Aggressive mimicry

The Humpback anglerfish uses a modified dorsal spine as a bioluminescent 'fishing rod' to capture prey.

Aggressive mimicry is a form of mimicry where predators, parasites or parasitoids share similar signals with a harmless model, allowing them to avoid being correctly identified by their prey or host. In its broadest sense, it involves any type of exploitation, such as an orchid exploiting a male insect by mimicking a sexually receptive female (see pseudocopulation),^[1] but will here be restricted to forms of exploitation involving feeding. The alternative term Peckhamian mimicry (after George and Elizabeth Peckham^[2][3]) has also been suggested,^[4] but it is seldom used.^[5] The metaphor of a wolf in sheep's clothing can be used as an analogy, but with the caveat that mimics are not intentionally deceiving their prey. For example, indigenous Australians who dress up as and imitate kangaroos when hunting would not be considered aggressive mimics, nor would a human angler. Treated separately is molecular mimicry, which also shares some similarity; for instance a virus may mimic the molecular properties of its host, allowing it access to its cells.

Aggressive mimicry is opposite in principle to defensive mimicry, where the mimic generally benefits from being treated as harmful. The mimic may resemble its own prey, or some other organism which is beneficial or at least not harmful to the prey. The model, i.e. the organism being 'imitated', may experience increased or reduced fitness, or may not be affected at all by the relationship. On the other hand, the signal receiver inevitably suffers from being tricked, as is the case in most mimicry complexes.

Aggressive mimicry often involves the predator employing signals which draw its potential prey towards it, a strategy which allows predators to simply sit and wait for prey to come to them. The promise of food or sex are most commonly used as lures. However, this need not be the case; as long as the predator's true identity is concealed, it may be able to approach prey more easily than would otherwise be the case. In terms of species involved, systems may be composed of two or three species; in two-species systems the signal receiver, or "dupe", is the model.

In terms of the visual dimension, distinction between aggressive mimicry and camouflage is not always clear. Authors such as Wickler^[4] have emphasized the significance of the signal to its receiver as delineating mimicry from camouflage. However, it is not easy to assess how 'significant' a signal may be for the dupe, and the distinction between the two can thus be rather fuzzy. Mixed signals may also be employed. Aggressive mimics often have a specific part of the body sending a deceptive signal, with the rest being hidden or camouflaged.

Comparison with other forms of mimicry

Batesian mimics, like this bumblebee-mimicking hoverfly, are the antithesis of aggressive mimics.

Mimicry that is aggressive stands in semantic contrast with defensive mimicry, forms of mimicry where it is the prey that acts as a mimic, with predators being duped. Defensive mimicry includes the well-known Batesian and Müllerian forms of mimicry, where the mimic shares outward characteristics with an aposematic or harmful model. In Batesian mimicry, the mimic is modeled on a dangerous (usually unpalatable) species, while in Müllerian mimicry both species are harmful, and act as comimics, converging on a common set of signals and sharing the burden of 'educating' their predators. Also included in defensive mimicry is the lesser known Mertensian mimicry, where the mimic is more harmful than the model, and Vavilovian mimicry, where weeds come to mimic crops through unintentional artificial selection. In defensive mimicry, the mimic benefits by avoiding a harmful interaction with another organism that would be more likely to take place without the deceptive signals employed. Harmful interactions might involve being eaten, or pulled out of the ground as a weed. In contrast, the aggressive mimic benefits from an interaction that would be less likely to take place without the deception, at the expense of its target. However, it is important to note that there are other forms of mimicry that are described by the previous sentence, which are not aggressive mimicry—flowers exploiting a pollinator with deceptive signals, for example. There is no analogous word that encompasses all such cases of mimicry, however (see Pasteur, 1982 for a review of classification).^[6]

Classification

Luring prey

In some cases the signal receiver is lured toward the mimic. This involves mimicry of a resource that is often vital to the prey's survival (or more precisely, the survival of its genes) such as nutrition or a mate. If the bait offered is of little value to prey they would not be expected to take such a risk. For example in all known cases of sexual signal mimicry it is always the male sex that is deceived (in fact, it has been suggested that females of some species have evolved mimicry as a strategy to avoid unwanted matings).^[7] In these cases the predator need not move about foraging for prey, but may simply stay still and allow prey to come to it.

Some studies suggest that the Northern Shrikes (Lanius excubitor) sings in winter often imitating small passerines that may be preyed upon when lured within reach.^[8]

There has been one report of a margay using mimicry of the cry of an infant pied tamarin to try to lure an adult tamarin within striking distance.^[9]

Food as an attractant

The Alligator Snapping Turtle uses its tongue to lure fish.

Many aggressive mimics use the promise of nourishment as a way of attracting prey. Though apparent to observers, the irony of falling prey when trying to capture its own is certainly lost on the deceived animal. The Alligator Snapping Turtle (Macrochelys temminckii) is a well-camouflaged ambush predator. Its tongue bears a conspicuous pink extension that resembles a worm and can be wriggled around;^[10] fish that try to eat the "worm" are themselves eaten by the turtle. Similarly, some snakes employ caudal luring (tail luring) to entice small vertebrates into striking range.

Argiope argentata and its web.

Aggressive mimicry is also common amongst spiders, both in luring prey and stealthily approaching predators.^[11] One case is the Golden Orb Weaver (Nephila clavipes), which spins a conspicuous golden colored web in well-lit areas. Experiments show that bees are able to associate the webs with danger when the yellow pigment is not present, as occurs in less well-lit areas where the web is much harder to see. Other colors were also learned and avoided, but bees seemed least able to effectively associate yellow pigmented webs with danger. Yellow is the color of many nectar bearing flowers, however, so perhaps avoiding yellow is not worth while. Another form of mimicry is based not on color but pattern. Species such as Argiope argentata employ prominent patterns in the middle of their webs, such as zigzags. These may reflect ultraviolet light, and mimic the pattern seen in many flowers known as nectar guides. Spiders change their web day to day, which can be explained by bee's ability to remember web patterns. Bees are able to associate a certain pattern with a spatial location, meaning the spider must spin a new pattern regularly or suffer diminishing prey capture.^[12]

Spiders can also be the prey of aggressive mimics. The assassin bug Stenolemus bituberus preys on spiders, entering their web and plucking its silk threads until the spider approaches. This vibrational aggressive mimicry matches a general pattern of vibrations which spiders treat as prey, having a similar temporal structre and amplitude to leg and body movements of typical prey caught in the web.^[13]

The bright leaves of the venus flytrap (Dionaea muscipula) attract insects in the same way as flowers.

Although plants are better known for defensive mimicry, there are exceptions. For example, many flowers use mimicry to attract pollinators, while others may trick insects into dispersing their seeds. Nonetheless, most mimicry occurring in plants (for an overview see Wiens, 1978^[14]) would not be classified as aggressive, as although luring pollinators etc. is similar to cases above, they are certainly not eaten by the plant. However some carnivorous plants may be able to increase their rate of capture through mimicry.^[15] For example, some have patterns in the ultraviolet region of the electromagnetic spectrum, much like the spider webs described above.^[16]

Aggressive mimicry involving two species

Mimicry systems involving only two species are known as bipolar.^[6] Only one bipolar arrangement is possible here: that where the dupe is itself the model.^[17] There are two such variants on this arrangement of mimic imitating its target, in the first case, termed Batesian-Wallacian mimicry^[6] after Henry Walter Bates^[18] and Alfred Russell Wallace,^[19] the model is the prey species. Similarly, the model is the host of a brood parasite in the second such case.

Batesian-Wallacian

In some cases of Batesian-Wallacian mimicry, the model is a sexually receptive female, which provides a strong attractive effect on males. Some spiders use chemical rather than visual means to ensnare prey. Female bolas spiders of the genus Mastophora allure male moths by producing analogues of the moth species' sex pheromones. Each species of spider appears to specialize in a particular species of prey in the family Psychodidae. Juveniles use their front pair of legs to capture prey, such as flies. Older spiders use a different strategy however, swinging a sticky ball known as a bolas suspended by a silk thread at moths. But both old and juvenile are able to lure prey items via this olfactory signal; even young spiderlings have been shown to attract prey species.^[20]

Beginning in the 1960s, James E. Lloyd's investigation of female fireflies of the genus Photuris revealed they emit the same light signals that females of the genus Photinus use as a mating signal.^[21] Further research showed male fireflies from several different genera are attracted to these mimics, and are subsequently captured and eaten. Female signals are based on that received from the male, each female having a repertoire of signals matching the delay and duration of the female of the corresponding species. This mimicry may have evolved from non-mating signals that have become modified for predation.^[22]

The Spotted Predatory Katydid (Chlorobalius leucoviridis) is an acoustic aggressive mimic of cicadas.

The listroscelidine katydid Chlorobalius leucoviridis of inland Australia is capable of attracting male cicadas of the Tribe Cicadettini by imitating the species-specific reply clicks of sexually receptive female cicadas. This example of acoustic aggressive mimicry is similar to the Photuris firefly case in that the predator’s mimicry is remarkably versatile – playback experiments show that C. leucoviridis is able to attract males of many cicada species, including Cicadettine cicadas from other continents, even though cicada mating signals are species-specific. The evolution of versatile mimicry in C. leucoviridis may have been facilitated by constraints on song evolution in duetting communication systems in which reply signals are recognizable only by their precise timing in relation to the male song (<< 100 ms reply latency).^[23][24]

Host mimicry by brood parasites

Though less than obvious here, brood parasites mimic certain qualities of their host species.

Further information: Brood parasitism

Host-parasite mimicry is a situation where a parasite mimics its own host. As with mimicry of the female sex outlined previously, only two species are involved, the model and mimic being of the same species. Brood parasitism, a form of kleptoparasitism where the mother has its offspring raised by another unwitting organism, is one such situation where host-parasite mimicry has evolved. Pasteur^[6] terms this form of aggressive-reproductive mimicry Kerbyan mimicry, after the English entomologist William Kirby.^[25]

Mimicry of mutualistic species

Two Bluestreak cleaner wrasse cleaning a Potato grouper, Epinephelus tukula

Attraction of the target toward the mimic is not seen in all aggressive mimicry systems. The predator will still have a significant advantage by simply not being identified as such. Such mimics may resemble a mutualistic ally, or a species of little significance to the prey.

The former situation has been termed Wicklerian-Eisnerian mimicry.^[6] This involves the mimic resembling a species that is an important partner of the dupe, whether they live together or not. A case of the latter situation is a species of cleaner fish and its mimic, though in this example the model is greatly disadvantaged by the presence of the mimic. Cleaner fish are the allies of many other species, which allow them to eat their parasites and dead skin. Some allow the cleaner to venture inside their body to hunt these parasites. However, one species of cleaner, the Bluestreak cleaner wrasse (Labroides dimidiatus), is the unknowing model of a mimetic species, the Sabre-toothed blenny (Aspidontus taeniatus). This wrasse, shown to the left cleaning a grouper of the genus Epinephelus, resides in coral reefs in the Indian and the Pacific Oceans, and is recognized by other fishes who then allow it to clean them. Its imposter, a species of blenny, lives in the Indian Ocean and not only looks like it in terms of size and coloration, but even mimics the cleaner's 'dance'. Having fooled its prey into letting its guard down, it then bites it, tearing off a piece of its fin before fleeing the scene. Fish grazed upon in this fashion soon learn to distinguish mimic from model, but because the similarity is close between the two they become much more cautious of the model as well, such that both are affected. Due to victim's ability to discriminate between foe and helper, the blennies have evolved close similarity, right down to the regional level.^[26]

Cryptic aggressive mimicry

The Zone-tailed Hawk resembles the Turkey Vulture in flight.

Another case is cryptic mimicry, where the predator mimics an organism that its prey is indifferent to. Unlike in all cases above, the host is ignored by prey, allowing it to avoid detection until prey are close enough to strike. This is in principle very similar to camouflage, and is known as mimesis. The Zone-tailed Hawk (Buteo albonotatus), which resembles the Turkey Vulture (Cathartes aura), may provide one such example. It flies amongst them, suddenly breaking from the formation and ambushing its prey.^[27] Here the hawk's presence is of no evident significance to the vultures, affecting them neither negatively or positively. There is some controversy over whether this is a true case of mimicry.^[28]

Parasites mimicking host prey

Some of the predators described above have a feature that lures prey, and likewise some parasites mimic their host's natural prey, but in this case the roles are reversed; the parasite gets eaten by the host. This deception provides the parasite easy entry into the host, which they can then feed upon, allowing them to continue their life cycle. Researchers may be able to predict the host of such parasites based on their appearance and behavior.^[29]

One such case is a genus of shellfish, Lampsilis, which feeds on the gills of fish in the larval stage of their development. Once they mature, they leave the fish as adult mollusc. Gaining entry into the host is not an easy task though, despite the fact that several hundred thousand larvae are released at once.^[4] This is especially the case in flowing water bodies such as streams, where they cannot lie on the substrate and wait to be taken up in the course of foraging. Female shellfish have evolved a special technique for delivering their offspring into a suitable host, however. Structures on the edge of the mantle are able to capture the interest of fish. Some resemble small fish themselves, with eye spots, a 'tail' and horizontal stripes, and may even move in a similar fashion, as if facing the current (rheotaxis). When overshadowed by a fish, the larvae are forcefully expelled, becoming ectoparasites on their unsuspecting host.

Cercaria mirabilis, a trematode, has an especially large larval stage (known as a cercaria) which looks much like a small crustacean or mosquito larva. It also mimics the locomotory behavior of such animals, allowing it to be eaten by predaceous fish.^[29]

Another parasitic trematode example is seen in a terrestrial setting. Leucochloridium is a genus of flatworm (phylum Platyhelminthes) which matures in the intestine of songbirds. Their eggs pass out of the bird in the feces and are then taken in by Succinea, a terrestrial snail that lives in moist environments. The eggs develop into larvae inside this intermediate host, and then must find their way into the digestive system of a suitable bird. The problem here is that these birds do not eat snails, so the sporocyst must find some way of manipulating its future host into eating it. Unlike related species, these parasites are brightly colored and able to move in a pulsating manner. A sporocyst sac forces its way into the snail's eye stalks, and pulsates at high speed, enlarging the tentacle in the process.^[30] It also affects the host's behavior: the snail moves towards light, which it usually avoids. These combined factors make the sporocysts highly conspicuous, such that they are soon eaten by a hungry songbird. The snail then regenerates its tentacles, and Leucochloridium carries on with its life cycle.^[4]

See also

• Antipredator adaptation
• Apparent death

Further reading

• Wickler, W. (1968) Mimicry in Plants and Animals (Translated from the German) McGraw-Hill, New York. ISBN 0-07-070100-8. Pages 123-220 discuss aggressive mimicry.
• Pietsch, T. W.; Grobecker, D. B. (1978). "The Compleat Angler: Aggressive Mimicry in an Antennariid Anglerfish". Science 201 (4353): 369–370. doi:10.1126/science.201.4353.369. 
• Lloyd, J. E. (1981). "Mimicry in the sexual signals of fireflies". Scientific American 245: 110–1. 
• Nicolai, J. (1974) Mimicry in parasitic birds. Scientific American 231 :93-98.

References

1. ^ Wickler, W. (1965). "Mimicry and the evolution of animal communication". Nature 208 (5010): 519–21. doi:10.1038/208519a0. 
2. ^ Peckham, E. G. (1889). "Protective resemblances of spiders". Occasional Papers of Natural History Society of Wisconsin 1: 61–113. 
3. ^ Peckham, E. G.; Peckham, G. W. (1892). "Ant-like spiders of the family Attidae". Occasional Papers of Natural History Society of Wisconsin 2: 1–84. 
4. ^ ^{a b c d} Wickler, W. 1968. Mimicry in plants and animals. McGraw-Hill, New York
5. ^ Pasteur (1982) describes the term as redundant, and points out that there are many different forms of aggressive mimicry. The term was also used earlier by Bates (1862) and Kirby & Spence (1823).
6. ^ ^{a b c d e} Pasteur, Georges (1982). "A classificatory review of mimicry systems". Annual Review of Ecology and Systematics 13: 169–199. doi:10.1146/annurev.es.13.110182.001125. 
7. ^ Fincke, O. M. (2004). "Polymorphic signals of harassed female odonates and the males that learn them support a novel frequency-dependent model". Animal behaviour 67 (5): 833–845. doi:10.1016/j.anbehav.2003.04.017. 
8. ^ Atkinson, Eric C. (1997) Singing for your supper: acoustical luring of avian prey by Northern Shrikes. The Condor 99:203-206 PDF
9. ^ Calleia, F. O.; Rohe, F.; Gordo, M. (June 2009). "Hunting Strategy of the Margay (Leopardus wiedii) to Attract the Wild Pied Tamarin (Saguinus bicolor)". Neotropical Primates (Conservation International) 16 (1): 32–34. doi:10.1896/044.016.0107. http://www.primate-sg.org/PDF/NP16.1.pdf. Retrieved 2010-07-18. 
10. ^ Spindel, E. L.; Dobie, J. L.; Buxton, D. F. (2005). "Functional mechanisms and histologic composition of the lingual appendage in the alligator snapping turtle, Macroclemys temmincki (Troost) (Testudines: Chelydridae)". Journal of Morphology 194: 287–301. 
11. ^ Jackson, R. R. (1995). "Eight-legged tricksters: Spiders that specialize at catching other spiders". BioScience 42: 590–98. 
12. ^ Craig, C. L. (1995). "Webs of Deceit". Natural History 104 (3): 32–35. 
13. ^ Wignall, A.E.; Taylor, P.W. (2010). "Assassin bug uses aggressive mimicry to lure spider prey". Proceedings of the Royal Society B 278 (1710): published online before print October 27. doi:10.1098/rspb.2010.2060. 
14. ^ Wiens, Derbert (1978). "Mimicry in plants". Evolutionary Biology 11: 364–403. 
15. ^ Moran, Jonathan A. (1996). "Pitcher dimorphism, prey composition and the mechanisms of prey attraction in the pitcher plant Nepenthes rafflesiana in Borneo". Journal of Ecology 84 (4): 515–525. doi:10.2307/2261474. 
16. ^ Joel, D. M.; Juniper, B. E.; Dafni, A. (1985). "Ultraviolet Patterns in the Traps of Carnivorous Plants". New Phytologist 101 (4): 585–593. doi:10.1111/j.1469-8137.1985.tb02864.x. 
17. ^ The only theoretical possibilities outside this scope are a) a two species system with a model-mimic - perhaps a predator pretending to be a sleeping predator (this also stretches the usual scope of mimicry somewhat); and b) a cannibalistic species where a cannibalistic organism individual mimics another species.
18. ^ Bates, H. W. (1862). "Contributions to an insect fauna of the Amazon valley. Lepidoptera: Heliconidae". Transactions of the Linnean Society 23 (3): 495–566. doi:10.1111/j.1096-3642.1860.tb00146.x. 
19. ^ Wallace, A. R. (1870) Mimicry, and other protective resemblances among animals. In Contributions to the Theory of Natural Selection. A Series of Essays, pp. 45-129. London: Macmillan.
20. ^ Yeargan, K. V.; Quate, L. W. (1996). "Juvenile bolas spiders attract psychodid flies". Oecologia 106 (2): 266–271. doi:10.1007/BF00328607. 
21. ^ Lloyd, J. E. (1965) Aggressive Mimicry in Photuris: Firefly Femmes Fatales Science 149:653-654.
22. ^ Lloyd, J. E. (1975). "Aggressive Mimicry in Photuris Fireflies: Signal Repertoires by Femmes Fatales". Science 187 (4175): 452–453. doi:10.1126/science.187.4175.452. PMID 17835312. 
23. ^ Marshall, D. C.; Hill, K. B. R. (2009). Chippindale, Adam K.. ed. "Versatile Aggressive Mimicry of Cicadas by an Australian Predatory Katydid". PLoS One 4 (1): e4185. doi:10.1371/journal.pone.0004185. PMC 2615208. PMID 19142230. http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pmcentrez&artid=2615208. 
24. ^ Pain, S.. 2009. Monster insect mimc lures prey with siren song. New Scientist 23 September 2009.
25. ^ Kirby, W., Spence, W. 1823. An Introduction to Entomology, vol. 2. London: Longman, Hurst, Rees, Orme & Brown. 3rd ed.
26. ^ Wickler, W. (1966). "Mimicry in Tropical Fishes". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 251 (772): 473–474. doi:10.1098/rstb.1966.0036. 
27. ^ Willis, E. O. (1963). "Is the Zone-Tailed Hawk a Mimic of the Turkey Vulture?". The Condor 65 (4): 313–317. doi:10.2307/1365357. 
28. ^ Clark, William S. (2004). "Is the Zone-tailed Hawk a Mimic?". Birding 36 (5): 495–498. 
29. ^ ^{a b} Wickler, Wolfgang (1998). “Mimicry”. Encyclopædia Britannica, 15th edition. Macropædia 24, 144–151. http://www.britannica.com/eb/article-11910
30. ^ See here for a photo.

External links

• Feeding behavior of the frogfishes (Antennariidae) Description, images and video of aggressive mimicry in frogfish.
• Acoustic aggressive mimicry of cicadas by an Australian predatory katydid..