Skip to main content
Log in

“Spinner” cephalopods: defects of statocyst suprastructures in an invertebrate analogue of the vestibular apparatus

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

Individuals of seven species of coleoid cephalopods (three species of octopus, three of squid, and one of cuttlefish), that were cultured and reared in laboratory aquarium systems, had a behavioral defect at hatching which was characterized by an inability to control orientation while swimming. These defective animals were designated as “spinners.”

An examination of statocysts from individuals of five of the affected species revealed abnormalities of the neuroepithelial suprastructures: absence or malformation of the statolith of the gravity receptor system and absence of the cupulae of the angular acceleration receptor systems. The sensory epithelia did not differ from those of normal animals, nor did the synaptic structures and relationships, when examined both with scanning and transmission electron microscopy. The abnormalities were compared with congenital defects of the neuropeithelial suprastructures of the vestibular apparatus (especially in mammals). The defects observed in statocysts of spinner animals are thought to be the result of environmental causes, such as the temperature or chemistry of the seawater in the transportation vessels or rearing systems, rather than genetic causes.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Barber VC (1966) The fine structure of the statocyst of Octopus vulgaris. Z Zellforsch 70:91–107

    Google Scholar 

  • Boletzky S von, Hanion RT (1983) A review of the laboratory maintenance, rearing, an culture of cephalopod molluscs. Mem Nat Mus Victoria 44:136–182

    Google Scholar 

  • Boycott BB (1960) The functioning of the statocysts of Octopus vulgaris. Proc R Soc Lond [Biol] 152:78–87

    Google Scholar 

  • Budelmann BU (1970) Die Arbeitsweise der Statolithenorgane von Octopus vulgaris. Z Vgl Physiol 70:278–312

    Google Scholar 

  • Budelmann BU (1975) Gravity receptor function in cephalopods with particular reference to Sepia officinalis. Fortschr Zool 23:84–96

    Google Scholar 

  • Budelmann BU (1976) Equilibrium receptor systems in molluscs. In: Mill PJ (ed) Structure and function of proprioceptors in the invertebrates. Chapman and Hall, London, pp 529–566

    Google Scholar 

  • Budelmann BU (1977) Structure and function of the angular acceleration receptor systems in the statocysts of cephalopods. Symp Zool Soc Lond 38:309–324

    Google Scholar 

  • Budelmann BU (1978) The function of the equilibrium receptor systems of cephalopods. In: Claussen C-F (ed) Equilibriometric vestibular-spinal tests and their clinical importance. Proceedings of the Neurootological and Equilibriometric Society Vol. IV, edition m + p, Hamburg Neu Isenburg, p 15

  • Budelmann BU, Thies G (1977) Secondary sensory cells in the gravity receptor system of the statocysts of Octopus vulgaris. Cell Tissue Res 182:93–98

    Google Scholar 

  • Budelmann BU, Wolff HG (1976) Mapping of neurons in the gravity receptor system of the Octopus statocyst by iontophoretic cobalt staining. Cell Tissue Res 171:403–406

    Google Scholar 

  • Budelmann BU, Young JZ (1982) Studies on the oculomotor system of Octopus vulgaris. Verh Dtsch Zool Ges 75:266

    Google Scholar 

  • Budelmann BU, Barber VC, West S (1973) Scanning electron microscopical studies of the arrangements and numbers of hair cells in the statocysts of Octopus vulgaris, Sepia officinalis, and Loligo vulgaris. Brain Res 56:25–41

    Google Scholar 

  • Colmers WF (1977) Neuronal and synaptic organization in the gravity receptor system of the statocyst of Octopus vulgaris. Cell Tissue Res 185:491–503

    Google Scholar 

  • Colmers WF (1981) Afferent synaptic connections between hair cells and the somata of intramacular neurons in the gravity receptor system of the statocyst of Octopus vulgaris. J Comp Neurol 197:385–394

    Google Scholar 

  • Colmers WF (1982) The central afferent and efferent organization of the gravity receptor system of the statocyst of Octopus vulgaris. Neuroscience 7:461–476

    Google Scholar 

  • Colmers WF, Hixon RF, Hanlon RT, Forsythe JW, Ackerson MV, Wiederhold ML, Hulet WH (1983) “Spinner” cephalopods — defects of statolith formation in an invertebrate model of the vestibular system. In: Lim DJ (ed) Abstracts of the Sixth Midwinter Research Meeting, Association for Research in Otolaryngology, p 87

  • Crow T, Harrigan JF (1979) Reduced behavioral variability in laboratory-reared Hermissenda crassicomis (Eschscholtz 1831) (Opisthobranchia: nudibranchia). Brain Res 173:179–184

    Google Scholar 

  • Dijkgraaf S (1961) The statocyst of Octopus vulgaris as a rotation receptor. Pubbl Stn Zool Napoli 32:64–87

    Google Scholar 

  • Dilly PN (1976) The structure of some cephalopod statoliths. Cell Tissue Res 175:147–163

    Google Scholar 

  • Erway LC, Hurley LS, Fraser AS (1970) Congenital ataxia and otolith defects due to manganese deficiency in mice. J Nutr 100:643–654

    Google Scholar 

  • Forkel J (1980) Ein Beitrag zur strukturellen Organization der Statocysten frisch geschlüpfter Sepia officinalis. Zulassungsarbeit, Wissenschaftliche Prüfung für das Lehramt an Höheren Schulen, University of Regensburg, Federal Republic of Germany

    Google Scholar 

  • Forsythe JW, Hanlon RT (1980) A closed marine culture system for rearing Octopus joubini and other large-egged benthic octopods. Lab Anim 14:137–142

    Google Scholar 

  • Geuze JJ (1968) Observations on the function and the structure of the statocysts of Lymnaea stagnalis (L.). Neth J Zool 18:155–204

    Google Scholar 

  • Johnsson L-G, Wright CG, Preston RE, Henry PJ (1980) Defects of the otoconial membranes in normal guinea pigs. Acta Otolaryngol 89:93–104

    Google Scholar 

  • Johnsson L-G, Rouse RC, Wright CG, Henry PJ, Hawkins JE Jr (1982) Pathology of neuroepithelial suprastructures of the human inner ear. Am J Otolaryngol 3:77–90

    Google Scholar 

  • Larsen MM (1959) Mouse News Lett 20:49

    Google Scholar 

  • Lim DJ (1980) Morphogenesis and malformation of otoconia: a review. In: Birth defects: original article series, XVI (4), pp 111–146

  • Lim DJ, Erway LC (1974) Influence of manganese on genetically defective otolith. A behavioral and morphological study. Ann Otol Rhinol Laryngol 83:565–581

    Google Scholar 

  • Lim DJ, Erway LC, Clark DL (1978) Tilted-head mice with genetic otoconial anomaly. Behavioural and morphological correlates. In: Hood JD (ed) Vestibular mechanisms in health and disease. Academic Press, London, pp 195–206

    Google Scholar 

  • Lyon MF (1951) Hereditary absence of otoliths in the house mouse. J Physiol (Lond) 114:410–418

    Google Scholar 

  • Purichia N, Erway LC (1972) Effects of dichlorophenamide, zinc and manganese on otolith development in mice. Dev Biol 27:395–405

    Google Scholar 

  • Shrader RE, Everson GJ (1967) Anomalous development of otoliths associated with postural defects in manganese-deficient guinea pigs. J Nutr 91:453–460

    Google Scholar 

  • Stephens PR, Young JZ (1982) The statocyst of the squid Loligo. J Zool (Lond) 197:241–266

    Google Scholar 

  • Wells MJ (1960) Proprioception and visual discrimination of orientation in Octopus. J Exp Biol 37:489–499

    Google Scholar 

  • Wells MJ (1978) Octopus. Physiology and behavior of an advanced invertebrate. Chapman and Hall, London

    Google Scholar 

  • Yang WT, Hanlon RT, Krejci ME, Hixon RF, Hulet WH (1983) Laboratory rearing of Loligo opalescens, the market squid of California. Aquaculture 31:77–88

    Google Scholar 

  • Young JZ (1960) The statocysts of Octopus vulgaris. Proc R Soc Lond [Biol] 152:3–29

    Google Scholar 

  • Young JZ (1971) The anatomy of the nervous system of Octopus vulgaris. Clarendon, Oxford

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Colmers, W.F., Hixon, R.F., Hanlon, R.T. et al. “Spinner” cephalopods: defects of statocyst suprastructures in an invertebrate analogue of the vestibular apparatus. Cell Tissue Res. 236, 505–515 (1984). https://doi.org/10.1007/BF00217217

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00217217

Key words

Navigation