The complex business of survival by aposematism Johanna Mappes 1 , Nicola Marples 2 and John A. Endler 3,4 1 Department of Biological and Environmental Science, University of Jyva ¨ skyla ¨ . PO Box 35, FIN 40351, Jyva ¨ skyla ¨ , Finland 2 Department of Zoology, Trinity College, Dublin 2, Ireland 3 Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, CA 93106-9610, USA 4 Department of Zoology & Tropical Ecology, James Cook University, Townsville, QLD 4811, Australia The theory of warning signals dates back to Wallace but is still confusing, controversial and complex. Because predator avoidance of warningly coloured prey (apo- sematism) is based upon learning and reinforcement, it is difficult to understand how initially rare conspicuous forms subsequently become common. Here, we discuss several possible resolutions to this apparent paradox. Many of these ideas have been largely ignored as a result of implicit assumptions about predator behaviour and assumed lack of variation in the predators, prey and the predation process. Considering the spatial and temporal variation in and mechanisms of behaviour of both predators and prey will make it easier to under- stand the process and evolution of aposematism. Introduction Warning signals manipulate predator foraging behaviour by sending a signal, which can be a distinctive colour, odour or behaviour, to the predator that the prey is unprofitable [1–4] (Figure 1; Box 1). This, in turn, enables and encourages the predator to switch to more profitable prey [5–7]. The association between the signal and unprofitability is called ‘aposematism’ [1]. Aposematic signals work best when they are easily detectable and memorable, which facilitates avoidance learning [4]. However, by sending conspicuous signals, prey also increase their own risk of damage or death if the predator is immune to their defences [8], has forgotten the asso- ciation between signal and unprofitability, or is naı ¨ve [4]. The benefits of aposematism increase as a function of the density of the similarly signalling individuals [8], making maintenance understandable but origin apparently para- doxical [9]. The concepts and evidence for aposematism have been reviewed recently [4], therefore we discuss the largely neglected mechanisms that might aid or prevent the initial spread and maintenance of aposematism. Predator behaviour It is commonly assumed that the initial stages of the evolution of aposematism proceed slowly or inefficiently because learning and reinforcement mechanisms work better at high prey densities [4,10]. This assumption Figure 1. Examples of warning colouration. (a) Seven-spot ladybirds Coccinella septempunctata are a classic example of aposematic species. Conspicuous coloration warns predators that the prey is toxic. (b) Aposematism and crypsis combined: the noxious swallowtail butterfly, Papilio machaon is cryptic from a distance but conspicuous close up [70]. (c) The zig-zag pattern of many venomous snakes is suggested to be an example of a disruptive colour pattern. Recent studies show that the zig-zag pattern of Vipera species can also function as a warning to predators [71]. Reproduced with permission from Jarkko Ma ¨ kineva/Nature Photo Agency, Aarni Nurmila/Nature Photo Agency and Martti Niskanen. Corresponding author: Mappes, J. (mappes@bytl.jyu.fi). Available online 8 August 2005 Review TRENDS in Ecology and Evolution Vol.20 No.11 November 2005 www.sciencedirect.com 0169-5347/$ - see front matter Q 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2005.07.011