Why are warning displays multimodal?

Behavioral Ecology and Sociobiology

Volumn 67, Issue 9, 2013, Pages 1425-1439

  Rowe, Candy ^a   Halpin, Christina ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Aposematism; Mimicry; Multicomponent signal; Multimodal warning display; Predator; Prey; Receiver psychology

Indexed keywords

APOSEMATISM; DATA ACQUISITION; DEFENSE BEHAVIOR; EVOLUTION; INSECT; MIMICRY; PREDATOR; PREDATOR-PREY INTERACTION; PSYCHOLOGY; SIGNAL;

HEXAPODA;

EID: 84883768537     PISSN: 03405443     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00265-013-1515-8     Document Type: Review

References (129)

1. Alatalo RV, Mappes J (1996) Tracking the evolution of warning signals. Nature 382: 708-710.
2. Alexander RD (1964) Acoustic communication in arthropods. Ann Rev Ent 12: 495-526.
3. Barber JR, Conner WE (2007) Acoustic mimicry in a predator-prey interaction. Proc Nat Acad Sci 104: 9331-9334.
4. Barnett CA (2007) The effects of energetic and physiological state on the foraging decisions of birds. Unpublished PhD thesis, Newcastle University.
5. Barnett CA, Skelhorn J, Bateson M, Rowe C (2012) Educated predators make strategic decisions to eat defended prey according to their toxin content. Behav Ecol 23: 418-424.
6. Bates HW (1862) Contributions to an insect fauna of the Amazon valley (Lepidoptera: Heliconidae). Trans Linn Soc Lond 23: 495-566.
7. Bates DL, Fenton MB (1990) Aposematism or startle? Predators learn their responses to the defenses of prey. Can J Zool 68: 49-52.
8. Bedford GO, Chinnick LJ (1966) Conspicuous displays in two species of Australian stick insects. Anim Behav 14: 518-521.
9. Bennett AD, Cuthill IC (1994) Ultraviolet vision in birds: what is its function? Vis Res 34: 1471-1478.
10. Bezzerides AL, McGraw KJ, Parker RS, Husseini J (2007) Elytra color as a signal of chemical defense in the Asian ladybird beetle Harmonia axyridis. Behav Ecol Sociobiol 61: 1401-1408.
11. Bisset GW, Frazer JFD, Rothschild M, Schachter M (1960) A pharmacologically active choline ester and other substances in the garden tiger moth Arctia caja (L.). Proc R Soc Lond B 152: 255-262.
12. Blest AD (1964) Protective display and sound production in some New World arctiid and ctenuchid moths. Zoologica 49: 161-181.
13. Blount JD, Rowland HM, Drijfhout FP, Endler JA, Inger R, Sloggett JJ, Hurst GDD, Hodgson DJ, Speed MP (2012) How the ladybird got its spots: effects of resource limitation on the honesty of aposematic signals. Funct Ecol 26: 334-342.
14. Boppré M (1986) Insect pharmacophagously utilizing defensive plant chemicals (pyrrolizidine alkaloids). Naturwissenschaften 73: 17-26.
15. Brower LP, Calvert WH (1985) Foraging dynamics of bird predators on overwintering monarch butterflies in Mexico. Evolution 39: 852-868.
16. Brower LP, Fink LS (1985) A natural toxic defense system: cardenolides in butterfly versus birds. Ann N Y Acad Sci 443: 171-188.
17. Brown SG, Boettner GH, Yack JE (2007) Clicking caterpillars: acoustic aposematism in Antheraea polyphemus and other Bombycoidea. J Exp Biol 210: 993-1005.
18. Bruum H, Slabbekoorn H (2005) Acoustic communication in noise. Adv Study Behav 35: 151-209.
19. Bura VL, Fleming AJ, Yack JE (2009) What's the buzz? Ultrasonic and sonic warning signals in caterpillars of the great peacock moth (Saturnia pyri). Naturwiss 96: 713-718.
20. Bura VL, Rohwer VG, Martin PR, Yack JE (2011) Whistling in caterpillars (Amorpha juglandis, Bombycoidea): sound-producing mechanism and function. J Exp Biol 214: 30-37.
21. Bura VL, Hnain AK, Hick JN, Yack JE (2012) Defensive sound production in the tobacco hornworm, Manduca sexta (Bombycoidea: Sphingidae). J Insect Behav 25: 114-126.
22. Candolin U (2003) The use of multiple cues in mate choice. Biol Rev 78: 559-571.
23. Carpenter GDH (1938) Audible emission of defensive froth by insects. Proc Zool Soc A 242-251.
24. Carpenter GDH, Ford EB (1933) Mimicry. Methuen, London.
25. Claridge MF (1974) Stridulation and defensive behaviour in the ground beetle, Cychrus caraboides (L.). J Entomol A 49: 7-15.
26. Cohen JA (1985) Differences and similarities in cardenolide contents of Queen and Monarch butterflies in Florida and their ecological and evolutionary implications. J Chem Ecol 11: 85-103.
27. Conner WE, Corcoran AJ (2012) Sound strategies: The 65-million-year-old battle between bats and insects. Annu Rev Entomol 57: 21-39.
28. Corcoran AJ, Barber JR, Hristov NI, Conner WE (2011) How do tiger moths jam bat sonar? J Exp Biol 214: 2416-2425.
29. Cott HB (1940) Adaptive coloration in animals. Methuen, London.
30. Cuthill IC, Stevens M, Sheppard J, Maddocks T, Parraga CA, Troscianko TS (2005) Disruptive coloration and background pattern matching. Nature 434: 72-74.
31. Darwin C (1887) The life and letters of Charles Darwin: including an autobiographical chapter, edited by his son Francis Darwin. Murray, London.
32. de Jong PW, Holloway GJ, Brakefield PM, Vos H (1991) Chemical defense in the ladybird beetles (Coccinellidae). II. Amount of reflex fluid, the alkaloid adaline and individual variation in defense in 2-spot ladybirds (Adalia bipunctata). Chemoecology 2: 15-19.
33. Dean J (1980) Encounters between bomardier beetles and two species of toads (Bufo americanus, Bufo marinus): speed pf prey capture does not determine success. J Comp Physiol 135: 41-50.
34. Dittrich W, Gilbert F, Green P, McGregor P, Grewcock D (1993) Imperfect mimicry: a pigeon's perspective. Proc R Soc Lond B 251: 195-200.
35. Dunning DC (1968) Warning sounds of moths. Z Tierpsychol 25: 129-138.
36. Edmunds M (1974) Defence in animals. Longman, Harlow.
37. Eisner T (2003) For the love of insects. Harvard University Press, Cambridge.
38. Eisner T, Grant RP (1980) Toxicity, odor aversion and "olfactory aposematism". Science 213: 416.
39. Eisner T, Aneshansley D, Eisner M, Rutowski R, Chong B, Meinivald J (1974) Chemical defense and sound production in Australian tenebrionid bettles (Adelium spp.). Psyche 81: 189-208.
40. Endler JA (1993) The color of light in forests and its implications. Ecol Monogr 63: 1-27.
41. Exnerová A, Landová E, Stys P, Fuchs R, Prokopová M, Cehláriková P (2003) Reactions of passerine birds to aposematic and non-aposematic firebugs (Pyrrhocoris apterus; Heteroptera). Biol J Lonn Soc 78: 517-525.
42. Fenton MB, Roeder KD (1974) The microtymbals of some Arctiidae. J Lepidopt Soc 28: 205-211.
43. Franchina JJ, Moon C, Peters S (1997) Effects of toxin magnitude on taste aversion and taste-potentiated aversion to visual cues in chicks (Gallus domesticus). Physiol Behav 62: 605-609.
44. Fryday SL, Greig-Smith PW (1994) The effects of social learning on the food choice of the house sparrow (Passer domesticus). Behaviour 128: 281-300.
45. Gaul AT (1952) Audio mimicry: an adjunct to colour mimicry. Psyche 59: 82-83.
46. Ghirlanda S, Enquist M (2003) A century of generalization. Anim Behav 66: 15-36.
47. Gilbert FS (2005) The evolution of imperfect mimicry. In: Fellowes MDE, Holloway GJ, Rolff J (eds) Insect evolutionary ecology. CABI, Wallingford, pp 231-288.
48. Gittleman JL, Harvey PH (1980) Why are distasteful prey not cryptic? Nature 286: 149-150.
49. Guilford T (1994) Go-slow signaling and the problem of automimicry. J Theor Biol 170: 311-316.
50. Guilford T, Dawkins MS (1991) Receiver psychology and the evolution of animal signals. Anim Behav 42: 1-14.
51. Guilford T, Rowe C (2000) Aposematism: to be red or dead. Trends Ecol Evol 15: 261-262.
52. Guilford T, Nicol C, Rothschild M, Moore BP (1987) The biological roles of pyrazines: evidence for a warning odour function. Biol J Linn Soc 31: 113-128.
53. Halpin CG, Skelhorn J, Rowe C (2008a) Being conspicuous and defended: selective benefits for the individual. Behav Ecol 19: 1012-1017.
54. Halpin CG, Skelhorn J, Rowe C (2008b) Naïve predators and selection for rare conspicuous defended prey: the initial evolution of aposematism revisited. Anim Behav 75: 771-781.
55. Halpin CG, Skelhorn J, Rowe C (2012) The relationship between sympatric defended species depends upon predators' discriminatory behaviour. PLoS One 7: e44895.
56. Haskell PT (1956) tape recording of sounds emitted by the peacock butterfly. Proc R Ent Soc C 21: 20-22.
57. Haskell PT (1961) Insect sounds. HF&G Witherby, London.
58. Hatle JD, Salazar BA, Whitman DW (2002) Survival advantage of sluggish individuals in aggregations of aposematic prey during encounters with ambush predators. Evol Ecol 16: 415-431.
59. Hauglund K, Snorre HB, Lampe H (2006) Responses of domestic chicks Gallus gallus domesticus to multimodal aposematic signals. Behav Ecol 17: 392-398.
60. Hebets EA, Papaj DR (2005) Complex signal function: developing a framework of testable hypotheses. Behav Ecol Sociobiol 57: 197-214.
61. Hill SA (2007) Sound generation in Mantis religiosa (Mantodea: Mantidae): stridulatory structures and acoustic signal. J Orthopt Res 16: 35-49.
62. Ingalls V (1993) Startle and habituation responses of blue jays (Cyanocitta cristata) in a laboratory simulation of anti-predator defenses of Catocala moths (Lepidoptera: Noctuidae). Behaviour 126: 77-96.
63. Järrvi T, Sillen-Tullberg D, Wiklund C (1981) The cost of being aposematic: an experimental study of predation on larvae of Papilio machaon by the great tit Parus major. Oikos 36: 267-272.
64. Jetz W, Rowe C, Guilford T (2001) Non-warning odors trigger innate color aversions-as long as they are novel. Behav Ecol 12: 134-139.
65. Johnstone RA (1996) Multiple displays in animal communication: "back-up signals" and "multiple messages". Phil Trans R Soc Lond B 352: 329-338.
66. Jones CG, Whitman DW, Compton SJ, Silk PJ, Blum MS (1989) Reduction in diet breadth results in sequestration of plant chemicals and increases efficacy of chemical defense in a generalist grasshopper. J Chem Ecol 15: 1811-1822.
67. Kaye H, Mackintosh NJ, Rothschild M, Moore BP (1989) Odour of pyrazine potentiates an association between environmental cues and unpalatable taste. Anim Behav 37: 563-568.
68. 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: 1049-1054.
69. Kirchner WH, Röschard J (1999) Hissing in bumblebees: an interspecific defence signal. Insect Soc 46: 239-243.
70. Laurent P, Braekman JC, Daloze D (2005) Insect chemical defence. Top Curr Chem 240: 167-229.
71. Lindström L, Alatalo RV, Mappes J, Riipi M, Vertainen L (1999) Can aposematic signals evolve by gradual change? Nature 397: 249-251.
72. Lindström L, Rowe C, Guilford T (2001) Pyrazine odour makes visually conspicuous prey aversive. Proc R Soc Lond B 268: 1-4.
73. Mackintosh NJ (1974) The psychology of animal learning. Academic, London.
74. Marples NM, Roper TJ (1996) Effects of colour and smell on the response of naive chicks towards food and water. Anim Behav 51: 1417-1424.
75. Marples NM, van Veelen W, Brakefield PM (1994) The relative importance of colour, taste and smell in the protection of an aposematic insect Coccinella septempunctata. Anim Behav 48: 967-974.
76. Mason JR, Reidinger RF (1982) Observational learning of food aversions in red-winged blackbirds (Agelaius phoeniceus). Auk 99: 548-554.
77. Masters WM (1979) Insect disturbance stridulation: its defensive role. Behav Ecol Sociobiol 5: 187-200.
78. Møller AP, Pomiankowski A (1993) Why have birds got multiple sexual ornaments? Behav Ecol Sociobiol 32: 167-176.
79. Moore BP, Brown MV, Rothschild M (1990) Methylalkylpyrazines in aposematic insects, their hostplants and their mimics. Chemoecology 1: 43-51.
80. Nickle DA, Castner JL, Smedley SR, Attygalle AB, Meinwald J, Eisner T (1996) Pyrazine emission by a tropical katydid: an example of chemical aposematism? (Orthoptera Tettigoniidae: Copiphorinae: Vestra Stål). J Orthopt Res 5: 221-223.
81. Olofsson M, Vallin A, Jakobsson S, Wiklund C (2011) Winter predation on two species of hibernating butterflies: monitoring rodent attacks with infrared cameras. Anim Behav 81: 529-534.
82. Pasteels JM, Grégoire J-C, Rowell-Rahier M (1983) The chemical ecology of defense in arthropods. Ann Rev Ent 28: 263-289.
83. Pearson DL (1989) What is the adaptive significance of multicomponent defensive repertoires? Oikos 54: 251-253.
84. Pomini AM, Machado G, Pinto-da-Rocha R, Macías-Ordóñez R, Marsaioli AJ (2010) Lines of defense in the harvestman Hoplobunus mexicanus (Arachnid: Opiliones): aposematism, stridulation, thanatosis, and irritant chemicals. Biochem Syst Ecol 38: 300-308.
85. Poulton EB (1890) The colours of animals: their meaning and use especially considered in the case of insects. Kegan Paul, Trench, Trübner and Co, London.
86. Prudic KL, Skemp AK, Papaj DR (2007) Aposematic coloration, luminance contrast and the benefits of conspicuousness. Behav Ecol 18: 41-46.
87. Raab DH (1962) Statistical facilitation of simple reaction times. Trans NY Acad Sci 24: 574-590.
88. Rashed A, Khan MI, Dawson JW, Yack JE, Sherratt TN (2009) Do hoverflies (Diptera: Syrphidae) sound like the Hymenoptera they morphologically resemble? Behav Ecol 20: 396-402.
89. Ratcliffe JM, Nydam ML (2008) Multimodal warning signals for a multiple predator world. Nature 455: 96-99.
90. Ritland DB (1994) Variation in palatability of queen butterflies (Danaus gilippus) and implications regarding mimicry. Ecology 75: 732-746.
91. Roper TJ, Cook SE (1989) Responses of chicks to brightly coloured insect prey. Behaviour 110: 276-293.
92. Roper TJ, Marples NM (1997) Odour and colour as cues for taste-avoidance learning in domestic chicks. Anim Behav 53: 1241-1250.
93. Roper TJ, Redston S (1987) Conspicuousness of distasteful prey affects the strength and durability of one-trial aversive learning. Anim Behav 35: 739-747.
94. Roth LM, Eisner T (1962) Chemical defenses of arthropods. Annu Rev Entomol 7: 107-136.
95. Rothschild M (1961) Defensive odours and Mullerian mimicry among insects. Trans R Ent Soc Lond 113: 101-121.
96. Rothschild M (1965) Proc R Ent Soc Lond C 30: 3.
97. Rothschild M, Haskell PT (1966) Stridulation of the garden tiger moth Arctia caja L. audible to the human ear. Proc R Ent Soc Lond A 41: 167-170.
98. Rothschild M, Moore BP (1987) Pyrazines as alerting signals in toxic plants and insects. In: Labeyrie V, Fabres G, Fachaise D (eds) Insect-plants. W. Junk, Dordrecht.
99. Rothschild M, Moore BP, Brown WV (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.
100. Rowe C (1998) Multicomponent signals. Unpubl. DPhil thesis, University of Oxford.
101. Rowe C (1999) Receiver psychology and the evolution of multicomponent signals. Anim Behav 58: 921-931.
102. Rowe C (2002) Sound improves visual discrimination learning in avian predators. Proc R Soc Lond B 269: 1353-1357.
103. Rowe C, Guilford T (1996) Hidden colour aversions in domestic chicks triggered by pyrazine odours of insect warning displays. Nature 383: 520-522.
104. Rowe C, Guilford T (1999) Novelty effects in a multimodal warning signal. Anim Behav 57: 341-346.
105. Rowe C, Guilford T (2000) Aposematism: to be red or dead. Trends Ecol Evol 15: 261-262.
106. Rowe C, Guilford T (2001) The evolution of multimodal warning displays. Evol Ecol 13: 655-671.
107. Rowe C, Skelhorn J (2005) Colour biases are a question of taste. Anim Behav 69: 587-594.
108. Ruxton GD, Kennedy MW (2006) Peppers and poisons: the evolutionary ecology of bad taste. J Anim Ecol 75: 1224-1226.
109. Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack: the evolutionary ecology of crypsis, warning signals and mimicry. OUP, Oxford.
110. Schilman PE, Lazzari CR, Manrique G (2001) Comparison of disturbance stridulations in five species of triatominae bugs. Acta Trop 79: 171-178.
111. Schlenoff DH (1985) The startle responses of blue jays (Cyanocitta cristata) to Catocala (Lepidoptera: Noctuidae) prey models. Anim Behav 33: 1057-1067.
112. Schuler W, 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.
113. Sen-Sarma M, Fuchs S, Werber C, Tautz J (2002) Worker piping triggers hissing for coordinated colony defence in the dwarf honeybee Apis florae. Zoology 105: 215-223.
114. Sherratt TN, Speed MP, Ruxton GD (2004) Natural selection on unpalatable species imposed by state-dependent foraging behaviour. J Theor Biol 228: 217-226.
115. Siddall EC, Marples NM (2008) Better to be bimodal: the interaction of color and odor on learning and memory. Behav Ecol 19: 425-432.
116. Siddall EC, Marples NM (2011a) The effect of pyrazine odor on avoidance learning and memory in wild robins Erithacus rubecula. Curr Zool 57: 208-214.
117. Siddall EC, Marples NM (2011b) Hear no evil: the effect of auditory warning signals on avian innate avoidance, learned avoidance and memory. Curr Zool 57: 197-207.
118. Skelhorn J (2011) Colour biases are a question of conspecifics' taste. Anim Behav 81: 825-829.
119. Skelhorn J, Rowe C (2006) Avian predators taste-reject aposematic prey on their level of chemical defence. Biol Lett 2: 348-350.
120. Skelhorn J, Rowe C (2007) Predators' toxin burdens influence their strategic decisions to eat toxic prey. Curr Biol 17: 1479-1483.
121. Skelhorn J, Rowe C (2009) Distastefulness as an antipredator defence strategy. Anim Behav 78: 761-766.
122. Skelhorn J, Rowe C (2010) Birds learn to use distastefulness as a signal of toxicity. Proc R Soc Lond B 277: 1729-1734.
123. Skelhorn J, Griksaitis D, Rowe C (2008) Colour biases are more than a question of taste. Anim Behav 75: 827-835.
124. Smith SM (1975) Innate recognition of coral snake pattern by a possible avian predator. Science 187: 759-760.
125. Speed MP, Alderson NJ, Hardman C, Ruxton GD (2000) Testing Müllerian mimicry: an experiment with wild birds. Proc R Soc Lond B 267: 725-731.
126. Srygley RB (2004) The aerodynamic costs of warning signals in palatable mimetic butterflies and their distasteful models. Proc R Soc Lond B 271: 589-594.
127. Vallin A, Jakobsson S, Lind J, Wiklund C (2005) Prey survival by predator intimidation: an experimental study of peacock butterfly defense against blue tits. Proc R Soc Lond B 272: 1203-1207.
128. Wallace AR (1867) Journal of Proceeding of the Entomological Society of London meeting March 4th, 5: lxxx-lxxxi, In Transactions of the Entomological Society of London 3rd series, vol III, London 1864-1869.
129. Wheeler JW, Chung RH, Oh SK, Benfield EF, Neef SE (1970) Defensive secretions of cychrine beetles (Coleoptera: Carabidae). Ann Ent Soc Am 63: 469-471.