Automimicry destabilizes aposematism: predator sample-and-reject behaviour may provide a solution

Abstract

Aposematism, the use of conspicuous colours to advertise unpalatability to predators, is perhaps the most studied signalling system in nature. However, its evolutionary stability remains paradoxical. The paradox is illustrated by the problem of automimicry. Automimics are palatable individuals within a population of unpalatable aposematics. Automimics benefit from predators avoiding warning coloration without carrying the models' cost of unpalatability, and should increase in the population, destabilizing the signalling system, unless selected against in some way. Cautious sampling, instead of avoidance, by predators may offer a solution to this problem. Here, we investigate the effect of automimic frequency on predator sampling behaviour, and whether predator sampling behaviour may provide a selection pressure against mimics. Domestic chicks (Gallus gallus domesticus) were subjected to the task of discriminating between green (signalling) and untreated brown chick crumbs. Some of the green crumbs were quinine treated and thus unpalatable. The frequency of palatable signalling prey items varied in four treatments; all unpalatable, low automimic frequency, high automimic frequency and all palatable. The results show that predator sampling behaviour is sensitive to automimic frequency and that predators may discriminate between models and mimics through sampling, and thereby benefit unprofitable prey. The results suggest somewhat surprisingly that aposematic signalling is stable only because of the actions of those predators not actually deterred by warning signals.

Parameterising a public good: how experiments on predation can be used to predict cheat frequencies

“…Published work uses young domesticated chickens (Gamberale-Stille and Guilford 2004;Skelhorn and Rowe 2007) whose feeding behaviour is rather different from most passerine birds. For example, chicks learn to find food items by pecking and tasting everything from non-organic objects to organic items.…”

“…Daly et al (2012a) for example showed that frequency of nondefended prey increased with group size in caterpillars of the large white butterfly (Pieris brassicae). Such non-defended individuals might be considered parasitic cheats if their presence in a population of defended prey has a consequence of raising the attack rates as indicated in several recent experiments (Gamberale-Stille and Guilford 2004;Skelhorn and Rowe 2007;Jones et al 2013). These cheats are often known as ''automimics'' .…”

“…For the public good explanation of automimicry to apply, it is key to demonstrate experimentally both individual and public benefits from chemical defence. This has been investigated most thoroughly with lab models of bird-insect systems, in which the predator is usually a young, naïve domestic chicken (Gallus gallus) and the prey are artificial crumbs (Gamberale-Stille and Guilford 2004;Skelhorn and Rowe 2006b;Skelhorn and Rowe 2007). In this context both individual benefits (raised survival) and public benefits (reduced predation frequency) have been demonstrated from chemical defence but it is important to note that the ''survival rate'' of tasterejected prey is not easy to estimate when chick crumbs take the place of insect prey.…”

Taste-rejection behaviour by predators can promote variability in prey defences

“…Recent laboratory experiments have shown that birds can taste the difference between defended and undefended prey in both aposematic and cryptic populations (Skelhorn & Rowe 2006b;Halpin et al 2008a,b). However, if birds can accurately taste-reject prey that invest in different levels of toxins (Gamberale-Stille & Guilford 2004;Skelhorn & Rowe 2005), this leaves a different problem of trying to explain the widespread existence of variation in toxicity in prey populations (e.g. Brower et al 1967;.…”

The Evolutionary Dynamics of Aposematism: a Numerical Analysis of Co-Evolution in Finite Populations

“…Hence key questions of current importance in aposematism theory focus on the question: how conspicuous should a signal be, and how much should be invested into secondary defences [16,25,29,30]? Moreover, which factors influence evolutionary stability of honest signalling and what is the role of mimics in maintaining or destabilising aposematic display [10]? To explain stability and persistence of aposematic signals we require a theory of co-evolution of defence and signals [27,38].…”