Camouflage and colour change: antipredator responses to bird and snake predators across multiple populations in a dwarf chameleon

Potential prey are often exposed to multiple predators that vary in their foraging tactics and ability to detect prey. For animals that rely on crypsis to avoid predators, one solution is to alter their behaviour or appearance to maximize crypsis in ways that are specific to different types of predator. We tested whether dwarf chameleons ( Bradypodion transvaalense ) showed different behavioural responses, including colour change, towards multiple predators (bird and snake models) that detect and capture prey in different ways, and whether these antipredator responses varied geographically. Chameleons consistently used the same body postures (lateral compression and flipping to the opposite side of the branch) and displayed similar chromatic (colour) contrast against the natural background in response to both predator types. However, they became significantly more achromatically contrasting (brighter) in the presence of the snake compared to the bird. This relative difference in achromatic contrast towards the two types of predator was consistent among populations. There were also significant differences in both absolute achromatic and chromatic contrast among populations despite very similar light environment, background coloration and habitat structure. Our results highlight facultative crypsis as one type of flexible antipredator tactic and emphasize the importance of visual ecology in understanding prey–predator interactions.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 437–446.     

Evolution of color variation in dragon lizards: quantitative tests of the role of crypsis and local adaptation

Abstract Many animal species display striking color differences with respect to geographic location, sex, and body region. Traditional adaptive explanations for such complex patterns invoke an interaction between selection for conspicuous signals and natural selection for crypsis. Although there is now a substantial body of evidence supporting the role of sexual selection for signaling functions, quantitative studies of crypsis remain comparatively rare. Here, we combine objective measures of coloration with information on predator visual sensitivities to study the role of crypsis in the evolution of color variation in an Australian lizard species complex (Ctenophorus decresii). We apply a model that allows us to quantify crypsis in terms of the visual contrast of the lizards against their natural backgrounds, as perceived by potential avian predators. We then use these quantitative estimates of crypsis to answer the following questions. Are there significant differences in crypsis conspicuousness among populations? Are there significant differences in crypsis conspicuousness between the sexes? Are body regions “exposed” to visual predators more cryptic than “hidden” body regions? Is there evidence for local adaptation with respect to crypsis against different substrates? In general, our results confirmed that there are real differences in crypsis conspicuousness both between populations and between sexes; that exposed body regions were significantly more cryptic than hidden ones, particularly in females; and that females, but not males, are more cryptic against their own local background than against the background of other populations. Body regions that varied most in contrast between the sexes and between populations were also most conspicuous and are emphasized by males during social and sexual signaling. However, results varied with respect to the aspect of coloration studied. Results based on chromatic contrast (“hue’ of color) provided better support for the crypsis hypothesis than did results based on achromatic contrast (“brightness’ of color). Taken together, these results support the view that crypsis plays a substantial role in the evolution of color variation and that color patterns represent a balance between the need for conspicuousness for signaling and the need for crypsis to avoid predation.     

Aposematic coloration, luminance contrast, and the benefits of conspicuousness

Many organisms use warning, or aposematic, coloration to signaltheir unprofitability to potential predators. Aposematicallycolored prey are highly visually conspicuous. There is considerableempirical support that conspicuousness promotes the effectivenessof the aposematic signal. From these experiments, it is welldocumented that conspicuous, unprofitable prey are detectedsooner and aversion learned faster by the predator as comparedwith cryptic, unprofitable prey. Predators also retain memoryof the aversion longer when prey is conspicuous. The presentstudy focused on the elements of conspicuousness that conferthese benefits of aposematic coloration. Drawing on currentunderstanding of animal vision, we distinguish 2 features ofwarning coloration: high chromatic contrast and high brightness,or luminance, contrast. Previous investigations on aposematicsignal efficacy have focused mainly on the role of high chromaticcontrast between prey and background, whereas little researchhas investigated the role of high luminance contrast. Usingthe Chinese mantid as a model predator and gray-painted milkweedbugs as model prey, we found that increased prey luminance contrastincreased detection of prey, facilitated predator aversion learning,and increased predator memory retention of the aversive response.Our results suggest that the luminance contrast component ofaposematic coloration can be an effective warning signal betweenthe prey and predator. Thus, warning coloration can even evolveas an effective signal to color blind predators.     

Sexual dichromatism and differential conspicuousness in two populations of the common collared lizard (Crotaphytus collaris) from Utah and New Mexico, USA

The common collared lizard (Crotaphytus collaris) exhibits considerable geographical colour variation, particularly among males. Populations of this diurnal saxicolous iguanian inhabit patches of rocky habitat throughout the species’ broad distribution in North America and are anticipated to experience local differences in selective pressures that influence colouration. Specifically, while social interactions might favour conspicuous colouration, crypsis may be advantageous in interactions with visually orienting predator and prey species. To address the local relationship between lizard and substrate colouration we compared the reflectance spectra of two geographically distant and phenotypically divergent populations of collared lizards with the rocky substrates they inhabit. Our northern study population (C. c. auriceps in eastern Utah) occurs on red rocks, where males exhibit boldly coloured turquoise bodies and bright yellow heads. In contrast, our southern study population (C. c. fuscus in southern New Mexico) lives on grey and tan rocks, and males in this location exhibit subdued brown and tan dorsal colours. Spectral comparisons revealed that males in the northern population contrasted strongly with their local rocks, whereas males in the southern population matched their rock colours with reasonably good fidelity. This relationship held under a variety of lighting conditions. Females in both populations were less conspicuously coloured than males, although northern females contrasted more with their rocks than did southern females. In addition, sexual dichromatism was pronounced in the northern population but minimal in the southern population. Finally, sexual size and weight dimorphism was strong in the southern population while being virtually absent in the northern population. A comparison of the local predator and prey assemblages suggests that the conspicuous and sexually dichromatic colouration of the northern population may have evolved in response to reduced pressure from visually orienting predators as well as reduced dependence on saurian prey. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 77 , 67–85     

The interplay between multiple predators and prey colour divergence

Evolutionary divergence in the coloration of toxic prey is expected when geographic variation in predator composition and behavior favours shifts in prey conspicuousness. A fundamental prediction of predator‐driven colour divergence is that the local coloration should experience lower predation risk than novel prey phenotypes. The dorsal coloration of the granular poison frog varies gradually from populations of conspicuous bright red frogs to populations of dull green and relatively cryptic frogs. We conducted experiments with clay models in four populations to examine the geographic patterns of taxon‐specific predation. Birds avoided the local phenotype while lizards consistently selected for decreased conspicuousness and crab predation did not depend on frog coloration. Importantly, birds and lizards favoured low conspicuousness in populations where relatively cryptic green morphs have evolved. This study provides evidence for the interplay among distinct selective pressures, from multiple‐predator taxa, acting on the divergence in protective coloration of prey species. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 580–589.     

Colors of primate pelage and skin: objective assessment of conspicuousness

We present a quantitative means of assessing the conspicuousness of animal coats or other objects in terms of the color vision of each possible observer. We measured reflectance spectra from the fur and skin of many primate species in order to provide an objective survey of the possibilities of pelage coloration found in extant primates. We show that the orange coloration displayed by many platyrrhine and some strepsirhine primates, while being conspicuous to humans, would be cryptic amongst foliage to all males and many females of their own species. In relation to this finding, we briefly review what is known of the color vision of birds that prey on primates, and assess how conspicuous the orange pelage would be to these predators.     

Size and sex matter: reproductive biology and determinants of offspring survival in Gazella marica

For prey, many behavioural traits are constrained by the risk of predation. Therefore, shifts between warning and cryptic coloration have been suggested to result in parallel changes in several behaviours. In the present study, we tested whether changes in chromatic contrast among eight populations of the strawberry poison‐dart frog, Dendrobates pumilio, co‐vary with behaviour, as expected if selection is imposed by predators relying on visual detection of prey. These eight populations are geographically isolated on different island in the Bocas del Toro region of Panama and have recently diverged morphologically and genetically. We found that aggression and explorative behaviour were strongly correlated and also that males tended to be more aggressive and explorative if they belonged to populations with conspicuously coloured individuals. We discuss how evolutionary switches between predator avoidance strategies and associated behavioural divergence between populations may affect reproductive isolation. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ●● , ●●–●●.     

Local adaptation and divergence in colour signal conspicuousness between monomorphic and polymorphic lineages in a lizard

Population differences in visual environment can lead to divergence in multiple components of animal coloration including signalling traits and colour patterns important for camouflage. Divergence may reflect selection imposed by different receivers (conspecifics, predators), which depends in turn on the location of the colour patch. We tested for local adaptation of two genetically and phenotypically divergent lineages of a rock‐inhabiting lizard, Ctenophorus decresii, by comparing the visual contrast of colour patches to different receivers in native and non‐native environments. The lineages differ most notably in male throat coloration, which is polymorphic in the northern lineage and monomorphic in the southern lineage, but also differ in dorsal and lateral coloration, which is visible to both conspecifics and potential predators. Using models of animal colour vision, we assessed whether lineage‐specific throat, dorsal and lateral coloration enhanced conspicuousness to conspecifics, increased crypsis to birds or both, respectively, when viewed against the predominant backgrounds from each lineage. Throat colours were no more conspicuous against native than non‐native rock but contrasted more strongly with native lichen, which occurs patchily on rocks inhabited by C. decresii. Conversely, neck coloration (lateral) more closely matched native lichen. Furthermore, although dorsal coloration of southern males was consistently more conspicuous to birds than that of northern males, both lineages had similar absolute conspicuousness against their native backgrounds. Combined, our results are consistent with local adaptation of multiple colour traits in relation to multiple receivers, suggesting that geographic variation in background colour has influenced the evolution of lineage‐specific coloration in C. decresii.     

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.     

Conspicuousness,color resemblance,and toxicity in geographically diverging mimicry: The pan‐Amazonian frog Allobates femoralis

Predation risk is allegedly reduced in Batesian and Müllerian mimics, because their coloration resembles the conspicuous coloration of unpalatable prey. The efficacy of mimicry is thought to be affected by variation in the unpalatability of prey, the conspicuousness of the signals, and the visual system of predators that see them. Many frog species exhibit small colorful patches contrasting against an otherwise dark body. By measuring toxicity and color reflectance in a geographically variable frog species and the syntopic toxic species, we tested whether unpalatability was correlated with between‐species color resemblance and whether resemblance was highest for the most conspicuous components of coloration pattern. Heterospecific resemblance in colorful patches was highest between species at the same locality, but unrelated to concomitant variation in toxicity. Surprisingly, resemblance was lower for the conspicuous femoral patches compared to the inconspicuous dorsum. By building visual models, we further tested whether resemblance was affected by the visual system of model predators. As predicted, mimic‐model resemblance was higher under the visual system of simulated predators compared to no visual system at all. Our results indicate that femoral patches are aposematic signals and support a role of mimicry in driving phenotypic divergence or mimetic radiation between localities.     

The fitness consequences of the autotomous blue tail in lizards: an empirical test of predator response using clay models

Numerous vertebrates employ one or more autotomous body parts as an anti-predation mechanism. Many lizards possess an autotomous tail that is brightly colored blue, which has been suggested to either serve as a decoy mechanism to divert predator attention to the autotomous body part, as an interspecific signal, or as an aposematic signal to predators that it is distasteful or dangerous. While theoretical studies suggest that a conspicuous autotomous body part that increases the probability of escape while not increasing the rate of detection will be favorable over a completely cryptic form, there is little empirical evidence supporting the adaptive benefit of an autotomous blue tail. We used in situ clay models of a scincid lizard to test the fitness consequences of blue coloration. Lizard models with a dark base color and blue decoy coloration experienced no measurable difference in avian predation relative to an all-dark model, which suggests that blue coloration neither serves as an aposematic signal nor increases the conspicuousness of the lizard model. Despite statistically similar attack rates, avian attacks on models with blue coloration were indeed focused on body sections that were colored blue. Our results suggest that the blue tail in lizards serves as an effective decoy, and that avian predation has possibly played a role in the evolution of the blue tail.     

Variation in the Visual Habitat May Mediate the Maintenance of Color Polymorphism in a Poeciliid Fish

The conspicuousness of animal signals is influenced by their contrast against the background. As such, signal conspicuousness will tend to vary in nature because habitats are composed of a mosaic of backgrounds. Variation in attractiveness could result in variation in conspecific mate choice and risk of predation, which, in turn, may create opportunities for balancing selection to maintain distinct polymorphisms. We quantified male coloration, the absorbance spectrum of visual pigments and the photic environment of Poecilia parae, a fish species with five distinct male color morphs: a drab (i.e., grey), a striped, and three colorful (i.e., blue, red and yellow) morphs. Then, using physiological models, we assessed how male color patterns can be perceived in their natural visual habitats by conspecific females and a common cichlid predator, Aequidens tetramerus. Our estimates of chromatic and luminance contrasts suggest that the three most colorful morphs were consistently the most conspicuous across all habitats. However, variation in the visual background resulted in variation in which morph was the most conspicuous to females at each locality. Likewise, the most colorful morphs were the most conspicuous morphs to cichlid predators. If females are able to discriminate between conspicuous prospective mates and those preferred males are also more vulnerable to predation, variable visual habitats could influence the direction and strength of natural and sexual selection, thereby allowing for the persistence of color polymorphisms in natural environments.     

The detectability of the colour pattern in the aposematic firebug,Pyrrhocoris apterus: an image‐based experiment with human ‘predators’

Crypsis and aposematism are often regarded as two opposite protective strategies. However, there is large variation in prey appearance within both strategies. In this article, we investigated the conspicuousness of the aposematic red‐and‐black firebug, Pyrrhocoris apterus, by presenting images of natural and digitally manipulated phenotypes in their natural habitat on a computer screen to human ‘predators’, and comparing the detection times. We asked whether the natural colour pattern can be made more or less conspicuous by rearranging the spatial distribution of colour elements. Hence, we created a phenotype in which the black colour elements were moved to the body outline to test for a possible disruptive effect. In the ‘black’ and ‘red’ manipulations, we removed one of the two colours, creating two uniform colour variants. We found that some of our manipulations increased, but none reduced, the detection time significantly; this indicates that the naturally coloured firebug is highly conspicuous. The detection time varied among backgrounds and there was a significant relationship between detection time and chromatic similarity between the bug and the background for the natural and black phenotypes. Although background colour composition has an important effect on the signal, we argue that the coloration of P. apterus has evolved for high conspicuousness. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 806–816.     

An Analysis of Predator Selection to Affect Aposematic Coloration in a Poison Frog Species

Natural selection is widely noted to drive divergence of phenotypic traits. Predation pressure can facilitate morphological divergence, for example the evolution of both cryptic and conspicuous coloration in animals. In this context Dendrobatid frogs have been used to study evolutionary forces inducing diversity in protective coloration. The polytypic strawberry poison frog (Oophaga pumilio) shows strong divergence in aposematic coloration among populations. To investigate whether predation pressure is important for color divergence among populations of O. pumilio we selected four mainland populations and two island populations from Costa Rica and Panama. Spectrometric measurements of body coloration were used to calculate color and brightness contrasts of frogs as an indicator of conspicuousness for the visual systems of several potential predators (avian, crab and snake) and a conspecific observer. Additionally, we conducted experiments using clay model frogs of different coloration to investigate whether the local coloration of frogs is better protected than non-local color morphs, and if predator communities vary among populations. Overall predation risk differed strongly among populations and interestingly was higher on the two island populations. Imprints on clay models indicated that birds are the main predators while attacks of other predators were rare. Furthermore, clay models of local coloration were equally likely to be attacked as those of non-local coloration. Overall conspicuousness (and brightness contrast) of local frogs was positively correlated with attack rates by birds across populations. Together with results from earlier studies we conclude that conspicuousness honestly indicates toxicity to avian predators. The different coloration patterns among populations of strawberry poison frogs in combination with behavior and toxicity might integrate into equally efficient anti-predator strategies depending on local predation and other ecological factors.     

Poison frog colors are honest signals of toxicity, particularly for bird predators

Antipredator defenses and warning signals typically evolve in concert. However, the extensive variation across taxa in both these components of predator deterrence and the relationship between them are poorly understood. Here we test whether there is a predictive relationship between visual conspicuousness and toxicity levels across 10 populations of the color-polymorphic strawberry poison frog, Dendrobates pumilio. Using a mouse-based toxicity assay, we find extreme variation in toxicity between frog populations. This variation is significantly positively correlated with frog coloration brightness, a viewer-independent measure of visual conspicuousness (i.e., total reflectance flux). We also examine conspicuousness from the view of three potential predator taxa, as well as conspecific frogs, using taxon-specific visual detection models and three natural background substrates. We find very strong positive relationships between frog toxicity and conspicuousness for bird-specific perceptual models. Weaker but still positive correlations are found for crab and D. pumilio conspecific visual perception, while frog coloration as viewed by snakes is not related to toxicity. These results suggest that poison frog colors can be honest signals of prey unpalatability to predators and that birds in particular may exert selection on aposematic signal design.     

The role of size and colour pattern in protection of developmental stages of the red firebug (Pyrrhocoris apterus) against avian predators

We investigated how predator/prey body‐size ratio and prey colour pattern affected efficacy of prey warning signals. We used great and blue tits (Parus major and Cyanistes caeruleus), comprising closely related and ecologically similar bird species differing in body size, as experimental predators. Two larval instars and adults of the unpalatable red firebug (Pyrrhocoris apterus), differing in body size and/or coloration, were used as prey. We showed that prey body size did not influence whether a predator attacked the prey or not during the first encounter. However, smaller prey were attacked, killed, and eaten more frequently in repetitive encounters. We assumed that body size influences the predator through the amount of repellent chemicals better than through the amount of optical warning signal. The larger predator attacked, killed and ate all forms of firebug more often than the smaller one. The difference between both predators was more pronounced in less protected forms of firebug (chemically as well as optically). Colour pattern also substantially affected the willingness of predators to attack the prey. Larval red–black coloration did not provide a full‐value warning signal, although a similarly conspicuous red‐black coloration of the adults reliably protected them. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 890–898.     

Conspicuous males suffer higher predation risk: visual modelling and experimental evidence from lizards

Colour pattern variation is a striking and widespread phenomenon. Differential predation risk between individuals is often invoked to explain colour variation, but empirical support for this hypothesis is equivocal. We investigated differential conspicuousness and predation risk in two species of Australian rock dragons, Ctenophorus decresii andC. vadnappa . To humans, the coloration of males of these species varies between ‘bright’ and ‘dull’. Visual modelling based on objective colour measurements and the spectral sensitivities of avian visual pigments showed that dragon colour variants are differentially conspicuous to the visual system of avian predators when viewed against the natural background. We conducted field experiments to test for differential predation risk, using plaster models of ‘bright’ and ‘dull’ males. ‘Bright’ models were attacked significantly more often than ‘dull’ models suggesting that differential conspicuousness translates to differential predation risk in the wild. We also examined the influence of natural geographical range on predation risk. Results from 22 localities suggest that predation rates vary according to whether predators are familiar with the prey species. This study is among the first to demonstrate both differential conspicuousness and differential predation risk in the wild using an experimental protocol. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

PREDATOR PERCEPTION OF BATESIAN MIMICRY AND CONSPICUOUSNESS IN A SALAMANDER

In Batesian mimicry a palatable mimic deceives predators by resembling an unpalatable model. The evolution of Batesian mimicry relies on the visual capabilities of the potential predators, as prey detection provides the selective force driving evolutionary change. We compared the visual capabilities of several potential predators to test predictions stemming from the hypothesis of Batesian mimicry between two salamanders: the model species Notophthalmus viridescens, and polymorphic mimic, Plethodon cinereus. First, we found mimicry to be restricted to coloration, but not brightness. Second, only bird predators appeared able to discriminate between the colors of models and nonmimic P. cinereus. Third, estimates of salamander conspicuousness were background dependent, corresponding to predictions only for backgrounds against which salamanders are most active. These results support the hypothesis that birds influence the evolution of Batesian mimicry in P. cinereus, as they are the only group examined capable of differentiating N. viridescens and nonmimetic P. cinereus. Additionally, patterns of conspicuousness suggest that selection from predators may drive the evolution of conspicuousness in this system. This study confirms the expectation that the visual abilities of predators may influence the evolution of Batesian mimicry, but the role of conspicuousness may be more complex than previously thought.     

Losing the trait without losing the signal: Evolutionary shifts in communicative colour signalling

Colour signalling traits are often lost over evolutionary time, perhaps because they increase vulnerability to visual predators or lose relevance in terms of sexual selection. Here, we used spectrometric and phylogenetic comparative analyses to ask whether four independent losses of a sexually selected blue patch are spectrally similar, and whether these losses equate to a decrease in conspicuousness or to loss of a signal. We found that patches were lost in two distinct ways: either increasing reflectance primarily at very long or at very short wavelengths, and that species with additional colour elements (UV, green and pink) may be evolutionary intermediates. In addition, we found that patch spectral profiles of all species were closely aligned with visual receptors in the receiver's retina. We found that loss of the blue patch makes males less conspicuous in terms of chromatic conspicuousness, but more conspicuous in terms of achromatic contrast, and that sexual dimorphism often persists regardless of patch loss. Dorsal surfaces were considerably more cryptic than were ventral surfaces, and species in which male bellies were the most similar in conspicuousness to their dorsal surfaces were also the most sexually dimorphic. These results emphasize the consistent importance of sexual selection and its flexible impact on different signal components through evolutionary time.     

Inferring Predator Behavior from Attack Rates on Prey-Replicas That Differ in Conspicuousness

Behavioral ecologists and evolutionary biologists have long studied how predators respond to prey items novel in color and pattern. Because a predatory response is influenced by both the predator’s ability to detect the prey and a post-detection behavioral response, variation among prey types in conspicuousness may confound inference about post-prey-detection predator behavior. That is, a relatively high attack rate on a given prey type may result primarily from enhanced conspicuousness and not predators’ direct preference for that prey. Few studies, however, account for such variation in conspicuousness. In a field experiment, we measured predation rates on clay replicas of two aposematic forms of the poison dart frog Dendrobates pumilio, one novel and one familiar, and two cryptic controls. To ask whether predators prefer or avoid a novel aposematic prey form independently of conspicuousness differences among replicas, we first modeled the visual system of a typical avian predator. Then, we used this model to estimate replica contrast against a leaf litter background to test whether variation in contrast alone could explain variation in predator attack rate. We found that absolute predation rates did not differ among color forms. Predation rates relative to conspicuousness did, however, deviate significantly from expectation, suggesting that predators do make post-detection decisions to avoid or attack a given prey type. The direction of this deviation from expectation, though, depended on assumptions we made about how avian predators discriminate objects from the visual background. Our results show that it is important to account for prey conspicuousness when investigating predator behavior and also that existing models of predator visual systems need to be refined.