Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-23T00:39:58.193Z Has data issue: false hasContentIssue false
  • English
  • Français

Histochemical and Ultrastructural Characterization of the Posterior Esophagus of Bulla striata (Mollusca, Opisthobranchia)

Published online by Cambridge University Press:  01 October 2010

Alexandre Lobo-da-Cunha ,
Elsa Oliveira ,
Íris Ferreira ,
Rita Coelho  and
Gonçalo Calado
Alexandre Lobo-da-Cunha*
Affiliation:
Laboratory of Cell Biology, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, 4099-003 Porto, Portugal Centre of Marine and Environmental Research (CIIMAR), 4050-123 Porto, Portugal Portuguese Institute of Malacology, 8201-864 Guia, Portugal
Elsa Oliveira
Affiliation:
Laboratory of Cell Biology, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, 4099-003 Porto, Portugal
Íris Ferreira
Affiliation:
Laboratory of Cell Biology, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, 4099-003 Porto, Portugal
Rita Coelho
Affiliation:
Portuguese Institute of Malacology, 8201-864 Guia, Portugal
Gonçalo Calado
Affiliation:
Portuguese Institute of Malacology, 8201-864 Guia, Portugal Lusophone Universityof Humanities and Technologies, 1749-024 Lisbon, Portugal Institute for Marine Research (IMAR), FCT/UNL, 2829-516 Caparica, Portugal
*
Corresponding author. E-mail: [email protected]
Get access

Abstract

The posterior esophagus of Bulla striata, running from the gizzard to the stomach, was investigated with light and electron microscopy to obtain new data for a comparative analysis of the digestive system in cephalaspidean opisthobranchs. In this species, the posterior esophagus can be divided into two regions. In the first, the epithelium is formed by columnar cells with apical microvilli embedded in a cuticle. Many epithelial and subepithelial secretory cells are present in this region. In both, electron-lucent secretory vesicles containing filaments and a peripheral round mass of secretory material fill the cytoplasm. These acid mucus-secreting cells may also contain a few dense secretory vesicles. In the second part of the posterior esophagus, the cuticle is absent and the epithelium is ciliated. In this region, epithelial cells may contain larger lipid droplets and glycogen reserves. Subepithelial secretory cells are not present, and in epithelial secretory cells the number of dense vesicles increases, but most secretory cells still contain some electron-lucent vesicles. These cells secrete a mixture of proteins and acid polysaccharides and should be considered seromucous. The secretory cells of the posterior esophagus are significantly different from those previously reported in the anterior esophagus of this herbivorous species.

Keywords

TEMcytochemistrydigestive tractsecretory cellsepithelial cellsGastropoda
Type
Special Section from Portugal Meeting
Information
Microscopy and Microanalysis , Volume 16 , Issue 6 , December 2010 , pp. 688 - 698
Copyright
Copyright © Microscopy Society of America 2010

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

Andrews, E.B. (1992). The fine structure and function of the anal gland of the muricid Nucella lapillus (Neogastropoda) (and a comparison with that of the trochid Gibbula cineraria). J Moll Stud 58, 297–313.Google Scholar
Bloom, F.E. & Aghajanian, G.K. (1968). Fine structural and cytochemical analysis of the staining of synaptic junctions with phosphotungstic acid. J Ultastruct Res 22, 361–375.CrossRefGoogle ScholarPubMed
Boer, H.H. & Kits, K.S. (1990). Histochemical and ultrastructural study of the alimentary tract of the freshwater snail Lymnaea stagnalis. J Morphol 205, 97–111.Google Scholar
Bourne, N.B., Jones, G.W. & Bowen, I.D. (1991). Endocytosis in the crop of the slug, Deroceras reticulatum (Müller) and the effects of the ingested molluscicides, metaldehyde and methiocarb. J Moll Stud 57, 71–80.Google Scholar
Bush, M.S. (1989). The ultrastructure and function of the oesophagus of Patella vulgata Linnaeus. J Moll Stud 55, 111–124.CrossRefGoogle Scholar
Charrier, M., Fonty, G., Gaillard-Martinie, B., Ainouche, K. & Andant, G. (2006). Isolation and characterization of cultivable fermentative bacteria from the intestine of two edible snails, Helix pomatia and Cornu aspersum (Gastropoda: Pulmonata). Biol Res 39, 669–681.CrossRefGoogle ScholarPubMed
Dimitriadis, V.K., Hondros, D. & Pirpasopoulou, A. (1992). Crop epithelium of normal fed, starved and hibernated snails Helix lucorum: A fine structural-cytochemical study. Malacologia 34, 343–354.Google Scholar
Fretter, V. (1939). The structure and function of the alimentary canal of some tectibranch molluscs, with a note on excretion. Trans R Soc Edinb 59, 599–646.Google Scholar
Fretter, V. & Ko, B.H. (1979). The specialization of the Aplysiid gut. Malacologia 18, 7–11.Google Scholar
Ganter, P. & Jollès, G. (1970). Histochimie Normal et Pathologique, 2. Paris: Gauthier-Villars.Google Scholar
Howells, H. (1942). The structure and function of the alimentary canal of Aplysia punctata. Q J Microsc Sci 83, 357–397.Google Scholar
Hunt, S. & Nixon, M. (1981). A comparative study of protein composition in the chitin-protein complexes of the beak, pen, sucker, radula and oesophageal cuticle of the cephalopods. Comp Biochem Physiol B68, 535–546.Google Scholar
Jones, R. & Reid, L. (1973). The effect of pH on Alcian Blue staining of epithelial acid glycoproteins. I. Sialomucins and sulphomucins (singly or in simple combinations). Histochem J 5, 9–18.Google Scholar
Klussmann-Kolb, A. & Brodie, G.D. (1999). Internal storage and production of symbiotic bacteria in the reproductive system of a tropical marine gastropod. Mar Biol 133, 443–447.CrossRefGoogle Scholar
Knight, D.P. & Lewis, P.R. (1992). General cytochemical methods. In Practical Methods in Electron Microscopy, 14, Glauert, A.M. (Ed.), pp. 79–138. Amsterdam: Elsevier.Google Scholar
Lane, B.P. & Europa, D.L. (1965). Differential staining of ultrathin sections of Epon-embedded tissues for light microscopy. J Histochem Cytochem 13, 579–582.Google Scholar
Lobo-da-Cunha, A. & Batista-Pinto, C. (2003). Stomach cells of Aplysia depilans (Mollusca, Opisthobranchia): A histochemical, ultrastructural, and cytochemical study. J Morphol 256, 360–370.CrossRefGoogle ScholarPubMed
Lobo-da-Cunha, A. & Batista-Pinto, C. (2005). Light and electron microscopy studies of the oesophagus and crop epithelium in Aplysia depilans (Mollusca, Opisthobranchia). Tissue & Cell 37, 447–456.CrossRefGoogle ScholarPubMed
Lobo-da-Cunha, A. & Calado, G. (2008). Histological and ultrastructural study of the salivary glands of Bulla striata (Mollusca, Opisthobranchia). Invert Biol 127, 33–44.CrossRefGoogle Scholar
Lobo-da-Cunha, A., Ferreira, I., Coelho, R. & Calado, G. (2009). Light and electron microscopy study of the salivary glands of the carnivorous opisthobranch Philinopsis depicta (Mollusca, Gastropoda). Tissue & Cell 41, 367–375.Google Scholar
Lobo-da-Cunha, A., Oliveira, E., Alves, A., Coelho, R. & Calado, G. (2010). Light and electron microscopic study of the anterior oesophagus of Bulla striata (Mollusca, Opisthobranchia). Acta Zool 91, 125–138.Google Scholar
Malaquias, M.A.E., Bericibar, E. & Reid, D. (2009a). Reassessment of the trophic position of Bullidae (Gastropoda: Cephalaspidea) and the importance of diet in the evolution of cephalaspidean gastropods. J Zool 227, 88–97.Google Scholar
Malaquias, M.A.E., Dodds, J.M., Bouchet, P. & Reid, D.G. (2009b). A molecular phylogeny of the Cephalaspidea sensu lato (Gastropoda: Euthyneura): Architectibranchia redefined and Runcinacea reinstated. Zool Scr 38, 23–41.CrossRefGoogle Scholar
Malaquias, M.A.E. & Reid, D. (2008). Systematic revision of living species of Bullidae (Mollusca: Gastropoda: Cephalaspidea), with a molecular phylogenetic analysis. Zool J Linn Soc 153, 453–543.CrossRefGoogle Scholar
Payne, C.M. & Crisp, M. (1989). Ultrastructure and histochemistry of the posterior oesophagus of Nassarius reticulatus (Linnaeus). J Moll Stud 55, 313–321.CrossRefGoogle Scholar
Rudman, W.B. (1971). Structure and functioning of the gut in the Bullomorpha (Opisthobranchia). Part 1. Herbivores. J Nat Hist 5, 647–675.CrossRefGoogle Scholar
Rudman, W.B. (1972a). Structure and functioning of the gut in the Bullomorpha (Opisthobranchia). Part 2. Acteonidae. J Nat Hist 6, 311–324.CrossRefGoogle Scholar
Rudman, W.B. (1972b). Structure and functioning of the gut in the Bullomorpha (Opisthobranchia). Part 3. Philinidae. J Nat Hist 6, 459–474.CrossRefGoogle Scholar
Rudman, W.B. (1972c). Structure and functioning of the gut in the Bullomorpha (Opisthobranchia). Part 4. Aglajidae. J Nat Hist 6, 547–560.Google Scholar
Rudman, W.B. & Willan, R.C. (1998). Opistobranchia. In Mollusca: The Southern Synthesis. Fauna of Australia, 5, Beesley, P.L., Ross, G.J.B. & Wells, A. (Eds.), pp. 915–1035. Melbourne: CSIRO Publishing.Google Scholar
Sannes, P.L., Katsuyama, T. & Spicer, S. (1978). Tannic acid-metal salt sequences for light and electron microscopic localization of complex carbohydrates. J Histochem Cytochem 26, 55–61.Google Scholar
Stockert, J.C. & Pelling, C. (1994). Reactivity of protamines and model guadininium compounds with tungsten and molybdenum heteropolyacids. Biocell 18, 77–87.Google Scholar
Tandler, B. & Phillips, C.J. (1993). Structure of serous cells in salivary glands. Microsc Res Tech 26, 32–48.CrossRefGoogle ScholarPubMed
Tas, J. (1975). Histochemical conditions influencing metachromatic staining. A comparative study by means of a model system of polyacrylamide films. Histochem J 7, 1–19.Google Scholar
Tato, A., Ferrer, J.M. & Stockert, J.C. (2000). Electron microscopic contrast of the cytoskeleton and junctional complexes of intestinal epithelial cells by ethanolic phosphotungstic acid. Eur J Morphol 38, 134–141.CrossRefGoogle ScholarPubMed
Thiéry, J.P. (1967). Mise en évidence des polysaccharides sur coupes fines en microscopie électronique. J Microsc 6, 987–1018.Google Scholar
Wägele, H. (2004). Potential key characters in Opisthobranchia (Gastropoda, Mollusca) enhancing adaptive radiation. Org Div Evol 4, 175–188.Google Scholar
Wägele, H. & Klussmann-Kolb, A. (2005). Opisthobranchia (Mollusca, Gastropoda)—More than just slimy slugs. Shell reduction and its implications on defence and foraging. Front Zool 2(3), 1–18.Google Scholar
Walker, A.J., Glen, D.M. & Shewry, P.R. (1999). Bacteria associated with the digestive system of the slug Deroceras reticulatum are not required for protein digestion. Soil Biol Biochem 31, 1387–1394.Google Scholar
Walker, G. (1972). The digestive system of the slug, Agriolimax reticulatus (Müller): Experiments on phagocytosis and nutrient absorption. Proc Malac Soc Lond 40, 33–43.Google Scholar