Proceedings of the Royal Society B: Biological Sciences
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Bioluminescent signals spatially amplified by wavelength-specific diffusion through the shell of a marine snail

Published:https://doi.org/10.1098/rspb.2010.2203

    Some living organisms produce visible light (bioluminescence) for intra- or interspecific visual communication. Here, we describe a remarkable bioluminescent adaptation in the marine snail Hinea brasiliana. This species produces a luminous display in response to mechanical stimulation caused by encounters with other motile organisms. The light is produced from discrete areas on the snail's body beneath the snail's shell, and must thus overcome this structural barrier to be viewed by an external receiver. The diffusion and transmission efficiency of the shell is greater than a commercial diffuser reference material. Most strikingly, the shell, although opaque and pigmented, selectively diffuses the blue-green wavelength of the species bioluminescence. This diffusion generates a luminous display that is enlarged relative to the original light source. This unusual shell thus allows spatially amplified outward transmission of light communication signals from the snail, while allowing the animal to remain safely inside its hard protective shell.

    References

    • 1
      Hastings W. J.& Morin J. G.. 1991Bioluminescence. Comparative animal physiology. Volume 1: neural and integrative animal physiology (ed. & Prosser C. L.), pp. 131–170. New York, NY: John Wiley & Sons. Google Scholar
    • 2
      Herring P. J.. 1990Bioluminescent communication in the sea. Light and life in the sea (eds , Herring P. J., Campbell A. K., Whitfield M.& Maddock L.), pp. 245–264. Cambridge, UK: University Press. Google Scholar
    • 3
      Herring P. J.. 1978Bioluminescence in action.London, UK: Academic Press. Google Scholar
    • 4
      Haddock S. H. D., Moline M. A.& Case J. F.. 2009Bioluminescence in the Sea. Annu. Rev. Mar. Sci. 2, 293–343.doi:10.1146/annurev-marine-120308-081028 (doi:10.1146/annurev-marine-120308-081028). CrossrefGoogle Scholar
    • 5
      Herring P. J.. 2000Species abundance, sexual encounter and bioluminescent signalling in the deep sea. Phil. Trans. R. Soc. Lond. B 355, 1273–1276.doi:10.1098/rstb.2000.0682 (doi:10.1098/rstb.2000.0682). LinkGoogle Scholar
    • 6
      Herring P. J.. 2007Sex with the lights on? A review of bioluminescent sexual dimorphism in the sea. J. Mar. Biol. Assoc. UK 87, 829–842.doi:10.1017/S0025315407056433 (doi:10.1017/S0025315407056433). CrossrefGoogle Scholar
    • 7
      Rivers T. J.& Morin J. G.. 2008Complex sexual courtship displays by luminescent male marine ostracods. J. Exp. Biol. 211, 2252–2262.doi:10.1242/jeb.011130 (doi:10.1242/jeb.011130). Crossref, PubMedGoogle Scholar
    • 8
      Herring P. J.& Morin J. G.. 1978Bioluminescence in fishes. Bioluminescence in action (ed. & Herring P. J.), pp. 287–329. London, UK: Academic Press. Google Scholar
    • 9
      Morin J. G.. 1983Coastal bioluminescence: patterns and functions. Bull. Mar. Sci. 33, 787–817. Google Scholar
    • 10
      Morin J. G., Harrington A., Nealson K., Krieger N., Baldwin T. O.& Hastings J. W.. 1975Light for all reasons—versatility in behavioral repertoire of flashlight fish. Science 190, 74–76. CrossrefGoogle Scholar
    • 11
      Clarke W. D.. 1963Function of bioluminescence in mesopelagic organisms. Nature 198, 1244–1246.doi:10.1038/1981244a0 (doi:10.1038/1981244a0). CrossrefGoogle Scholar
    • 12
      Hastings J. W.. 1971Light to hide by—ventral luminescence to camouflage the silhouette. Science 173, 1016–1017.doi:10.1126/science.173.4001.1016 (doi:10.1126/science.173.4001.1016). Crossref, PubMedGoogle Scholar
    • 13
      Lawry J. V.. 1974Lantern fish compare downwelling light and bioluminescence. Nature 247, 155–157.doi:10.1038/247155a0 (doi:10.1038/247155a0). CrossrefGoogle Scholar
    • 14
      Young R. E.& Roper C. F. E.. 1976Bioluminescent countershading in midwater animals: evidence from living squid. Science 191, 1046–1048.doi:10.1126/science.1251214 (doi:10.1126/science.1251214). Crossref, PubMedGoogle Scholar
    • 15
      Deheyn D., Mallefet J.& Jangoux M.. 2000Expression of bioluminescence in Amphipholis squamata (Ophiuroidea: Echinodermata) in presence of various organisms: a laboratory study. J. Mar. Biol. Assoc. UK 80, 179–180.doi:10.1017/S0025315499001733 (doi:10.1017/S0025315499001733). CrossrefGoogle Scholar
    • 16
      Fristrup K. M.& Harbison G. R.. 2002How do sperm whales catch squids?Mar. Mamm. Sci. 18, 42–54.doi:10.1111/j.1748-7692.2002.tb01017.x (doi:10.1111/j.1748-7692.2002.tb01017.x). CrossrefGoogle Scholar
    • 17
      Grober M.. 1988Brittle-star bioluminescence functions as an aposematic signal to deter crustacean predators. Anim. Behav. 36, 493–501.doi:10.1016/S0003-3472(88)80020-4 (doi:10.1016/S0003-3472(88)80020-4). CrossrefGoogle Scholar
    • 18
      Widder E. A.. 1998A predatory use of counterillumination by the squaloid shark, Isistius brasiliensis. Environ. Biol. Fish. 53, 267–273.doi:10.1023/A:1007498915860 (doi:10.1023/A:1007498915860). CrossrefGoogle Scholar
    • 19
      Hastings J. W.. 1983Biological diversity, chemical mechanisms, and the evolutionary origins of bioluminescent systems. J. Mol. Evol. 19, 309–321.doi:10.1007/BF02101634 (doi:10.1007/BF02101634). Crossref, PubMedGoogle Scholar
    • 20
      Herring P. J.. 1988Luminescent organs. The Mollusca: form and function, vol. 11 (eds , Trueman E. R.& Clarke M. R.), pp. 449–489. New York, NY: Academic Press. Google Scholar
    • 21
      Johnsen S., Balser E. J., Fisher E. C.& Widder E. A.. 1999Bioluminescence in the deep-sea cirrate octopod Stauroteuthis syrtensis Verrill (Mollusca: Cephalopoda). Ecol. Evol. 197, 26–39. Google Scholar
    • 22
      Johnsen S., Balser E. J.& Widder E. A.. 1999Light-emitting suckers in an octopus. Nature 398, 113.doi:10.1038/18131 (doi:10.1038/18131). CrossrefGoogle Scholar
    • 23
      Jones B. W.& Nishiguchi M. K.. 2004Counterillumination in the Hawaiian bobtail squid, Euprymna scolopes Berry (Mollusca: Cephalopoda). Mar. Biol. 144, 1151–1155.doi:10.1007/s00227-003-1285-3 (doi:10.1007/s00227-003-1285-3). CrossrefGoogle Scholar
    • 24
      Kubodera T., Koyama Y.& Mori K.. 2007Observations of wild hunting behaviour and bioluminescence of a large deep-sea, eight-armed squid, Taningia danae. Proc. R. Soc. B 274, 1029–1034.doi:10.1098/rspb.2006.0236 (doi:10.1098/rspb.2006.0236). LinkGoogle Scholar
    • 25
      Tsuji F. I.& Leisman G. B.. 1981K+/ Na+-triggered bioluminescence in the oceanic squid Symplectoteuthis oualaniensis. Proc. Natl Acad. Sci. USA 78, 6719–6723.doi:10.1073/pnas.78.11.6719 (doi:10.1073/pnas.78.11.6719). Crossref, PubMedGoogle Scholar
    • 26
      Anctil M.. 1977Development of bioluminescence and photophores in the midshipman fish, Porichthys notatus. J. Morphol. 151, 363–395.doi:10.1002/jmor.1051510305 (doi:10.1002/jmor.1051510305). Crossref, PubMedGoogle Scholar
    • 27
      Lohrmann K. B.. 2008Subcutaneous photophores in the jumbo squid Dosidicus gigas (d'Orbigny, 1835) (Cephalopoda: Ommastrephidae). Rev. Biol. Mar. Oceanogr. 43, 275–284.doi:10.4067/S0718-19572008000200006 (doi:10.4067/S0718-19572008000200006). CrossrefGoogle Scholar
    • 28
      Arnold J. M., Young R. E.& King M. V.. 1974Ultrastructure of a cephalopod photophore. II. Iridophores as reflectors and transmitters. Biol. Bull. 147, 522–534.doi:10.2307/1540737 (doi:10.2307/1540737). Crossref, PubMedGoogle Scholar
    • 29
      Butcher S., Dilly P. N.& Herring P. J.. 1982The comparative morphology of the photophores of the squid Pyroteuthis margaritifera (Cephalopoda, Enoploteuthidae). J. Zool. 196, 133–150.doi:10.1111/j.1469-7998.1982.tb03497.x (doi:10.1111/j.1469-7998.1982.tb03497.x). CrossrefGoogle Scholar
    • 30
      Denton E. J., Herring P. J., Widder E. A., Latz M. I.& Case J. F.. 1985The roles of filters in the photophores of oceanic animals and their relation to vision in the oceanic environment. Proc. R. Soc. Lond. B 225, 63–97.doi:10.1098/rspb.1985.0051 (doi:10.1098/rspb.1985.0051). LinkGoogle Scholar
    • 31
      Herring P. J.. 2000Bioluminescent signals and the role of reflectors (Review). J. Opt. A Pure Appl. Opt. 2, R29–R38.doi:10.1088/1464-4258/2/6/202 (doi:10.1088/1464-4258/2/6/202). CrossrefGoogle Scholar
    • 32
      Herring P. J., Dilly P. N.& Cope C.. 1994The bioluminescent organs of the deep-sea cephalopod Vampyroteuthis infernalis (Cephalopoda, Vampyromorpha). J. Zool. 233, 45–55.doi:10.1111/j.1469-7998.1994.tb05261.x (doi:10.1111/j.1469-7998.1994.tb05261.x). CrossrefGoogle Scholar
    • 33
      McFall-Ngai M.& Montgomery M. K.. 1990The anatomy and morphology of the adult bacterial light organ of Euprymna scolopes Berry (Cephalopoda, Sepiolidae). Biol. Bull. 179, 332–339.doi:10.2307/1542325 (doi:10.2307/1542325). Crossref, PubMedGoogle Scholar
    • 34
      Herring P. J., Dilly P. N.& Cope C.. 1985The photophore morphology of Selenoteuthis scintillans Voss and other Lycoteuthids (Cephalopoda, Lycoteuthidae). J. Zool. 206, 567–589.doi:10.1111/j.1469-7998.1985.tb03559.x (doi:10.1111/j.1469-7998.1985.tb03559.x). CrossrefGoogle Scholar
    • 35
      Bertelsen E.& Munk O.. 1964Rectal light organs in the argentinoid fishes Opisthoproctus and Winteria. Dana Rep. 62, 1–17. Google Scholar
    • 36
      McFall-Ngai M. J.. 1983Adaptations for reflection of bioluminescent light in the gas bladder of Leiognathus equulus (Perciformes, Leiognathidae). J. Exp. Zool. 227, 23–33.doi:10.1002/jez.1402270105 (doi:10.1002/jez.1402270105). Crossref, PubMedGoogle Scholar
    • 37
      Munk O.& Bertelsen E.. 1980On the esca light organ and its associated light-guiding structures in the deep-sea anglerfish Chaenophryne draco (Pisces, Ceratioidei). Vidensk. Meddr. Dansk. Naturh. Foren. 142, 103–129. Google Scholar
    • 38
      Munk O., Hansen K.& Herring P. J.. 1998On the development and structure of the escal light organ of some melanocetid deep sea anglerfishes (Pisces: Ceratioidei). J. Mar. Biol. Assoc. UK 78, 1321–1335. CrossrefGoogle Scholar
    • 39
      Kawahara M., Gleadall I. G.& Tsukahara Y.. 1998A note on the fibre-optic light-guides in the eye photophores of Watasenia scintillans. S. Afr. J. Mar. Sci. 20, 123–127.doi:10.2989/025776198784126250 (doi:10.2989/025776198784126250). CrossrefGoogle Scholar
    • 40
      Harvey E. N.. 1952Bioluminescence.New York, NY: Academic Press. Google Scholar
    • 41
      Haneda Y.. 1958Studies on luminescence in marine snails. Pac. Sci. 12, 152–156. Google Scholar
    • 42
      Ponder W. F.. 1988Bioluminescence in Hinea braziliana (Lamarck) (Gastropoda, Planaxidae). J. Molluscan Stud. 54, 361–361. CrossrefGoogle Scholar
    • 43
      Houbrick R. S.. 1987Anatomy, reproductive biology, and phylogeny of the Planaxidae (Cerithiacea: Prosobranchia). Smithson. Contrib. Zool. 445, 1–57. CrossrefGoogle Scholar
    • 44
      Shimomura O.. 2006Bioluminescence: chemical principles and methods.Singapore: World Scientific. CrossrefGoogle Scholar
    • 45
      Latz M. I.& Lee A. O.. 1995Spontaneous and stimulated bioluminescence of the dinoflagellate Ceratocorys horrida (Peridiniales). J. Phycol. 31, 120–132.doi:10.1111/j.1529-8817.1995.tb03766.x (doi:10.1111/j.1529-8817.1995.tb03766.x). CrossrefGoogle Scholar
    • 46
      Maldonado E. M.& Latz M. I.. 2007Shear-stress dependence of dinoflagellate bioluminescence. Biol. Bull. 212, 242–249. Crossref, PubMedGoogle Scholar
    • 47
      Zar J. H.. 1996Biostatistical analysis.Upper Saddle River, NJ: Prentice-Hall. Google Scholar
    • 48
      Widder E. A., Latz M. I., Herring P. J.& Case J. F.. 1984Far red bioluminescence from two deep-sea fishes. Science 225, 512–514.doi:10.1126/science.225.4661.512 (doi:10.1126/science.225.4661.512). Crossref, PubMedGoogle Scholar
    • 49
      Zorner S. A.& Fischer A.. 2007The spatial pattern of bioluminescent flashes in the polychaete Eusyllis blomstrandi (Annelida). Helgoland Mar. Res. 61, 55–66.doi:10.1007/s10152-006-0053-4 (doi:10.1007/s10152-006-0053-4). CrossrefGoogle Scholar
    • 50
      Grober M.. 1988Responses of tropical reef fauna to brittle-star luminescence (Echinodermata: Ophiuroidea). J. Exp. Mar. Biol. Ecol. 115, 157–168.doi:10.1016/0022-0981(88)90100-1 (doi:10.1016/0022-0981(88)90100-1). CrossrefGoogle Scholar
    • 51
      Grober M. S.. 1989Aposematism and bioluminescence. Anim. Behav. 37, 341–343.doi:10.1016/0003-3472(89)90127-9 (doi:10.1016/0003-3472(89)90127-9). CrossrefGoogle Scholar
    • 52
      Grober M. S.. 1990Luminescent flash avoidance in the nocturnal crab Portunus xantusii. 1. The effects of luminescence and mechanical stimulation on heart rate. J. Exp. Biol. 148, 415–426. Google Scholar
    • 53
      Grober M. S.. 1990Luminescent flash avoidance in the nocturnal crab Portunus xantusii. 2. Cardiac and visual responses to variations in simulated luminescent flashes. J. Exp. Biol. 148, 427–448. Google Scholar
    • 54
      Copeland J.& Daston M. M.. 1993Adult and juvenile flashes in the terrestrial snail Dyakia striata. Malacologia 35, 1–7. Google Scholar
    • 55
      Copeland J.. 1988Optic nerve responses to light stimulation in the bioluminescent terrestrial snail, Dyakia (Quantula) striata. Comp. Biochem. Physiol. 89A, 391–400.doi:10.1016/0300-9629(88)91046-8 (doi:10.1016/0300-9629(88)91046-8). CrossrefGoogle Scholar
    • 56
      Isobe M., Uyakul D., Goto T.& Counsilman J. J.. 1988Dyakia bioluminescence. 1. Bioluminescence and fluorescence spectra of the land snail, Dyakia striata. J. Biolum. Chemilum. 2, 73–79.doi:10.1002/bio.1170020204 (doi:10.1002/bio.1170020204). Crossref, PubMedGoogle Scholar
    • 57
      Copeland J.& Daston M. M.. 1989Bioluminescence in the terrestrial snail Dyakia (Quantula) striata. Malacologia 30, 317–324. Google Scholar
    • 58
      Counsilman J. J., Loh D., Chan S. Y., Tan W. H., Copeland J.& Maneri M.. 1987Factors affecting the rate of flashing and loss of luminescence in an Asian land snail, Dyakia striata. Veliger 29, 394–399. Google Scholar
    • 59
      Counsilman J. J.& Ong P. P.. 1988Responses of the luminescent land snail Dyakia (Quantula) striata to natural and artificial lights. J. Ethol. 6, 1–8.doi:10.1007/BF02348856 (doi:10.1007/BF02348856). CrossrefGoogle Scholar
    • 60
      Daston M. M.& Copeland J.. 1993The luminescent organ and sexual maturity in Dyakia striata. Malacologia 35, 9–19. Google Scholar
    • 61
      De Bremaeker N., Mallefet J.& Baguet F.. 1996Luminescence control in the brittlestar Amphipholis squamata: effect of cholinergic drugs. Comp. Biochem. Physiol. C 115, 75–82.doi:10.1016/S0742-8413(96)00059-X (doi:10.1016/S0742-8413(96)00059-X). CrossrefGoogle Scholar
    • 62
      Brehm P.. 1977Electrophysiology and luminescence of an ophiuroid radial nerve. J. Exp. Biol. 71, 213–227. PubMedGoogle Scholar
    • 63
      Latz M. I., Nauen J. C.& Rohr J.. 2004Bioluminescence response of four species of dinoflagellates to fully developed pipe flow. 26, 1529–1546.doi:10.1093/plankt/fbh141 (doi:10.1093/plankt/fbh141). Google Scholar
    • 64
      Widder E. a.& Case J. F.. 1981Two flash forms in the bioluminescent dinoflagellate, Pyrocystis fusiformis. 143, 43–52. Google Scholar
    • 65
      Hastings W. J.. 1995Bioluminescence. Cell physiology, vol. 31 (ed. & Sperelakis N.), pp. 665–681. New York, NY: Academic Press. CrossrefGoogle Scholar
    • 66
      Wilson T.& Hastings J. W.. 1998Bioluminescence. Ann. Rev. Cell Dev. Biol. 14, 197–230.doi:10.1146/annurev.cellbio.14.1.197 (doi:10.1146/annurev.cellbio.14.1.197). Crossref, PubMedGoogle Scholar
    • 67
      Herring P. J.. 1977Bioluminescence of marine organisms. Nature 267, 788–793.doi:10.1038/267788a0 (doi:10.1038/267788a0). CrossrefGoogle Scholar
    • 68
      Herring P. J.. 1983The spectral characteristics of luminous marine organisms. Proc. R. Soc. Lond. B 220, 183–217.doi:10.1098/rspb.1983.0095 (doi:10.1098/rspb.1983.0095). LinkGoogle Scholar
    • 69
      Broadley R. A.& Stringer I. A. N.. 2001Prey attraction by larvae of the New Zealand glowworm, Arachnocampa luminosa (Diptera: Mycetophilidae). Invertebr. Biol. 120, 170–177.doi:10.1111/j.1744-7410.2001.tb00121.x (doi:10.1111/j.1744-7410.2001.tb00121.x). CrossrefGoogle Scholar
    • 70
      Sivinski J. M.. 1998Phototropism, bioluminescence, and the Diptera. Fla Entomol. 81, 282–292. CrossrefGoogle Scholar