Bird Senses. Graham R. Martin

      Figure 3.6 shows some examples of fruits whose seed dispersal is aided by birds. It is clear that they reflect light from different parts of the spectrum, from the red and orange wavelengths to the blues and ultraviolets. Interestingly, the same bird species may consume fruits with all of these different colours, suggesting that there are no specialisations of vision associated with detecting fruits of particular colours. For example, European Robins are known to consume all of the fruits shown in Figure 3.6, plus many more.

      FIGURE 3.6 Fruits that are commonly eaten by birds in the British Isles, all of which have been recorded in the diets of European Robins Erithacus rubecula. Top row, left to right: Common Buckthorn Rhamnus cathartica, Elder Sambucus nigra. Middle row: Blackthorn (Sloe) Prunus spinosa, Common Juniper Juniperus communis, Spindle Euonymus europaeus. Bottom row: Hawthorn Crataegus monogyna, Rowan Sorbus aucuparia.

      All of these fruits occur in large concentrations, creating a large target for the bird to detect. This suggests that their detection does not require vision of high spatial resolution. As Figure 3.6 shows, although the individual fruits tend to be relatively small, they usually occur in large clusters. Therefore, the initial task for a bird is to detect these clusters at a long distance. Once it has found a cluster it is more or less guaranteed access to a large food source. Individual fruits can be detected when the birds work over the tree or shrub, but they can find this food source at a distance because of the large aggregations of individual fruits.

      The ability to detect colour differences within the spectrum has not been determined directly in many bird species. Although colour might seem conspicuous, it is surprisingly difficult to show definitively that an animal is using colour vision. This is because surfaces may be discriminated both by colour and by brightness at the same time. To sort between these possibilities requires careful, and typically laborious, behavioural experiments. The most detailed knowledge available is from behavioural and electrophysiological studies in Rock Doves (Feral Pigeons) Columba livia. It is, however, possible to say something about colour vision, and the breadth of the spectrum visible, in birds in general.

      This is based on knowledge of the visual sensitivity of individual cone receptors, and it seems safe to assume that practically all birds have colour vision. Furthermore, the ability to differentiate colours in much of the spectrum differs little between species. Even the nocturnally active owls are thought to have some colour vision, although it is not as sophisticated or as subtle as that of other bird species. However, genome analysis, although not the determination of visual pigments directly, suggests that colour vision may be absent from the kiwi species, and these may be the only group of birds that are not capable of making colour discriminations.

      Types of cone photoreceptors

      Classifying the different types of cone photoreceptors in the retinas of all animals is done by reference to the position in the spectrum of the peak sensitivity of the photopigments that they contain (Box 3.1). In our own retinas there are rods that contain a single type of photopigment, but our cones are of three types defined by which one of three different photopigments they contain. These pigments, and hence the cone types in which they occur, are commonly labelled red, green, and blue, to indicate the spectral regions in which they are most sensitive. It is these three types of cone receptors that provide the basis for human colour vision. It is referred to as trichromatic vision, because it is based on three receptor types.

Box 3.1 The photoreceptors of bird retinas

      At one level of analysis bird retinas are highly complex. Even the smallest eyes contain many millions of individual photoreceptors, the rods and cones. However, at another level there is relative simplicity. This is because these photoreceptors are of few types and they are very similar in all bird species. Their essential features are depicted in the accompanying diagram. What varies between species are the relative numbers and distributions of the different receptor types across their retinas. As discussed in the ‘The image analysis system‘ section above, it is these patterns of receptor distribution that are the primary foundations of differences in the visual abilities of species.

      The cone receptors are the ones that function primarily at higher, daytime light levels. Rods function at low light levels. During twilight both rods and cones may function, depending on the exact light level. In birds, rods are of one type, but the cones are of five different types: four types of single cones, and double cones. The different types of single cones are classified by reference to the position in the spectrum of the peak sensitivity of the photopigments that they contain.

      The top portion of the diagram depicts the types of retinal photoreceptors as they appear when viewed through a relatively high-powered light microscope. The outer segments are extremely narrow, generally between 1 and 2 μm (microns) in diameter, but they are relatively long. Each outer segment contains many millions of photosensitive pigment molecules, and each individual molecule of photopigment can absorb the energy from a single photon of light. When this happens, the receptor triggers a signal to the brain. Of course, at high light levels many millions of photons are simultaneously absorbed by the pigment molecules scattered throughout the outer segment.

      The four types of single cone provide the fundamental mechanism upon which colour vision is based. The double cones provide a neural channel that is thought to signal luminance (brightness) and they are not part of the colour vision system. Within all cone types there is an oil droplet. As depicted in the diagram, most oil droplets are highly coloured. The colour is due to carotenoid pigments which are derived from the bird’s diet. Birds fed on carotenoid-free diets have colourless oil droplets.

      The blue arrow on the left indicates the direction in which light travels from the optics of the eye to the focused image on the retina. In one sense the retina would seem to be back to front, because light does not reach the photopigment until it has travelled through the neural layers of the retina. However, this arrangement means that the light that makes up the retinal image must pass through the oil droplets before it enters the outer segments.

      The fact that the oil droplets are coloured means that they have light-filtering properties: they let light of certain wavelengths pass through and absorb light of other wavelengths. In fact, the oil droplets act as cut-off filters, that is they allow light only above particular wavelengths to pass through to the pigment molecules, while light of shorter wavelength is absorbed. The combination of photopigment types and oil droplet types results in there being four main types of single-cone photoreceptors in birds’ retinas, with each cone type able to absorb light only within a particular part of the spectrum, although there is overlap between them.

      The lower section of the diagram shows the resultant ‘photoreceptor sensitivities’ and the labels used to describe them. These are LW (long wave), which absorb light at the orange–red end of the visible spectrum; MW (middle wave), absorbing light in the green–yellow spectral region; SW (short wave), absorbing light in the blue–green spectral region; and VS (violet-sensitive), which absorbs light in the violet-ultraviolet spectral region.

      The photoreceptor pigments in the LW, MW, and SW types of cone receptor differ one from another, but each cone type is highly similar across all birds species. However, the VS cones can contain two different types of photopigments. One type has a peak sensitivity in the violet at about 410 nm, which is within the human visible spectrum. The other type has its sensitivity centred around 360 nm, which is in the part of the spectrum not visible to humans. It is referred to as the UVS pigment. Cone photoreceptors that contain UVS pigment are found only in songbirds (oscine passerines) and in some non-passerine species: gulls, ostriches, and parrots. It is those species which have the UVS photopigments that have true ultraviolet vision.

      Double cones are widespread in vertebrates but are absent from mammals. In birds, the double cones always contain one type of pigment. It has broad sensitivity across the spectrum centred