In The Blink Of An Eye

by Andrew Parker

  Between 544 and 543 million years ago a revolution took place. During this one million year period, vision was born.

  We are now in a position to interpret the statement ‘How ancient already in the Lower Cambrian must the compound eye have been’ made by Frank Raw. Yes, the compound eye and vision were well developed in the Lower Cambrian. But no, it was not ancient - it was contemporary. And it became the new fashion.

  There was always going to be one moment in history when the eye suddenly appeared on Earth, as if out of nowhere. Now we can identify that moment. And a really important point to bear in mind at all times is that light-sensitive patches and other stages of rudimentary light receptors are not eyes. While only these patches existed, when eyes were awaiting their introduction to Earth, there was no such thing as vision.

  We now know that eyes existed at the very beginning of the Cambrian . . . but not before. These two facts could be as important as each other. Considered together, they describe the introduction of a sense. Not just any old sense, but the most powerful sense or stimulus to animal behaviour and evolution in sunlit environments. And a sunlit environment is where the Burgess Shale and other well-known Cambrian animals lived. It also played host to the Cambrian explosion.

  Extrapolating further, there are lifestyles that can be reconstructed based on the optics of eyes. The architecture of eyes alone can provide information on how animals lived. For instance, the position of the eyes in the head can reveal the position of the animal in the food chain. Eyes positioned at the sides of the head, facing sideways like those of a rabbit, can scan a wide angle and spot movement from nearly all directions. The movement pursued in this case is that of predators - eyes of this type belong mainly to plant eaters. In contrast, eyes positioned together at the front of the head, facing forward like those of an owl, see less of the environment but are better for pinpointing targets and judging the distance between them. These eyes generally belong to meat eaters. But this is a theme for another chapter.

  8

  The Killer Instinct

  A little alarm now and then keeps life from stagnation

  F. BURNEY (Mme d’Arbley), Camilla (1796)

  THE LAWS OF LIFE

  For the survival of animals everywhere

  CONTENTS

  Basic Rules 1. Every man for himself: stay alive!

  1a. Avoid being eaten

  1b. ‘Eat’

  2. For the good of one’s kind.

  2a. Breed

  2b. Find a niche and protect it

  2c. Adapt to changes in the environment

  Lifestyle 1. Predator

  2. Prey

  Tactics 1. Conspicuousness

  2. Crypsis/illusiveness

  3. Genuine strength/ability

  The previous chapter could be viewed as ‘end of story’. Certainly, there is considerable evidence within that chapter suitable for the Cambrian files. But it is too early to jump to conclusions just yet, for there is something else to consider, a subject that has raised its head, either plainly or rather more cryptically, in every chapter so far. In each case it merged into the background as quickly as it appeared. Before ending our Cambrian investigation, we should introduce predators into the evidence.

  The first rule of animal survival is to stay alive. The other rules, such as feeding and breeding, are academic if this first rule is not followed. But from the beginning we must distinguish between an individual and a species. A species is a collection of like individuals, which interbreed in their natural environment. Staying alive and feeding are factors that directly affect individuals, then indirectly species. Breeding and niche occupations are concerns for the long-term survival of the species. Of course animals don’t really receive rules - in reality the rules for their survival are the selective pressures for evolution, invisible forces acting on the genes, carrying messages for enhanced survival. And selective pressures act directly upon individuals, not species, so even the species-level survival factors are relayed through individuals.

  The first basic rule of species survival - for individuals to stay alive - will form the subject of this chapter. And more specifically, I will centre on the most important aspect of that rule, to avoid being eaten. This chapter is a stage for the predators. And, in keeping with the previous chapters, the stage will have a space and a time dimension.

  Before launching into the world of T. rex and the like, I will make a brief disclaimer relating to The Laws of Life outlined on the previous page. These are the general rules but do not cover all possibilities, particularly those less common natural catastrophes. Some things are beyond evolution, such as meteor impacts, sudden ice ages, and disease. Disease is density dependent, and so it is a factor operating at the species level. On the one hand, species can become too successful for their own good. From another viewpoint, this is just evolution maintaining biodiversity, preventing one species from taking over the world. But in general, biodiversity is maintained by all branches of the evolutionary tree adhering to The Laws of Life. A predator does not become an overnight success by growing bigger teeth. The other side of the coin is the ‘Avoid being eaten’ alarm for its prey species, which favours genetic mutations for stronger armour. Cichlid fishes feed on snails, and where the fishes evolve stronger teeth, the snails simply evolve harder shells. Evolution can take animals down different roads. There are roads to predation and there are roads to prey, with the predator and prey roads running between. But all roads are endless, and animals are continuously moving along all of them. However, all animals today are travelling along an established evolutionary road - snails already possess armour that may yet become reinforced.

  Central to this book so far have been the subjects of light and vision. When superimposed on to The Laws of Life, their capacity will become evident. Specifically, they fall into the ‘Tactics’ section. Consider the Hawaiian unicorn fish with its conspicuous yellow spine near its tail. The spine serves to protect the fish from predators and competitors, and consequently the unicorn fish avoids being eaten and protects its niche. But the unicorn fish rarely calls upon its spine because in reality this armament is only an ornament. Here the messenger is light. Potential predators and competitors see the armoury and have second thoughts.

  When adaptations to vision include shape and behaviour, in addition to colour, it is clear that vision is a major tactic used in the struggle for both conspicuousness and illusiveness. Genuine strength or ability is actually a rare attribute in animals; rarely does an animal dominate an ecosystem without considerable employment of warnings or illusions. The lioness is the main predator in the Serengeti, but she cannot outrun her prey over short and long distances, so she must rely on camouflage colours and stalking behaviour to take up a competitive position in her race for food. An exception here can be found in many birds, and the reason for this exception will offer another clue towards solving the Cambrian enigma. Birds will be considered in the following chapter.

  There are tactics animals can use other than vision to achieve either conspicuousness or illusiveness; other senses do exist, as also described earlier. Once again, adaptation to light is generally the main tactic to employ within The Laws of Life because of the factor separating light from all other stimuli - occurrence. Light exists, like it or not. Add Chapter 7 to the mixture and we have ‘Vision exists, like it or not’. Over 95 per cent of all multicelled animals today have eyes, so if one of them is to avoid being eaten, it must be adapted to the light in its environment. We are beginning to take our knowledge of light and vision into the subject of predation.

  Another thing about eyes

  Chapter 7 centred on the optics of eyes, the equipment that forms an image on a retina. The reason for this was the link between the living and extinct - the optical origins of today’s eyes can be traced in the fossil record, right back to the very first eyes in the Cambrian. But there is something else we can learn from the type of image formed in the past, or the view of the world through fossil eyes, that
is relevant to this chapter. Just as we did in Chapter 7, we must first look for evidence in the present day.

  We have learnt that there are alternative ways of producing an image today - different types of eyes do exist. But that is not the end of the variation. There are also different ways in which eyes can be arranged in a head, and these provide different views of the world.

  Among the vertebrates within the chordate phylum only camera-type eyes exist. In humans they lie next to each other in the front plane of the head - they face forward. But more than that, they always focus on the same object. So why bother with two eyes, when one would appear to do the job of seeing on its own? Has evolution been excessive in our case?

  When eyes are positioned on the sides of the head, like those of rabbits, the wide field of view encapsulates almost the entire horizon. At first this would seem like the ideal form of vision, but to gain such a panoramic outlook, each eye sees a different picture - each approaching 180° of the horizon - and never the same object. With one eye, however, the view will be two-dimensional, and so distances are difficult to estimate.

  When two eyes are positioned on the front of the head, distances and the direction in which one is travelling can be estimated. So it follows that eyes in this arrangement can perceive the three-dimensionality of an object. Differences in the positions of images create impressions of depth, as can be demonstrated using stereograms. Each eye sees the same object but from a different angle. Stereograms probably work because the optic nerves serving slightly different regions of the two retinas converge on the same ‘binocular’ cell in the brain. The view of an object from two different angles is superimposed and averaged - and its depth is perceived. So animals with two eyes facing forward are said to have stereoscopic vision - they can perceive images in 3D.

  Figure 8.1 One of the original stereograms of 1838. Blur the picture to produce a fused image in the centre. The inner ring will appear nearer than the outer ring.

  The stereogram, albeit merely a demonstrative game, would not work for a rabbit, or for ourselves if we closed one eye. So we should again consider whether it is better to have two eyes at the front of our head, facing forwards, or on the sides of the head, giving a panoramic view. The answer would appear to depend on the purpose of vision. Would you like to observe events happening all around you in two dimensions? Or would you prefer to view objects in front of you in three dimensions and with information on distances? Now we can return to The Laws of Life, and consider whether you are a predator or prey.

  For a prey species, staying alive first means keeping off the dinner plate and then eating becomes important. So it is ideal for the prey species to be surrounded by open space, where the possibility of a sudden ambush is minimised. Minimised, that is, if a 360° view of the terrain is possible - blind spots on the horizon are dangerous. We often find rabbits grazing in the middle of open fields rather than at its edges near hedgerows. And we always find them with their eyes positioned for a panoramic view: eyes positioned at the sides of the head are good for spotting predators.

  For a predator, in contrast, staying alive usually means eating first and worrying about their predators and competitors after that. Eating lively animals involves hunting. Estimating distances is a critical part of hunting - the lioness cannot begin her charge when the prey is within its safety zone, where its head start is insurmountable for the lioness. Equally, a fox cannot catch a rabbit if the rabbit is given the distance in which to reach full speed. So where vision is the major sense employed by predators, two eyes at the front of the head are needed - an accurate assessment of distances is the difference between a meal and hunger. And that is just what is found in the lioness and the fox.

  This trend can often be found within other animal phyla with eyes. But in mid-water, things become more complicated. There is not only the horizon to worry about, there is also above and below. In mid-water, danger can approach from all directions. The great bearers of marine compound eyes, the crustaceans, have evolved a solution to this problem - many crustaceans have eyes positioned at the ends of moveable stalks. They can move their precision eyes to cover a wide area of their surroundings. Because of this, stalked eyes generally do not provide clues as to predator or prey, although many crustaceans, like insects on land, are often both. Today they lie somewhere in the middle of the food web where avoiding predation is finely balanced with the need to eat. Other types of compound eyes, however, are more obliging to the Cambrian detective.

  Later in this chapter, I will attempt to relate the feeding information provided by eyes to the inhabitants of the Cambrian. Eye stalks in this respect are like gloves to the fingerprint detective - they mask potentially useful information. But compound eyes that are fixed in position do offer some clues, and such eyes are found commonly in the fossil record.

  In the air, dragonflies are expert hunters. They have three pairs of grasping limbs positioned near to their blade-like mouthparts, and large wings to provide speed and manoeuvrability. But first the helpless prey must be found, identified as prey, and then tracked. This is achieved using vision - huge eyes are fused to the head. These eyes lock the prey in their sights, their ‘sights’ being just parts of the eyes and not all the facets. This is food for palaeontological thought.

  The compound eyes of dragonflies contain several hundred or even thousand facets, not all of which are equal. There are one or two regions of the eye that contain larger facets and these are known as the acute zones, the ‘sights’. Larger facets provide higher magnification and better resolution - they see with greater sensitivity. One acute zone is positioned at the top of the eye, and this is used to scan through the air and identify prey insects against the sky. When a prey insect has been spotted, the dragonfly moves into its horizontal plane and tracks it with a forward facing acute zone - the prey is now locked into a line of fire. But the relevant point here is that the size and positions of the facets within the eye provide information on feeding - predation in this case. The eyes of prey can be quite different.

  For animals that require vision only to avoid being eaten, having two eyes is just one solution. Rather than evolving a pair of good image-forming eyes capable of scanning the entire environment, they may evolve numerous, less efficient eyes distributed over a large area of the body. At the sacrifice of images, numerous eyes are ideal for detecting movement - as an object passes over them, its moving shadow is detected. When the environmental light changes, as when a fish passes through the ocean, a response is triggered. Numerous compound eyes are indeed found in nature. They occur in ark clams (molluscs) and fan worms (bristle worms) where they are employed to detect predators.

  The real advantage of this multiple eye system probably lies in the word ‘evolve’ used at the beginning of the previous paragraph. Evolution involves changes, changes from one structure to another, for instance. Here we are back to Darwin’s original doubts caused by the eye - from what could our highly complex and specialised eyes have evolved? We now know that skin and ears can share nerves, and that part of the animal brain may have converted from touch to vision at some stage. Dan-Eric Nilsson suggests that the light detector cells in the compound eyes of ark clams and fan worms evolved from chemical detector cells that were inhibited by light. Originally, these chemical detectors were distributed over a large area of the body and, consequently, so too are the eyes today. In other words, it was most accommodating in these cases to evolve eyes all over the body.

  Ark clams and fan worms are preyed upon by fishes. They have soft parts used for feeding, which can be enclosed within hard parts in the form of a shell and tube respectively. So these animals would benefit from a burglar alarm, an early warning system to detect a predator’s approach. And that is the function of their eyes. When the movement detected in the water equates to that of a fish, the ark clam closes its shell tight and the fan worm withdraws into its tube. The armoured doors are closed. And their many compound eyes were the cheapest evolutionary option capable of perf
orming this function from the building materials or starting points available.

  Clearly, signs are appearing that the architecture and position of eyes can reveal not only how an animal sees but also its position in the food web - whether it is a predator or prey. Chapter 7 used fossil eye architecture to trace vision in the past. Now I will re-examine the fossil evidence, where appropriate, and use it in an attempt to trace the history of predation.

  The Cambrian arthropod Cambropachycope had a single compound eye. Other than the weird Opabinia, the failed five-eyed experiment, all other Cambrian eyes producing good images and with the potential for image analysis were paired. When cross-sectioned, each of Opabinia’s five eyes revealed the general architecture of a compound eye. But Opabinia had a flexible tube-like mouthpart extending from its head and terminating in a grasping jaw. The arrangement of the eyes at the front, side and top of the head are not so easy to interpret because of that mouthpart - it could extend in front of, to the sides or above the head. So which direction ‘faces forwards’ for Opabinia? Because there are several ‘forward’ directions for the mouth, we cannot say whether Opabinia’s eyes served to view the entire environment or to centre on just one direction. Before tackling the remainder of the Burgess fossils, first we must reassess Cambropachycope.

  Cambropachycope was an ancestor of the crustaceans. Although only a few millimetres in size, it is known in great detail from a fossil site in Sweden thanks to very favourable preservation conditions. As mentioned in Chapter 7, the bulbous front end of Cambropachycope was an eye - a single, large compound eye. An examination of the cornea of this eye revealed that it completely covered the slightly flattened front surface of the animal. Facets were evident on the surface as it curved away towards the sides, but generally the sides were bare. Importantly, the facets on the curved edges were small compared to those of the central part of the eye. It seems that the centre of the eye saw with the greatest precision. Cambropachycope’s eye could scan a 120° sector of the environment - that sector in front of it. And just like in dragonflies of today, the central region of the eye could achieve finer resolution. In conclusion, this was the eye of a predator. Cambropachycope would have terrorised the tiny inhabitants of the Cambrian around 510 million years ago.