The effect of colour vision status on the detection and selection of fruits by tamarins (Saguinus spp.)
1 Scottish Primate Research Group, Department of Psychology, University of
Stirling, Stirling FK9 4LA, UK
2 School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ,
UK
3 Biological Sciences, University of Sussex, Brighton BN1 9QG, UK
4 Department of Zoology, Downing St, University of Cambridge, Cambridge CB2
3EJ, UK
* Author for correspondence (e-mail: a.c.smith{at}stir.ac.uk)
Accepted 10 June 2003
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Summary |
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Key words: polymorphic colour vision, trichromacy, dichromacy, sex differences, individual differences, tamarin, Saguinus
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Introduction |
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Within placental mammals, trichromacy is unique amongst primates: all other
species so far examined are either dichromats or monochromats
(Jacobs, 1993;
Ahnelt and Kolb, 2000
;
Arrese et al., 2002
). It has
been hypothesized that the evolution of trichromatic colour vision by the
majority of primate species is a direct result of the chromatic signals
produced by fruits (Regan et al.,
2001
) or leaves (Dominy and
Lucas, 2001
). For an animal to feed on fruits it has first to
detect them against a background of leaves. Vision and olfaction are probably
the principal senses employed. Theoretically, trichromacy has been predicted
to be more efficient than dichromacy when detecting and identifying fruits
against a leaf background (Osorio and
Vorobyev, 1996
; Sumner and
Mollon, 2000a
; Regan et al.,
2001
). In addition to detecting fruiting trees, an animal has to
select ripe from unripe fruits. Physical and chemical defences may protect
fruits until their seeds are ready to be dispersed. The ripening process is
often characterized by a colour change that can give a clear visual signal to
potential dispersers of the increased palatability of the ripe fruits
(Regan et al., 2001
).
Theoretically, trichromats have also been predicted to be capable of
distinguishing a greater number of ripe from unripe fruit species
(Sumner and Mollon, 2000b
;
Regan et al., 2001
).
Despite its theoretical advantages, trichromacy is not uniform within the
primates. Whilst all catarrhines so far studied are trichromatic, all
platyrrhines, with the two exceptions of howler (Alouatta spp.
uniformly trichromatic; Jacobs et
al., 1996a) and night monkeys (Aotus spp.
uniformly monochromatic; Jacobs et al.,
1996b
; Jacobs,
1984
; Mollon et al.,
1984
), and some strepsirhines
(Tan and Li, 1999
;
Jacobs et al., 2002
) have a
polymorphic colour vision system. All males and homozygous females are
dichromats, whilst heterozygous females are trichromats. In platyrrhines, two
loci code for the visual pigment proteins or opsins. The first, an autosomal
locus, has a single allele that codes for the short wavelength (S) opsin and
is common to all individuals. The second, on the X chromosome, codes for
opsins within the long to medium wavelength (LM) range. A single X-linked
locus model, with three alleles, explains the visual polymorphism observed in
callitrichids (Mollon et al.,
1984
).
For non-human species it is necessary to take account of the animal's perceptual abilities. Thus, we should not relate our verbal classification of colours to colour discriminability or memorability for another species; even one with the same set of photopigments. A good starting point for understanding how other species might discriminate colours is to measure spectral stimuli and estimate the responses of their photoreceptors (Table 1).
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The perceptual capabilities of various primate visual systems have been
modelled to examine the potential advantages of trichromacy in detecting ripe
fruits (e.g. Osorio and Vorobyev,
1996; Sumner and Mollon,
2000a
,b
;
Regan et al., 2001
) or flush
leaves (Dominy and Lucas,
2001
). The most pertinent stimuli for such modelling are those
actually seen by the visual system of the primate in question in the wild.
However, these models make (varying) assumptions about how photoreceptor
signals are used to make behavioural decisions (e.g.
Vorobyev and Osorio, 1998
).
For any given perceptual task we cannot be sure that model assumptions will
hold. To examine whether an actual foraging advantage is conferred by
trichromacy, the relative performance of actual subjects must be measured. For
example, Caine and Mundy (2000
)
used artificially coloured food to show a trichromatic advantage for
Geoffroy's marmosets (Callithrix geoffroyi) in a foraging task.
Whilst modelling and behavioural experiments imply that trichromacy is advantageous, this has yet to be demonstrated for a colour discrimination task that closely resembles that faced by primates foraging in their natural habitat. This is the goal of the present study. The relative efficiency of di- and trichromacy for tamarins (Saguinus spp.) is evaluated through an experimental protocol utilising captive monkeys and stimuli recreated from the reflectance spectra of actual fruits eaten (and their associated leaves) by wild tamarins in Peru and presented in a dappled naturalistic leaf canopy.
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Materials and methods |
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Data collection and analysis
All observed instances of fruit feeding were recorded. From these data, the
number of `tamarin feeding minutes' was calculated (where one `tamarin feeding
minute' equals one tamarin feeding for 1 min) and divided by the number of
tamarins of the given species to account for differences in group size between
groups, and species, and over the course of the study. Furthermore, each
month's data were weighted equally to account for slight differences in the
number of observation days.
Colour measurement
Colour measurements were taken using a portable S2000 spectrometer, HL2000
halogen light source (both Ocean Optics, Dunedin, FL, USA) and Satellite
4030CDT laptop computer (Toshiba) running SpectraWin 4.1 software (Top Sensor
Systems, Eerbeek, The Netherlands). Reflectance spectra from a minimum of
three fruits and three associated mature leaves were recorded for each species
eaten. Where possible, spectra were recorded from parts of fruits discarded by
tamarins as they fed and taken from both the upper and lower surfaces of leaf
samples. Spectra were recorded on the day that the samples were collected.
Colour modelling
We estimated the responses of the tamarin's photoreceptors, and hence
colour signals to spectral stimuli, as follows. We derived tamarin
photoreceptor spectral sensitivities in vivo by fitting a standard
exponential model of rhodopsin absorption
(Stavenga et al., 1993) to
spectral sensitivity maxima measured for common marmoset (Callithrix
jacchus) cones with sensitivity maxima at 425 nm, 543 nm, 555 nm and 562
nm (Williams et al., 1992
),
which are close to those for Saguinus
(Jacobs et al., 1987
) assuming
a maximum optical density of 0.4. Spectral absorption by the ocular media was
also based on the common marmoset
(Tovée et al., 1992
).
Recent work (Kawamura et al.,
2001
) lowers the estimated sensitivity maximum of the common
marmoset 543 nm receptor to 539 nm; this difference is of negligible
significance for the design and interpretation of our study.
Spectral stimuli reaching the eye depend upon the reflectance and
illumination spectra. Reflectance was measured as described above, and the
illumination spectrum was natural sunlight measured by a spectroradiometer
calibrated with a known standard (LS1-cal; Ocean Optics). For an eye viewing
the surface of an object, the (relative) quantum catch of the receptor
i (Qi) is given by the following
expression:
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Results |
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The fruits and leaves of A. fluminum occupy roughly mid positions
on the L/(L+M) axis (the redgreen parameter available only to
trichromats) of all the species sampled. Of the ripe fruits sampled, those of
A. fluminum have a value of 0.5474±0.0052 (N=12
fruits), from a range spanning 0.50320.5914 (N=137 species),
whereas the leaves of A. fluminum have a value of
0.5009±0.0021 (N=9 leaves), from a range of
0.49570.5147 (N=154 species). Their chromaticity is similar to
that of other fruits eaten by tamarins and also by other primates
(Sumner and Mollon, 2000b;
Regan et al., 2001
).
Captive experiment
Animals and housing
Eight captive adult saddleback (S. fuscicollis weddelli Deville
1849) and six red-bellied tamarins (S. labiatus labiatus Geoffroy in
Humboldt 1812) held at the Belfast Zoological Gardens were observed (by
A.C.S.) in the experiment. The numbers of each species are given for each sex
and visual phenotype in Table
1. Effort was made to balance sex and visual status across species
from the animals available.
The monkeys were housed in standard indoor/outdoor enclosures off-exhibit. Testing took place in the outside enclosures (1.95 mx1.55 mx3.50 m). Each was furnished with a network of approximately eight branches (5 cm to >10 cm diameter), with the three branches closest to the test apparatus placed in the same configuration. The monkeys were accustomed to being held individually in the outside enclosures.
Genotyping
Visual status was determined genetically (by A.K.S.), by amplification and
sequencing of the X-linked opsin gene. Tamarin opsin alleles can be defined by
four amino acid substitutions at positions 180 in exon 3, 229 and 233 in exon
4 and 285 in exon 5, which are important for spectral tuning
(Shyue et al., 1998). DNA was
extracted from plucked hair samples from each individual tamarin using a
QIAamp DNA mini-kit (Qiagen, Crawley, UK). PCR and sequence analysis of exons
3, 4 and 5 were performed as previously described
(Surridge and Mundy, 2002
).
Genotypes were assigned according to the combined sequence of the four
important amino acids in each of the exons mentioned above. These are as
follows for each of the three opsin alleles: 543 nm=Ala, Ile, Ser, Ala; 556
nm=Ala, Phe, Ser, Thr; 563 nm=Ser, Phe, Gly, Thr. Trichromatic females were
identified by the presence of heterozygous sites in the DNA sequence at these
important positions.
Test apparatus
The apparatus consisted of two rigid, wire grid panels. One was covered
with laminated paper leaves (leaf background) and the other was unadorned (no
background). The leaves, in the oval shape of A. fluminum, ranged
from 70 mmx50 mm to 150 mmx115 mm. They were arranged to form a
naturalistic canopy, giving dappled lighting from the incident daylight. The
randomly varying degrees of illumination from the dappled light ensured that
the task could not be solved by brightness cues of the targets alone.
Twenty-one fruit bases, made from 1.5 mm card, were fixed at regular intervals
as per Fig. 3. Each was covered
with a lid, also made from 1.5 mm card that overhung and covered its sides.
The lids were covered in one of three colours of paper corresponding to
unripe, mid-ripe and ripe A. fluminum fruit. Ripe fruits contained
0.5 g fudge, mid-ripe contained 0.25 g fudge and unripe fruits contained no
reward. The pattern of the fruit locations was varied systematically.
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The leaves were made from a commercially available green paper, the
reflectance spectrum of which roughly matched that of real A.
fluminum leaves, although overall the colour was somewhat brighter than
the real leaves (Table
2;
Fig. 4). Fruit lid colours were
calculated to differ in chromaticity from the model leaves in the same way
that natural fruits differ from natural leaves
(Fig. 1). This design, with
dappled lighting, means that as a test of colour vision the experimental task
closely resembles the task faced in natural foraging. We modelled ripe,
mid-ripe and unripe A. fluminum fruit
(Table
2
). Colours were
made in Adobe Photoshop and printed using an Epson Color 580 inkjet
printer.
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Protocol
Tamarins were tested individually in their outside enclosures. There were
two conditions: condition 1, where 21 fruits, seven of each of three colours,
were presented against no background (the plain wire mesh of the guide frame
and cage wall), and condition 2, where the same fruits were presented against
a leaf background (Fig. 4).
Each tamarin received training trials until it had successfully located and
taken six fruits. These trials were performed as for condition 2. The
experiment was split into two phases: phase 1 was three trials of condition 1,
and phase 2 was three trials of condition 2.
Trials were terminated either after the tamarin had taken all 21 fruits or after 15 min, whichever was sooner. During each trial, the time and colour of the fruit the tamarin took was continuously recorded using a hand-held computer running the Observer TM package (Tracksys Ltd., Nottingham, UK). General linear models run through SPSS were used for statistical comparisons.
Results
Trichromats required significantly fewer training trials than their
dichromatic counterparts (1.83±1.33 vs 4.60±2.88,
respectively: F1,10=9.40, P<0.05) to reach the
criterion of six fruits taken. Neither species (saddleback, 2.38±1.60;
redbellied, 4.75±3.20: F1,10=1.29,
P>0.05) nor sex (male, 3.17±2.64; female, 3.80±2.90:
F1,10=4.52, P>0.05) had a significant effect
on number of trials to criterion, nor were the interactions of species and
vision (F1,10=0.97, P>0.05) and species and
sex (F1,10=0.01, P>0.05) significant.
To examine the efficiency with which fruits were selected, the number of ripe fruits within the first six fruits taken was calculated. When the fruits were presented against both the no background and the leaf background, trichromats took significantly more ripe fruits than did dichromats (Table 3). There were no other significant effects.
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Whether the fruits were presented against a leaf background or not had no significant effect on the number of ripe fruits within the first six fruits taken (no background 2.70±0.71; leaf background 2.48±0.82: F1,14=1.41, P>0.05). There was no interaction of visual status and background (F1,14=0.001, P>0.05) nor was there a difference between dichromats and trichromats in the total number of ripe fruits taken by the end of each trial, either when presented against no background (dichromat, 6.30±0.66; trichromat, 6.33±0.73: F1,14=0.009, P>0.05) or a leaf background (dichromat, 5.43±1.29; trichromat, 6.05±0.53: F1,14=1.25, P>0.05).
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Discussion |
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The three alleles of the single-locus model give three trichromat phenotypes and three dichromat phenotypes. The spectral tuning of the opsins of each phenotype may render them each more or less advantageous under different photic conditions. Even at a given time of day there are vast differences in illumination within a rain forest. It would repay investigation to examine the actual foraging efficiencies of the different phenotypes using real-world stimuli under a variety of naturalistic lighting conditions. Similarly, it would have been informative to examine differences in the relative performance of each of the three dichromatic and three trichromatic phenotypes, but distribution of the phenotypes of the available animals did not permit this. Indeed, all of the trichromats were 423 nm, 543 nm, 563 nm, and the small sample size did not permit examination of differences between the two dichromat phenotypes in the study, namely 423 nm, 563 nm and 423 nm, 543 nm.
Although we have found that trichromacy is advantageous for detection and
selection of ripe fruit (at least for the phenotypes present in our study),
this does not give a complete picture of the likely costs and benefits of
colour vision. Nor does this result demonstrate that trichromacy originally
evolved for foraging. For example, trichromacy has been suggested as being
more efficient for detecting yellow predators against a green leafy background
(Coss and Ramakrishnan, 2000).
Examples might include the yellowish jaguar (Panthera onca), ocelot
(Leopardus pardalis), margay (L. wiedii) and oncilla (L.
tigrina), all of which live in the Neotropics. Dichromacy, however, may
be advantageous in breaking camouflage
(Morgan et al., 1992
). This is
relevant not only for detection of predators but also for the detection of
insect and other prey items that are taken by many primate species. However, a
recent study failed to find any evidence of a dichromat advantage in terms of
the number of prey captured by wild and captive tamarins (H. M.
Buchanan-Smith, A. C. Smith, A. K. Surridge, M. J. Prescott, D. Osorio and N.
I. Mundy, manuscript in preparation).
The detection and discrimination of fruits is a complex task. Fruits must
be distinguished from leaves, edible fruits must be discriminated from
inedible or toxic fruits, and ripe fruits must be typically picked over unripe
fruits. Colouration may aid in all of these tasks; indeed, as this study has
shown, primate trichromacy is advantageous in the efficient selection of ripe
fruits from an array of unripe, mid-ripe and ripe fruits. However, there are
many subtle factors other than colour per se that can influence the
choice of fruits by wild primates. As Savage et al.
(1987) point out,
discrimination may be most acute for those foods that are rarely consumed yet
are an essential source of one or more nutrients.
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Acknowledgments |
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