Advertisement

Evolutionary Ecology

, 23:919 | Cite as

Newly emerged Batesian mimicry protects only unfamiliar prey

  • Petr VeselýEmail author
  • Roman Fuchs
Original Paper

Abstract

The evolution of Batesian mimicry was tested experimentally using avian predators. We investigated the effect of a search image on the protection effectiveness of a newly emerged Batesian mimic. The two groups of predators (adult great tits, Parus major) differed in prior experience with prey from which the mimic evolved. The Guyana spotted roach (Blaptica dubia) was used as a palatable prey from which the mimic emerged, and red firebug (Pyrrhocoris apterus) was used as a model. Optical signalization of the insect prey was modified by a paper sticker placed on its back. The cockroaches with the firebug pattern sticker were significantly better protected against tits with no prior experience with cockroaches. The protection of the firebug sticker was equally effective on cockroaches as it was on firebugs. The cockroaches with firebug stickers were not protected against attacks of tits, which were familiar with unmodified cockroaches better than cockroaches with a cockroach sticker. We suppose that pre-trained tits acquired the search image of a cockroach, which helped them to reveal the “fake” Batesian mimic. Such a constraint of Batesian mimicry effectiveness could substantially decrease the probability of evolution of pure Batesian mimic systems.

Keywords

Evolution of Batesian mimicry Warning signalization Neophobia Search image 

Notes

Acknowledgments

We thank Dr. Keith Edwards for the language improvement. We thank the Academy of Sciences of the Czech Republic (IAA601410803), Ministry of Education, Youth and Sport of the Czech Republic (MSM 6007665801) and the Grant Agency of the Czech Republic (206/08/H044) for financial support. Authors are licensed for catching and ringing birds (Bird Ringing Centre Prague No. 1004) and for animal experimentation (Czech Animal Welfare Commission No. 489/01).

References

  1. Alatalo RV, Mappes J (1996) Tracking the evolution of warning signals. Nature 382(6593):708–710CrossRefGoogle Scholar
  2. Audinet-Serville JG (1838) Suites à buffon. ParisGoogle Scholar
  3. Bates HW (1862) Contributions to an insect fauna of the Amazon Valley. Trans Linn Soc Zool 23:495–566 CrossRefGoogle Scholar
  4. Blough DS (1985) Discrimination of letters and random dot patterns by pigeons and humans. J Exp Psychol Anim B 11(2):261–280CrossRefGoogle Scholar
  5. Blough DS (1989a) Contrast as seen in visual-search reaction-times. J Exp Anal Behav 52(3):199–211CrossRefPubMedGoogle Scholar
  6. Blough DS (1989b) Odd-item search in pigeons—display size and transfer effects. J Exp Psychol Anim B 15(1):14–22CrossRefGoogle Scholar
  7. Blough DS, Franklin JJ (1985) Pigeon discrimination of letters and other forms in texture displays. Percept Psychophys 38(6):523–532PubMedGoogle Scholar
  8. Bond AB, Kamil AC (1999) Searching image in blue jays: facilitation and interference in sequential priming. Anim Learn Behav 27(4):461–471Google Scholar
  9. Chiszar D, Radcliffe CW, Overstreet R et al (1985) Duration of strike-induced chemosensory searching in cottonmouths (Agkistrodon piscivorus) and a test of the hypothesis that striking prey creates a specific search image. Can J Zool 63(5):1057–1061CrossRefGoogle Scholar
  10. Darst CR, Cummings ME (2006) Predator learning favours mimicry of a less-toxic model in poison frogs. Nature 440(7081):208–211CrossRefPubMedGoogle Scholar
  11. Davies NB (1977) Prey selection and search strategy of spotted flycatcher (Muscicapa striata)—field study on optimal foraging. Anim Behav 25:1016–1024CrossRefGoogle Scholar
  12. Dawkins M (1971) Perceptual changes in chicks: another look at the ‘search image’ concept. Anim Behav 19:566–574CrossRefGoogle Scholar
  13. Dittrich W, Gilbert F, Green P et al (1993) Imperfect mimicry—a pigeons perspective. P R Soc B-Biol Sci 251(1332):195–201CrossRefGoogle Scholar
  14. Dukas R (2002) Behavioural and ecological consequences of limited attention. Philos T R Soc B 357(1427):1539–1547CrossRefGoogle Scholar
  15. Dukas R (2004) Causes and consequences of limited attention. Brain Behav Evol 63(4):197–210CrossRefPubMedGoogle Scholar
  16. Dukas R, Ellner S (1993) Information processing and prey detection. Ecology 74:1337–1346CrossRefGoogle Scholar
  17. Dukas R, Kamil AC (2001) Limited attention: the constraint underlying search image. Behav Ecol 12:192–199CrossRefGoogle Scholar
  18. Exnerová A, Landová E, Štys P et al (2003) Reactions of passerine birds to aposematic and non-aposematic bugs (Pyrrhocoris apterus; Heteroptera). Biol J Linn Soc 78:517–525CrossRefGoogle Scholar
  19. Exnerová A, Štys P, Fučíková E et al (2007) Avoidance of aposematic prey in European Tits (Paridae): Learned or innate? Behav Ecol 18(1):148–156CrossRefGoogle Scholar
  20. Farine JP, Bombard O, Brossut R et al (1992) Chemistry of defensive secretions in nymphs and adults of fire bug, Pyrrhocoris apterus L. (Heteroptera, Pyrrhocoridae). J Chem Ecol 18(10):1673–1682CrossRefGoogle Scholar
  21. Fisher RA (1922) On the interpretation of χ2 from contingency tables, and the calculation of P. J R Stat Soc 85(1):87–94CrossRefGoogle Scholar
  22. Fisher RA (1930) The genetical theory of natural selection. Mimicry, 2nd edn. Dover, New YorkGoogle Scholar
  23. Gazit I, Goldblatt A, Terkel J (2005) Formation of an olfactory search image for explosives odours in sniffer dogs. Ethology 111(7):669–680CrossRefGoogle Scholar
  24. Golding YC, Edmunds M (2000) Behavioural mimicry of honeybees (Apis mellifera) by droneflies (Diptera:Syrphidae:Eristalis spp.). P R Soc B-Biol Sci 267(1446):903–909CrossRefGoogle Scholar
  25. Golding YC, Nenos AR, Edmunds M (2001) Similarity in flight behaviour between the honeybee Apis mellifera (Hymenoptera:Apidae) and its presumed mimic, the dronefly Eristalis tenax (Diptera:Syrphidae). J Exp Biol 204(1):139–145PubMedGoogle Scholar
  26. Greenberg R, Mettke-Hoffman C (2001) Ecological aspects of neophobia and exploration in birds. Cur Ornit 16:119–169Google Scholar
  27. Guilford T (1990) Evolutionary pathways to Aposematism. Int J Ecol 11(6):835–841Google Scholar
  28. Hetz M, Slobodchikoff CN (1988) Predation pressure on an imperfect Batesian Mimicry Complex in the presence of alternative prey. Oecologia 76(4):570–573Google Scholar
  29. Howarth B, Edmunds M, Gilbert F (2004) Does the abundance of hoverfly (syrphidae) mimics depend on the numbers of their hymenopteran models? Evolution 58(2):367–375PubMedGoogle Scholar
  30. Johnstone RA (2002) The evolution of inaccurate mimics. Nature 418(6897):524–526CrossRefPubMedGoogle Scholar
  31. Kauppinen J, Mappes J (2003) Why are wasps so intimidating: field experiments on hunting dragonflies (Odonata: Aeshna grandis). Anim Behav 66:505–511CrossRefGoogle Scholar
  32. Kelly DJ, Marples NM (2004) The effects of novel odour and colour cues on food acceptance by the zebra finch, Taeniopygia guttata. Anim Behav 68:1049–1054CrossRefGoogle Scholar
  33. Komárek S (2003) Mimicry, Aposematism and related phenomena—Mimetism in nature and the history of its study. LINCOM, MünchenGoogle Scholar
  34. Lindström L (1999) Experimental approaches to studying the initial evolution of conspicuous aposematic signalling. Evol Ecol 13(7–8):605–618CrossRefGoogle Scholar
  35. Lindström L, Alatalo RV, Mappes J (1997) Imperfect Batesian mimicry—the effects of the frequency and the distastefulness of the model. P R Soc B-Biol Sci 264(1379):149–153CrossRefGoogle Scholar
  36. Lindström L, Rowe C, Guilford T (2001) Pyrazine odour makes visually conspicuous prey aversive. P R Soc B-Biol Sci 268(1463):159–162CrossRefGoogle Scholar
  37. Lindström L, Alatalo RV, Lyytinen A et al (2004) The effect of alternative prey on the dynamics of imperfect Batesian and Mullerian mimicries. Evolution 58(6):1294–1302PubMedGoogle Scholar
  38. Lindström L, Lyytinen A, Mappes J et al (2006) Relative importance of taste and visual appearance for predator education in Mullerian mimicry. Anim Behav 72:323–333CrossRefGoogle Scholar
  39. Mappes J, Alatalo RV (1997) Batesian mimicry and signal accuracy. Evolution 51:2050–2053CrossRefGoogle Scholar
  40. Marples NM, Kelly DJ (1999) Neophobia and dietary conservatism: two distinct processes? Evol Ecol 13:641–653CrossRefGoogle Scholar
  41. Marples NM, Roper TJ (1996) Effects of novel colour and smell on the response of naive chicks towards food and water. Anim Behav 51:1417–1424CrossRefGoogle Scholar
  42. Marples NM, Roper TJ, Harper DGC (1998) Responses of wild birds to novel prey: evidence of dietary conservatism. Oikos 83(1):161–165CrossRefGoogle Scholar
  43. Marples NM, Kelly DJ, Thomas RJ (2005) Perspective: the evolution of warning coloration is not paradoxical. Evolution 59(5):933–940PubMedGoogle Scholar
  44. Nachtigall W (2003) High flight speeds in subalpine diptera. Entomol Gen 26(4):235–239Google Scholar
  45. Nelson XJ, Jackson RR (2006) Compound mimicry and trading predators by the males of sexually dimorphic Batesian mimics. P R Soc B-Biol Sci 273(1584):367–372CrossRefGoogle Scholar
  46. Nelson XJ, Jackson RR, Li DQ et al (2006a) Innate aversion to ants (Hymenoptera:Formicidae) and ant mimics: experimental findings from mantises (Mantodea). Biol J Linn Soc 88(1):23–32CrossRefGoogle Scholar
  47. Nelson XJ, Li DQ, Jackson RR (2006b) Out of the frying pan and into the fire: a novel trade-off for batesian mimics. Ethology 112(3):270–277CrossRefGoogle Scholar
  48. Osorio D, Miklosi A, Gonda Z (1999) Visual ecology and perception of coloration patterns by domestic chicks. Evol Ecol 13(7–8):673–689CrossRefGoogle Scholar
  49. Pietrewicz A, Kamil AC (1979) Search image formation in the blue jay (Cyanocitta cristata). Science 204:1332–1333CrossRefPubMedGoogle Scholar
  50. Poulton EB (1890) The colours of animals. Int Sci Ser 68:360–395Google Scholar
  51. Prudic KL, Shapiro AM, Clayton NS (2002) Evaluating a putative mimetic relationship between two butterflies, Adelpha bredowii and Limenitis lorquini. Ecol Entomol 27(1):68–75CrossRefGoogle Scholar
  52. Ritland DB (1991) Revising a classic butterfly mimicry scenario-demonstration of Mullerian mimicry between Florida viceroys (Limenitis-Archippus-Floridensis) and queens (Danaus-Gilippus-Berenice). Evolution 45(4):918–934CrossRefGoogle Scholar
  53. Roper TJ, Marples NM (1997) Odour and colour as cues for taste-avoidance learning in domestic chicks. Anim Behav 53:1241–1250CrossRefPubMedGoogle Scholar
  54. Rowe C, Guilford T (1999) The evolution of multimodal warning displays. Evol Ecol 13(7–8):655–671CrossRefGoogle Scholar
  55. Sherbrooke WC, Westphal MF (2006) Responses of greater roadrunners during attacks on sympatric venomous and nonvenomous snakes. Southwest Nat 51(1):41–47CrossRefGoogle Scholar
  56. Sherratt TN (2002) The evolution of imperfect mimicry. Behav Ecol 13(6):821–826CrossRefGoogle Scholar
  57. Socha R (1993) Pyrrhocoris apterus (Heteroptera)—an experimental model species: a review. Eur J Entomol 90(3):241–286Google Scholar
  58. Speed MP (2000) Warning signals, receiver psychology and predator memory. Anim Behav 60:269–278CrossRefPubMedGoogle Scholar
  59. Speed MP (2001) Can receiver psychology explain the evolution of aposematism? Anim Behav 61:205–216CrossRefPubMedGoogle Scholar
  60. Srygley RB (2004) The aerodynamic costs of warning signals in palatable mimetic butterflies and their distasteful models. P R Soc B-Biol Sci 271(1539):589–594CrossRefGoogle Scholar
  61. Taniguchi K, Maruyama M, Ichikawa T et al (2005) A case of Batesian mimicry between a myrmecophilous staphylinid beetle, Pella comes, and its host ant, Lasius (Dendrolasius) spathepus: an experiment using the Japanese treefrog, Hyla japonica as a real predator. Ins Soc 52(4):320–322CrossRefGoogle Scholar
  62. Thomas RJ, Marples NM, Cuthill IC et al (2003) Dietary conservatism may facilitate the initial evolution of aposematism. Oikos 101(3):458–466CrossRefGoogle Scholar
  63. Tinbergen N (1960) The natural control of insects in pine woods: Vol. I. Factors influencing the intensity of predation by songbirds. Arch Neeland Zool 13:265–343Google Scholar
  64. Turner JRG, Speed MP (1999) How weird can mimicry get? Evol Ecol 13(7–8):807–827CrossRefGoogle Scholar
  65. Wiklund C, Järvi T (1982) Survival of distasteful insects after being attacked by naive birds: reappraisal of the theory of aposematic coloration evolving through individual selection. Evolution 36:998–1002CrossRefGoogle Scholar
  66. Yamawaki Y (2000) Effects of luminance, size, and angular velocity on the recognition of nonlocomotive prey models by the praying mantis. J Ethol 18(2):85–90CrossRefGoogle Scholar
  67. Yamawaki Y (2003) Responses to worm-like-wriggling models by the praying mantis: effects of amount of motion on prey recognition. J Ethol 21(2):123–129Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  1. 1.Department of Zoology, Faculty of Biological SciencesUniversity of South BohemiaÈeské BudìjoviceCzech Republic

Personalised recommendations