Bird Senses. Graham R. Martin

      FIGURE 3.5 Examples of isodensity maps of the ganglion cells in bird retinas. In each diagram the retina has been spread flat, but its orientation is as in the eyes in the intact birds shown above. Flattening the retina causes splits, hence the rather ragged shape. The densities of the ganglion cells (×1000 per square millimetre) have been analysed across the whole of the retina and points with similar density have been joined to give contour maps, much as a topographical map links places of the same height. Clear patterns emerge in these maps showing how the images projected onto the retina by the eye’s optics are analysed to extract different degrees of detail. On the left is the retina of a Manx Shearwater Puffinus puffinus, and the map shows that their retinas have a band running horizontally across the field of view in which details are particularly resolved (receptors are at high density, providing greater detail). On the right, the Rock Dove Columba livia shows a retina with two distinct areas from which detailed information is extracted: one looks out close to the axis of the eye (in this view almost directly out of the page), while the other also projects laterally but downwards and slightly forward within the bird’s field of view. (The diagram of the dove is redrawn from work published by Bingelli and Paul.)

      The importance of these density patterns can be appreciated by considering the photoreceptors of a retina to be analogous with the photodiodes of the receptor surface of a digital camera. In a camera we understand that the photodiodes are responsible for pixelating the image, and we expect that the photodiodes are not jumbled but spread at an even density across the whole image-analysing surface. This guarantees that the same amount of detail is available across the whole of the image. However, in retinas the densities of receptors and ganglion cells vary markedly across the image surface. Furthermore, there are consistent and different photoreceptor and ganglion cell patterns in the retinas of every bird species. It is as though we were able to choose between cameras not just on their overall density of photodiodes, but also on how the photodiodes are placed across the image surface. It is as if we could choose between one camera that analysed the image in greater detail at its centre, another that could analyse with greater detail in a band horizontally across the middle of the image, another more to one side, and so on. An endless number of possible arrangements would be possible.

      Such patterns are indeed found in bird retinas, and indeed in all retinas, including our own. In human eyes the image is analysed in greatest detail more or less at its centre, and in less detail towards the periphery, but even in our eyes the patterns are not symmetrical. In birds highly complex patterns are found (Figure 3.5). What this means is that across bird species there is a wide range of patterns in the way that information is extracted from the environment surrounding the bird. The eyes of two different species may be imaging the same scene, but because of differences in their retinas the scene is analysed in different ways. These different receptor patterns are the result of natural selection driven by the need for the extraction of key information used in the control of different visually guided tasks in different species.

      While knowing about these patterns gives valuable insight into the vision of different species, knowledge of the absolute density of ganglion cells or photoreceptors in a particular eye is also of great value. It allows an estimation to be made of the upper limits of the resolution (acuity) of an eye and can also provide an idea of acuity in different parts of the field of view. To achieve this, data on ganglion cell density must be combined with information on the size of the image. Using this method, estimates of the maximum spatial resolution of eyes have been calculated for a range of species (see Appendix). Furthermore, this method has been validated by determinations of maximum acuity using training techniques (of the kind described in Chapter 2) in the same species, most notably in some birds of prey, including both eagles and falcons.

       Photoreceptors: rods and cones

      Photoreceptors are of two basic types, rods and cones. The rods have higher absolute sensitivity and function principally at low light levels (between dusk and dawn in natural environments) while the cones underpin vision during higher, daytime light levels. Cones are the photoreceptors that provide colour vision.

      Every photoreceptor contains millions of photosensitive molecules (visual pigment), and each molecule is capable of trapping an individual photon of light. Trapping just a small number of photons is sufficient to kick off the process of phototransduction. This is a cascade of chemical changes which results in a neural signal being generated and transmitted to the brain via the optic nerve.

      An important aspect of visual pigment molecules is that they do not absorb light of all wavelengths. Each molecule is selective within the spectrum, responding maximally to a relatively narrow range of wavelengths. Because only one type of photopigment occurs in each photoreceptor they sample the spectrum of the light falling upon them. The result is that for a particular eye the relative numbers of receptors with different photopigments will determine its sensitivity across the spectrum. This is explored in more detail in the ‘Types of cone photoreceptors’ section below and in Box 3.1.

      Sensitivity in the spectrum

      It is clear that many birds detect light over a wider range of wavelengths than humans are able to; in other words, they have a broader visible spectrum. Also, it seems that birds may be able to discern more colours within their spectrum; that is, they can probably make finer colour discriminations, at least in some parts of the spectrum. Some birds can detect light in the ultraviolet (UV) part of the spectrum, light to which human vision is insensitive. However, vision in the UV part of the spectrum is not unique to birds, for some terrestrial mammals and many invertebrates are also able to detect information using UV light.

      It is important to note that not all birds see in the UV part of the spectrum. In fact those bird species which have true UV vision are found only in the gulls (Laridae, Charadriiformes), ostriches (Struthioniformes), parrots (Psittaciformes), and the oscine passerines (Passeriformes), but excluding the crows (Corvidae). Other bird species may have visual sensitivity that extends into the violet spectrum, but they cannot be considered truly UV-sensitive, while others, notably some birds of prey, have optical systems that filter out UV light from the image so that it never reaches the retina.

      Colour vision

      As noted in the ‘What eyes do‘ section above, the prime function of colour vision is that it allows the extraction of spatial detail by using differences in the wavelengths of light that make up the image. It seems unlikely that colour vision evolved specifically for enhancing information about the presence and properties of certain types of objects that are key in the life of an animal. It is more likely that it first evolved to meet a broad range of spatial tasks.

      Examples of situations where detection is enhanced by colour vision in birds include the use of objects in display behaviours (as seen, for example, among bowerbirds (Ptilonorhynchidae, order Passeriformes)), and the detection of plumage patterns and particular flowers or fruits against foliage backgrounds. This does not mean, however, that these specific tasks were the prime drivers for the evolution of colour vision. Indeed, it seems more likely that the colour of plumages, flowers or fruits evolved to become more conspicuous in response to the vision of the observing birds, rather than that the vision of the birds evolved to detect these particular objects.

      Fruits that are eaten regularly by birds have probably evolved to encourage their detectability. This is because consumption of the fruit will result in wider dispersal of seeds. Thus, many fruits have evolved to be detected by birds and this is achieved in two ways. First, the ripe fruits (ready for seed dispersal) reflect light that contrasts with the surrounding foliage, both in brightness and in colour. Second, smaller fruits often occur in conspicuous concentrations, so that they present a larger target that can be detected with relatively low-resolution vision at a