Organisms with bright and conspicuous color patterns tend I to attract the most attention both scientifically and aesthetically. However, the majority of insects and other animals rely on camouflage or crypsis for survival from predators that hunt them by sight. Furthermore, crypsis may extend to include the other senses, namely, smell, touch, and sound. Indeed, any stimulus or signal that can alert a potential predator could be expected to become part of a coordinated suite of cryptic traits. A form of crypsis is also shown by some predators that disguise themselves by assuming the same color and patterns as the background on which they hunt. H. B. Cott in 1940 wrote perhaps the best known topic on animal color patterns, but many of the great entomologists of the 19th century had already considered insect camouflage. It is not usual to consider insect crypsis as a subject of applied biology but there are certainly many parallels with military expertise in either the hiding of or the searching for personnel and armaments in a landscape.
COLOR MATCHING AND CRYPSIS
An insect that is perfectly camouflaged is perhaps one of the most striking exhibitions of the power of evolution by natural selection to mold and adapt organisms to fit their environment and to maximize survival and reproductive success. Wonderful examples of camouflage are presented by many species of insects, including some butterflies in tropical forests (Fig. 1A’ , which rest on carpets of dead brown leaves. The apparent perfection of crypsis is emphasized in many such insects by a similarity of, and matching of, the color pattern of the wings, body, and appendages to the background on which they normally rest. The color pattern of these different body parts and structures must involve different genetic and developmental pathways, and yet evolution has led to a corresponding perfection of matching, albeit using entirely different mechanisms of pattern formation. Such an example of an underlying complexity of patterning is given by some caterpillars of the family Lasiocampidae that rest on the bark of trees and survive by resemblance to the background color pattern of the bark, including epiphytic lichens and algae (Fig. 1C). Such larvae are encircled by long hairs that are flattened around their margin when at rest. This breaks up their shape, smoothing their outline. These hairs are also patterned in a very specific way and one that is fully coordinated with the body cuticle, including the short bristles of the dorsal areas of the body segments. These elements are exposed, and the whole insect becomes highly conspicuous as soon as a larva is forced to move along a twig of fine diameter (Fig. 1D).
Furthermore, color matching in crypsis is almost always only one component of the strategy for survival; both habitat choice and, frequently, the adoption of very specific patterns of behavior and activity are required for effective crypsis. One such example is shown by some species of moths that attain crypsis by appearing to be a dead patch of tissue within a large leaf on which they rest (Fig. 1B). They achieve this not only through the generally brown color of their wings and some details of patterning, which may resemble small patches of fungal-attacked leaf tissue, but also through a precise positioning on the leaf. For example, the moth in Fig. 1B has rolled up the leading edge of its forewing, wrapped its abdomen along the trailing edge of one hind wing, hidden its appendages, and positioned itself alongside the midrib of the leaf.
Despite the potential fascination of understanding crypsis, it is only relatively recently that scientists have begun to analyze what is meant precisely when it is stated that an organism is well camouflaged. John Endler in 1978 stated that “a color pattern is cryptic if it resembles a random sample of the background perceived by predators at the time and age, and in the microhabitat where prey is most vulnerable to visually hunting predators.” There are several crucial components in this definition. First, a color pattern is cryptic only with respect to the specific environment in which the organism is potentially encountered by the predator or the guild of predators to whom the pattern is an adaptive response. What is a cryptic pattern on the resting background of that environment may be conspicuous and ineffective on any other background. Second, the effectiveness of a particular pattern is considered with respect to the normal time and lighting conditions under which crypsis is functional. Third, to be cryptic the color pattern of a prey organism must essentially reflect a random sample of the background on which it rests.
INDUSTRIAL MELANISM AND CRYPSIS
Perhaps the first analysis of crypsis and the evolution of a color pattern from the perspective of changes in camouflage involved industrial melanism in the salt-and-pepper moth, Biston betularia. Industrial melanism refers to an association of high frequencies of dark, melanic forms or phenotypes of a species with high levels of air pollution. The fundamental components of this classic example of the evolution of an adaptive trait also apply to numerous other species of moth and other insects that have evolved melanism as a response to environments influenced by air pollution. These components are: (1) the environment was changed by air pollution in such a way that the camouflage of the “typical” or wild type of color pattern was impaired, (2) a mutant phenotype occurred in this new environment that had a functional design or color pattern that improved survival from birds hunting the moths at rest, and (3) the dominant allele at the gene that specified this favored mutant phenotype then increased in frequency under the influence of natural selection, leading to the species exhibiting industrial melanism.
In the salt-and-pepper moth, we know from museum collections that prior to the middle of the 19th century in northern England the moths had pale-colored wings with a speckling of dark dots (the
FIGURE 1 Crypsis illustrated for different insects. (A) An individual of the dry season form of the evening brown, Melanitis leda, resting among dead leaves on the forest floor in the Shimba Hills, Kenya. The insect is at the center with head pointing to the right; forewing length is ca. 4.5 cm. (B) A small moth that resembles a dead patch on a large leaf in a forest in Costa Rica (wing span is ca. 3 cm). (C) The caterpillar of a moth of the family Lasiocampidae resting on a tree trunk in the Shimba Hills, Kenya; it is ca. 6 cm in length and is positioned horizontally, head to the right, in the center of the figure (image has been rotated 90 degrees). (D) The same larva when actively moving in the same direction along a twig.
typical form). Also, up until that time in the early industrial revolution the bark of trees was predominantly pale and covered in epiphytic lichens and algae. The salt-and-pepper moth rests on bark, and females lay their eggs under foliose lichens or in cracks in the bark. The moths are active at night and rely on background matching and crypsis for survival from birds during daylight hours. Survival enables males to mate at night and females to lay their eggs over a number of nights. The gaseous (e.g., sulfur dioxide) and particulate (soot) air pollution produced by industry both killed the epiphytic communities on the trees and blackened the resting surfaces of the moths. The typical, pale-colored moths became more conspicuous. The fully black, melanic form known as carbonaria was not collected until 1848, near Manchester. It may have occurred shortly before through a mutation (producing a new allele of the gene), or perhaps it had already existed for some time in that region as a rare allele. Whatever its precise origin, the carbonaria form rose rapidly in frequency and spread extensively through the industrial regions of Great Britain over the following decades; the adult moth as well as newly emerged larvae can move long distances. Clear geographical associations were established between the amount of air pollution and the frequency of the fully melanic carbonaria and also of several intermediate melanic forms known as insularia.
Up until the mid-20th century this remained a verbal, albeit persuasive, reasoning for the evolution of melanism as an adaptive response to a changed environment. It was only then that some classic early experiments in evolutionary biology began to add scientific rigor to this explanation. Several researchers performed a series of experiments that showed beyond doubt that, whereas the survival of the pale typical form was higher in rural, unpolluted regions of Great Britain than that of the carbonaria form, this relationship is reversed in the polluted industrial environments. Although there have been discussions about the precise details of some of these types of experiments, the fundamental finding of a switch in survival and relative fitnesses (reproductive success) of the pale and dark phenotypes across the extreme environments, principally the result of corresponding changes in crypsis, has been corroborated. Other differences in fitness among the phenotypes that are not directly related to the visual differences in color pattern may also be involved in determining the precise dynamics of the evolution.
There has, however, more recently been an additional finding that proves beyond any doubt the role of evolution by natural selection. Great Britain and other countries in northern Europe have over the past few decades reduced levels of air pollution from soot and gases such as sulfur dioxide. This has in turn led to declines in the frequencies of the melanic forms and the coining of the phrase “evolution in reverse.” As the resting environment returns, at least in a qualitative sense, back toward the original, unpolluted state, the relative fitnesses are also reversed, leading to present-day declines in melanism. Although it has not been precisely quantified, the conclusion must be that in previously polluted regions, while the fully black melanic (carbonaria) has again become conspicuous and vulnerable to birds, the paler typicals have become well camouflaged on the changed background.
ANALYSIS OF CRYPSIS
This example of the salt-and-pepper moth illustrates that cryp-sis still needed to be scientifically measured and fully quantified. In 1984 Endler began to use early techniques of image analysis to mathematically describe how well matched in terms of color patterning were moths in a North American woodland community with respect to different potential resting environments. If crypsis is “optimal” the patterning of the insect will represent a random assemblage of the pattern elements of the background. Endler also pointed out that there will be matching with respect to different components of the color patterns of both insect and resting background, namely, size, color, shape, and brightness. In some backgrounds, such as pine needles or bark with striations, the component of orientation should also be added. Failure to match with respect to any one of these components will lead to mismatching and ineffective crypsis. Because the color vision of many predators, including birds and insects, extends into the ultraviolet part of the spectrum, when color matching in crypsis is considered it often has to include the UV. Researchers have recently begun to use computer-generated patterns, image analysis, and “visual predators” to explore more fully the potential effects of interactions among predators and their prey that lead to the evolution of cryptic color patterns.
Cryptic color patterns may also include an element of banding, which is disruptive and can serve to break up the outline of the prey. Usually, such an element also has to blend into the resting background in terms of the prey representing a random assemblage of its pattern. However, this restriction is perhaps relaxed when crypsis is used only to protect a prey from a distance, such as in the brightly colored, banded moth caterpillars, including the cinnabar, Tyria jacobaeae, and the strikingly striped forewings of some arctiid moths, for example, Callimorpha quadripunctaria.
CRYPSIS AND NATURAL SELECTION
Although testing of these ideas, at least in the context of animal color patterns and their camouflage, has not been completed, Endler has also performed experiments with guppies that dramatically illustrate the power of natural selection to lead to the evolution of effective crypsis. Male guppies can be very colorful with a patterning of bright spots and patches on their lateral flanks and fins. Laboratory experiments in which females can choose whether to mate with males of different patterns show that there is female preference for the more brightly colored males. In the wild in Trinidad, there is a correlation between the degree of color patterning on males in a population and the presence of predatory fish and invertebrates ranging from weak to strong mortality factors on guppies. Male fish are colorful and brightly patterned when either no predators or only weak predators are present, whereas they are drab and unpatterned brown fish when strong predators such as certain cichlids are present. A series of experimental pools with natural backgrounds in a greenhouse was established to examine the efficacy of natural selection on crypsis in this system. Endler showed that guppy populations with the weak predators showed no divergence over subsequent generations in their average color pattern; in contrast, in those pools to which strong predators were added the guppies showed a marked and progressive decline in the brightness and spottiness of the males. This result was highly consistent with selection favoring a more effective crypsis through a lower conspicuousness and improved background matching of the prey populations. In the absence of such strong predators, the balance of sexual selection through female choice and of natural selection by visually hunting predators favors colorful males because they survive to maturity and then achieve a higher mating success than their less colorful competitors.
Such a balance of selection on animal color patterns is probably the norm in natural populations. Thus, in animal communication, a color pattern is usually a compromise between being conspicuous to conspecifics and being poorly visible to predators (or prey). Indeed, one of the potential disadvantages of adopting crypsis as the primary means of survival is that it almost inevitably ties the organism down to a sedentary style of life at least during the hours of daylight. In contrast, when organisms are distasteful and adopt a conspicuous, aposematic lifestyle or when they evolve Batesian mimicry to resemble such warningly colored species, there is no such disadvantage associated with daytime activity.
INTERACTION OF CRYPSIS AND OTHER DEFENSES
In many insects, an organism may not rely only on crypsis for survival. There may be some secondary means of defense once crypsis has failed and the prey has been detected by a potential predator. Insects that are cryptic at a distance but conspicuous when seen close up (including the banded larvae and arctiid moths mentioned above) are often chemically protected. This type of multiple defense is also illustrated by the moth caterpillar in Fig. 1C. If the caterpillar is disturbed and begins to move it can expose a series of glands in the dorsal cuticle of several segments toward the front of the body. These are visible as a pair of partial bands in Fig. 1D ) the largest immediately to the right of the largest white-colored region. These produce a pungent odor and probably provide a potential chemical defense against birds and other predators.
The effectiveness of crypsis will also show complex interactions with the visual processing abilities of the specialist predator or the guild of predators. Some insects that rely on camouflage for survival often exhibit extreme individual variation. One example is the tropical evening brown, Melanitis leda. This large brown butterfly is common throughout the Old World tropics. In wet-dry seasonal environments, the species shows classical seasonal polyphenism (i.e., distinct color patterns that result from phenotypic plasticity), with a wet season form having conspicuous marginal eyespots and a cryptic dry season form without such eyespots. The latter form relies on survival through crypsis on a resting background of dead brown leaves (Fig. 1A). In large numbers of the dry season form it is difficult to find two individuals with exactly the same color pattern. Dramatic variation across individuals is produced by high genetic variation in several different pattern elements across the wing (such as the contrast and brightness of particular patches and bands and the background wing color in different regions). This variation can be interpreted as an evolutionary response involving ” apostatic selection” to make it more difficult for browsing predators in the leaf litter to form a specific “search image” for a particular form of dead leaf pattern corresponding to the color pattern of the prey. Although like many of the detailed ideas about the significance of crypsis and particular animal color patterns, this hypothesis remains to be tested rigorously; it does once again illustrate the fascination of crypsis.
