Countershading

Application

In animals

Countershading is observed in a wide range of animal groups, both terrestrial, such as deer, and marine, such as sharks. It is the basis of camouflage in both predators and prey. It is used alongside other forms of camouflage including colour matching and disruptive coloration. Among predatory fish, the gray snapper, Lutianus griseus, is effectively flattened by its countershading, while it hunts an "almost invisible" prey, the hardhead silverside, Atherina laticeps which swims over greyish sands. Other countershaded marine animals include blue shark, herring, and dolphin; while fish such as the mackerel and sergeant fish are both countershaded and patterned with stripes or spots.

It tones the canvas on which are painted the Leopard's spots, the Tiger's stripes ... It is the dress almost universally worn by rodents... It is the essential uniform adopted by Conies, Asses, Antelopes, Deer ... It is repeated extensively among the marsupials ... It provides a basic livery for the great majority of snakes, lizards, and amphibians. Among insects it reaches a fine state of perfection in different caterpillars and grasshoppers. ... It is, however, in rivers, and in the surface waters of the sea, that countershading reaches its maximum development and significance.

— Hugh Cott

Mesozoic marine reptiles had countershading. Fossilised skin pigmented with dark-coloured eumelanin reveals that ichthyosaurs, leatherback turtles and mosasaurs had dark backs and light bellies. The ornithischian dinosaur Psittacosaurus similarly appears to have been countershaded, implying that its predators detected their prey by deducing shape from shading. Modelling suggests further that the dinosaur was optimally countershaded for a closed habitat such as a forest.

Counter-illumination

Another form of animal camouflage uses bioluminescence to increase the average brightness of an animal to match the brightness of the background. This is called counter-illumination. It is common in mid-water pelagic fish and invertebrates especially squid. It makes the counter-illuminated animal practically invisible to predators viewing it from below. As such, counter-illumination camouflage can be seen as an extension beyond what countershading can achieve. Where countershading only paints out shadows, counter-illumination can add in actual lights, permitting effective camouflage in changing conditions, including where the background is bright enough to make an animal that is not counter-illuminated appear as a shadow.

Military

Countershading, like counter-illumination, has rarely been applied in practice for military camouflage, though not because military authorities were unaware of it. Both Abbott Thayer in the First World War and Hugh Cott in the Second World War proposed countershading to their countries' armed forces. They each demonstrated the effectiveness of countershading, without succeeding in persuading their armed forces to adopt the technique, though they influenced military adoption of camouflage in general.

Cott was a protege of John Graham Kerr who had quarrelled with Norman Wilkinson in the First World War about dazzle camouflage for ships. Wilkinson remained influential in 1939 as an inspector of camouflage, so a political argument developed. Cott was invited to camouflage a 12-inch rail-mounted gun, alongside a similar gun camouflaged conventionally. Cott carefully combined disruptive contrast to break up the gun barrel's outlines with countershading to flatten out its appearance as a solid cylinder. The guns were then photographed from the air from various angles, and in Peter Forbes's view "the results were remarkable." Cott's gun is "invisible except to the most minute scrutiny by someone who knows exactly where to look and what to look for. The other gun is always highly visible." The authorities hesitated, appearing to be embarrassed by the evidence that Cott was right, and argued that countershading would be too difficult to use as an expert zoologist would be needed to supervise every installation. Cott was posted to the Middle East, and Kerr unsuccessfully intervened, pleading for guns to be painted Cott's way and Cott to be brought home.

The Australian zoologist William Dakin in his 1941 book The Art of Camouflage followed Thayer in describing countershading in some detail, and the book was reprinted as a military handbook in 1942. Dakin photographed model birds, much as Thayer and Cott had done, and argued that the shoulders and arms of battledress should be countershaded.

Countershading was described in the US War Department's 1943 Principles of Camouflage, where after four paragraphs of theory and one on its use in nature, the advice given is that:

Upper surfaces should be painted and textured so as to conform to the color and tone of the surrounding country (background) and the sides graded and toned from this to the white which the under surfaces and parts in shade should be painted.

Inventors have continued to advocate military usage of countershading, with for example a 2005 US patent for personal camouflage including countershading in the form of "statistical countercoloring" with varying sizes of rounded dark patches on a lighter ground.

Research by Ariel Tankus and Yehezkel Yeshurun investigating "camouflage breaking", the automated detection of objects such as tanks, showed that analysing images for convexity by looking for graded shadows can "break very strong camouflage, which might delude even human viewers." More precisely, images are searched for places where the gradient of brightness crosses zero, such as the line where a shadow stops becoming darker and starts to become lighter again. The technique defeated camouflage using disruption of edges, but the authors observed that animals with Thayer countershading are using "counter-measures to convexity based detectors", which implied "predators who use convexity based detectors."

Function

Hannah Rowland, reviewing countershading 100 years after Abbott Thayer, observed that countershading, which she defines as "darker pigmentation on those surfaces exposed to the most lighting" is a common but poorly understood aspect of animal coloration. She noted there had been "much debate" about how countershading works. She considered the evidence for Thayer's theory that this acts as camouflage "by reducing ventral shadowing", and reviewed alternative explanations for countershading.

Camouflage theories of countershading, Rowland wrote, include "self-shadow concealment which results in improved background matching when viewed from the side"; "self-shadow concealment that flattens the form when viewed from the side"; "background matching when viewed from above or below"; and "body outline obliteration when viewed from above". These are examined in turn below.

Flattening and background matching when viewed from the side

Cott, like Thayer, argued that countershading would make animals hard to see from the side, as they would "fade into a ghostly elusiveness". Rowland notes that Cott is here reviewing Thayer's theory and "reinforcing the view that a gradation in shading would act to eliminate the effects of ventral shadowing." Kiltie measured the effect of the countershading of the eastern gray squirrel, Sciurus carolinensis, showing that when the squirrel is horizontal the self-shadowing of the belly is partly concealed, but that when the squirrel is vertical (as when climbing a tree trunk) this effect did not occur.

Thayer's original argument, restated by Cott, was that nature did the exact opposite with countershading that an artist did with paint when creating the illusion of solid three-dimensionality, namely counteracting the effect of shade to flatten out form. Shading is a powerful cue used by animals in different phyla to identify the shapes of objects. Research with chicks showed that they preferred to peck at grains with shadows falling below them (as if illuminated from above), so both humans and birds may make use of shading as a depth cue.

Background matching from above or below

A completely different function of animal (and military vehicle) coloration is to camouflage the top and bottom surfaces differently, to match their backgrounds below and above respectively. This was noted, for example, by Frank Evers Beddard in 1892:

Among pelagic fish it is common to find the upper surface dark-coloured and the lower surface white, so that the animal is inconspicuous when seen either from above or below.

— Frank Evers Beddard

Early researchers including Alfred Russel Wallace, Beddard, Cott and Craik argued that in marine animals including pelagic fish such as marlin and mackerel, as well as dolphins, sharks, and penguins the upper and lower surfaces are sharply distinct in tone, with a dark upper surface and often a nearly white lower surface. They suggested that when seen from the top, the darker dorsal surface of the animal would offer camouflage against the darkness of the deep water below. When seen from below, the lighter ventral area would similarly provide the least possible contrast with the sunlit ocean surface above. There is some evidence for this in birds, where birds that catch fish at a medium depth, rather than at the surface or on the seabed, are more often coloured in this way, and the prey of these birds would see only the underside of the bird. Rowland concluded that each possible role for coloration patterns lumped together as "countershading" needs to be evaluated separately, rather than just assuming it functions effectively.

Outline obliteration from above

Rowland (2009) identified an additional mechanism of countershading not previously analysed, namely that a round body such as a cylinder illuminated and seen from above appears to have dark sides. Using a graphics tool, she demonstrated that this effect can be flattened out by countershading. Since predators are known to use edges to identify prey, countershading may therefore, she argues, make prey harder to detect when seen from above.

Non-camouflage theories

Non-camouflage theories include protection from ultraviolet light; thermoregulation; and protection from abrasion. All three of these "plausible" theories remained largely untested in 2009, according to Rowland.

Evidence

Despite demonstrations and examples adduced by Cott and others, little experimental evidence for the effectiveness of countershading was gathered in the century since Thayer's discovery. Experiments in 2009 using artificial prey showed that countershaded objects do have survival benefits and in 2012, a study by William Allen and colleagues showed that countershading in 114 species of ruminants closely matched predictions for "self-shadow concealment", the function predicted by Poulton, Thayer and Cott.

Mechanism

Evolutionary developmental biology has assembled evidence from embryology and genetics to show how evolution has acted at all scales from the whole organism down to individual genes, proteins and genetic switches. In the case of countershaded mammals with dark (often brownish) upper parts and lighter (often buff or whitish) under parts, such as in the house mouse, it is the Agouti gene which creates the difference in shading. Agouti encodes for a protein, the Agouti signalling peptide (ASP), which specifically inhibits the action of the Melanocortin 1 receptor (MC1R). In the absence of the Agouti protein, alpha-melanocyte-stimulating hormone stimulates the cells bearing MC1R, melanocytes, to produce dark eumelanin, colouring the skin and fur dark brown or black. In the presence of the Agouti protein, the same system produces the lighter-coloured, yellow or red phaeomelanin. A genetic switch active in the cells of the embryo that will become the belly skin causes the Agouti gene to become active there, creating the countershading seen in adult mammals.

Reverse countershading

If countershading paints out shadows, the reverse, darkening the belly and lightening the back, would maximise contrast by adding to the natural fall of light. This pattern of animal coloration is found in animals such as the skunk and honey badger with strong defences—the offensive stink of the skunk, and the sharp claws, aggressive nature and stink of the honey badger. These animals do not run when under attack, but move slowly, often turning to face the danger, and giving deimatic or threat displays either to startle inexperienced predators, or as an aposematic signal, to warn off experienced ones.

The caterpillar of the Luna moth, as discovered by Thayer, is in Cott's phrase "countershaded in relation to [its] attitude", i.e. shaded with a light back grading to a dark belly, as is the Nile catfish, Synodontis batensoda for the same reason: these animals (and other caterpillars including Automeris io and the eyed hawkmoth, Smerinthus ocellatus) habitually live 'upside down' with the belly uppermost. Similarly in the sea slug Glaucus atlanticus, the reverse countershading is associated with inverted habits. These animals are thus employing countershading in the usual way for camouflage.

Examples in animals