Acta Biologica Hungarica

, Volume 63, Supplement 2, pp 129–140 | Cite as

Morphology, Ultrastructure and Contractile Properties of Muscles Responsible for Superior Tentacle Movements of the Snail

  • Nóra Krajcs
  • L. Márk
  • K. Elekes
  • T. KissEmail author


Bending, twitching and quivering are different types of tentacle movements observed during olfactory orientation of the snail. Three recently discovered special muscles, spanning along the length of superior tentacles from the tip to the base, seem to be responsible for the execution of these movements. In this study we have investigated the ultrastructure, contractile properties and protein composition of these muscles. Our ultrastructural studies show that smooth muscle fibers are loosely embedded in a collagen matrix and they are coupled with long sarcolemma protrusions. The muscle fibers apparently lack organized SR and transverse tubular system. Instead subsarcolemmal vesicles and mitochondria have been shown to be possible Ca2+ pools for contraction. It was shown that external Ca2+ is required for contraction elicited by high (40 mM) K+ or 10−4 M ACh. Caffeine (5 mM) induced contraction in Ca2+-free solution suggesting the presence of a substantial intracellular Ca2+ pool. High-resolution electrophoretic analysis of columellar and tentacular muscles did not reveal differences in major contractile proteins, such as actin, myosin and paramyosin. Differences were observed however in several bands representing presumably regulatory enzymes. It is concluded that, the ultrastructural, biochemical and contractile properties of the string muscles support their special physiological function.


String muscles Helix ultrastructure contractile properties contractile proteins 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Bone, Q., Inoue, I., Tsutsui, I. (1997) Contraction and relaxation in the absence of a sarcoplasmic reticulum: muscle fibres in the small pelagic tunicate Doliolum. J. Muscle Res. Cell. Motil. 18, 375–380.CrossRefGoogle Scholar
  2. 2.
    Brooks, D. D., Huddart, H., Lennard, R., Hill, R. B. (1990) Calcium utilization in contractures induced by acetylcholine or high-potassium saline in molluscan proboscis muscles. J. Exp. Biol. 149, 379–394.Google Scholar
  3. 3.
    Chase, R., Hall, B. (1996) Nociceptive inputs to C3, a motoneuron of the tentacle withdrawal reflex in Helix aspersa. J. Comp. Physiol. A 179, 809–818.CrossRefGoogle Scholar
  4. 4.
    Chase, R., Pryer, K., Baker, R., Medison, D. (1978) Responses to conspecific chemical stimuli in the terrestrial snail Achatina fulica. Behav. Biol. 22, 302–315.CrossRefGoogle Scholar
  5. 5.
    Chen, C.-J. (1983) A study of the longitudional body wall muscle of the sea cucumber Sclerodactyla briareus. PhD thesis, University of Rhode Island, USA.Google Scholar
  6. 6.
    Cianchetti, M., Arienti, A., Follador, M., Mazzolai, B., Dario, P., Laschi, C. (2011) Design concept and validation of a robotic arm inspired by the octopus. Mat. Sci. Eng. 31, 1230–1239.CrossRefGoogle Scholar
  7. 7.
    Dorsett, D. A., Roberts, J. B. (1980) A transverse tubular system and neuromuscular junctions in a molluscan unstriated muscle. Cell Tissue Res. 206, 251–260.CrossRefGoogle Scholar
  8. 8.
    Emery, D. G. (1992) Fine structure of olfactory epithelia of gastropod molluscs. Microsc. Res. Tech. 22, 307–324.CrossRefGoogle Scholar
  9. 9.
    Frescura, M., Hodgson, A. N. (1989) On collagen and its potential role in the columellar muscle of some gastropod molluscs. Suid-Afrikaanse Tydskrif Vir Wetenskap, 85, 613–614.Google Scholar
  10. 10.
    Gelperin, A. (1974) Olfactory basis of homing behavior in the giant garden slug, Limax maximus. Proc. Nat. Acad. Sci. USA 71, 966–970.CrossRefGoogle Scholar
  11. 11.
    Hernádi, L., Teyke, T. (2012) Novel triplet of flexor muscles in the posterior tentacles of the snail, Helix pomatia. Acta Biol. Hung. 63 (Suppl. 2) 123–128.CrossRefGoogle Scholar
  12. 12.
    Hill, R. B. (2001) Role of Ca2+ in excitation-contraction coupling in echinoderm muscle: comparison with role in other tissues. J. Exp. Biol. 204, 897–908.PubMedGoogle Scholar
  13. 13.
    Huddart, H., Hunt, S., Oates, K. (1977) Calcium movements during contraction in molluscan smooth muscle, and the loci of calcium binding and release. J. Exp. Biol. 68, 45–56.PubMedGoogle Scholar
  14. 14.
    Kendrick-Jones, J., Lehman, W., Szent-Györgyi, A. G. (1970) Regulation in molluscan muscles. J. Mol. Biol. 54, 313.CrossRefGoogle Scholar
  15. 15.
    Kier, W. M. (1992) Hydrostatic skeletons and muscular hydrostats. In: Biewener, A. A. (ed.) Biomechanics (Structure and Systems): A Practical Approach. Oxford Univ. Press, New York, pp. 205–231.Google Scholar
  16. 16.
    Kier, W. M., Schachat, F. H. (1992) Biochemical comparison of fast- and slow-contracting squid muscle. J. Exp. Biol. 168, 41–56.PubMedGoogle Scholar
  17. 17.
    Kier, W. M., Stella, M. P. (2007) The arrangement and function of Octopus arm musculature and connective tissue. J. Morphol. 268, 831–843.CrossRefGoogle Scholar
  18. 18.
    Laemmili, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 277, 680–685.CrossRefGoogle Scholar
  19. 19.
    Lemaire, M., Chase, R. (1998) Twitching and quivering of the tentacles during snail olfactory orientation. J. Comp. Physiol. A 182, 81–87.CrossRefGoogle Scholar
  20. 20.
    Lüllmann, H., Sunano, S. (1973) Acetylcholine contracture and excitation-contraction coupling in denervated rat diaphragm muscle. Pflügers Arch. 342, 271–282.CrossRefGoogle Scholar
  21. 21.
    Margulis, B. A., Galaktionov, K. I., Podgornaya, O. I., Pinaev, G. P. (1982) Major contractile proteins of mollusc: tissue polymorphism of actin, tropomyosin and myosin light chains is absent. Comp. Biochem. Physiol. B 72, 473–476.CrossRefGoogle Scholar
  22. 22.
    Moore, P. A., Atema, J., Gerhard, G. A. (1991) Fluid dynamics and microscale chemical movement in the chemosensory appendages of the lobster, Homarus americanus. Chem. Senses 16, 663–674.CrossRefGoogle Scholar
  23. 23.
    Motokawa, T. (1982) Factors regulating the mechanical properties of holothurian dermis. J. Exp. Biol. 99, 29–41.Google Scholar
  24. 24.
    Peschel, M., Straub, V., Teyke, T. (1996) Consequences of food-attraction conditioning in Helix: a behavioral and electrophysiological study. J. Comp. Physiol. A 178, 317–327.CrossRefGoogle Scholar
  25. 25.
    Prescott, S. A., Gill, N., Chase, R. (1997) Neural circuit mediating tentacle withdrawal in Helix aspersa, with specific reference to the competence of the motor neuron C3. J. Neurophysiol. 78, 2951–2965.CrossRefGoogle Scholar
  26. 26.
    Rigon, F., Manica, G., Guma, F., Achaval, M., Faccioni-Heuser, M. C. (2010) Ultrastructural features of the columellar muscle and contractile protein analyses in different muscle groups of Megalobulimus abbreviatus. Tissue Cell. 42, 53–60.CrossRefGoogle Scholar
  27. 27.
    Somlyo, A. P. (1972) Excitation-contraction coupling in vertebrate smooth muscle: Correlation of ultrastructure with function. Physiologist 15, 338–348.PubMedGoogle Scholar
  28. 28.
    Treiman, M., Caspersen, C., Christensen, S. B. (1998) A tool coming of age: Thapsigargin as an inhibitor of sarco-endoplasmic reticulum Ca2+-ATPases. TIPS 19, 131–135.PubMedGoogle Scholar
  29. 29.
    Wilkie, I. C. (1996) Mutable collagenous structure or not? A comment on the re-interpretation by del Castillo et al. of the catch mechanism in the sea urchin spine ligament. Biol. Bull. 190, 237–242.CrossRefGoogle Scholar
  30. 30.
    Zakharov, I. S. (1992) Avoidance behavior of the snail. J. Higher Nerv. Act. 42, 1156–1169. (in Russian)Google Scholar

Copyright information

© Akadémiai Kiadó, Budapest 2012

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (, which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  1. 1.Department of Experimental ZoologyMTA Centre for Ecological Research, Balaton Limnological InstituteTihanyHungary
  2. 2.Department of Biochemistry and Medical ChemistryMedical School, University of PécsPécsHungary

Personalised recommendations