Abstract
European vipers (genus Vipera) are venomous and often have a distinctive dorsal zigzag pattern. The zigzag pattern of vipers has been suggested to be an example of disruptive colouration which reduces the detectability of a snake. However, recent studies suggest that the patterns have an aposematic function, although those experiments did not exclude the possibility of disruptive colouration. We used plasticine replicas of snakes to examine whether the zigzag pattern of European vipers provides protection from avian predator attacks via disruptive or aposematic function, or if the zigzag pattern might simultaneously serve both antipredatory functions. Experiments were conducted in the Coto Doñana National Park southern Spain. In the experiment, predation pressure caused by birds was compared between zigzag pattern (patterns were painted with and without disruptive effect i.e. breaking body outline or not), classical disruptive colouration (non-randomly placed patterns that breaks body outline) and control markings (replicas with length wise stripes and models without painted pattern) on natural and controlled backgrounds. We found that zigzag patterned snake replicas suffered less predation than striped ones regardless of the background, providing further evidence that the zigzag pattern of European vipers functions as a warning signal against predators. However, we did not find evidence that the zigzag pattern involves a disruptive effect.
Similar content being viewed by others
References
Andrén C, Nilson G (1981) Reproductive success and risk of predation in normal and melanistic colour morphs of the adder, Vipera berus. Biol J Linn Soc 15:235–246
Arnold EN, Burton JA (1978) A field guide to the reptiles and amphibians of Britain and Europe [Finnish edition—Viitanen P, Koskela P, Lindholm E (1981)] Kustannusosakeyhtiö Tammi, Helsinki
Bohlin T, Tullberg BS, Merilaita S (2008) The effect of signal appearance and distance on detection risk in an aposematic butterfly larva (Parnassius apollo). Anim Behav 76:577–584
Brodie ED (1993) Differential avoidance of coral snake banded patterns by free-ranging avian predators in Costa Rica. Evolution 47:277–285
Brodie ED, Janzen FD (1995) Experimental studies of Coral Snake mimicry: generalized avoidance of ringed patterns by free-ranging avian predators. Funct Ecol 9:186–190
Brower LP, Ryerson WN, Coppinger LL, Glazier SC (1968) Ecological chemistry and the palatability spectrum. Science 161:1349–1351
Cott HB (1940) Adaptive colouration in animals. Methuen, London
Cramp S (1985) Handbook of the birds of Europe, the Middle East and North Africa, vol IV. Oxford University Press, Oxford
Cuthill IC, Stevens M, Sheppard J, Maddocks T, Pàrraga CA, Troscianko TS (2005) Disruptive colouration and background pattern matching. Nature 434:72–74
Darst CR, Cummings ME, Cannatela DC (2006) A mechanism for diversity in warning sinals: conspicuousness versus toxicity in poison frogs. Proc Natl Acad Sci USA 103:5852–5857
De Smedt J (2001) Die europäischen Vipern. Artbestimmung, Sysematic, Haltung ung Zucht. Johan De Smedt, Füssen
Edmunds ME (1974) Defence in animals: a survey of anti-predator defences. Longman, Harlow, Essex
Endler JA (1991) Interactions between predators and prey. In: Krebs JR, Davies NB (eds) Behavioural ecology, 3rd edn. Blackwell Scientific Publications, Oxford, pp 169–196
Endler JA, Mappes J (2004) Predator mixes and the conspicuousness of aposematic signals. Am Nat 163:532–547
Evans DL, Schmidt JO (1990) Insect defenses: adaptive mechanisms and strategies of prey and predators. University of New York Press, New York
Forsman A (1995a) Heating rates and body temperature variation in melanistic and zigzag Vipera berus: does colour make a difference? Ann Zool Fenn 32:365–374
Forsman A (1995b) Opposing fitness consequences of color pattern in male and female snakes. J Evol Biol 8:53–70
Forsman A, Merilaita J (1999) Fearful symmetry: pattern size and symmetry affects aposematic signal efficacy. Evol Ecol 13:131–140
Gamberale G, Tullberg BS (1996) Evidence for a peak-shift in predator generalization among aposematic prey. Proc R Soc Lond B 263:1329–1334
Gittleman JL, Harvey PH (1980) Why are distasteful prey not cryptic? Nature 286:149–150
Gittleman JL, Harvey PH, Greenwood PJ (1980) The evolution of conspicuous colouration: some experiments in bad taste. Anim Behav 28:897–899
Herczeg G, Saarikivi J, Gonda A, Perälä J, Tuomola A, Merilä J (2007) Suboptimal thermoregulation in male adders (Vipera berus) after hibernation imposed by spermiogenesis. Biol J Linn Soc 92:19–27
Lindell LE, Forsman A (1996) Sexual dichromatism in snakes: support for the flicker-fusion hypothesis. Can J Zool 75:2254–2256
Lindstedt C, Lindström L, Mappes J (2008) Hairiness and warning colours as components of antipredator defence: additive or interactive benefits? Anim Behav 75(5):1703–1713
Linström L, Alatalo RV, Mappes J, Riipi M, Vertainen L (1999) Can aposematic signals evolve by gradual change? Nature 397:249–251
Marshal NJ (2000) Communication and camouflage in reef fishes. Phil Trans Soc Lond B 355:1243–1248
Merilaita S, Lind J (2005) Background-matching and disruptive colouration and the evolution of cryptic colouration. Proc R Soc B 272:665–670
Niskanen M, Mappes J (2005) Significance of the dorsal zigzag pattern of Vipera latastei gaditana against avian predators. J Anim Ecol 74:1091–1101
Poulton EB (1890) The colours of animals: their meaning and use especially considered in the case of insects. Kegan, Trennch, Trubnes & Co
Rangen SA, Clarl RG, Hobson KA (2000) Visual and olfactory attributes of artificial nests. Auk 117:136–146
Roper TJ, Wistow R (1986) Aposematic colouration and avoidance-learning in chicks. Q J Exp Psychol B 38:141–149
Ruxton GD, Sherrat TN, Speed MP (2004) Avoiding attack. Oxford University Press, Oxford
Schaefer MH, Stobbe N (2006) Disruptive colouration provides camouflage independent of background matching. Proc R Soc B 273:2427–2432
Selas V (2001) Predation on reptiles and birds by the common buzzard, Buteo buteo, in relation to changes in its main prey voles. Can J Zool 79:2086–2093
Sherrat TN, Beatty CD (2003) The evolution of warning signals as reliable indicators of prey defence. Am Nat 162:377–389
Shine R, Madsen T (1994) Sexual dichromatism in snakes of the genus Viperia: a review and a new evolutionary hypothesis. J Herpet 28:114–117
Sokal RR, Rohlf JF (1995) Biometry: the principles and practice of statistics in biological research. W.H. Freeman and Company, New York
Stevens M, Cuthill IC (2006) Disruptive colouration, crypsis and edge detection in early visual processing. Proc R Soc B 273:2141–2147
Stevens M, Merilaita S (2009a) Animal camouflage: current issues and new perspectives. Phil Trans R Soc B 364:423–427
Stevens M, Merilaita S (2009b) Defining disruptive colouration and distinguishing its functions. Phil Trans R Soc B 364:481–488
Stevens M, Cuthill IC, Windsor AMM, Walker HJ (2006) Disruptive contrast in animal camouflage. Proc R Soc B 273:2433–2438
Stevens M, Castor-Perry SA, Price JRF (2008) The protective value of conspicuous signals is not impaired by shape, size, or position asymmetry. Behav Ecol 20:96–102
Thayer GH (1909) Concealing-colouration in the animal kingdom: an exposition of the laws of disguise through color and pattern: being a summary of Abbott H. Thayer’s discoveries. NY Macmillan, New York
Tulberg BS, Merilaita S, Wiklund C (2005) Aposematism and crypsis combined as a result of distance dependence: functional versatility of the colour pattern in the swallowtail butterfly larva. Proc R Soc B 272:1315–1321
Wüster W, Allum CSE, Bjargardóttir IB, Bailey KL, Dawson KJ, Guenoui J, Lewis J, Mc Gurk J, Moore AG, Niskanen M, Pollard CP (2004) Do aposematism and Batesian mimicry require bright colours? A test, using European viper markings. Proc R Soc B 271:2495–2499
Acknowledgments
We would like to thank Consenjo Superior De Investigaciones Cientificas (CSIC) for providing funding and the opportunity to work in Coto Doñana national park. Also, many thanks to Begoña Arrizabalga and Rosa Rodriguez for arrangements and help in Sevilla. Dr. Martin Stevens, Dr. Carita Lindstedt, Prof. Mikko Mönkkönen, Prof. Janne Kotiaho, MSc Robert Hegna and three anonymous reviewers gave many helpful comments on the earlier version of the manuscript. MSc Ossi Nokelainen assisted with field work and Matt Wilson provided photographs of the ladder snake. Part of the funding was provided by the Centre of Excellence in Evolutionary Research and the University of Jyväskylä.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Valkonen, J., Niskanen, M., Björklund, M. et al. Disruption or aposematism? Significance of dorsal zigzag pattern of European vipers. Evol Ecol 25, 1047–1063 (2011). https://doi.org/10.1007/s10682-011-9463-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10682-011-9463-0