In Color

Color is an important physical characteristic that can be used as a cue by primates to procure and ingest foods. Undoubtedly, the major importance of color vision in primates is in relation to angiosperms because these plants use color extensively in a reproductive context to attract pollinators and seed dispersers. Lemurs are effective pollinators (Birkinshaw and Colquhoun, 1998; Kress et al., 1994; Nilsson et al., 1993), which Sussman and Raven (1978) have suggested might have great significance for early primate evolution. However, color does not seem to play an important role in the lemur pollination syndromes that these authors describe. Some primates are also effective seed dispersers (Chapman, 1995), which connects to the proposal that the main reason for good color vision in primates is to find fruits (Allen, 1879; Mollon, 1989; Polyak, 1957), even though seed dispersal was not originally associated with this idea. However, recent evidence suggests that color vision that allows the discrimination of red hues largely evolved in primates in response to a search for young new red leaves (Lucas et al. 2003a; Stoner et al. 2005).

Analysis of the colors of fruits in primate diets indicates that yellow, orange-brown, and red fruits are common (Dominy, 2004a). As described later, the discrimination of these hues from a monotonous green background of mature foliage requires a type of color vision found, at least partially, in many primate species, called trichromacy. The wide variety of colors displayed by flowers and ripe fruit in tropical regions has not yet been fully explained in terms of the color preferences of presumed target pollinators or seed dispersers. In contrast, at least from the perspective of a reader living in temperate zones, foliage appears a dark uniform green and holds little interest for the color vision debate. However, depending on the time of year, a visitor to tropical rainforests often sees isolated flashes of red produced, not by flowers and fruits, but by young leaves. In fact, between 20% and 60% of forest plants in the tropics flush leaves with reddish tints (Dominy et al., 2002). The reasons are uncertain, but a major one appears to be crypsis (camouflage) from potential herbivores. Most herbivores appear to lack receptors for detecting the long wavelengths that dominate the reflectance spectra (which determines the color) of these leaves. If fruits are first in importance in the diets of most primates, then leaves run a close second for many larger species and dominate in some. Lucas et al. (1998, 2003a) have suggested that a reliance on leaves, at least as a fallback when fruits are unavailable, influenced the evolution of color vision in primates.

Color vision allows animals to discriminate light spectra by comparing responses of two or more photoreceptors with differing spectral sensitivities (Jacobs, 1993; Surridge et al., 2003). Spectral sensitivity is defined here as the relative probability of a photon of a given wavelength incident on the eye producing a response in the photoreceptor cell. The number of spectral receptors limits the dimensionality of color vision: two spectral types allow dichromacy with two primaries needed to match any spectrum; three spectral types allow trichromacy with three primaries being required, and so forth. As well as number of receptors, the ability to discriminate light spectra is affected by neural mechanisms of vision, and by spectral tuning of the photo receptors.

Cones are active only in daylight and the number of spectral types varies between taxonomic groups. In birds, for example, there are four types giving relatively even spectral coverage of 350-600 nm, and good color discrimination. By comparison most diurnal mammals have only two types of cone: a short-wavelength cone containing a pigment (opsin) with a peak absorbance in primates of about 420-440 nm and a long-wavelength cone with a variable peak absorbance of about 520-560 nm (Jacobs, 1993). Two groups of anthropoid primate—the catarrhines and the howler monkeys (genus Alouatta)—possess three cone types. The third cone has been produced by duplication of the gene coding for the opsin pigment in the long-wavelength cone. This occurred independently in Alouatta and in catarrhines, but the three cone types in both have remarkably consistent peak absorbances of around 430, 530, and 560 nm, respectively (Hunt et al., 1998).

The brain of a mammal with two cone types can compare the relative strengths of their outputs to give a "chromatic" signal. Color vision that is based on comparison of just two receptor types is termed dichromatic. Following human color psychology, these chromatic signals lie on what we call the "blue-yellow" perceptual axis (e.g., Regan et al., 2001). A dichromatic mammal will confuse many spectra that we can discriminate, especially those we recognize as reds, yellows, and greens. This is because, with three cone types, we can make two independent sets of comparisons between three outputs to give two sets of chromatic signals, and hence trichromatic color vision.

Many primate species with only two opsin gene loci have polymorphisms of the long-wavelength opsin (of still generally unknown gene frequencies) that, lying on the X chromosome, confer trichromacy on some females. These species include all New World monkey genera to be tested except Alouatta, which is fully trichromatic (Jacobs et al., 1996), and Aotus, which has only one cone type and is colorblind (Jacobs et al., 1993). Recently, the polymorphism has also been found among several strepsirrhines, including Propithecus verreauxi and Varecia variegata (Jacobs et al., 2002; Tan and Li, 1999).

Measurement of color is now beginning in primate field studies (Smith et al., 2003 a,b), and its analysis is developing rapidly (Kelber et al., 2003; Osorio et al., 2004), indicating its potential value to primates. Importantly for this chapter, mature leaves vary in color almost entirely in yellow-blueness, not in red-greenness (Dominy and Lucas, 2001; Osorio and Vorobyev, 1996; Regan et al., 2001; Sumner and Mollon, 2000) while both very young leaves and ripening fruits can show great differences in their red-green signal from mature foliage (Dominy and Lucas, 2001; Sumner and Mollon, 2000). In fruits though, this varies greatly depending on the final hue. Compared to mature foliage, some fruits stay green when ripe (and primates eat a surprisingly large amount of green fruit—Dominy, 2004a), while others ripen with change in the blue-yellow signal, the red-green signal, or with both.

In Black and White

Nocturnal vision utilizes rod photoreceptors that are sensitive to low-light intensities. In all mammals, these cells have only one spectral tuning (Ahnelt and Kolb, 2000). Since cones do not operate at low-light levels, no comparators are available with the result that rod vision is colorblind. Achromatic vision provided by rods or summed (rather than compared) red and green cone signals is used for many visual tasks including perception of motion, stereo-depth, and (for cones) fine spatial detail, which are all colorless (Livingstone and Hubel, 1988). Like most mammals, primates have both rods and cones in their retina, which implies activity in both night and day. Some primates are in fact capable of varying their activity patterns, day and night, to environmental conditions (e.g., the mongoose lemur, Eulemur mongoz—Curtis et al., 1999). A cone-rod balance is not universal. Some mammals have cone-dominated retinas, like squirrels and tupaiid tree shrews (Jacobs, 1993), while others like the pen-tailed tree shrew (Ptilocercus lowii) possess a retina that is almost entirely filled with rods (Emmons, 2000). The importance of light levels to all uses of color vision has been recognized in some work now being reported (Yamashita et al., 2005).

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