Innes Cuthill of University of Bristol takes us on a journey into the world of concealment and camouflage, how have these complex forms of disguise evolved, and what role does the viewer play? This blog is part of our colourful countdown to the holiday season where we’re celebrating the diversity and beauty of the natural world. Click here to read the rest of the colour countdown series.

Fig.1. The colouration of the peppered moth, Biston betularia, helps conceal it against tree bark. During the industrial revolution, the typical form (on the right) was replaced by a dark melanic form (on the left), better matched to bark free of lichen and darkened by pollution. Photo © Gerard Cheshire. 

Go to any introductory textbook on evolution, and it’s a fair bet that you’ll find the peppered moth, Biston betularia, used as an example of natural selection in the wild. The classic story is of the rise and fall of a dark melanic morph, as opposed to the mottled lichen-matching wild type, in industrial Britain. The cause (or at least a major cause) was the trees on which the moths sat becoming dark and lichen-free during the Industrial Revolution, but recovering with the Clean Air Acts from the 1950s onwards. The selective agent here is bird predation and the function of the colour is camouflage. 

‘Concealing colouration’ has a long history in the study of adaptation; indeed, going back to before that word acquired its technical meaning for evolutionary biologists. Charles Darwin’s grandfather, Erasmus, wrote “The colours of many animals seem adapted to their purposes of concealing themselves, either to avoid danger, or to spring upon their prey” some 15 years before Charles was even born. Camouflage was widely used by early evolutionists such as Poulton and Wallace to illustrate the power of natural selection to produce apparent design. Why then, compared to other classic evolutionary paradigms, such as mimicry and aposematism, has it only recently received a comparable intensity of research effort? Probably because the mechanism appears self-evident. Look like the background and you can’t be spotted, right? 

The orange fur of a tiger (Panthera tigris) blends with the green foliage when seen by (a) a red-green colour-blind prey such as a deer, but not when seen by (b) a normally sighted human. Reproduced under CC BY 4.0 licence from Fennell et al. (2019).

Understanding camouflage is in fact not so simple, and the reason is that it is an adaptation, not so much to the environment, as to the perception and cognition of the species that you are hiding from. For example, if we are to understand insect camouflage, we need to model how their predators, which will often be birds, see the colours and patterns. Birds have very different colour vision from us, based around four rather than three cone photoreceptors and extending into the ultraviolet. If we are impressed by the camouflage of an animal, from an evolutionary perspective it is a happy coincidence because, in most cases, the colours and patterns have not evolved to deceive humans. But equally, if we are perplexed by apparently poor camouflage, it may be because the coloration is effective against the evolutionarily relevant receiver, but not us. For example, we might wonder why a tiger has orange and black stripes, rather than green and black (or at least brown and black). But a tiger’s prey, such as deer and other large mammals, are red-green colour-blind, and so there is no perceptible difference between the tiger’s orange and leaf’s green

Visual systems use disparities in colour, lightness or pattern to detect where one object stops and another starts. That boundary in turn provides a cue to the shape of the object, often the most powerful means of identifying it. Matching the colour and pattern of the background minimises the disparity between the object and background, and so, even if the object’s presence is detected, an indistinct boundary can make recognition by shape difficult. But camouflaged animals have other tricks. Disruptive coloration breaks up the outline by placing contrasting colours at the body’s edge . Large differences between adjacent colour patches generate strong responses in the neurones that detect edges through contrast, so the ‘signal’ of the true outline of the animal is lost amid the ‘noise’ of the false edges. Minimisation of the signal-to-noise ratio, either by reducing the signal (e.g. matching the background) or increasing the noise (e.g. false edges) provides a useful conceptual framework for understanding camouflage. 

The angle shades moth (Phlogophora meticulosa) shows disruptive coloration. Notice that at the border of the dark and light brown wing patches, the light side gets even lighter near the boundary and the dark side gets darker. The enhanced boundaries create strong ‘false edge’ signals in the viewer, helping to disguise the true shape of the animal. Photo © Gerard Cheshire.

Some disruptively coloured animals actually have enhanced boundaries between colour patches and this makes shape recognition even harder. By making the light side of the boundary lighter and the dark side darker, the neurones that respond to edges are ‘super-stimulated’; clear evidence that camouflage evolves to exploit visual systems rather than merely reproduce background colours. Another example of this is one of the oldest theories used to explain animal coloration, self-shadow concealment through countershading, proposed independently some 130 years ago by British entomologist (and ardent Darwinist) Edward Bagnall Poulton and the American artist Abbott Thayer. Light comes from above and so a uniformly coloured animal would appear lighter on the side facing the light and its other side would be in shade. The shading provides a cue to 3D shape; indeed, it is one of the main tools an artist has to create the impression of depth and structure on a 2D canvas. Many animals are darker on their back than belly, so Poulton and Thayer argued that this countered the gradient due to illumination, obliterating the cues to shape from shading.

The caterpillar of the tau emperor moth (Aglia tau) is easy to see when flipped upside down from its normal pose under a stem (top). Its countershading enhances rather than conceals the gradient of illumination However, its usual position (bottom) the countershading obliterates the shape-from-shading cues and it is well concealed. (Reproduced under CC BY 3.0 licence from Penacchio et al. (2015). Photos by Olivier Penacchio).

Previously accepted as a universal explanation to a very widespread form of coloration, doubt started to creep in with the recognition that being darker on the side facing the light could have other adaptive explanations, such as UV protection (compared the back of your hand and palm in summer; you are countershaded, but not for camouflage). Even Thayer argued that countershading could be the best coloration for an animal seen against different backgrounds, such as a fish viewed against the light sky from below and the dark depths from above. This is camouflage, but not through self-shadow concealment. However, comparisons of species’ shading patterns to what one would predict from the light environment they live in, and experiments with artificial prey designed to match different lighting, all support the self-shadow concealment mechanism. Now that we can model light fields and the cues to shape from shading, we can even use this to predict the environments that extinct animals lived in, based on their fossilised pigmentation. That said, showing the mechanism can work is not the same as establishing the breadth of its explanatory power; the dark backs and light bellies of some animals certainly do not match the predictions for self-shadow concealment. 

When I started to work on camouflage, it was as a biologist seeking to explain the adaptive value of coloration. Collaboration with vision scientists was a pragmatic step because you can’t understand camouflage without understanding how the colour is perceived. However now I am as interested in what camouflage can tell us about how other animals see the world as I am in the colours themselves.