Color vision in marmosets and tamarins - behavioral evidence.pdf

8/14/2019 Color vision in marmosets and tamarins - behavioral evidence.pdf

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Over the past 20 years, the color vision of marmosets and tamarins has beenstudied. With the exception of the genus Mico, representatives from all theremaining genera of callitrichids [Rylands et al., 2000], totaling 17 differentspecies, have been studied by different methodologies (see Table I). Except for a study by Savage et al. [1987], previous works supported the existence of a visualpolymorphism in these animals. This X-linked visual polymorphism is producedby the activity of genes at a single locus on the X-chromosome. There are threealleles at this locus, and their individual actions result in the production of thethree cone types (about 543 nm, 556 nm, and 563 nm) found among callitrichids[Surridge & Mundy, 2002]. This results in up to six different color-visionphenotypes in the population.

Color perception is a result of active operations carried out in the nervoussystem as a whole [Gegenfurtner & Kiper, 2003; Zeki, 1999], and cannot beinferred directly from knowledge of the photoreceptor sensitivities [Surridgeet al., 2003]. Consequently, a good survey on color vision should include directbehavioral evidence and carefully control for brightness cues [Jacobs, 1993]. Some

behavioral experiments using monochromatic lights have established a directcorrelation between each color-vision phenotype and its corresponding colorperception (e.g., in Saguinus fuscicollis [Jacobs et al., 1987] and Callithrix

jacchus [Tovee et al., 1992]). This linkage between behavioral test results andpigment measurements implies that measurements of either kind can be used todraw inferences about the other [Jacobs, 1996].

The spectral tuning of the opsins of each phenotype may render them eachmore or less advantageous under different photic conditions [Smith et al., 2003].It is possible that different color-vision phenotypes occupy various locationswithin the rainforest, such as the canopy or relatively open areas at the forestedge [Mollon et al., 1984]. Smith et al. [2003] pointed out that it would be

TABLE I. List of Callitrichid Species Previously Studied for Color Vision

Species Method Reference

Callimico goeldii G Surridge & Mundy [2002]Callithrix geoffroyi G Caine & Mundy [2000]Callithrix jacchus B, M, G Tovee et al. [1992]; Hunt et al. [1993]Callithrix penicillata B Pessoa et al. [2005a]Cebuella pygmaea G Surridge & Mundy [2002]

Leontopithecus chrysomelas G, B Surridge & Mundy [2002]; Pessoa et al. [2005b] Leontopithecus chrysopygus G Surridge & Mundy [2002] Leontopithecus rosalia G, E Surridge & Mundy [2002]; Jacobs & Deegan

[2003]Saguinus bicolor G Surridge & Mundy [2002]Saguinus fuscicollis B, E, G Jacobs et al. [1987]; Jacobs et al. [1993]Saguinus geoffroyi G Surridge & Mundy [2002]Saguinus imperator G Surridge & Mundy [2002]Saguinus labiatus G Surridge & Mundy [2002]Saguinus midas midas E Jacobs & Deegan [2003]Saguinus midas niger B Pessoa et al. [2003]Saguinus mystax G Shyue et al. [1998]Saguinus oedipus oedipus B, G, E Savage et al. [1987]; Surridge & Mundy [2002];

Jacobs & Deegan [2003]

B, behavior; E, electroretinography; G, molecular genetics; M, microspectrophotometry.

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Am. J. Primatol. DOI 10.1002/ajp



informative to examine the actual foraging efficiency of the six phenotypes, andthe differences among them in performing color discrimination tasks.

Therefore, to obtain a better understanding of the color-vision capabilities of marmosets and tamarins, we performed a series of experiments using a behavioral paradigm of discrimination learning, and stimuli of wide and complexspectral reflectance compositions and varying brightness.

MATERIALS AND METHODS

Subjects

Five adult black-tufted-ear marmosets (Callithrix penicillata; two males(MC1 and MC2) and three females (FC1, FC2, and FC3)), six adult golden-headedlion tamarins ( Leontopithecus chrysomelas; three males (ML1, ML2, and ML3)and three females (FL1, FL2, and FL3)), and four adult black-handed tamarins(Saguinus midas niger; three males (MS1, MS2, and MS3) and one female (FS1))were used in the experiments. The subjects were housed and maintained at thePrimate Center of the University of Brasilia, alone or in groups of two or threeindividuals. The animals were tested in their own home cages (1.0 m wide 1.5mlong 1.9 m high) to avoid the stress inflicted by daily capture and transportationto a novel environment [Savage et al., 1987]. They were not deprived of foodor water. However, during the experimental sessions, food was removed fromthe cage. The experimental sessions were conducted three times a week between8:00 A.M. and 12:00 P.M., under natural daylight diffuse illumination. Informationabout the color-vision genotypes of these animals was unavailable.

Stimuli

The Munsell Book of Color, which contains over 1,600 color chips, was used toassess the animals’ color discrimination abilities. In this system every color patchis specified by three attributes of color: hue, brightness, and saturation. The huesare based on 10 categories that were derived from standard human observers(normal trichromats): red (R), yellow-red (YR), yellow (Y), green-yellow (GY),green (G), blue-green (BG), blue (B), purple-blue (PB), purple (P), and red-purple(RP). Each hue category has four different spectral points: 2.5, 5, 7.5, and 10. Tomake sure that discriminations were based on color rather than brightness cues,we tested the animals with stimuli of the same hue but of random brightnessvalues [Pessoa et al., 2005b].

The pairs of Munsell color chips used in this study were selected in an earlier

experiment with six human subjects (three deutans (showing color-visionanomalies in the green range) and three protans (showing color-vision anomaliesin the red range)) who were diagnosed by the Ishihara test. The subjects wereinitially required to organize 150 different Munsell color chips (of varying hues,brightness, and saturations) in as many groups as desired, according to colorappearance. Afterwards they were required to pair similar chips in each group.

Any odd pairing detected by the experimenter, a trichromat, was interpreted as a range of spectral reflectance confusion. Only odd pairs that where selected byevery protan subject (protan ‘‘difficult’’ pair) and every deutan subject (deutan‘‘difficult’’ pair) – 2.5YR vs. 7.5GY and 10YR vs. 5GY, respectively – were chosenfor the experiments. Furthermore, to estimate the degree of difficulty of each pairof stimuli, four human subjects (one protan, one deutan, and two trichromats)were tested in two choice color discrimination tasks, using the same apparatusand a procedure similar to that used for the monkeys [Gomes et al., 2002].

Color Vision in Callitrichids / 489




Some of the pairs (YR vs. G) presented during the experimental sessionsresembled the hues of natural targets (fruits and leaves) [Savage et al., 1987;Terborgh, 1983] as judged by a human observer. Recent studies successfully usedstimuli in this same spectral reflectance range to assess the color vision of dichromatic and trichromatic primates [Caine & Mundy, 2000; Gomes et al.,2002; Pessoa et al., 2003, 2005a; Smith et al., 2003]. Similarly to natural elements,Munsell color chips show wide and complex surface reflectance functions [Pessoa et al., 2003] and varying brightness levels.

Apparatus and Procedure

A plexiglas version of the Wisconsin General Test Apparatus [Pessoa et al.,2005a] was used to assess the color perception of the callitrichids. The animalshad to perform two choice discrimination tasks between a positive discriminativestimulus (SD1, the rewarded stimulus) and a negative discriminative stimulus(SD–, never rewarded). The left or right position of the SD1 was determined

according to the Gellerman table of random numbers [Gellerman, 1933]. Someof these pairs of stimuli were 1) easily discriminated by trichromats anddichromats (‘‘easy’’ pairs), 2) easily discriminated by trichromats and poorlydiscriminated by dichromats (‘‘difficult’’ pairs), or 3) poorly discriminatedby trichromats and dichromats (‘‘impossible’’ pairs). The ‘‘easy’’ pairs were outof the dichromats’ confusion range and represented the pairing of purple-blues,blues, and blue-greens (2.5PB, 7.5B, and 10BG) with yellow-reds (2.5YR and10YR). The ‘‘difficult’’ pairs were composed of green-yellows (5GY and 7.5GY) vs.

yellow-reds (2.5YR and 10YR). The ‘‘impossible’’ pair was constituted by pairing yellow-reds (10YR) against yellow-reds (10YR), making their discriminationunattainable. Each brightness level of the SD1 was paired to each brightness

level of the SD–, for a total of 16 pairs. These pairs were presented three timeseach, totaling 48 trials per experimental session. Based on these 48 trials,a percentage of correct responses was determined. After the subjects finishedthe testing phase, they were introduced into another training phase with a different SD1.

Statistical Analyses

The binomial test was used to construct the 95% confidence limits aroundchance performance based on the number of test trials. For 48 test trials, theupper limit was determined as 65%. The performance of all subjects wascompared to these confidence limits, and any performance above the upper limit

was considered significant ( Po0.05). Performances between pairs were comparedvia the McNemar test, and differences were considered significant at Po0.05.

RESULTS

Data from humans show that protans and deutans perceive the pairings of 2.5YR vs. 7.5GY, and 10YR vs. 5GY differently. Chips from the former pairing (2.5YR vs. 7.5GY) but not the latter (10YR vs. 5GY) are perceptually identical forprotans, and vice versa for deutans. This finding suggests that these twoexperimental pairings represent different perceptual challenges to individualswith red/green color-vision deficiencies. Therefore, we compared the two in thisstudy.

As shown in Figs. 1 and 2, 10 subjects (eight males (MC1, MC2, ML1, ML2,ML3, MS1, MS2, and MS3) and two females (FC1 and FL1)) made good

490 / Pessoa et al.




0

20

40

% C

o r r e c t r e s p o n s e s

60

80

100 #

2.5YR vs. 10BG* 2.5YR vs. 7.5GY**

Pairing

MC1

MC2

ML1

ML2

ML3

MS1

MS2

MS3

FC1

FL1

FL2

FL3

FC2

FC3

FS1

Fig. 1. Color perception in callitrichids, with the Munsell chip 2.5YR (yellow-red) as positivediscriminating stimulus (SD1). The negative discriminating stimuli (SD–) are shown on theabscissa: 10BG (blue-green) and 7.5GY (green-yellow). The horizontal line indicates the upper limit(65% of correct responses) of the 95% confidence interval for discriminative performance. easypair; difficult pair, ] significantly different performance ( Po0.05).

0

20

40

60

80

100

10YR vs. 7.5B* 10YR vs. 5GY**

Pairing

MC1

MC2

ML1

ML2

ML3

MS1

MS2

MS3FC1

FL1

FL2

FL3

FC2

FC3

FS1

% C

o r

r e c t r e s p o n s e s

Fig. 2. Color perception in callitrichids, with the Munsell chip 10YR (yellow-red) as the positive

discriminating stimulus (SD1). The negative discriminating stimuli (SD–) are shown on theabscissa: 7.5B (blue) and 5GY (green-yellow). easy pair, difficult pair. Other conventions as inFig. 1.





discriminations between ‘‘easy’’ pairs ( Po0.05), but performed poorly with bothof the ‘‘difficult’’ pairs ( P40.05). Alternatively, five female subjects (FL2, FL3,FC2, FC3, and FS1) did well on both ‘‘easy’’ and ‘‘difficult’’ pairs ( Po0.05).However, some behavioral differences were observed among these five subjects.

While FC3 and FS1 performed well with both YR vs. GY pairs ( Po0.05), FL2 andFL3 showed a chance performance for the deutan ‘‘difficult’’ pair (10YR vs. 5GY,

P40.05; Fig. 2), and FC2 had a lower performance on the protan ‘‘difficult’’ pair(2.5YR vs. 7.5GY; Fig. 1). Although FC2 showed an above chance performance( Po0.05) in ‘‘difficult’’ pairs, her performance differed significantly between2.5YR vs. 7.5GY (‘‘difficult’’ pair) and 2.5YR vs. 10BG (‘‘easy’’ pair) (w2511.077,

Po0.05). As a control for hue cues, all of the marmosets and tamarins showed a chance

level performance ( P40.05) in the ‘‘impossible’’ pair, when YRs were pairedagainst YRs (Fig. 3), demonstrating that their discriminations were based solelyon hue.

These findings are in accordance with the existence of a visual polymorphism

in callitrichids. Based on the data shown in Figs. 1–3, four kinds of behavioralphenotypes can be identified among the 15 callitrichids investigated (Table II).Phenotype A includes those subjects that could not discriminate any ‘‘difficult’’pair (MC1, MC2, ML1, ML2, ML3, MS1, MS2, MS3, FC1, and FL1). Animals thatcould discriminate any ‘‘difficult’’ pair (FC3 and FS1) comprise phenotype B.Phenotypes C and D include animals that showed discriminative problems withthe deutan ‘‘difficult’’ pair (FL2 and FL3) or the protan ‘‘difficult’’ pair (FC2),respectively.

0

20

40

60

80

100

10 YR vs. 2.5PB* 10YR vs. 10YR***

Pairing

MC1

MC2

ML1

ML2

ML3

MS1

MS2

MS3FC1

FL1

FL2

FL3

FC2

FC3

FS1

% C

o r r

e c t r e s p o n s e s

Fig. 3. Color perception in callitrichids, with the Munsell chip 10YR (yellow-red) as the positive

discriminating stimulus (SD1). The negative discriminating stimuli (SD–) are shown on theabscissa: 2.5PB (purple-blue) and 10YR (yellow-red). easy pair, impossible pair. Otherconventions as in Fig. 1.

492 / Pessoa et al.




DISCUSSION

It is well known that marmosets and tamarins have three different middle(M) to long (L) wavelength alleles that code for opsins with maximum spectralsensitivities of about 543 nm, 556 nm, and 563 nm [Surridge & Mundy, 2002].

These alleles allow the existence of six separate color-vision phenotypes in thepopulation, three kinds of trichromacy, and three kinds of dichromacy. Twoexperiments [Jacobs et al., 1987; Tovee et al., 1992] involving a total of 13 animals(six dichromats and seven trichromats) tested with monochromatic stimulishowed that each of these phenotypes appear to have different color-discrimina-tive abilities.

Similarly, our behavioral data from 15 additional subjects, tested with stimuliof wide and complex spectral compositions, suggest the existence of four differentkinds of color-vision phenotypes (Table II). No behavioral differences weredetected among the 10 subjects of phenotype A, which supposedly weredichromats. Since our animals have not been genotyped, we cannot affirm that

they have the same photopigments. However, considering that these 10 subjectscome from different species, some genetic variation is expected. Therefore, it isreasonable to think that regardless of genotype, dichromats’ color discriminationabilities are very similar for this kind of task. On the other hand, three possiblytrichromatic phenotypes were observed, with phenotype B exhibiting a bettercolor discrimination than phenotypes C or D. Actually, as Regan et al. [2001]pointed out, phenotypes that experience a smaller range of absolute input signalsmay exhibit poorer color discrimination on the red/green axis. In other words,trichromats with more widely separated photopigments may experience bettercolor discrimination. It is not known whether the behavioral phenotypes B, C, andD have a different genetic basis, nor has their relationship to the three differenttrichromatic genotypes found among callitrichids been determined. Molecular-

TABLE II. Subjects’ Behavioral Performances and Phenotypes

Behavioral performance on each pair

Subjects2.5YR vs

10BG2.5YR vs

7.5GY 10YR vs

7.5B10YR vs

5GY 10YR vs

2.5PB10YR vs

10YRBehavioralphenotypes

MC1 AC R AC R AC R Phenotype A MC2 AC R AC R AC R Phenotype A

ML1 AC R AC R AC R Phenotype A ML2 AC R AC R AC R Phenotype A ML3 AC R AC R AC R Phenotype A MS1 AC R AC R AC R Phenotype A MS2 AC R AC R AC R Phenotype A MS3 AC R AC R AC R Phenotype A FC1 AC R AC R AC R Phenotype A FL1 AC R AC R AC R Phenotype A FC3 AC AC AC AC AC R Phenotype BFS1 AC AC AC AC AC R Phenotype BFL2 AC AC AC R AC R Phenotype CFL3 AC AC AC R AC R Phenotype CFC2 AC AC AC AC AC R Phenotype D

AC, above chance; R, random; AC*, above chance but performance significantly less than on 2.5YR vs 10BGdiscrimination.





genetic analyses would help to answer this question; however, we predict thatphenotype B is the behavioral form of a trichromacy that involves more widelyseparated photopigments.

Color vision appears to impose costs on spatial vision [Regan et al., 2001]. Thespectral tuning of the M and L cone pigments observed in primates may be a trade-off to maintain a certain minimum separation between the M and Lpigments in order to have good color discrimination, while causing the leastpossible impairment in spatial vision [Regan et al., 2001]. Dichromats lackspectrally distinct L and M cone classes, and therefore have improved spatialvision, which would account for better detection of edges and camouflaged targets[Morgan et al., 1992]. Moreover, just as dichromats may have the advantage overtrichromats for some tasks, different trichromatic phenotypes may haveadvantages over each other. Regan et al. [2001] showed that in extreme cases,certain fruits may be more detectable by one platyrrhine phenotype than another.

As a matter of fact, a study [Surridge & Mundy, 2002] that examined a totalof 233 photopigment alleles from 172 callitrichids found that 33% of alleles coded

for 543 nm opsins, 17% coded for 556 nm opsins, and 50% coded for 563 nm opsins. A more recent and complete survey by Rowe and Jacobs [2004] supports thispattern (with 37%, 20%, and 44% reported for the 543, 556, and 562 nm opsins,respectively), as does a new data set reported in this volume by Surridge et al.Taken together, these findings suggest that the intermediate opsin (556 nm) maybe less advantageous than the other two opsins (543 and 563 nm). By means of frequency-dependent selection, an opposing advantage and disadvantage wouldmaintain the minority allele at a stable frequency [Mollon et al., 1984], ensuring the perpetuation of a color-vision polymorphism in callitrichids.

ACKNOWLEDGMENTS

D.M.A.P. received a doctoral fellowship from CNPq. We thank R.C.A. Ajuz,M.F.P. Araujo, L.A. Guimaraes, A.J. Baptista, F.C. Bicudo, L.S. Carvalho, J.F.Cunha, P.Q. Cruz, E.S. Perini, and R.V.L. Silva for their help in running theexperiments, and R. de Oliveira for animal care and maintenance. We also thankH. Buchanan-Smith for the extensive editorial work done on the manuscript. The

Animal Research Ethics Committee of the University of Brasilia approved theresearch protocol.

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Color vision in marmosets and tamarins - behavioral evidence.pdf