Evolutionary Ecology

, Volume 13, Issue 7–8, pp 655–671 | Cite as

The Evolution of Multimodal Warning Displays



Multimodal warning displays combine visual signals with components produced in other sensory modalities, for instance, aposematically coloured insects often produce a pungent odour or harsh sound when they are attacked. Recent research has focussed upon a particular odour, pyrazine, which is commonly associated with warning coloration. Our experiments have shown that pyrazine elicits hidden unlearned biases against particular visual aspects of food in foraging domestic chicks. Here we asses the current state of our knowledge about these biases, reviewing our results using pyrazine and other odours, and also presenting new data showing that sound can produce similar effects. We will discuss potential psychological mechanisms by which these foraging biases are achieved in avian predators, and potential pathways for their evolution.

aposematism hidden biases multimodal warning signals predation pyrazine 


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  1. Alexander, R.D. (1964) Acoustic communication in arthropods. Ann. Rev. Ent. 12, 495-526.CrossRefGoogle Scholar
  2. Bedford, G.O. and Chinnick, L.J. (1966) Conspicuous displays in two species of Australian stick insects. Anim. Behav. 14, 518-521.PubMedCrossRefGoogle Scholar
  3. Blest, A.D. (1957) The evolution of protective displays in the Saturnioidae and Sphingidae (Lepidoptera). Behaviour 11, 257-309.Google Scholar
  4. Blest, A.D. (1964) Protective display and sound production in some new world arctiid and ctenuchid moths. Zoologica 49, 161-181.Google Scholar
  5. Caldwell, G.S. and Rubinoff, R.W. (1983) Avoidance of venomous sea snakes by naïve herons and egrets. Auk 100, 195-198.Google Scholar
  6. Carpenter, G.D.H. (1921) Trans. R. Ent. Soc. of Lond, pp. 1-105.Google Scholar
  7. Carpenter, G.D.H. (1938) Audible emission of defensive froth by insects. Proc. Zool. Soc. A 242-251.Google Scholar
  8. Carpenter, G.D.H. and Ford, E.B. (1933) Mimicry. Methuen, London.Google Scholar
  9. Coppinger, R.P. (1970) The effects of experience and novelty on avian feeding behavior with reference to the evolution of warning coloration in butterflies. II: reactions of naïve birds to novel insects. Am. Nat. 104, 323-335.CrossRefGoogle Scholar
  10. Cott, H.B. (1940) Adaptive Coloration in Animals. Methuen, London.Google Scholar
  11. Dunning, D.C. (1967) Warning sounds of moths. Z. Tierpsy. 25, 129-138.Google Scholar
  12. Edmunds, M. (1974) Defence in Animals. Longman, Harlow, Essex.Google Scholar
  13. Ford, E.B. (1955) Moths. Methuen, London.Google Scholar
  14. Fullard, J.H. and Fenton, M.B. (1979) Jamming bat echolocation: the clicks of arctiid moths. Can. J. f. Zoo. 57, 647-649.CrossRefGoogle Scholar
  15. Gaul, A.T. (1952) Audio mimicry: an adjunct to colour mimicry. Psyche 59, 82-83.CrossRefGoogle Scholar
  16. Gittleman, J. and Harvey, P. (1980) Why are distasteful prey not cryptic? Nature 286, 149-150.CrossRefGoogle Scholar
  17. Guilford, T. (1990) Predator psychology and the evolution of prey coloration. In M.J. Crawley (ed.) Natural Enemies: the Population Biology of Predators, Parasites and Diseases. Blackwell Scientific, Oxford.Google Scholar
  18. Guilford, T. (1992) The evolution of aposematism. In D.L. Evans and J.O. Schmidt (eds) Insect defenses. State of New York Press, Albany.Google Scholar
  19. Guilford, T. (1994) Go-slow signaling and the problem of automimicry. J. Theor. Biol. 170, 311-316.CrossRefGoogle Scholar
  20. Guilford, T. and Dawkins, M.S. (1991) Receiver psychology and the evolution of animal signals. Anim. Behav. 42, 1-14.CrossRefGoogle Scholar
  21. Guilford, T. and Dawkins, M.S. (1993) Are warning colors handicaps? Evolution 47, 400-416.CrossRefGoogle Scholar
  22. Guilford, T., Nicol, C., Rothschild, M. and Moore, B.P. (1987) The biological roles of pyrazines: evidence for a warning odour function. Biol. J. Linn Soc. 31, 113-128.Google Scholar
  23. Haskell, P.T. (1956) Proc. R. Ent. Soc. Lond. C 21, 21-22.Google Scholar
  24. Haskell, P.T. (1961) Insect Sounds. H., F. & G. Witherby, London.Google Scholar
  25. Jetz, W., Rowe, C. and Guilford, T. (in press) Non-warning odors trigger innate color aversions — as long as they are novel. Behav. Ecol. Google Scholar
  26. Jones, R.B. (1986) Responses of domestic chicks to novel food as a function of sex, strain and previous experience. Behav. Proc. 12, 261-271.CrossRefGoogle Scholar
  27. Kaye, H., Mackintosh, N.J., Rothschild, M. and Moore, B.P. (1989) Odour of pyrazine potentiates an association between environmental cues and unpalatable taste. Anim. Behav. 37, 563-568.CrossRefGoogle Scholar
  28. Lane, C. and Rothschild, M. (1959) A very toxic moth: the Five-spot burnet (Zygaena trifolii Esp.). Ent. Mono.s Mag. 95, 93-94.Google Scholar
  29. Lindström, L., Rowe, C. and Guilford, T. (in press) Pyrazine odour makes visually conspicuous prey aversive. Proc. R. Soc. Lond. B. Google Scholar
  30. Majerus, M.E.N. (1994) Ladybirds. Harper Collins, London.Google Scholar
  31. Mappes, J. and Alatalo, R.V. (1997) Effects of novelty and gregariousness in survival of aposematic prey. Behav. Ecol. 8, 174-177.Google Scholar
  32. Marples, N.M. and Roper, T.J. (1996) Effects of colour and smell on the response of naive chicks towards food and water. Anim. Behav. 51, 1417-1424.CrossRefGoogle Scholar
  33. Marples, N.M. and Roper, T.J. (1997) Response of domestic chicks to methyl anthranilate odour. Anim. Behav. 53, 1263-1270.PubMedCrossRefGoogle Scholar
  34. Marples, N.M., Roper, T.J. and Harper, D.G.C. (1998) Responses of wild birds to novel prey: evidence of dietry conservatism. Oikos 83, 161-165.Google Scholar
  35. 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
  36. Masters, W.M. (1979) Insect disturbance stridulation: its defensive role. Behav. Ecol. Sociobiol. 5, 187-200.CrossRefGoogle Scholar
  37. Mastrota, F.N. and Mench J.A. (1995) Colour avoidance learning in northern bobwhites: effects of age, sex and previous experience. Anim. Behav. 50, 519-526.CrossRefGoogle Scholar
  38. Moore, B.P., Brown, M.V. and Rothschild, M. (1990) Methylalkylpyrazines in aposematic insects, their hostplants and their mimics. Chemoecology 1, 43-51.CrossRefGoogle Scholar
  39. Roper, T.J. and Cook, S.E. (1989) Responses of chicks to brightly coloured insect prey. Behaviour 110, 276-293.Google Scholar
  40. Roper, T.J. and Marples, N.M. (1996) Colour preferences of domestic chicks in relation to food and water presentation. Appl. Anim. Behav. Sci. 54, 207-213.CrossRefGoogle Scholar
  41. 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
  42. Roper, T.J. and Redston, S. (1987) Conspicuousness of distasteful prey a.ects the strength and durability of one-trial aversive learning. Anim. Behav. 35, 739-747.CrossRefGoogle Scholar
  43. Roper, T.J. and Wistow, R. (1986) Aposematic coloration and avoidance learning in chicks. Q. J. Exp. Psychol. 38, 141-149.Google Scholar
  44. Rothschild, M. (1961) Defensive odours and Mullerian mimicry among insects. Trans. R. Ent. Soc. Lond. 113, 101-121.Google Scholar
  45. Rothschild, M. (1964) A note on the evolution of defensive and repellent odours of insects. Entomologist 97, 276-279.Google Scholar
  46. Rothschild, M. (1965). Proc. R. Ent. Soc. Lond. C 30, 3.Google Scholar
  47. Rothschild, M. and Haskell, P.T. (1966) Stridulation of the garden tiger moth Arctia caja L. audible to the human ear. Proc. R. Ent. Soc. Lond. A 41, 167-170.Google Scholar
  48. Rothschild, M. and Moore, B.P. (1987) Pyrazines as alerting signals in toxic plants and insects. In V. Labeyrie, G. Fabres and D. Fachaise (eds) Insect-Plants. W. Junk, Dordrecht.Google Scholar
  49. Rothschild, M., Moore, B.P. and Brown, W.V. (1984) Pyrazines as warning odour components in the monarch butterfly, Danaus plexippus, and in moths of the genera Zygaena and Amata (Lepidoptera). Biol. J. Linn. Soc. 23, 372-380.Google Scholar
  50. Rowe, C. (1998) Multicomponent signals. Unpublished D.Phil thesis, University of Oxford, Oxford.Google Scholar
  51. Rowe, C. (1999) Receiver psychology and the evolution of multicomponent signals. Anim. Behav. 58, 921-931.PubMedCrossRefGoogle Scholar
  52. 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
  53. Rowe, C. and Guilford, T. (1999) Novelty effects in a multimodal warning signal. Anim. Behav. 57, 341-346.PubMedCrossRefGoogle Scholar
  54. Schuler, W. and Hesse, E. (1985) On the function of warning coloration: a black and yellow pattern inhibits prey-attack by naive domestic chicks. Behav. Ecol. Sociobiol. 16, 249-255.CrossRefGoogle Scholar
  55. Síllen-Tullberg, B. (1985) The significance of coloration per se, independent of background, for predator avoidance of aposematic prey. Anim. Behav. 33, 1382-1384.CrossRefGoogle Scholar
  56. Smith, S.M. (1975) Innate recognition of coral snake pattern by a possible avian predator. Science 187, 759-760.PubMedGoogle Scholar
  57. Wallace, A.R. (1891) Natural Selection and Tropical Nature: essays on Descriptive and Theoretical Biology. MacMillan & Co, London.Google Scholar
  58. Wood-Gush, D.G.M. (1989) The Behaviour of the Domestic Fowl. Nimrod Press, Alton, Hants.Google Scholar
  59. Woolfson, A. and Rothschild, M. (1990) Speculating about pyrazines. Proc. R. Soc. Lond. B 242, 113-119.Google Scholar

Copyright information

© Kluwer Academic Publishers 1999

Authors and Affiliations

  1. 1.Department of PsychologyUniversity of NewcastleNewcastle upon TyneUK
  2. 2.Department of ZoologyOxfordUK

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