Deception in Animals

mimic octopus

apparent death

Deception in animals is the giving of information by one animal to another, of the same or different species, in a way that propagates beliefs that are not true. Deception in animals does not automatically imply conscious mind, but can occur at different levels. Mimicry and camouflage enable animals to appear to be other than they are. Prey animals may appear as predators, or vice versa; both predators and prey may be hard to see (crypsis), or may be mistaken for other objects (mimesis). In Batesian mimicry, harmless animals may appear to be distasteful or poisonous. In automimicry, animals may have eyespots in less important parts of the body than the head, helping to distract attack and increase the chance of survival.

More actively, animals may feign death when they detect a predator, or may quickly conceal themselves or take action to distract a predator, such as when a squid releases ink. In deimatic behavior, a harmless animal adopts a threatening pose or displays startling, brightly colored parts of its body to startle a predator or rival. Some animals may use tactical deception, behavior that is deployed in a way that other animals misinterpret (to the advantage of the agent). Some of the evidence for this is anecdotal, but in the great apes in particular, experimental studies suggest that deception is actively practiced.

Some types of deception in animals are completely involuntary (e.g. disruptive coloration), but others are under voluntary control and may involve an element of learning. Most instances of voluntary deception in animals involve a simple behavior, such as a cat arching its back and raising its hackles, to make itself appear larger than normal when attacked. There are relatively few examples of animal behavior which might be attributed to the manipulative type of deception which we know occurs in humans. It has been argued that true deception assumes the deceiver knows that (1) other animals have minds, (2) different animals’ minds can believe different things are true (when only one of these is actually true), and (3) it can make another mind believe that something false is actually true. These criteria indicate that true deception is not a trivial achievement. The deceiver needs to have the mental capacity to assess different representations of reality. Animal behavior scientists are therefore wary of attributing a single instance of behavior to true deception, and explain it with simpler mental processes such as learned associations. In contrast, human activities such as military deception are certainly intentional, even when they involve methods such as camouflage which physically directly parallel camouflage methods used by animals.

There are four levels of deception in animals: level one (false markings), level two (false behavior), level three (feigned injury), and level four (verbal deception).

Mimicry is the similarity of one species to another which protects one or both species. This similarity can be in appearance, behavior, sound, scent, and location, with the mimics found in similar places to their models. There are many forms of mimicry, and an individual example may fall into more than one of the recognized categories. Defensive or protective mimicry takes place when organisms are able to avoid encounters that would be harmful to them by deceiving enemies into treating them as something else. Batesian mimicry is a form of mimicry typified by a situation where a harmless species has evolved to imitate the warning signals of a harmful species directed at a common predator. The harmful species (the model) might have spines, stingers, or toxic chemistry, while its apparent double has no defense other than resembling the unpalatable species. Protection of the mimic from predators is afforded by its resemblance to the unpalatable species which the predator associates with a certain appearance and a bad experience.

Examples of Batesian mimicry are the several species of butterflies that mimic the toxic Heliconid butterflies. Another butterfly mimic is the non-toxic Great Mormon of Indonesia. Each female butterfly (regardless of her coloration) can produce one or more different female forms which mimic any of five other species of foul-tasting butterflies. Batesian mimicry is also found in venomous coral snakes and the harmless milk snake. Both snakes are marked with alternating yellow, red, and black bands causing potential predators to avoid both. The snakes can often be distinguished by using an old saying: ‘Red against yellow: kill a fellow. Red against black: friend to Jack.’ Deception by Batesian mimicry need not involve visual mimicry, but can be deception of any of the senses. For example, some moths use a highly effective defence against bats: in response to hearing ultrasound emitted by hunting bats, they produce loud ultrasonic clicks to mimic the unpalatable tiger moth – a case of auditory Batesian mimicry.

Müllerian mimicry occurs when two or more poisonous species, that may or may not be closely related and share one or more common predators, have come to mimic each other’s warning (aposematic) signals. For example, to the viceroy butterfly appears very similar to the noxious-tasting monarch butterfly. Although it was for a long time purported to be an example of Batesian mimicry, the viceroy has recently been discovered to be just as unpalatable as the monarch, making this a case of Müllerian mimicry. Poison dart frogs of South America and Mantella frogs of Madagascar are examples of Müllerian mimicry with their conspicuous colouration of bright colors against black markings and toxic composition.

Aggressive mimicry describes predators (or parasites) which share the same characteristics as a harmless species, allowing them to avoid detection by their prey (or host). For example, anglerfish are named for their characteristic method of predation. They typically have at least one long filament (the illicium) sprouting from the middle of the head, protruding above the fish’s eyes and terminating in an irregular growth of flesh (the esca) at the tip of the filament. The filament is moveable in all directions and the esca can be wiggled so as to resemble a prey animal thus acting as bait to lure other predators close enough for the anglerfish to devour them whole. Some deep-sea anglerfishes of the bathypelagic zone emit light from their escas to attract prey. This bioluminescence is a result of symbiosis with bacteria.

Another example of aggressive mimicry is where males are lured towards what would seem to be a sexually receptive female only to be eaten. Studies on female fireflies of the genus Photuris revealed they emit the same light signals that females of the genus Photinus use as a mating signal. Further research showed male fireflies from several different genera are attracted to these ‘femmes fatales,’ 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. However, aggressive mimicry need not involve the sense of vision. The assassin bug 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 structure and amplitude to leg and body movements of typical prey caught in the web.

Automimicry, or intraspecific mimicry, is when animals have one body part that mimics another to increase survival during an attack, or helps predators appear innocuous. Many moth, butterfly and fish species have ‘eye-spots’: large dark markings that help prey escape by deceiving predators to attack a false target. An animal has a better chance of surviving an attack to the outer part of its body than an attack to the head. Among moths showing automimicry, the eyed hawkmoth displays its large eyespots on its wings and moves them slowly as if it were a vertebrate predator such as an owl. Another example of automimicry is the ‘two-headed’ snake of Central Africa, which has a tail that resembles a head and a head that resembles a tail. The snake even moves its tail in the way most snakes move their heads. This adaptation functions to deceive prey into believing the attack is originating from where it is not.

Camouflage is the use of any combination of materials, colouration or illumination for concealment, by making animals difficult to see (crypsis), or by disguising them as something else (mimesis). This can be as simple as having green skin or pelage coloration for a background of foliage, a nest whose shape, emissions and entries are all disguised by local materials (dirt, twigs, stones, etc.), or as complex as an animal actively changing its appearance according to the changing background. There are several methods of achieving crypsis. These include, resemblance to the surroundings, disruptive coloration, eliminating shadow, self-decoration, cryptic behavior, motion camouflage, changeable skin appearance, countershading, counter-illumination, transparency, and silvering to reflect the environment.

There are many examples of species which are cryptically colored to resemble their surroundings. For example, the Uroplatus geckos are masters of disguise and can be almost totally unnoticeable, even to a nearby observer. Similarly, the katydids, a group of grasshopper-like insects found worldwide, are nocturnal and use their cryptic coloration to remain unnoticed during the day. They remain perfectly still, often in a position that increases the effectiveness of their camouflage.

Some animals have disruptive coloration in which their colors or patterning appear highly conspicuous when outside their normal environment but highly cryptic when in it. For example, the blue Morpho, a forest butterfly, has iridescent blue upper wings and a 17 cm wingspan. However, because the underwings are dark, when the Morpho flies through the flickering light of the forest or even out in daylight, it seems to disappear. Other forest species, especially mammals, use disruptive coloration and have spotted or striped pelage which helps break up the animal’s outline. In the shade created by trees or other foliage, even large mammals such as leopards, jaguars, ocelots, and okapi are surprisingly difficult to see because of their disruptive coloration.

Most forms of camouflage are ineffective when the camouflaged animal moves because the motion is easily seen by the observing predator or prey. However, insects such as hoverflies and dragonflies use motion camouflage to approach possible mates in the former case, and to approach rivals when defending territories in the latter case. Motion camouflage is achieved by moving so as to stay on a straight line between the target and a fixed point in the landscape; the pursuer thus deceives the target animal by appearing not to move but only to loom larger in the target’s field of vision.

Katydids, known for mimicry, have evolved a wide range of camouflage adaptations so their body coloring and shape match entire leaves, half-eaten leaves, dying leaves, leaves with bird droppings, sticks, twigs and tree bark. Other well-known mimetic animals include beetles, mantids, caterpillars, moths, snakes, lizards, frogs and fish.

There are two mechanisms of active camouflage in animals: counter-illumination camouflage, and color change (sometimes called ‘metachrosis’). Counter-illumination camouflage is the production of light to blend in against a lit background. In water, light comes down from the surface, so when animals are seen from below, they appear darker than the background. Some species of cephalopod, such as the midwater squid and the sparkling enope squid, produce light in photophores on their undersides to match the background. Bioluminescence is common among marine animals, so counter-illumination camouflage may be a widespread mode of deception.

Color change permits camouflage against different backgrounds. In the context of deception, this can be used as a defence or predatory strategy, or during courtship and mating. Color change is made possible by chromatophores; pigment-containing and light-reflecting organelles in cells found in amphibians, fish, reptiles, crustaceans and cephalopods. Inside the chromatophore cell of cephalopods, pigment granules are enclosed in an elastic sac. To change color, the animal distorts the sac by muscular contraction, changing its translucency, reflectivity or opacity. This differs from the mechanism used in fish, amphibians and reptiles, in that the shape of the sac is being changed rather than a translocation of pigment vesicles within the cell.

Some chameleon and anole species are able to voluntarily change their skin colors. Different chameleon species are able to change different colors which can include pink, blue, red, orange, green, black, brown, light blue, yellow, turquoise and purple. Some species, such as the Smith’s dwarf chameleon, adjust their colors for camouflage in accordance with the vision of the specific predator species (bird or snake) that they are being threatened by. Some octopuses can use muscles in the skin to change both the color and texture of their mantle to achieve a greater camouflage. In some species, the mantle can take on the spiky appearance of seaweed, or the scraggly, bumpy texture of a rock, among other disguises. A few species, such as the mimic octopus, have another defence mechanism. They can combine their highly flexible bodies with their color-changing ability to accurately mimic other, more dangerous animals, such as lionfish, sea snakes, and eels.

A well-researched form of deception is death feigning, often referred to by non-specialists as ‘playing dead’ or ‘playing possum,’ although specialists use the terms ‘tonic immobility’ or ‘thanatosis.’ A wide range of animals, e.g. lizards, birds, rodents and sharks, will behave as if to appear dead, usually as a defensive method of avoiding predation as predators will usually take only live prey. In beetles, artificial selection experiments have shown that there is heritable variation for length of death-feigning. Those selected for longer death-feigning durations are at a selective advantage to those at shorter durations when a predator is introduced. Death-feigning birds often take advantage of escape opportunities; tonic immobility in quail reduces the probability of the birds being predated by cats.

Death feigning can also be used in reproduction (e.g. in the nursery web spider, the male sometimes feigns death to avoid getting eaten by females during mating) and to improve predation (e.g. the predatory cichlid fish will lie on its side on the bottom sediments until approached by scavengers attracted to what appears to be a dead fish, whereupon it abandons the pretence, rights itself and attacks the scavenger).

Death feigning behavior can be deliberately induced by humans, particularly chickens, colloquially known as ‘hypnosis.’ According to Gilman et al. the investigation of ‘animal hypnosis’ dates back to the year 1646 in a report by Kircher. It has been shown that the intensity and duration of death feigning is related to the intensity of fear prior to the feigning state being induced. This has been used to show that hens in cages are more fearful than those in pens, hens on the top tier of battery cages are more fearful than those on the lower levels, hens carried by hand are more fearful than hens carried on a mechanical conveyor, and hens undergoing longer transportation times are more fearful than those undergoing transport of a shorter duration.

Concealment is the use of cover and terrain by the deceiver to hide from observation. Some animals will select and carry around parts of the environment either to conceal themselves or behave as a form of mimicry based on the environment. In 2005, an article reported that the veined octopus has a bipedal behavior. This behavior was discovered in octopuses in an area off Sulawesi, Indonesia where the sandy bottom was littered with coconut shells. The bipedal motion appears to mimic a floating coconut. At least four individual veined octopuses have been observed retrieving discarded coconut shells, manipulating them, and then reassembling them to use as shelter. This discovery was documented in the journal ‘Current Biology’ and has also been recorded on video.

‘Distraction displays,’ also known as ‘deflection display,’ ‘diversionary display,’ or ‘paratrepsis,’ are anti-predator behaviors used to attract the attention of a predator away from an object, typically the nest or young. They are particularly well known in birds but also occur in fish. The broken-wing display is well known in nesting waders and plovers and doves such as the Mourning Dove. Birds that are at the nest walk away from the nest with one wing hung low and dragging on the ground to appear as an easy target for a predator thereby deceiving predators and distracting their attention away from the nest or young.

The traditional view in ethology (the study of animal behavior) is that animal displays are almost always accurate barometers of the capabilities of the signaler, and that it is not possible for deception to become a stable feature of any such communication system. Deception in this case means that the signaler misrepresents its true capabilities in order to ‘win’ a confrontation with a potential competitor. Ethologists argue that the widespread and continued use of deception by many individuals would cause the whole system to break down, as the recipients of the signal become more ‘skeptical’ about its validity as more and more deceivers’ bluffs are called.

However, researchers working on mantis shrimp and their front limbs (known as ‘smashers’) have disagreed, and have shown that deception seems to be a stable feature in their communities. Their studies revealed that newly-molted mantis shrimps frequently deceived potential competitors by engaging in the meral-spread threat display (a spreading of the legs), even though their still-soft exoskeletons meant that they could not use their smashers without causing massive and serious damage to themselves.

Tactical deception has been defined as ‘acts from the normal repertoire of [an] agent, deployed such that another individual is likely to misinterpret what acts signify, to the advantage of the agent.’ Some color changes in cuttlefish (cephalopods related to squid) may be tactical deception as they are able to simultaneously communicate two entirely different displays to two different observers. When a male cuttlefish courts a female in the presence of other males, he displays two different sides: a male pattern facing the female (courtship), and a female pattern facing away, to deceive other males.

In an anecdotal account, Simmons reported that a female marsh harrier birds courted a male to obtain access to food he had stored. She then took this food and fed it to chicks which had been fathered by another male. More extensive studies focus on possibly deceitful behavior in the pied flycatcher, a species in which males may possess more than one territory simultaneously. Females gain from mating with a male which has no other mates; males may attempt to deceive females about their mating status (mated or unmated). Females assess whether a male has already mated; if he is alone on a territory during repeated visits by the female, then he is probably unmated. Mated males will be absent from the territory (presumably because they are at another territory with their mate). By repeated sampling of male behavior, females are usually able to avoid mating with previously mated males.

Several great apes have been trained to use sign language and in some instances, have apparently used this to attempt to deceive human observers. Koko, a female gorilla trained to use a form of American Sign Language, once tore a steel sink out of its moorings. When her handlers confronted her, Koko signed ‘cat did it’” and pointed at her innocent pet kitten. Nim Chimpsky was a chimpanzee also trained to use a form of Sign Language. In a documentary about the chimp (‘Project Nim’) trainers claimed that when Nim got bored of learning to sign words she would sign ‘dirty’ indicating she wanted to go to the toilet, with the effect that the trainer stopped the lesson and took her to another room.

Observations on great apes have been widely reported as evidence of tactical deception. A well-known example involves a chimpanzee that was approached from behind by a loud aggressive rival. Here, the chimpanzee manipulated his lips several times before losing his fear grin and only after he had done so, he turned around to face the challenger, thereby concealing his fearful expression.

Studies on deceit in great apes have also been performed under experimental conditions, one of which is summarized by Kirkpatrick: ‘…food was hidden and only one individual, named Belle, in a group of chimpanzees was informed of the location. Belle was eager to lead the group to the food but when one chimpanzee, named Rock, began to refuse to share the food, Belle changed her behavior. She began to sit on the food until Rock was far away, then she would uncover it quickly and eat it. Rock figured this out though and began to push her out of the way and take the food from under her. Belle then sat farther and farther away waiting for Rock to look away before she moved towards the food. In an attempt to speed the process up, Rock looked away until Belle began to run for the food. On several occasions he would even walk away, acting disinterested, and then suddenly spin around and run towards Belle just as she uncovered the food.’

Withholding information, a form of tactical deception, can result in costs of increased aggression by other group members. Rhesus monkeys discovering food announce their discoveries by calling on 45% of occasions. Discoverers who fail to call, but are detected with food by other group members, receive significantly more aggression than vocal discoverers. Moreover, silent female discoverers eat significantly less food than vocal females.

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