Skip to main content
Log in

Comparison of the statolith structures of Chironex fleckeri (Cnidaria, Cubozoa) and Periphylla periphylla (Cnidaria, Scyphozoa): a phylogenetic approach

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The rhopalia and statocysts of Periphylla periphylla (Péron and Lesueur in Ann Mus Hist Nat Marseille 14:316–366,1809) and Chironex fleckeri Southcott (Aust J Mar Freshw Res 7(2):254–280 1956) were examined histologically and showed several homologous characteristics. Differences in sensory area distribution could be connected to a slightly different functionality of equilibrium sensing. In P. periphylla, the statoliths (crystals) grow independently of each other; whereas in C. fleckeri, one large crystal covers the smaller ones. The structures of both statoliths were examined in detail with single-crystal diffraction, microtomography and diffraction contrast tomography. The single compact statolith of C. fleckeri consisted of bassanite as was previously known only for other rhopaliophoran medusae. An origin area with several small oligocrystals was located in the centre of the cubozoan statolith. The origin areas and the accretion of statoliths are similar in both species. Our results lead to the assumption that the single bassanite statolith of C. fleckeri (Cnidaria, Cubozoa) is a progression of the scyphozoan multiplex statolith. It is therefore suggested that the Cubozoa are derived from a scyphozoan ancestor and are a highly developed taxa within the Rhopaliophora.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abriel W, Nesper R (1993) Determination of crystal structure of CaSO4(H2O)0.5 by X-ray diffraction and potential profile calculations (in German). Z Kristallogr 205:99–113

    Article  CAS  Google Scholar 

  • Adam H, Czihak G (1964) Arbeitsmethoden der makroskopischen und mikroskopischen Anatomie. Ein Laboratoriumshandbuch für Biologen, Mediziner und technische Hilfskräfte. Fischer, Stuttgart

    Google Scholar 

  • Adler L, Röper M, Jarms G, Rothgänger M (2007) Erstnachweis einer fossilen Hydromeduse vom Typ der rezenten Aequoreidae (Hydrozoa, Cnidaria) in den Plattenkalken von Painten. Acheopteryx 25:15–20

    Google Scholar 

  • Arai MN (1997) A functional biology of Scyphozoa. Chapman & Hall, London

    Google Scholar 

  • Arneson AC, Cutress CE (1976) Life history of Carybdea alata Reynaud (1830) (Cubomedusae). In: Mackie GO (ed) Coelenterate ecology and behaviour. Plenum, New York, pp 227–236

    Google Scholar 

  • Ax P (1995) Das System der Metazoa I-III. Fischer/Spektrum, Stuttgart

    Google Scholar 

  • Becker A, Sötje I, Paulmann C, Beckmann F, Donath T, Boese R, Prymak O, Tiemann H, Epple M (2005) Calcium sulfate hemihydrate is the inorganic mineral in statoliths of scyphozoan medusae (Cnidaria). Dalton Trans 1:1545–1550

    Article  Google Scholar 

  • Beckmann F, Bonse U, Biermann T (1999) New developments in attenuation and phase-contrast microtomography using synchrotron radiation with low and high photon energies. Proc SPIE 3772:179–187

    Article  Google Scholar 

  • Berger EW (1900) Physiology and histology of the cubomedusae including Dr. F.S. Conants notes on the physiology. The Hohns Hopkins Press, Baltimore, pp 1–81

    Google Scholar 

  • Bigelow RP (1910) A comparison of the sense organs in medusae of the family Pelagiidae. J Exp Zool 9:751–785

    Article  Google Scholar 

  • Bonse U, Busch F (1996) X-ray computed microtomography (μCT) using synchrotron radiation (SR). Prog Biophys Molec Biol 65:133–169

    Article  CAS  Google Scholar 

  • Boßelmann F, Epple M, Sötje I, Tiemann H (2007) Statoliths of calcium sulfate hemihydrate are used for gravity sensing in rhopaliophoran medusae (Cnidaria). In: Baeuerlein E (ed) Biomineralisation: biological aspects and structure formation. Wiley-VCH, Weinheim, pp 261–272

    Google Scholar 

  • Calder DR (1973) Laboratory observations on the life history of Rhopilema verrilli (Scyphozoa: Rhizostomeae). Mar Biol 21:109–114

    Article  Google Scholar 

  • Calder DR (1982) Life history of the cannonball jellyfish, Stomolophus meleagris L. Agassiz, 1860 (Scyphozoa, Rhizostomida). Biol Bull 162:149–162

    Article  Google Scholar 

  • Cartwright P, Halgedahl SL, Hendricks JR, Jarrard RD, Marques AC, Collins AG, Liebermann BS (2007) Exceptionally preserved jellyfish from the Middle Cambrian. PLoS ONE 2:e1121

    Article  Google Scholar 

  • Chapman DM (1985) X-ray microanalysis of selected coelenterate statoliths. J Mar Biol Assoc UK 65:617–627

    Article  Google Scholar 

  • Claus C (1878) Untersuchungen über Charybdea marsupialis. Alfred Hölder, Wien, pp 1–56

    Google Scholar 

  • Coates MM (2003) Visual ecology and functional morphology of Cubozoa (Cnidaria). Integr Comp Biol 43:542–548

    Article  Google Scholar 

  • Collins AG (2002) Phylogeny of Medusozoa and the evolution of cnidarian life cycles. J Evol Biol 15:418–432

    Article  Google Scholar 

  • Collins AG, Bentlage B, Matsumoto GI, Haddock HD, Osborn KJ, Schierwater B (2006) Solution to the phylogenetic enigma of Tetraplatia, a worm-shaped cnidarian. Biol Lett 2:120–124

    Article  Google Scholar 

  • Conant FS (1898) The cubomedusae. Johns Hopkins University morphological monographs. The Johns Hopkins Press, Baltimore, pp 1–61

    Google Scholar 

  • Donath T, Beckmann F, Heijkants RGJC, Brunke O, Schreyer A (2004) Characterization of polyurethane scaffolds using synchrotron radiation based computed microtomography. SPIE: Dev X-Ray Tomogr IV 5535:775–782

    CAS  Google Scholar 

  • Ekström P, Garm A, Pålsson J, Vihtelic TS, Nilsson D-E (2008) Immunohistochemical evidence for multiple photosystems in box jellyfish. Cell Tissue Res 333:115–124

    Article  Google Scholar 

  • Fraser JH (1968) Standardization of zooplankton sampling methods at sea. In: Zooplankton sampling, part II. UNESCO Press, Paris, pp 149–168

  • Garm A, Ekström P, Boudes M, Nilsson D-E (2006) Rhopalia are integrated parts of the central nervous system in box jellyfish. Cell Tissue Res 325:333–343

    Article  CAS  Google Scholar 

  • Gordon M, Hatcher C, Seymour J (2004) Growth and age determination of the tropical Australian cubozoan Chiropsalmus sp. Hydrobiologia 530(531):339–345

    Article  Google Scholar 

  • Haeckel E (1879) Das System der Medusen. Erster Teil einer Monographie der Medusen. Fischer, Jena

    Google Scholar 

  • Hertwig O, Hertwig R (1878) Das Nervensystem und die Sinnesorgane der Medusen. FCW Vogel, Leipzig

    Google Scholar 

  • Hesse R (1895) Über das Nervensystem und die Sinnesorgane von Rhizostoma buvieri. Tübinger Zoologische Arbeiten 1:85–130

    Google Scholar 

  • Hofman DK, Neumann R, Henne K (1978) Strobilation, budding and initiation of scyphistoma morphogenesis in the rhizostome Cassiopea andromeda (Cnidaria: Scyphozoa). Mar Biol 47:161–176

    Article  Google Scholar 

  • Holst S, Sötje I, Tiemann H, Jarms G (2007) Life cycle of the rhizostome jellyfish Rhizostoma octopus (L.) (Scyphozoa, Rhizostomeae), with studies on cnidocysts and statoliths. Mar Biol 151:1695–1710

    Article  Google Scholar 

  • Holtmann M, Thurm U (2001) Variations of concentric hair cells in a cnidarian sensory epithelium (Coryne tubulosa). J Comp Neuro 432:550–563

    Article  CAS  Google Scholar 

  • Horridge GA (1966) Some recently discovered underwater vibration receptors in invertebrates. In: Barnes H (ed) Some contemporary studies in marine science. George Allen and Unwin Ltd, London, pp 395–405

    Google Scholar 

  • Horridge GA (1969) Statocysts of medusae and evolution of stereocilia. Tissue Cell 1:341–353

    Article  CAS  Google Scholar 

  • Horridge GA (1971) Primitive examples of gravity receptors and their evolution. In: Solon AG, Melvin JC (eds) Gravity and the organism. The University of Chicago Press, Chicago, pp 203–221

    Google Scholar 

  • Horridge GA, MacKay B (1962) Naked axons and symmetrical synapses in coelenterates. Quart J micr Sci 103:531–541

    Google Scholar 

  • Hündgen M, Biela C (1982) Fine structure of the touch-plate in the scyphomedusan Aurelia aurita. J Ultrastruct Res 80:178–184

    Article  Google Scholar 

  • Johnson G, King A, Gonclaves Honnicke M, Marrow J, Ludwig W (2008) X-ray diffraction contrast tomography: a novel technique for three-dimensional grain mapping of polycrystals. II. The combined case. J Appl Crystallogr 41:310–318

    Google Scholar 

  • Kawamura M, Ueno S, Iwanaga S, Oshiro N, Kubota S (2003) The relationship between fine rings in the statolith and growth of the cubomedusa Chiropsalmus quadrigus (Cnidaria: Cubozoa) form Okinawa Island, Japan. Plankton Biol Ecol 50:37–42

    Google Scholar 

  • Laska G, Hündgen M (1982) Morphologie und Ultrastruktur der Lichtsinnesorgane von Tripedalia cystophora Conant (Cnidaria, Cubozoa). Zool Jb Anat 108:107–123

    Google Scholar 

  • Laska G, Hündgen M (1984) die Ultrastruktur des neuromuskulären Systems der Medusen von Tripedalia cystophora und Carybdea marsupialis (Coelentata, Cubozoa). Zoomorphol 104:163–170

    Article  Google Scholar 

  • Laska-Mehnert G (1985) Cytologische Veränderungen während der Metamorphose des Cubopolypen Tripedalia cystophora (Cubozoa, Carybdeidae) in die Meduse. Helgoländer Meeresunters 39:129–164

    Article  Google Scholar 

  • Lowenstam HA, Weiner S (1989) On Biomineralization. Oxford University Press, New York

    Google Scholar 

  • Ludwig W, Schmidt S, Mejdal Lauridsen E, Poulsen HF (2008) X-ray diffraction contrast tomography: a novel technique for three-dimensional grain mapping of polycrystals. I. Direct beam case. J Appl Cryst 41:302–309

    Article  CAS  Google Scholar 

  • Ludwig W, Reischig P, King A, Herbig M, Lauridsen EM, Johnson G, Marrow TJ, Buffiere JY (2009) Three-dimensional grain mapping by X-ray diffraction contrast tomography and the use of Friedel pairs in diffraction data analysis. Rev Sci Instrum 80:033905–033909

    Article  CAS  Google Scholar 

  • Maas O (1903) Die Scyphomedusen der Siboga Expedition. In: Weber M (ed) Siboga-expeditie XI. EJ Brill, Leiden, pp 1–91

    Google Scholar 

  • Marques AC, Collins AG (2004) Cladistic analysis of Medusozoa and Cnidarian evolution. Invertebr Biol 123:23–42

    Article  Google Scholar 

  • Martin VJ (2004) Photoreceptors of cubozoan jellyfish. Hydrobiologia 530(531):135–144

    Article  Google Scholar 

  • Matsumoto GI (1995) Observations on the anatomy and behaviour of the cubozoan Carybdea rastonii Haacke. Mar Fresh Behav Physiol 26:139–148

    Article  Google Scholar 

  • Mirone A, Wilcke R, Hammersley A, Ferrero C (2009) PyHST—high speed tomographic reconstruction. http://www.esrf.eu/UsersAndScience/Experiments/TBS/SciSoft

  • Nakanishi N, Hartenstein V, Jacobs DK (2009) Development of the rhopalial nervous system in Aurelia sp. 1. (Cnidaria, Scyphozoa). Dev Genes Evol 219:301–317

    Article  Google Scholar 

  • Neues F, Beckmann F, Ziegler A, Epple M (2007) The application of synchrotron radiation-based micro-tomography in biomineralization. In: Baeuerlein E (ed) Biomineralisation: biological aspects and structure formation. Wiley-VCH, Weinheim, pp 369–380

    Google Scholar 

  • O’Connor M, Garm A, Nilsson D-E (2009) Structure and optics of the eyes of the box jellyfish Chiropsella bronzie. J Comp Physiol A 195:557–569

    Article  Google Scholar 

  • Péron F, Lesueur CA (1809) Histoire générale et particuliére de tout les animaux qui composent la famille des Méduses. Ann Mus Hist Nat Marseille 14:316–366

    Google Scholar 

  • Pollmanns D, Hündgen M (1981) Licht- und elektronenmikroskopische Untersuchung der Rhopalien von Aurelia aurita (Scyphozoa, Semaeostomae). Zool Jb Anat 105:508–525

    Google Scholar 

  • Prymak O, Tiemann H, Sötje I, Marxen J, Klocke A, Kahl-Nieke B, Beckmann F, Donath T, Epple M (2005) Application of synchrotron radiation-based computer microtomography (SRμCT) to biominerals: embryonic snails, statoliths of medusae, and human teeth. J Bio Inorg Chem 10:688–695

    Article  CAS  Google Scholar 

  • Rack A, Weitkamp T, Bauer Trabelsi S, Modregger P, Cecilia A, dos Santos Rolo T, Rack T, Haas D, Simon R, Heldele R, Schulz M, Mayzel B, Danilewsky AN, Waterstradt T, Diete W, Riesemeier H, Müller BR, Baumbach T (2009) The micro-imaging station of the TopoTomo beamline at the ANKA synchrotron light source. Nucl Instr Phys Res B 267(11):1978–1988

    Article  CAS  Google Scholar 

  • Ralph PM (1960) Tetraplatia, a coronate scyphomedusan. Proc Royal Soc London B 152:263–281

    Article  CAS  Google Scholar 

  • Robinson DG, Ehlers U, Herken R, Herrmann B, Mayer F, Schürmann F-W (1985) Präparationsmethodik in der Elektronenmikroskopie. Eine Einführung für Biologen und Mediziner. Springer, Berlin, pp 1–208

    Google Scholar 

  • Ruppert EE, Fox RS, Barnes RD (2004) Cnidaria. In: Ruppert EE, Fox RS, Barnes RD (eds) Invertebrate zoology—a functional evolutionary approach. Thomson Brooks/Cole, Belmont, pp 111–180

  • Russell FS (1970) The medusae of the British Isles. J Mar Biol Ass UK 39:303–317

    Article  Google Scholar 

  • Salvini-Plawen L (1978) On the origin and evolution of the lower metazoa. Z Zool Syst Evol Forsch 16:40–88

    Article  Google Scholar 

  • Satterlie RA (2002) Neuronal control of swimming in jellyfish: a comparative story. Can J Zool 80:1654–1669

    Article  Google Scholar 

  • Satterlie RA, Nolan TG (2001) Why do cubomedusae have only four swim pacemakers? J Exp Biol 204:1413–1419

    CAS  Google Scholar 

  • Schäfer EA (1878) Observations o the nervous system of Aurelia aurita. Phil Trans Royal Soc London 169:563–575

    Article  Google Scholar 

  • Schewiakoff W (1889) Beiträge zur Kenntnis des Acalephenauges. Morphol Jb 15:21–60

    Google Scholar 

  • Schuchert P (1993) Phylogenetic analysis of the Cnidaria. Z Zool Syst Evol Forsch 31:161–173

    Article  Google Scholar 

  • Singla CL (1975) Statocysts of Hydromedusae. Cell Tissue Res 158:391–407

    Article  CAS  Google Scholar 

  • Skogh C, Garm A, Nilsson D-E, Ekström P (2006) Bilaterally symmetrical rhopalial nervous system of the box jellyfish Tripedalia cystophora. J Morphol 267:1391–1405

    Article  CAS  Google Scholar 

  • Southcott RV (1956) Studies on Australian Cubomedusae, including a new genus and species apparently harmful to man. Aust J Mar Freshw Res 7(2):254–280

    Article  Google Scholar 

  • Spangenberg DB (1968) Recent studies of strobilation in jellyfish. Oceanogr Mar Biol Ann Rev 6:231–247

    Google Scholar 

  • Spangenberg DB (1976) Intracellular statolith synthesis in Aurelia aurita. In: Watabe N, Wilbur KM (eds) The mechanisms of biomineralization in animals and plants. University of South Carolina Press, Columbia, pp 231–248

  • Spangenberg D (1991) Rhopalium development in Aurelia aurita ephyrae. Hydrobiologia 216(217):45–49

    Article  Google Scholar 

  • Spangenberg DB, Beck CW (1968) Calcium sulfate dihydrate statoliths in Aurelia. Trans Am Microsc Soc 87(3):329–335

    Article  Google Scholar 

  • Spangenberg DB, Jernigan T, Philput C, Lowe B (1994) Graviceptor development in jellyfish ephyrae in space and on earth. Adv Space Res 14:317–325

    Article  CAS  Google Scholar 

  • Spangenberg DB, Coccaro E, Schwarte R, Lowe B (1996) Touch-plate and statolith formation in graviceptors of ephyrae which developed while weightless in space. Scan Microsc 10:875–888

    CAS  Google Scholar 

  • Stangl K, Salvini-Plawen LV, Holstein TW (2002) Staging and induction of medusa metamorphosis in Carybdea marsupialis (Cnidaria, Cubozoa). Vie Milieu 52:131–140

    Google Scholar 

  • Straehler-Pohl I (2009) Die Phylogenie der Rhopaliophora (Scyphozoa und Cubozoa) und die Paraphylie der “Rhizostomeae”. Doctoral Thesis University of Hamburg, Faculty of Mathematics, Informatics and Natural Sciences

  • Straehler-Pohl I, Jarms G (2005) Life cycle of Carybdea marsupialis Linnaeus, 1758 (Cubozoa, Carybdeidae) reveals metamorphosis to be a modified strobilation. Mar Biol 147:1271–1277

    Article  Google Scholar 

  • Tadic D, Beckmann F, Donath T, Epple M (2004) Comparison of different methods for the preparation of porous bone substitution materials and structural investigations by synchrotron (micro)-computer tomography Mat-wiss u Werkstofftech 35:240–244

    Google Scholar 

  • Tanner BK (1976) X-ray diffraction topography. Pergammon, Oxford

    Google Scholar 

  • Tardent P, Schmid V (1972) Ultrastructure of mechanoreceptors of the polyp Coryne pintnere (Hydrozoa, Athecata). Exp Cell Res 72:265–275

    Article  CAS  Google Scholar 

  • Thiel ME (1936) Scyphomedusae. In: Bronns HG (ed) Klassen und Ordnungen des Tierreichs. Akademische Verlagsgesellschaft, Leipzig

    Google Scholar 

  • Thiel H (1966) The evolution of Scyphozoa. A review. In: Rees WJ (ed) The Cnidaria and their evolution Symp Zool Soc Lond, vol 16. Academic Press, London, pp 77–117

  • Tiemann H, Jarms G (2010) Organ-like gonads, complex oocyte formation, and long-term spawning in Periphylla periphylla (Cnidaria, Scyphozoa, Coronatae). Mar Biol 157:527–535

    Article  Google Scholar 

  • Tiemann H, Sötje I, Jarms G, Paulmann C, Epple M, Hasse B (2002) Calcium sulphate hemihydrate in statoliths of deep-sea medusae. J Chem Soc, Dalton Trans 7:1266–1268

    Google Scholar 

  • Tiemann H, Sötje I, Becker A, Jarms G, Epple M (2006) Calcium sulfate hemihydrate (bassanite) statoliths in the cubozoan Carybdea sp. Zool Anz 245:13–17

    Article  Google Scholar 

  • Ueno S, Imai C, Mitsutani A (1995) Fine growth rings found in statolith of a cubomedusa Carybdea rastoni. J Plankton Res 17:1381–1384

    Article  Google Scholar 

  • Ueno S, Imai C, Mitsutani A (1997) Statolith formation and increment in Carybdea rastoni Haacke, 1886 (Scyphozoa: Cubomedusae): evidence of synchronization with semilunar rhythms. In: Proceedings of the 6th international conference on coelenterate biology, pp 491–496

  • Vanhöffen E (1900) Über Tiefseemedusen und ihre Sinnesorgane. Zool Anz 23:277–279

    Google Scholar 

  • Vanhöffen E (1902) Die acraspeden Medusen der deutschen Tiefsee-Expedition 1898–1899. Deutschen-Tiefsee Expedition 1898–1899, Bd III 3:1–49

  • Vinnikow YA, Aronove MZ, Kharkeevich TA, Tsirulis TP, Lavrowa EA, Natochin YV (1981) Structural and chemical features of the invertebrate otoliths. Z mikrosk-anat Forsch 95:127

    Google Scholar 

  • Werner B (1973) New investigations on systematics and evolution of the class Scyphozoa and the phylum Cnidaria. Pub Seto Mar Biol Lab 20:35–61

    Google Scholar 

  • Werner B (1975) Bau und Lebensgeschichte des Polypen von Tripedalia cystophora (Cubozoa, class, nov. Carybdeidae) und seine Bedeutung für die Evolution der Cnidaria. Helgoländer wiss Meeresunters 27:461–504

    Article  Google Scholar 

  • Werner B (1976) Die neue Cnidarierklasse Cubozoa. Verh Dtsch Zool Ges, p 230

  • Werner B (1993) Stamm Cnidaria, Nesseltiere. In: Kaestner A (ed) Lehrbuch der speziellen Zoologie, vol I/2. Fischer, Stuttgart, pp 11–305

    Google Scholar 

  • Werner B, Cutress EC, Studebaker JP (1971) Life cycle of Tripedalia cystophora Conant (Cubomedusae). Nature 232:582–583

    Article  CAS  Google Scholar 

  • Wilt FH, Ettensohn CA (2007) The morphogenesis and biomineralization of the sea urchin larval skeleton. In: Bauerlein E (ed) Handbook of biomineralization: biological aspects and structure formation, vol 1. Wiley-VCH, pp, pp 183–210

    Google Scholar 

  • Yamaguchi M, Hartwick R (1980) Early life history of the Sea Wasp, Chironex fleckeri (Class Cubozoa). In: Tardent P, Tardent R (eds) Developmental and cellular biology of coelenterates. Elsevier/North-Holland Biomedical Press, Amsterdam, pp 11–16

    Google Scholar 

Download references

Acknowledgments

We are grateful to HASYLAB at DESY, Hamburg and ANKA, Karlsruhe as well as the European Synchrotron Radiation Facility in Grenoble (France) for generous allocation of beamtime. For technical assistance and reconstruction of the microtomography scans at DESY, we thank Felix Beckmann and Julia Herzen. Paulina Kämpfe and Henning Urch we thank for assistance during image recording at DESY. For assistance in specimen collection, we thank Jamie Seymour of TASRU (JCU) and grants from the Lions Foundation, National Geographic, Australian Geographic, Cairns City Council, Cardwell City Council, Smart State QLD, JCUPRS & GRS and Rio Tinto.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to I. Sötje.

Additional information

Communicated by J. Purcell.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sötje, I., Neues, F., Epple, M. et al. Comparison of the statolith structures of Chironex fleckeri (Cnidaria, Cubozoa) and Periphylla periphylla (Cnidaria, Scyphozoa): a phylogenetic approach. Mar Biol 158, 1149–1161 (2011). https://doi.org/10.1007/s00227-011-1637-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-011-1637-3

Keywords

Navigation