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The ecology of multiple colour defences

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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.

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References

  • Allen WL, Baddeley R, Scott-Samuel NE, Cuthill IC (2013) The evolution and function of pattern diversity in snakes. Behav Ecol 24:1237–1250

    Article  Google Scholar 

  • Bagnara JT, Hadley ME (1973) Chromatophores and color change: the comparative physiology of animal pigmentation. Prentice-Hall Inc., Englewood Cliffs

    Google Scholar 

  • Barnet JB, Cuthill IC (2015) Distance-dependent defensive coloration. Curr Biol 24:R1157–R1158

    Article  Google Scholar 

  • 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 75:703–710

    Google Scholar 

  • Bond AB, Kamil AC (2002) Visual predators select for crypticity and polymorphism in virtual prey. Nature 415:609–613

    Article  CAS  PubMed  Google Scholar 

  • Bond AB, Kamil AC (2006) Spatial heterogeneity, predator cognition, and the evolution of color polymorphism in virtual prey. PNAS 103:3214–3219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Booth CL (1990) Evolutionary significance of ontogenetic colour change in animals. Biol J Linn Soc 40:125–163

    Article  Google Scholar 

  • Briffa M, Twyman C (2011) Do I stand out or blend in? Conspicuousness awareness and consistent behavioural differences in hermit crabs. Biol Lett 7:330–332

    Article  PubMed  Google Scholar 

  • Carlberg U (1981) Defensive behaviour in females of the stick insect Sipyloidea sipylus (Westwood) (Phasmida). Zool Anz Jena 207:177–180

    Google Scholar 

  • Caro T (2005) Antipredator defenses in birds and mammals. University of Chicago Press, Chicago

    Google Scholar 

  • Caro T, Graham CM, Stoner CJ, Vargas J (2004) Adaptive significance of antipredator behaviour in artiodactyls. Anim Behav 67:205–228

    Article  Google Scholar 

  • Caro T, Stankowich T, Mesnick SL, Costa DP, Beeman K (2012) Pelage coloration in pinnipeds: functional considerations. Behav Ecol 23:765–774

    Article  Google Scholar 

  • Caro T, Stankowich T, Kiffner C, Hunter J (2013) Are spotted skunks conspicuous or cryptic? Ethol Ecol Evol 25:144–160

    Article  Google Scholar 

  • Chassard C (1956) Polymorphisme des populations d’Hippolyte varians Leach et comportement en function de leur adaptation chromatique presente. Bull Soc Zool Fr 81:413–418

    Google Scholar 

  • 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 65:1237–1247

    Article  Google Scholar 

  • Cooper WE, Vitt LJ (1985) Blue tails and autonomy—enhancement of predation avoidance in juvenile skinks. Z Tierpsychol 70:265–276

    Article  Google Scholar 

  • Cott HB (1940) Adaptive coloration in animals. Methuen & Co. Ltd, London

    Google Scholar 

  • 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 75:175–188

    Article  Google Scholar 

  • Dafni J, Diament A (1984) School-oriented mimicry: a new type of mimicry in fishes. Mar Ecol Prog Ser 20:45–50

    Article  Google Scholar 

  • 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):e11582

    Article  PubMed  PubMed Central  Google Scholar 

  • Edmunds M (1974) Defence in animals: a survey of anti-predator defences. Longman, Harlow

    Google Scholar 

  • Endler JA (1978) A predator’s view of animal color patterns. Evol Biol 11:319–364

    Article  Google Scholar 

  • Endler JA (1991) Interactions between predators and prey. In: Krebs JR, Davies NB (eds) Behavioral ecology. Blackwell, Oxford, pp 169–196

    Google Scholar 

  • Endler J (1992) Signals, signal condition, and the direction of evolution. Am Nat 139:125–153

    Article  Google Scholar 

  • Forsman A, Karlsson M, Wennersten L, Johansson J, Karpestam E (2011) Rapid evolution of fire melanism in replicated populations of pygmy grasshoppers. Evolution 65:2530–2540

    Article  PubMed  Google Scholar 

  • Gamble FW, Keeble FW (1900) Hippolyte varians: a study in color- change. J Cell Sci S2–43:589–698

    Google Scholar 

  • Gillespie J (1974) The role of environmental grain in the maintenance of genetic variation. Am Nat 108:831–836

    Article  Google Scholar 

  • Grant JB (2007) Ontogenetic colour change and the evolution of aposematism: a case study in panic moth caterpillars. J Anim Ecol 76:439–447

    Article  PubMed  Google Scholar 

  • 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 93:23–38

    Article  Google Scholar 

  • 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 264:429–437

    Article  Google Scholar 

  • 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 17:889–896

    Article  Google Scholar 

  • Higginson AD, Ruxton GD (2010) Optimal defensive coloration strategies during the growth period of prey. Evolution 64:53–67

    Article  PubMed  Google Scholar 

  • 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 10:350–359

    Article  PubMed  Google Scholar 

  • Honma A, Mappes J, Valkonen JJ (2015) Warning coloration can be disruptive: aposematic marginal wing patterning in the wood toger moth. Ecol Evol 5:4863–4874

    Article  PubMed  PubMed Central  Google Scholar 

  • Hossie TJ, Sherratt TN (2014) Does defensive posture increase mimetic fidelity of caterpillars with eyespots to their putative snake models? Curr Zool 60:76–89

    Article  Google Scholar 

  • Hossie TJ, Skelhorn J, Breinholt JW, Kawahara AY, Sherratt TN (2015) Body size affects the evolution of eyespots in caterpillars. Proc Nat Acad Sci 112:6664–6669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huey RB, Pianka ER (1977) Natural selection for juvenile lizards mimicking noxious beetles. Science 195:201–203

    Article  CAS  PubMed  Google Scholar 

  • 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 173:566–578

    Article  CAS  PubMed  Google Scholar 

  • 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 126:77–95

    Article  Google Scholar 

  • 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 91:248–251

    Article  Google Scholar 

  • 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:e78117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kettlewell HBD (1955) Recognition of appropriate backgrounds by the pale and black phases of Lepidoptera. Nature 175:943–944

    Article  CAS  PubMed  Google Scholar 

  • 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 201–232

    Google Scholar 

  • Kjernsmo K, Merilaita S (2013) Eyespots divert attacks by fish. Proc R Soc Lond B 280:20131458

    Article  Google Scholar 

  • Landridge KV, Broom M, Osorio D (2007) Selective signalling by cuttlefish to predators. Curr Biol 17:R1044–R1045

    Article  Google Scholar 

  • Lee WL (1966) Color change and the ecology of the marine isopod Idothea (Pentidothea) montereyensis Maloney, 1933. Ecology 47:930–941

    Article  Google Scholar 

  • Levins R (1968) Evolution in changing environments: some theoretical explorations, vol 2. Princeton University Press, Princeton

    Google Scholar 

  • Londoño GA, García DA, Martínez MAS (2015) Morphological and behavioral evidence of Batesian mimicry in nestlings of a lowland Amazonian bird. Am Nat 185:135–141

    Article  PubMed  Google Scholar 

  • Mänd T, Tammaru T, Mappes J (2007) Size dependent predation risk in cryptic and conspicuous insects. Evol Ecol 21:485–498

    Article  Google Scholar 

  • Mappes J, Marples N, Endler JA (2005) The complex business of survival by aposematism. Trends Ecol Evol 20:598–603

    Article  PubMed  Google Scholar 

  • Marshall NJ (2000) Communication and camouflage with the same ‘bright’ colours in reef fishes. Phil Trans R Soc Lond B 355:1243–1248

    Article  CAS  Google Scholar 

  • Marshall KLA, Stevens M (2014) Wall lizards display conspicuous signals to conspecifics and reduce detection by avian predators. Behav Ecol 25:1325–1337

    Article  PubMed  PubMed Central  Google Scholar 

  • Mäthger LM, Chiao CC, Barbosa A, Hanlon RT (2008) Color matching on natural substrates in cuttlefish, Sepia officinalis. J Comp Physiol A 194:577–585

    Article  Google Scholar 

  • Merilaita S, Tullberg BS (2005) Constrained camouflage facilitates the evolution of conspicuous warning coloration. Evolution 59:38–45

    Article  PubMed  Google Scholar 

  • Montgomerie R, Lyon B, Holder K (2001) Dirty ptarmigan: behavioral modification of conspicuous male plumage. Behav Ecol 12:429–438

    Article  Google Scholar 

  • Nachman MW, Hoekstra HE, D’Agostino SL (2003) The genetic basis of adaptive melanism in pocket mice. PNAS 100:5268–5273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niskanen M, Mappes J (2005) Significance of the dorsal zig-zag pattern of Vipera latastei graditana against avian predators. J Anim Ecol 74:1091–1101

    Article  Google Scholar 

  • Nosil P, Crespi BJ (2006) Experimental evidence that predation promotes divergence in adaptive radiation. PNAS 103:9090–9095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e47092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oxford GS, Gillespie RG (1998) Evolution and ecology of spider coloration. Ann Rev Entomol 43:619–643

    Article  CAS  Google Scholar 

  • Penney HD, Hassall C, Skevington JH, Abbott KR, Sherratt TN (2012) A comparative analysis of the evolution of imperfect mimicry. Nature 483:461–464

    Article  CAS  PubMed  Google Scholar 

  • 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 237:269–315

    Google Scholar 

  • Powell BL (1962) The responses of the chromatophores of Carcinus maenas (L. 1758) to light and temperature. Crustaceana 4:93–102

    Article  Google Scholar 

  • 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 104:19381–19386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 104:14372–14376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruxton GD, Speed MP, Kelly DJ (2004) What, if anything, is the adaptive function of countershading? Anim Behav 68:445–451

    Article  Google Scholar 

  • Simpson SJ, Sword GA, Lo N (2011) Polyphenism in insects. Curr Biol 21:R738–R749

    Article  CAS  PubMed  Google Scholar 

  • Stevens M (2005) The role of eyespots as anti-predator mechanisms, principally demonstrated in the Lepidoptera. Biol Rev 80:573–588

    Article  PubMed  Google Scholar 

  • Stevens M (2007) Predator perception and the interrelation between different forms of protective coloration. Proc R Soc B 274:1457–1464

    Article  PubMed  PubMed Central  Google Scholar 

  • Stevens M (2013) Sensory ecology, behaviour, and evolution. Oxford University Press, Oxford

    Book  Google Scholar 

  • Stevens M (2016) Color change, phenotypic plasticity, and camouflage. Front Ecol Evol 4:51

    Article  Google Scholar 

  • Stevens M, Ruxton GD (2012) Linking the evolution and form of warning coloration in nature. Proc R Soc Lond B 279:417–426

    Article  Google Scholar 

  • Stevens M, Yule DH, Ruxton GD (2008) Dazzle coloration and prey movement. Proc R Soc B 275:2639–2643

    Article  PubMed  PubMed Central  Google Scholar 

  • Stevens M, Rong CP, Todd PA (2013) Colour change and camouflage in the horned ghost crab Ocypode ceratophthalmus. Biol J Linn Soc 109:257–270

    Article  Google Scholar 

  • Stevens M, Lown AE, Denton AM (2014a) Rockpool gobies change colour for camouflage. PLoS ONE 9:e110325

    Article  PubMed  PubMed Central  Google Scholar 

  • Stevens M, Wood LE, Lown AE (2014b) Camouflage and individual variation in shore crabs (Carcinus maenas) from different habitats. PLoS ONE 9:e115586

    Article  PubMed  PubMed Central  Google Scholar 

  • Stoner CJ, Caro T, Graham CM (2003) Ecological and behavioral correlates of coloration in artiodactyls: systematic attempts to verify conventional hypotheses. Behav Ecol 14:823–840

    Article  Google Scholar 

  • Stuart-Fox D, Moussalli A (2009) Camouflage, communication and thermoregulation: lessons from colour changing organisms. Philos Trans R Soc Lond B 364:463–470

    Article  Google Scholar 

  • 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 88:437–446

    Article  Google Scholar 

  • Todd PA, Qui W, Chong KY (2009) Ontogenetic shifts in carapace patterning and/or colouration in intertidal and subtidal brachyuran crabs. Raffles Bull Zool 57:543–550

    Google Scholar 

  • 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 272:1315–1321

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 62:1389–1396

    Article  Google Scholar 

  • Umbers KDL, Fabricant SA, Gawryszewski FM, Seago AE, Herberstein ME (2014) Reversible colour change in arthropoda. Biol Rev 89:820–848

    Article  PubMed  Google Scholar 

  • Umbers KDL, Lehtonen J, Mappes J (2015) Deimatic displays. Curr Biol 25:R58–R59

    Article  CAS  PubMed  Google Scholar 

  • 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 60:114–122

    Article  Google Scholar 

  • 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 272:1203–1207

    Article  Google Scholar 

  • Wallace AR (1867) Mimicry and other protective resemblances among animals. Westminster Review, London, pp 1–43

    Google Scholar 

  • Wallace AR (1877) The colours of animals and plants. Part I. Am Nat 11(11):384–406

    Article  Google Scholar 

  • 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 364:503–510

    Article  Google Scholar 

  • Williams DD, Tavares AF, Bryant E (1987) Respiratory device or camouflage?: A case for the caddisfly. Oikos 50:42–52

    Article  Google Scholar 

  • Young RE, Roper CF (1976) Bioluminescent countershading in midwater animals: evidence from living squid. Science 191:1046–1048

    Article  CAS  PubMed  Google Scholar 

  • Zimova M, Mills LS, Lukacs PM, Mitchell MS (2014) Snowshoe hares display limited phenotypic plasticity to mismatch in seasonal camouflage. Proc R Soc B 281:20140029

    Article  PubMed  PubMed Central  Google Scholar 

  • Zylinski S, Johnsen S (2011) Mesopelagic cephalopods switch between transparency and pigmentation to optimize camouflage in the deep. Curr Biol 21:1937–1941

    Article  CAS  PubMed  Google Scholar 

  • 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 283:20160062

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank Daniel Osorio, Devi Stuart-Fox and the associate editor for helpful comments.

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Correspondence to Tim Caro.

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Caro, T., Sherratt, T.N. & Stevens, M. The ecology of multiple colour defences. Evol Ecol 30, 797–809 (2016). https://doi.org/10.1007/s10682-016-9854-3

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