Evolutionary Ecology

, Volume 13, Issue 7–8, pp 619–639

Aposematism and Bioluminescence: Experimental evidence from Glow-worm Larvae(Coleoptera: Lampyridae)

Article

Abstract

Bioluminescence most likely evolved under selection from the visually guided behaviours of co-occurring organisms, in particular that of predators. Many possible functions of light signals have been proposed and some are supported, but whatever their function may be, they make an easy target of the emitter unless it is defended. Therefore, we want to emphasise that in many cases bioluminescence can only have evolved through a defensive function. If this were the case, one would expect multimodal adaptiveness of luminescence with at least some evidence for a defensive function. Light signals could be used in many ways to reduce predation, but for spontaneous glowing species in particular, aposematism seems the only functional strategy. In a preliminary experiment with glowing and non-glowing dummy prey, we found that wild-caught toads discriminated against glowing prey. They showed significantly lower attack responses and higher latencies towards glowing prey dummies. However, some of the toads were less reluctant because they did not distinguish initially between prey with or without the light stimulus. Since the toads were collected in areas abundant with lampyrid glow-worms, which is the only luminous organism at this locality, and our results concur with the general evidence that they may have had previous experiences with this prey, we attribute the result to luminescent aposematism. From the literature, and from our own experiments, we know that toads and many other potential predators experience lampyrids as disagreeable prey. In future experiments we will test whether glow-worms are defended by luminescent aposematism or not.

aposematism bioluminescence Bufo bufo defence evolution Lampyridae predation 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abraham, M.V. and Townsend, L.D. (1993) Bioluminescence in dinoflagellates a test of the burglar alarm hypothesis. Ecology 74, 258-260.CrossRefGoogle Scholar
  2. Aho, A.-C., Donner, K., Hydén, C., Larsen, L.O. and Reuter, T. (1988) Low retinal noise in animals with low body temperature allows high visual sensitivity. Nature 334, 348-350.PubMedCrossRefGoogle Scholar
  3. Aho, A.-C., Donner, K., Helenius, S., Larsen, L.O. and Reuter, T. (1993) Visual performance of the toad (Bufo bufo) at low light levels: retinal ganglion cell responses and prey-catching accuracy. J. Comp. Physiol. A 172, 671-682.PubMedCrossRefGoogle Scholar
  4. Balduf, W.V. (1935) The Bionomics of Entomophagous Coleoptera. John Swift and Co., St Louis, MD, USA.Google Scholar
  5. Barth, F.G., Nakagawa, T. and Eguchi, E. (1993) Vision in the ctenid spider Cupiennus salei: spectral range and absolute sensitivity. J. Exp. Biol. 181, 63-79.Google Scholar
  6. Blair, K.G. (1927) An aquatic lampyrid larva from S. Celebes. Trans. Ent. Soc. Lond. 1927, 43-45.Google Scholar
  7. Blum, M.S. and Sannasi, A. (1974) Reflex bleeding in the lampyrid Photinus pyralis: defensive function. J. Insect Physiol. 20, 451-460.CrossRefGoogle Scholar
  8. Branham, M. and Wenzel, J.W. (2000) The evolution of sexual communication in fireflies. In Abstracts of the XIth International Symposium in Bioluminescence and Chemiluminescence (coordinated by Haddock, S.). Luminescence 15, 202.Google Scholar
  9. Buck, J.B. (1948) The anatomy and physiology of the light organ in fireflies. Ann. N.Y. Acad. Sci. 49, 397-482.Google Scholar
  10. Buck, J.B. (1978) Functions and Evolutions of Bioluminescence. In P.J. Herring (ed.) Bioluminescence in Action, Academic Press, London, pp. 419-460.Google Scholar
  11. Bushman, L.L. (1984) Biology of the firefly Pyractomena lucifera (Coleoptera: Lampyridae). Florida Entomologist 67, 529-542.Google Scholar
  12. Bushman, L.L. (1988) Light organs of immature fireflies (Coleoptera: lampyridae) as eye-spot/false-head displays. Coleops. Bull. 42, 94-97.Google Scholar
  13. Buskey, E.J. and Swift, E. (1990) An encounter model to predict natural planktonic bioluminescence. Limnol. Oceanogr. 35, 1469-1485.Google Scholar
  14. Carlson, A.D. and Copeland, J. (1978) Behavioral plasticity in the flash communication systems of fireflies. Am. Sci. 66, 340-346.Google Scholar
  15. Carlson, A.D. and Copeland, J. (1985) Communication in insects. I. Flash communication in fireflies. Q. Rev. Biol. 60, 415-436.CrossRefGoogle Scholar
  16. Case, J.F., Haddock, S.H.D. and Harper, R.D. (1993) The Ecology of Bioluminescence. In A.A. Szalay, L.J. Kricka and P.E. Stanley (eds.), Bioluminescence and Chemiluminescence, John Wiley, New York, pp. 115-122.Google Scholar
  17. Christensen, T.A. and Carlson, A.D. (1982) The neurophysiology of larval firefly luminescence: direct activation through four bifurcating (DUM) neurons. J. Comp. Physiol. 148, 503-514.CrossRefGoogle Scholar
  18. Costa, C., Vanin, S.A. and Neto, P.C. (1986) Larvae of neotropical Coleoptera. XIV. First record of bioluminescence in the Family Staphylinidae (Xantholinini). Revta. Bras. Ent. 30, 101-104.Google Scholar
  19. Cott, H.B. (1940) Adaptive Coloration in Animals. Menthuen & Co Ltd, London.Google Scholar
  20. Crawley, M.J. (1993) GLIM for Ecologists (Methods in Ecology). Blackwell Science Ltd., Oxford, London.Google Scholar
  21. Crowson, R.A. (1972) A review of the classification of Cantharoidea (Coleoptera), with the definition of two new families, Cneoglossidae and Omethidae. Revta. Univ. Madr. 21, 35-77.Google Scholar
  22. Daly, M. (1978) The cost of mating. Am. Nat. 112, 771-774.CrossRefGoogle Scholar
  23. Donner, K.O. and Rushton, W.A.H. (1959) Rod-cone interaction in the frog's retina analysed by the Stiles-Crawford effect and by dark-adaptation. J. Physiol. 149, 303-317.PubMedGoogle Scholar
  24. Dreisig, H. (1974) Observations on the luminescence of the larval glowworm, Lampyris noctiluca. Ent. Scand. 5, 103-109.Google Scholar
  25. Edmunds, M. (1974) Defence in Animals. A Survey of Anti-predator Defences. Longman, New York.Google Scholar
  26. Eisner, T., Goetz, M.A., Hill, D.E., Smedley, S.R. and Meinwald, J. (1997) Firefly 'femmes fatales’ acquire defensive steroids (lucibufagins) from their firefly prey. Proc. Natl. Acad. Sci. USA 94, 9723-9728.PubMedCrossRefGoogle Scholar
  27. Eisner, T., Wiemer, D.F., Haynes, L.W. and Meinwald, J. (1978) Lucibufagins: defensive steroids from the fireflies Photinus ignitus and P. marginellus (Coleoptera: Lampyridae). Proc. Nat. Acad. Sci. USA. 75, 905-908.PubMedCrossRefGoogle Scholar
  28. Endler, J.A. (1993) Interactions between predators and prey. In J.R. Krebs and N.B. Davies (eds.), Behavioural Ecology, Blackwell Scientific Publications, Oxford, pp. 169-196.Google Scholar
  29. Esaias, W.E. and Curl, H.C. (1972) Effect of dinoflagellate bioluminescence on copepod ingestion rates. Limnol. Oceanogr. 17, 901-906.CrossRefGoogle Scholar
  30. Ewert, J.P. (1987) Neuroethology of releasing mechanisms: prey-catching in toads. Behav. Brain Sci. 10, 337-405.Google Scholar
  31. Ewert, J.P., Burghagen, H and Schürg-Pfeiffer, E. (1983) Neuroethological analysis of the innate releasing mechanism for prey-catching behaviour in toads. In P.J. Ewert, R.R. Capranica and D.J. Ingle (eds.), Advances in vertebrate neuroethology, NATO ASI Series. Series A: Life Sciences 56. Plenum Press, New York and London, pp. 413-475.Google Scholar
  32. González, A., Hare, J.F. and Eisner, T. (1999) Chemical egg defense in Photuris firefly 'femmes fatales'. Chemoecology 9, 177-185.CrossRefGoogle Scholar
  33. Granit, R. (1942) Colour receptors of the frog's retina. Acta Physiol. Scan. 3, 137-151.Google Scholar
  34. Grober, M.S. (1988a) Brittle-star bioluminescence functions as an aposematic signal to deter crustacean predators. Anim. Behav. 36, 493-501.Google Scholar
  35. Grober, M.S. (1988b) Responses of tropical reef fauna to brittle-star luminescence (Echinodermata: Ophiuroidea). J. Exp. Mar. Biol. Ecol. 115, 157-168.CrossRefGoogle Scholar
  36. Grober, M.S. (1989) Bioluminescent aposematism: a reply to Guilford & Cuthill. Anim. Behav. 37, 341-343.CrossRefGoogle Scholar
  37. Guilford, T. (1988) The evolution of conspicuous coloration. Am. Nat. 131, s7-s21.CrossRefGoogle Scholar
  38. Guilford, T. and Cuthill, I. (1989) Aposematism and bioluminescence. Anim. Behav. 37, 339-341.CrossRefGoogle Scholar
  39. Guilford, T., Nicol, C., Rothschild, M. and Moore, B. (1987) The biological roles of pyrazines: evidence for a warning odour function. Biol. J. Linn. Soc. 31, 113-128.Google Scholar
  40. Halverson, R.C., Case, J.F., Buck, J. and Tiemann, D. (1973) Control of luminescence in phengodid beetles. J. Insect Physiol. 19, 1327-1339.CrossRefGoogle Scholar
  41. Harper, R.D. and Case, J.F. (1999) Disruptive counterillumination and its anti-predatory value in the plainfish midshipman Porichthys notatus. Marine Biol. 134, 529-540.CrossRefGoogle Scholar
  42. Harvey, E.N. (1952) Bioluminescence. Academic Press, New York.Google Scholar
  43. Hastings, J.W. (1971) Ventral luminescence to camouflage the silhouette. Science 173, 1016-1017.PubMedGoogle Scholar
  44. Hastings, J.W. (1982) O2 and emitting species in bioluminescence. In M. Nozaki (ed.), Oxygenases and Oxygen Metabolism, Academic Press, New York, pp. 225-237.Google Scholar
  45. Hastings, J.W. (1983) Biological diversity, chemical mechanisms, and the evolutionary origins of bioluminescent systems. J. Mol. Evolution 19, 309-321.CrossRefGoogle Scholar
  46. Hastings, J.W. and Morin, J.G. (1991) Bioluminescence. Chap. 3. In C.L. Prosser (ed.), Neural and Integrative Animal Physiology, Wiley Interscience, New York, pp. 131-170.Google Scholar
  47. Herring, P.J. (1978) A classification of luminous organisms. In P.J. Herring (ed.), Bioluminescence in Action, Academic Press, London, pp. 461-476.Google Scholar
  48. Ingle, D.J. (1971) Prey-catching behavior of anurans toward moving and stationary objects. Vision Res. (suppl.) 3, 447-456.PubMedCrossRefGoogle Scholar
  49. Jacobs, G.H. (1981) Comparative Color Vision. Academic Press, New York.Google Scholar
  50. Jones, F.M. (1932) Insect coloration and the relative acceptability of insects to birds. Trans. Ent. Soc. London 80, 345-385.Google Scholar
  51. Kaufmann, T. (1965) Ecological and biological studies on the West African firefly Luciola discicollis (Coleoptera: Lampyridae). Ann. Ent. Soc. Am. 58, 414-426.Google Scholar
  52. Koskelainen, A., Hemilä, S. and Donner, K. (1994) Spectral sensitivities of short-wavelength and long-wavelength sensitive cone mechanisms in the frog retina. Acta Physiol. Scand. 152, 115-124.PubMedCrossRefGoogle Scholar
  53. Larsen, L.O. and Pedersen, J.N. (1982) The snapping response of the toad, Bufo bufo, towards prey dummies at very low light intensities. Amphibia-Reptilia 2, 321-327.Google Scholar
  54. Lindström, L (2000) Evolution of Conspicuous warning Signals. Academic Dissertation. Jyväskylä Studies in Biological and Environmental Science 81. University of Jyväskylä, Finland.Google Scholar
  55. Littel, R.C., Milliken, G.A., Stroup, W.W. and Wolfinger, R.D. (1996) SAS® System for Mixed Models. SAS Institute Inc., Cary.Google Scholar
  56. Lizotte, R.S. and Rovner, J.S. (1988) Nocturnal capture of fireflies by lycosid spiders: visual vs. vibratory stimuli. Anim. Behav. 36, 1809-1815.Google Scholar
  57. Lloyd, J.E. (1968) Illumination, another function of firefly flashes? Ent. News 79, 265-268.Google Scholar
  58. Lloyd, J.E. (1972) Chemical communication in fireflies. Env. Ent. 1, 265-266.Google Scholar
  59. Lloyd, J.E. (1973) Firefly parasites and predators. Coleops. Bull. 27, 90-106.Google Scholar
  60. Lloyd, J.E. (1978) Insect Bioluminescence. In P.J. Herring (ed.), Bioluminescence in Action, Academic Press, London, pp. 241-272.Google Scholar
  61. Lloyd, J.E. (1983) Bioluminescence and communication in insects. Ann. Rev. Entomol. 28, 131-160.CrossRefGoogle Scholar
  62. Lloyd, J.E. (1989) Bat (Chiroptera) connections with firefly (Coleoptera: Lampyridae) luminescence. Coleops. Bull. 43, 83-91.Google Scholar
  63. Mallet, J and Singer, M.C. (1987) Individual selection, kin selection, and the shifting balance in the evolution of warning colours: the evidence from butterflies. Biol. J. Linn. Soc. 32, 337-350.Google Scholar
  64. Mallet, J. and Joron, M. (1999) Evolution of diversity in warning color and mimicry: Polymorphism, shifting balance and speciation. Ann. Rev. Ecol. System. 30, 201-234.CrossRefGoogle Scholar
  65. Marples, N.M. and Roper, T.J. (1996) Effects of novel colour and smell on the response of na chicks towards food and water. Anim. Behav. 51, 1417-1424.CrossRefGoogle Scholar
  66. Marples, N.M., van Veelen, W. and Brakefield, P.M. (1994) The relative importance of colour, taste and smell in the protection of an aposematic insect Coccinella septempunctata. Anim. Behav. 48, 967-974.CrossRefGoogle Scholar
  67. McDermott, F.A. (1964) The taxonomy of the Lampyridae (Coleoptera). Trans. Am. Entom. Soc. 90, 1-72.Google Scholar
  68. McElroy, W.D. and Seliger, H.H. (1962) Origin and evolution of bioluminescence. In A. Szent-Gyürgyi, M. Kasha and B. Pullman (eds.), Horizon in Biochemistry, Academic Press, New York, pp. 91-101.Google Scholar
  69. Mensinger, A.F. and Case, J.F. (1992) Dinoflagellate luminescence increases susceptibility of zooplankton to teleost predation. Mar. Biol. 112, 207-210.CrossRefGoogle Scholar
  70. Morin, J.G. (1983) Review of coastal bioluminescence. Bull. Mar. Sci. 33, 787-817.Google Scholar
  71. Partridge, J.C. and Douglas, R.H. (1995) Far-red sensitivity of dragon fish. Nature 375, 21-22.CrossRefGoogle Scholar
  72. Porter, K.G. and Porter, J.W. (1979) Bioluminescence in marine plankton: a coevolved antipredation system. Am. Nat. 114, 458-461.CrossRefGoogle Scholar
  73. Poulton, E.B. (1890) The Colours of Animals. Their Meaning and Use. Especially Considered in the Case of Insects. Kegan Paul, Trench, Trübner & Co, Ltd, London.Google Scholar
  74. Redford, K.H. (1982) Prey attraction as a possible function of bioluminescence in the larvae of Pyrearinus termitilluminans (Coleoptera: Elateridae). Revta. Bras. Zool. S. Paulo 1, 31-34.Google Scholar
  75. Richards, A.M. (1960) Observations on the New Zealand glowworm Arachnocampa luminosa (Skuse) 1890. Trans. R. Soc. N.Z. 88, 559-574.Google Scholar
  76. Roper, T.J. and Marples, N.M. (1997) Odour and colour as cues for taste-avoidance learning in domestic chicks. Anim. Behav. 53, 1241-1250.PubMedCrossRefGoogle Scholar
  77. Rothschild, M. (1961) Defensive odours and müllerian mimicry among insects. Trans. R. Ent. Soc. Lond. 113, 101-121.Google Scholar
  78. Rowe, C. and Guilford, T. (1996) Hidden colour aversions in domestic chicks triggered by pyrazine odours of insect warning displays. Nature 383, 520-522.CrossRefGoogle Scholar
  79. Rowe, C. and Guilford, T. (2001) The evolution of multimodal warning displays. Evol. Ecol. 13, 655-671.CrossRefGoogle Scholar
  80. Schwalb, H.H. (1961) Beiträge zur Biologie der einheimischen Lampyriden Lampyris noctiluca Geoffr. und Phausis splendidula Lec. und experimentelle Analyse ihres Beutefang-und Sex-ualsverhaltens. Zool. Jb. Syst. 88, 399-550.Google Scholar
  81. Seliger, H.H. (1975) The origin of bioluminescence. Photochem. Photobiol. 21, 355-361.PubMedGoogle Scholar
  82. Sexton, O.J. (1960) Experimental studies of artificial batesian mimics. Behaviour 3–4, 244-252.Google Scholar
  83. Sexton, O.J. (1966) Differential predation by the lizard, Anolis carolinensis, upon unicoloured and polycoloured insects after an interval of no contact. Anim. Behav. 12, 101-110.CrossRefGoogle Scholar
  84. Sexton, O.J., Hoger, C. and Ortleb, E. (1963) Anolis carolinensis: effects of feeding on reaction to aposematic prey. Science 153, 1140.Google Scholar
  85. Sivinski, J. (1981a) The nature and possible functions of luminescence in Coleoptera larvae. Coleops. Bull. 35, 167-179.Google Scholar
  86. Sivinski, J. (1981b) Arthropods attracted to luminous fungi. Psyche 3–4, 383-390.Google Scholar
  87. Sivinski, J. (1982) Prey attraction by luminous larvae of the fungus gnat Orfelia fultoni. Ecol. Entom. 7, 443-446.CrossRefGoogle Scholar
  88. Sydow, S.L. and Lloyd, J.E. (1975) Distasteful fireflies sometimes emetic, but not lethal. Fla. Ent. 58, 312.Google Scholar
  89. Turner, J.R.G. and Mallet, J.L.B. (1996) Did forest islands drive the diversity of warningly coloured butterflies? Biotic drift and the shifting balance. Phil. Trans. R. Soc. Lond. B 351, 835-845.Google Scholar
  90. Tyler, J. (1994). Glow-worms. Herald Press, Stratford-upon-Avon, UK.Google Scholar
  91. Underwood, T.J., Tallamy, D.W. and Pesek, J.D. (1997) Bioluminescence in firefly larvae: a test of the aposmatic display hypothesis (Coleoptera: Lampyridae). J. Insect Behav., 10: 365-370.Google Scholar
  92. Verbeke, G. and Molenberghs, G. (1997) Linear Mixed Models in Practice. A SAS-Oriented Approach. In P. Bickel, P. Diggle, S. Fienberg, K. Krickeberg, I. Olkin, N. Wermuth and S. Zeger (eds), Lecture Notes in Statistics 126, Springer-Verlag, New York.Google Scholar
  93. Viviani, V.R. and Bechara, E.J.H. (1995) Bioluminescence of Brazilian fireflies (Coleoptera: Lampyridae): spectral distribution and pH effect on luciferase-elicited colors. Comparison with elaterid and phengodid luciferases. Photochem. Photobiol. 62, 490-495.Google Scholar
  94. Viviani, V.R. and Bechara, E.J.H. (1997) Bioluminescence and biological aspects of Brazilian railroad-worms (Coleoptera: Phengodidae). Ann. Ent. Soc. Am. 90, 389-398.Google Scholar
  95. Wang, D. and Ewert, J.P. (1992) Configurational pattern discrimination responsible for dishabituation in common toads Bufo bufo (L.): behavioral tests of the predictions of a neural model. J. Comp. Physiol. A 170, 317-325.PubMedCrossRefGoogle Scholar
  96. White, H.H. (1979) Effects of dinoflagellate bioluminescence on the ingestion rates of herbivorous zooplankton. J. Exp. mar. Biol. Ecol. 36, 217-224.CrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1999

Authors and Affiliations

  1. 1.Group of Animal Ecology, Department of BiologyUniversity of Antwerp (U.I.A.)AntwerpBelgium

Personalised recommendations