The evolution and ecology of multiple antipredator defences.

Prey seldom rely on a single type of antipredator defence, often using multiple defences to avoid predation. In many cases, selection in different contexts may favour the evolution of multiple defences in a prey. However, a prey may use multiple defences to protect itself during a single predator encounter. Such "defence portfolios" that defend prey against a single instance of predation are distributed across and within successive stages of the predation sequence (encounter, detection, identification, approach (attack), subjugation and consumption). We contend that at present, our understanding of defence portfolio evolution is incomplete, and seen from the fragmentary perspective of specific sensory systems (e.g., visual) or specific types of defences (especially aposematism). In this review, we aim to build a comprehensive framework for conceptualizing the evolution of multiple prey defences, beginning with hypotheses for the evolution of multiple defences in general, and defence portfolios in particular. We then examine idealized models of resource trade-offs and functional interactions between traits, along with evidence supporting them. We find that defence portfolios are constrained by resource allocation to other aspects of life history, as well as functional incompatibilities between different defences. We also find that selection is likely to favour combinations of defences that have synergistic effects on predator behaviour and prey survival. Next, we examine specific aspects of prey ecology, genetics and development, and predator cognition that modify the predictions of current hypotheses or introduce competing hypotheses. We outline schema for gathering data on the distribution of prey defences across species and geography, determining how multiple defences are produced, and testing the proximate mechanisms by which multiple prey defences impact predator behaviour. Adopting these approaches will strengthen our understanding of multiple defensive strategies.

A synthesis of deimatic behaviour.

Deimatic behaviours, also referred to as startle behaviours, are used against predators and rivals. Although many are spectacular, their proximate and ultimate causes remain unclear. In this review we aim to synthesise what is known about deimatic behaviour and identify knowledge gaps. We propose a working hypothesis for deimatic behaviour, and discuss the available evidence for the evolution, ontogeny, causation, and survival value of deimatic behaviour using Tinbergen's Four Questions as a framework. Our overarching aim is to direct future research by suggesting ways to address the most pressing questions in this field.

The peppered moth Biston betularia.

Hannah Rowland and colleagues introduce the peppered moth whose industrial melanism was an early evidence for evolution.

Dietary wariness.

What causes an animal to resist trying new food or incorporating it into their diet? In this Quick guide, Heyworth et al. discuss the phenomenon known as dietary wariness.

Variable crab camouflage patterns defeat search image formation.

Understanding what maintains the broad spectrum of variation in animal phenotypes and how this influences survival is a key question in biology. Frequency dependent selection - where predators temporarily focus on one morph at the expense of others by forming a "search image" - can help explain this phenomenon. However, past work has never tested real prey colour patterns, and rarely considered the role of different types of camouflage. Using a novel citizen science computer experiment that presented crab "prey" to humans against natural backgrounds in specific sequences, we were able to test a range of key hypotheses concerning the interactions between predator learning, camouflage and morph. As predicted, switching between morphs did hinder detection, and this effect was most pronounced when crabs had "disruptive" markings that were more effective at destroying the body outline. To our knowledge, this is the first evidence for variability in natural colour patterns hindering search image formation in predators, and as such presents a mechanism that facilitates phenotypic diversity in nature.

The antipredator benefits of postural camouflage in peppered moth caterpillars.

Camouflage is the most common form of antipredator defense, and is a textbook example of natural selection. How animals' appearances prevent detection or recognition is well studied, but the role of prey behavior has received much less attention. Here we report a series of experiments with twig-mimicking larvae of the American peppered moth Biston betularia that test the long-held view that prey have evolved postures that enhance their camouflage, and establish how food availability and ambient temperature affect these postures. We found that predators took longer to attack larvae that were resting in a twig-like posture than larvae resting flat against a branch. Larvae that were chilled or food restricted (manipulations intended to energetically stress larvae) adopted a less twig-like posture than larvae that were fed ad libitum. Our findings provide clear evidence that animals gain antipredator benefits from postural camouflage, and suggest that benefits may come at an energetic cost that animals are unwilling or unable to pay under some conditions.

Distaste and disgust responses.

John Skelhorn introduces the innate responses to aversive tastes.

Avoiding death by feigning death.

Thanatosis is a common phenomenon in which prey appear to feign death when attacked by predators. It was once widely believed that thanatosis exploited predators' tendencies to avoid dead prey. However, this hypothesis has never been tested, and its feasibility has been questioned to the point that it has been largely abandoned [1,2]. Here, I show that naive birds quickly learned that dead Indian stick insects Carausius morosus were unpalatable, and subsequently rejected live insects that displayed thanatosis, but not those that failed to show thanatosis. Thanatosis had no effect on the behavior of birds that had never experienced dead insects, or those that had experienced dead insects whose resemblance to thanatosic insects had been destroyed. Therefore, thanatosis clearly caused predators to avoid prey that they mistakenly perceived to be dead.

Camouflage strategies interfere differently with observer search images.

Numerous animals rely on camouflage for defence. Substantial past work has identified the presence of multiple strategies for concealment, and tested the mechanisms underpinning how they work. These include background matching, D-RUP coloration to destroy target edges, and distractive markings that may divert attention from key target features. Despite considerable progress, work has focused on how camouflage types prevent initial detection by naive observers. However, predators will often encounter multiple targets over time, providing the opportunity to learn or focus attention through search images. At present, we know almost nothing about how camouflage types facilitate or hinder predator performance over repeated encounters. Here, we use experiments with human subjects searching for targets on touch screens with different camouflage strategies, and control the experience that subjects have with target types. We show that different camouflage strategies affect how subjects improve in detecting targets with repeated encounters, and how performance in detection of one camouflage type depends on experience of other strategies. In particular, disruptive coloration is effective at preventing improvements in camouflage breaking during search image formation, and experience with one camouflage type (distraction) can decrease the ability of subjects to switch to and from search images for new camouflage types (disruption). Our study is, to our knowledge, the first to show how the success of camouflage strategies depends on how they prevent initial and successive detection, and on predator experience of other strategies. This has implications for the evolution of prey phenotypes, how we assess the efficacy of defences, and predator-prey dynamics.

Testing the feasibility of the startle-first route to deimatism.

Many prey species perform deimatic displays that are thought to scare or startle would-be predators, or elicit other reflexive responses that lead to attacks being delayed or abandoned. The form of these displays differs among species, but often includes prey revealing previously-hidden conspicuous visual components. The evolutionary route(s) to deimatism are poorly understood, but it has recently been suggested that the behavioural component of the displays evolves first followed by a conspicuous visual component. This is known as the "startle-first hypothesis". Here we use an experimental system in which naïve domestic chicks forage for artificial deimatic prey to test the two key predictions of this hypothesis: (1) that movement can deter predators in the absence of conspicuously coloured display components; and, (2) that the combination of movement and conspicuously coloured display components is more effective than movement alone. We show that both these predictions hold, but only when the movement is fast. We thus provide evidence for the feasibility of 'the startle-first hypothesis' of the evolution of deimatism.

Prey mistake masquerading predators for the innocuous items they resemble.

Understanding how natural selection has shaped animals' visual appearance to aid predator avoidance and prey capture has been an ongoing challenge since the conception of evolutionary theory [1,2]. Masquerade - animals resembling inedible objects common in the local environment (e.g. twigs, leaves, stones) - is one of a handful of strategies that has been suggested to serve both protective and aggressive functions (i.e. to work for both prey and predators) [3]. There is now good evidence for protective masquerade: predators detect masquerading prey but ignore them because they mistake them for the inedible objects they resemble [4]. However, there is no direct evidence that predators can benefit from aggressive masquerade [3,5]. Here, I tested the idea that prey detect masquerading predators but mistake them for the innocuous items that they resemble, making them less wary and easier for predators to catch. Because prey can only mistake masquerading predators for the objects they resemble if they have previous experience of those items, I manipulated house crickets' (Acheta domesticus) experience with dead leaves, before placing them in tanks with dead-leaf-resembling Ghost mantises (Phyllocrania paradoxa). I found that mantises given crickets with experience of unmanipulated dead leaves caught crickets faster and after fewer attempts than mantises given crickets without experience of dead leaves, or crickets with experience of manipulated dead leaves that no longer resembled mantises. These findings demonstrate that predators can indeed benefit from aggressive masquerade.

The biology of color.

Coloration mediates the relationship between an organism and its environment in important ways, including social signaling, antipredator defenses, parasitic exploitation, thermoregulation, and protection from ultraviolet light, microbes, and abrasion. Methodological breakthroughs are accelerating knowledge of the processes underlying both the production of animal coloration and its perception, experiments are advancing understanding of mechanism and function, and measurements of color collected noninvasively and at a global scale are opening windows to evolutionary dynamics more generally. Here we provide a roadmap of these advances and identify hitherto unrecognized challenges for this multi- and interdisciplinary field.

The Impact of Detoxification Costs and Predation Risk on Foraging: Implications for Mimicry Dynamics.

Prey often evolve defences to deter predators, such as noxious chemicals including toxins. Toxic species often advertise their defence to potential predators by distinctive sensory signals. Predators learn to associate toxicity with the signals of these so-called aposematic prey, and may avoid them in future. In turn, this selects for mildly toxic prey to mimic the appearance of more toxic prey. Empirical evidence shows that mimicry could be either beneficial ('Mullerian') or detrimental ('quasi-Batesian') to the highly toxic prey, but the factors determining which are unknown. Here, we use state-dependent models to explore how tri-trophic interactions could influence the evolution of prey defences. We consider how predation risk affects predators' optimal foraging strategies on aposematic prey, and explore the resultant impact this has on mimicry dynamics between unequally defended species. In addition, we also investigate how the potential energetic cost of metabolising a toxin can alter the benefits to eating toxic prey and thus impact on predators' foraging decisions. Our model predicts that both how predators perceive their own predation risk, and the cost of detoxification, can have significant, sometimes counterintuitive, effects on the foraging decisions of predators. For example, in some conditions predators should: (i) avoid prey they know to be undefended, (ii) eat more mildly toxic prey as detoxification costs increase, (iii) increase their intake of highly toxic prey as the abundance of undefended prey increases. These effects mean that the relationship between a mimic and its model can qualitatively depend on the density of alternative prey and the cost of metabolising toxins. In addition, these effects are mediated by the predators' own predation risk, which demonstrates that, higher trophic levels than previously considered can have fundamental impacts on interactions among aposematic prey species.

Quantifying camouflage: how to predict detectability from appearance.

BACKGROUND: Quantifying the conspicuousness of objects against particular backgrounds is key to understanding the evolution and adaptive value of animal coloration, and in designing effective camouflage. Quantifying detectability can reveal how colour patterns affect survival, how animals' appearances influence habitat preferences, and how receiver visual systems work. Advances in calibrated digital imaging are enabling the capture of objective visual information, but it remains unclear which methods are best for measuring detectability. Numerous descriptions and models of appearance have been used to infer the detectability of animals, but these models are rarely empirically validated or directly compared to one another. We compared the performance of human 'predators' to a bank of contemporary methods for quantifying the appearance of camouflaged prey. Background matching was assessed using several established methods, including sophisticated feature-based pattern analysis, granularity approaches and a range of luminance and contrast difference measures. Disruptive coloration is a further camouflage strategy where high contrast patterns disrupt they prey's tell-tale outline, making it more difficult to detect. Disruptive camouflage has been studied intensely over the past decade, yet defining and measuring it have proven far more problematic. We assessed how well existing disruptive coloration measures predicted capture times. Additionally, we developed a new method for measuring edge disruption based on an understanding of sensory processing and the way in which false edges are thought to interfere with animal outlines. RESULTS: Our novel measure of disruptive coloration was the best predictor of capture times overall, highlighting the importance of false edges in concealment over and above pattern or luminance matching. CONCLUSIONS: The efficacy of our new method for measuring disruptive camouflage together with its biological plausibility and computational efficiency represents a substantial advance in our understanding of the measurement, mechanism and definition of disruptive camouflage. Our study also provides the first test of the efficacy of many established methods for quantifying how conspicuous animals are against particular backgrounds. The validation of these methods opens up new lines of investigation surrounding the form and function of different types of camouflage, and may apply more broadly to the evolution of any visual signal.

Cognition and the evolution of camouflage.

Camouflage is one of the most widespread forms of anti-predator defence and prevents prey individuals from being detected or correctly recognized by would-be predators. Over the past decade, there has been a resurgence of interest in both the evolution of prey camouflage patterns, and in understanding animal cognition in a more ecological context. However, these fields rarely collide, and the role of cognition in the evolution of camouflage is poorly understood. Here, we review what we currently know about the role of both predator and prey cognition in the evolution of prey camouflage, outline why cognition may be an important selective pressure driving the evolution of camouflage and consider how studying the cognitive processes of animals may prove to be a useful tool to study the evolution of camouflage, and vice versa. In doing so, we highlight that we still have a lot to learn about the role of cognition in the evolution of camouflage and identify a number of avenues for future research.

Eyespots.

Skelhorn et al. introduce eyespots the circular markings resembling vertebrate eyes found on many animals.

Masquerade.

John Skelhorn introduces masquerade, a strategy of prey animals to resemble inanimate (and inedible) objects.

Body size affects the evolution of eyespots in caterpillars.

Many caterpillars have conspicuous eye-like markings, called eyespots. Despite recent work demonstrating the efficacy of eyespots in deterring predator attack, a fundamental question remains: Given their protective benefits, why have eyespots not evolved in more caterpillars? Using a phylogenetically controlled analysis of hawkmoth caterpillars, we show that eyespots are associated with large body size. This relationship could arise because (i) large prey are innately conspicuous; (ii) large prey are more profitable, and thus face stronger selection to evolve such defenses; and/or (iii) eyespots are more effective on large-bodied prey. To evaluate these hypotheses, we exposed small and large caterpillar models with and without eyespots in a 2 × 2 factorial design to avian predators in the field. Overall, eyespots increased prey mortality, but the effect was particularly marked in small prey, and eyespots decreased mortality of large prey in some microhabitats. We then exposed artificial prey to naïve domestic chicks in a laboratory setting following a 2 × 3 design (small or large size × no, small, or large eyespots). Predators attacked small prey with eyespots more quickly, but were more wary of large caterpillars with large eyespots than those without eyespots or with small eyespots. Taken together, these data suggest that eyespots are effective deterrents only when both prey and eyespots are large, and that innate aversion toward eyespots is conditional. We conclude that the distribution of eyespots in nature likely results from selection against eyespots in small caterpillars and selection for eyespots in large caterpillars (at least in some microhabitats).

Increased predation of nutrient-enriched aposematic prey.

Avian predators readily learn to associate the warning coloration of aposematic prey with the toxic effects of ingesting them, but they do not necessarily exclude aposematic prey from their diets. By eating aposematic prey 'educated' predators are thought to be trading-off the benefits of gaining nutrients with the costs of eating toxins. However, while we know that the toxin content of aposematic prey affects the foraging decisions made by avian predators, the extent to which the nutritional content of toxic prey affects predators' decisions to eat them remains to be tested. Here, we show that European starlings (Sturnus vulgaris) increase their intake of a toxic prey type when the nutritional content is artificially increased, and decrease their intake when nutritional enrichment is ceased. This clearly demonstrates that birds can detect the nutritional content of toxic prey by post-ingestive feedback, and use this information in their foraging decisions, raising new perspectives on the evolution of prey defences. Nutritional differences between individuals could result in equally toxic prey being unequally predated, and might explain why some species undergo ontogenetic shifts in defence strategies. Furthermore, the nutritional value of prey will likely have a significant impact on the evolutionary dynamics of mimicry systems.

Predators' decisions to eat defended prey depend on the size of undefended prey.

Predators that have learned to associate warning coloration with toxicity often continue to include aposematic prey in their diet in order to gain the nutrients and energy that they contain. As body size is widely reported to correlate with energetic content, we predicted that prey size would affect predators' decisions to eat aposematic prey. We used a well-established system of wild-caught European starlings, Sturnus vulgaris, foraging on mealworms, Tenebrio molitor, to test how the size of undefended (water-injected) and defended (quinine-injected) prey, on different coloured backgrounds, affected birds' decisions to eat defended prey. We found that birds ate fewer defended prey, and less quinine, when undefended prey were large compared with when they were small, but that the size of the defended prey had no effect on the numbers eaten. Consequently, we found no evidence that the mass of the defended prey or the overall mass of prey ingested affected the amount of toxin that a predator was willing to ingest, and instead the mass of undefended prey eaten was more important. This is a surprising finding, challenging the assumptions of state-dependent models of aposematism and mimicry, and highlighting the need to understand better the mechanisms of predator decision making. In addition, the birds did not learn to discriminate visually between defended and undefended prey based on size, but only on the basis of colour. This suggests that colour signals may be more salient to predators than size differences, allowing Batesian mimics to benefit from aposematic models even when they differ in size.