires. Arch Zool Exp Gén 10:557–656Google Scholar
  97. Reed CG (1988) The reproductive biology of the gymnolaemate bryozoan Bowerbankia gracilis (Ctenostomata: Vesiculariida). Ophelia 29(1):1–23Google Scholar
  98. Reed CG (1991) Bryozoa. In: Giese AC, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates, VI. Echinoderms and Lophophorates. Boxwood Press, Pacific Grove, pp 85–245Google Scholar
  99. Ruppert EE, Fox RS, Barnes RD (2004) Invertebrate zoology: a functional evolutionary approach, 7th edn. Thomson Brooks, ColeGoogle Scholar
  100. Ryland JS (1970) Bryozoans. Hutchinson University Library, LondonGoogle Scholar
  101. Ryland JS (1976) Physiology and ecology of marine bryozoans. In: Russell FS, Yonge CM (eds) Advances in marine biology, 14. Academic Press, London, pp 285–443Google Scholar
  102. Ryland JS (2001) Convergent colonial organization and reproductive function in two bryozoan species epizoic on gastropod shells. J Nat Hist 35:1085–1101CrossRefGoogle Scholar
  103. Ryland JS, Hayward PJ (1977) British anascan bryozoans. Syn Brit Fauna 10:1–188Google Scholar
  104. Ryland JS, Porter JS (2000) Alcyonidium reticulum sp. nov., a common intertidal bryozoan from south-west Britain. J Mar Biol Assoc UK 80:563–564CrossRefGoogle Scholar
  105. Ryland JS, Porter JS (2006) The identification, distribution and biology of encrusting species of Alcyonidium (Bryozoa: Ctenostomatida) around the coasts of Ireland. Proc R Irish Acad 106B(1):19–33CrossRefGoogle Scholar
  106. Santagata S, Banta WC (1996) Origin of brooding and ovicells in cheilostome bryozoans: interpretive morphology of Scrupocellaria ferox. Invert Biol 115(2):170–180CrossRefGoogle Scholar
  107. Schulz K (1901) Untersuchungen über den Bau der Bryozoen mit besonderer Berücksichtigung der Exkretionsorgane. Arch Natur 67(1):115–144Google Scholar
  108. Shunatova NN, Ostrovsky AN (2001) Individual autozooidal behaviour and feeding in marine bryozoans. Sarsia 86:113–142Google Scholar
  109. Shunatova NN, Ostrovsky AN (2002) Group behaviour and chimneys in marine bryozoans. Mar Biol 140(3):503–518CrossRefGoogle Scholar
  110. Silén L (1944) The anatomy of Labiostomella gisleni Silén (Bryozoa Protocheilostomata). Kungl Sven Vetenskap Handl, Ser 3(21):1–111Google Scholar
  111. Silén L (1945) The main features of the development of the ovum, embryo and ooecium in the ooecioferous Bryozoa Gymnolaemata. Ark Zool 35A(17):1–34Google Scholar
  112. Silén L (1966) On the fertilization problem in the gymnolaematous Bryozoa. Ophelia 3:113–140Google Scholar
  113. Silén L (1972) Fertilization in the Bryozoa. Ophelia 10(1):27–34Google Scholar
  114. Smith DG, Werle SF, Klekowski EJ (2003) The anatomy and brooding biology of Pottsiella erecta (Potts, 1884) (Ectoprocta: Gymnolaemata: Ctenostomata) with an expanded diagnosis of the Pottsiellidae. Hydrobiologia 490:135–145CrossRefGoogle Scholar
  115. Smitt FA (1866) Kritisk Förteskning öfver Scandinaviens Hafs-Bryozoernas. Aftr Öfvers Kongl Vetens-Akad Förh 23:395–533Google Scholar
  116. Strathmann RR (1978) The evolution and loss of feeding larval stages of marine invertebrates. Evolution 32(4):894–906CrossRefGoogle Scholar
  117. Ström R (1969) Sexual reproduction in a stoloniferous bryozoan, Triticella koreni (G. O. Sars). Zool Bidr Uppsala 38:113–128Google Scholar
  118. Ström R (1977) Brooding patterns of bryozoans. In: Woollacott RM, Zimmer RL (eds) Biology of Bryozoans. Academic Press, New York, pp 23–56Google Scholar
  119. Taylor PD (1988) Major radiation of cheilostome bryozoans: triggered by the evolution of a new larval type. Hist Biol 1:45–64CrossRefGoogle Scholar
  120. Taylor PD (1990) Bioimmured ctenostomes from the Jurassic and the origin of the cheilostome Bryozoa. Palaeontology 33:19–34Google Scholar
  121. Taylor PD (1994) An early cheilostome bryozoan from the Upper Jurassic of Yemen. N Jb Geol Palaeont Abh 191:331–344Google Scholar
  122. Temkin MH (1994) Gamete spawning and fertilization in the gymnolaemate bryozoan Membranipora membranacea. Biol Bull 187:143–155PubMedCrossRefGoogle Scholar
  123. Temkin MH (1996) Comparative fertilization biology of gymnolaemate bryozoans. Mar Biol 127(2):329–339CrossRefGoogle Scholar
  124. Temkin MH, Bortolami SB (2004) Waveform dynamics of spermatozeugmata during the transfer from paternal to maternal individuals of Membranipora membranacea. Biol Bull 206:35–45PubMedCrossRefGoogle Scholar
  125. Todd JA (2000) The central role of ctenostomes in bryozoan phylogeny. In: Herrera Cubilla A, Jackson JBC (eds) Proceedings of the 11th international bryozoology association conference. Smithsonian Tropical Research Institute, Republic of Panama, pp 104–135Google Scholar
  126. Tsyganov A, Hayward PJ, Porter JS, Skibinski DOF (2009) Bayesian phylogenetics of bryozoa. Mol Phyl Evol 52:904–910CrossRefGoogle Scholar
  127. van Beneden PJ (1844) Recherches sur l’organisation des Laguncula et l’histoire naturelle des différents polypes Bryozoaires qui habitent la côte d’Ostende. Nouv Mém Acad Roy Bruxelles 18:1–29Google Scholar
  128. Waters A (1904) Bryozoa. Résultats du Voyage du S.Y. “Belgica” en 1897–1898–1899. Exp Antarct Belge Zool Anvers, pp 1–114Google Scholar
  129. Wiebach F (1953) Über den Ausstoss von Flottoblasten bei Plumatellen. Zool Anz 151(9–10):266–272Google Scholar
  130. Winston JE (1978) Polypide morphology and feeding behaviour in marine ectoprocts. Bull Mar Sci 28(1):1–31Google Scholar
  131. Winston JE (1979) Current-related morphology and behaviour in some Pacific coast bryozoans. In: Larwood GP, Abbott MB (eds) Advances in bryozoology. Systematics association special vol 13. Academic Press, London, pp 247–268Google Scholar
  132. Woollacott RM (1999) Bryozoa (Ectoprocta). In: Knobil E, Neill JD (eds) Encyclopedia of reproduction, vol 1. Academic Press, London, pp 439–448Google Scholar
  133. Zimmer RL (1991) Phoronida. In: Giese AC, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates, VI. Echinoderms and Lophophorates. Boxwood Press, Pacific Grove, pp 85–245Google Scholar
  134. Zimmer RL, Woollacott RM (1977) Structure and classification of gymnolaemate larvae. In: Woollacott RM, Zimmer RL (eds) Biology of Bryozoans. Academic Press, New York, pp 57–89Google Scholar

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Authors and Affiliations

  1. 1.Department of Invertebrate Zoology, Faculty of Biology and Soil ScienceSt. Petersburg State UniversitySt. PetersburgRussia
  2. 2.Department of Palaeontology, Faculty of Earth Sciences, Geography and Astronomy, GeozentrumUniversity of ViennaViennaAustria
  3. 3.School of Life Sciences, Centre for Marine Biodiversity and BiotechnologyHeriot-Watt UniversityEdinburghUK

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