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Deception in animals

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Deception in animals is the voluntary or involuntary transmission of misinformation by one animal to another, of the same or different species, in a way that misleads the other animal. Robert Mitchell identifies four levels of deception in animals. At the first level, as with protective mimicry like false eyespots and camouflage, the action or display is inbuilt. At the second level, an animal performs a programmed act of behaviour, as when a prey animal feigns death to avoid being eaten. At the third level, the deceptive behaviour is at least partially learnt, as when a bird puts on a distraction display, feigning injury to lure a predator away from a nest. Fourth level deception involves recognition of the other animal's beliefs, as when a chimpanzee tactically misleads other chimpanzees to prevent their discovering a food source.

Definitions

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True deception

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Some types of deception in animals are completely involuntary (e.g. disruptive colouration), but others are under voluntary control and may involve an element of learning. Most instances of voluntary deception in animals involve a simple behaviour, 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 behaviour which might be attributed to the manipulative type of deception which we know occurs in humans, i.e. "tactical deception". 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. True deception requires the deceiver to have the mental capacity to assess different representations of reality. Animal behaviour scientists are therefore wary of interpreting a single instance of behaviour as true deception, and explain it with simpler mental processes such as learned associations.[1] In contrast, human activities such as military deception are certainly intentional, even when they involve methods such as camouflage which physically parallel camouflage methods used by animals.

Levels

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Robert Mitchell lists four levels of deception in animals:[2]

  1. First-level deception: an animal acts because it cannot do otherwise, it is programmed to deceive in a certain way. For example, false eyespots such as butterfly markings that indicate their heads are at the back end of their bodies as an aid to escape, or markings to make predators appear safe[2]
  2. Second-level deception: a programmed act of behaviour when another organism is registered. Examples include a predator acting in a way to hide its predatory nature around prey[2]
  3. Third-level deception: involves learning, and is based upon trial and error. An example is feigned injury to get or divert attention; for example, a parent mockingbird feigning an injury to attract a predator away from its defenceless offspring[2]
  4. Fourth-level deception: includes recognition of other animals' beliefs, i.e., second-order thinking. This can be verbal deception such as a chimp misleading other chimps to hide a food source.[2]

All four levels are found in nature, including bacteria and plants, but the third and fourth levels seem to be exclusive to animals.[3]

First-level deception: mimicry and camouflage

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Four-eye butterflyfish conceals its eyes using a disruptive eye mask, a type of camouflage, and displays false eyespots that mimic its eyes near its tail

At the first level, an animal acts because it cannot do otherwise, it is programmed to deceive in a certain way. For example, false eyespots such as butterfly markings that indicate their heads are at the back end of their bodies as an aid to escape, or markings to make predators appear safe[2]

Mimicry

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Main article: Mimicry

Mimicry is a resemblance of one species to another which protects one or both species. The can be in visual appearance, behaviour, sound, and scent. There are many types, which can be combined.[4] Defensive or protective mimicry enables organisms are able to avoid encounters that would be harmful to them by deceiving enemies by appearing to be something that they are not. For example, mantis shrimps spread their powerful front limbs to threaten rivals in a behaviour called the "meral spread".[5] Newly moulted mantis shrimps frequently deceive potential competitors by spreading their front limbs, even though their still-soft exoskeletons meant that they could not use their smashers without damaging themselves.[6][5]

Aggressive mimicry is the mimicking by predators or parasites of harmless species, allowing the predator to approach and sometimes to attract its prey.[7] Anglerfish are named for their characteristic method of predation. Anglerfish 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 can move 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.[7] 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.[8][9] Among fireflies, males are lured toward what seems to be a sexually receptive female, only to be eaten. Photuris females emit the same light signals that females of the genus Photinus emit as a mating signal.[10] Male fireflies from several different genera are attracted to these "femmes fatales" because the predatory females can identify the male's species and emit the signal used by the female of the male's species.[11]

In automimicry, one body part of an animal mimics another. This may help and animal survive an attack, or help predators to appear innocuous. Examples include many moth, butterfly, and fish species that have "eye-spots". These are large dark markings that help prey escape by causing predators to attack a false target. For example, the gray hairstreak (Strymon melinus) shows the false head at its rear; it has a better chance of surviving an attack to that part than an attack to the head.[12]

Camouflage

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Main article: Camouflage
Uroplatus gecko relies on multiple methods of camouflage, including disruptive colouration, eliminating shadow, and cryptic behaviour (lying low and keeping still).

Camouflage is the use of any combination of materials, colouration, or behaviour that helps to conceal an animal by making it hard to see (crypsis) or by disguising it as something else (mimesis). There are many methods of achieving crypsis. These include, resemblance to the surroundings, disruptive colouration, eliminating shadow, self-decoration, cryptic behaviour, motion camouflage, changeable skin appearance, countershading, counter-illumination, transparency, and silvering to reflect the environment. Many species are cryptically coloured to resemble their surroundings. For example, Uroplatus geckos can be almost completely invisible, even to a nearby observer. Similarly, the katydids, a group of grasshopper-like insects found worldwide, are nocturnal and use their cryptic colouration to remain unnoticed during the day. They remain perfectly still, often in a position that increases the effectiveness of their camouflage.[13][14]

Second-level deception: programmed behaviours

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At the second level, an animal conducts a programmed act of behaviour when another organism is registered. Examples include a predator's behaving in such a way as to hide its predatory nature around prey.[2]

Feigning death

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Main article: Apparent death
A grass snake feigning death

A well-researched form of deception is feigning death, familiarly known 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, behave as if dead as an anti-predator adaptation, as predators usually take only live prey.[15]

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.[16] Birds often feign death to escape predation; for example tonic immobility in quail reduces the probability of attacks by cats.[17]

Death feigning may also play a role in reproduction, for example, in the nursery web spider, the male sometimes feigns death to avoid getting eaten by females during mating.[18] In some cases, death feigning is used by a predator. For example, the predatory cichlid Nimbochromis livingstonii lies on its side on the bottom sediments until approached by scavengers attracted to what appears to be a dead fish, whereupon H. livingstoni abandons the pretence, rights itself and attacks the scavenger.[19]

Third-level deception: learnt behaviours

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The third level involves learning, and is based upon trial and error. An example is a distraction display of feigned injury to get or divert attention; for example, a parent mockingbird feigning an injury to attract a predator away from its defenceless offspring.[2]

Distraction displays

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Main article: Distraction display
Killdeer feigning a broken wing

Distraction displays, also known as deflection displays and diversionary displays,[20] are behaviours that draw the attention of a predator away from an object, typically the nest or young.[21] These are well known in birds, as first described by Aristotle in the 4th century BC,[22] but also occur in fish.[23] A familiar example is the broken-wing display seen in nesting waders, plovers and doves such as the mourning dove.[24] In this display, a bird walks away from its nest with one wing dragging on the ground. It seems to be an easy target, thus distracting the predator's attention away from the nest. Once the bird is far enough away it "recovers" and quickly flies off.

Self-deception

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Mitchell[2] has proposed that self-deception occurs if the deceiver and the object of deception are the same organism. Two approaches are tied to self-deception: intentionalism (self-deception is an intentional act) and revisionism (self-deception is not an intensional act). In both cases, there is a higher-level theory of mind present. Namely, intentionality is tied to the third and fourth level of deception, especially the fourth.[25] For Mitchell and for Šekrst, intentionality can only be analyzed at the third level, but not as the animal being intentionally deceptive (having recognition of what the other animal effecting that result believes about the action).[26]

Cases of self-deception have been found in the animal world as well regarding dishonest behaviour of slender crayfish (Cherax dispar).[27] Šekrst[28] uses the findings to show that if we consider this case to be a case of self-deception, then we are acknowledging beliefs, in which case we must talk about first-order intentionality and at least Mitchell's third level of deception. Angiletta et al.[29] show that to establish adaptive self-deception, biologists must quantify the cost and benefit of ignoring one's true competitive ability: in this case, deceptive signallers largely ignored their own strength when escalating or evading aggression.

Angiletta et al. established two conditions for self-deception. First, dishonest individuals must escalate aggression using the same signals that honest individuals do. Second, both dishonest individuals and honest individuals must escalate aggression according to the quality they have signaled, regardless of their actual quality. If both conditions hold, natural selection might have favored genotypes with little or no awareness of their deceptive signaling.[30]

Fourth-level deception: tactical

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At the fourth level, deception includes recognition of other animals' beliefs, i.e., second-order thinking, as when a chimpanzee misleads other chimpanzees to prevent their discovering a food source.[2]

Tactical deception (or functional deception) is the use of signals or displays from an animal's normal repertoire to mislead or deceive another individual.[31] Some researchers limit this term to intraspecific[32] behaviour, meaning that it occurs between members of the same species. Most other kinds of deception are meant to fool members of a different species. Tactical deception can also be achieved when the deceiver withholds information by failing to perform an expected action, such as giving a warning call when danger is observed.

Tactical deception has been used as a measure of advanced social cognition, as it relates to brain function. Primates have larger brains, relative to body size, than in any other mammal except for dolphins, and this size difference is mainly due to an enlarged neocortex. Research has suggested that the evolution of the primate brain is selected-for in highly social species. One study used 18 species with varying brain volumes (three strepsirrhines, four New World monkeys, seven Old World monkeys, and four ape species). The study used the frequency of tactical deception as a measure of social cognition, and it found a strong correlation between the use of social deception and size of the neocortex.[33]

Among cephalopods, some colour changes in cuttlefish might be called tactical deception, as these fish sometimes present entirely different displays to two different observers. When a male cuttlefish courts a female in the presence of other males, he displays a male pattern facing the female (courtship), and a female pattern facing away, to deceive other males.[34]

In domestic pigs, in a setting where the behaviour of a trained animal could reveal the source of food to another animal, the trained animal spent longer at the food source before other pigs arrived.[35]

In an anecdotal account, Simmons reported that a female marsh harrier courted a male to obtain access to food he had stored. She then took this food and fed it to chicks that had been fathered by another male.[36] More extensive studies focused on possibly deceitful behaviour in the pied flycatcher, a species in which males may possess more than one territory. Females gain from mating with a male that has no other mates and males may try to deceive females about their mating status (mated or unmated). Females frequently visit the male, and if he is always alone on his territory he is probably unmated. Thus, by repeated sampling of male behaviour, females are usually able to avoid mating with previously mated males.[37][38]

Group-foraging common ravens hoard their food in a number of places, and also raid the caches made by others. Cachers withdraw from conspecifics when hiding their food and usually place their caches behind structures, out of sight of potential observers. Raiders remain inconspicuous, keeping at a distance from cachers near their cache sites, but within sight. In response, cachers often interrupt caching, change cache sites, or empty their caches. These behaviours suggest that ravens can withhold information about their intentions, which may qualify as tactical deception.[39] Similarly, if a Eurasian jay (Garrulus glandarius) is being watched by another jay, it tends to cache food behind an opaque barrier rather than a transparent barrier, apparently to reduce the likelihood of other jays pilfering their caches.[40]

Observations on great apes have been widely reported as evidence of tactical deception. Several great apes have been trained to use sign language, and in some instances these animals seem to have used language in an attempt to deceive human observers. Koko, a female gorilla, was trained to use a form of American Sign Language. It has been claimed that she once tore a steel sink out of its moorings and when her handlers confronted her, Koko signed "cat did it" and pointed at her innocent pet kitten.[41] Nim Chimpsky was a common chimpanzee trained in American Sign Language. Trainers claimed that when Nim grew bored of learning to sign words, she would sign 'dirty' indicating she wanted to go to the toilet, which caused the trainer to stop the lesson.[42]

Another example involves a chimpanzee approached from behind by a loud aggressive rival. Here, the chimpanzee moved his lips until he lost his fear grin thereby concealing his fear. Only then did he turn around to face the challenger.[31][43][44]

Deceit in great apes has been studied under experimental conditions, one of which is summarised by Kirkpatrick:[44]

"...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 behaviour. 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."

Deceptive behaviour has been observed in Old World monkeys including baboons (Papio ursinus). In one of their articles, Byrne and Whiten recorded observations of "intimate tactical deception" within a group of baboons, and documented examples that they classified as follows: A juvenile using warning screams to gain access to underground food storages which otherwise would have been inaccessible; an exaggerated "looking" gesture (which in an honest context would mean detection of a predator) produced by a juvenile to avoid attack by an adult male; recruitment of a "fall-guy" (a third party used by the deceiver to draw attention or aggression); and using one's own movement pattern to draw group-mates away from food caches. Byrne and Whiten also broke these categories into subcategories denoting the modality of the action (e.g. vocalization) and what the action would have signified if observed in an honest context. They noted whether the individual that had been manipulated was in turn used to manipulate others, what the costs had been to the manipulated individual, and whether or not there were additional costs to third parties. Byrne and Whiten expressed concern that these observations might be exceptions, and that such deceptive behaviour s might not be common to the species.[32]

Among New World monkeys, tufted capuchin (Cebus apella) monkey subordinates have been found to employ a vocal form of tactical deception when competing with dominant monkeys over valuable food resources. They use alarm calls normally reserved for predator sightings— either barks (used specifically for aerial stimuli), peeps, or hiccups— to elicit a response in fellow group members and then take advantage of the distraction to pilfer food. In a series of experiments directed by Brandon Wheeler a group of tufted capuchin monkeys was provided with bananas on feeding platforms. Here, subordinate monkeys made nearly all of the alarm calls that could be classified as "false", and in many of the false alarms, the caller was on or within two meters of the feeding platform. The calls made dominant monkeys leave the platform while the subordinate caller stayed behind to eat.[45]

Intentional tactical deception has been proposed also for mice.[46] In particular, d'Isa et al. have observed that free-living black-striped mice (Apodemus agrarius) perform a peculiar deceptive dodging maneuver to escape from a chaser mouse. In this deceptive dodge, a chased black-striped mice enters a single-entrance chamber, hides inside the chamber next to the entrance, awaits that the chaser has entered and then, exploiting the distraction of the back-turned chaser, it takes the entrance/exit of the chamber to escape away in the opposite direction.

Costs of tactical deception

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Withholding information, a form of tactical deception, can be costly to the deceiver. For example, 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.[47] Presumably because of such costs to deceivers, tactical deception occurs rather rarely. It is thought to be more common in forms and species where the cost of ignoring the possibly deceptive act is even higher than the cost of believing. For example, tufted capuchin monkeys sometimes emit false alarm calls. The cost of ignoring one of these calls could be death, which may lead to a "better safe than sorry" philosophy even when the caller is a known deceiver.[45]

See also

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References

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  46. ^ d'Isa, Raffaele; Parsons, Michael; Chrzanowski, Marcin; Bebas, Piotr; Stryjek, Rafal (2024). "Catch me if you can: free-living mice show a highly flexible dodging behaviour suggestive of intentional tactical deception". Royal Society Open Science. 11 (7): 231692. doi:10.1098/rsos.231692. PMC 11382684. PMID 39253095.
  47. ^ Hauser, M. D. (1992). "Costs of deception: Cheaters are punished in rhesus monkeys". Proceedings of the National Academy of Sciences USA. 89 (24): 12137–12139. Bibcode:1992PNAS...8912137H. doi:10.1073/pnas.89.24.12137. PMC 50713. PMID 1465451.

Further reading

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