The cleaner mimic

One of the few cases of mimicry reported among vertebrates is that of a so-called cleaner fish. This example involves a particularly close model imitation involving shape, coloration, and behaviour. The model, a wrasse (Labroides dimidiatus) of the Indo-Pacific Ocean, is known as a cleaner fish because it removes and eats externally attached parasites and, occasionally, damaged skin fragments from other marine fish. It occupies specific sites, or territories, on coral reefs, where, within a six-hour period, the individual cleaner may be visited by up to 300 other fish seeking its services. The other fish are attracted by the conspicuous black and white coloration of the cleaner and by its dancelike swimming pattern, in which the tail fin is spread and the posterior part of the fish oscillates up and down. The fish undergoing cleaning acts as though it were in a trance, while the cleaner fish cleans its body, including the inside of the mouth and gills. Even large predatory fish allow themselves to be cleaned, and the much smaller cleaner almost invariably emerges uninjured from their throats. It is quite apparent that the cleaners are protected from these predators although neither inedible nor capable of self-defense.

At the cleaning stations of the cleaner fish, there is often found quite another fish, the sabre-toothed blenny (Aspidontus taeniatus). It is similar to the cleaner fish in size, coloration, and swimming behaviour, and it even exhibits the same dance as the cleaner. Fish that have had experience with the cleaner position themselves unsuspectingly in front of this mimic, which approaches carefully and bites off a semicircular piece of fin from the victim and eats it. After having been repeatedly bitten in this way, fish become distrustful even toward genuine cleaners. Observations in the wild indicate that younger fish are the principal victims of the mimic, whereas older fish avoid it whenever possible. It is unlikely that the ability to discriminate between the mimic and the model develops automatically with age and is independent of experience; this is borne out by the finding that adult fish kept in an aquarium and not previously exposed to the mimic confuse cleaner and mimic just as younger fish do. If such adult fish are kept with the mimics for a certain length of time, however, they eventually avoid these and the genuine cleaners.

The obvious conclusion from these experiments is that other fish cannot distinguish between the model and the mimic without having had experience with both. Evidently, victims of the mimic seek out and learn characteristics that enable them to distinguish between reliable and unreliable cleaners—that is, between the model and the mimic, respectively. The most successful individuals among the mimics, therefore, are those that most confuse their victims. As a result, the further development of the mimic is steered in the direction determined by the characteristics of the cleaner; for example, the model occurs as a number of local races within its area of distribution, each of which shows its own peculiarities in coloration, such as a small or large black vertical stripe at the base of the pectoral fins or an orange-red spot on the flanks. In every case, the local population of the mimic shows the same special coloration as does the model in that particular area.

One of the interesting and highly unusual aspects of the cleaner–mimic relationship is that the individual characters of the mimicry pattern, especially the behavioral ones, have been traced to their origins. Certain characteristics, such as body size and shape and swimming pattern, amount to chance similarities. The mimic’s drive to approach other fish, for example, is a specialization of a more general pattern, observable in non-mimicking relatives of the blenny, involving searching for food on suitable surfaces. The basic colour pattern of light and dark horizontal stripes is characteristic of fish that swim in open water, but the actual coloration of the mimicking blenny, owing to the forces of natural selection, bears a close resemblance to the cleaner wrasse. Interestingly enough, the blenny alters its coloration with its motivational state and adopts the appearance of the cleaner only under the specific conditions of self-confidence and intent to attack. As a group, blennies tend to wriggle while swimming, in order to counteract a strong tendency to sink at the tail. The sabre-toothed blenny, however, when confronted with danger holds the body stiffly without wriggling, allowing the hindquarters to sink somewhat, and advances solely by the use of the pectoral fins, in the manner common to wrasses. Superimposed on this motion is a nodding of the blenny’s head, which is typical of approach-retreat conflict behaviour in blennies but which results in a simulation of the swaying dance of the cleaner. The combination of coloration and behavioral signals has a particular significance for the experienced visitor to the cleaner’s station and causes it to adopt the posture that invites cleaning. In so doing, the visitor gives the mimic an opportunity to take a bite from a fin.

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community ecology: Mimicry complexes

Fireflies

A form of aggressive mimicry that relies entirely on behaviour occurs in certain North American fireflies (Lampyridae). Males of these familiar nightflying beetles emit light bursts in flight according to highly specific patterns. The females, usually stationary, respond to the flash patterns of males of their own species with specific patterns of their own. The flying male responds to the appropriate female signal by approaching, landing, and courting. Most adult fireflies are short-lived and do not feed at all, but females of the genus Photuris have been found to feed on other beetles, including males of the genus Photinus. Upon perceiving a flashing male Photinus, the female Photuris responds with a flash that mimics the slower response time of the female Photinus. As the male Photinus approaches, the female Photuris even reduces the intensity of her flashes, to resemble more closely the weaker signals of the smaller female Photinus. The hapless male, after landing, is seized and eaten by the Photuris. In response to males of her own species, of course, the female Photuris gives a flash response quite different from that of Photinus.

Cuckoos

The European cuckoo (Cuculus canorus) is a brood parasite; i.e., it lays its eggs in the nests of other birds, which act as foster parents for the young cuckoos. The most frequent foster parents are various species of small songbirds. Although the eggs of the various host species span a great range of colours and spotting, there is a striking correspondence in appearance between the eggs of the cuckoo and those of the host. Most small birds react unfavourably if they perceive a foreign egg in the nest and either abandon the nest, build another nest right over the first, or eject the strange egg. Each female cuckoo consistently lays eggs of one colour pattern and must therefore parasitize a particular host species. One survey has shown that of 1,642 cuckoo eggs laid in the nests of the correct (matching) hosts, only 8 percent were lost, whereas of 298 in the nests of the wrong hosts, 24 percent were lost. It is logical to conclude, therefore, that a cuckoo that lays its egg randomly, leaving the survival of the eggs to chance, would produce fewer offspring than one that selects hosts whose eggs match her own. Although the control of egg coloration is probably genetically determined, the choice of correct hosts is believed to be the result of a learning process that takes place when the female cuckoo is a nestling and learns to recognize her own foster parents.

Parasitic weaverbirds

Brood parasitism is also found in African whydahs, or widow birds, of the subfamily Viduinae of the weaverbird family, Ploceidae. Each species of whydah parasitizes a single species of estrildid (a waxbill or another small finchlike bird in the family Estrildidae). In this case, egg colour does not seem to be a factor in acceptance of the parasite’s egg, because both groups have pure white eggs. It has been argued that the whydah, many relatives of which have spotted eggs, has evolved white eggs in order to match those of its estrildid host.

More significant than the mimicry of egg colour, however, is the highly specific pattern of spots and protuberances at the corners of the mouth (gape) and on the palate, tongue, and lower mandible of the nestling. This pattern, which varies from one species of finch to another, serves as a releaser for feeding behaviour on the part of the parents, which ignore any nestling that does not display the proper pattern for the particular species. In every species of parasitic weaverbird studied, the nestling has been found to match perfectly the mouth pattern of the estrildid host. In addition to mimicking the mouth patterns of their hosts, whydah nestlings also duplicate the specific begging calls and peculiar head movements of their hosts. The coloration of the juvenile plumage of the young whydah is identical to that of the host species, ensuring that the whydah will be fed after fledging. The digestive system of the young whydah is closely adapted to the particular type of food utilized by its host species, unlike that of the young cuckoo, which seems to be able to accept a variety of foods, from insects to mouse meat.

With each species of parasitic weaverbird closely committed to a single species of estrildid, it is obviously important that whydah species not hybridize, for the hybrid offspring would certainly not match either possible host in all of the important features. It is surprising to find seven forms of the paradise whydah (Steganura) so similar in appearance that they were once considered races of one species. Each of the seven, however, has its own estrildid host species, indicating that seven species of paradise whydah are represented.

As is frequently the case with closely similar bird species, hybridization is effectively prevented through the use of species-specific vocalizations by the males. An unusual feature of this situation is that each whydah species uses the same vocal pattern as its estrildine host. The young parasitic weaverbirds learn the songs of their host species during the critical learning period common to songbirds generally. As adults, the male whydahs use these estrildid vocalizations and gain response only from females that have been reared by the same foster species. This example is the only known one of a species-isolating mechanism consisting of vocalizations learned from another species. Vocal imitations by some bird species that have not been shown to give rise to mimicry systems are nevertheless frequently called mimicry.