Bates observed, but could not explain, a resemblance among several unrelated butterflies, including danaids (see milkweed butterfly), all of which were known to be inedible. There seemed to be no reason for these species, each of which had an ample defense with which to back up the warning coloration, to be similar. In 1878 Fritz Müller, a German zoologist, suggested that an explanation for this so-called Bates’s paradox might lie in the advantage to one inedible species in having a predator learn from another. Once the predator has learned to avoid the particular colour pattern with which it had its initial contact, it would then avoid all other similarly patterned species, edible and inedible. The initial learning experience of the predator often results in death or damage to the inedible individual that provided the lesson; there is thus some cost to the species that teaches the predator of its inedibility. Evidence indicates that there is little or no inherited recognition by certain predators; each individual learns of noxious or inedible species by sampling them. Other inedible species resembling the first, however, do not have to sacrifice individuals to teach this same predator, and the number of individuals sacrificed in educating the entire predator population is spread over all of the species sharing the same warning pattern. The tendency of inedible or noxious species to resemble each other is called Müllerian mimicry.
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In some situations it is of advantage to a predator to resemble its prey, or a parasite its host. Aggressive mimicry, for which the phrase “a wolf in sheep’s clothing” is an apt description, does not involve warning mechanisms. The mimic adopts certain of the recognition marks of its model in order to secure advantage over the model itself or over a third species that interacts with the model. The model may be mimicked during only a single stage of the life cycle, as in the case of parasitic cuckoos, the eggs of which resemble those of their hosts (see below The occurrence of mimicry among plants and animals), or the model may be a prey of the mimic’s victim, as in the case of anglerfishes, which possess rodlike spines tipped with a fleshy “bait” to lure other fishes within reach.
The phenomenon of automimicry involves the advantage gained by some members of a species from its resemblance to others of the same species. Males of many bees and wasps, although defenseless, are protected from predators by their resemblance to females that are equipped with stingers. Some butterflies are able to gain protection against predators through the ability to absorb, tolerate, and retain in the immature (larval) stage, poisons from the plants on which they feed. Individuals or even subpopulations of such butterflies may fail to acquire such protection, as a result of feeding on nonpoisonous plants, but they are avoided by predators that have sampled protected individuals of the same species.
Many forms of mimicry do not fit neatly into any of the above categories. The roles of mimic, model, and receiver may be juxtaposed and multiplied to provide intricate and remarkable relationships, the unraveling of which may take years of study. One such case involves the South American coral snakes (Micrurus), long recognized as dangerously poisonous—which possess a brilliant red, black, and yellow ringed pattern—and several genera of nonpoisonous and mildly poisonous “false coral snakes” with nearly identical colour patterns.
Müllerian mimicry involving (left) the venomous Eastern coral snake Micrurus fulvius, (right) the harmless king snake Lampropeltis polyzone, and (bottom) the moderately venomous rear-fanged false coral snake (Oxyrhopus).
The chemical basis for repulsion
Many plants are characterized by the production of large amounts of metabolic end products, often called secondary metabolites—complex chemicals that include alkaloids, terpenes, phenylpropanes, resins, lignins, saponins, flavonols, and anthocyanins—stored in the plant tissues. Many such substances are also found in animals that feed upon such plants. Some animals produce substances similar to the secondary metabolites of plants; they store these substances in glandular pockets (as in toads, salamanders, and some insects) or in musk glands (as in beavers and muskrats). Arthropods, particularly insects, are notable for the production of excretory substances that serve as means of defense. Millipedes of the family Glomeridae, for example, secrete a bitter substance (a quinazoline) that repels birds; similar substances, differing only slightly in molecular structure, are found in palms. The fact that a certain chemical substance is restricted to a specific function, such as sex attraction, does not necessarily mean that it was evolved solely for that purpose. It seems rather that natural selection follows the easiest course and makes use of substances already present and sometimes widely distributed. If so, the appearance of such substances in other organisms is not too surprising.
Among the chemical compounds that protect certain plants from insects or other animals that might feed on them are the cardenolides, or cardiac glycosides. These substances have a highly specific toxic effect on the vertebrate heart and also activate the nerve centre in the brain that causes vomiting. Because the amount necessary to cause vomiting is about half the amount necessary to cause death through heart failure, an animal that samples a plant containing cardenolides is not killed but survives with the knowledge that the plant is inedible. Certain milkweeds (Asclepias) that contain cardenolides are the primary food of the larvae of danaine butterflies, including the familiar monarch and queen butterflies (Danaus plexippus and D. gilippus). The larvae consume the poison without ill effects and retain it through the pupal stage to adulthood. As adult butterflies, they enjoy protection from vertebrate predators.
There is, of course, no such thing as complete protection. Just as danaine larvae are able to eat the protected milkweeds, some predators are able to prey upon the protected butterflies. Birds of the Old World bee-eater family (Meropidae) and a few other birds are able to eat bees because the horny beak protects them from being stung while the insect is being killed and because they have evolved behavioral mechanisms for removing the stinger (usually by wiping the insect on a perch) before swallowing the prey. Rabbits are able to eat the extremely poisonous mushrooms of the genus Amanita without ill effects. The larvae of the Florida feather moth (Trichoptilus parvulus) consume the insect-trapping glands on the leaves of the sundew (Drosera).
The evolution of warning systems
The selective advantage of warning
When an organism possesses a mechanism that provides protection from predators, there is a further advantage in preventing the potential predator from even sampling the protected organism. By the act of learning of the danger, the predator may well kill or maim the individual if, for instance, the protected species must be tasted for its inedibility to become known. Many protected insects are provided with tougher skins than their unprotected relatives, but the sampling by a vertebrate predator is almost sure to do some damage. Many noxious organisms have evolved warning (aposematic) mechanisms that serve to identify them clearly to a predator who has had prior experience with the same or similar species.
Warning systems often rely primarily on bright colours, but these may be supplemented by olfactory, acoustic, or behavioral means. The New World skunks, for example, have a prominent black and white pattern that renders them clearly recognizable to potential nocturnal predators. When threatened, skunks perform a highly stylized display dance, thus ensuring that the predator will see and recognize the warning coloration.
Acoustic warning signals are often favoured over visual ones because they allow the animal the option of remaining hidden. The rattlesnakes (Crotalus and relatives), which need protective coloration to avoid alerting their prey, are able to provide acoustic warning to large animals that threaten them. Many moths of the families Arctiidae and Ctenuchidae are foul-tasting but would be vulnerable to nocturnal predation by bats were it not for the emission of a series of high-pitched clicks, audible to bats, made when the moths hear the bats’ own ultrasonic navigational pulses. That the moth clicks actually do serve as warnings is borne out by the fact that captive bats ignore thrown mealworms (which they normally eat) when the mealworms are accompanied by recorded moth clicks. Several species of edible moths also produce clicks and may be regarded as Batesian mimics of the unpalatable species.
The role of the receiver
In some cases, the animal who serves as the receiver of the warning signal reacts by means of an innate system that exists independently of experience. Generally, however, a predator must learn the significance of the warning signal through experience. If the predator is a slow learner, or if the warning signal is not sufficiently distinct to avoid confusion with beneficial sensory impressions that the predator receives, several experiences may be necessary. Natural selection, therefore, will favour warning systems that are devoid of ambiguity. Experimentation has shown that certain birds and mammals, at least, are capable of acquiring and retaining knowledge of some aposematic mechanisms from a single experience.
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Combination of warning systems with concealing coloration
It is of obvious advantage for an aposematic organism to be able to control the display of the warning system, partly to minimize the amount of sampling, with its concomitant liability of injury, by naive receivers. Acoustic and chemical warning systems allow this. Many protected animals are coloured to match their backgrounds but provided with flash areas of warning coloration. Examples of these organisms are the tiger moths (certain of the Arctiidae), in which the hind wings are yellow or orange but are kept under the streaked brown forewings until the moth is molested.