Naturwissenschaften

, Volume 99, Issue 9, pp 739–749 | Cite as

Light-mimicking cockroaches indicate Tertiary origin of recent terrestrial luminescence

  • Peter Vršanský
  • Dušan Chorvát
  • Ingo Fritzsche
  • Miroslav Hain
  • Robert Ševčík
Original Paper

Abstract

Bioluminescence is a common feature of the communication and defence of marine organisms, but this phenomenon is highly restricted in the terrestrial biota. Here, we present a geographical distribution of only the third order of luminescent insects—luminescent cockroaches, with all 13 known and/or herein reported new living species (based on deposited specimens). We show that, for the first time, photo-characteristics of three examined species are nearly identical with those of toxic luminescent click beetles, which they mimic. These observations are the evidence for the mimicry by light—a new type of defensive, Batesian and interordinal mimicry. Our analysis surprisingly reveals an evolutionary novelty of all living luminescent insects, while in the sea (and possibly in the soil) luminescence is present also phylogenetically in very primitive organisms.

Keywords

Evolutionary ecology Luminescence Batesian mimicry Endangered species Cockroaches 

Notes

Acknowledgments

This work has been generated during the stay of PV (NMNH award) in the Departments of Paleobiology and Entomology, National Museum of Natural History, Smithsonian Institution, Washington, DC, USA. We thank Conrad Labandeira, Finnegan Marsch and David Furth (all NMNH Washington, D.C.) for organising the stay of PV. We also thank Martina Zemanová (Institute of Physics, Bratislava), Michal Poljak (Comenius University, Bratislava) and Ľubomír Vidlička (Zoological Institute SAV, Bratislava) for technical help. We thank Adam Tomášových for revision of the manuscript and Brendan FR Edwards for linguistic revision. Supported by UNESCO-Amba, IGCP 458, Research Grant Agency VEGA 6002, 02/0152, 2/0201/10, International Scientifical and Technical Cooperation Programme (MVTS), Literary fund, Schwarz stipend, the EC’s 7FP project LASERLAB-EUROPE (grant agreement no. 228334) and ERDF—Operational Program Research and Development by means of projects NanoNet2 (ITMS:26240120018) and CEKOMAT (ITMS: 26240120006) 26240120020.

References

  1. Branham MA, Wenzel JW (2001) The evolution of bioluminescence in cantharoids (Coleoptera: Elateroidea). Fla Entomol 84:565–586CrossRefGoogle Scholar
  2. Bruggeman O, Dupont S, Mallefet J, Bannister R, Thomdyke MC (2001) Bioluminescence in the ophiuroid Amphiura filiform (O.E Miiller, 1776) is not temperature dependant. Feral and David (eds). Echinoderm Research 177–180Google Scholar
  3. Buck J (1978) Functions and evolutions of bioluminescence. In: Herring PJ (ed) Bioluminescence in action. Academic, New York, pp 419–460Google Scholar
  4. Chorvat D Jr, Chorvatova A (2006) Spectrally resolved time-correlated single photon counting: a novel approach for characterization of endogenous fluorescence in isolated cardiac myocytes. Eur Biophys J 36:73–83PubMedCrossRefGoogle Scholar
  5. Colepicolo Neto P, Bechara EJH, Costa C (1986) Oxygen toxicity aspects in luminescent and non-luminescent elaterid larvae. Insect Biochem 16:381–385CrossRefGoogle Scholar
  6. Copeland J, Daston MM (1989) Bioluminiscence in the terrestrial snail Dyakia (Quantula) striata. Malacologia 30:317–324Google Scholar
  7. Costa C, Vanin SA, Colepicolo PN (1986) Larvae of Neotropical Coleoptera. XIV. First record of bioluminescence in the family Staphylinidae (Xantholinini). Rev Bras Entomol 30:101–104Google Scholar
  8. Davies TW, Bennie J, Gaston KJ (2012) Street lighting changes the composition of invertebrate communities. Biol Lett. doi:10.1098/rsbl.2012.0216
  9. De Cock R, Matthysen E (2002) Glow-worm larvae bioluminescence (Coleoptera: Lampyridae) operates as an aposematic signal upon toads (Bufo bufo). Behav Ecol 14:103–108CrossRefGoogle Scholar
  10. Fu X et al (2007) Structure and function of the reversible glands of the aquatic firefly Luciola leii (Coleoptera: Lampyridae). Chemoecology 17:117–124CrossRefGoogle Scholar
  11. Gradstein FM et al (2004) A geologic time scale. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  12. Gray JE (1834) Alphabetical list of the figures of Mollusca, vol. 12. In: Griffith E, Pidgeon E (eds) The mollusca and radiata. Whittaker & Co, London, pp 595–601Google Scholar
  13. Gray JE (1850) Description of a new genus and several new species of terrestrial, fluviatile and marine Molluscous animals inhabiting New Zealand. Proc Zool Soc London 17:164–169Google Scholar
  14. Grober MS (1988) Brittle-star bioluminescence functions as an aposematic signal to deter crustacean predators. Anim Behav 36:493–501CrossRefGoogle Scholar
  15. Harvey EN (1956) Evolution and bioluminescence. Q Rev Biol 31:270–287CrossRefGoogle Scholar
  16. Isobe M, Takahashi H, Usami K, Hattori M, Nishigohri Y (1994) Bioluminescence mechanism on new systems. J Macromol Sci Pure Appl Chem 66:765–772Google Scholar
  17. Klass KD (1997) The external male genitalia and the phylogeny of Blattaria and Mantodea. Bonner Zool Monogr 42:1–341Google Scholar
  18. Lewis SM, Cratsley CK (2008) Flash signal evolution, mate choice, and predation in fireflies. Annu Rev Entomol 53:293–321PubMedCrossRefGoogle Scholar
  19. Lewis SM, Cratsley CK, Rooney JA (2004) Nuptial gifts and sexual selection in Photinus fireflies. Integr Comp Biol 44:234–237PubMedCrossRefGoogle Scholar
  20. Liang JH, Vršanský P, Ren D (2012) Variability and symmetry of a Jurassic nocturnal predatory cockroach (Blattida: Raphidiomimidae). Rev Mex Cienc Geol 29(2):411–421Google Scholar
  21. Lloyd JE (1965) Aggressive mimicry in Photuris: firefly femmes fatales. Science 149:653–654PubMedCrossRefGoogle Scholar
  22. Lloyd JE (1980) Male Photuris fireflies mimic sexual signal of their females’ prey. Science 210:669–671PubMedCrossRefGoogle Scholar
  23. Lloyd JE (1981) Firefly mate-rivals mimic their predators and vice versa. Nature 250:498–499CrossRefGoogle Scholar
  24. Lloyd JE (1983) Bioluminescence and communication in insects. Ann Rev Entomol 28:131–160CrossRefGoogle Scholar
  25. Lloyd JE (1984) Occurrence of aggressive mimicry in fireflies. Fla Entomol 67:368–376CrossRefGoogle Scholar
  26. Meyer-Rochow VB (2007) Glowworms: a review of Arachnocampa spp. and kin. Luminescence 22:251–265PubMedCrossRefGoogle Scholar
  27. Nicolet H (1847) Essai sur une classification des insectes aptères, de l’ordre des Thysanoures. Ann Soc Entomol Fr 2:335–395Google Scholar
  28. Ohmiya Y, Kojima S, Nakamura M, Niwa H (2005) Bioluminescence in the limpet-like snail, Latia neritoides. Bull Chem Soc Jpn 78:1197–1205CrossRefGoogle Scholar
  29. Osborn KJ, Haddock SHD, Pleijel F, Madin LP, Rouse GW (2009) Deep-sea, swimming worms with luminescent bombs. Science 325:964PubMedCrossRefGoogle Scholar
  30. Paiziev A, Krakhmalev V (2004) In vivo observation the super-weak luminescence of single living cotton cells. Abstracts of the 13th International Symposium on Bioluminescence and chemiluminescence. Luminescence 19:170Google Scholar
  31. Pellens R, Grandcolas P (2008) Catalogue of Blattaria (Insecta) from Brazil. Zootaxa 1709:1–109Google Scholar
  32. Poinar GO (2011) The evolutionary history of nematodes—as revealed in stone, amber and mummies. Nematology monographs and perspectives 9. Brill, Leiden, p 429Google Scholar
  33. Redfort KH (1982) Prey attraction as a possible function of bioluminescence in the larvae of Pyrearinus termitilluminans (Coleoptera: Elateridae). Rev Bras Zool 1:31–34CrossRefGoogle Scholar
  34. Shimomura O (2006) Bioluminescence: chemical principles and methods. World Scientific, New JerseyCrossRefGoogle Scholar
  35. Sivinski JM (1998) Phototropism, bioluminescence, and the Diptera. Fla Entomol 81:282–292CrossRefGoogle Scholar
  36. Tamura M, Yokoyama J, Ohba N, Kawata M (2005) Geographic differences in flash intervals and premating isolation between populations of the Genji firefly Luciola cruciata. Ecol Entomol 30:241–245CrossRefGoogle Scholar
  37. Vidlička Ľ (2001) Fauna Slovenska Blattaria—šváby Mantodea—Modlivky (Insecta: Orthopteroidea). Veda vydavateľstvo SAV, BratislavaGoogle Scholar
  38. Vidlička Ľ (2012) Annotated catalogue of cockroaches from Ecuador. ZootaxaGoogle Scholar
  39. Vishniakova VN (1968) Mesozoic cockroaches with external ovipositor and peculiarities of their reproduction (Blattodea). In: Rohdendorf BB (ed) Jurassic insects of Karatau. Nauka, Moscow, pp 55–86Google Scholar
  40. Viviani VR (2002) The origin, diversity, and structure function relationships of insect luciferases. Cell Mol Life Sci 59:1833–1850PubMedCrossRefGoogle Scholar
  41. Viviani VR (2004) Luciferase-like enzymes in nonluminescent beetles: a model of beetle protoluciferase? Abstracts of the 13th International Symposium on Bioluminescence and Chemiluminescence. Luminescence 19:184Google Scholar
  42. Viviani VR, Bechara EJH (1997) Bioluminescence and biological aspects of Brazilian railroad-worms (Coleoptera: Phengodidae). Ann Entomol Soc Am 90:389–398Google Scholar
  43. Viviani VR et al (2006) Active-site properties of Phrixotrix railroad worm green and red bioluminescence-eliciting luciferases. J Biochem 140:467–474PubMedCrossRefGoogle Scholar
  44. Viviani VR, Okawachi FM, Scorsato V, Abdalla FC (2008) CCD imaging of basal bioluminescence in larval fireflies: clues on the anatomic origin and evolution of bioluminescence. Photochem Photobiol Sci 7:448–452PubMedCrossRefGoogle Scholar
  45. Vršanský P (2008) Vybrané aspekty evolúcie hmyzu. Quo vadis evolúcia, DonovalyGoogle Scholar
  46. Vršanský P, Cifuentes-Ruiz P, Vidlička L, Čiampor FJR, Vega FJ (2011) Afro-Asian cockroach from Chiapas amber and the lost Tertiary American entomofauna. Geol Carpath 62:463–475CrossRefGoogle Scholar
  47. Vršanský P, Vidlička Ľ, Čiampor F Jr, Marsh F (2012a) Derived, still living cockroach genus Cariblattoides (Blattida: Blattellidae) from the Eocene sediments of Green River in Colorado, USA. Insect Sci 19(2):143–152CrossRefGoogle Scholar
  48. Vršanský P, Vidlička Ľ, Bugdaeva E, Markevich V (2012) Paleocene origin of the cockroach families Blaberidae and Polyphagidae: evidence from Amur River region of Russia. ZootaxaGoogle Scholar
  49. Wallace AR (1878) Tropical nature and other essays. Macmillan, LondonCrossRefGoogle Scholar
  50. Wilson T, Hastings JW (1998) Bioluminescence. Annu Rev Cell Dev Biol 14:197–230PubMedCrossRefGoogle Scholar
  51. SR Wing (1982) The reproductive ecologies of three species of fireflies. MS thesis, University of Florida: GainesvilleGoogle Scholar
  52. Yuma M (2007) The effect of rainfall on the long-term population dynamics of the aquatic firefly, Luciola cruciata. Entomol Sci 10:237–244CrossRefGoogle Scholar
  53. Zompro O, Fritzsche I (1999) Lucihormetica n. gen. n. sp., the first record of luminescence in an orthopteroid insect (Dictyoptera: Blaberidae: Blaberinae: Brachycolini). Amazoniana 15:211–219Google Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Peter Vršanský
    • 1
    • 2
  • Dušan Chorvát
    • 3
  • Ingo Fritzsche
    • 4
  • Miroslav Hain
    • 5
  • Robert Ševčík
    • 5
  1. 1.Geological InstituteSlovak Academy of SciencesBratislavaSlovakia
  2. 2.Paleontological InstituteRussian Academy of SciencesMoscowRussia
  3. 3.International Laser CentreBratislavaSlovakia
  4. 4.Wernigerode OT SilstedtGermany
  5. 5.Institute of Measurement ScienceSlovak Academy of SciencesBratislavaSlovakia

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