Density-dependent predation influences the evolution and behavior of masquerading prey

Abstract

Predation is a fundamental process in the interaction between species, and exerts strong selection pressure. Hence, anti-predatory traits have been intensively studied. Although it has long been speculated that individuals of some species gain protection from predators by sometimes almost-uncanny resemblances to uninteresting objects in the local environment (such as twigs or stones), demonstration of antipredatory benefits to such "masquerade" have only very recently been demonstrated, and the fundamental workings of this defensive strategy remain unclear. Here we use laboratory experiments with avian predators and twig-mimicking caterpillars as masqueraders to investigate (i) the evolutionary dynamics of masquerade; and (ii) the behavioral adaptations associated with masquerade. We show that the benefit of masquerade declines as the local density of masqueraders relative to their models (twigs, in our system) increases. This occurs through two separate mechanisms: increasing model density both decreased predators' motivation to search for masqueraders, and made masqueraders more difficult to detect. We further demonstrated that masquerading organisms have evolved complex microhabitat selection strategies that allow them to best exploit the densitydependent properties of masquerade. Our results strongly suggest the existence of opportunity costs associated with masquerade. Careful evaluation of such costs will be vital to the development of a fuller understanding of both the distribution of masquerade across taxa and ecosystems, and the evolution of the life history strategies of masquerading prey.camouflage | crypsis | habitat selection | misclassification | Selenia dentaria

Cognition and the evolution of camouflage

“…However, it is important to note that our understanding of how masquerading prey exploit the cognitive processes of predators is still very much in its infancy. Most experiments investigating the evolution of masquerade have focused on determining whether predators misclassify a particular masquerader as the inedible model it resembles [16,29,[31][32][33][34], and/or what aspects of the masquerader's appearance or environment influences the probability of this happening [29,32,33]. Only a small number of experiments have investigated how predators learn to discriminate between masqueraders and their inedible models [28], and in these experiments, the masquerading prey were the only source of food available to predators.…”

“…Other prey that are unable to change how they look can reduce their predation risk by restricting themselves to substrates that they readily match [49] or selecting microhabitats that are more concealing [25,28,29]. Again, the mechanisms underlying these kinds of decisions remain largely unexplored.…”

“…This is likely to influence predators' decisions about whether or not to include masquerading prey in their diet, because attempting to discriminate between models and masqueraders becomes less economically attractive as the density of models increases relative to that of masqueraders. Indeed, experiments have shown that predators are both less motivated to search for masqueraders, and more likely to misclassify them when models are common in comparison to masqueraders [29]. Intriguingly, individuals that differ in their appearance may also choose to live in different microhabitats (see prey cognition section below).…”

“…However, if predation risk is reduced by giving the same choice in the dark, or hunger is increased through food deprivation prior to testing, the caterpillars show a stronger preference for the branch offering the best feeding opportunities. They are able to adjust their decisions according to their physiological state and environmental cues that inform them about probable predation risk (see also [29]). Again such behaviour could be attributed to the use of either innate rules of thumb or more cognitive processes; and if the latter is true, then prey cognition may be an important selective agent driving the evolution of the appearance and behaviour of camouflaged prey.…”

“…We will define cognition in the broadest terms: including how animals perceive, learn, classify and make decisions [22][23][24]. We will not only consider the cognitive abilities of predators, but also the cognitive abilities of the prey themselves since the behaviour of both cryptic and masquerading prey can influence the degree to which they benefit from their visual appearance [25][26][27][28][29]. We will limit our discussion to camouflage in the visual domain, since most research into the function and evolution of camouflage focuses on this.…”