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.     

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.     

Does spatial variation in predation pressure modulate selection for aposematism?

It is widely believed that aposematic signals should be conspicuous, but in nature, they vary from highly conspicuous to near cryptic. Current theory, including the honest signal or trade‐off hypotheses of the toxicity–conspicuousness relationship, cannot explain why adequately toxic species vary substantially in their conspicuousness. Through a study of similarly toxic Danainae (Nymphalidae) butterflies and their mimics that vary remarkably in their conspicuousness, we show that the benefits of conspicuousness vary along a gradient of predation pressure. Highly conspicuous butterflies experienced lower avian attack rates when background predation pressure was low, but attack rates increased rapidly as background predation pressure increased. Conversely, the least conspicuous butterflies experienced higher attack rates at low predation pressures, but at high predation pressures, they appeared to benefit from crypsis. Attack rates of intermediately conspicuous butterflies remained moderate and constant along the predation pressure gradient. Mimics had a similar pattern but higher attack rates than their models and mimics tended to imitate the signal of less attacked model species along the predation pressure gradient. Predation pressure modulated signal fitness provides a possible mechanism for the maintenance of variation in conspicuousness of aposematic signals, as well as the initial survival of conspicuous signals in cryptic populations in the process of aposematic signal evolution, and an alternative explanation for the evolutionary gain and loss of mimicry.     

Ontogenetic colour change and the evolution of aposematism: a case study in panic moth caterpillars

1. Aposematism is a widely used antipredator strategy in which an organism possesses both warning coloration and unprofitable characters. Theoretical evidence suggests that aposematic colour should develop when high opportunity costs imposed by crypsis force an organism to engage in conspicuous behaviours. Hence, it is expected that ontogenetic colour change (OCC) in larval insects should include aposematism when foraging needs compel behavioural modifications that preclude a continued state of crypsis. 2. To test this idea, I first investigated whether OCC in caterpillars of the panic moth Saucrobotys futilalis was indicative of a switch from cryptic to aposematic coloration. I then examined the context of panic moth OCC as it related to foraging patterns and behavioural conspicuousness. 3. Early Saucrobotys instars are a cryptic green, but later instars become progressively more orange and develop black spots. Early instar larvae forage cryptically on the inner parenchyma of silked-together host plant leaves to avoid predation, but are rapidly forced to engage in conspicuous foraging behaviours as they outgrow the resources afforded by their shelters. Both coloration and behaviour reach maximal conspicuousness in final instar larvae. 4. As predicted, OCC encompassed a change from crypsis to aposematism in Saucrobotys. Aposematic function was demonstrated by changes in both antipredator behaviour patterns and effectiveness of predator deterrence in early and late instars. Moreover, increased opportunity costs of crypsis and behavioural conspicuousness coincided with the onset of aposematic coloration. 5. This pattern of OCC suggests that aposematic coloration in Saucrobotys develops as a response to constraints imposed by crypsis. Moreover, my study illustrates the importance of the study of ontogenetic patterns in determining how behaviour, morphology, and predator responses interact to influence the initial evolution of phenomena such as aposematism.     

Interaction between seed crypsis and habitat structure influence patch choice in a granivorous bird, the chaffinch Fringilla coelebs

Food abundance is an important determinant in habitat and patch selection but food accessibility and detectability is less often considered. Foraging on more cryptic seeds may increase predation risk by increasing the length of head down periods. Habitat structure may interact with this as birds are less able to detect predators with their head lowered in riskier obstructed habitats. We investigated patch choice in chaffinches Fringilla coelebs foraging in obstructed and open habitats and artificially manipulated the search times of seeds by colouring them either yellow or black. One trial consisted of a choice between the conspicuous seed in the open patch, and the cryptic seed in the obstructed patch; in the second trial the treatments were reversed. Individuals were more willing to forage in the obstructed habitat when the yellow seeds were present (43% of pecks made in the obstructed patch) than when the black seeds were present (18% of pecks in the obstructed patch). Differences in search time are likely to explain this result: yellow seeds were located almost twice as fast (1.26±0.60 seconds) as black ones (2.36±0.88 seconds). This experiment shows that individual foraging decisions may be influenced not only by food abundance but by the properties of individual food items (in this case seed crypsis) and the structure of the habitat they are present in.     

A reversible color polyphenism in American peppered moth (Biston betularia cognataria) caterpillars

Insect body color polyphenisms enhance survival by producing crypsis in diverse backgrounds. While color polyphenisms are often indirectly induced by temperature, rearing density, or diet, insects can benefit from immediate crypsis if they evolve polyphenisms directly induced by exposure to the background color, hence immediately deriving protection from predation. Here, we examine such a directly induced color polyphenism in caterpillars of the geometrid peppered moth (Biston betularia). This larval color polyphenism is unrelated to the genetic polymorphism for melanic phenotypes in adult moths. B. betularia caterpillars are generalist feeders and develop body colors that closely match the brown or green twigs of their host plant. We expand on previous studies examining the proximal cues that stimulate color development. Under controlled rearing conditions, we manipulated diets and background reflectance, using both natural and artificial twigs, and show that visual experience has a much stronger effect than does diet in promoting precise color matching. Their induced body color was not a simple response to reflectance or light intensity but instead specifically matched the wavelength of light to which they were exposed. We also show that the potential to change color is retained until the final (sixth) larval instar. Given their broad host range, this directly induced color polyphenism likely provides the caterpillars with strong protection from bird predation.     

OPTIMAL DEFENSIVE COLORATION STRATEGIES DURING THE GROWTH PERIOD OF PREY

Defensive coloration that reduces the risk of predation is considered to be widespread in animals. Many closely related species adopt differing coloration strategies during the life cycle, including crypsis, conspicuousness, and ontogenic change between the two coloration types. Here, we use a dynamic state-dependent approach to use ecological and intrinsic factors to predict the proportion of the developmental period of immature animals that should be spent as cryptic or conspicuous, and when conspicuous coloration should be reliably associated with investment in defenses. The model predicts that animals should change color more than once during development only in specific circumstances. In contrast, change from crypsis to conspicuous can occur over a range of conditions related to the frequency of detection by predators, but may also depend on the opportunity costs of crypsis and the effect of size on the deterrent effect of conspicuous coloration. We also report the results of a survey of coloration strategies in lepidopteron larvae, and note a qualitative agreement with the predictions of our model in the relationship between body size and coloration strategy. Our results provide explanations for several widespread antipredator coloration phenomena in prey animals, and provide a comprehensive predictive framework for the types of coloration strategies that are employed in nature.     

Speed-accuracy tradeoffs and false alarms in bee responses to cryptic predators

Learning plays a crucial role in predator avoidance [1-3], but little is known about how the type of experience with predators molds future prey behavior. Specifically, is predator-avoidance learning and memory retention disrupted by cryptic coloration of predators, such as crab spiders [4, 5]? How does experience with different predators affect foraging decisions? We evaluated these questions by exposing foraging bumblebees to controlled predation risk from predators (robotic crab spiders) that were either cryptic or highly contrasting, as assessed by a quantitative model of bee color perception [6]. Our results from 3D tracking software reveal a speed-accuracy tradeoff [7]: Bees slow their inspection flights after learning that there is a risk from cryptic spiders. The adjustment of inspection effort results in accurate predator detection, leveling out predation risk at the expense of foraging time. Overnight-retention tests reveal no decline in performance, but bees that had experienced cryptic predators are more prone to "false alarms" (rejection of foraging opportunities on safe flowers) than those that had experienced conspicuous predators. Therefore, bees in the cryptic-spider treatment made a functional decision to trade off reduced foraging efficiency via increased inspection times and false-alarm rates against higher potential fitness loss from being injured or eaten.     

Predation and cryptic coloration in a managed landscape

Protective forms of animal color, such as crypsis, are thought to reduce the probability of detection by visual predators. However, because crypsis is ostensibly intuitive, the working hypothesis of cryptic coloration is seldom tested. Additionally because crypsis is a background-specific adaptation, events which alter habitat structure and substrate composition are likely to affect rates of predation on cryptic animals; animal colors that are cryptic against one visual background may be conspicuous against different visual backgrounds. Populations of Sceloporus woodi, a cryptic diurnal lizard, occupy clear-cut stands of sand pine scrub and prescribe-burned longleaf pine habitat within the Ocala National Forest. Here, we used a combination of clay models resembling S. woodi, and spectral analysis, to examine the effects of spatial heterogeneity and model-substrate contrast on rates of predation. The rate of attack on clay models differed between substrate types and habitats, and was highest when clay models were conspicuous against the local visual background. The dorsal color of models greatly contrasted open sand and dead wood, but had similar reflectance values to leaf litter, suggesting that models were most cryptic on leaf litter. We conclude that crypsis is adaptive in this species, and that variation in rates of attack between sampling locations is related to changes in substrate composition due to management history. For instance, the data suggest that the rate of attack on clay models would decrease in response to succession in sand pine scrub, because aging in sand pine scrub results in increased amounts of leaf litter and decreased amounts of open sand. Overall, the results of this study support the theory of protective coloration.     

Mixed-phenotype grouping: the interaction between oddity and crypsis

Aggregations of different-looking animals are frequently seen in nature, despite well-documented selection pressures on individuals to maintain phenotypically homogenous groups. Two well-known theories, the ‘confusion effect’ (reduced ability of a predator to accurately target an individual in a group) and the ‘oddity effect’ (preferential targeting of phenotypically distinct, ‘odd’, individuals) act together to predict the evolution of behaviours in prey that lead to groups of animals that are homogeneous in appearance. In contrast, a recently proposed mechanism suggests that mixed groups could be maintained if one species in a mixed group is more conspicuous against the habitat than the other, as confusion effects generated by the conspicuous species impede predator targeting of the cryptic species; thus, cryptic species benefit from association with conspicuous ones. We test these contrasting predictions from the perspective of both predators and prey, and show that cryptic individual Daphnia are at reduced risk of predation from three-spine sticklebacks Gasterosteus aculeatus when in mixed-phenotype groups, a risk that is reduced further as the number of conspicuous individuals increases, supporting the hypothesis for the evolution of mixed groups. In contrast, while the preference for associating with colour-matched conspecifics by mollies (Poecilia sphenops) was reduced when they were cryptic, we found no evidence for active association with conspicuous conspecifics. We conclude that prey animals must balance the relative risks of oddity and conspicuousness in their social decisions, and that this could potentially lead to the evolution of mixed-phenotype grouping as a response to predation risk alone.     

Aposematism: what should our starting point be?

The evolution of aposematism is considered to be a major evolutionary problem because if new aposematic forms emerged in defended cryptic populations, they would face the dual problems of rarity and conspicuousness. We argue that this commonly assumed starting point might not have wide validity. We describe a novel evolutionary computer model in which prey evolve secondary defences and become conspicuous by moving widely over a visually heterogeneous habitat. Unless crypsis imposes high opportunity costs (for instance, preventing prey from efficient foraging, thermoregulation and communication), costly secondary defences are not predicted to evolve at all. However, when crypsis imposes opportunity costs, prey evolve secondary defences that facilitate raised behavioural conspicuousness as prey exploit opportunities within their environment. Optimal levels of secondary defence and of behavioural conspicuousness increase with population sizes and the costs imposed by crypsis. When prey are already conspicuous by virtue of their behaviours, the evolution of aposematic appearances (bright coloration, etc.) is much easier to explain because aposematic traits add little further costs of conspicuousness, but can bring large benefits.     

Rattling Behavior of Prairie Rattlesnakes (Crotalus viridis viridis,Viperidae) in Relation to Sex,Reproductive Status,Body Size,and Body Temperature

We examined whether sex, reproductive status, body size, or body temperature of prairie rattlesnakes (Crotalus viridis viridis) was related to when snakes rattled in response to an approaching observer. We found that gravid females allowed significantly closer approaches than males, suggesting that females relied on crypsis to avoid predation, possibly because pregnancy constrained their locomotive ability. Smaller snakes allowed significantly closer approaches than did larger snakes. Smaller snakes may be more cryptic or slower, which may influence their waiting to rattle until the observer was close. Overall, we found no consistent relationship between the distance from the observer that a snake rattled and its body temperature. However, cooler gravid females allowed closer approaches by the observer than did warmer gravid females. In summary, reproductive status, body size, and body temperature appear to influence the costs and benefits of crypsis vs. active defense of rattlesnakes.     

An ethogram of body patterning behavior in the biomedically and commercially valuable squid Loligo pealei off Cape Cod, Massachusetts.

Squids have a wide repertoire of body patterns; these patterns contain visual signals assembled from a highly diverse inventory of chromatic, postural, and locomotor components. The chromatic components reflect the activity of dermal chromatophore organs that, like the postural and locomotor muscles, are controlled directly from the central nervous system. Because a thorough knowledge of body patterns is fundamental to an understanding of squid behavior, we have compiled and described an ethogram (a catalog of body patterns and associated behaviors) for Loligo pealei. Observations of this species were made over a period of three years (> or = 440 h) and under a variety of behavioral circumstances. The natural behavior of the squid was filmed on spawning grounds off Cape Cod (northwestern Atlantic), and behavioral trials in the laboratory were run in large tanks. The body pattern components--34 chromatic (including 4 polarization components), 5 postural, and 12 locomotor--are each described in detail. Eleven of the most common body patterns are also described. Four of them are chronic, or long-lasting, patterns for crypsis; an example is Banded Bottom Sitting, which produces disruptive coloration against the substrate. The remaining seven patterns are acute; they are mostly used in intraspecific communication among spawning squids. Two of these acute patterns--Lateral Display and Mate Guarding Pattern--are used during agonistic bouts and mate guarding; they are visually bright and conspicuous, which may subject the squids to predation; but we hypothesize that schooling and diurnal activity may offset the disadvantage presented by increased visibility to predators. The rapid changeability and the diversity of body patterns used for crypsis and communication are discussed in the context of the behavioral ecology of this species.     

Fig Foraging by Dichromatic and Trichromatic <Emphasis Type="Italic">Cebus capucinus</Emphasis> in a Tropical Dry Forest

Figs are important resources for frugivores, and Ficus is an ideal taxon for evaluating patterns of primate foraging related to food color. Ficus spp. can be classified as conspicuous (color change from greenish to reddish during ripening) or cryptic (green throughout ripening). To investigate the effect on foraging of color vision phenotype variation for these 2 types of figs, we conducted a 20-mo study on 4 groups of white-faced capuchins (Cebus capucinus) in the Santa Rosa Sector of the ACG, Costa Rica between May 2004 and September 2008. We genotyped all individuals and collected behavioral data on feeding rates, acceptance indices, and foraging sequences. We found a significant effect of fig type; feeding rates and acceptance indices were higher for conspicuous figs than for cryptic figs, and subjects sniffed cryptic figs more often than conspicuous figs. We also found that dichromats sniffed more figs and had longer foraging sequences than trichromats, especially for cryptic figs. Among 6 subtypes of dichromats and trichromats, monkeys possessing the trichromat phenotype with the most spectrally separated L-M opsin alleles showed the highest acceptance index for conspicuous figs, though there were no differences in feeding rates among phenotypes. We conclude: 1) conspicuous figs are visually salient not only for trichromats but also for dichromats, 2) olfaction is important for evaluating edibility of cryptic figs, and 3) the reliance on olfaction for selecting fruit is greater in dichromats. These results indicate divergent foraging strategies among color vision phenotypes for assessing food items.     

Once a Batesian mimic, not always a Batesian mimic: mimic reverts back to ancestral phenotype when the model is absent

Batesian mimics gain protection from predation through the evolution of physical similarities to a model species that possesses anti-predator defences. This protection should not be effective in the absence of the model since the predator does not identify the mimic as potentially dangerous and both the model and the mimic are highly conspicuous. Thus, Batesian mimics should probably encounter strong predation pressure outside the geographical range of the model species. There are several documented examples of Batesian mimics occurring in locations without their models, but the evolutionary responses remain largely unidentified. A mimetic species has four alternative evolutionary responses to the loss of model presence. If predation is weak, it could maintain its mimetic signal. If predation is intense, it is widely presumed the mimic will go extinct. However, the mimic could also evolve a new colour pattern to mimic another model species or it could revert back to its ancestral, less conspicuous phenotype. We used molecular phylogenetic approaches to reconstruct and test the evolution of mimicry in the North American admiral butterflies (Limenitis: Nymphalidae). We confirmed that the more cryptic white-banded form is the ancestral phenotype of North American admiral butterflies. However, one species, Limenitis arthemis, evolved the black pipevine swallowtail mimetic form but later reverted to the white-banded more cryptic ancestral form. This character reversion is strongly correlated with the geographical absence of the model species and its host plant, but not the host plant distribution of L. arthemis. Our results support the prediction that a Batesian mimic does not persist in locations without its model, but it does not go extinct either. The mimic can revert back to its ancestral, less conspicuous form and persist.     

Loss of conspicuous coloration has co-evolved with decreased body size in populations of poison dart frogs

Larger signal size is known to facilitate the learning process of predators to warning signals. Further, smaller objects are generally harder to detect than large, which suggests that smaller sized prey are less likely to benefit from an aposematic strategy compared to crypsis. However, whether body size changes in concert with shifts between crypsis and aposematism in natural populations, remains largely unexplored. I tested whether body size was larger in visually conspicuous population than in cryptic populations among recently diverged populations of the Strawberry Poison frog, Oophaga pumilio. By analysing spectral reflectance and body size data from individuals from 18 discrete populations I found a larger mean body size in conspicuous populations, which was confirmed by an analysis of a subset of 12 populations accounting for phylogenetic history. This shows that the loss of conspicuous colour likely co-evolved repeatedly with a decrease in body size. Thus, selection on body size may influence evolutionary shifts between aposematism and crypsis and vice versa.     

Progressive background in moths, and a quantitative measure of crypsis

A method is presented for quantitative estimation of the degree of crypsis of species seen by visual predators against known backgrounds. It is based upon a comparison between transects taken across animal and background colour patterns. The method was applied to day-resting moths in deciduous forest in New Jersey. Each species is found for two to four weeks at characteristic dates, and there is a constant turnover of species. In both moths and backgrounds there is a regular change in the colour pattern parameters from winter through spring to early summer. Moths are on average more cryptic at their normal dates than they would be if present earlier or later in the year. Species with known resting sites are on average more cryptic on their resting sites than other background habitats. Species that rest on more than one background habitat are less cryptic on their preferred habitats than are specialists. Species that rest under leaves and are not visible from above are not very cryptic. Specific v. general resemblance, disruptive coloration, and factors affecting 'aspect diversity' are discussed. The new method of estimating crypsis is useful for studies of crypsis as well as in sexual selection. It is necessary to know much about the resting sites and behaviour of moths, as well as other functions of colour patterns, to understand colour pattern evolution.     

Camouflaging in a complex environment--octopuses use specific features of their surroundings for background matching

Living under intense predation pressure, octopuses evolved an effective and impressive camouflaging ability that exploits features of their surroundings to enable them to "blend in." To achieve such background matching, an animal may use general resemblance and reproduce characteristics of its entire surroundings, or it may imitate a specific object in its immediate environment. Using image analysis algorithms, we examined correlations between octopuses and their backgrounds. Field experiments show that when camouflaging, Octopus cyanea and O. vulgaris base their body patterns on selected features of nearby objects rather than attempting to match a large field of view. Such an approach enables the octopus to camouflage in partly occluded environments and to solve the problem of differences in appearance as a function of the viewing inclination of the observer.     

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.     

Evidence for search image in blackbirds Turdus merula L.: long-term learning

The feeding behaviour of free-flying and captive blackbirds Turdus merula L. was observed over a number of days to investigate their ability to see cryptic food. Sequences of eight tests which contained equal numbers of ‘cryptic’ and ‘conspicuous’ tests were presented to the birds of the first two experiments. The blackbirds in experiment 1 increased their feeding rate for both cryptic and conspicuous food, which suggests that search images were not acquired but that the physical acts of feeding were perfected (or that they altered their acceptance of green food). In contrast, the ‘residual search time’ (the bird's total search time minus handling and movement times) decreased over the series of four tests with cryptic green prey, but remained constant over the four tests with conspicuous prey (experiment 2). The blackbirds exploited the cryptic prey using their previous experience of searching for such food. This suggests that search images can be effective over eight feeding sessions, spanning 4–30 days. Similar results were obtained over a 9-day period with four juvenile blackbirds in captivity (experiment 3). With experience they also became expert in their assessment of backgrounds set up without prey.