Defence Cheats Can Degrade Protection of Chemically Defended Prey

Abstract

Many species defend themselves against enemies using repellent chemicals. An important but unanswered question is why investment in chemical defence is often variable within prey populations. One explanation is that some prey benefit by cheating, paying no costs of defence, but gaining a reduced attack rate because of the presence of defended conspecifics. Two important assumptions about predator behaviour must be met to explain cheating as a stable strategy: first, predators increase attack rates as cheats increase in frequency; second, defended prey survive attacks better than non‐defended conspecifics. We lack data from wild predators that evaluate these hypotheses. Here, we examine how changes in the frequency of non‐defended ‘cheats’ affect predation by wild birds on a group of otherwise defended prey. We presented mealworm larvae that were either edible (‘cheats’) or unpalatable (bitter tasting), and varied the proportion of cheats from 0 to 1 by increments of 0.25. We found strong frequency‐dependent effects on the birds' foraging behaviour, with the proportion of prey attacked increasing nonlinearly with the frequency of cheats. We did not, however, observe that birds taste‐rejected defended prey at the site of capture. One explanation is that wild birds may not assess prey palatability at the site of capture, but do this elsewhere. If so, defended and undefended prey may pay high costs of initial attack and relocation away from ecologically favourable locations. Alternatively, defended prey may not be taste‐rejected because with acute time constraints, wild birds do not have time to make fine‐grained decisions during feeding. We discuss the data in relation to the evolutionary ecology of prey defences.

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

“…There are fewer examinations with wild predators, though Carroll and Sherratt (2013) recently demonstrated reduced damage to individual prey. In our own investigations with free living adult birds (Jones et al 2013) and mealworms as prey we found strong public benefits of reduced attack rates as chemical defence (a distasteful bitrex treatment) became more common, but we did not observe individual survival, in which defended prey are released before ingestion. Rather birds either ate the prey at the foraging site, or flew away from our feeding stations before deciding to eat or reject prey, making it difficult to determine whether, or the extent to which, individual prey benefitted from their chemical defence.…”

“…To examine whether the birds could to any extent discriminate mimics from models we used the method employed by Jones et al (2013), in which we determine the difference between the observed proportion of prey attacked that are defended with that expected by their frequency in the set of prey presented. We then used a one-tailed t test, to determine if the mean difference across birds was different from zero.…”

“…Hence here we present great tits (Parus major) with mealworm prey that are either edible or unpalatable (soaked in quinine), and we gradually varied the frequency of distasteful prey (Mappes et al 1999b). We extended the approach of Jones et al (2013) by adding in variation in the degree of aggregation of the mealworms in this experiment.…”

“…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'' .…”

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

“…from a food source. In our co-evolutionary model the inter-population diversification is a consequence of drift which is an interesting result: intra-population cheating (or automimicry) is problematic in the context of evolutionary stability as it undermines the effectiveness of the signal since cheating appears to be at a selective advantage [26]. Drift instead allows a wide diversity of inter-population aposematic solutions without the introduction of destabilising cheating or automimicry on the intra-population level.…”