Master of Disguises

Camouflage is the use of any combination of materials, coloration, or illumination for concealment, either by making animals or objects hard to see (crypsis), or by disguising them as something else (mimesis).

Peacock Flounder: it can change according to the environment

History:

The study of camouflage has a long history in biology, and the numerous ways of concealment and disguise found in the animal kingdom provided Darwin and Wallace with important examples for illustrating and defending their ideas of natural selection and adaptation. Thus, various forms of camouflage have become classic examples of evolution. In a broader sense, camouflage has been adopted by humans, most notably by the military and hunters, but it has also influenced other parts of society, for example, arts, popular culture, and design. 

Grasshopper: Professional in disguise 

Animals use camouflage to make detection or recognition more difficult, with most examples associated with visual camouflage involving body coloration. However, in addition to coloration, camouflage may make use of morphological structures or material found in the environment, and may even act against senses other than vision (Ruxton 2009). 

Dead Leaf Butterfly: the perfect camouflage

In nature, some of the most striking examples of adaptation can be found with respect to avoid being detected or recognized, with the strategies employed diverse and sometimes extraordinary. Such strategies can include using markings to match the color and pattern of the background, as in various moths (e.g. Kettlewell 1955), and to break up the appearance of the body, as in some marine isopods (Merilaita 1998). 

Camouflage is a technique especially useful if the animal can change color to match the background on which it is found, such as can some cephalopods (Hanlon & Messenger 1988) and chameleons. Further remarkable examples include insects bearing an uncanny resemblance to bird droppings or fish resembling fallen leaves on a stream bed (Sazima et al. 2006), to even making the body effectively transparent, as occurs in a range of, in particular, aquatic species.

Animal camouflage represents one of the most important ways of preventing (or facilitating) predation. It attracted the attention of the earliest evolutionary biologists and today remains a focus of investigation in areas ranging from evolutionary ecology, animal decision-making, optimal strategies, visual psychology, computer science, to materials science. Most work focuses on the role of animal morphology per se and its interactions with the background in affecting detection and recognition. However, the behavior of organisms is likely to be crucial in affecting camouflage too, through

• background choice
• body orientation
• positioning
• strategies of camouflage that require movement.

In most natural environments, animals face a problem in ensuring that their camouflage is effective – most visual environments vary. This means that a single fixed phenotype is unlikely to be optimally concealed against all or even many potential backgrounds. Three main solutions exist. 

1. Many animals change color for camouflage, enabling them to tune their appearance to the background. However, while a few animals such as cephalopods, chameleons, and some fish can rapidly adjust their appearance in seconds, color change in most animals take longer, meaning that there will often be a mismatch between appearance and background during changes.
2. Animals might adopt a ‘compromise’ appearance, which matches no background perfectly but several to some degree although evidence for how widespread this approach is in nature is lacking.
3. For animals to choose where to rest or sit in a way that best matches their appearance.

BACKGROUND CHOICE:

The most obvious way that animals could use behavior to improve camouflage is through choosing to rest on backgrounds that match their own appearance. This could arise at a number of levels. 

1. First, all individuals of a species may have the same fixed preference for a background type (e.g. all individuals always show a preference for black backgrounds; species-level choice). 
2. Second, all individuals may show the same preferences, but these are context-dependent (flexible species-level choices). For example, when Inhabitat a, all individuals choose white, but all choose black in habitat b. Context factors include not just habitat but also, for example, age, activity, reproductive status, or level of parasitic infection.

Evidence of background choice

(a)    Species-level choices

Boardmanet al. (1974) undertook tests with more natural backgrounds, finding that those species which normally preferred black or white in uniform controlled apparatus also tended to choose dark or light natural substrates, respectively. There was general consistency in the coloration and pattern types of individuals and the substrates that they chose. For example, grey and mottled individuals tended to choose sandy grey soils, whereas individuals with green markings tended to use greener leaves. In other work, recently metamorphosed American toads (Bufo americanus) show preferences for dark soil and mixed sandy substrates

American toad: Bufo americanus

over plain sand and this coincides with a higher predation risk on plain sand backgrounds from snakes (Heinen, 1993). Some lizards have also been shown to prefer microhabitats that are likely to confer better camouflage. Studies manipulating aspects like vegetation cover also report that ground-nesting birds choose backgrounds related to camouflage and

Common potoo (Nyctibius griseus)

predation risk. In species like the common potoo (Nyctibius griseus), which subjectively often ensemble branches of trees (masquerade), choice of perch sites seems driven for both enhanced background matching and masquerade. Instead of choosing backgrounds that individuals' best match, the authors 

suggest that prey may instead choose more complex visual backgrounds since background complexity is known to impede visual detection of targets. The authors compared choice between differently patterned achromatic backgrounds, controlled to have the same amount of black and white across treatments, but with different arrangements and orientations of stripes and other small shapes. The fish 

generally preferred backgrounds that allowed better matching with the orientation and shape of their body markings, although in one instance females preferred a more complex background.

(b) Morph-specific choices

Many species exist in a number of discrete morphs, and here we would expect background choice to be consistent with morph appearance. Kettlewell (1955) first tested this in an experiment with pale (typical) and melanic (carbonara) forms of the peppered moth (Biston betularia) and found support

Peppered moth (Biston betularia) 

for each morph choosing appropriate dark or light backgrounds. Furthermore, in predation experiments with garter snakes (Thamnophis elegans), mismatched frogs were

more likely to be attacked than camouflaged individuals. This contrasts with previous experiments on the same color morphs (Brattstrom & Warren, 1955) that found no evidence of substrate choice. In behavioral choice experiments (Wente & Phillips, 2005), fixed green frogs preferred matching substrates, but brown morphs only preferred matching substrates when in the presence of predator (snake odor) cues. 

   
   (c)   Individual-level choices

Variation in appearance within species is frequently not characterized by discrete morphs, but rather by continuous individual variation (although it can be challenging to distinguish the two). Many species show considerable variation among individuals, and this can vary with age and ability to change color. The ability of individuals to select backgrounds that match their own unique appearance has not been widely considered until recently, except to an extent in color-changing species, but several studies have recently tested this idea. One of the most comprehensive studies of individual background choice was on Japanese quail

(Coturnix japonica) (Lovell et al.,2013). Quail lay eggs that are highly divergent in appearance among females; some mothers lay light eggs with little maculation, whereas others lay dark eggs with a prominence of dark markings. 

In lizards, background choice seems linked to both individual appearance and predation risk. Marshall, Philpot & Stevens (2016) showed that in Aegean wall lizards (Podarcis erhardii),

individuals were found on chosen backgrounds that resembled their own individual dorsal coloration (to predator vision models) better than would be the case if found in locations chosen by other individuals.

(d) Color-changing species

Differences in individual appearance frequently arises due to the ability of some animals to change color (Duarte et al., 2017a). Here, we would expect that individuals of species that can change color fairly slowly show background choice (with choice changing to maximize camouflage as the animal changes color). By contrast, in animals with rapid color change there may be no need for substrate choice since they can match many backgrounds quickly (subject to constraints regarding the degree of match possible). The available evidence broadly supports this prediction, but not for all species or individuals. For example, work on cuttlefish (Sepia

Officinalis) has tended not to reveal strong preferences for substrate appearance (Allen et al., 2010), although one study on Sepia pharaonic(Lee, Yan & Chiao, 2012) found that cuttlefish raised in an environment with enriched visual information including light and dark rocks and artificial algae showed greater/earlier preferences for high-contrast patterned backgrounds than individuals reared in environments of plain grey or checkerboard patterns. 

(2) The ecological context of choice

Background-choice the behaviour of animals should have a range of important outcomes and implications for the exploitation of resources and (micro-)habitats. In the first instance, a range of camouflaged animals shows phenotype–environment associations, which can lead to matching to specific habitats (Stevens et al., 2015; Xiao et al., 2016). Such associations and matching can arise through genetic adaptation (e.g. Rosenblum et al., 2010) or phenotypic plasticity and ontogenetic color change (Todd et al., 2006; Stevens, Lown & Wood, 2014). However, even in phenotypically plastic species, such as shore crabs (Carcinus

maenas), which are extremely variable in color and pattern, background choice is also likely to explain associations at the microscale.Behavior and camouflage type can also be linked to habitat use in other ways. For example, the prawn Hippolyte obliquimanus exists in two main morphs – the homogenous type that 

uses background matching to resemble different algal backgrounds, and a striped form that seems to rely on transparency for concealment (Duarte & Flores, 2017). The homogenous types are able to change color between algal background species, and stick closely to their matching substrate, whereas the transparent the form shows less background affinity and more mobile behavior and associated morphology.

ORIENTATION, POSTURE, SHAPE, AND HIDING SHADOWS

Behavior can be used to fine-tune camouflage by controlling the orientation, posture, and shape of the organism.

(1) Orientation and positioning behavior

Webster et al. (2009)  found evidence that some species of Catocala moth have consistent orientation behavior, whereas other species of moth do not. They presented human subjects with images of moths superimposed on images of trees with changed orientation, and found that orientation was a key

attribute contributing to detection. In addition, when they rotated the tree bark images horizontally, the optimal orientation changed accordingly, showing that the effect of orientation on detection was not due to the moth position per se, but rather its interaction with background features. 

(2) Posture, shape, and minimizing shadows

The positions that animals adopt can also affect types of camouflage beyond crypsis, such as masquerade. Suzuki & Sakurai (2015) noted that many caterpillars which are thought to resemble bird droppings rest in a posture with their bodies curled up or bent, seemingly increasing their similarity to real droppings. They created an artificial caterpillar prey that was either black and white or green and pinned them either in a straight posture or bent, and measured predation from birds in the field. Models that were green (cryptic) did not differ in survival with posture, whereas black-and-white models resembling bird droppings survived better when placed in a bent posture.

MECHANISMS OF CHOICE AND ORIENTATION

Here we focus both on the senses that animals use to control their behavior and the underlying mechanisms that govern how information from the senses is used to control behavior: whether fixed genetic preference, imprinting, assessment of own camouflage, or otherwise.

(1) Use of different sensory modalities to judge the background

A range of sensory information can be used to find suitable backgrounds and resting sites. For example, some shrimp use visual information on shape, size, and contrast to locate

preferred habitats (Barry, 1974). Gillis (1982) studied substrate choice in the polymorphic grasshopper Circotettix rabula and found that when the eyes of individual grasshoppers were damaged, substrate choice disappeared.

(2) How animals could choose correct backgrounds

One of the most important issues regarding background choice and positioning concerns the mechanisms that enable animals to make appropriate choices. There are several potential ways this could be achieved. 

1. First, there may exist a genetic basis for choice (‘preference gene’), linked to genes governing appearance. 
2. Second, animals could imprint on or learn about certain visual backgrounds that are important or that they are likely to associate with. 
3. Third, individuals may actively use their senses to assess how closely their body coloration matches the backgrounds that they choose. 

DECORATION AND BACKGROUND MODIFICATION:

Animals interact behaviourally with the world around them, and so now we focus on aspects of this interaction related to the exploitation of materials from the environment (or secreted by the animal itself) to influence their camouflage.

(1) Decoration

Ruxton & Stevens (2015, p. 2) reviewed the literature on decorating by animals, and define a decorator as ‘an organism that (by means of specialist behavior and/or morphology that has been favored by selection for that purpose) accumulates and retains environmental material that becomes attached to the exterior of the decorator’.

(2) Modifying the visual background

We have already considered how animals can influence camouflage behaviourally by a selection of the background against which they are seen. It seems at least conceptually n plausible that animals could go a step further and behaviourally modify that environment to enhance crypsis.

(3) Hiding built structures

The evidence that animals employ the behavior to hide the structures that they build is scarce. Almost by definition, traps such as spider’s webs must be constructed in such a way as to be difficult for prey to detect in order to be effective, and there is evidence that certain specific features of webs can be linked to reduced avoidance by prey. Turning to homes built

by animals, Bailey et al. (2014) provide evidence that birds may actively select materials that camouflage their nests. They demonstrate that captive zebra finches (Taeniopygia guttata) preferentially select nesting material that is similar in color to the provided nest cup and surrounding cage walls. 

MOVEMENT

It is generally considered that stillness is an integral aspect to camouflage, and there are many reports of cryptic prey ‘freezing’ in response to heightened danger from visual predators (e.g. Caro, 2005). This is backed up by experimental demonstrations that movement by an organism with cryptic color and patterning can greatly increase its chance of detection (e.g. Ioannou & Krause, 2009; Stevens et al., 2011). Here we explore if there might be some exceptions to this generality.

(1) Flicker-fusion

The flicker-fusion effect occurs if a patterned object moves sufficiently quickly across the visual field of a viewer that the patterning becomes blurred and the appearance of the patterned object changes (Endler, 1978; Stevens, 2007; Umeton, Read & Rowe, 2017). It is plausible that such an effect could reduce the predation risk of moving objects by providing a better match to their background, but while this has been postulated to occur in some fast-moving striped snakes, the evidence is scant.

(2) Motion dazzle

Motion dazzle is the phenomenon where the pattern of a moving object can make an estimation of its speed and/or trajectory harder (Thayer, 1909; Stevens, 2007; Stevens, Yule & Ruxton, 2008). Proof of concept in artificial systems has been repeatedly demonstrated for human observers (e.g. Scott-Samuel et al., 2011; Stevens et al., 2011, 2008, and references therein), but highly suggestive evidence also exists

for non-human observers. Patterning that may cause a motion-dazzle effect has been hypothesized for a number of animals (especially lizards: Halperin, Carmel & Hawlena, 2017; Murali & Kodandaramaiah, 2018), but has been investigated most fully in the case of zebra (Equus spp.) stripes.

(3) Motion to facilitate masquerade

Bian, Elgar & Peters (2016) present evidence that is suggestive that a stick insect (Extatsoma tiaratum) shows swaying behavior in windy conditions in order to reduce the ease with which it can be distinguished visually from surrounding moving foliage. They found that the frequencies

adopted by the insect overlapped strongly with those of the surrounding foliage. Further, they show that this is an environmentally sensitive behavior – with swaying being more sustained in response to time-varying (blustery) wind and ceasing at high wind-speeds.

ROLE OF BEHAVIOURAL CAMOUFLAGE IN A CHANGING WORLD

Humans are having a huge impact on other organisms globally, but these impacts are diverse and not always easy to predict. Here we provide case studies that argue for behaviourally mediated camouflage to be considered an important trait that can mediate the impact of humans on different animals in nature.

Finally, it is possible that behavioral flexibility in camouflage may sometimes be an important trait facilitating the invasion of natural habitats consequent to deliberate or inadvertent

introduction by humans. The shore crab (Carcinus maenas) is known as a globally invasive species (Darling et al., 2008), and several studies have shown phenotype–environment associations. 

Camouflage has long been known to be mediated by behavior, including potentially in the choice of appropriate resting backgrounds, body positions and orientations, hiding key features such as shadows, maintaining concealment during motion, and modifying bodies, structures, and surroundings.