Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Serotonergic and FMRFamidergic nervous systems in gymnolaemate bryozoan larvae


A growing body of data from nervous systems of marine invertebrate larvae provides an ideal background for comparisons among higher taxa. The currently available data from Bryozoa, however, do not allow for a consistent hypothesis of an ancestral state for this taxon, which would be necessary for phylogenetic inferences. The larval nervous systems of the four gymnolaemate species Flustrellidra hispida, Bugula fulva, Alcyonidium gelatinosum, and Bowerbankia gracilis are examined by means of antibody staining against the neurotransmitters serotonin and FMRFamide, as well as against acetylated α-tubulin. Despite considerable variation, a comparison reveals a common pattern of the distribution of serotonin. The neurotransmitter is found in at least two cells in the apical organ as well as in paired axial and lateral nerves emerging from a central nerve nodule. A ring nerve is present below the corona and at least two serotonergic cells are found between the corona cells. Serotonergic coronal cells might represent unique bryozoan features, whereas the remaining elements show resemblance to the situation found in most spiralian taxa. The data do not provide support for a closer relationship of Bryozoa to Phoronida or Brachiopoda.

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

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


  1. Ax P (2001) Das System der Metazoa III. Spektrum Akademischer Verlag, Heidelberg

  2. Baguna J, Martinez P, Paps J, Riutort M (2008) Back in time: a new systematic proposal for the Bilateria. Philos Trans Roy Soc B Biol Sci 363:1481–1491. doi:10.1098/rstb.2007.2238

  3. Bourlat S, Nielsen C, Economou AD, Telford MJ (2008) Testing the new animal phylogeny: a phylum level molecular analysis of the animal kingdom. Mol Phylogenet Evol 49:23–31. doi:10.1016/j.ympev.2008.07.008

  4. Brinkmann N, Wanninger A (2008) Larval neurogenesis in Sabellaria alveolata reveals plasticity in polychaete neural patterning. Evol Dev 10:606–618. doi:10.1111/j.1525-142X.2008.00275.x

  5. Byrne M, Nakajima Y, Chee FC, Burke RD (2007) Apical organs in echinoderm larvae: insights into larval evolution in the Ambulacraria. Evol Dev 9:432–445

  6. Calvet L (1900) Contribution à l’histoire naturelle des bryozoaires ectoproctes marins. Trav Inst Zool Univ Montpellier 8:1–488

  7. Couper JM, Leise EM (1996) Serotonin injections induce metamorphosis in larvae of the gastropod mollusc Ilyanassa obsoleta. Biol Bull 191:178–186. doi:10.2307/1542921

  8. d’Hondt JL (1973) Etude anatomique, histologique, et cytologique de la larve d’Alcyonidium polyoum (Hassal, 1841). Arch Zool Exp Gén 114:537–602

  9. d’Hondt JL (1975) Etude anatomique et cytologique comparee de quelques larves de bryozoaires ctenostomes. In: Pouyet S (ed) Bryozoa 1974. Université Claude Bernard, Lyon, pp 125–134

  10. d’Hondt JL (1977a) Structure larvaire et histogenese postlarvaire chez Bowerbankia imbricata (Adams, 1798). Arch Zool Exp Gén 118:211–243

  11. d’Hondt JL (1977b) Larval structure and post-larval organogenesis of Flustrellidra hispida (Fabricius, 1780), Bryozoa, Ctenostomata. Zoomorphologie 87:165–189

  12. Dickinson AJG, Croll RP (2003) Development of the larval nervous system of the gastropod Ilyanassa obsoleta. J Comp Neurol 466:197–218

  13. Franzén Å, Sensenbaugh T (1983) Fine structure of the apical plate in the larva of the freshwater Bryozoan Plumatella fungosa (Pallas) (Bryozoa: Phylactolaemata). Zoomorphology 102:87–98

  14. Friedrich S, Wanninger A, Bruckner M, Haszprunar G (2002) Neurogenesis in the mossy chiton, Mopalia muscosa (Gould) (Polyplacophora): evidence against molluscan metamerism. J Morphol 253:109–117

  15. Fuchs J, Wanninger A (2008) Reconstruction of the neuromuscular system of the swimming-type larva of Loxosomella atkinsae (Entoproxta) as inferred by fluorescence staining and confocal microscopy. Organ Divers Evol 8:325–335

  16. Gruhl A (2008) Muscular systems in gymnolaemate bryozoan larvae (Bryozoa: Gymnolaemata). Zoomorphology 127:143–159

  17. Hadfield MG, Meleshkevitch EA, Boudko DY (2000) The apical sensory organ of a gastropod veliger is a receptor for settlement cues. Biol Bull 198:67–76

  18. Halanych KM, Bacheller JD, Aguinaldo AMA, Liva SM, Hills DM, Lake JA (1995) Evidence from 18S ribosomal DNA that the lophophorates are protostome animals. Science 267:1641–1643

  19. Haszprunar G, Wanninger A (2008) On the fine structure of the creeping larva of Loxosomella murmanica: additional evidence for a clade of Kamptozoa (Entoprocta) and Mollusca. Acta Zool (in press)

  20. Haszprunar G, Friedrich S, Wanninger A, Ruthensteiner B (2002) Fine structure and immunocytochemistry of a new chemosensory system in the chiton larva (Mollusca : Polyplacophora). J Morphol 251:210–218

  21. Hay-Schmidt A (1990a) Catecholamine-containing, serotonin-like, and FMRFamide-like immunoreactive neurons and processes in the nervous system of the early actinotroch larva of Phoronis vancouverensis (Phoronida)—distribution and development. Can J Zool 68:1525–1536

  22. Hay-Schmidt A (1990b) Catecholamine-containing, serotonin-like and neuropeptide FMRFamide-like immunoreactive cells and processes in the nervous system of the pilidium larva (Nemertini). Zoomorphology 109:231–244

  23. Hay-Schmidt A (1990c) Distribution of catecholamine-containing, serotonin-like and neuropeptide FMRFamide-like immunoreactive neurons and processes in the nervous system of the actinotroch larva of Phoronis muelleri (Phoronida). Cell Tissue Res 259:105–118

  24. Hay-Schmidt A (1992) Ultrastructure and immunocytochemistry of the nervous system of the larvae of Lingula anatina and Glottidia sp. (Brachiopoda). Zoomorphology 112:189–205

  25. Hay-Schmidt A (1995) The larval nervous system of Polygordius lacteus Scheinder, 1868 (Polygordiidae, Polychaeta)—immunocytochemical data. Acta Zool 76:121–140

  26. Hay-Schmidt A (2000) The evolution of the serotonergic nervous system. Proc R Soc B 267:1071–1079

  27. Helmkampf M, Bruchhaus I, Hausdorf B (2008a) Multigene analysis of lophophorate and chaetognath phylogenetic relationships. Mol Phylogenet Evol 46:206–214

  28. Helmkampf M, Bruchhaus I, Hausdorf B (2008b) Phylogenomic analyses of lophophorates (brachiopods, phoronids and bryozoans) confirm the Lophotrochozoa concept. Proc R Soc B 275:1927–1933

  29. Hessling R (2002) Metameric organisation of the nervous system in developmental stages of Urechis caupo (Echiura) and its phylogenetic implications. Zoomorphology 121:221–234

  30. Hughes RLJ, Woollacott RM (1978) Ultrastructure of potential photoreceptor organs in the larva of Scrupocellaria bertholetti (Bryozoa). Zoomorphologie 91:225–234

  31. Hughes RLJ, Woollacott RM (1980) Photoreceptors of bryozoan larvae (Cheilostomata, Cellularioidea). Zool Scr 9:129–138

  32. Hyman LH (1959) The invertebrates V: smaller coelomate groups. McGraw-Hill, New York

  33. Kempf SC, Page LR, Pires A (1997) Development of serotonin-like immunoreactivity in the embryos and larvae of nudibranch mollusks with emphasis on the structure and possible function of the apical sensory organ. J Comp Neurol 386:507–528

  34. Kristof A, Wollesen T, Wanninger A (2008) Segmental mode of neural patterning in Sipuncula. Curr Biol 18:1129–1132

  35. Kupelwieser H (1905) Untersuchungen über den feineren Bau und die Metamorphose des Cyphonautes. Zoologica 47:1–50

  36. Marcus E (1926) Sinnesphysiologie und Nervensystem der Larve von Plumatella fungosa (Pall.). Verh Dtsch Zool Ges 31:86–90

  37. Marois R, Carew TJ (1990) The gastropod nervous system in metamorphosis. J Neurobiol 21:1053–1071

  38. McCauley DW (1997) Serotonin plays an early role in the metamorphosis of the hydrozoan Phialidium gregarium. Dev Biol 190:229–240

  39. McDougall C, Chen WC, Shimeld SM, Ferrier DE (2006) The development of the larval nervous system, musculature and ciliary bands of Pomatoceros lamarckii (Annelida): heterochrony in polychaetes. Front Zool 3:16

  40. Mukai H, Terakado K, Reed CG (1997) Bryozoa. In: Harrison FW, Woollacott RM (eds) Microscopic anatomy of invertebrates: lophophorates, entoprocta and cycliophora, vol 13. Wiley-Liss, New York, pp 45–206

  41. Nezlin LP (2000) Tornaria of hemichordates and other dipleurula-type larvae: a comparison. J Zool Syst Evol Res 38:149–156

  42. Nezlin LP, Yushin VV (2004) Structure of the nervous system in the tornaria larva of Balanoglossus proterogonius (Hemichordata: Enteropneusta) and its phylogenetic implications. Zoomorphology 123:1–13

  43. Nielsen C (1970) On metamorphosis and ancestrula formation in cyclostomatous bryzoans. Ophelia 7:217–256

  44. Nielsen C (1971) Entoproct life-cycles and the entoproct/ectoproct relationship. Ophelia 9:209–341

  45. Nielsen C (2001) Animal evolution. Interrelationships of the living phyla. Oxford University Press, Oxford

  46. Nielsen C (2004) Trochophora larvae: cell-lineages, ciliary bands, and body regions. 1. Annelida and mollusca. J Exp Zool B 302:35–68

  47. Nielsen C (2005a) Larval and adult brains. Evol Dev 7:483–489

  48. Nielsen C (2005b) Trochophora larvae: cell-lineages, ciliary bands, and body regions. 2. Other groups and general discussion. J Exp Zool B 304:401–447

  49. Nielsen C (2008) Ontogeny of the spiralian brain. In: Minelli A, Fusco G (eds) Evolving pathways: key themes in evolutionary developmental biology. Cambridge University Press, Cambridge, pp 399–415

  50. Nielsen C, Hay-Schmidt A (2007) Development of the enteropneust Ptychodera flava: ciliary bands and nervous system. J Morphol 268:551–570

  51. Page LR (2002) Apical sensory organ in larvae of the patellogastropod Tectura scutum. Biol Bull 202:6–22

  52. Page LR, Parries SC (2000) Comparative study of the apical ganglion in planktotrophic caenogastropod larvae: ultrastructure and immunoreactivity to serotonin. J Comp Neurol 418:383–401

  53. Passamaneck YJ, Halanych KM (2004) Evidence from Hox genes that bryozoans are lophotrochozoans. Evol Dev 6:275–281

  54. Passamaneck YJ, Halanych KM (2006) Lophotrochozoan phylogeny assessed with LSU and SSU data: evidence of lophophorate polyphyly. Mol Phylogenet Evol 40:20–28

  55. Philippe H, Lartillot N, Brinkmann H (2005) Multigene analyses of bilaterian animals corroborate the monophyly of Ecdysozoa, Lophotrochozoa and Protostomia. Mol Biol Evol 22:1246–1253

  56. Pires A, Woollacott RM (1997) Serotonin and dopamine have opposite effects on phototaxis in larvae of the bryozoan Bugula neritina. Biol Bull Woods Hole 192:399–409

  57. Prouho H (1890) Recherches sur la larve de Flustrellidra hispida: Structure et metamorphose. Arch Zool Exp Gén 8(2. Ser):409–459

  58. Prouho H (1892) Contribution a l’histoire des bryozoaires. Arch Zool Exp Gén 10(2. Ser):557–656

  59. Purschke G, Arendt D, Hausen H, Müller MCM (2006) Photoreceptor cells and eyes in Annelida. Arthropod Struct Dev 35:211–230

  60. Reed CG (1980) The reproductive biology, larval morphology, and metamorphosis of the marine bryozoan, Bowerbankia gracilis (Vesicularioidea, Ctenostomata). PhD Thesis, University of Washington, Seattle, WA, USA

  61. Reed CG (1988) Organization of the nervous system and sensory organs in the larva of the marine bryozoan Bowerbankia gracilis (Ctenostomata: Vesiculariidae): functional significance of the apical disc and pyriform organ. Acta Zool 69:177–194

  62. Reed CG (1991) Bryozoa. In: Giese AC, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates. VI. Echinoderms and lophophorates. Boxwood Press, Pacific Groove, California, pp 85–245

  63. Reed CG, Cloney RA (1982) The larval morphology of the marine bryozoan Bowerbankia gracilis (Ctenostomata: Vesicularioidea). Zoomorphology 100:23–54

  64. Reed CG, Woollacott RM (1982) Mechanisms of rapid morphogenetic movements in the metamorphosis of the bryozoan Bugula neritina (Cheilostomata, Cellularioidea). I. Attachment to the substratum. J Morphol 172:335–348

  65. Reed CG, Ninos JM, Woollacott RM (1988) Bryozoan larvae as mosaics of multifunctional ciliary fields: ultrastructure of the sensory organs of Bugula stolonifera. J Morphol 197:127–145

  66. Ryland JS (1960) Experiments on the influence of light on the behaviour of a polyzoan larva. J Exp Biol 37:783–800

  67. Ryland JS (1974) Behaviour, settlement and metamorphosis of bryozoan larvae. Thalassia Jugosl 10:239–262

  68. Ryland JS (1976) Physiology and ecology of marine bryozoans. Adv Mar Biol 14:285–443

  69. Ryland JS (1977) Taxes and tropisms of bryozoans. In: Woollacott RM, Zimmer RL (eds) Biology of bryozoans. Academic Press, New York, pp 411–436

  70. Santagata S (2002) Structure and metamorphic remodeling of the larval nervous system and musculature of Phoronis pallida (Phoronida). Evol Dev 4:28–43

  71. Santagata S (2008) Evolutionary and structural diversification of the larval nervous system among marine bryozoans. Biol Bull 215:3–23

  72. Shimizu K, Hunter E, Fusetani N (2000) Localisation of biogenic amines in larvae of Bugula neritina (Bryozoa: Cheilostomatida) and their effects on settlement. Mar Biol 136:1–9

  73. Sopott-Ehlers B (1991) Comparative morphology of photoreceptors in free-living plathelminths—a survey. Hydrobiologia 227:231–239

  74. Strathmann RR (1978) The evolution and loss of feeding larval stages of marine invertebrates. Evolution 32:894–906

  75. Stricker SA (1987) Ultrastructure of the apical organ in a Cyphonautes larva. In: Ross JRP (ed) Bryozoa: present and past. Western Washington University, Bellingham, pp 261–268

  76. Stricker SA, Reed CG, Zimmer RL (1988a) The cyphonautes larva of the marine bryozoan Membranipora membranacea. I. General morphology, body wall, and gut. Can J Zool 66:368–383

  77. Stricker SA, Reed CG, Zimmer RL (1988b) The cyphonautes larva of the marine bryozoan Membranipora membranacea. II. Internal sac, musculature, and pyriform organ. Can J Zool 66:384–398

  78. Vernet G (1974) Étude ultrastructurale de cellules présumées photoréceptrices dans les ganglions cérébroïdes des Lineidae (Hétéronemertes). Annales des sciences naturelles/Zoologie et biologie animale 16:27–36

  79. Voronezhskaya EE, Tsitrin EB, Nezlin LP (2002a) Neuronal development in larval polychaete Phyllodoce maculata (Phyllodocidae). J Comp Neurol 455:299–309

  80. Voronezhskaya EE, Tyurin SA, Nezlin LP (2002b) Neuronal development in larval chiton Ischnochiton hakodadensis (Mollusca : Polyplacophora). J Comp Neurol 444:25–38

  81. Voronezhskaya E, Nezlin L, Odintsova N, Plummer J, Croll R (2008) Neuronal development in larval mussel Mytilus trossulus (Mollusca: Bivalvia). Zoomorphology 127:97–110

  82. Waeschenbach A, Telford MJ, Porter JS, Littlewood DTJ (2006) The complete mitochondrial genome of Flustrellidra hispida and the phylogenetic position of Bryozoa among the Metazoa. Mol Phylogenet Evol 40:195–207

  83. Wanninger A, Haszprunar G (2003) The development of the serotonergic and FMRF-amidergic nervous system in Antalis entalis (Mollusca, Scaphopoda). Zoomorphology 122:77–85

  84. Wanninger A, Koop D, Bromham LD, Noonan E, Degnan BM (2005a) Nervous and muscle system development in Phascolion strombus (Sipuncula). Dev Genes Evol 215:509–518

  85. Wanninger A, Koop D, Degnan BM (2005b) Immunocytochemistry and metamorphic fate of the larval nervous system of Triphyllozoon mucronatum (Ectoprocta : Gymnolaemata : Cheilostomata). Zoomorphology 124:161–170

  86. Wanninger A, Fuchs J, Haszprunar G (2007) Anatomy of the serotonergic nervous system of an entoproct creeping-type larva and its phylogenetic implications. Inv Biol 126:268–278

  87. Wendt DE, Woollacott RM (1999) Ontogenies of phototactic behavior and metamorphic competence in larvae of three species of Bugula (Bryozoa). Inv Biol 118:75–84

  88. Woollacott RM, Zimmer RL (1972) Fine structure of a potential photoreceptor organ in the larva of Bugula neritina (Bryozoa). Z Zellforsch 123:458–469

  89. Zega G, Pennati R, Groppelli S, Sotgia C, De Bernardi F (2005) Dopamine and serotonin modulate the onset of metamorphosis in the ascidian Phallusia mammillata. Dev Biol 282:246–256

  90. Zega G, Pennati R, Fanzago A, De Bernardi F (2007) Serotonin involvement in the metamorphosis of the hydroid Eudendrium racemosum. Int J Dev Biol 51:307–313

  91. Zimmer RL, Reed CG (1994) Morphology and ultrastructure of the larva of the bryozoan Tanganella muelleri (Ctenostomata: Victorellidae). In: Wilson WH (ed) Reproduction and development of marine invertebrates : papers from a symposium held at Friday Harbor Laboratories of the University of Washington, June 9–11. Johns Hopkins University Press, Baltimore, pp 224–245

  92. Zimmer RL, Woollacott RM (1977a) Metamorphosis, ancestrulae, and coloniality in bryozoan life cycles. In: Woollacott RM, Zimmer RL (eds) Biology of bryozoans. Academic Press, New York, pp 91–142

  93. Zimmer RL, Woollacott RM (1977b) Structure and classification of gymnolaemate larvae. In: Woollacott RM, Zimmer RL (eds) Biology of bryozoans. Academic Press, New York, pp 57–89

  94. Zimmer RL, Woollacott RM (1989a) Intercoronal cell complex of larvae of the bryozoan Watersipora arcuata (Cheilostomata: Ascophora). J Morphol 199:151–164

  95. Zimmer RL, Woollacott RM (1989b) Larval morphology of the bryozoan Watersipora arcuata (Cheilostomata: Ascophora). J Morphol 199:125–150

  96. Zimmer RL, Woollacott RM (1993) Anatomy of the larva of Amathia vidovici (Bryozoa: Ctenostomata) and phylogenetic significance of vesiculariform larva. J Morphol 215:1–29

Download references


I thank Thomas Bartolomaeus for support and helpful advice. I am also grateful to Thomas Stach (Berlin), Andrew N. Ostrovsky (Vienna) and Olga N. Kotenko (St. Petersburg) for valuable suggestions on the manuscript. Figure 6d and f was taken during a graduate course held by Harald Hausen and me at the Free University of Berlin, many thanks to all participants. Anja Jachmann (Helgoland) kindly helped with collection of animals.

Author information

Correspondence to Alexander Gruhl.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Gruhl, A. Serotonergic and FMRFamidergic nervous systems in gymnolaemate bryozoan larvae. Zoomorphology 128, 135–156 (2009).

Download citation


  • Bryozoa
  • Gymnolaemata
  • Larvae
  • Nervous system
  • Serotonin
  • FMRFamide