In The Blink Of An Eye

by Andrew Parker

  The Victorian naturalist Henry Bates spent the years between 1849 and 1860 wandering the Amazonian rainforests. After collecting ninety-four species of butterfly, he published an article. That article has generated heated discussion ever since.

  Bates grouped together his butterflies based on their colouration, as did every collector of the day. Some nice relationships emerged - the butterflies with similar colour patterns could be placed neatly into apparently related groups. But then Bates discovered some conflicting evidence - the shapes of the butterflies’ bodies told a different story. Wings apart, the shapes of the body and limbs varied considerably within a supposedly related group. In fact new groups could be formed based on body and limb shapes alone, groups very different from those based on colour. So why did unrelated butterflies share the same colouration? Was this simply a ‘wonder of nature’, according to pre-Victorian philosophy?

  Darwin and Wallace had demonstrated that wonders of nature do not exist, and Bates shared their views. He delved deeper into his dilemma of contradiction and noted that the most brightly coloured butterflies also flew the slowest, making them the easiest of prey for birds. Bates concluded, however, from the lack of evidence from discarded wings, that birds avoided them. From this he assumed these defenceless butterflies were unpalatable. Then followed an assumption which had serious repercussions - that birds understood the butterflies were distasteful based on their colouration.

  Now Bates could explain his relationship dilemma. It was the shape of the body and limbs of butterflies that marked their true evolutionary relationships. While many within a genuinely related group did possess similar colours, some had departed from the norm with a purpose - that of enjoying a greater chance of survival. First, a butterfly group that has not evolved distasteful chemicals may evolve camouflage colouration, like the peppered moth. But if the camouflage code can be cracked under certain circumstances, then another evolutionary option is to pretend to be unappetising - to copy the colours of those armed with distasteful chemicals. This behavioural and evolutionary strategy is known as mimicry.

  The precise mechanism of mimicry and colouration that warns of indiscernible defences is a subject in its own right. Especially interesting is how predatory species and individuals learn to interpret visual warning codes without wiping out the potential prey species in the process. John Maynard Smith is particularly well known for untangling this academic web in the twentieth century. But for the purposes of this book it is enough to know that mimicry does work. After all, it exists in abundance, and that’s the real proof.

  In his statement on colour, Darwin used the words, ‘whenever colour has been modified for some special purpose . . .’. The use of the word ‘whenever’ is interesting here. Does this mean that colour can sometimes be incidental in that the colour effect has no purpose?

  Black sharks may be red herrings as far as colour is concerned, where their colour provides a warning only to biologists studying adaptations to light. Kanoeohe Bay in Hawaii is a nursery for the scalloped hammerhead shark. The shark pups prefer the safety of the sea floor, even though this reaches a depth of between only 1 and 15 metres within the bay. At the deepest part of the bay, the pups are almost white in colour, but at the shallowest parts they are black. The sea floor, on the other hand, is consistently white. So do the pups require camouflage from a predator or prey only in the deeper water? Or are they making a statement with their colour in the shallows? In this case, the answer to both questions is ‘no’. Sometimes colour has no visual function and is said to be incidental. An example of this is the blue we see of our veins.

  Pigments can serve a function other than providing a visual effect. The black or brown pigment melanin can increase the strength properties of a structure, such as a beetle’s exoskeleton, or it can provide protection from the sun’s ultraviolet rays. For many animals, ultraviolet light can cause tissue damage. Just as we tan in the sun, in very shallow water the hammerhead sharks do the same. At a depth of 1 metre, the ultraviolet content of the water is six hundred times greater than at 15 metres. So in the shallowest waters the hammerhead pups were gathering a layer of melanin in their skin. Melanin not only absorbs the harmful ultraviolet light but also other wavelengths or colours. Consequently, no light is reflected and the shallow-water sharks appear as a colour void. Black, that is.

  This function for pigments has no place in the literature of colour, and rightly does not appear in the Origin. Darwin did, nonetheless, omit a function in his bold statement on colour - the ‘wolf in sheep’s clothing’ function. We have seen examples of camouflage for indirect protection, against one’s enemies. But camouflage colouration can also be employed to conceal oneself from one’s prey.

  I had my first active encounter with pigments while snorkelling in Greece. Although there were no coral reefs, the water was remarkably clear, blue and inviting. In the shallow water were large, brown rocks distributed randomly on the white sea floor. I noticed the rear end of a bright yellow fish emerging from the gap between two rocks and dived down to take a closer look. At first I saw nothing unusual, although I did wonder why the fish did not swim away in my presence. It appeared, through my naive eyes, to be almost jammed between the rocks, so I reached out to help it. Just as I touched its tail, something moved. Not the fish, but the rock. Part of the rock ‘changed’ slightly, and, on closer inspection, that part turned out to be an eye. The rock was a rock-plus-moray eel. A large brown moray eel, camouflaged perfectly against the rock it had wrapped itself around, was grasping the yellow fish head first in its gaping jaws. I was young and, since the yellow fish was about the same size as my head, I felt it was time to leave the water. Later I learnt that generally in shallow seas fish must beware all rocks . . . and stones.

  This colour, like that of the Great Barrier Reef and the Amazonian angelfish, was apparent in very shallow water. It was within a few metres of the surface. And this is why we see the full spectrum of colour on the reef. If the reef were deeper, its spectrum would be limited considerably.

  Monet’s paintings taught us that on land the colour of sunlight changes with the position of the sun in the sky. This also happens in the sea, but there is another factor affecting the sun’s spectrum under water - depth. As sunlight travels through water, it becomes absorbed and eventually disappears. But it does reach a kilometre in depth, at a level that can still be detected, albeit extremely faintly. However, as we plunge further down into the sea, different wavelengths or colours are absorbed at different rates. Red, ultraviolet and violet are the first to fade away, and at 200 metres sunlight is exclusively blue. But regardless of depth, blue transmits best through seawater, even in the shallows. This effect is quite noticeable. Diving beyond about 10 metres, the world appears blue-green. And, as expected, animals are adapted only to the colours left in their specific environment.

  Below 200 metres, many animals are red. The light here is blue, and only blue. The lack of red light means that red pigments have no chance to reflect. Instead they absorb the blue light and so appear invisible. Red is a good camouflage colour in the deep.

  A problem faced in mid-water is how to appear camouflaged from both above and below. From below, a fish is viewed against a light background - the sky. From above it is viewed against the darkness of the deep. The answer is to have a dark upper surface and a pale lower body. This strategy of ‘countershading’ is common under water, so again it must work. The marlin is a fish that appears conspicuously coloured when out of water. But put it in the water and its hues and patterns take on the roles of countershading and disruptive colouration, and the fish disappears from sight. The marlin is a huge fish, yet it can swim in front of your very eyes without your knowing it. It may be camouflaged either against predators (sharks), its own prey (smaller fish), or both, and the camouflage is so important to the survival of the fish that even the parasites on its skin have to maintain the camouflage. Abigail Ingram, a postgraduate student at Oxford University, has found that the se
a lice of marlin possess chromatophores, so they can maintain the fishes’ camouflage whether they occur on dark or light areas of skin. This is a different strategy from that of the flatworm parasites of marlin that steal the marlin’s pigments, but it has the same result. If the marlin dies, so do the parasites. And then there are sucker fish, which clean the marlin of its parasites, to consider. So marlin parasites must appear camouflaged to these fish too. Consequently light is a selection pressure acting on the marlin and its parasites.

  Victoria Welch, another postgraduate student at Oxford, has been tackling another form of camouflage. Countershading is a possibility for fish because generally they remain horizontal. But some animals vary their orientation. Jellyfish often roll around in the water and effectively have no upper and lower surface. They lack the sophistication in hardware and software to handle chromatophores and are often left with only one option to help them blend into their background - transparency.

  Throughout their evolution, many jellyfish have bypassed the road to colour matching. Instead, these jellies blend into their backgrounds using the background light itself - it shines right through them. But this solution is not that simple. Jellyfish often can maintain transparent innards - that is not their biggest problem. Victoria Welch is considering some less obvious stumbling blocks - polarisation and surface reflections.

  Predatory fish can detect light that is polarised. Consequently, selective pressures act on the jellyfish to avoid becoming a polarisation filter. Light of all polarisations must pass through the jellyfish, and not just some polarisations. If this demand is not met, the jellyfish will match its background light in terms of colour, but not polarisation, and so it will not be completely invisible.

  And then there are the surface reflections. We see a reflection of ourselves in glass windows - the effect of any completely smooth surface at the microscopic scale. But jellyfish must not act like glass and reflect only some light from their very outer surfaces. Indeed, jellyfish may have surfaces that reduce reflection considerably, in which case the potential problem is solved.

  Light is certainly a major force in governing the behaviour of animals today. And for life to have reached this point, light must have been a considerable factor of evolution in the past. Such thoughts will be pursued later in this book; they will form another piece of the Cambrian puzzle. But the current subject, light in environments today, will emerge as perhaps the most important clue of all in solving this enigma, although a less obvious piece of the puzzle at this stage. Certainly this is a subject into which we should delve as deeply as space will allow. But we should understand what we are really dealing with here, and not lose sight of this throughout the rest of this book. I refer to an animal’s complete visual appearance.

  The officer’s hat, or the relevance of size and shape

  In my earlier description of an eighteenth-century soldier’s uniform, I touched on another point relevant to nature - size and perceived appearance. The balance between visual camouflage and conspicuousness is not influenced by colour alone. Colour in nature is not the sole component of an animal’s visual appearance. Size, shape and movement relay considerable information, too.

  Just as soldiers wore exaggerated headwear to appear larger, and consequently a greater threat to the enemy, so the puffer fish inflates itself when danger approaches. And when a toad encounters a snake, the toad instinctively stands on fully outstretched legs and inflates its body to some three times its normal size. Now the snake registers a different image - from one that looked like an easy meal to one that has become a possible aggressor. Suddenly the snake is less likely to attack, its judgement based purely on the visual appearance of the other animal. And in all environments with light, visual appearances as a whole influence interactions and relationships between species.

  More obviously, the shape of an animal is an important component of camouflage and mimicry. The stick and leaf insects, and weedy sea dragons, must possess the colours and shapes of sticks, leaves and seaweeds respectively. The movement of these animals is just as vital. The praying mantis that mimics leaves must sway in the wind just as the leaves around it does.

  These are physical and behavioural adaptations to light. Light not only affects the colour of an animal but its whole form and behaviour. Remember that if an animal is not adapted to its light environment it will not survive. Now we can see that this rule calls for great responses throughout the evolution of a species. It is not enough for a lioness to have beige pigments that allow it to blend into the surrounding grass. The lioness cannot evolve the contours of its environment so it must possess another weapon to enable it to catch food - it must be capable of keeping a low profile, not unlike a military sniper. This again is an adaptation to light. But then the lioness’s prey is itself adapted to light too. Wildebeest often graze in circles, facing out from the centre. They are looking out for the lioness, and now collectively they can scan the entire plain. Their circle is also a behavioural adaptation to light.

  To successfully achieve camouflage, even shadows must be considered. A green beetle on a green leaf is not camouflaged if it casts a shadow. But again evolution has responded so as to make life difficult for predators. Many beetles living on leaves are hemispherical in shape. This is a physical adaptation to light. A sphere will always cast a shadow, but from most positions a hemisphere will not. It is important to consider the tremendous evolutionary cost of yielding such a change to the standard beetle design. Not only is the body affected, but also the legs and wings, and any walking and flying that subsequently takes place. Light must really be a powerful stimulus.

  Shape and behaviour are important components of conspicuousness, too. Bees perform dances that carry in them directions leading to nectar. Their wiggles and pirouettes are all adaptations to light - they are visual signals. More familiar, the peacock displays spectacular colours to the comparatively drab peahen. Of relevance here are the eyespots, apparent at the tip of each tail feather. The number of eyespots are ‘counted’ by the female, and as far as she is concerned the more the merrier. The static peacock may possess a hundred eyespots, but during courtship the peacock is not static. He shakes his tail feathers.

  As a comparison, hold up a pen and shake it rapidly from side to side. The single pen will appear as two, one at each extremity of the movement. The same thing happens to a peacock’s tail feather. When shaken, two eyespots emerge from the single feather. Now consider the complete peacock. When his eyespots are under scrutiny, he shakes them, so that his hundred eyespots become two hundred, indicating a much fitter individual. No peahen would be content with a mere hundred eyespots. And again, this shaking behaviour is part of an adaptation to light.

  Eyespots are common in the animal kingdom. Often they perform the ‘officer’s hat’ role - that of making their host look bigger. A butterfly with eyespots at the edges of its wings appears as one large head to some potential predators, in which case the whole animal becomes conceptually much larger. But not all predators are so easily fooled. And eyespots can have further drawbacks.

  Pictures of butterflies in reference books tend to show their wings from above. But sometimes potential predators or partners approach the butterfly from an angle. Then, the eyespots become eggspots - the circles appear elongated.

  In 1533, the German artist Hans Holbein the Younger painted one of the first portraits showing a full-length, life-size person. The Ambassadors features two men and at first everything appears quite normal . . . until the observer notices a strange, elongated object at their feet. The painting was originally hung at the top of a great staircase, where it could be seen either straight on or from an oblique angle. As described, the view is from the front, but from an oblique angle at certain points on the stairs the two men become blurred and eternal death takes over. The men no longer are perceived as bodies, and the mysterious object reveals itself as a distinct human skull (see Plate 10).

  During the courtship of some butterflies, the male views t
he female’s wings from an oblique angle. Any female patterns that serve to attract the male must, therefore, emerge from an oblique view. The results of evolution may not be those that first meet the human eye. Up to this point I have discussed pigments, but the effect of the viewing angle will become even more significant when structural colours are considered.

  Now we can begin to understand why the animals we see are the colours they are, and also that there is a degree of sophistication in the system. But in fact we are merely at the base of the scale of sophistication where nature’s colours are concerned. There is another way that animals can appear coloured other than by employing pigments. Ironically, the brightest colours in nature result from purely transparent materials.

  Structural colours

  The Romans were highly skilled in the art of glass making. We know this because in Roman burials artefacts were often placed in the coffins of the dead, and among those artefacts were pieces of glassware. Much of that glassware has survived and been recovered completely intact.

  One Roman glass plate in particular caught my eye because, not only was it complete and undamaged, it bore an iridescent glaze. Reds, yellows, greens and blues - in fact a complete spectrum - were shining from the surface of this specimen. The colours possessed a metallic appearance. They were much brighter, or more noticeable, than a plate painted with pigments. Interestingly, the colour observed appeared to change as I moved around the plate, an effect also seen to take place on the otherwise transparent wings of a housefly. But what do the Roman plate and an ordinary housefly have in common?