Cell and Tissue Research

, Volume 325, Issue 2, pp 333–343 | Cite as

Rhopalia are integrated parts of the central nervous system in box jellyfish

Regular Article

Abstract

In cubomedusae, the central nervous system (CNS) is found both in the bell (the ring nerve) and in the four eye-bearing sensory structures (the rhopalia). The ring nerve and the rhopalia are connected via the rhopalial stalks and examination of the structure of the rhopalial stalks therefore becomes important when trying to comprehend visual processing. In the present study, the rhopalial stalk of the cubomedusae Tripedalia cystophora has been examined by light microscopy, transmission electron microscopy, and electrophysiology. A major part of the ring nerve is shown to continue into the stalk and to contact the rhopalial neuropil directly. Ultrastructural analysis of synapse distribution in the rhopalial stalk has failed to show any clustering, which indicates that integration of the visual input is probably spread throughout the CNS. Together, the results indicate that cubomedusae have one coherent CNS including the rhopalia. Additionally, a novel gastrodermal nerve has been found in the stalk; this nerve is not involved in visual processing but is likely to be mechanosensory and part of a proprioceptory system.

Keywords

Rhopalia Eyes CNS Synapse Tripedalia cystophora, jellyfish (Cnidaria: Cubozoa) 

References

  1. Anderson PAV, Moosler A, Grimmelikhuijzen CJP (1992) The presence and distribution of antho-RFamide-like material in scyphomedusae. Cell Tissue Res 267:67–74CrossRefPubMedGoogle Scholar
  2. Berger EW (1898) The histological structure of the eyes of cubomedusae. J Comp Neurol 8:223–230CrossRefGoogle Scholar
  3. Buskey EJ (2003) Behavioral adaptations of the cubozoan medusa Tripedalia cystophora for feeding on copepod (Dioithona oculata) swarms. Mar Biol 142:225–232Google Scholar
  4. Chapman DM (1978) Microanatomy of the cubopolyp, Tripedalia cystophora (class Cubozoa). Helgoländer Wiss Meeresunters 31:128–168CrossRefGoogle Scholar
  5. Claus C (1878) Ueber Charybdea marsupialis. Arbeiten Zool Instit Universität Wien 1:1–56Google Scholar
  6. Derby CD (1995) Single unit electrophysiological recordings from crustacean chemoreceptor neurons. In: Spielman AI, Brand JG (eds) Experimental cell biology of taste and olfaction. Current techniques and protocols. CRC Press, New York, pp 241–250Google Scholar
  7. Grimmelikhuijzen CJP (1985) Antisera to the sequence Arg-Phe-amide visualize neuronal centralization in hydroid polyps. Cell Tissue Res 241:171–182CrossRefGoogle Scholar
  8. Grimmelikhuijzen CJP, Spencer AN (1984) FMRFamide immunoreactivity in the nervous system of the medusa Polyorchis penicillatus. J Comp Neurol 230:361–371CrossRefPubMedGoogle Scholar
  9. Grimmelikhuijzen CJP, Spencer AN, Carré D (1986) Organization of the nervous system of physonectid siphonophores. Cell Tissue Res 246:463–479CrossRefGoogle Scholar
  10. Hartwick RF (1991) Observations on the anatomy, behaviour, reproduction and life cycle of the cubozoan Carybdea sivickisi. Hydrobiologia 216/217:171–179CrossRefGoogle Scholar
  11. Kinsey B (1986) Barnes on box jellyfish. James Cook University, TownsvilleGoogle Scholar
  12. Laska G, Hündgen M (1982) Morphologie und Ultrastruktur der Lichtsinnesorgane von Tripedalia cystophora Conant (Cnidaria, Cubozoa). Zool Jb Anat 108:107–123Google Scholar
  13. Laska G, Hündgen M (1984) Die Ultrastructur des neuromuskuläre Systems der Medusen von Tripedalia cystophora und Carybdea marsupialis (Coelenterata, Cubozoa). Zoomorphology 104:163–170CrossRefGoogle Scholar
  14. Lewis C, Long TAF (2005) Courtship and reproduction in Carybdea sivickisi (Cnidaria: Cubozoa). Mar Biol 147:477–483CrossRefGoogle Scholar
  15. Mackie GO (1971) Neurological complexity in medusae: a report of central nervous organization in Sarsia. Actas del I Simposio International de Zoofilogenia. University of Salamanca, Salamanca, pp 269–280Google Scholar
  16. Mackie GO (2004) Central neural circuitry in the jellyfish Aglantha: a model "simple nervous system”. Neuro-Signals 13:5–19PubMedCrossRefGoogle Scholar
  17. Mackie GO, Meech RW (1995a) Central circuitry in the jellyfish Aglantha digitale. I. The relay system. J Exp Biol 198:2261–2270PubMedGoogle Scholar
  18. Mackie GO, Meech RW (1995b) Central circuitry in the jellyfish Aglantha digitale. II. The ring gigant and carrier systems. J Exp Biol 198:2271–2278PubMedGoogle Scholar
  19. Mackie GO, Meech RW (2000) Central circuitry in the jellyfish Aglantha digitale. III. The rootlet and pacemaker systems. J Exp Biol 203:1797–1807PubMedGoogle Scholar
  20. Martin VJ (2002) Photoreceptors of cnidarians. Can J Zool 80:1703–1722CrossRefGoogle Scholar
  21. Martin VJ (2004) Photoreceptors of cubozoan jellyfish. Hydrobiologia 530/531:135–144CrossRefGoogle Scholar
  22. Moroz L, Meech RW, Sweedler JV, Mackie GO (2004) Nitric oxide regulates swimming in the jellyfish Aglantha digitale. J Comp Neurol 471:26–36CrossRefPubMedGoogle Scholar
  23. Nilsson DE, Coates M, Gislén l, Skogh C, Garm A (2005) Advanced optics in a jellyfish eye. Nature 435:201–205CrossRefPubMedGoogle Scholar
  24. Parkefelt L, Skogh C, Nilsson DE, Ekström P (2005) Bilateral symmetric organization of neural elements in the visual system of a coelenterate, Tripedalia cystophora (Cubozoa).J Comp Neurol 492:251–262CrossRefPubMedGoogle Scholar
  25. Satterlie RA (1979) Central control of swimming in the cubomedusan jellyfish Carybdea rastonii. J Comp Physiol [A] 133:357–367CrossRefGoogle Scholar
  26. Satterlie RA (2002) Neural control of swimming in jellyfish: a comparative story. Can J Zool 80:1654–1669CrossRefGoogle Scholar
  27. Satterlie RA, Spencer AN (1979) Swimming control in a cubomedusan jellyfish. Nature 231:141–142CrossRefGoogle Scholar
  28. Satterlie RA, Nolen TG (2001) Why do cubomedusae have only four swim pacemakers? J Exp Biol 204:1413–1419PubMedGoogle Scholar
  29. Singla CL (1978) Locomotion and neuromuscular system of Agantha digitale. Cell Tissue Res 188:317–327CrossRefPubMedGoogle Scholar
  30. Singla CL, Weber C (1982a) Fine structure of the ocelli of Polyorchis penicillatus (Hydrozoa: Anthomedusae) and their connection with the nerve ring. Zoomorphology 99:117–129CrossRefGoogle Scholar
  31. Singla CL, Weber C (1982b) Fine structure of the ocellus of Sarsia tubulosa (Hydrozoa, Anthomedusae). Zoomorphology 100:11–22CrossRefGoogle Scholar
  32. Spencer AN (1979) Neurobiology of Polyorchis. II. Structure of effector systems. J Neurobiol 10:95–117CrossRefPubMedGoogle Scholar
  33. Spencer AN, Arkett SA (1984) Radial symmetry and the organization of central neurones in a hydrozoan jellyfish. J Exp Biol 110:69–90Google Scholar
  34. Toh Y, Yoshida M, Tateda H (1979) Fine structure of the ocellus of the hydromedusan, Spirocodon saltatrix. I. Receptor cells. J Ultrastruc Res 68:341–352CrossRefGoogle Scholar
  35. Weber C (1981) Structure, histochemistry, ontogenetic development, and regeneration of the ocellus of Cladonema radiatum Dujardin (Cnidaria, Hydrozoa, Anthomedusae). J Morphol 167:313–331CrossRefGoogle Scholar
  36. Weber C, Singla CL, Kerfoot PAH (1982) Microanatomy of the subumbrellar motor innervation in Aglantha digitale (Hydromedusae: Trachylina). Cell Tissue Res 223:305–312CrossRefPubMedGoogle Scholar
  37. Yamamoto M, Yoshida M (1980) Fine structure of ocelli of an anthomedusan, Nemiopsis dofleini, with special reference to synaptic organization. Zoomorphology 96:169–181CrossRefGoogle Scholar
  38. Yamasu T, Yoshida M (1976) Fine structure of complex ocelli of a cubomedusan, Tamoya bursaria Haeckel. Cell Tissue Res 170:325–339CrossRefPubMedGoogle Scholar
  39. Yi-Chan JL, Gallin WJ, Spencer AN (2001) The anatomy of the nervous system of the hydrozoan jellyfish, Polyorchis penicillatus, as revealed by a monoclonal antibody. Invertebr Neurosci 4:65–75Google Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • A. Garm
    • 1
  • P. Ekström
    • 1
  • M. Boudes
    • 2
  • D.-E. Nilsson
    • 1
  1. 1.Department of Cell and Organism BiologyLund UniversityLundSweden
  2. 2.Department of BiologyUniversity of Montpellier IIMontpellierFrance

Personalised recommendations