Camouflage in predators

Camouflage – adaptations that prevent detection and/or recognition – is a key example of evolution by natural selection, making it a primary focus in evolutionary ecology and animal behaviour. Most work has focused on camouflage as an anti‐predator adaptation. However, predators also display specific colours, patterns and behaviours that reduce visual detection or recognition to facilitate predation. To date, very little attention has been given to predatory camouflage strategies. Although many of the same principles of camouflage studied in prey translate to predators, differences between the two groups (in motility, relative size, and control over the time and place of predation attempts) may alter selection pressures for certain visual and behavioural traits. This makes many predatory camouflage techniques unique and rarely documented. Recently, new technologies have emerged that provide a greater opportunity to carry out research on natural predator–prey interactions. Here we review work on the camouflage strategies used by pursuit and ambush predators to evade detection and recognition by prey, as well as looking at how work on prey camouflage can be applied to predators in order to understand how and why specific predatory camouflage strategies may have evolved. We highlight that a shift is needed in camouflage research focus, as this field has comparatively neglected camouflage in predators, and offer suggestions for future work that would help to improve our understanding of camouflage.     

The multiple disguises of spiders: web colour and decorations, body colour and movement

Diverse functions have been assigned to the visual appearance of webs, spiders and web decorations, including prey attraction, predator deterrence and camouflage. Here, we review the pertinent literature, focusing on potential camouflage and mimicry. Webs are often difficult to detect in a heterogeneous visual environment. Static and dynamic web distortions are used to escape visual detection by prey, although particular silk may also attract prey. Recent work using physiological models of vision taking into account visual environments rarely supports the hypothesis of spider camouflage by decorations, but most often the prey attraction and predator confusion hypotheses. Similarly, visual modelling shows that spider coloration is effective in attracting prey but not in conveying camouflage. Camouflage through colour change might be used by particular crab spiders to hide from predator or prey on flowers of different coloration. However, results obtained on a non-cryptic crab spider suggest that an alternative function of pigmentation may be to avoid UV photodamage through the transparent cuticle. Numerous species are clearly efficient locomotory mimics of ants, particularly in the eyes of their predators. We close our paper by highlighting gaps in our knowledge.     

Constrained camouflage facilitates the evolution of conspicuous warning coloration

The initial evolution of aposematic and mimetic antipredator signals is thought to be paradoxical because such coloration is expected to increase the risk of predation before reaching a stage when predators associate it effectively with a defense. We propose, however, that constraints associated with the alternative strategy, cryptic coloration, may facilitate the evolution of antipredator signals and thus provide a solution for the apparent paradox. We tested this hypothesis first using an evolutionary simulation to study the effect of a constraint due to habitat heterogeneity, and second using a phylogenetic comparison of the Lepidoptera to investigate the effect of a constraint due to prey motility. In the evolutionary simulation, antipredator warning coloration had an increased probability to invade the prey population when the evolution of camouflage was constrained by visual difference between microhabitats. The comparative study was done between day-active lepidopteran taxa, in which camouflage is constrained by motility, and night-active taxa, which rest during the day and are thus able to rely on camouflage. We compared each of seven phylogenetically independent day-active groups with a closely related nocturnal group and found that antipredator signals have evolved at least once in all the diurnal groups but in none of their nocturnal matches. Both studies lend support to our idea that constraints on crypsis may favor the evolution of antipredator warning signals.     

Visual background complexity facilitates the evolution of camouflage

Abstract.— Cryptic animal coloration or camouflage is an adaptation that decreases the risk of detection. The study of the evolution of camouflage has strongly emphasized the minimization of visual information that predators receive from prey, by means of background matching. However, the evolutionary effects of information processing after its reception have been virtually ignored. I constructed a model that employs an artificial neural network and simulates the evolution of prey coloration in a visually complex and simple habitat. The model suggests: (1) the difficulty of a detection task is related to the visual complexity of the habitat; (2) it is easier to decrease the risk of detection by the means of camouflage in a visually complex habitat; (3) selection on camouflage can exploit limitations in predators information processing; and (4) there are shortcomings in using the degree of background matching as the measure of camouflage.     

Artificial neural networks and the study of evolution of prey coloration

In this paper, I investigate the use of artificial neural networks in the study of prey coloration. I briefly review the anti-predator functions of prey coloration and describe both in general terms and with help of two studies as specific examples the use of neural network models in the research on prey coloration. The first example investigates the effect of visual complexity of background on evolution of camouflage. The second example deals with the evolutionary choice of defence strategy, crypsis or aposematism. I conclude that visual information processing by predators is central in evolution of prey coloration. Therefore, the capability to process patterns as well as to imitate aspects of predator's information processing and responses to visual information makes neural networks a well-suited modelling approach for the study of prey coloration. In addition, their suitability for evolutionary simulations is an advantage when complex or dynamic interactions are modelled. Since not all behaviours of neural network models are necessarily biologically relevant, it is important to validate a neural network model with empirical data. Bringing together knowledge about neural networks with knowledge about topics of prey coloration would provide a potential way to deepen our understanding of the specific appearances of prey coloration.     

Chromaticity in the UV/blue range facilitates the search for achromatically background-matching prey in birds

A large variety of predatory species rely on their visual abilities to locate their prey. However, the search for prey may be hampered by prey camouflage. The most prominent example of concealing coloration is background-matching prey coloration characterized by a strong visual resemblance of prey to the background. Even though this principle of camouflage was recognized to efficiently work in predator avoidance a long time ago, the underlying mechanisms are not very well known. In this study, we assessed whether blue tits (Cyanistes caeruleus) use chromatic cues in the search for prey. We used two prey types that were achromatically identical but differed in chromatic properties in the UV/blue range and presented them on two achromatically identical backgrounds. The backgrounds had either the same chromatic properties as the prey items (matching combination) or differed in their chromatic properties (mismatching combination). Our results show that birds use chromatic cues in the search for mismatching prey, whereupon chromatic contrast leads to a ‘pop-out’ of the prey item from the background. When prey was presented on a matching background, search times were significantly higher. Interestingly, search for more chromatic prey on the matching background was easier than search for less chromatic prey on the matching background. Our results indicate that birds use both achromatic and chromatic cues when searching for prey, and that the combination of both cues might be helpful in the search task.     

Disruptive coloration provides camouflage independent of background matching

Natural selection shapes the evolution of anti-predator defences, such as camouflage. It is currently contentious whether crypsis and disruptive coloration are alternative mechanisms of camouflage or whether they are interrelated anti-predator defences. Disruptively coloured prey is characterized by highly contrasting patterns to conceal the body shape, whereas cryptic prey minimizes the contrasts to background. Determining bird predation of artificial moths, we found that moths which were dissimilar from the background but sported disruptive patterns on the edge of their wings survived better in heterogeneous habitats than did moths with the same patterns inside of the wings and better than cryptic moths. Despite lower contrasts to background, crypsis did not provide fitness benefits over disruptive coloration on the body outline. We conclude that disruptive coloration on the edge camouflages its bearer independent of background matching. We suggest that this result is explainable because disruptive coloration is effective by exploiting predators' cognitive mechanisms of prey recognition and not their sensory mechanisms of signal detection. Relative to disruptive patterns on the body outline, disruptive markings on the body interior are less effective. Camouflage owing to disruptive coloration on the body interior is background-specific and is as effective as crypsis in heterogeneous habitats. Hence, we hypothesize that two proximate mechanisms explain the diversity of visual anti-predator defences. First, disruptive coloration on the body outline provides camouflage independent of the background. Second, background matching and disruptive coloration on the body interior provide camouflage, but their protection is background-specific.     

Dazzle camouflage affects speed perception

Movement is the enemy of camouflage: most attempts at concealment are disrupted by motion of the target. Faced with this problem, navies in both World Wars in the twentieth century painted their warships with high contrast geometric patterns: so-called "dazzle camouflage". Rather than attempting to hide individual units, it was claimed that this patterning would disrupt the perception of their range, heading, size, shape and speed, and hence reduce losses from, in particular, torpedo attacks by submarines. Similar arguments had been advanced earlier for biological camouflage. Whilst there are good reasons to believe that most of these perceptual distortions may have occurred, there is no evidence for the last claim: changing perceived speed. Here we show that dazzle patterns can distort speed perception, and that this effect is greatest at high speeds. The effect should obtain in predators launching ballistic attacks against rapidly moving prey, or modern, low-tech battlefields where handheld weapons are fired from short ranges against moving vehicles. In the latter case, we demonstrate that in a typical situation involving an RPG7 attack on a Land Rover the reduction in perceived speed is sufficient to make the grenade miss where it was aimed by about a metre, which could be the difference between survival or not for the occupants of the vehicle.     

Model of a predatory stealth behaviour camouflaging motion

A computational model of a stealth strategy inspired by the apparent mating tactics of male hoverflies is presented. The stealth strategy (motion camouflage) paradoxically allows a predator to approach a moving prey in such a way that it appears to be a stationary object. In the model, the predators are controlled by neural sensorimotor systems that base their decisions on realistic levels of input information. They are shown to be able to employ motion camouflage to approach prey that move along both real hoverfly flight paths and artificially generated flight paths. The camouflaged approaches made demonstrate that the control systems have an ability to predict future prey movements. This is illustrated using two- and three-dimensional simulations.     

Animal camouflage: compromise or specialize in a 2 patch-type environment?

Many animals possess camouflage markings that reduce the riskof detection by visually hunting predators. A key aspect ofcamouflage involves mimicking the background against which theanimal is viewed. However, most animals experience a wide varietyof backgrounds and cannot change their external appearance tomatch each selectively. We investigate whether such animalsshould adopt camouflage specialized with respect to one backgroundor adopt a compromise between the attributes of multiple backgrounds.We do this using a model consisting of predators that hunt preyin patches of 2 different types, where prey adopt the camouflagethat minimizes individual risk of predation. We show that theoptimal strategy of the prey is affected by a number of factors,including the relative frequencies of the patch types, the traveltime of predators between patches, the mean prey number in eachpatch type, and the trade-off function between the levels ofcrypsis in the patch types. We find evidence that both specialistand compromise strategies of prey camouflage are favored underdifferent model parameters, indicating that optimal concealmentmay not be as straightforward as previously thought.     

Red trap colour of the carnivorous plant Drosera rotundifolia does not serve a prey attraction or camouflage function

The traps of many carnivorous plants are red in colour. This has been widely hypothesized to serve a prey attraction function; colour has also been hypothesized to function as camouflage, preventing prey avoidance. We tested these two hypotheses in situ for the carnivorous plant Drosera rotundifolia. We conducted three separate studies: (i) prey attraction to artificial traps to isolate the influence of colour; (ii) prey attraction to artificial traps on artificial backgrounds to control the degree of contrast and (iii) observation of prey capture by D. rotundifolia to determine the effects of colour on prey capture. Prey were not attracted to green traps and were deterred from red traps. There was no evidence that camouflaged traps caught more prey. For D. rotundifolia, there was a relationship between trap colour and prey capture. However, trap colour may be confounded with other leaf traits. Thus, we conclude that for D. rotundifolia, red trap colour does not serve a prey attraction or camouflage function.     

Testing Thayer's hypothesis: can camouflage work by distraction?

One of the oldest theories of animal camouflage predicts that apparently conspicuous markings enhance concealment. Such 'distraction' marks are hypothesized to work by drawing the viewer's attention away from salient features, such as the body outline, that would otherwise reveal the animal. If distraction marks enhance concealment, then they offer a route for animals to combine camouflage markings with conspicuous signalling strategies, such as warning signals. However, the theory has never been tested and remains controversial. By using camouflaged artificial prey presented to wild avian predators, we test whether distractive markings enhance concealment. In contrast to predictions, we find that markings, both circular and irregular shapes, increase predation compared with unmarked targets. Markings became increasingly costly as their contrast against the prey increased. Our experiments failed to find any empirical support for the hypothesis that distraction markings are an important aspect of camouflage in animals.     

What Enables Size-Selective Trophy Hunting of Wildlife?

Although rarely considered predators, wildlife hunters can function as important ecological and evolutionary agents. In part, their influence relates to targeting of large reproductive adults within prey populations. Despite known impacts of size-selective harvests, however, we know little about what enables hunters to kill these older, rarer, and presumably more wary individuals. In other mammalian predators, predatory performance varies with knowledge and physical condition, which accumulates and declines, respectively, with age. Moreover, some species evolved camouflage as a physical trait to aid in predatory performance. In this work, we tested whether knowledge-based faculty (use of a hunting guide with accumulated experience in specific areas), physical traits (relative body mass [RBM] and camouflage clothing), and age can predict predatory performance. We measured performance as do many hunters: size of killed cervid prey, using the number of antler tines as a proxy. Examining ∼4300 online photographs of hunters posing with carcasses, we found that only the presence of guides increased the odds of killing larger prey. Accounting for this effect, modest evidence suggested that unguided hunters presumably handicapped with the highest RBM actually had greater odds of killing large prey. There was no association with hunter age, perhaps because of our coarse measure (presence of grey hair) and the performance trade-offs between knowledge accumulation and physical deterioration with age. Despite its prevalence among sampled hunters (80%), camouflage had no influence on size of killed prey. Should these patterns be representative of other areas and prey, and our interpretations correct, evolutionarily-enlightened harvest management might benefit from regulatory scrutiny on guided hunting. More broadly, we suggest that by being nutritionally and demographically de-coupled from prey and aided by efficient killing technology and road access, wildlife hunters in the developed world might have overcome many of the physical, but not knowledge-based, challenges of hunting.     

Specific color sensitivities of prey and predator explain camouflage in different visual systems

In situations of aggressive mimicry, predators adapt their colorto that of the substrate on which they sit for hunting, a behaviorthat is presumed to hide them from prey as well as from theirown predators. Females of few crab-spider species encountersuch situations when lying on flowers to ambush pollinators.To evaluate the efficiency of spider camouflage on flowers,we measured by spectroradiometry adult female Thomisus onustusand marguerite daisies, Leucanthemum vulgare. We compared chromaticcontrast (color used for short-range detection) of each pairof spider and flower to detection thresholds computed in thevisual systems of both Hymenopteran prey and passerine birdpredator. We also computed achromatic contrast (brightness)used for long-range detection. In both visual systems, eachindividual spider was efficiently matching the precise colorof the flower center on which it was hunting. Being significantlydarker than flowers, crab-spiders could in theory be detectedat long range by either predator or prey using achromatic contrast.However, long-range detection is unlikely, owing to small spidersize. Spiders also generated significant chromatic and achromaticcontrasts to both Hymenoptera and bird when moving on flowerperiphery. Our study is the first to identify which photoreceptorsof both prey and predator are involved in camouflage. The analysissuggests more research on bird predation and vision to determineto which extent bird predators effectively constrain spidercrypsis.     

Influence of a dorsal trash-package on interactions between larvae of Mallada signata (Schneider) (Neuroptera: Chrysopidae)

Abstract Larvae of the native Australian chrysopid Mallada signata use discarded prey items and environmental debris ('trash'), carried on the dorsal abdominal segments, as camouflage. Larvae that carry trash were confirmed experimentally to experience lower rates of cannibalism, an effect attributed to the camouflage conferred by the package. Larvae preferred physically hard material over normal dietary items when constructing their trash-package. The inclusion of these materials in the package may provide both physical and chemical camouflage from predator and prey alike. When encounter rates between conspecifics were low, larvae that carried trash increased their activity rates as they aged. In contrast, trash-denuded larvae decreased activity rates as they aged. Among first-instar larvae, as the density of larvae increased and encounters became more frequent, those with trash moved further than those without. Larvae with trash packages exhibited lower cannibalism and higher activity rates, which may subsequently enhance foraging capacity.     

Comparative and experimental studies on the relationship between body size and countershading in caterpillars

Countershading is a gradient of colouration in which the illuminated dorsal surfaces are darker than the unilluminated ventral surface. It is widespread in the animal kingdom and endows the body with a more uniform colour to decrease the chance of detection by predators. Although recent empirical studies support the theory of survival advantage conferred by countershading, this camouflage strategy has evolved only in some of the cryptic animals, and our understanding of the factors that affect the evolution of countershading is limited. This study examined the association between body size and countershading using lepidopteran larvae (caterpillars) as a model system. Specifically, we predicted that countershading may have selectively evolved in large-sized species among cryptic caterpillars if (1) large size constrains camouflage which facilitates the evolution of a trait reinforcing their crypsis and (2) the survival advantage of countershading is size-dependent. Phylogenetic analyses of four different lepidopteran families (Saturniidae, Sphingidae, Erebidae, and Geometridae) suggest equivocal results: countershading was more likely to be found in larger species in Saturniidae but not in the other families. The field predation experiment assuming avian predators did not support size-dependent predation in countershaded prey. Collectively, we found only weak evidence that body size is associated with countershading in caterpillars. Our results suggest that body size is not a universal factor that has shaped the interspecific variation in countershading observed in caterpillars.     

Contemporary evolution and genetic change of prey as a response to predator removal

The ecological effects of predator removal and its consequence on prey behavior have been investigated widely; however, predator removal can also cause contemporary evolution of prey resulting in prey genetic change. Here we tested the role of predator removal on the contemporary evolution of prey traits such as movement, reproduction and foraging. We use EcoSim simulation which allows complex intra- and inter-specific interactions, based on individual evolving behavioral models, as well as complex predator–prey dynamics and coevolution in spatially homogenous and heterogeneous worlds. We model organisms' behavior using fuzzy cognitive maps (FCM) that are coded in their genomes which has a clear semantics making reasoning about causality of any evolved behavior possible. We show that the contemporary evolution of prey behavior owing to predator removal is also accompanied by prey genetic change. We employed machine learning methods, now recognized as holding great promise for the advancement of our understanding and prediction of ecological phenomena. A classification algorithm was used to demonstrate the difference between genomes belonging to prey coevolving with predators and prey evolving in the absence of predation pressure. We argue that predator introductions to naive prey might be destabilizing if prey have evolved and adapted to the absence of predators. Our results suggest that both predator introductions and predator removal from an ecosystem have widespread effects on the survival and evolution of prey by altering their genomes and behavior, even after relatively short time intervals. Our study highlights the need to consider both ecological and evolutionary time scales, as well as the complex interplay of behaviors between trophic levels, in determining the outcomes of predator–prey interactions.     

Concealed by conspicuousness: distractive prey markings and backgrounds

High-contrast markings, called distractive or dazzle markings, have been suggested to draw and hold the attention of a viewer, thus hindering detection or recognition of revealing prey characteristics, such as the body outline. We tested this hypothesis in a predation experiment with blue tits (Cyanistes caeruleus) and artificial prey. We also tested whether this idea can be extrapolated to the background appearance and whether high-contrast markings in the background would improve prey concealment. We compared search times for a high-contrast range prey (HC-P) and a low-contrast range prey (LC-P) in a high-contrast range background (HC-B) and a low-contrast range background (LC-B). The HC-P was more difficult to detect in both backgrounds, although it did not match the LC-B. Also, both prey types were more difficult to find in the HC-B than in the LC-B, in spite of the mismatch of the LC-P. In addition, the HC-P was more difficult to detect, in both backgrounds, when compared with a generalist prey, not mismatching either background. Thus, we conclude that distractive prey pattern markings and selection of microhabitats with distractive features may provide an effective way to improve camouflage. Importantly, high-contrast markings, both as part of the prey coloration and in the background, can indeed increase prey concealment.     

Predator perception of detritus and eggsac decorations spun by orb-web spiders Cyclosa octotuberculata: Do they function to camouflage the sniders?

Camouflage is one of the most widespread and powerful strategies that animals use to make detection/recognition more difficult. Many orb-web spiders of the genus Cyclosa add prey remains, plant debris, moults, and/or eggsacs to their webs called web decorations. Web decorations resembling spider body colour pattern have been considered to camouflage the spider from predators. While this camouflage is obvious from a human's perspective, it has rarely been investigated from a predator's perspective. In this study, we tested the visibility of web decorations by calculating chromatic and achromatic contrasts of detritus and eggsac decorations built by Cyclosa octotuberculata, against four different backgrounds viewed by both bird (e.g., blue tits) and hymenopteran (e.g. Wasps) predators. We showed that both juvenile and adult spiders on webs with detritus or egg-sac deco-rations were undetectable by both hymenopteran and bird predators over short and long distances. Our results thus suggest that decorating webs with detritus or eggsacs by C. Octotuberculata may camouflage the spiders from both hymenopteran and bird predators in their common habitats.     

Dazzle coloration and prey movement

Many traits in animals reduce the rate of attack from visually hunting predators, including camouflage, warning signals and mimicry. In addition, some animal markings may reduce the likelihood that an attack ends in successful capture. These might include dazzle markings, high-contrast patterns that make the estimation of speed and trajectory difficult. However, until now, no study has experimentally tested whether some markings may achieve such an effect. We developed a computer 'game' where human 'predators' have to capture computer-generated prey moving across a background. In two experiments, we find that although uniform camouflaged targets were among the hardest to capture, so were a range of high-contrast conspicuous patterns, such as bands and zigzags. Prey were also more difficult to capture against more heterogeneous than uniform backgrounds, and at faster speeds of movement. As such, we find the first experimental evidence that conspicuous patterns, similar to those found in a wide range of real animals, make the capture of moving prey more challenging. Various anti-predator markings may work prey during motion, and some animals may combine such dazzle patterns with other functions, such as camouflage, thermoregulation, sexual and warning signals.