What constitutes optical warning signals of ladybirds (Coleoptera: Coccinellidae) towards bird predators: Colour, pattern or general look?

Biological Journal of the Linnean Society

Volumn 98, Issue 1, 2009, Pages 234-242

  DolenskÁ, Michaela ^a   NedvĚd, OldŘich ^a   VeselÝ, Petr ^a   TesaŘovÁ, Monika ^a   Fuchs, Roman ^a  

^a UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

Author keywords

Body shape; Chemical signal; Prey recognition; Warning coloration

Indexed keywords

BEETLE; DEFENSE BEHAVIOR; INNATE BEHAVIOR; PREDATOR-PREY INTERACTION; PREY LOCATION; SIGNALING; SPECIES DIVERSITY;

AVES; COCCINELLA SEPTEMPUNCTATA; COCCINELLIDAE; COLEOPTERA; EXOCHOMUS QUADRIPUSTULATUS; PARUS MAJOR; SCYMNUS FRONTALIS;

EID: 69449096797     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2009.01277.x     Document Type: Article

References (60)

1. Agarwala BK, Dixon AFG. 1992. Laboratory study of cannibalism and interspecific predation in ladybirds. Ecological Entomology 17 : 303 309.
2. Camarano S, Gonzalez A, Rossini C. 2006. Chemical defense of the ladybird beetle Epilachna paenulata. Chemoecology 16 : 179 184.
3. Coppinger RP. 1969. The effect of experience and novelty on avian feeding behavior with refference to the evolution of warning coloration in butterflies. I. Reactions of wild-caught adult Blue jays to novel insects. Behaviour 35 : 45 60.
4. Cott HB. 1940. Adaptive coloration in animals. London : Methuen.
5. Cramp S, Perrins CM. 1993. Handbook of the birds of Europe, The Middle East, and North Africa, Vol. VII. Oxford : Oxford University Press.
6. Cuthill IC, Stevens M, Windsor AMM, Walker HJ. 2006. The effects of pattern symmetry on detection of disruptive and background-matching coloration. Behavioral Ecology 17 : 828 832.
7. Edmunds M. 1974. Defence in animals. A survey in antipredator defences. Harlow : Longman.
8. Endler JA. 1978. A predator's view of animal color patterns. Evolutionary Biology 11 : 319 364.
9. Endler JA, Mielke PW. 2005. Comparing entire colour patterns as birds see them. Biological Journal of the Linnean Society 86 : 405 431.
10. Evans DL, Schmidt JO. 1990. Insect defences. Adaptive mechanisms and strategies of prey and predators. New York, NY : State University of New York Press.
11. Exnerová A, Landová E, Štys P, Fuchs R, Prokopová M, Cehláriková P. 2003. Reactions of passerine birds to aposematic and nonaposematic firebugs (Pyrrhocoris apterus; Heteroptera). Biological Journal of the Linnean Society 78 : 517 525.
12. Exnerová A, Svádová K, Štys P, Barcalová S, Landová E, Prokopová M, Fuchs R, Socha R. 2006. Importance of colour in the reaction of passerine predators to aposematic prey: experiments with mutants of Pyrrhocoris apterus (Heteroptera). Biological Journal of the Linnean Society 88 : 143 153.
13. Exnerová A, Štys P, Fučíková E, Veselá S, Svádová K, Prokopová M, Jarošík V, Fuchs R, Landová E. 2007. Avoidance of aposematic prey in European tits (Paridae): learned or innate? Behavioral Ecology 18 : 148 156.
14. Forsman A, Herrström J. 2004. Asymmetry in size, shape, and color impairs the protective value of conspicuous color patterns. Behavioral Ecology 15 : 141 147.
15. Forsman A, Merilaita S. 1999. Fearful symmetry: pattern size and asymmetry affects aposematic signal efficacy. Evolutionary Ecology 13 : 131 140.
16. Forsman A, Merilaita S. 2003. Fearful symmetry? Intra-individual comparisons of asymmetry in cryptic vs. signalling colour patterns in butterflies. Evolutionary Ecology 17 : 491 507.
17. Gittleman JL, Harvey PH, Greenwood PL. 1980. The evolution of conspicuous coloration: some experiments in bad taste. Animal Behaviour 28 : 897 899.
18. Guilford T. 1986. How do warning colors work - conspicuousness may reduce recognition errors in experienced predators. Animal Behaviour 34 : 286 288.
19. Guilford T. 1988. The evolution of conspicuous coloration. The American Naturalist 131 : 7 21.
20. Guilford T. 1990. The evolution of aposematism. In : Evans DL, Schmidt JO, eds. Insect defences. Adaptive mechanisms and strategies of prey and predators. Albany, NY : State University of New York Press, 23 62.
21. Guilford T, Nicol C, Rothschild M, Moore BP. 1987. The biological roles of pyrazines - evidence for a warning odor function. Biological Journal of the Linnean Society 31 : 113 128.
22. Hagen SB, Leinaas HP, Lampe HM. 2003. Responses of great tits Parus major to small tortoiseshells Aglais urticae in feeding trials; evidence of aposematism. Ecological Entomology 28 : 503 509.
23. Ham AD, Ihalainen E, Lindström L, Mappes J. 2006. Does colour matter? The importance of colour in avoidance learning, memorability and generalisation. Behavioral Ecology and Sociobiology 60 : 482 491.
24. Harvey PH, Paxton RJ. 1981. The evolution of aposematic coloration. Oikos 37 : 391 393.
25. Holloway GJ, Brakefield PM, Dejong PW, Ottenheim MM, Devos H, Kesbeke F, Peynenburg L. 1995. A quantitative genetic-analysis of an aposematic color pattern and its ecological implications. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences 348 : 373 379.
26. Honěk A, Martínková Z, Pekar S. 2005. Temporal stability of morph frequency in central European populations of Adalia bipunctata and A. decempunctata (Coleoptera: Coccinellidae). European Journal of Entomology 102 : 437 442.
27. HoughGoldstein J, Cox J, Armstrong A. 1996. Podisus maculiventris (Hemiptera: Pentatomidae) predation on ladybird beetles (Coleoptera: Coccinellidae). Florida Entomologist 79 : 64 68.
28. Ito F, Hashim R, Huei YS, Kaufmann E, Akino T, Billen J. 2004. Spectacular Batesian mimicry in ants. Naturwissenschaften 91 : 481 484.
29. Karlsson R, Losman D. 1972. The crystal structure of the hemihydrochloride of coccinellin, the defensive N-oxide alkaloid of the beetle Coccinella septempunctata, a case of symmetrical hydrogen bonding. Journal of the Chemical Society - Chemical Communications 11 : 626 627.
30. Kauppinen J, Mappes J. 2003. Why are wasps so intimidating: field experiments on hunting dragonflies (Odonata: Aeshna grandis). Animal Behaviour 66 : 505 511.
31. Kholin SK. 1990. Stability of the genetic-polymorphism in color of Harmonia axyridis Pall. (Coccinellidae, Coleoptera) in maritime province, USSR. Genetika 26 : 2207 2214.
32. Komárek S. 2003. Mimicry, aposematism and related phenomena: mimetism in nature and the history of its study. München : Lincom.
33. Laurent P, Braekman JC, Daloze S. 2005. Insect chemical defense. Chemistry of Pheromones and other Semiochemicals II : 167 229.
34. Lindström L. 1999. Experimental approaches to studying the initial evolution of conspicuous aposematic signalling. Evolutionary Ecology 13 : 605 618.
35. Lucas E. 2005. Intraguild predation among aphidophagous predators. European Journal of Entomology 102 : 351 363.
36. Lyytinen A, Alatalo RV, Lindström L, Mappes J. 1999. Are European white butterflies aposematic? Evolutionary Ecology 13 : 709 719.
37. Majerus MEN. 1994. Ladybirds. London : HarperCollins Publishers.
38. Marples N. 1993. Toxicity assays of ladybirds using natural predators. Chemoecology 4 : 33 38.
39. Marples NM, Kelly DJ. 1999. Neophobia and dietary conservatism: two distinct processes? Evolutionary Ecology 13 : 641 653.
40. Marples NM, Brakefield PM, Cowie RJ. 1989. Differences between the 7-spot and 2-spot ladybird beetles (Coccinellidae) in their toxic effects on a bird predator. Ecological Entomology 14 : 79 84.
41. Marples NM, van Veelen W, Brakefield PM. 1994. The relative importance of color, taste and smell in the protection of an aposematic insect Coccinella-Septempunctata. Animal Behaviour 48 : 967 974.
42. Nelson XJ, Jackson RR, Li D, Barrion AT, Edwards GB. 2006. Innate aversion to ants (Hymenoptera: Formicidae) and ant mimics: experimental findings from mantises (Mantodea). Biological Journal of the Linnean Society 88 : 23 32.
43. Niskanen M, Mappes J. 2005. Significance of the dorsal zigzag pattern of Vipera latastei gaditana against avian predators. Journal of Animal Ecology 74 : 1091 1101.
44. Osorio D, Miklosi A, Gonda Z. 1999. Visual ecology and perception of coloration patterns by domestic chicks. Evolutionary Ecology 13 : 673 689.
45. Pasteels JM. 2007. Chemical defence, offence and alliance in ants-aphids-ladybirds relationships. Population Ecology 49 : 5 14.
46. Roper TJ, Marples NM. 1997. Colour preferences of domestic chicks in relation to food and water presentation. Applied Animal Behaviour Science 54 : 207 213.
47. Rothschild M, Moore B. 1987. Pyrazines as alerting signals in toxic plants and insects. In : Labeyrie V, Fabres G, Lachaise D, eds. Insects-Plants. Dordrecht : Dr W. Junk, 97 101.
48. Schuler W, Hesse E. 1985. On the function of warning coloration: a black and yellow pattern inhibits prey-attack by naive domestic chicks. Behavioral Ecology and Sociobiology 16 : 249 255.
49. Schuler W, Roper TJ. 1992. Responses to warning coloration in avian predators. Advances in the Study of Behavior 21 : 111 146.
50. Shettleworth SJ. 1998. Cognition, evolution and behavior. New York, NY : Oxford University Press.
51. Sillén-Tullberg B. 1985. The significance of coloration per se, independent background, for predator avoidance of aposematic prey. Animal Behaviour 33 : 1382 1384.
52. Sillén-Tullberg B, Wiklund C, Järvi T. 1982. Aposematic coloration in adults and larvae of Lygaeus-Equestris and its bearing on mullerian mimicry - an experimental-study on predation on living bugs by the great tit Parus-Major. Oikos 39 : 131 136.
53. Sloggett JJ, Wood RA, Majerus MEN. 1998. Adaptations of Coccinella magnifica Redtenbacher, a myrmecophilous coccinellid, to aggression by wood ants (Formica rufa group). I. Adult behavioral adaptation, its ecological context and evolution. Journal of Insect Behavior 11 : 889 904.
54. Smith SM. 1980. Responses of naive temperate birds to warning coloration. The American Midland Naturalist 103 : 346 352.
55. Speed MP. 2001. Can receiver psychology explain the evolution of aposematism? Animal Behaviour 61 : 205 216.
56. Timmermans M, Braekman JC, Daloze D, Pasteels JM, Merlin J, Declercq JP. 1992. Exochomine, a dimeric alkaloid, isolated from Exochomus quadripustulatus (Coleoptera: Coccinellidae). Tetrahedron Letters 33 : 1281 1284.
57. Tursch B, Daloze D, Dupont M, Pasteels JM, Tricot MC. 1971. A defense alkaloid in a carnivorous beetle. Experientia 27 : 1380.
58. Veselý P, Veselá S, Fuchs R, Zrzavý J. 2006. Are gregarious red-black shieldbugs, Graphosoma lineatum (Hemiptera: Pentatomidae), really aposematic? An experimental approach. Evolutionary Ecology Research 8 : 881 890.
59. Wang SF, Braekman JC, Daloze D, Pasteels JM, Soetens P, Handjieva NV, Kalushkov P. 1996. Nα-quinaldyl-L-arginine·HCl, a new defensive alkaloid from Subcoccinella-24-punctata (Coleoptera, Coccinellidae). Experientia 52 : 628 630.
60. Wuster W, Allum CSE, Bjargardottir IB, Bailey KL, Dawson KJ, Guenioui J, Lewis J, McGurk J, Moore AG, Niskanen M, Pollard CP. 2004. Do aposematism and Batesian mimicry require bright colours? A test, using European viper markings. Proceedings of the Royal Society of London Series B, Biological Sciences 271 : 2495 2499.