Skip to main content

Light-mimicking cockroaches indicate Tertiary origin of recent terrestrial luminescence

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Branham MA, Wenzel JW (2001) The evolution of bioluminescence in cantharoids (Coleoptera: Elateroidea). Fla Entomol 84:565–586

    Article  Google Scholar 

  • 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 177–180

  • Buck J (1978) Functions and evolutions of bioluminescence. In: Herring PJ (ed) Bioluminescence in action. Academic, New York, pp 419–460

    Google Scholar 

  • 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 36:73–83

    Article  PubMed  Google Scholar 

  • Colepicolo Neto P, Bechara EJH, Costa C (1986) Oxygen toxicity aspects in luminescent and non-luminescent elaterid larvae. Insect Biochem 16:381–385

    Article  CAS  Google Scholar 

  • Copeland J, Daston MM (1989) Bioluminiscence in the terrestrial snail Dyakia (Quantula) striata. Malacologia 30:317–324

    Google Scholar 

  • Costa C, Vanin SA, Colepicolo PN (1986) Larvae of Neotropical Coleoptera. XIV. First record of bioluminescence in the family Staphylinidae (Xantholinini). Rev Bras Entomol 30:101–104

    Google Scholar 

  • Davies TW, Bennie J, Gaston KJ (2012) Street lighting changes the composition of invertebrate communities. Biol Lett. doi:10.1098/rsbl.2012.0216

  • De Cock R, Matthysen E (2002) Glow-worm larvae bioluminescence (Coleoptera: Lampyridae) operates as an aposematic signal upon toads (Bufo bufo). Behav Ecol 14:103–108

    Article  Google Scholar 

  • Fu X et al (2007) Structure and function of the reversible glands of the aquatic firefly Luciola leii (Coleoptera: Lampyridae). Chemoecology 17:117–124

    Article  CAS  Google Scholar 

  • Gradstein FM et al (2004) A geologic time scale. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • 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 595–601

    Google Scholar 

  • 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 17:164–169

    Google Scholar 

  • Grober MS (1988) Brittle-star bioluminescence functions as an aposematic signal to deter crustacean predators. Anim Behav 36:493–501

    Article  Google Scholar 

  • Harvey EN (1956) Evolution and bioluminescence. Q Rev Biol 31:270–287

    Article  Google Scholar 

  • Isobe M, Takahashi H, Usami K, Hattori M, Nishigohri Y (1994) Bioluminescence mechanism on new systems. J Macromol Sci Pure Appl Chem 66:765–772

    CAS  Google Scholar 

  • Klass KD (1997) The external male genitalia and the phylogeny of Blattaria and Mantodea. Bonner Zool Monogr 42:1–341

    Google Scholar 

  • Lewis SM, Cratsley CK (2008) Flash signal evolution, mate choice, and predation in fireflies. Annu Rev Entomol 53:293–321

    Article  PubMed  CAS  Google Scholar 

  • Lewis SM, Cratsley CK, Rooney JA (2004) Nuptial gifts and sexual selection in Photinus fireflies. Integr Comp Biol 44:234–237

    Article  PubMed  Google Scholar 

  • Liang JH, Vršanský P, Ren D (2012) Variability and symmetry of a Jurassic nocturnal predatory cockroach (Blattida: Raphidiomimidae). Rev Mex Cienc Geol 29(2):411–421

    Google Scholar 

  • Lloyd JE (1965) Aggressive mimicry in Photuris: firefly femmes fatales. Science 149:653–654

    Article  PubMed  CAS  Google Scholar 

  • Lloyd JE (1980) Male Photuris fireflies mimic sexual signal of their females’ prey. Science 210:669–671

    Article  PubMed  CAS  Google Scholar 

  • Lloyd JE (1981) Firefly mate-rivals mimic their predators and vice versa. Nature 250:498–499

    Article  Google Scholar 

  • Lloyd JE (1983) Bioluminescence and communication in insects. Ann Rev Entomol 28:131–160

    Article  Google Scholar 

  • Lloyd JE (1984) Occurrence of aggressive mimicry in fireflies. Fla Entomol 67:368–376

    Article  Google Scholar 

  • Meyer-Rochow VB (2007) Glowworms: a review of Arachnocampa spp. and kin. Luminescence 22:251–265

    Article  PubMed  CAS  Google Scholar 

  • Nicolet H (1847) Essai sur une classification des insectes aptères, de l’ordre des Thysanoures. Ann Soc Entomol Fr 2:335–395

    Google Scholar 

  • Ohmiya Y, Kojima S, Nakamura M, Niwa H (2005) Bioluminescence in the limpet-like snail, Latia neritoides. Bull Chem Soc Jpn 78:1197–1205

    Article  CAS  Google Scholar 

  • Osborn KJ, Haddock SHD, Pleijel F, Madin LP, Rouse GW (2009) Deep-sea, swimming worms with luminescent bombs. Science 325:964

    Article  PubMed  CAS  Google Scholar 

  • 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 19:170

    Google Scholar 

  • Pellens R, Grandcolas P (2008) Catalogue of Blattaria (Insecta) from Brazil. Zootaxa 1709:1–109

    Google Scholar 

  • Poinar GO (2011) The evolutionary history of nematodes—as revealed in stone, amber and mummies. Nematology monographs and perspectives 9. Brill, Leiden, p 429

    Google Scholar 

  • Redfort KH (1982) Prey attraction as a possible function of bioluminescence in the larvae of Pyrearinus termitilluminans (Coleoptera: Elateridae). Rev Bras Zool 1:31–34

    Article  Google Scholar 

  • Shimomura O (2006) Bioluminescence: chemical principles and methods. World Scientific, New Jersey

    Book  Google Scholar 

  • Sivinski JM (1998) Phototropism, bioluminescence, and the Diptera. Fla Entomol 81:282–292

    Article  Google Scholar 

  • 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 30:241–245

    Article  Google Scholar 

  • Vidlička Ľ (2001) Fauna Slovenska Blattaria—šváby Mantodea—Modlivky (Insecta: Orthopteroidea). Veda vydavateľstvo SAV, Bratislava

    Google Scholar 

  • Vidlička Ľ (2012) Annotated catalogue of cockroaches from Ecuador. Zootaxa

  • 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 55–86

    Google Scholar 

  • Viviani VR (2002) The origin, diversity, and structure function relationships of insect luciferases. Cell Mol Life Sci 59:1833–1850

    Article  PubMed  CAS  Google Scholar 

  • 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 19:184

    Google Scholar 

  • Viviani VR, Bechara EJH (1997) Bioluminescence and biological aspects of Brazilian railroad-worms (Coleoptera: Phengodidae). Ann Entomol Soc Am 90:389–398

    Google Scholar 

  • Viviani VR et al (2006) Active-site properties of Phrixotrix railroad worm green and red bioluminescence-eliciting luciferases. J Biochem 140:467–474

    Article  PubMed  CAS  Google Scholar 

  • 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 7:448–452

    Article  PubMed  CAS  Google Scholar 

  • Vršanský P (2008) Vybrané aspekty evolúcie hmyzu. Quo vadis evolúcia, Donovaly

    Google Scholar 

  • 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 62:463–475

    Article  Google Scholar 

  • 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):143–152

    Article  Google Scholar 

  • 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. Zootaxa

  • Wallace AR (1878) Tropical nature and other essays. Macmillan, London

    Book  Google Scholar 

  • Wilson T, Hastings JW (1998) Bioluminescence. Annu Rev Cell Dev Biol 14:197–230

    Article  PubMed  CAS  Google Scholar 

  • SR Wing (1982) The reproductive ecologies of three species of fireflies. MS thesis, University of Florida: Gainesville

  • Yuma M (2007) The effect of rainfall on the long-term population dynamics of the aquatic firefly, Luciola cruciata. Entomol Sci 10:237–244

    Article  Google Scholar 

  • Zompro O, Fritzsche I (1999) Lucihormetica n. gen. n. sp., the first record of luminescence in an orthopteroid insect (Dictyoptera: Blaberidae: Blaberinae: Brachycolini). Amazoniana 15:211–219

    Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Peter Vršanský.

Additional information

Communicated by: Sven Thatje

First two authors contributed equally to this work.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Vršanský, P., Chorvát, D., Fritzsche, I. et al. Light-mimicking cockroaches indicate Tertiary origin of recent terrestrial luminescence. Naturwissenschaften 99, 739–749 (2012). https://doi.org/10.1007/s00114-012-0956-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-012-0956-7

Keywords