Coincident disruptive coloration

Even if an animal matches its surroundings perfectly in colour and texture, any mismatch between the spatial phase of its pattern and that of the background, or shadow created by its three-dimensional relief, is potentially revealing. Nevertheless, for camouflage to be fully broken, the shape must be recognizable. Disruptive coloration acts against object recognition by the use of high-contrast internal colour boundaries to break up shape and form. As well as the general outline, characteristic features such as eyes and limbs must also be concealed; this can be achieved by having the colour patterns on different, but adjacent, body parts aligned to match each other (i.e. in phase). Such 'coincident disruptive coloration' ensures that there is no phase disjunction where body parts meet, and causes different sections of the body to blend perceptually. We tested this theory using field experiments with predation by wild birds on artificial moth-like targets, whose wings and (edible pastry) bodies had colour patterns that were variously coincident or not. We also carried out an experiment with humans searching for analogous targets on a computer screen. Both experiments show that coincident disruptive coloration is an effective mechanism for concealing an otherwise revealing body form.     

Defining disruptive coloration and distinguishing its functions

Disruptive coloration breaks up the shape and destroys the outline of an object, hindering detection. The principle was first suggested approximately a century ago, but, although research has significantly increased, the field remains conceptually unstructured and no unambiguous definition exists. This has resulted in variable use of the term, making it difficult to formulate testable hypotheses that are comparable between studies, slowing down advancement in this field. Related to this, a range of studies do not effectively distinguish between disruption and other forms of camouflage. Here, we give a formal definition of disruptive coloration, reorganize a range of sub-principles involved in camouflage and argue that five in particular are specifically related to disruption: differential blending; maximum disruptive contrast; disruption of surface through false edges; disruptive marginal patterns; and coincident disruptive coloration. We discuss how disruptive coloration can be optimized, how it can relate to other forms of camouflage markings and where future work is particularly needed.     

Crypsis through disruptive coloration in an isopod

The white-spotted colour morph of the marine isopod Idotea baltica appears cryptic on the brown alga Fucus vesiculosus with its white-coloured epizoites Electra crustulenta and Balanus improvisus. This study shows that the crypsis of this coloration is achieved through disruptive coloration rather than through background matching. Crypsis through background matching requires that the sizes and the shapes of the pattern elements should closely resemble those of the visual background. Comparisons between the white spots of the isopods and those of their natural background contradicted this prediction. Disruptive coloration, which aims to obscure the true form of the animal by partly blending with the background and distracting the attention of the viewer from the contour of the animal to unessential patterns, presupposes more marginal elements than expected by the pattern element distribution in the background, and also highly variable and complex elements. Comparison between the observed spot distribution and simulated individuals with randomly distributed spots showed that the spots in these isopods do indeed touch the body outline more often than expected. Furthermore, the spots were highly variable and complex.     

Adaptive evolution of cryptic coloration: the shape of host plants and dorsal stripes in Timema walking-sticks

The adaptive significance of cryptic colour patterns has seldom been analysed in a phylogenetic context. We mapped data on the presence vs. absence of dorsal stripes, and the use of needle-like vs. broad foliage, onto a recent phylogeny of Timema walking-sticks, in order to infer the evolutionary history of these traits and test the hypothesis that the dorsal stripe is an adaptation for crypsis on needle-like leaves. By maximum parsimony optimization, the dorsal stripe has evolved five or six times in this clade, each time in association with the use of vegetation with needle-like leaves. Maddison's concentrated changes test showed that this association between morphology and habitat was statistically significant. By contrast, results based on Pagel's maximum likelihood analyses did not reach significance, probably because the large number of origins of dorsal stripe introduces statistical uncertainty. These results suggest that the adaptations for crypsis can arise readily and in parallel, in the appropriate selective environment. However, they may also constrain the evolution of host-plant use, as there is no unambiguous case of Timema species with dorsal stripes shifting to broad-leaved plants.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 1–5.     

Optimization of cryptic coloration in heterogeneous habitats

We present a theoretical approach to the optimization of crypsis in heterogeneous habitats. Our model habitat consists of two different microhabitats, and the optimal combination of crypsis in the microhabitats is supposed to maximize the probability of escaping detection by a predator. The probability of escaping detection for a prey is a function of: (i)degree of crypsis, (ii) probability of occurrence in the microhabitats and (iii) probability of encountering a predator in the microhabitats. Because crypsis is background-specific there is a trade-off between crypsis in two visually different microhabitats. Depending on the nature of the trade-off, the optimal coloration is either a compromise between the requirements of the differing microhabitats or entirely adapted to only one of them. An increased risk of predation in one of the microhabitats favours increased crypsis in that microhabitat. Because the trade-off constrains possible optimal solutions, it is not possible to predict the optimal coloration only from factors (i)-(iii). However, habitat choice may fundamentally change the situation. If minimizing predation risk does not incur any costs, the prey should exclusively prefer the microhabitat where it has a lower probability of encountering a predator and better crypsis. The implications of these results for variation in cryptic coloration and polymorphism are discussed.     

The predation costs of symmetrical cryptic coloration

In psychological studies of visual perception, symmetry is accepted as a potent cue in visual search for cryptic objects, yet its importance for non-human animals has been assumed rather than tested. Furthermore, while the salience of bilateral symmetry has been established in laboratory-based search tasks using human subjects, its role in more natural settings, closer to those for which such perceptual mechanisms evolved, has not, to our knowledge, been investigated previously. That said, the salience of symmetry in visual search has a plausible adaptive rationale, because biologically important objects, such as prey, predators or conspecifics, usually have a plane of symmetry that is not present in their surroundings. We tested the conspicuousness to avian predators of cryptic artificial, moth-like targets, with or without bilateral symmetry in background-matching coloration, against oak trees in the field. In two independent experiments, symmetrical targets were predated at a higher rate than otherwise identical asymmetrical targets. There was a small, but significant, fitness cost to symmetry in camouflage patterns. Given that birds are the most commonly invoked predators shaping the evolution of defensive coloration in insects, this raises the question of why bilateral asymmetry is not more common in cryptic insects.     

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.     

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.     

Selection,constraint, and the evolution of coloration in African starlings

Colorful plumage plays a prominent role in the evolution of birds, influencing communication (sexual/social selection), and crypsis (natural selection). Comparative studies have focused primarily on these selective pressures, but the mechanisms underlying color production can also be important by constraining the color gamut upon which selection acts. Iridescence is particularly interesting to study the interaction between selection and color‐producing mechanisms because a broad range of colors can be produced with a shared template, and innovations to this template further expand this by increasing the parameters interacting to produce colors. We examine the patterns of ornamentation and dichromatism evolution in African starlings, a group remarkably diverse in color production mechanisms, social systems, and ecologies. We find that the presence of iridescence is ancestral to the group, being predominantly lost in females and cooperative breeders, as well as species with less labile templates. Color‐producing mechanisms interact and are the main predictors of plumage ornamentation and elaboration, with little influence of selective pressures in their evolution. Dichromatism, however is influenced by social system and the loss of iridescence. Our results show the importance of considering both selection and constraints, and the different roles that they may have, in the evolution of ornamentation and dimorphism.     

Cephalopod dynamic camouflage: bridging the continuum between background matching and disruptive coloration

Individual cuttlefish, octopus and squid have the versatile capability to use body patterns for background matching and disruptive coloration. We define—qualitatively and quantitatively—the chief characteristics of the three major body pattern types used for camouflage by cephalopods: uniform and mottle patterns for background matching, and disruptive patterns that primarily enhance disruptiveness but aid background matching as well. There is great variation within each of the three body pattern types, but by defining their chief characteristics we lay the groundwork to test camouflage concepts by correlating background statistics with those of the body pattern. We describe at least three ways in which background matching can be achieved in cephalopods. Disruptive patterns in cuttlefish possess all four of the basic components of ‘disruptiveness’, supporting Cott''s hypotheses, and we provide field examples of disruptive coloration in which the body pattern contrast exceeds that of the immediate surrounds. Based upon laboratory testing as well as thousands of images of camouflaged cephalopods in the field (a sample is provided on a web archive), we note that size, contrast and edges of background objects are key visual cues that guide cephalopod camouflage patterning. Mottle and disruptive patterns are frequently mixed, suggesting that background matching and disruptive mechanisms are often used in the same pattern.     

The effects of pattern symmetry on detection of disruptive and background-matching coloration

Two, logically distinct but sometimes compatible, mechanismsof camouflage are background-matching and disruptive coloration.In the former, an animal's coloration comprises a random sampleof the background, and so target–background discriminationis impeded. In the latter, object or feature recognition iscompromised by placing bold, high-contrast colors so that theybreak up the prey's body into apparently unconnected objects.Recent experimental evidence for the utility of disruptive colors,above and beyond that conferred by background matching, hasbeen based on artificial prey with patterns lacking a planeof symmetry. However, it is plausible that the bilateral symmetrypresent in natural prey may compromise the efficiency of disruptivecoloration, on account of the potency of symmetry as a cue invisual search. In this study, we tested this prediction in thefield, by tracking the "survival" under bird predation of artificialmothlike targets placed on oak trees. These had background-matchingcolor patches placed either disruptively or nondisruptivelyand with or without bilateral symmetry. We found that symmetryreduced the effectiveness of both nondisruptive and disruptivebackground-matching coloration to a similar degree so that thenegative effects of symmetry on concealment are no greater fordisruptive than nondisruptive patterns.     

Community structure and the evolution of aposematic coloration

Studies on the evolution of aposematic coloration (prey coloration advertising for unpalatability) have mainly focused on predator psychology in simplified single-prey species systems. We chose, instead, to model population dynamics on the community level. We studied the invasion by an aposematic phenotype in the presence and absence of another prey species. The single-prey and two-prey models differed in two major ways. First, with two prey species the invasion was possible only with a weak aposematic signal, whereas with a single prey species there was no such an upper limit for signal strength. Second, with a single prey species, increase of the aposematic phenotype always resulted in rapid extinction of the predator. Resource value and growth rate of the alternative prey species affected the invasion. These results suggest that community structure is an important determinant of the conditions for invasion of aposematism, and may have contributed to its initial evolution.     

Selection for cryptic coloration in a visually heterogeneous habitat

We studied selection by predators for cryptic prey coloration in a visually heterogeneous habitat that consists of two microhabitats. It has been suggested that the probability of escaping detection in such habitats might be optimized by maximizing crypsis in one of the microhabitats. However, a recent model indicates that a coloration that compromises the requirements of different microhabitats might sometimes be the optimal solution. To experimentally study these hypotheses, we allowed great tits (Parus major L.) to search for artificial prey items in two different microhabitats (background boards): small patterned and large patterned. On each board there was one prey item that was either small-patterned, large-patterned or medium-patterned and thus compromised. Search time was used as the measure of crypsis and was on average longer on the large-patterned than on the small-patterned background. On the small-patterned background, the small-patterned prey was more cryptic than the compromised prey, which was in turn more cryptic than the large-patterned prey. On the large-patterned background, the small-patterned prey was least cryptic, but the compromised prey did not differ significantly from the large-patterned prey. The compromised coloration had lower predation risk than the matching colorations. This indicates that in some conditions a compromised coloration might be the best strategy for the prey and has important implications for the study of animal coloration.     

Background matching,disruptive coloration,and differential use of microhabitats in two neotropical grasshoppers with sexual dichromatism

Cryptic coloration is an adaptative defensive mechanism against predators. Color patterns can become cryptic through background coloration‐matching and disruptive coloration. Disruptive coloration may evolve in visually heterogeneous microhabitats, whereas background matching could be favored in chromatically homogeneous microhabitats. In this work, we used digital photography to explore the potential use of disruptive coloration and background matching in males and females of two grasshopper species of the Sphenarium genus in different habitats. We found chromatic differences in the two grasshopper species that may be explained by local adaptation. We also found that the females and males of both species are dichromatic and seem to follow different color cryptic strategies, males are more disruptive than females, whereas females have a high background matching with less disruptive elements. The selective pressures of the predators in different microhabitats and the differences in mobility between sexes may explain the color pattern divergence between females and males. Nevertheless, more field experiments are needed in order to understand the relative importance of disruptive and background matching coloration in the evolution of sexual dichromatism in these grasshoppers.     

The evolution of human skin coloration

Skin color is one of the most conspicuous ways in which humans vary and has been widely used to define human races. Here we present new evidence indicating that variations in skin color are adaptive, and are related to the regulation of ultraviolet (UV) radiation penetration in the integument and its direct and indirect effects on fitness. Using remotely sensed data on UV radiation levels, hypotheses concerning the distribution of the skin colors of indigenous peoples relative to UV levels were tested quantitatively in this study for the first time. The major results of this study are: (1) skin reflectance is strongly correlated with absolute latitude and UV radiation levels. The highest correlation between skin reflectance and UV levels was observed at 545 nm, near the absorption maximum for oxyhemoglobin, suggesting that the main role of melanin pigmentation in humans is regulation of the effects of UV radiation on the contents of cutaneous blood vessels located in the dermis. (2) Predicted skin reflectances deviated little from observed values. (3) In all populations for which skin reflectance data were available for males and females, females were found to be lighter skinned than males. (4) The clinal gradation of skin coloration observed among indigenous peoples is correlated with UV radiation levels and represents a compromise solution to the conflicting physiological requirements of photoprotection and vitamin D synthesis. The earliest members of the hominid lineage probably had a mostly unpigmented or lightly pigmented integument covered with dark black hair, similar to that of the modern chimpanzee. The evolution of a naked, darkly pigmented integument occurred early in the evolution of the genus Homo. A dark epidermis protected sweat glands from UV-induced injury, thus insuring the integrity of somatic thermoregulation. Of greater significance to individual reproductive success was that highly melanized skin protected against UV-induced photolysis of folate (Branda & Eaton, 1978, Science201, 625-626; Jablonski, 1992, Proc. Australas. Soc. Hum. Biol.5, 455-462, 1999, Med. Hypotheses52, 581-582), a metabolite essential for normal development of the embryonic neural tube (Bower & Stanley, 1989, The Medical Journal of Australia150, 613-619; Medical Research Council Vitamin Research Group, 1991, The Lancet338, 31-37) and spermatogenesis (Cosentino et al., 1990, Proc. Natn. Acad. Sci. U.S.A.87, 1431-1435; Mathur et al., 1977, Fertility Sterility28, 1356-1360).As hominids migrated outside of the tropics, varying degrees of depigmentation evolved in order to permit UVB-induced synthesis of previtamin D(3). The lighter color of female skin may be required to permit synthesis of the relatively higher amounts of vitamin D(3)necessary during pregnancy and lactation. Skin coloration in humans is adaptive and labile. Skin pigmentation levels have changed more than once in human evolution. Because of this, skin coloration is of no value in determining phylogenetic relationships among modern human groups.     

Speciational evolution of coloration in the genus Carduelis

Sexual selection has been hypothesized to promote speciation, but evidence relating sexual selection to differences in speciation rates among taxa is equivocal. We note that evolutionary changes in ornaments are the link connecting sexual selection to speciation, and that ornament evolution is influenced by many factors so that its relationship with the strength of sexual selection may not be linear. We test if the evolution of ornamental coloration in Carduelis finches is related with speciation and if more ornamented lineages speciate more. We found that coloration evolves with a speciational pattern, but we found no evidence that the evolutionary changes associated with speciation are predominantly gains in ornamentation. The speciational pattern was found for both carotenoid- and melanin-based coloration, suggesting that traits putatively under stronger sexual selection by female choice (carotenoid coloration) are not the sole ones facilitating reproductive isolation. We conclude that in the genus Carduelis the evolutionary lability of ornaments influences speciation more than the strength of sexual selection, and we suggest that ornament lability should be considered as a possible causal factor in studies comparing cladogenesis among taxa.     

Effects of carotenoid sequestration on a caterpillar's cryptic coloration and susceptibility to predation

Carotenoids are used for many functions by animals, including combining with other pigments to produce aposematic and cryptic coloration. Carotenoids in combination with blue pigments are responsible for green coloration in many caterpillars, and thus carotenoid sequestration may reduce their contrast against a green foliage background. We tested the hypothesis that carotenoid sequestration reduces contrast and enhances survival by rearing Trichoplusia ni Hübner (Lepidoptera: Noctuidae) on Brassica oleracea L. var. Acephala (Brassicaceae) leaves and exposing them to predators. We found that carotenoids derived from the host plant are partially excreted, along with chlorophyll, but also sequestered in hemolymph. Larvae that were given plants that provided carotenoids showed less contrast against their host plants within 1 day compared to larvae that were not provided with carotenoids. Last, both short‐term field observations and laboratory trials of larvae caged with predatory Podisus maculiventris Say (Hemiptera: Pentatomidae) nymphs showed that survival of carotenoid‐sequestering larvae was higher compared to larvae that did not sequester. These results suggest that carotenoid sequestration may be an important adaptive strategy that reduces susceptibility to natural enemies that hunt by sight. Further research that examines the mechanisms by which carotenoids are absorbed and modified will lend insights into the evolution of carotenoids functioning as passive defensive compounds.     

Spermicide, cryptic female choice and the evolution of sperm form and function

Sperm competition and cryptic female choice profoundly affect sperm morphology, producing diversity within both species and individuals. One type of within-individual sperm variation is sperm heteromorphism, in which each male produces two or more distinct types of sperm simultaneously, only one of which is typically fertile (the "eusperm"). The adaptive significance of nonfertile "parasperm" types is poorly understood, although numerous sperm-heteromorphic species are known from many disparate taxa. This paper examines in detail two female-centred hypotheses for the evolution and maintenance of this unconventional sperm production strategy. First, we use game theoretical models to establish that parasperm may function to protect eusperm from female-generated spermicide, and to elucidate the predictions of this idea. Second, we expand on the relatively undeveloped idea that parasperm are used by females as a criterion for cryptic female choice, and discuss the predictions generated by this idea compared to other hypotheses proposed to explain sperm heteromorphism. We critically evaluate both hypotheses, suggest ways in which they could be tested, and propose taxa in which they could be important.     

Bold coloration and the evolution of aposematism in terrestrial carnivores

Several species of terrestrial carnivores (Mammalia: Carnivora) have bold contrasting color patterns that, in some species, apparently signal possession of noxious anal gland secretions, or even physical strength and great ferocity; yet the evolutionary drivers of both placement and patterning of these contrasting pelage colors on the body, and the ecological selection pressures underlying them, have yet to be systematically examined. Here we explore these issues and find not only that both boldly colored and dichromatic species do indeed often use anal gland secretions for defense, but also that such species are stockier, and live in more exposed habitats where other forms of antipredator defense are limited. We also show that white dorsa are found in sprayers that are primarily nocturnal; that horizontal stripes are found in species that have an ability to spray anal secretions accurately; and that facial stripes are found in burrowing species that typically leave only their heads exposed to attack. Our phylogenetic reconstructions suggest that aposematic coloration has evolved more than once in terrestrial carnivores. We finish by outlining five evolutionary routes for patterns of pelage coloration in this taxon.