Bird Senses. Graham R. Martin

paths and time courses over which eyes have evolved. However, Dan Nilsson of Lund University has argued that the evolution of eyes has not been linearly progressive. It seems that eyes, like many other structures, have evolved in fits and starts. This means that relatively long periods of stasis in eye structure were punctuated by periods of rapid change, triggered by the emergence of new tasks as the environment changed. These changes will have included the availability of new food sources and feeding opportunities, and the appearance of new species that provided new threats and opportunities.

      Just what these tasks were is very difficult to determine. However, the overall tasks that seem to have driven the evolution of eyes in birds are concerned with the control of the bill or feet towards specific targets, especially in foraging, and in the detection of predators. These two main sorts of tasks typically make substantial, but often conflicting, demands upon eye design and most aspects of bird vision. It seems likely that other tasks, especially the control of locomotion (flight, swimming, or walking) are achieved within constraints imposed by these two key tasks of foraging and predator detection. Surprisingly, it seems that the control of locomotion may not be a prime driver of vision in birds. These arguments will be expanded upon later, but the important point to note here is that vision, alongside other aspects of an animal’s biology, is driven by its utility. In the case of vision (and other senses) that utility lies in gaining information for the control of behaviour. Vision of a certain kind is not just something that a bird happens to have, it must fulfil important functions.

      The importance of vision in birds

      The primary reliance of birds on vision is easily asserted. It can be based just upon casual observations of birds completing their everyday behaviours. However, this assertion is also well supported by evidence that in most species of birds relatively large portions of their brains are devoted to the analysis of information from vision. Also, the so-called ‘intelligent’ behaviours of birds seem to be based primarily upon visual information. Thus, extracting information from vision and using it to guide sophisticated behaviours is the essential function of the brains of most birds.

      Only in a handful of extant bird species is vision not the primary sense. Even in such birds vision was at one time highly likely to have been the prime source of information. However, vision can become secondary through a process of regressive evolution. At the same time other senses, particularly olfaction, hearing, and touch sensitivity, can come to take on some of the primary functions usually carried out by vision. These include food detection, predator detection, and guidance of locomotion – all of which are underpinned by vision in most birds.

      The prime examples of ‘non-visual’ birds are the five species of flightless kiwi, which probably lost their reliance on vision as they evolved in the absence of mammalian predators on the islands of New Zealand. The downgrading, but not complete loss, of vision in these birds is discussed in Chapter 9.

      In other bird species, including some of the petrels (Procellariidae), shorebirds (Scolopacidae), and owls (Strigidae), olfaction, touch, and hearing respectively play a key role or one that is complementary to vision, especially when it comes to finding and ingesting food items. However, in these birds vision is still the primary guide for locomotion.

      What eyes do

      The crucial property of the first camera eyes, and indeed of all eyes since, is that they were able to determine the position of a light source relative to the animal. They were more than simple light detectors; they also had the capacity of spatial vision. Spatial vision provides information on where objects are relative to the observer. What’s more, it can do this more or less instantaneously and continuously.

      This might seem an obvious attribute of vision, but it is not true of any other sense, nor was it an attribute of the very first eyes. Not until camera eyes evolved was it possible to obtain accurate information about the positions of objects within a large part of the environment in which an animal sits. Furthermore, most camera eyes can do this over a range of light levels, although as light levels fall the accuracy of spatial vision usually decreases. Being able to function over a range of light levels is an important attribute of vision because in natural environments light levels change both constantly and dramatically. In open habitats at all latitudes except close to the poles, ambient light levels change over many million-folds on a daily cycle; from noontide sunlight to starlight. Therefore, a key aspect of an animal’s eye is not only how much spatial detail it can detect but also over how much of the daily light cycle it can provide useful spatial information.

      Functioning over the full range of naturally occurring light levels is difficult. Some eyes have evolved to provide spatial information over a wide range of light levels, but many have evolved to function primarily within a relatively narrow range, typically those experienced during daytime (dawn to dusk) or night-time (dusk to dawn). Even within these periods light levels are not static and change over many thousand-folds.

      Colour vision is primarily an elaboration of spatial vision. Colour vision is often thought of as something rather different or special, something that is additional to ‘simple’ spatial vision – perhaps regarded as simple because it can be achieved in what appears to be a less sophisticated world of black and white. However, colour vision has value because it enhances the extraction of spatial detail by using differences in how light of different wavelengths is reflected from different surfaces.

      Lit by sunlight, a ‘blue’ surface reflects light only within a relatively narrow range of the wavelengths of light that fall upon it. The surface absorbs light from the rest of the spectrum. A ‘red’ surface reflects and absorbs light in other parts of the spectrum. However, the colour vision mechanism that determines which part of the spectrum light is from is rather wasteful of photons. This is because the visual system must make elaborate comparisons between light reflected from the different surfaces. The consequence is that the ability to detect levels of contrast between patterns is always lower for coloured than for black and white patterns. Faced with the task of detecting contrast in a grating (of the kind discussed above in the ‘Measuring senses’ section of Chapter 2), or with the task of resolving the finest stripe width that can be reliably detected, performance with stripes of different colours is always inferior compared with black and white patterns.

      Lack of colour vision at low, night-time, light levels occurs in most vertebrates. It is not because there is no colour information potentially available in the environment. The lack of colour is a property of the visual system, not of the environment. At night, photons are relatively scarce. To see something at night necessitates maximum use of any photons that are available. Having a mechanism that detects the part of the spectrum that photons come from is too wasteful of light to have general utility compared with the advantage of simply being able to detect that something is actually present. The stimuli for colour vision are present in the environment at night as much as they are during the day, but vision does not make use of them. Colour vision is a bonus of high light levels.

      This simple observation tells us that colour is not a property of the world but a property of the visual systems that extract information from the world. Light itself is not coloured. Colour is an attribute added by visual systems. This observation was first made by Isaac Newton in his Opticks (published in 1704) and captured in the famous phrase ‘The Rays, to speak properly, are not coloured’. It was based initially upon his observations of how white light can be broken up into prismatic colours. Newton elaborated this key idea by further experiments on many aspects of human vision. The implications of this observation have been investigated and discussed from both scientific and philosophical viewpoints ever since. Humans have projected many aesthetic properties onto ‘colour’, and this has given philosophers a rich theme for speculation and theorising. It is essential, however, to be aware that colour vision is an elaboration of the mechanisms that extract spatial detail from the environment.

      Sources of variation in vision

      We are familiar with the idea that there are many different designs of bird wings