Evolutionary Ecology

, Volume 30, Issue 5, pp 797–809

The ecology of multiple colour defences

Ideas & Perspectives

Abstract

Individuals of many species are considered to rely on a single type of external appearance to escape predation but there are many notable exceptions. To develop an ecological framework to explain why some individuals employ different colour patterns as part of their defensive repertoire, we collate examples of colour change that are associated with living in different environments and microhabitats, examples of age-related colour change, colour defences tailored to different predators, and startle displays, where hidden conspicuous colour patterns are suddenly revealed. The over-arching commonality to all these examples is that the use of more than one defense-related external appearance is associated with a spatial or temporal change in predation risk. For example, coarse scale temporal changes in an animal’s background frequently select for gradual colour changes, while fine-scale spatial heterogeneity selects for more rapid colour changes and we provide a graphical framework for this. Irrespective of the mechanisms underlying colour change, using more than one colour defence appears driven by variation in predation risk rather than by idiosyncratic abilities to alter external appearances as is commonly believed, although physiological and energetic factors will play some role.

Keywords

Aposematism Ontogenetic colour change Conspicuousness Crypsis Deimatic displays Predation pressure 

References

  1. Allen WL, Baddeley R, Scott-Samuel NE, Cuthill IC (2013) The evolution and function of pattern diversity in snakes. Behav Ecol 24:1237–1250CrossRefGoogle Scholar
  2. Bagnara JT, Hadley ME (1973) Chromatophores and color change: the comparative physiology of animal pigmentation. Prentice-Hall Inc., Englewood CliffsGoogle Scholar
  3. Barnet JB, Cuthill IC (2015) Distance-dependent defensive coloration. Curr Biol 24:R1157–R1158CrossRefGoogle Scholar
  4. Bedini R (2002) Colour change and mimicry from juvenile to adult: Xantho poressa (Olivi, 1792) (Brachyura, Xanthidae) and Carcinus maenas (Linnaeus, 1758) (Brachyura, Portunidae). Crusteana Int J Crustacean Res 75:703–710Google Scholar
  5. Bond AB, Kamil AC (2002) Visual predators select for crypticity and polymorphism in virtual prey. Nature 415:609–613CrossRefPubMedGoogle Scholar
  6. Bond AB, Kamil AC (2006) Spatial heterogeneity, predator cognition, and the evolution of color polymorphism in virtual prey. PNAS 103:3214–3219CrossRefPubMedPubMedCentralGoogle Scholar
  7. Booth CL (1990) Evolutionary significance of ontogenetic colour change in animals. Biol J Linn Soc 40:125–163CrossRefGoogle Scholar
  8. Briffa M, Twyman C (2011) Do I stand out or blend in? Conspicuousness awareness and consistent behavioural differences in hermit crabs. Biol Lett 7:330–332CrossRefPubMedGoogle Scholar
  9. Carlberg U (1981) Defensive behaviour in females of the stick insect Sipyloidea sipylus (Westwood) (Phasmida). Zool Anz Jena 207:177–180Google Scholar
  10. Caro T (2005) Antipredator defenses in birds and mammals. University of Chicago Press, ChicagoGoogle Scholar
  11. Caro T, Graham CM, Stoner CJ, Vargas J (2004) Adaptive significance of antipredator behaviour in artiodactyls. Anim Behav 67:205–228CrossRefGoogle Scholar
  12. Caro T, Stankowich T, Mesnick SL, Costa DP, Beeman K (2012) Pelage coloration in pinnipeds: functional considerations. Behav Ecol 23:765–774CrossRefGoogle Scholar
  13. Caro T, Stankowich T, Kiffner C, Hunter J (2013) Are spotted skunks conspicuous or cryptic? Ethol Ecol Evol 25:144–160CrossRefGoogle Scholar
  14. Chassard C (1956) Polymorphisme des populations d’Hippolyte varians Leach et comportement en function de leur adaptation chromatique presente. Bull Soc Zool Fr 81:413–418Google Scholar
  15. Clark DJ, Roberts JA, Rector M, Uetz GW (2011) Spectral reflectance and communication in the wolf spider, Schizocosa ocreata (Hentz): simultaneous crypsis and background contrast visual signals. Behav Ecol Sociobiol 65:1237–1247CrossRefGoogle Scholar
  16. Cooper WE, Vitt LJ (1985) Blue tails and autonomy—enhancement of predation avoidance in juvenile skinks. Z Tierpsychol 70:265–276CrossRefGoogle Scholar
  17. Cott HB (1940) Adaptive coloration in animals. Methuen & Co. Ltd, LondonGoogle Scholar
  18. Cummings ME, Jordao JM, Cronin TW, Oliveira RF (2008) Visual ecology of the fiddler crab, Uca tangeri: effects of sex, viewer and background on conspicuousness. Anim Behav 75:175–188CrossRefGoogle Scholar
  19. Dafni J, Diament A (1984) School-oriented mimicry: a new type of mimicry in fishes. Mar Ecol Prog Ser 20:45–50CrossRefGoogle Scholar
  20. Delhey K, Burger C, Fiedler W, Peters A (2010) Seasonal changes in colour: a comparison of structural, melanin- and carotenoid-based plumage colours. PLoS ONE 5(7):e11582CrossRefPubMedPubMedCentralGoogle Scholar
  21. Edmunds M (1974) Defence in animals: a survey of anti-predator defences. Longman, HarlowGoogle Scholar
  22. Endler JA (1978) A predator’s view of animal color patterns. Evol Biol 11:319–364CrossRefGoogle Scholar
  23. Endler JA (1991) Interactions between predators and prey. In: Krebs JR, Davies NB (eds) Behavioral ecology. Blackwell, Oxford, pp 169–196Google Scholar
  24. Endler J (1992) Signals, signal condition, and the direction of evolution. Am Nat 139:125–153CrossRefGoogle Scholar
  25. Forsman A, Karlsson M, Wennersten L, Johansson J, Karpestam E (2011) Rapid evolution of fire melanism in replicated populations of pygmy grasshoppers. Evolution 65:2530–2540CrossRefPubMedGoogle Scholar
  26. Gamble FW, Keeble FW (1900) Hippolyte varians: a study in color- change. J Cell Sci S2–43:589–698Google Scholar
  27. Gillespie J (1974) The role of environmental grain in the maintenance of genetic variation. Am Nat 108:831–836CrossRefGoogle Scholar
  28. Grant JB (2007) Ontogenetic colour change and the evolution of aposematism: a case study in panic moth caterpillars. J Anim Ecol 76:439–447CrossRefPubMedGoogle Scholar
  29. Hanlon RT, Conroy L-A, Forsythe JW (2008) Mimicry and foraging behaviour of two tropical sand-flat octopus species off North Sulawesi, Indonesia. Biol J Linn Soc 93:23–38CrossRefGoogle Scholar
  30. Hanlon RT, Chiao C-C, Mathger LM, Barbosa A, Buresch KC, Chubb C (2009) Cephalopod dynamic camouflage: bridging the continuum between background matching and disruptive coloration. Philos Trans R Soc B 264:429–437CrossRefGoogle Scholar
  31. Hawlena D, Boochnik R, Abramsky Z, Bouskila A (2006) Blue tail and striped body: why do lizards change their infant costume when growing up? Behav Ecol 17:889–896CrossRefGoogle Scholar
  32. Higginson AD, Ruxton GD (2010) Optimal defensive coloration strategies during the growth period of prey. Evolution 64:53–67CrossRefPubMedGoogle Scholar
  33. Hochkirch A, Deppermann J, Groning J (2008) Phenotypic plasticity in insects: the effects of substrate color on the coloration of two ground-hopper species. Evol Dev 10:350–359CrossRefPubMedGoogle Scholar
  34. Honma A, Mappes J, Valkonen JJ (2015) Warning coloration can be disruptive: aposematic marginal wing patterning in the wood toger moth. Ecol Evol 5:4863–4874CrossRefPubMedPubMedCentralGoogle Scholar
  35. Hossie TJ, Sherratt TN (2014) Does defensive posture increase mimetic fidelity of caterpillars with eyespots to their putative snake models? Curr Zool 60:76–89CrossRefGoogle Scholar
  36. Hossie TJ, Skelhorn J, Breinholt JW, Kawahara AY, Sherratt TN (2015) Body size affects the evolution of eyespots in caterpillars. Proc Nat Acad Sci 112:6664–6669CrossRefPubMedPubMedCentralGoogle Scholar
  37. Huey RB, Pianka ER (1977) Natural selection for juvenile lizards mimicking noxious beetles. Science 195:201–203CrossRefPubMedGoogle Scholar
  38. Hultgren KM, Stachowicz JJ (2009) Evolution of decoration in majoid crabs: a comparative phylogenetic analysis of the role of body size and alternative defensive strategies. Am Nat 173:566–578CrossRefPubMedGoogle Scholar
  39. 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 126:77–95CrossRefGoogle Scholar
  40. Jackson JF, Drummond BA III (1974) A batesian ant-mimicry complex from the mountain pine ridge of British Honduras, with an example of transformational mimicry. Am Midl Nat 91:248–251CrossRefGoogle Scholar
  41. Kang C-K, Moon J-Y, Lee S-I, Jablonski PG (2013) Cryptically patterned moths perceive bark structure when choosing body orientations that match wing color pattern to the bark pattern. PLoS ONE 8:e78117CrossRefPubMedPubMedCentralGoogle Scholar
  42. Kettlewell HBD (1955) Recognition of appropriate backgrounds by the pale and black phases of Lepidoptera. Nature 175:943–944CrossRefPubMedGoogle Scholar
  43. Kilner RM (2006) Function and evolution of color in young birds. In: Hill GE, McGraw KJ (eds) Bird coloration: function and evolution. Harvard University Press, Cambridge, pp 201–232Google Scholar
  44. Kjernsmo K, Merilaita S (2013) Eyespots divert attacks by fish. Proc R Soc Lond B 280:20131458CrossRefGoogle Scholar
  45. Landridge KV, Broom M, Osorio D (2007) Selective signalling by cuttlefish to predators. Curr Biol 17:R1044–R1045CrossRefGoogle Scholar
  46. Lee WL (1966) Color change and the ecology of the marine isopod Idothea (Pentidothea) montereyensis Maloney, 1933. Ecology 47:930–941CrossRefGoogle Scholar
  47. Levins R (1968) Evolution in changing environments: some theoretical explorations, vol 2. Princeton University Press, PrincetonGoogle Scholar
  48. Londoño GA, García DA, Martínez MAS (2015) Morphological and behavioral evidence of Batesian mimicry in nestlings of a lowland Amazonian bird. Am Nat 185:135–141CrossRefPubMedGoogle Scholar
  49. Mänd T, Tammaru T, Mappes J (2007) Size dependent predation risk in cryptic and conspicuous insects. Evol Ecol 21:485–498CrossRefGoogle Scholar
  50. Mappes J, Marples N, Endler JA (2005) The complex business of survival by aposematism. Trends Ecol Evol 20:598–603CrossRefPubMedGoogle Scholar
  51. Marshall NJ (2000) Communication and camouflage with the same ‘bright’ colours in reef fishes. Phil Trans R Soc Lond B 355:1243–1248CrossRefGoogle Scholar
  52. Marshall KLA, Stevens M (2014) Wall lizards display conspicuous signals to conspecifics and reduce detection by avian predators. Behav Ecol 25:1325–1337CrossRefPubMedPubMedCentralGoogle Scholar
  53. Mäthger LM, Chiao CC, Barbosa A, Hanlon RT (2008) Color matching on natural substrates in cuttlefish, Sepia officinalis. J Comp Physiol A 194:577–585CrossRefGoogle Scholar
  54. Merilaita S, Tullberg BS (2005) Constrained camouflage facilitates the evolution of conspicuous warning coloration. Evolution 59:38–45CrossRefPubMedGoogle Scholar
  55. Montgomerie R, Lyon B, Holder K (2001) Dirty ptarmigan: behavioral modification of conspicuous male plumage. Behav Ecol 12:429–438CrossRefGoogle Scholar
  56. Nachman MW, Hoekstra HE, D’Agostino SL (2003) The genetic basis of adaptive melanism in pocket mice. PNAS 100:5268–5273CrossRefPubMedPubMedCentralGoogle Scholar
  57. Niskanen M, Mappes J (2005) Significance of the dorsal zig-zag pattern of Vipera latastei graditana against avian predators. J Anim Ecol 74:1091–1101CrossRefGoogle Scholar
  58. Nosil P, Crespi BJ (2006) Experimental evidence that predation promotes divergence in adaptive radiation. PNAS 103:9090–9095CrossRefPubMedPubMedCentralGoogle Scholar
  59. Olofsson M, Eriksson S, Jakobsson S, Wiklund C (2012) Deimatic display in the European swallowtail butterfly as a secondary defence against attacks from great tits. PLoS ONE 7:e47092CrossRefPubMedPubMedCentralGoogle Scholar
  60. Oxford GS, Gillespie RG (1998) Evolution and ecology of spider coloration. Ann Rev Entomol 43:619–643CrossRefGoogle Scholar
  61. Penney HD, Hassall C, Skevington JH, Abbott KR, Sherratt TN (2012) A comparative analysis of the evolution of imperfect mimicry. Nature 483:461–464CrossRefPubMedGoogle Scholar
  62. Poulton EB (1885) The essential nature of the colouring of phytophagous larvae (and their pupae); with an account of some experiments upon the relation between the colour of such larvae and that of their food-plants. Proc R Soc B 237:269–315Google Scholar
  63. Powell BL (1962) The responses of the chromatophores of Carcinus maenas (L. 1758) to light and temperature. Crustaceana 4:93–102CrossRefGoogle Scholar
  64. Prudic KL, Oliver JC, Sperling FAH (2007) The signal environment is more important than diet or chemical specialization in the evolution of warning coloration. Proc Nat Acad Sci 104:19381–19386CrossRefPubMedPubMedCentralGoogle Scholar
  65. Rundus AS, Owings DH, Joshi SS, Chinn E, Giannini N (2007) Ground squirrels use an infrared signal to deter rattlesnake predation. Proc Nat Acad Sci USA 104:14372–14376CrossRefPubMedPubMedCentralGoogle Scholar
  66. Ruxton GD, Speed MP, Kelly DJ (2004) What, if anything, is the adaptive function of countershading? Anim Behav 68:445–451CrossRefGoogle Scholar
  67. Simpson SJ, Sword GA, Lo N (2011) Polyphenism in insects. Curr Biol 21:R738–R749CrossRefPubMedGoogle Scholar
  68. Stevens M (2005) The role of eyespots as anti-predator mechanisms, principally demonstrated in the Lepidoptera. Biol Rev 80:573–588CrossRefPubMedGoogle Scholar
  69. Stevens M (2007) Predator perception and the interrelation between different forms of protective coloration. Proc R Soc B 274:1457–1464CrossRefPubMedPubMedCentralGoogle Scholar
  70. Stevens M (2013) Sensory ecology, behaviour, and evolution. Oxford University Press, OxfordCrossRefGoogle Scholar
  71. Stevens M (2016) Color change, phenotypic plasticity, and camouflage. Front Ecol Evol 4:51CrossRefGoogle Scholar
  72. Stevens M, Ruxton GD (2012) Linking the evolution and form of warning coloration in nature. Proc R Soc Lond B 279:417–426CrossRefGoogle Scholar
  73. Stevens M, Yule DH, Ruxton GD (2008) Dazzle coloration and prey movement. Proc R Soc B 275:2639–2643CrossRefPubMedPubMedCentralGoogle Scholar
  74. Stevens M, Rong CP, Todd PA (2013) Colour change and camouflage in the horned ghost crab Ocypode ceratophthalmus. Biol J Linn Soc 109:257–270CrossRefGoogle Scholar
  75. Stevens M, Lown AE, Denton AM (2014a) Rockpool gobies change colour for camouflage. PLoS ONE 9:e110325CrossRefPubMedPubMedCentralGoogle Scholar
  76. Stevens M, Wood LE, Lown AE (2014b) Camouflage and individual variation in shore crabs (Carcinus maenas) from different habitats. PLoS ONE 9:e115586CrossRefPubMedPubMedCentralGoogle Scholar
  77. Stoner CJ, Caro T, Graham CM (2003) Ecological and behavioral correlates of coloration in artiodactyls: systematic attempts to verify conventional hypotheses. Behav Ecol 14:823–840CrossRefGoogle Scholar
  78. Stuart-Fox D, Moussalli A (2009) Camouflage, communication and thermoregulation: lessons from colour changing organisms. Philos Trans R Soc Lond B 364:463–470CrossRefGoogle Scholar
  79. Stuart-Fox D, Whiting MJ, Moussalli A (2006) Camouflage and colour change: antipredator responses to bird and snake predators across multiple populations in a dwarf chameleon. Biol J Linn Soc 88:437–446CrossRefGoogle Scholar
  80. Todd PA, Qui W, Chong KY (2009) Ontogenetic shifts in carapace patterning and/or colouration in intertidal and subtidal brachyuran crabs. Raffles Bull Zool 57:543–550Google Scholar
  81. Tullberg BS, Merilaita S, Wiklund C (2005) Aposematism and crypsis combined as a result of distance dependence: functional versality of the colour pattern in the swallowtail butterfly larva. Proc R Soc B 272:1315–1321CrossRefPubMedPubMedCentralGoogle Scholar
  82. Tullberg BS, Gamberale-Stille G, Bohlin T, Merilaita S (2008) Seasonal ontogenetic colour plasticity in the adult striated shieldbug Graphosoma lineatum (Heteroptera) and its effect on detectability. Behav Ecol Sociobiol 62:1389–1396CrossRefGoogle Scholar
  83. Umbers KDL, Fabricant SA, Gawryszewski FM, Seago AE, Herberstein ME (2014) Reversible colour change in arthropoda. Biol Rev 89:820–848CrossRefPubMedGoogle Scholar
  84. Umbers KDL, Lehtonen J, Mappes J (2015) Deimatic displays. Curr Biol 25:R58–R59CrossRefPubMedGoogle Scholar
  85. Valkonen JK, Nokelainen O, Jokimaki M, Kuusinen E, Paloranta M, Peura M, Mappes J (2014) From deception to frankness: benefits of ontogenetic shift in the anti-predator strategy of alder moth Acronicta alni larvae. Curr Zool 60:114–122CrossRefGoogle Scholar
  86. Vallin A, Jakobsson S, Lind J, Wiklund C (2005) Prey survival by predator intimidation: an experimental study of peacock butterfly defence against blue tits. Proc R Soc Lond B 272:1203–1207CrossRefGoogle Scholar
  87. Wallace AR (1867) Mimicry and other protective resemblances among animals. Westminster Review, London, pp 1–43Google Scholar
  88. Wallace AR (1877) The colours of animals and plants. Part I. Am Nat 11(11):384–406CrossRefGoogle Scholar
  89. Webster RJ, Callahan A, Godin J-GJ, Sherratt TN (2009) Behaviourally mediated crypsis in two nocturnal moths with contrasting appearance. Philos Trans R Soc B 364:503–510CrossRefGoogle Scholar
  90. Williams DD, Tavares AF, Bryant E (1987) Respiratory device or camouflage?: A case for the caddisfly. Oikos 50:42–52CrossRefGoogle Scholar
  91. Young RE, Roper CF (1976) Bioluminescent countershading in midwater animals: evidence from living squid. Science 191:1046–1048CrossRefPubMedGoogle Scholar
  92. Zimova M, Mills LS, Lukacs PM, Mitchell MS (2014) Snowshoe hares display limited phenotypic plasticity to mismatch in seasonal camouflage. Proc R Soc B 281:20140029CrossRefPubMedPubMedCentralGoogle Scholar
  93. Zylinski S, Johnsen S (2011) Mesopelagic cephalopods switch between transparency and pigmentation to optimize camouflage in the deep. Curr Biol 21:1937–1941CrossRefPubMedGoogle Scholar
  94. Zylinski S, Osorio D, Johnsen S (2016) Cuttlefish see shape from shading, fine-tuning coloration in response to pictorial depth cues and directional illumination. Proc R Soc B 283:20160062CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Wildlife, Fish and Conservation Biology, and Center for Population BiologyUniversity of CaliforniaDavisUSA
  2. 2.Wissenschaftskolleg zu BerlinBerlinGermany
  3. 3.Department of BiologyCarleton UniversityOttawaCanada
  4. 4.Centre for Ecology and Conservation, College of Life and Environmental SciencesUniversity of ExeterPenrynUK

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