Colour Discrimination in the Black\u0026hyphen;Tufted\u0026hyphen;Ear Marmoset (Callithrix penicillata): Ecological Implications

$Page 1: Colour Discrimination in the Black\u0026hyphen;Tufted\u0026hyphen;Ear Marmoset (Callithrix penicillata): Ecological Implications$
Fax + 41 61 306 12 34 E-Mail [email protected] www.karger.com

�2005 S. Karger AG, Basel 0015–5713/05/0763–0125$22.00/0 Accessible online at: www.karger.com/fpr

Valdir Filgueiras Pessoa Laboratório de Neurociências e Comportamento CFS, IB, Universidade de Brasília, CEP 70910-900 Brasília, DF (Brazil), Tel. +55 61 3072175 Fax +55 61 2721497, E-Mail [email protected]

Original Article

Folia Primatol 2005;76:125–134 Received: November 13, 2003 DOI: 10.1159/000084375 Accepted after revision: June 26, 2004

Colour Discrimination in the Black-Tufted-Ear Marmoset (Callithrix penicillata): Ecological Implications

Daniel M.A. Pessoa Juliana F. Cunha Carlos Tomaz Valdir F. Pessoa

Laboratory of Neurosciences and Behaviour and Primate Centre, University of Brasilia, Brasilia, Brazil

Key Words Colour vision � Callithrix penicillata � Marmosets � New World monkeys � Feeding ecology � Discrimination learning � Munsell colour system � Naturalistic stimuli

Abstract The dietary diversity of marmosets is substantial, which may reflect differ-

ences in their colour vision. This study examined the colour discrimination ability of a gummivore/insectivore callitrichid, Callithrix penicillata, which inhabits the Brazilian cerrado (bush savanna). A series of ecologically relevant tasks, involv-ing a behavioural paradigm of discrimination learning in semi-natural conditions and the usage of ecologically relevant stimuli, was executed. Three marmosets, 2 males and a female, behaved like human dichromats, showing an impaired performance when orange and green stimuli had to be discriminated. In con-trast, 2 females resembled human trichromats, discriminating those kinds of pairs. Our data suggest that Callithrix penicillata presents a polymorphic trichro-macy, with dichromatic males and dichromatic or trichromatic females.

Introduction

In order to have colour vision, an animal must possess at least two types of photoreceptors, which differ in their absorption spectra and the presence of appro-priate nervous-system connections [Jacobs, 2002]. The number of cone pigment types found in the retina normally map directly into the dimensionality of colour vision as defined by behavioural tests of colour matching. This means that mea-

Copyright © 2005 S. Karger AG, Basel

http://dx.doi.org/10.1159%2F000084375

126 Folia Primatol 2005;76:125–134 Pessoa/Cunha/Tomaz/Pessoa

surements of either kind can be used to draw inferences about the other [Jacobs, 1996]. Therefore, if an animal has two types of functional photoreceptors, its vision is said to be dichromatic, whereas when three types of photoreceptors are active together, trichromacy results. Nevertheless, colour perception is a result of active operations carried out in the nervous system as a whole [Zeki, 1999; Gegenfurtner and Kiper, 2003] and cannot be inferred by knowledge of the photoreceptor sensi-tivities only [Surridge et al., 2003]. Supporting this idea, Jacobs et al. [1999] showed that some transgenic mice, diagnosed as trichromats by electrophysiology and molecular genetics, exhibited a dichromatic behaviour when tested in visual discrimination tasks. On the other hand, human dichromats expand their colour visual perception and behave as trichromats when colour stimuli reach parafoveal retinal areas [Smith and Pokorny, 1977] or are presented under low luminance lev-els [Paramei et al., 1998].

Generally, mammals present a dichromatic colour vision, with primates being exceptions to this rule [Jacobs, 1993]. The only non-primate mammals so far dis-covered to have trichromatic colour vision are two species of marsupials [Arrese et al., 2002]. All catarrhines (Old World monkeys and apes) show a routine trichro-macy that is exemplified by normal human vision [Jacobs and Deegan, 1999]. In contrast, most platyrrhines (New World monkeys) [Jacobs, 2002] and some prosimians [Tan and Li, 1999] display a sex-linked polymorphism, characterized by the presence of trichromatic and dichromatic females and only dichromatic males. The trichromacy of Alouatta (howler monkeys) and monochromacy of Aotus (owl monkeys) constitute two well-known exceptions to this rule [Jacobs, 2002].

The callitrichids form a specialized group of monkeys that fills a unique eco-logical role in the forests of Central and South America [Sussman and Kinzey, 1984]. They feed on three primary types of food items: insects; plant exudates; fruits, flowers and nectar. However, marmosets include more gum in their diet than do tamarins [Sussman and Kinzey, 1984]. Due to their large geographical range, occupation of diverse habitats and ecological differentiation within particular envi-ronments, the dietary diversity of marmosets is substantial [Sussman and Kinzey, 1984]. The precise foraging tasks involved in maintaining trichromacy are therefore likely to vary from species to species [Surridge and Mundy, 2002].

Marmosets comprise three genera (Callithrix, Cebuella and Mico) and 21 spe-cies [Rylands et al., 2000], of which only three, Callithrix jacchus, Callithrix geof-froyi and Cebuella pygmaea, have been investigated relative to their colour vision [Tovée et al., 1992; Caine and Mundy, 2000; Surridge and Mundy, 2002]. These animals are specialists [Rosenberger, 1992], presenting adaptations in their anterior dentition, mandible and caecum that seem to be directly related to gum feeding [Garber, 1992]. One of the most gummivorous species of marmosets, C. penicillata [Lacher et al., 1984], is able to occupy extremely seasonal habitats, such as gallery forest in savannahs, which lack fruits during extended periods [Rylands, 1996]. In the Brazilian savannah (Cerrado), during the dry season, gum comprises up to 50% of the plant items consumed by C. penicillata [Coimbra-Filho, 1992]. Flowers (e.g. Symphonia) and insects (e.g. grasshoppers) are also important food resources [Sussman and Kinzey, 1984; Rylands, 1989]. In spite of these peculiarities, few studies have analysed the visual system of C. penicillata [Pessoa et al., 1992].

We performed a series of experiments in semi-natural conditions to elucidate the colour vision capabilities of marmosets. Considering that a good survey on col-

Colour Perception in Callithrix penicillata 127 Folia Primatol 2005;76:125–134

our vision perception should include behavioural tests with careful control for brightness cues [Jacobs, 1993], we assessed the colour perception of C. penicillata by a behavioural paradigm of discrimination learning, using naturalistic stimuli.

Methods

Subjects Five adult black-tufted-ear marmosets (C. penicillata), 2 males (MC1, MC2) and 3

females (FC1, FC2, FC3), were used in the experiments. The subjects were kept in pairs, being housed and maintained in the Primate Centre of the University of Brasilia. The ani-mals were tested in their own home cages (1.0 m width × 1.5 m length × 1.9 m height) to avoid the stress inflicted by daily capture and transportation to a novel environment [Savage et al., 1987]. They were not food or water deprived. However, during the experimental ses-sions, food was removed from the cage. The subjects had no previous experience with two-choice colour discrimination training. In order to reach the experimental apparatus, each animal had to enter an experimental cage, placed inside its home cage. During each experi-ment, only a given subject was allowed into the experimental cage.

Stimuli The Munsell Book of Colour, containing over 1,600 colour chips, was used to assess

colour discrimination abilities. In this system, every colour patch is specified by 3 attributes: hue, brightness and saturation. Hues are based on 10 categories: 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 4 different spectral points: 2.5, 5, 7.5 and 10. A number and a letter represent the hue, whereas a fraction stands for brightness over saturation (e.g. the notation 5YR 7/8 corresponds to a 5 yellow-red colour chip, with brightness 7 and saturation 8). The Munsell system is a suitable method for testing colour discrimination in primates [Gomes et al., 2002; Pessoa et al., 2003].

To make sure that discriminations were based on colour rather than brightness cues, the animals were tested with stimuli of the same hue but different brightness values [Pessoa et al., 2003]. Eight colour chips accomplished each pair of stimuli: 4 different brightness levels from a determined hue paired against 4 different brightnesses of another hue. This resulted in a total of 16 different possible combinations.

The degree of difficulty of each pair was estimated, in a previous study [Gomes et al., 2002], by experiments involving human subjects and corroborated by experiments involving different Neotropical primates, such as Cebus apella [Gomes et al., 2002], Sa-guinus midas niger [Pessoa et al., 2003] and Leontopithecus chrysomelas [Pessoa et al., 2005].

Some pairs (oranges vs. greens) presented during the experimental sessions resembled the foraging conditions in which Neotropical primates search for food [Terborgh, 1983; Savage et al., 1987]. As occurs for natural elements, Munsell colour chips show wide spec-tral compositions [Pessoa et al., 2003], which qualifies them as naturalistic stimuli. Recent studies have successfully used stimuli in this same spectral range to assess the colour vision of dichromatic and trichromatic primates [Caine and Mundy, 2000; Gomes et al., 2002; Pes-soa et al., 2003; Smith et al., 2003].

Apparatus A Plexiglas version of the Wisconsin General Test Apparatus [Harlow and Bromer,

1938] was mounted in front of the marmosets’ home cage (fig. 1). This apparatus consisted of a portable tray, 2 stimulus holders and a movable screen. The portable tray had 2 food wells, spaced 12 cm apart, designed to hold the rewards (pieces of raisins). Stimulus hold-ers (3 cm × 5 cm × 2 cm) could be positioned to hide the food wells. These stimulus hold-ers had a 1.2 cm diameter round window in their upper surface, allowing visualization of stimuli by the subjects. The movable screen prevented the monkeys from observing the


stimuli between trials. Besides its naturalistic approach, the present experimental apparatus has other practical advantages. It is a totally portable, non-invasive and cheap methodol-ogy, which makes it suitable for use with endangered species and in a great variety of cap-tive conditions.

Procedure The experimental sessions were conducted three times a week, between 10:00 and

12:00 h, under natural daylight diffuse illumination. The training phase began after the subjects had learned how to manipulate the stimulus

holders and pick up the reward. The animals had to perform a two-choice discrimination task between a positive discriminative stimulus (SD+, the rewarded stimulus) and a negative discriminative stimulus (SD–, never rewarded). In this phase, only pairs of stimuli that were easily discriminated by dichromats were used. The subjects were rewarded when they dis-placed the stimulus holder containing the SD+. A non-correction procedure was used; i.e., following an incorrect choice the screen was lowered and another trial begun. The intertrial interval was about 15 s. A variable number of trials was made on each training session, hav-ing a total duration of 40 min. The left or right position of the SD+ was determined accord-ing to the Gellerman table of random numbers [Gellerman, 1933].

After reaching the criterion of 80% correct responses, the animals proceeded to the testing phase. In this phase, the subjects were faced with a two-choice discrimination task involving the same SD+ of the training phase and 6 different SD–. Some of these pairs of stimuli were: (1) easily discriminated by trichromats and dichromats (‘easy’ pairs); (2) easily discriminated by trichromats but difficult to discriminate by dichromats (‘difficult’ pairs); (3) difficult to discriminate by trichromats and dichromats (‘impossible’ pairs). The ‘easy’ pairs were out of the dichromats’ confusion range and represented the pairing of purples,

Fig. 1. Schematic view of the experimental apparatus mounted in front of the marmosets’home cage.


blues and reds (7.5P, 2.5PB, 5PB, 7.5PB 5B, 7.5B, 10BG) with oranges (2.5YR, 5YR, 10YR). The ‘difficult’ pairs were composed of greens (5GY, 7.5GY, 10GY) versus oranges (2.5YR, 5YR, 10YR). The ‘impossible’ pairs were constituted by pairing oranges (2.5YR, 5YR, 10YR) against oranges (2.5YR, 5YR, 10YR), making their discrimination unattain-able. As stated before, each brightness level of the SD+ was paired to each brightness level of the SD–, adding up to 16 pairs. These pairs were presented 3 times each, totalling 48 trials per experimental session. Based on these 48 trials, a percentage of correct responses was determined. After finishing the testing phase, the subjects were introduced into another train-ing phase, with a different SD+.

Statistical Analyses The binomial test was used to construct the 95% confidence limits around chance per-

formance based on the number of test trials. For 48 test trials, the upper limit was deter-mined as 65%. The performance of all subjects was compared to these confidence limits, and any performance above the upper limit was considered significant (p < 0.05).

Results

Figures 2–4 show the marmosets’ colour vision performance, based on per-centage of correct responses, when SD+ was, respectively, 2.5YR, 5YR and 10YR. On 3 occasions, 2 females (FC2 and FC3) exhibited a performance above the upper chance limit (p < 0.05) for all ‘easy’ and ‘difficult’ pairs. However, 3 subjects, 2 males (MC1 and MC2) and 1 female (FC1), showed a response indiscriminate from chance (p > 0.05) for orange versus green pairs, that is the ‘difficult’ pairs. These

Fig. 2. Colour discrimination performance in C. penicillata, with the Munsell chip 2.5YR (yellow-red) as positive discriminating stimulus (SD+). The negative discriminating stimuli(SD–) are shown on the horizontal axis: 10BG (blue-green), 5PB (purple-blue), 7.5P (purple), 7.5GY (green-yellow), 5B (blue) and 2.5YR (yellow-red). The horizontal line indicates the upper limit (65% of correct responses) of the 95% confidence interval fordiscriminative performance. * = Easy pair; ** = difficult pair; *** = impossible pair.


Fig. 3. Colour discrimination performance in C. penicillata, with the Munsell chip 5YR (yellow-red) as positive discriminating stimulus (SD+). The negative discriminating stimuli(SD–) are shown on the horizontal axis: 5B (blue), 10BG (blue-green), 5PB (purple-blue), 10GY (green-yellow), 7.5P (purple) and 5YR (yellow-red). Other conventions as in figure 2.

Fig. 4. Colour discrimination performance in C. penicillata, with the Munsell chip 10YR (yellow-red) as positive discriminating stimulus (SD+). The negative discriminating stimuli(SD–) are shown on the horizontal axis: 7.5B (blue), 2.5PB (purple-blue), 5PB (purple-blue), 5GY (green-yellow), 7.5PB (purple-blue) and 10YR (yellow-red). Other conventions as in figure 2.


findings indicate that, while FC2 and FC3 behaved like trichromats, MC1, MC2 and FC1 behaved like dichromats.

As a control for hue cues, all marmosets showed chance level performance (p > 0.05) in the ‘impossible’ pairs, when oranges were paired against oranges (fig. 2–4).

Discussion

Our data suggest that C. penicillata presents a polymorphic trichromacy, with dichromatic males and dichromatic or trichromatic females. These findings are in accordance with the hypothesis of the obligatory dichromatism in males [Mollon et al., 1984]. Studies conducted in other marmoset species [Tovée et al., 1992; Hunt et al., 1993; Caine and Mundy, 2000; Surridge and Mundy, 2002] corroborate this view.

Trichromacy has long been thought to be the result of an adaptive process in-volving the detection of targets (i.e. fruits, flowers and leaves) against a foliage background [Mollon, 1989; Lucas et al., 1998; Sumner and Mollon, 2000; Dominy and Lucas, 2001; Párraga et al., 2002]. While Dominy and Lucas [2001, 2004] claim that leaf consumption has a unique value in maintaining trichromacy in catar-rhines, Regan et al. [1998, 2001] have shown that the spectral positioning of the cone pigments found in trichromatic platyrrhine primates is well matched to the task of detecting fruits against a background of leaves. In either case, platyrrhines would be expected to show some difference in their foraging behaviour that could allow dichromats to find food through their trichromatic conspecifics [Sumner and Mollon, 2000]. Apparently, males have been found to be less exploratory and more vigilant than females, the last demonstrating priority of access to food [Box, 1997]. Mollon [1989] suggested that the heterozygous females, among all individuals in the troop, would have the task of searching for ripe fruits. This could explain the gender differences observed in foraging and feeding strategies of callitrichids [Box, 1997; Moura and Alonso, 2000].

Ancient Neotropical primates were small-bodied animals [Houle, 1999] that used to feed on fruits and insects [Kay, 1984]. Branisella boliviana (26 Ma), weighed about 760 g [Kay et al., 2002] and probably presented a polymorphic trichromacy [Heesy and Ross, 2001]. According to Kay [1984], primates at or be-low this weight do not have a significant component of leaves in their diet. This leads to the prediction that folivory has never been important during the evolution of callitrichids, and that frugivory and/or insectivory are more likely selective fac-tors maintaining trichromacy [Surridge and Mundy, 2002].

Indeed, Dominy et al. [2003] suggest that the abundance of cryptically col-oured keystone fruits, such as figs and palms in the Neotropics and Madagascar, never favoured the evolution of routine trichromacy because young leaves never became critical fallback foods. Instead, polymorphic trichromacy should represent a balance between dichromatic advantages for detecting cryptic keystone resources (e.g. fruits and insects) [Morgan et al., 1992] and trichromatic advantages for de-tecting conspicuous fruits [Mollon, 1989; Caine and Mundy, 2000; Smith et al., 2003]. In fact, callitrichids live in small family groups [Sussman and Kinzey, 1984] and forage as a team [Menzel and Juno, 1985]. Therefore, if there are complemen-


tary advantages to dichromacy and trichromacy, co-operative foraging could be responsible for the maintenance, by kin selection, of the visual polymorphism found in the New World monkeys [Tovée et al., 1992].

Recently, Callithrix has been subdivided into two separate genera [Rylands et al., 2000]. The Atlantic forest marmosets (jacchus group), more gummivorous, remained as Callithrix, while the Amazonian marmosets (argentata group), more frugivorous, were grouped into a new genus called Mico. Some representatives from different habitats, such as Callithrix jacchus (Caatinga, semi-arid thorn scrub), Callithrix geoffroyi (Atlantic forest) and Callithrix penicillata (Cerrado, bush savanna), have already had their colour vision investigated [Tovée et al., 1992; Caine and Mundy, 2000; present study]. However, the colour vision of Ama-zonian marmosets, genus Mico, has not been evaluated yet.

Yellow to orange fruits seem predominant in the diet of many Neotropical primates. Terborgh [1983] found that 62% of fruit eaten by New World monkeys belonged to the yellow/orange/red region of the spectrum. Similarly, 54% of the fruit consumed by callitrichids are in the yellow/orange/red range [Savage et al., 1987]. Therefore, to resemble the task of discriminating conspicuous fruits from the foliage background, the present study used, in the ‘difficult’ pairs, orange (SD+) versus green (SD–) stimuli. Recent studies that used stimuli in this spectral range to assess the colour capabilities of dichromatic and trichromatic platyrrhines have been successful [Caine and Mundy, 2000; Gomes et al., 2002; Pessoa et al., 2003; Smith et al., 2003].

Within the genus Callithrix, C. penicillata is among the most exudativores, fruits and insects having small participation in their diet [Rylands and Faria, 1993]. Nevertheless, a recent study reported the ingestion of 14 different species of native fruits by this marmoset [Miranda and Faria, 2001]. Combining this information with the descriptive characteristics of each fruit [Silva et al., 1994; Proença et al., 2000] we found that only 36% of those fruits had conspicuous colours (i.e. red, orange and yellow), while 64% were cryptically coloured (i.e. green 21% and black/dark purple 43%). This high proportion of black/dark purple fruits is note-worthy, especially considering that they comprise the most extensively exploited fruits by C. penicillata [Miranda and Faria, 2001]. Further experiments focusing upon the discriminative abilities of marmosets under cryptic foraging and predator detection situations are still needed.

Acknowledgments

This research was partially supported by CAPES/DAAD/PROBAL (137/02) and FI-NATEC. D.M.A.P. was a recipient of a doctoral fellowship from CNPq. We thank R.C.A. Ajuz, L.A. Guimaraes, P.Q. Cruz and R.V.L. Silva for helping to run the experiments, and Dr. R. de Oliveira for animal care and maintenance. The Animal Research Ethics Committee from the University of Brasilia approved this research protocol.


References

Arrese CA, Hart NS, Thomas N, Beazley LD, Shand J (2002). Trichromacy in Australian marsupials. Current Biology 12: 657–660.

Box HO (1997). Foraging strategies among male and female marmosets and tamarins (Callitrichidae): New perspectives in an underexplored area. Folia Primatologica 68: 296−306.

Caine NG, Mundy NI (2000). Demonstration of a foraging advantage for trichromatic marmosets (Callithrix geoffroyi) dependent on food colour. Proceedings of the Royal Society of London B 267: 439−444.

Coimbra-Filho AF (2002). Apontamentos sobre Callithrix aurita (E. Geoffroy, 1812) um sagüi pouco conhecido (Callitrichidae, Primates). In A primatologia no Brasil (Mello MT, ed.), pp 145–158. Belo Horizonte, Sociedade Brasileira de Primatologia.

Dominy NJ, Lucas PW (2001). Ecological importance of trichromatic vision to primates. Nature 410: 363−366.

Dominy NJ, Lucas PW (2004). Significance of color, calories, and climate to the visual ecology of catarrhines. American Journal of Primatology 62: 189–207.

Dominy NJ, Svenning JC, Li WH (2003). Historical contingency in the evolution of primate color vision. Journal of the Human Evolution 44: 25–45.

Garber PA (1992). Vertical clinging, small body size, and the evolution of feeding adaptations in the callitrichinae. American Journal of Physical Anthropology 88: 469–482.

Gegenfurtner KR, Kiper DC (2003). Color vision. Annual Review of Neuroscience 26: 181–206. Gellerman LW (1933). Chance orders of alternating stimuli in visual discrimination experiments. Jour-

nal of General Psychology 42: 207–208. Gomes UR, Pessoa DMA, Tomaz C, Pessoa VF (2002). Colour vision perception in the capuchin mon-

key Cebus apella: A re-evaluation of procedures using Munsell papers. Behavioral Brain Re-search 129: 153−157.

Harlow H, Bromer J (1938). A test-apparatus for monkeys. Psychological Review 19: 434−438. Heesy CP, Ross CF (2001). Evolution of activity patterns and chromatic vision in primates: Mor-

phometrics, genetics and cladistics. Journal of Human Evolution 40: 111−149. Houle A (1999). The origin of platyrrhines: An evaluation of the Antartic scenario and the floating

island model. American Journal of Physical Anthropology 109: 541–559. Hunt DM, Williams AJ, Bowmaker JK, Mollon JD (1993). Structure and evolution of the polymorphic

photopigment gene of the marmoset. Vision Research 33: 147–154. Jacobs GH (1993). The distribution and nature of colour vision among the mammals. Biological Re-

views 68: 413−471. Jacobs GH (1996). Primate photopigments and primate colour vision. Proceedings of the National

Academy of Science of the United States of America 93: 577−581. Jacobs GH (2002). Progress toward understanding the evolution of primate color vision. Evolutionary

Anthropology 1: 132–135. Jacobs GH, Deegan JF (1999). Uniformity of colour vision in Old World monkeys. Proceedings of the

Royal Society of London B 266: 2023–2028. Jacobs GH, Fenwick JC, Calderone JB, Deeb SS (1999). Human cone pigment expressed in transgenic

mice yields altered vision. Journal of Neuroscience 19: 3258−3265. Kay RF (1984). On the use of anatomical features to infer foraging behavior in extinct primates. In

Adaptations for Foraging in Nonhuman Primates (Rodman PS, Cant JGH, eds.), pp 21–53. New York, Columbia University Press.

Kay RF, Williams BA, Anaya F (2002). The adaptations of Branisella boliviana, the earliest South American monkey. In Reconstructing Behavior in the Primate Fossil Record (Plavcan JM, Kay RF, Jungers WL, van Schaik CP, eds.), pp 339–370. New York, Kluwer-Plenum.

Lacher TE, Fonseca GAB, Alves C, Magalhães-Castro B (1984). Parasitism of trees by marmosets in a central Brazilian gallery forest. Biotropica 16: 202–209.

Lucas PW, Darvell BW, Lee PKD, Yuen TDB, Choong MF (1998). Colour cues for leaf food selection by long-tailed macaques (Macaca fascicularis) with a new suggestion for the evolution of trichro-matic colour vision. Folia Primatologica 69: 139−152.

Menzel EW, Juno C (1985). Social foraging of marmoset monkeys and the question of intelligence. Philosophical Transactions of the Royal Society of London B 208: 145−158.

Miranda GHB, Faria DS (2001). Ecological aspects of black-pincelled marmoset (Callithrix penicillata) in the cerradão and dense cerrado of the Brazilian central plateau. Brazilian Journal of Biology 61: 397–404.

Mollon JD (1989). ‘Tho’she kneel’d in that place where they grew...’ The uses and origins of primate colour vision. Journal of Experimental Biology 146: 21−38.

Mollon JD, Bowmaker JK, Jacobs GH (1984). Variations of colour vision in a New World primate can be explained by polymorphism of retinal photopigments. Proceedings of the Royal Society of London B 222: 373−399.


Morgan MJ, Adam A, Mollon JD (1992). Dichromats detect colour-camouflaged objects that are not detected by trichromats. Proceedings of the Royal Society of London B 248: 291−295.

Moura ACA, Alonso C (2000). Sex and age differences in foraging and vigilance behavior of captive Saguinus midas midas (Primates: Callitrichidae). In A primatologia no Brasil (Alonso C, Lang-guth A, eds.), pp 223–238. João Pessoa, SBPr e Editora Unversitária.

Paramei GV, Bimler DL, Cavonius CR (1998). Effect of luminance on color perception of protanopes. Vision Research 38: 3397–3401.

Párraga CA, Troscianko T, Tolhurst DL (2002). Spatiochromatic properties of natural images and hu-man vision. Current Biology 12: 483–487.

Pessoa DMA, Araujo MFP, Tomaz C, Pessoa VF (2003). Colour discrimination learning in black-handed tamarin (Saguinus midas niger). Primates 44: 413–418.

Pessoa DMA, Perini ES, Carvalho LS, Tomaz C, Pessoa VF (2005). Color vision in Leontopithecus chrysomelas: A behavioral study. International Journal of Primatology 26: 143–154.

Pessoa VF, Abrahão JCH, Pacheco RA, Pereira LCM, Magalhães-Castro B, Saraiva PES (1992). Rela-tive sizes of cortical visual areas in marmosets – Functional and phylogenetic implications. Ex-perimental Brain Research 88: 459–462.

Proença C, Oliveira RS, Silva AP (2000). Flowers and Fruits of the Cerrado. Brasília, Editora Univer-sidade de Brasília.

Regan BC, Julliot C, Simmen B, Viénot F, Charles-Dominique P, Mollon JD (1998). Frugivory and colour vision in Alouatta seniculus, a trichromatic platyrrhine monkey. Vision Research 38: 3321−3327.

Regan BC, Julliot C, Simmen B, Viénot F, Charles-Dominique P, Mollon JD (2001). Fruits, foliage and the evolution of primate colour vision. Philosophical Transactions of the Royal Society of London B 356: 229−283.

Rosenberger AL (1992). Evolution of feeding niches in New World monkeys. American Journal of Physical Anthropology 88: 525–562.

Rylands AB (1989). Sympatric Brazilian callitrichids: The black tufted-ear marmoset, Callithrix kuhli, and the golden-headed lion tamarin, Leontopithecus chrysomelas. Journal of Human Evolution 18: 679–695.

Rylands AB (1996). Habitat and the evolution of social and reproductive behavior in Callitrichidae. American Journal of Primatology 38: 5–18.

Rylands AB, Faria DS (1993). Habitats, feeding ecology, and home range size in the genus Callithrix. In Marmosets and Tamarins: Systematics, Behaviour, and Ecology. (Rylands AB, ed.), pp 262–272. Oxford, Oxford Science Publications.

Rylands AB, Schneider H, Langguth A, Mittermeier RA, Groves CP, Rodríguez-Luna E (2000). An assessment of the diversity of New World primates. Neotropical Primates 8: 61−93.

Savage A, Dronzek LA, Snowdon CT (1987). Colour discrimination by the cotton-top tamarin (Saguinus oedipus oedipus) and its relation to fruit coloration. Folia Primatologica 49: 57−69.

Silva JA, Silva DB, Junqueira NTV, Andrade LRM (1994). Frutos nativos dos cerrados. Brasília, EM-BRAPA.

Smith AC, Buchanan-Smith HM, Surridge AK, Osorio D, Mundy NI (2003). The effect of colour vision status on the detection and selection of fruits by tamarins (Saguinus spp.). Journal of Experimen-tal Biology 206: 3159–3165.

Smith VC, Pokorny J (1977). Large-field trichromacy in protanopes and deuteranopes. Journal of the Optical Society of America 67: 213–220.

Sumner P, Mollon JD (2000). Catarrhine photopigments are optimised for detecting targets against a foliage background. Journal of Experimental Biology 203: 1963−1986.

Surridge AK, Mundy NI (2002). Trans-specific evolution of opsin alleles and the maintenance of trichromatic colour vision in Callitrichine primates. Molecular Ecology 11: 2157–2169.

Surridge AK, Osorio D, Mundy NI (2003). Evolution and selection of trichromatic vision in primates. Trends in Ecology and Evolution 18: 198–205.

Sussman RW, Kinzey WG (1984). The ecological role of the Callitrichidae: A review. American Jour-nal of Physical Anthropology 64: 419−449.

Tan Y, Li WH (1999). Trichromatic vision in prosimians. Nature 402: 36. Terborgh J (1983). Five New World Primates: A Study in Comparative Ecology. Princeton, Princeton

University Press. Tovée MJ, Bowmaker JK, Mollon JD (1992). The relationship between cone pigments and behavioural

sensitivity in a New World monkey (Callithrix jacchus jacchus). Vision Research 32: 867−878. Zeki S (1999). Inner Vision. Oxford, Oxford University Press.

Documents

Colour Discrimination in the Black\u0026hyphen;Tufted\u0026hyphen;Ear Marmoset (Callithrix penicillata): Ecological Implications