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Histological and ultrastructural reconstruction of ventral epidermal glands of Spio (Polychaeta, Spionidae, Annelida)

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Abstract

With present study, we confirm that the ventral structures on anterior and middle chaetigers of two species of Spio are special kind of intraepidermal multicellular glands. The general anatomy and coherence morphology of these ventral epidermal glands (VEGs) were 3D-reconstructed based on semithin section series. Specific anatomical characters were explored using electron microscopy, such as scanning electron microscopy for characterization of gland pores and transmission electron microscopy for investigation into cytoanatomical details. The VEGs are tubular or acinar; their pores are spherical or lens-shaped. The glands consist of three cell types: secretory cells, sheath cells and canal cells, forming and strengthening the short gland duct and the pore region. The secretory cells are tightly packed into a single-layered, curved glandular epithelium. Secretory cells are separated from each other by thin projections of interstitial sheath cells. The apices of the secretory and sheath cells surround a tubular or vase-shaped extracellular space, the reservoir. The reservoir is traversed by microvilli of the secretory and sheath cells. Two sorts of microvilli characterize the apex of secretory cells: slender, elongated ones located at the periphery (outer microvilli), and shorter but thicker ones, arranged in a distinct collar in the centre (inner microvilli). Secretion, encased in regular secretory granules and discharged only at the apex’ centre, is guided through the space enclosed by the collar of inner microvilli. Though also consisting of numerous cells, the VEGs of Spio spp. are not comparable to parapodial glands described in other spionid taxa since they remain in a strictly intraepidermal position, are distant from parapodia and contain sheath cells. Nonetheless, the VEGs are very helpful for taxonomic work on representatives of the genus Spio and closely related genera.

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References

  • Anctil M (1979) The epithelial luminescent system of Chaetopterus variopedatus. Can J Zool 57:1290–1310

    Article  Google Scholar 

  • Bick A (2005) A new polychaete genus and species of the Kongsfjorden, Spitsbergen, Svalbard. J Nat Hist 39:2987–2996

    Article  Google Scholar 

  • Bick A, Meißner K (2011) Redescription of four species of Spio and Microspio (Polychaeta, Spionidae) from the Kuril Islands and Peter the Great Bay, northwest Pacific. Zootaxa 2968:39–56

    Google Scholar 

  • Clark AW (1965) Microtubules in some unicellular glands of two leeches. Cell Tissue Res 68:568–588

    CAS  Google Scholar 

  • Dauer DM (2000) Functional morphology and feeding behavior of Spio setosa (Polychaeta: Spionidae). Bull Mar Sci 67:269–275

    Google Scholar 

  • Defretin R (1971) The tubes of polychaete annelids. In: Florkin MH, Stolz H (eds) Extracellular and supporting structures. Comp Biochem 26C:713-747

  • Dorsett DA (1961) The behaviour of Polydora ciliata (Johnst.). Tube-building and burrowing. J Mar Biol Assoc UK 41:577–590

    Article  Google Scholar 

  • Dorsett DA, Hyde R (1970a) The spiral glands of Nereis. Cell Tissue Res 110:204–218

    CAS  Google Scholar 

  • Dorsett DA, Hyde R (1970b) The epidermal glands of Nereis. Cell Tissue Res 110:219–230

    CAS  Google Scholar 

  • Eibye-Jacobsen D, Vinther J (2012) Reconstructing the ancestral annelid. J Zool Syst Evol Res 50:85–87

    Article  Google Scholar 

  • Evenkamp H (1931) Morphologie, Histologie und Biologie der Sabellidenspecies Laonome kroyeri Malmgr. und Euchone papillosa M. Sars. Zool Jahrb (Abt Anat Ontog) 53:405–534

    Google Scholar 

  • Gardiner SL (1992) Polychaeta: General organization, integument, musculature, coelom, and vascular system. In: Harrison FH (ed) Microscopic anatomy of invertebrates, vol 7., Annelida. Wiley-Liss, New York, pp 19–52

    Google Scholar 

  • Gelder SR, Jennings JB (1975) The nervous system of the aberrant symbiotic polychaete Histriobdella homari and its implications for the taxonomic position of Histriobdellidae. Zool Anz 194:293–304

    Google Scholar 

  • Gupta BL, Little C (1970) Studies on Pogonophora. 4. Fine structure of the cuticle and epidermis. Tissue & Cell 2:637–696

    Article  CAS  Google Scholar 

  • Hausen H (2005) Comparative structure of the epidermis in polychaetes (Annelida). In: Bartolomaeus T, Purschke G (eds) Morphology, molecules, evolution and phylogeny in Polychaeta and related taxa. Hydrobiologia 535/536:25–35

  • Hausmann K (1982) Electron microscopical studies on Anaitides mucosa (Annelida, Polychaeta). Cuticle and cilia, mucous cells and mucous extrusion. Helgoland Mar Res 35:79–96

    Google Scholar 

  • Hirokawa N, Keller TCS III, Chasan R, Mooseker MS (1983) Mechanism of brush border contractility studied by the quick-freeze, deep-etch method. J Cell Biol 96:1325–1336

    Article  CAS  PubMed  Google Scholar 

  • Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27:137–138

    Google Scholar 

  • Kryvi H (1971) Histology and biochemistry of the mucous glands of Sabella penicillium L. (Annelida, Polychaeta). Nor J Zool (Zool Scr) 19:37–44

    Google Scholar 

  • Kryvi H (1972) The fine structure of the ventral mucous cells of Sabella penicillum (Polychaeta). Sarsia 48:23–32

    Google Scholar 

  • Maciolek NJ (1990) A redescription of some species belonging to the genera Spio and Microspio (Polychaeta: Annelida) and descriptions of three new species from the northwestern Atlantic Ocean. J Nat Hist 24:1109–1141

    Article  Google Scholar 

  • Mastrodonato M, Lepore E, Gherardi M, Zizza S, Sciscioli M, Ferri D (2005) Histochemical and ultrastructural analysis of the epidermal gland cells of Branchiomma luctuosum (Polychaeta, Sabellidae). Inv Biol 124:303–309

    Article  Google Scholar 

  • Mastrodonato M, Gherardi M, Todisco G, Sciscioli M, Lepore E (2006) The epidermis of Timarete filigera (Polychaeta, Cirratulidae): histochemical and ultrastructural analysis of the gland cells. Tissue Cell 38:279–284

    Article  CAS  PubMed  Google Scholar 

  • Matsudaira PT, Burgess DR (1985) Structure and function of the brush-border cytoskeleton. Cold Spring Harb Symp Quant Biol 46:845–854

    Article  Google Scholar 

  • Meißner K (2005) Revision of the genus Spiophanes (Polychaeta: Spionidae); with new synonymies, new records and descriptions of new species. Mitt Mus Naturk Berlin, Zool Reihe 81:3–66

    Google Scholar 

  • Meißner K, Hutchings P (2003) Spiophanes species (Polychaeta: Spionidae) from Eastern Australia—with descriptions of new species, new records and an emended generic diagnosis. Rec Aus Mus 55:117–140

    Article  Google Scholar 

  • Meißner K, Bick A, Bastrop R (2011) On the identity of Spio filicornis (O.F. Müller, 1776)—with the designation of a neotype, and the description of two new species from the North East Atlantic Ocean based on morphological and genetic studies. Zootaxa 2815:1–27

    Google Scholar 

  • Meißner K, Bick A, Müller CHG (2012) Parapodial glandular organs in Spiophanes (Polychaeta: Spionidae)—studies on their functional anatomy and ultrastructure. J Morphol 273:291–311

    Article  Google Scholar 

  • Meißner K, Bick A, Guggolz T, Götting M (2014) Spionidae (Polychaeta: Canalipalpata: Spionida) from seamounts in the Northeast Atlantic. Zootaxa 3786:201–245

    Article  PubMed  Google Scholar 

  • Michel C, DeVillez EJ (1980) Cuticle and mucous glands in the oesophagus of an annelid (Nereis virens). Tissue & Cell 12:673–683

    Article  CAS  Google Scholar 

  • Moermans R (1974) Recherches sur l’histochimie des teguments et du tube d’une annelide polychète (Eunicidae): Hyalinoecia tubicola (O.F. Müller). Bull Biol Fr Bel 108:41–59

    CAS  Google Scholar 

  • Mooseker MS (1976) Brush border motility: microvillar contraction in Triton-treated brush borders isolated from intestinal epithelium. J Cell Biol 71:417–433

    Article  CAS  PubMed  Google Scholar 

  • Müller CHG, Hylleberg J, Michalik P (2014) Complex epidermal organs of Phascolion (Sipunculida): insights into the evolution of bimodal secretory cells in annelids. Acta Zool. doi:10.1111/azo.12082

    Google Scholar 

  • Neff JM (1967) Calcium carbonate tube formation by serpulid polychaete worms: Physiology and ultrastructure. Ph.D. Thesis, Duke University, 305 p

  • Neff JM (1971) Ultrastructure of calcium phosphate-containing cells in the serpulid polychaete worm Pomatoceros caeruleus. Cell Tissue Res 7:191–200

    CAS  Google Scholar 

  • Pflugfelder O (1934) Spinndrüsen und Excretionsorgane der Polyodontidae. Z wiss Zool 145:351–365

    Google Scholar 

  • Richards KS (1977) Structure and function in the oligochaete epidermis (Annelida). In: Sperman RIC (ed) Comparative biology of skin. Symp Zool Soc London 39:171-193

  • Richards KS (1978) Epidermis and cuticle (chapter 2). In: Mill PJ (ed) Physiology of annelids. Academic Press, London, pp 33–61

    Google Scholar 

  • Richardson KC, Jarett L, Finke EH (1960) Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol 35:313–323

    CAS  PubMed  Google Scholar 

  • Rouse GW, Pleijel F (2001) Polychaetes. Oxford University Press, Oxford

    Google Scholar 

  • Shillito B, Lechaire J-P, Gaill F (1993) Microvilli-like structures secreting chitin crystallites. J Struct Biol 111:59–67

    Article  CAS  Google Scholar 

  • Shillito B, Lübbering B, Lechaire J-P, Childress JJ, Gaill F (1995) Chitin localization in the tube secretion system of a repressurized deep-sea tube worm. J Struct Biol 114:67–75

    Article  CAS  Google Scholar 

  • Southward EC (1984) Pogonophora (chapter 17). VI. Annelid-related phyla and cuticle evolution. In: Bereiter-Hahn J, Matoltsy AG, Richards KS (eds) Biology of the integument. 1. Invertebrates. Springer, Berlin, pp 376–388

    Chapter  Google Scholar 

  • Southward EC, Schulze A, Gardiner SL (2005) Pogonophora (Annelida): form and function. In: Bartolomaeus T, Purschke G (eds) Morphology, molecules, evolution and phylogeny in Polychaeta and related taxa. Hydrobiologia 535/536:227–251

  • Sperling EA, Vinther J, Moy VN, Wheeler BM, Sémon M, Briggs DEG, Peterson KJ (2009) MicroRNAs resolve an apparent conflict between annelid systematic and their fossil record. Proc R Soc B 276:4315–4322

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Storch V (1988) I. Integument. In: Westheide W, Hermans CO (eds) The ultrastructure of polychaeta. Microfauna Marina 4. Gustav Fischer-Verlag, Stuttgart, pp 13–36

    Google Scholar 

  • Storch V, Welsch U (1972) The ultrastructure of epidermal mucous cells in marine invertebrates (Nemertini, Polychaeta, Prosobranchia, Opisthobranchia). Mar Biol 13:167–175

    Article  Google Scholar 

  • Struck TH (2011) Direction of evolution within Annelida and the definition of Pleistoannelida. J Zool Syst Evol Res 49:340–345

    Article  Google Scholar 

  • Struck TH, Purschke G, Dordel J, Hösel C, Nesnidal MP, Diersing F, Bleidorn C, Paul C, Hill N, Tiedemann R, Selbig J, Hartmann S (2014) Phylogeny and evolution of Annelida based on molecular data (chapter 9). In: Wägele JW, Bartolomaeus T (eds) Deep metazoan phylogeny: the backbone of the tree of live. New insights from analyses of molecules, morphology, and theory of data analysis. de Gruyter, Berlin, pp 143–160

    Google Scholar 

  • Thomas JG (1940) XXXIII. Pomatoceros, Sabella and Amphitrite. L.M.B.C. Mem Typ Br Pla Anim 33:1–89

    Google Scholar 

  • Truchet M, Vovelle J (1977) Etude de la glande cémentaire d’un Polychète tubicole (Pectinaria (=Lagis) koreni) à l’aide de la microsonde électronique, du microanalyseur ionique et du microscope électronique à balayage. Calcified Tiss Res 24:231–238

    Article  CAS  Google Scholar 

  • Vodopyanov S, Tzetlin A, Zhadan A (2014) The fine structure of epidermal papillae of Travisia forbesii (Annelida). Zoomorphology 133:7–19

    Article  Google Scholar 

  • Vovelle J (1956) Processus glandulaires impliqués dans la réconstitution du tube chez Pomatoceros triqueter L. Annelide Polychète (Serpulidae). Bull Lab Marit Dinard 42:10–32

    Google Scholar 

  • Vovelle J (1979) Les glandes cémentaires de Petta pusilla Malmgren, polychète tubicole Amphictenidae, et sur sécrétion organo-minérale. Arch Zool Exp Gén 120:219–246

    CAS  Google Scholar 

  • Vovelle J, Gaill F (1986) Données morphologiques, histochimiques et microanalytiques sur l’élaboration du tube organominéral d’Alvinella pompejana, Polychète des sources hydrothermales, et leurs implications phylogénétiques. Zool Scr 15:33–43

    Article  Google Scholar 

  • Vovelle J, Rusaouen-Innocent M, Grasset M, Truchet M (1994) Halogenation and quinone-tanning of the organic tube components of some Sabellidae (Annelida Polychaeta). Cah Biol Mar 35:441–459

    Google Scholar 

  • Wang CS, Svendsen KK, Stewart RJ (2010) Morphology of the adhesive system in the sandcastle worm, Phragmatopona californica. In: von Byern J, Grunwald I (eds) Biological adhesive systems. From nature to technical and medical application. Springer, Vienna, pp 169–179

    Google Scholar 

  • Welsch U, Storch V, Richards S (1984) V. Annelida. Epidermal cells (chapter 17). VI. Annelid-related phyla and cuticle evolution. In: Bereiter-Hahn J, Matoltsy AG, Richards KS (eds) Biology of the integument. 1. Invertebrates. Springer, Berlin, pp 269–296

    Chapter  Google Scholar 

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Acknowledgments

Our electron microscopic studies were supported by Prof. Gabriele Uhl from University of Greifswald and PD Dr. Markus Franck and his technician team from the Electron Microscopic Centre of the University of Rostock (Germany). We are grateful for their permission to use their microtomes and transmission electron microscopes. CHGM moreover thanks Prof. Dr. Steffen Harzsch (University of Greifswald, Germany) for having funded standard EM laboratory equipment. We are grateful to Kerstin Schwandt (Rostock University), who did the laboratory work for histological studies, and to Katharina Huckstorf (Rostock University) for giving an introduction into IMARIS software. Sampling permissions were kindly provided by Sra. Margarita Mercadal Camps, chief executive officer of the Direcció General de Medi Rural i Mari (Govern de les Illes Balears, Palma de Mallorca, Spain). We thank two anonymous reviewers for their valuable comments that helped to improve quality of present manuscript.

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The authors declare that they have no conflict of interest.

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All applicable international, national and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors. Informed consent was obtained from all individual participants included in the study.

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Correspondence to Carsten H. G. Müller.

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Communicated by A. Schmidt-Rhaesa.

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Rößger, A., Meißner, K., Bick, A. et al. Histological and ultrastructural reconstruction of ventral epidermal glands of Spio (Polychaeta, Spionidae, Annelida). Zoomorphology 134, 367–382 (2015). https://doi.org/10.1007/s00435-015-0264-9

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