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Bioluminescence of deep-sea coronate medusae (Cnidaria: Scyphozoa)

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Abstract

Bioluminescence is the production of visible light by a living organism. The light commonly appears as flashes from point sources (involving one or more cells, usually described as photocytes) or as a glandular secretion. A visible flash usually involves synchronous light emission from a group of cells or, if from a single-celled organism such as a dinoflagellate, from a group of organelles. The number of cells (or organelles) responding synchronously is the main determinant of the flash intensity. Bioluminescence is a common phenomenon in many deep-sea animals and is widespread among the Cnidaria. In this paper, we compare and contrast in situ and laboratory recordings of the bioluminescent responses of specimens of the deep-sea scyphozoans Atolla wyvillei, Atolla vanhoffeni, Atolla parva, Nausithoe rubra, Paraphyllina intermedia, Periphyllopsis braueri and Periphylla periphylla. Displays in all seven species consist of localised flashes and propagated waves of light in the surface epithelium. The first few single waves propagate at rates of up to 60 cm s-1 but subsequent ones in any sequence of stimuli gradually decrease in speed. After several single wave responses, a subsequent stimulus may elicit multiple waves that persist for several seconds. Following such a frenzy, the specimen becomes temporarily refractory to further stimuli, but if rested will recover its normal responses and may produce further frenzies. The dome area, situated above the coronal groove, of the genera Paraphyllina, Periphylla, and Nausithoe is covered with luminescent point sources. Such point sources are generally absent from the dome of species of Atolla. Captured specimens of A. parva also produce secretory bioluminescence, corroborating prior in situ observations of this ability. Secretory bioluminescence in P. periphylla takes the form of scintillating particles released from the lappet margins. We did not observe secretory displays in specimens of any other species in the laboratory, but one instance of apparent secretory luminescence was recorded in situ in a specimen of A. wyvillei.

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References

  • Anctil M, Shimomura O (1984) Mechanism of photoinactivation and re-activation in the bioluminescence system of the ctenophore Mnemiopsis. Biochem J 221:269–72

    CAS  PubMed  Google Scholar 

  • Anderson PAV (1980) Epithelial conduction: its properties and functions. Progr Neurobiol 15:161–203

    Article  CAS  PubMed  Google Scholar 

  • Anderson PAV (1985) The comparative electrobiology of gelatinous zooplankton. Bull Mar Sci 37:460–477

    Google Scholar 

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

  • Bassot J-M, Bilbaut A, Mackie GO, Passano LM, Pavans de Ceccatty M (1978) Bioluminescence and other responses spread by epithelial conduction in the siphonophore Hippopodius. Biol Bull 155: 473–98

    Google Scholar 

  • Buck J (1973) Bioluminescent behavior in Renilla. I. Colonial responses. Biol Bull 144:19–42

    Google Scholar 

  • Dahlgren U (1916) The production of light by animals: Porifera and Coelenterata. J Franklin Inst 181:243–261

    Article  Google Scholar 

  • Flood PR, Bassot J-M, Herring PJ (1997) The microscopical structure of the bioluminescence system in the medusa Periphylla periphylla. In: Hastings JW, Kricka LJ, Stanley PE (eds) Bioluminescence and chemiluminescence: molecular reporting with photons. Wiley, Chichester, UK, pp 149–153

  • Haddock SHD, Case JF (1999) Bioluminescence spectra of shallow and deep-sea gelatinous zooplankton: ctenophores, medusae and siphonophores. Mar Biol 133:571–582

    Article  Google Scholar 

  • Haddock SHD, Rivers TJ, Robison BH (2001) Can coelenterates make coelenterazine? Dietary requirement for luciferin in cnidarian bioluminescence. Proc Natl Acad Sci USA 98:11148–11151

    Article  CAS  PubMed  Google Scholar 

  • Herring PJ (1990) Bioluminescent responses of the deep-sea scyphozoan Atolla wyvillei. Mar Biol 106:413–417

    Google Scholar 

  • Herring PJ (1995) Bioluminescent echinoderms: unity of function in diversity of expression? In: Emson RH, Smith AB, Campbell AC (eds) Echinoderm research 1995. Balkema, Rotterdam, pp 1–17

  • Herring PJ, Widder EA, Haddock SHD (1992) Correlation of bioluminescence emissions with ventral photophores in the mesopelagic squid Abralia veranyi (Cephalopoda: Enoploteuthidae). Mar Biol 112:293–298

    Google Scholar 

  • Herring PJ, Bassot J-M, Flood PR (1997) Bioluminescent responses of the scyphozoan Periphylla periphylla from a Norwegian fjord. In: Hastings JW, Kricka LJ, Stanley PE (eds) Bioluminescence and chemiluminescence: molecular reporting with photons. Wiley, Chichester, UK, pp 154–157

  • Johnsen S, Balser EJ, Fisher EC, Widder EA (1999) Bioluminescence in the deep-sea cirrate octopod Stauroteuthis syrtensis Verrill (Mollusca: Cephalopoda). Biol Bull 197:26–39

    Google Scholar 

  • Josephson RK (1974) Cnidarian neurobiology. In: Muscatine L, Lenhoff HM (eds) Coelenterate biology: reviews and new perspectives. Academic Press, New York, pp 245–78

  • Larson RJ, Mills CE, Harbison GR (1991) Western Atlantic midwater hydrozoan and scyphozoan medusae: in situ studies using manned submersibles. Hydrobiologia 216/217:311–317

    Google Scholar 

  • Mackie GO (1975) Neurobiology of Stomotoca. II. Pacemakers and conduction pathways. J Neurobiol 6:357–378

    CAS  PubMed  Google Scholar 

  • Mackie GO (1976) Propagated spikes and secretion in a coelenterate glandular epithelium. J Gen Physiol 68:313–325

    Article  CAS  PubMed  Google Scholar 

  • Mackie GO (1991) Propagation of bioluminescence in Euphysa japonica hydromedusae (Tubulariidae). Hydrobiologia 216/217:581–588

    Google Scholar 

  • Mallefet J, De Bremaeker N (1999) Study of bioluminescence control in the medusa Periphylla periphylla. In: Roda A, Pazzagli M, Kricka LJ, Stanley PE (eds) Bioluminescence and chemiluminescence: perspectives for the 21st Century . Wiley, Chichester, UK, pp.577–580

  • Morin JG (1974) Coelenterate bioluminescence. In: Muscatine L, Lenhoff HM (eds) Coelenterate biology: reviews and new perspectives, Academic Press, New York, pp 397–438

  • Morin JG (1976) Probable functions of bioluminescence in the Pennatulacea (Cnidaria, Anthozoa). In: Mackie GO (ed) Coelenterate ecology and behavior. Plenum, New York, pp 629–638

  • Morin JG (1983) Coastal bioluminescence: patterns and functions. Bull Mar Sci 33:787–817

    Google Scholar 

  • Musik K (1978) A new bioluminescent gorgonian, Lepidisis olapa, new species (Coelenterata Octocorallia), from Hawaii. Bull Mar Sci 28:735–741

    Google Scholar 

  • Passano LM (1973) Behavioral control systems in medusae; a comparison between hydro- and scyphomedusae. Publ Seto Mar Biol Lab 20:615–645

    Google Scholar 

  • Passano LM (1982) Scyphozoa and Cubozoa. In: Shelton GAB (ed) Electrical conduction and behaviour in “simple” invertebrates. Clarendon Press, Oxford, pp 149–202

  • Passano LM (1988) Variability in the initiation of diffuse nerve-net impulses in the mangrove jellyfish Cassiopea xamachana (Coelenterata:Scyphozoa). Comp Biochem Physiol 91C: 273–279

    Google Scholar 

  • Passano KN, Passano LM (1971) The endodermal nerve net of Scyphozoa. J Morphol 133:105–123

    CAS  PubMed  Google Scholar 

  • Pugh PR (1989) Gelatinous plankton – the forgotten fauna. Progr Underwater Sci 14:67–78

    Google Scholar 

  • Satterlie RA, Anderson PAV, Case JF (1980) Colonial coordination in anthozoans: Pennatulacea. Mar Behav Physiol 7:25–46

    Google Scholar 

  • Shimomura O, Flood PR (1998) Luciferase of the scyphozoan medusa Periphylla periphylla. Biol Bull 196; 244–252

    Google Scholar 

  • Shimomura O, Flood PR, Inouye S, Bryan B, Shimomura A (2001) Isolation and properties of the luciferase stored in the ovary of the scyphozoan medusa Periphylla periphylla. Biol Bull 201:339–347

    CAS  PubMed  Google Scholar 

  • Spencer AM (1974) Non-nervous conduction in invertebrates and embryos. Am Zool 14:917–929

    Google Scholar 

  • Widder EA (2002) Bioluminescence and the pelagic visual environment. Mar Freshw Behav Physiol 35:1-26

    Article  Google Scholar 

  • Widder EA, Bernstein SA, Bracher DF, Case JF, Reisenbichler KR, Torres JJ, Robison BH (1989) Bioluminescence in the Monterey Submarine Canyon: image analysis of video recordings from a midwater submersible. Mar Biol 100:541–551

    Google Scholar 

  • Widder EA, Greene CH, Youngbluth MJ (1992a) Bioluminescence of sound-scattering layers in the Gulf of Maine. J Plankton Res 14:1607–1624

    Google Scholar 

  • Widder EA, Caimi FM, Taylor LD, Tusting RF (1992b) Design and development of an autocalibrating radiometer for deep sea biooptical studies. Oceanic Engineering Society of the IEEE, OCEANS ‘92 1:525–530

  • Widder EA, Johnsen S, Bernstein SA, Case JF, Neilson DJ (1999) Thin layers of bioluminescent copepods found at density discontinuities in the water column. Mar Biol 134:429–437

    Article  Google Scholar 

  • Wild RA, Darlington E, Herring PJ (1985) An acoustically controlled cod-end system for the recovery of deep-sea animals at in situ temperatures. Deep-Sea Res 32:1583-1589

    Google Scholar 

  • Youngbluth MJ, Bamstedt U. (2001) Distribution, abundance, behavior and metabolism of Periphylla periphylla, a mesopelagic coronate medusa in a Norwegian fjord. In: Purcell JE, Graham WM, Dumont HJ (eds) Jellyfish blooms: ecological and societal importance. Kluwer, Dordrecht, pp 321–333

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Acknowledgements

We are most grateful to Dr S.H.D. Haddock, Prof. G.O. Mackie and Prof. R. Satterlie for their constructive criticism of early drafts of this paper. P.J.H. is very grateful to Prof. P.R. Flood for the opportunity to work on Periphylla during two cruises of R/V “Håkon Mosby” and to cruise leader Prof. U. Båmstedt.

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Authors and Affiliations

  1. Southampton Oceanography Centre, Waterfront Campus, European Way, Southampton, SO14 3ZH, UK

    P. J. Herring

  2. Harbor Branch Oceanographic Institution, 4600 U.S. 1N, Fort Pierce, FL 34946, USA

    E. A. Widder

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  1. P. J. Herring
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  2. E. A. Widder
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Correspondence to P. J. Herring.

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Communicated by J. P. Thorpe, Port Erin

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Herring, P.J., Widder, E.A. Bioluminescence of deep-sea coronate medusae (Cnidaria: Scyphozoa). Marine Biology 146, 39–51 (2004). https://doi.org/10.1007/s00227-004-1430-7

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  • DOI: https://doi.org/10.1007/s00227-004-1430-7

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