Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-23T06:40:30.024Z Has data issue: false hasContentIssue false
  • English
  • Français

Ultrastructural characterization of the adhesive organ of Idiosepius biserialis and Idiosepius pygmaeus (Mollusca: Cephalopoda)

Published online by Cambridge University Press:  14 March 2011

Norbert Cyran ,
Waltraud Klepal  and
Janek von Byern
Norbert Cyran*
Affiliation:
Core Facility of Cell Imaging and Ultrastructural Research, Faculty of Life Sciences, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria
Waltraud Klepal
Affiliation:
Core Facility of Cell Imaging and Ultrastructural Research, Faculty of Life Sciences, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria
Janek von Byern
Affiliation:
Core Facility of Cell Imaging and Ultrastructural Research, Faculty of Life Sciences, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria
*
Correspondence should be addressed to: N. Cyran, Core Facility of Cell Imaging and Ultrastructural Research, Faculty of Life Sciences, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Water drift and tidal rise make the use of bonding mechanisms beneficial for small benthopelagic or interstitial marine animals. Chemical adhesives for attachment are very common in molluscs; however, only a few cephalopods have glue producing organs. The family Idiosepiidae is characterized by an epithelial adhesive organ (AO) located on the posterior part of the dorsal mantle area. Previous morphological and histological studies described three non-glandular cell types (basal, interstitial and fusiform cells) and three glandular cell types (goblet, columnar and granular cells) containing protein and carbohydrate components. However, these studies provide different information about the nomenclature and characteristics of the cell types. The present ultrastructural analyses and a 3D reconstruction of the AO of Idiosepius pygmaeus and Idiosepius biserialis therefore serve to investigate the cell distribution, the fine structure of the cells and possible interactions between the cells.We found that basal cells form a continuous cell layer along the basal membrane, overlapped by the other epithelial cells. Embedded in microvilli-covered interstitial cells the glandular cells are more or less evenly distributed within the AO. Goblet and granular cells are solitary glandular cells without conspicuous morphological characteristics, whereas the columnar cells are arranged in dense aggregations of 5–15 cells. Each columnar cell is enclosed by a narrow supporting interstitial cell which contains dense longitudinal filament strands. The secretory process of the cells in the aggregation is synchronized. Each columnar cell aggregate bears approximately two ciliated sensory fusiform cells. The fusiform cells are connected to a neuronal network, aligned along the epithelium base.The results suggest that the bonding system is affected by two secretory cell types (granular and columnar cells). Both are similar in content, synthesis and secretory process but columnar cells are embedded in a particular cell environment. It is unclear in what way this arrangement is associated with the function of the AO. The neurons in several parts of the AO point to a neuronal control of the bonding mechanism. Comparisons with the AO cells of other cephalopods provide no indications for a morphological relationship between the adhesive systems.

Keywords

ultrastructureadhesive organadhesioncephalopodglandular structureglueglue synthesis
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 91 , Issue 7 , November 2011 , pp. 1499 - 1510
Copyright
Copyright © Marine Biological Association of the United Kingdom 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Appellöf, A. (1898) Cephalopoden von Ternate. Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft 24, 570–637.Google Scholar
Cyran, N.von Byern, J. and Klepal, W. (2005) Ultrastructure of the adhesive organ of Idiosepius (Mollusca, Cephalopoda). Microscopy Conference 6. Dreiländertagung 28.08.–02.09.2005. Davos: Paul Scherrer Institut, 164 pp.Google Scholar
Flammang, P. (2006) Adhesive secretions in echinoderms: an overview. In Smith, A.M. and Callow, J.A. (eds) Biological adhesives. Heidelberg: Springer-Verlag, pp. 183–206.CrossRefGoogle Scholar
Fukuda, Y. (1980) Observations by SEM. In Hamada, T., Obata, I. and Okutani, T. (eds) Nautilus macromphalus in captivity—Japanese expert consultation on living Nautilus. Tokyo: Tokai University Press, pp. 23–33.Google Scholar
Fukuda, Y. (1988) Histology of the long digital tentacles. In Saunders, W.B. and Landman, N.H. (eds) Nautilus. The biology and paleobiology of a living fossil. New York: Plenum Publishing Corporation, pp. 249–256.Google Scholar
Gay, C. (2002) Stickiness—some fundamentals of adhesion. Integrative and Comparative Biology 42, 1123–1126.CrossRefGoogle ScholarPubMed
Gay, C. and Leibler, L. (1999) On stickiness. Physics Today 52, 48–52.CrossRefGoogle Scholar
Hermans, C.O. (1983). The duo-gland adhesive system. Oceanography and Marine Biology: an Annual Review 21, 283–339.Google Scholar
Kier, W.M. (1987) The functional morphology of the tentacle musculature of Nautilus pompilius. In Saunders, W.B. and Landman, N.H. (eds) Nautilus. The biology and paleobiology of a living fossil. New York: Plenum Publishing Corporation, pp. 257–269.CrossRefGoogle Scholar
Kier, W.M. and Smith, A.M. (2002) The structure and adhesive mechanism of Octopus suckers. Integrative and Comparative Biology 42, 1146–1153.CrossRefGoogle ScholarPubMed
Muntz, W.R.A. and Wentworth, S.L. (1995) Structure of the adhesive surface of the digital tentacles of Nautilus pompilius. Journal of the Marine Biological Association of the United Kingdom 75, 747–750.CrossRefGoogle Scholar
Nesis, K. (1982) Cephalopods of the world. An annotated and illustrated catalogue of species known to date. In Burgess, L. A. (eds) Translated from Russian by B.S. Levitov. V.A.A.P. Copyright Agency of the UdSSR for Light and Food Industry Publishing House; Moscow, 1987 T.F.H. Publications, Inc. Ltd., for English Translation, 351 pp.Google Scholar
Pennisi, E. (2002) Biology reveals new ways to hold on tight. Science 296, 250–251.CrossRefGoogle ScholarPubMed
Reynolds, E.S. (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. Journal of Cell Biology 17, 208–212.CrossRefGoogle ScholarPubMed
Roeleveld, M.A.C. (1972) A review of the Sepiidae (Cephalopoda) of Southern Africa. Annals of the South African Museum 59, 193–313.Google Scholar
Ruth, P., Schmidtberg, H., Westermann, B. and Schipp, R. (2002) The sensory epithelium of the tentacles and the rhinophore of Nautilus pompilius L. (Cephalopoda, Nautiloidea). Journal of Morphology 251, 239–255.CrossRefGoogle ScholarPubMed
Sasaki, M. (1921) On an adhering habit of a pygmy cuttlefish, Idiosepius pygmaeus Steenstrup. Annotationes Zoologicae Japonenses 10, 209–213.Google Scholar
Singley, C.T. (1982) Histochemistry and fine structure of the ectodermal epithelium of the sepiolid squid Euprymna scolopes. Malacologia 23, 177–192.Google Scholar
Smith, A.M. (1996) Cephalopod sucker design and the physical limits to negative pressure. Journal of Experimental Biology 199, 949–958.CrossRefGoogle ScholarPubMed
Smith, A.M. (2006). The biochemistry and mechanics of gastropod adhesive gels. In Smith, A.M. and Callow, J.A. (eds) Biological adhesives. Heidelberg: Springer-Verlag, pp. 167–182CrossRefGoogle Scholar
Steenstrup, J. (1881) Sepiadarium and Idiosepius two new genera of the family of Sepia. With remarks on the two related forms Sepioloidea d'Orb. and Spirula Lmk. Det Kongelige Danske Videnskabernes Selskabs skrifter Raekke 6, 211–242.Google Scholar
Suwanmala, J., von Byern, J. and Nabhitabhata, J. (2006) Observation of Idiosepius pygmaeus (Cephalopoda, Idiosepiidae) at Klong Bangrong, Phuket Island, Thailand. Phuket Marine Biological Center Research Bulletin 67, 49–51.Google Scholar
Tyler, S. (1976) Comparative ultrastructure of adhesive systems in the Turbellaria. Zoomorphology 84, 1–76.CrossRefGoogle Scholar
Tyler, S. (1988) The role of function in determination of homology and convergence-examples from invertebrate adhesive organs. Fortschritte der Zoologie 36, 331–347.Google Scholar
Tyler, S. and Rieger, G.E. (1980) Adhesive organs of the Gastrotricha I. Duo-gland organs. Zoomorphology 95, 1–15.CrossRefGoogle Scholar
von Boletzky, S. and Roeleveld, M.A.C. (2000) ‘Ventral adhesion’ to hard substrates: a thigmotactic response in sepiid cuttlefish (Mollusca, Cephalopoda). Vie et Milieu 50, 59–64.Google Scholar
von Byern, J. and Klepal, W. (2006) Adhesive mechanisms in cephalopods: a review. Biofouling 22, 329–338.CrossRefGoogle ScholarPubMed
von Byern, J., Rudoll, L.Cyran, N. and Klepal, W. (2008) Histochemical characterization of the adhesive organ of three Idiosepius spp. species. Biotechnic & Histochemistry 83, 29–46.CrossRefGoogle ScholarPubMed