Colour discrimination learning in black-handed tamarin (<Emphasis Type="Italic">Saguinus midas niger</Emphasis>)

Colour is one cue that monkeys use for perceptual segregation of targets and to identify food resources. For fruit-eating primates such as Saguinus, an accurate colour perception would be advantageous to help find ripe fruits at distance. The colour vision abilities of black-handed tamarins (Saguinus midas niger) were assessed through a discrimination learning paradigm using Munsell colour chips as stimuli. Pairs of chips were chosen from an early experiment with protan and deutan humans. The monkeys (three males and one female) were tested with stimuli of the same hue, but different brightness values, in order to make sure that discriminations were based on colour rather than brightness cues. The results showed that the female, but not the males, presented an above-chance performance for stimuli resembling hue conditions under which tamarins forage (oranges vs greens). Colour vision in S. m. niger is discussed according to the advantages and disadvantages of dichromatism in daily search for food as well as to aspects regarding polymorphism in New World monkeys.     

Advantage of dichromats over trichromats in discrimination of color-camouflaged stimuli in nonhuman primates

Due to a middle- to long-wavelength-sensitive (M/LWS) cone opsin polymorphism, there is considerable phenotypic variation in the color vision of New World monkeys. Many females have trichromatic vision, whereas some females and all males have dichromatic vision. The selective pressures that maintain this polymorphism are unclear. In the present study we compared the performance of dichromats and trichromats in a discrimination task. We examined tri- and dichromatic individuals of two species: brown capuchin monkeys (Cebus apella) and long-tailed macaques (Macaca fascicularis). We also examined one protanomalous chimpanzee (Pan troglodytes). The subjects' task was to discriminate a circular pattern from other patterns in which textural elements differed in orientation and thickness from the background. After they were trained with stimuli of a single color, the subjects were presented with color-camouflaged stimuli with a green/red mosaic overlaid onto the pattern. The dichromatic monkeys and the protanomalous chimpanzee selected the correct stimulus under camouflaged conditions at rates significantly above chance levels, while the trichromats did not. These findings demonstrate that dichromatic nonhuman primates possess a superior visual ability to discriminate color-camouflaged stimuli, and that such an ability may confer selective advantages with respect to the detection of cryptic foods and/or predators.     

Polymorphism of visual pigment genes in the muriqui (Primates, Atelidae)

Colour vision varies within the family Atelidae (Primates, Platyrrhini), which consists of four genera with the following cladistic relationship: {Alouatta[Ateles (Lagothrix and Brachyteles)]}. Spider monkeys (Ateles) and woolly monkeys (Lagothrix) are characteristic of platyrrhine monkeys in possessing a colour vision polymorphism. The polymorphism results from allelic variation of the single-locus middle-to-long wavelength (M/L) cone opsin gene on the X-chromosome. The presence in the population of alleles coding for different M/L photopigments results in a variety of colour vision phenotypes. Such a polymorphism is absent in howling monkeys (Alouatta), which, alone among platyrrhines, acquired uniform trichromatic vision similar to that of Old World monkeys, apes, and humans through opsin gene duplication. Dietary and morphological similarities between howling monkeys and muriquis (Brachyteles) raise the possibility that the two genera share a similar form of colour vision, uniform trichromacy. Yet parsimony predicts that the colour vision of Brachyteles will resemble the polymorphism present in Lagothrix and Ateles. Here we test this assumption. We obtained DNA from the blood or faeces of 18 muriquis and sequenced exons 3 and 5 of the M/L opsin gene. Our results affirm the existence of a single M/L cone opsin gene in the genus Brachyteles. We detected three alleles with predicted lambdamax values of 530, 550, and 562 nm. Two females were heterozygous and are thus predicted to have different types of M/L cone pigment. We discuss the implication of this result towards understanding the evolutionary ecology of trichromatic vision.     

Non-random association of opsin alleles in wild groups of red-bellied tamarins (Saguinus labiatus) and maintenance of the colour vision polymorphism

The remarkable X-linked colour vision polymorphism observed in many New World primates is thought to be maintained by balancing selection. Behavioural tests support a hypothesis of heterozygote advantage, as heterozygous females (with trichromatic vision) exhibit foraging benefits over homozygous females and males (with dichromatic vision) when detecting ripe fruit on a background of leaves. Whilst most studies to date have examined the functional relevance of polymorphic colour vision in the context of foraging behaviour, alternative hypotheses proposed to explain the polymorphism have remained unexplored. In this study we examine colour vision polymorphism, social group composition and breeding success in wild red-bellied tamarins Saguinus labiatus. We find that the association of males and females within tamarin social groups is non-random with respect to colour vision genotype, with identified mating partners having the greatest allelic diversity. The observed distribution of alleles may be driven by inbreeding avoidance and implies an important new mechanism for maintaining colour vision polymorphism. This study also provides the first preliminary evidence that wild trichromatic females may have increased fitness compared with dichromatic counterparts, as measured by breeding success and longevity.     

Colour cues proved to be more informative for dogs than brightness

The results of early studies on colour vision in dogs led to the conclusion that chromatic cues are unimportant for dogs during their normal activities. Nevertheless, the canine retina possesses two cone types which provide at least the potential for colour vision. Recently, experiments controlling for the brightness information in visual stimuli demonstrated that dogs have the ability to perform chromatic discrimination. Here, we show that for eight previously untrained dogs colour proved to be more informative than brightness when choosing between visual stimuli differing both in brightness and chromaticity. Although brightness could have been used by the dogs in our experiments (unlike previous studies), it was not. Our results demonstrate that under natural photopic lighting conditions colour information may be predominant even for animals that possess only two spectral types of cone photoreceptors.     

Color Vision in <Emphasis Type="Italic">Leontopithecus chrysomelas</Emphasis>: A Behavioral Study

We assessed the color discriminations by golden-headed lion tamarins (Leontopithecus chrysomelas) via a series of tasks involving a behavioral paradigm that maximizes the naturalness of the stimuli. The stimuli were pairs of Munsell color chips used in earlier experiments with human dichromats. We tested 3 male and 3 female monkeys with stimuli of random brightness values in order to assure that discriminations were based on color rather than brightness cues. Results indicate that each male and one female presented random performances for stimuli resembling hue conditions under which tamarins forage: oranges vs. greens. Two females exhibited discriminations consistent with allelic trichromacy. Findings indicate the presence of an M/L cone opsin polymorphism, a condition of most platyrrhines that is characterized by dichromatic and/or trichromatic females and dichromatic males. Interspecific differences in allelic frequency among lion tamarins raises the possibility that habitat fragmentation is affecting heterozygous frequencies, a trend that could impact tamarin foraging efficiency.     

Photopigments and colour vision in New World monkeys from the family Atelidae

Most New World monkeys have an X-chromosome opsin gene polymorphism that produces a variety of different colour vision phenotypes. Howler monkeys (Alouatta), one of the four genera in the family Atelidae lack this polymorphism. Instead, they have acquired uniform trichromatic colour vision similar to that of Old World monkeys, apes and people through opsin gene duplication. In order to determine whether closely related monkeys share this arrangement, spectral sensitivity functions that allow inferences about cone pigments were measured for 56 monkeys from two other Atelid genera, spider monkeys (Ateles) and woolly monkeys (Lagothrix). Unlike howler monkeys, both spider and woolly monkeys are polymorphic for their middle- and long-wavelength cone photopigments. However, they also differ from other polymorphic New World monkeys in having two rather than three possible types of middle- and long-wavelength cone pigments. This feature directly influences the relative numbers of dichromatic and trichromatic monkeys.     

A foraging advantage for dichromatic marmosets (Callithrix geoffroyi) at low light intensity

Most New World monkey species have both dichromatic and trichromatic individuals present in the same population. The selective forces acting to maintain the variation are hotly debated and are relevant to the evolution of the ‘routine’ trichromatic colour vision found in catarrhine primates. While trichromats have a foraging advantage for red food compared with dichromats, visual tasks which dichromats perform better have received less attention. Here we examine the effects of light intensity on foraging success among marmosets. We find that dichromats outperform trichomats when foraging in shade, but not in sun. The simplest explanation is that dichromats pay more attention to achromatic cues than trichromats. However, dichromats did not show a preference for foraging in shade compared with trichromats. Our results reveal several interesting parallels with a recent study in capuchin monkeys (Cebus capucinus), and suggest that dichromat advantage for certain tasks contributes to maintenance of the colour vision polymorphism.     

Evolutionary renovation of L/M opsin polymorphism confers a fruit discrimination advantage to ateline New World monkeys

New World monkeys exhibit prominent colour vision variation due to allelic polymorphism of the long‐to‐middle wavelength (L/M) opsin gene. The known spectral variation of L/M opsins in primates is broadly determined by amino acid composition at three sites: 180, 277 and 285 (the ‘three‐sites’ rule). However, two L/M opsin alleles found in the black‐handed spider monkeys (Ateles geoffroyi) are known exceptions, presumably due to novel mutations. The spectral separation of the two L/M photopigments is 1.5 times greater than expected based on the ‘three‐sites’ rule. Yet the consequence of this for the visual ecology of the species is unknown, as is the evolutionary mechanism by which spectral shift was achieved. In this study, we first examine L/M opsins of two other Atelinae species, the long‐haired spider monkeys (A. belzebuth) and the common woolly monkeys (Lagothrix lagotricha). By a series of site‐directed mutagenesis, we show that a mutation Y213D (tyrosine to aspartic acid at site 213) in the ancestral opsin of the two alleles enabled N294K, which occurred in one allele of the ateline ancestor and increased the spectral separation between the two alleles. Second, by modelling the chromaticity of dietary fruits and background leaves in a natural habitat of spider monkeys, we demonstrate that chromatic discrimination of fruit from leaves is significantly enhanced by these mutations. This evolutionary renovation of L/M opsin polymorphism in atelines illustrates a previously unappreciated dynamism of opsin genes in shaping primate colour vision.     

Patterns of chromatic information processing in the lobula of the honeybee, Apis mellifera L

The honeybee, Apis mellifera L., is one of the living creatures that has its colour vision proven through behavioural tests. Previous studies of honeybee colour vision has emphasized the relationship between the spectral sensitivities of photoreceptors and colour discrimination behaviour. The current understanding of the neural mechanisms of bee colour vision is, however, rather limited. The present study surveyed the patterns of chromatic information processing of visual neurons in the lobula of the honeybee, using intracellular recording stimulated by three light-emitting diodes, whose emission spectra approximately match the spectral sensitivity peaks of the honeybee. The recorded visual neurons can be divided into two groups: non-colour opponent cells and colour opponent cells. The non-colour opponent cells comprise six types of broad-band neurons and four response types of narrow-band neurons. The former might detect brightness of the environment or function as chromatic input channels, and the latter might supply specific chromatic input. Amongst the colour opponent cells, the principal neural mechanism of colour vision, eight response types were recorded. The receptive fields of these neurons were not centre surround as observed in primates. Some recorded neurons with tonic post-stimulus responses were observed, however, suggesting temporal defined spectral opponency may be part of the colour-coding mechanisms.     

Fruits, foliage and the evolution of primate colour vision

Primates are apparently unique amongst the mammals in possessing trichromatic colour vision. However, not all primates are trichromatic. Amongst the haplorhine (higher) primates, the catarrhines possess uniformly trichromatic colour vision, whereas most of the platyrrhine species exhibit polymorphic colour vision, with a variety of dichromatic and trichromatic phenotypes within the population. It has been suggested that trichromacy in primates and the reflectance functions of certain tropical fruits are aspects of a coevolved seed-dispersal system: primate colour vision has been shaped by the need to find coloured fruits amongst foliage, and the fruits themselves have evolved to be salient to primates and so secure dissemination of their seeds. We review the evidence for and against this hypothesis and we report an empirical test: we show that the spectral positioning of the cone pigments found in trichromatic South American primates is well matched to the task of detecting fruits against a background of leaves. We further report that particular trichromatic platyrrhine phenotypes may be better suited than others to foraging for particular fruits under particular conditions of illumination; and we discuss possible explanations for the maintenance of polymorphic colour vision amongst the platyrrhines.     

Trans-specific evolution of opsin alleles and the maintenance of trichromatic colour vision in Callitrichine primates

Many New World (NW) primates possess a remarkable polymorphism in an X-linked locus, which encodes for the visual pigments (opsins) used for colour vision. Females that are heterozygous for opsin alleles of different spectral sensitivity at this locus have trichromatic colour vision, whereas homozygous females and males are dichromatic, with poor colour discrimination in the red-green range. Here we describe an extensive survey of allelic variation in both exons and introns at this locus within and among species of the Callitrichines (marmosets and tamarins). All five genera of Callitrichines have the X-linked polymorphism, and only the three functional allelic classes described previously (with maximum wavelength sensitivities at about 543 nm, 556 nm and 563 nm) were found among the 16 species and 233 or more X-chromosomes sampled. In spite of the homogenizing effects of gene conversion, phylogenetic analyses provide direct evidence for trans-specific evolution of alleles over time periods of at least 5-6 million years, and up to 14 million years (estimated from independent phylogenies). These conclusions are supported by the distribution of insertions and deletions in introns. The maintenance of polymorphism over these time periods requires an adaptive explanation, which must involve a heterozygote advantage for trichromats. The lack of detection of alleles that are recombinant for spectral sensitivity suggests that such alleles are suboptimal. The two main hypotheses for the selective advantage of trichromacy in primates are frugivory for ripe fruits and folivory for young leaves. The latter can be discounted in Callitrichines, as they are not folivorous.     

New World Monkeys and Color

The visual worlds of most primates are rich with potential color signals, and many representatives of the order have evolved the biological mechanisms that allow them to exploit these sources of information. Unlike the catarrhines, platyrrhines typically have sex-linked polymorphic color vision that provides individuals with any of several distinct types of color vision, including both trichromatic and dichromatic variants. In recent years, this polymorphism has been the target of an expanding range of research efforts. As a result, researchers now reasonably understand the proximate biology underlying the polymorphisms, and a number of ideas have emerged as to their evolution. Progress has also been made in illuminating how color vision capacities may be related to the particular visual tasks that New World monkeys face.     

The effect of cholinergic substances on the mechanisms of visual recognition in monkeys

In monkeys (Macaca mulatta) instrumental reflex was elaborated with differentiation of black-and-white and colour visual stimuli in condition of systemic administration of pharmacological preparations selectively influencing the functional state of cholinergic brain structures. Differentiation of black-and-white and colour stimuli is not disturbed by atropine (0.1 mg/kg) and amizile (up to 1.5 mg/kg) injections; at greater doses frustration of the instrumental reflex takes place. Differentiation of black-and-white and colour stimuli is disturbed at injection of various doses of antidepressant phthoracizine: 5 mg/kg and 7 mg/kg, respectively. These disturbances are restored by the injection of definite doses of galantamine; for correction of colour differentiation a greater dose is required. The obtained data point to differences in neurophysiological and neurochemical processes responsible for black-and-white and colour vision.     

Demonstration of a foraging advantage for trichromatic marmosets (Callithrix geoffroyi) dependent on food colour

It has been suggested that the major advantage of trichromatic over dichromatic colour vision in primates is enhanced detection of red/yellow food items such as fruit against the dappled foliage of the forest. This hypothesis was tested by comparing the foraging ability of dichromatic and trichromatic Geoffroy's marmosets (Callithrix geoffroyi) for orange- and green-coloured cereal balls (Kix) in a naturalized captive setting. Trichromatic marmosets found a significantly greater number of orange, but not green, Kix than dichromatic marmosets when the food items were scattered on the floor of the cage (at a potential detection distance of up to 6 m from the animals). Under these conditions, trichromats but not dichromats found significantly more orange than green Kix, an effect that was also evident when separately examining the data from the end of the trials, when the least conspicuous Kix were left. In contrast, no significant differences among trichromats and dichromats were seen when the Kix were placed in trays among green wood shavings (detection distance < 0.5 m). These results support an advantage for trichromats in detecting orange-coloured food items against foliage, and also suggest that this advantage may be less important at shorter distances. If such a foraging advantage for trichromats is present in the wild it might be sufficient to maintain the colour vision polymorphism seen in the majority of New World monkeys.     

Optimum probabilistic processing in colour perception. II. Colour vision as template matching.

A statistical approach to account for psychophysical phenomena in human colour vision is presented. The central visual processor is viewed as an optimum recognizer of stochastic patterns supplied by the periphery. The processor makes an optimum estimate of the spectral parameters of the stimulus, given the wavelength filter characteristics of the periphery, the stochastic nature of the information and an internal template to which the external stimulus is matched. The estimate is constrained in ways inferred from empirical phenomena. Subjective brightness of monochromatic stimuli and related constant brightness manifolds in the colour space constitute the constraint for brightness estimation. Results analogous and in accord with those of earlier line element theories are obtained. The Bezold-Brücke hue shift constitutes the basic constraint for hue estimation. The hue estimate involves interrelation between the fields in the experiment. Similarities and differences both in basic conceptions and results introduced by the template matching notions are discussed.     

Innate colour preferences of flower visitors

Freshly emerged flower visitors exhibit colour preferences prior to individual experience with flowers. The understanding of innate colour preferences in flower visitors requires a detailed analysis, as, on the one hand, colour is a multiple-signal stimulus, and, on the other hand, flower visits include a sequence of behavioural reactions each of which can be driven by a preferential behaviour. Behavioural reactions, such as the distant approach, the close-range orientation, the landing, and the extension of mouthparts can be triggered by colour stimuli. The physiological limitations of spectral sensitivity, the neuro-sensory filters, and the animals' different abilities to make use of visual information such as brightness perception, wavelength-specific behaviour and colour vision shape colour preferences. Besides these receiverbased factors, there are restrictions of flower colouration due to sender-based factors such as the absorption properties of floral pigments and the dual function of flower colours triggering both innate and learned behaviour. Recordings of the spectral reflection of coloured objects, which trigger innate colour preferences, provide an objective measure of the colour stimuli. Weighting the spectral reflection of coloured objects by the spectral composition of the ambient light and the spectral sensitivity of the flower visitors' photoreceptors allows the calculation of the effective stimuli. Perceptual dimensions are known for only a few taxa of flower visitors.     

Diurnality and cone photopigment polymorphism in strepsirrhines: examination of linkage in Lemur catta

Trichromatic color vision is routine among catarrhine primates, but occurs only as a variant form of color vision in some individuals in most platyrrhine genera. This arises from a fundamental difference in the organization of X-chromosome cone opsin genes in these two lineages: catarrhines have two opsin genes specifying middle- and long-wavelength-sensitive cone pigments, while platyrrhines have only a single gene. Some female platyrrhine monkeys achieve trichromacy because of a species polymorphism that allows the possibility of different opsin gene alleles on the two X-chromosomes. Recently, a similar opsin gene polymorphism was detected in some diurnal strepsirrhines, while at the same time appearing to be absent in any nocturnal genera. The aim of this study was to assess whether cone pigment polymorphism is inevitably linked to diurnality in strepsirrhines. Cone photopigments were measured in a species usually classified as diurnal, the ring-tailed lemur (Lemur catta), using electroretinogram flicker photometry, a noninvasive electrophysiological procedure. Each of 12 animals studied was found to have the same middle-wavelength cone pigment, with peak sensitivity at about 547 nm. In conjunction with earlier results, this implies that cone pigment polymorphism is unlikely to exist in this species and that, accordingly, such variation is not a consistently predictable feature of vision in diurnal strepsirrhines.     

Colour and brightness coding in the central nervous system: theoretical aspects and visual evoked potentials to homogeneous red and green stimuli

We designed visual evoked potentials experiments to study the differential aspects of colour and brightness coding in man. The substitution of equally bright red and green stimuli for a background yellow was investigated and compared with different luminance increments and decrements of red and green. A dominant N87 component was found for a colour change from yellow to brighter red colours, which was less pronounced for green and absent for yellow luminance changes. It is also absent for pure red luminance increments and green luminance changes, but reappears with red luminance decrements or red-offset. The data are discussed within the framework of a new concept of how the visual system fuses red-green information and black-white border information. Retinal X-cells can transmit colour and high spatial frequency achromatic information simultaneously by encoding only the presence of edges (a.c.) for the black-white stimuli and the presence of both edges (a.c.) and uniform areas of colour (d.c.) for red-green stimuli. Phylogenetically this kind of information transmission enables colour vision to be implemented in a retina such as the cat's by adding only a second class of cones. Barlow's economy principle will be violated for colour in the periphery, but restored early in the striate cortex where there is an early decoding of the combined chromatic and achromatic information by the concentric double opponent cells. The N87 behaviour correlates with the proposed discharge of peripheral X-type cells, but not with the discharge of cortical double opponent concentric or simple cells, which no longer respond to homogeneous colour stimuli. It is suggested that N87 may be generated by geniculate afferents in the dendritic arborization of cortical cells, reflecting the behaviour of peripheral units, and thus the violation of the economy principle, rather than the next step in cortical processing. The early cortical restoration of the economy principle is supported by the absence of any further dissociated behaviour for colour and brightness in later components.