Asymmetry in size, shape, and color impairs the protective value of conspicuous color patterns

The received view of protective coloration in animals is thatconspicuous colors and patterns have evolved because they elicitavoidance behavior in potential predators. In the present study,we examine the spontaneous response of naive predators (Gallusgallus domesticus) to artificial prey to test the hypothesisthat deviations from bilateral symmetry of signaling patternelements may negatively influence the avoidance-inducing effectof conspicuous color patterns. Chicks displayed stronger aversionsto artificial "butterfly" prey items possessing symmetric colorpattern elements than to those possessing asymmetric signalswith pattern elements of different color or shape. Althoughthey attacked signals with a size asymmetry of 5% at the samerate as symmetric signals, signals with a size asymmetry of7.5% or more were attacked more often than were symmetric signals.These results suggest that the protective value of conspicuouscolor patterns is impaired by asymmetry in color, shape, andsize of color pattern elements. Our findings also argue againstthe notion that animals have inherent preferences for symmetricover asymmetric objects, and demonstrate the existence of athreshold for asymmetry detection, beyond which further incrementsin asymmetry have no influence on signal efficacy.     

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.     

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.     

Do bovids evolve hindquarter markings for anti-predation?

Conspicuous coloration in animals serves many functions such as anti-predation. Anti-predation strategies include motion dazzle and flash behavior. Motion dazzle markings can reduce the probability of being preyed on because the predators misjudge their movement. In flash behavior, prey demonstrate conspicuous cue while fleeing; the predators follow them; however, the prey hide their markings and the predators assume that the prey has vanished. To investigate whether bovids use conspicuous hindquarter markings as an anti-predatory behavior, we undertook phylogenetically controlled analyses to explore under what physiological characteristics and environmental factors bovids might have this color pattern. The results suggested that rump patches and tail markings were more prevalent in bovids living in larger-sized groups, which supports the hypothesis of intraspecific communication. Moreover, we observed the occurrence of conspicuous white hindquarter markings in bovids having smaller body size and living in larger groups, suggesting a motion dazzle function. However, the feature of facultative exposing color patterns (flash markings) was not associated with body size, which was inconsistent with predictions and implied that bovids may not adopt this as an anti-predator strategy. It was concluded that species in bovids with conspicuous white hindquarter markings adopt motion dazzle as an anti-predation strategy while fleeing and escaping from being prey on.     

Individuals from different-looking animal species may group together to confuse shared predators: simulations with artificial neural networks

Individuals of many quite distantly related animal species find each other attractive and stay together for long periods in groups. We present a mechanism for mixed-species grouping in which individuals from different-looking prey species come together because the appearance of the mixed-species group is visually confusing to shared predators. Using an artificial neural network model of retinotopic mapping in predators, we train networks on random projections of single- and mixed-species prey groups and then test the ability of networks to reconstruct individual prey items from mixed-species groups in a retinotopic map. Over the majority of parameter space, cryptic prey items benefit from association with conspicuous prey because this particular visual combination worsens predator targeting of cryptic individuals. However, this benefit is not mutual as conspicuous prey tends to be targeted most poorly when in same-species groups. Many real mixed-species groups show the asymmetry in willingness to initiate and maintain the relationship predicted by our study. The agreement of model predictions with published empirical work, the efficacy of our modelling approach in previous studies, and the taxonomic ubiquity of retinotopic maps indicate that we may have uncovered an important, generic selective agent in the evolution of mixed-species grouping.     

The function of animal ‘eyespots’:Conspicuousness but not eye mimicry is key

Many animals are marked with conspicuous circular features often called 'eyespots',which intimidate predators,preventing or halting an attack.It has long been assumed that eyespots work by mimicking the eyes of larger animals,but recent experiments have indicated that conspicuousness and contrast is important in eyespot function,and not eye mimicry.We undertake two further experiments to distinguish between the conspicuousness and mimicry hypotheses,by using artificial prey presented to wild avian predators...     

Empirical tests of the role of disruptive coloration in reducing detectability

Disruptive patterning is a potentially universal camouflage technique that is thought to enhance concealment by rendering the detection of body shapes more difficult. In a recent series of field experiments, artificial moths with markings that extended to the edges of their 'wings' survived at higher rates than moths with the same edge patterns inwardly displaced. While this result seemingly indicates a benefit to obscuring edges, it is possible that the higher density markings of the inwardly displaced patterns concomitantly reduced their extent of background matching. Likewise, it has been suggested that the mealworm baits placed on the artificial moths could have created differential contrasts with different moth patterns. To address these concerns, we conducted controlled trials in which human subjects searched for computer-generated moth images presented against images of oak trees. Moths with edge-extended disruptive markings survived at higher rates, and took longer to find, than all other moth types, whether presented sequentially or simultaneously. However, moths with no edge markings and reduced interior pattern density survived better than their high-density counterparts, indicating that background matching may have played a so-far unrecognized role in the earlier experiments. Our disruptively patterned non-background-matching moths also had the lowest overall survivorship, indicating that disruptive coloration alone may not provide significant protection from predators. Collectively, our results provide independent support for the survival value of disruptive markings and demonstrate that there are common features in human and avian perception of camouflage.     

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

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.     

Perspective: the evolution of warning coloration is not paradoxical

Animals that are brightly colored have intrigued scientists since the time of Darwin, because it seems surprising that prey should have evolved to be clearly visible to predators. Often this self-advertisement is explained by the prey being unprofitable in some way, with the conspicuous warning coloration helping to protect the prey because it signals to potential predators that the prey is unprofitable. However, such signals only work in this way once predators have learned to associate the conspicuous color with the unprofitability of the prey. The evolution of warning coloration is still widely considered to be a paradox, because it has traditionally been assumed that the very first brightly colored individuals would be at an immediate selective disadvantage because of their greater conspicuousness to predators that are naive to the meaning of the signal. As a result, it has been difficult to understand how a novel conspicuous color morph could ever avoid extinction for long enough for predators to become educated about the signal. Thus, the traditional view that the evolution of warning coloration is difficult to explain rests entirely on assumptions about the foraging behavior of predators. However, we review recent evidence from a range of studies of predator foraging decisions, which refute these established assumptions. These studies show that: (1) Many predators are so conservative in their food preferences that even very conspicuous novel prey morphs are not necessarily at a selective disadvantage. (2) The survival and spread of novel color morphs can be simulated in field and aviary experiments using real predators (birds) foraging on successive generations of artificial prey populations. This work demonstrates that the foraging preferences of predators can regularly (though not always) result in the increase to fixation of a novel morph appearing in a population of familiar-colored prey. Such fixation events occur even if both novel and familiar prey are fully palatable and despite the novel food being much more conspicuous than the familiar prey. These studies therefore provide strong empirical evidence that conspicuous coloration can evolve readily, and repeatedly, as a result of the conservative foraging decisions of predators.     

Sensory-based niche partitioning in a multiple predator–multiple prey community

Many predators and parasites eavesdrop on the communication signals of their prey. Eavesdropping is typically studied as dyadic predator–prey species interactions; yet in nature, most predators target multiple prey species and most prey must evade multiple predator species. The impact of predator communities on prey signal evolution is not well understood. Predators could converge in their preferences for conspicuous signal properties, generating competition among predators and natural selection on particular prey signal features. Alternatively, predator species could vary in their preferences for prey signal properties, resulting in sensory-based niche partitioning of prey resources. In the Neotropics, many substrate-gleaning bats use the mate-attraction songs of male katydids to locate them as prey. We studied mechanisms of niche partitioning in four substrate-gleaning bat species and found they are similar in morphology, echolocation signal design and prey-handling ability, but each species preferred different acoustic features of male song in 12 sympatric katydid species. This divergence in predator preference probably contributes to the coexistence of many substrate-gleaning bat species in the Neotropics, and the substantial diversity in the mate-attraction signals of katydids. Our results provide insight into how multiple eavesdropping predator species might influence prey signal evolution through sensory-based niche partitioning.     

Does avian conspicuous colouration increase or reduce predation risk?

Animals often announce their unprofitability to predators through conspicuous coloured signals. Here we tested whether the apparently conspicuous colour designs of the four European Coraciiformes and Upupiformes species may have evolved as aposematic signals, or whether instead they imply a cost in terms of predation risk. Because previous studies suggested that these species are unpalatable, we hypothesized that predators could avoid targeting them based on their colours. An experiment was performed where two artificial models of each bird species were exposed simultaneously to raptor predators, one painted so as to resemble the real colour design of these birds, and the other one painted using cryptic colours. Additionally, we used field data on the black kite’s diet to compare the selection of these four species to that of other avian prey. Conspicuous models were attacked in equal or higher proportions than their cryptic counterparts, and the attack rate on the four species increased with their respective degree of contrast against natural backgrounds. The analysis of the predator’s diet revealed that the two least attacked species were negatively selected in nature despite their abundance. Both conspicuous and cryptic models of one of the studied species (the hoopoe) received fewer attacks than cryptic models of the other three species, suggesting that predators may avoid this species for characteristics other than colour. Globally, our results suggest that the colour of coraciiforms and upupiforms does not function as an aposematic signal that advises predators of their unprofitability, but also that conspicuous colours may increase predation risk in some species, supporting thus the handicap hypothesis.     

Flower Symmetry Preferences in Honeybees and their Crab Spider Predators

Flowers exhibit symmetrical patterns, and innate preferences for symmetry in pollinators like honeybees are documented. Most previous studies of symmetry preferences in honeybees, Apis mellifera, tested levels of asymmetry using artificial flowers or stimuli. Here we investigated the effect of flower asymmetry on flower preferences of honeybees in a novel approach using real flowers, incorporating their spectral properties and how the receivers process the visual signals. Importantly, we also tested the response of an ‘eavesdropping’ predator, the crab spider Thomisus spectabilis, that also utilizes the same flower to prey on honeybees. Flowers (Chrysanthemum frutescens) were manipulated to contain asymmetrical and symmetrical patterns, excluding olfactory cues. Both crab spiders and honeybees exhibited a significant preference for symmetrical flowers. Moreover, honeybees exhibited a significant preference for radial symmetry over bilateral symmetry, but no corresponding effect was recorded in crab spiders. Further analyses demonstrated that flower reflectance and orientation of the axis of symmetry did not affect crab spider decisions. Field observations on T. spectabilis revealed that the natural variation in C. frutescens symmetry had no effect on the choice of crab spiders. This indicates that spiders and honeybees may use other flower characteristics, for example, olfactory cues, together with flower symmetry, to make their foraging decisions.     

The coevolution of warning signals

It has long been recognized that defended prey tend to be conspicuous. Current theories suggest that the association ('aposematism') has arisen because predators more readily learn to avoid attacking defended phenotypes when they are conspicuous. In this paper, I consider why such psychology has evolved. In particular, I argue that aposematism may have evolved not because of an independent and pre-existing receiver bias, but because the conspicuousness of a prey item provides a reliable indicator of its likelihood of being defended. To develop my case I consider how warning signals might coevolve in a system containing a number of predators, whose foraging behaviour is also subject to selection. In these cases, models readily show that the greater the conspicuousness of a novel prey item, the more likely that it has been encountered by other predators and survived. As a consequence, naive predators should be less likely to attack highly conspicuous novel prey on encounter, or at least more inclined to attack them cautiously. This adaptive predator behaviour will greatly facilitate the spread of aposematic phenotypes from extreme rarity, which in turn will enhance selection for forms of predator behaviour under which aposematism will coevolve even more readily.     

Why are wasps so intimidating: field experiments on hunting dragonflies (Odonata: Aeshna grandis)

The mechanisms of aposematism (unprofitability of prey combined with a conspicuous signal) have mainly been studied with reference to vertebrate predators, especially birds. We investigated whether dragonflies, Aeshna grandis, avoid attacking wasps, Vespula norwegica, which are an unprofitable group of prey for most predators. As a control we used flies that were painted either black or with yellow and black stripes. The dragonflies showed greater aversion to wasps than to flies. Black-and-yellow-striped flies were avoided more than black ones, suggesting that aposematic coloration on a harmless fly provides a selective advantage against invertebrate predators. There was no significant difference in reactions to black-painted and black-and-yellow wasps, indicating that, in addition to coloration, some other feature in wasps might deter predators. In further experiments we offered dragonflies artificial prey items in which the candidate warning signals (coloration, odour and shape) were tested separately while other confounding factors were kept constant. The dragonflies avoided more black-and-yellow prey items than solid black or solid yellow ones. However, we found no influence of wasp odour on dragonfly hunting. Dragonflies were slightly, but not significantly, more reluctant to attack wasp-shaped prey items than fly-shaped ones. Our results suggest that the typical black-and-yellow stripes of wasps, possibly combined with their unique shape, make dragonflies avoid wasps. Since black-and-yellow stripes alone significantly decreased attack rate, we conclude that even profitable prey species (i.e. Batesian mimics) are able to exploit the dragonflies' avoidance of wasps. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Prey selection by wild birds can allow novel and conspicuous colour morphs to spread in prey populations

Conspicuous warning coloration helps to protect prey because it signals to potential predators that the prey is unprofitable. However, such signals only work once predators have come to associate the conspicuous colour with the unprofitability of the prey. The evolution of warning coloration is generally considered to be paradoxical, because it has traditionally been assumed that the first brightly coloured individuals would be at an immediate selective disadvantage because of their greater conspicuousness to predators that are naïve to the meaning of the signal. As a result, it has been difficult to understand how a novel conspicuous colour morph could ever avoid rapid extinction, and instead survive and spread in the population until predators have become educated about the signal. In the present study, we experimentally simulated the appearance of a single novel coloured mutant in small populations (20 individuals) of palatable artificial pastry "prey". The colour morph frequencies in each "generation" of prey (presented on successive days of a trial) were determined by the relative survival of the previous generation under predation by free-living birds. We found that the novel colour morphs regularly persisted and increased from a starting frequency of 1/20 to reach fixation (100%), despite being fully palatable, even when the novel morph was much more conspicuous against the background than the familiar morph. This was true for both green (not normally considered a warning colour) and red (a classic warning colour) novel morphs. Novel colours reached fixation significantly faster than could be accounted for by random drift, indicating differential predation in relation to prey colour by the birds. Our experiments show that the immediate demise of a fully palatable new prey morph is not an inevitable outcome of predator behaviour, because even very conspicuous prey can gain protection from conservative foragers, simply by being novel.     

Stabilimenta attract unwelcome predators to orb-webs

Conspicuous behaviour exposes animals to predation; prey-attraction thus often conflicts with antipredator behaviour. The fact that a conspicuous ultraviolet-light reflecting silken structure in the orb-webs of certain spider species, known as a stabilimentum, makes the webs obvious to both prey and predators has been used to argue that spiders benefit from building stabilimenta by attracting prey and/or defending against visually hunting predators. Here, we provide experimental evidence that stabilimenta can act as visual signals that attract web-invading spider-eating predators with acute vision to the webs. We also show that the predators can learn to remember a particular type of stabilimentum. Thus, stabilimentum-building spiders risk a high level of predation by attracting visually hunting predators.     

Pyrazine odour makes visually conspicuous prey aversive

Unpalatable insects frequently adopt multimodal signals to ward off predators, incorporating sounds and odours into their colourful displays. Pyrazine is an odour commonly used in insect warning displays, and has previously been shown to elicit unlearned biases against common warning colours, e.g. yellow and red in naive predators. We designed two experiments to test for similar effects of pyrazine on the conspicuousness of prey, perhaps the most ubiquitous aspect of aposematic coloration. In the first experiment, we offered predators (Gallus gallus domesticus) a choice between conspicuous crumbs and cryptic crumbs in the presence or absence of pyrazine. In the second experiment, we manipulated the birds' experience of conspicuous prey during an initial training phase. Only in the presence of pyrazine did birds show a bias against conspicuously coloured food, and this occurred whether or not they had previously experienced food that contrasted with the background. This emergent behaviour relied upon the visual and odorous signal components being presented together. These unlearned, yet hidden, responses against conspicuousness demonstrate that there are initial benefits to prey being conspicuous when the multimodal nature of warning signals is accounted for.     

Identifying the ecological conditions that select for intermediate levels of aposematic signalling

Chemically defended species often have conspicuous signals that warn potential predators of these defences. Recent evidence suggests that some such aposematic prey are not as conspicuous as possible, even though increased conspicuousness would bring additional anti-predator benefits. Here we present a simple model to explore the generality of these observations. Our model predicts that optimal fitness will often be achieved at an intermediate level of conspicuousness and not simply by maximising conspicuousness. This comes about because of the ubiquitous trade-off that increased conspicuousness has an ecological cost in increasing the encounter rate with predators, as well as a benefit in terms of enhancing learned aversion by predators of defended prey. However, importantly, we also predict that a small deviation away from maximal crypsis generally causes a decrease in fitness, even if a larger deviation would lead to an intermediate level of conspicuousness that maximises fitness. Hence, further consideration of whether intermediate levels of aposematism are as common in nature as predicted in this model will require consideration of the underlying evolution of appearance, and the plausibility of evolution across the fitness trough, from maximal crypsis to an intermediate level of aposematism.     

Does homozygosity contribute to the asymmetry of common white leg markings in the Arabian horse?

Common white and facial markings have a multifactorial mode of inheritance inEquus caballus and result from the absence of melanocytes in the unpigmented areas. Directional asymmetry and fluctuating asymmetry apparently account for the total asymmetry of common white leg markings. Using computerized records obtained from the Arabian Horse Registry of America, Inc., and the International Arabian Horse Association, studies were carried out to determine if homozygosity increases the total asymmetry in common white leg markings by presumably promoting fluctuating asymmetry. The results were as follows: (1) Arabian horses that are symmetrical and asymmetrical for common white leg markings have similar distributions of inbreeding coefficients; (2) Arabian and half-Arabian horses have similar concordance values, in general, for specific white markings in both their forelegs and hind legs. It is concluded that homozygosity does not contribute to the total asymmetry of common white leg markings in the Arabian horse.     

Conditions for the spread of conspicuous warning signals: a numerical model with novel insights

The initial evolution of conspicuous warning signals presents an evolutionary problem because selection against rare conspicuous signals is presumed to be strong, and new signals are rare when they first arise. Several possible solutions have been offered to solve this apparent evolutionary paradox, but disagreement persists over the plausibility of some of the proposed mechanisms. In this paper, we construct a deterministic numerical simulation model that allows us to derive the strength of selection on novel warning signals in a wide range of biologically relevant situations. We study the effects of predator psychology (learning, rate of mistaken attacks, and neophobia) on selection. We also study the how prey escape, predation intensity, number of predators, and abundance of different prey types affects selection. The model provides several important results. Selection on novel warning signals is number rather than frequency dependent. In most cases, there exists a threshold number of aposematic individuals below which aposematism is selected against and above which aposematism is selected for. Signal conspicuousness (which increases detection rate) and distinctiveness (which allows predator to distinguish defended from nondefended prey) have opposing effects on evolution of warning signals. A more conspicuous warning signal cannot evolve unless it makes the prey more distinctive from palatable prey, reducing mistaken attacks by predators. A novel warning signal that is learned quickly can spread from lower abundance more easily than a signal that is learned more slowly. However, the relative rate at which the resident signal and the novel signal are learned is irrelevant for the spread of the novel signal. Long-lasting neophobia can facilitate the spread of novel warning signals. Individual selection via the ability of defended prey to escape from predator is not likely to facilitate evolution of conspicuous warning signals if both the resident (cryptic) morph and the novel morph have the same escape probability. Predation intensity (defined as the proportion of palatable prey eaten by the predator) has a strong effect on selection. More intense predation results in strong selection against rare signals, but also strong selective advantage to common signals. The threshold number of aposematic individuals is lower when predation is intense. Thus, the evolution of warning signals may be more likely in environments where predation is intense. The effect of numbers of predators depends on whether predation intensity also changes. When predation intensity is constant, increasing numbers of predators raises the threshold number of aposematic individuals, and thus makes evolution of aposematism more difficult. If predation intensity increases in parallel with number of predators, the threshold number of aposematic individuals does not change much, but selection becomes more intense on both sides of the threshold.