Effect of polymorphic colour vision for fruit detection in the spider monkey Ateles geoffroyi, and its implications for the maintenance of polymorphic colour vision in platyrrhine monkeys
1 Universidad de Costa Rica, Escuela de Biología, San Pedro, Costa
Rica
2 Centro de Investigaciones en Ecosistemas, Universidad Nacional
Autónoma de México, Apartado Postal 27-3 (Xangari), Morelia,
Michoacan, 48980 Mexico
3 School of Life Sciences, University of Sussex, Brighton BN1 9QG,
UK
* Author for correspondence (e-mail: kstoner{at}oikos.unam.mx)
Accepted 21 April 2004
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Summary |
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Key words: Costa Rica, platyrrhines, spider monkey, Ateles geoffroyi, fruit detection, colour vision, genetic polymorphism
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Introduction |
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An animal with trichromatic colour vision requires a mixture of three
primaries to match any colour, but it is probably of more practical relevance
that having two receptors with the greatest sensitivity to wavelengths above
500 nm allows animals to discriminate colours that we recognize as red, yellow
and green, and may otherwise be confused by dichromats. As fruit eaten by
primates are often yellow or red it has long been suggested that trichromacy
evolved for frugivory (Allen,
1879; Polyak,
1957
; Regan et al.,
2001
). Only fairly recently has this suggestion been tested, in
part prompted by the discovery of M/L opsin polymorphism in New World monkeys.
Modeling studies that estimate receptor responses to fruit and leaf spectra,
either for market fruits (Osorio and
Vorobyev, 1996
) or for food eaten by wild trichromatic primates
(Regan et al., 1998
; Sumner
and Mollon
2000a
,b
)
lend support to Allen's proposal, as do two recent experimental studies on
captive animals. These experiments, with omnivorous platyrrhines, showed that
trichromatic individuals of marmosets (Callithrix geoffroyi) and
tamarins (Saguinus spp.) were better than dichromatic individuals at
finding food objects with orange hues at >5m distance
(Caine and Mundy, 2000
), where
the colour had been chosen to match natural food colours
(Smith et al., 2003
).
If trichromatic colour vision is advantageous for finding fruit, how can we
explain why most New World monkeys are polymorphic? Mollon et al.
(1984) put forward four
potential explanations: (1) group selection; (2) frequency dependent
selection; (3) spatial heterogeneity of environment; and (4) heterozygote
advantage. Owing to its occurrence in many species with long independent
evolutionary histories, it is virtually certain that the M/L polymorphism is
stable (Surridge and Mundy,
2002
; Surridge et al.,
2003
) and therefore the fitness of the various alleles must be
frequency-dependent (i.e. alleles are selectively favoured when rare). This
means that of the four original hypotheses, the most plausible explanation is
either (hypothesis 2) frequency dependent selection for the
phenotypes, or (hypothesis 4) heterozygote advantage
(Surridge et al., 2003
).
Frequency dependent selection of the various colour vision phenotypes might
arise because different phenotypes can exploit different types of food,
thereby reducing competition. However, the actual variation in foraging
abilities of the different colour vision phenotypes is unknown. Alternatively,
polymorphism might be maintained simply by the advantage of trichromacy over
dichromacy (heterosis or overdominance;
Surridge and Mundy, 2002
). The
main difficulty with this explanation is to account for why most New World
primates have not benefited from the M/L gene duplication that has occurred
independently in both howling monkeys (Alouatta sp.) and Old World
primates (Catarrhines). Amongst these routinely trichromatic groups there is
very little polymorphism, with all individuals having a 535 nm M-pigment and a
562 nm L-pigment.
To understand the maintenance of M/L polymorphism in platyrrhines, it is
necessary not only to determine the advantage of trichromacy over dichromacy
in fruit detection, but also the performance of different phenotypes in
detecting different kinds of fruit. This question is especially pertinent to
spider monkeys, Ateles sp., which are highly frugivorous, with
different species spending between 57% and 77% of their total feeding time on
fruit (Cant, 1977;
Chapman, 1987
;
Symington, 1988
). They prefer
ripe to unripe fruit, or to any other food
(Symington, 1988
). Laboratory
tests on two individuals of Ateles geoffroyi suggest that this
species has more acute colour discrimination than most platyrrhines
(Blakeslee and Jacobs,
1982
).
This study evaluates different types of spider monkey colour vision by
modelling their performance in detecting fruit against a background of leaves.
The only published study (Jacobs and
Deegan, 2001) of spider monkey opsin genetics reported only 562 nm
and 550 nm alleles, but we believe that our study population had three M/L
alleles, giving pigments with sensitivity maxima at 535, 550 and 562 nm (W.-H.
Li, personal communication). The model here is similar to that used previously
by Osorio and Vorobyev (1996
).
It assumes that the contrast sensitivity of the animals is independent of
stimulus intensity (i.e. Weber's law holds), as is likely to be the case in
bright viewing conditions (Rovamo et al.,
2001
). We consider that a fruit is detectable if its difference
from the leaf background exceeds a specific threshold (1 just noticeable
difference; 1 jnd). This threshold is based on data from human laboratory
studies (Wyszecki and Stiles,
1982
; Vorobyev and Osorio,
1998
).
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Materials and methods |
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Foraging data collection
Foraging by one troop of Ateles geoffroyi containing 30
individuals was studied from May 1999 to May 2000. Data were collected 2 days
per week from 6:00 h to 18:00 h using 2 min continual focal animal
observations to obtain information on fruit consumption
(Altmann, 1974). All
individuals were identified to sex and age-class; focal animals were randomly
changed after each 2 min observation. Only data from adults were included in
the analysis because juveniles were infrequently observed.
Fruits were considered consumed when monkeys bit into the fruit more than twice, swallowing either the pulp or the entire fruit. Samples of food fruits were mostly collected when monkeys accidentally dropped fragments. However, when the entire fruit was consumed, samples were collected from fresh fruits that fell off the branch while the monkey foraged. When fruit samples could not be obtained while collecting foraging data, we returned the following day and used a telescopic tree pruner to collect samples from the same part of the same tree. To describe the background colours against which fruits were seen, we collected two mature leaves surrounding the fruits where monkeys were feeding. Only the upper surfaces of these leaves, those which we presumed the monkeys to be observing, were recorded.
Colour measurement
We recorded the reflectance spectra of consumed fruits and background
leaves in the field using a portable field kit
(Lucas et al., 2001) that
incorporates a fibre optic spectrometer (S2000, Ocean Optics, Dunedin, FL,
USA) connected to a laptop portable computer via a PCMCIA card
(DAQCard1200, National Instruments, Austin, TX, USA). Samples were placed in a
purpose-built chamber connected to the spectrometer with illumination provided
by a 12 V 3100k tungsten halogen lamp (LS-1, Ocean Optics, Palo Alto, CA,
USA). Spectra were referenced to a standard flat surface of barium sulphate
powder.
Estimating performance of phenotypes
To compare different visual phenotypes we use a model that accurately
describes colour thresholds of humans and other animals. The model assumes
that these thresholds are set by photoreceptor noise in chromatic (i.e. colour
opponent) mechanisms, and that the achromatic (brightness) signal is not used
(Vorobyev and Osorio, 1998;
Kelber et al., 2003
).
For an eye viewing a stimulus, the quantum catch of a photoreceptor i,
Qi, is given by:
![]() | (1) |
When Qi is high, the contrast threshold can be assumed
to be independent of intensity. Then noise levels are given by:
![]() | (2) |
![]() | (3) |
![]() | (4) |
![]() | (5) |
Evaluation of chromaticity differences
The discriminability of any two spectra is predicted by the above model in
terms of `just noticeable difference' units (or jnds), where 1 jnd is the
minimum threshold at which the performance of an observer can detect a target
against a background. When the difference between these two stimuli exceeds 1
jnd the target is detectable, while one falling below this threshold is not.
This model offers a clear criterion for the performance of colour vision close
to threshold. As thresholds in field conditions may not match those in the
laboratory, for example due to variations in stimulus size
(Rovamo et al., 2001;
Parraga et al., 2001
), we take
account of suprathreshold performance by noting when differences in
estimated detectability between two phenotypes exceed 1 jnd
(Table 1).
|
We assumed the following Weber fractions: L=0.02;
M=0.02 and
S=0.08, which are close to
measured psychophysical thresholds for humans
(Wyszecki and Stiles, 1982
;
Osorio and Vorobyev, 1996
). We
assume that the total number of M/L cones is fixed in dichromats and
trichromats, so that for the dichromat M/L mechanism
L=0.02/(2)0.5. Fruit and leaf spectra of a given
species of plant obviously vary, in part due to variation in solar exposure of
mature leaves (Dominy et al.,
2003
). Given that fruit are relatively rare amongst leaves, a
reasonable estimate of visibility is the minimum difference between a
fruit spectrum and all leaf spectra. For this reason, whenever possible, we
measured the spectra for more than one fruit sample and the performance for a
given species was then calculated as the median of these minima. A standard
illuminant of sunlight spectrum recorded from a large forest gap was used;
this illuminant closely approximates D65 (figured in
Lucas et al., 2003
). Although
illumination spectra vary substantially in the forest we do not take account
of the effects of such variation, as these are likely to be negligible for the
task modelled here (Osorio and Vorobyev,
1996
).
Calculation of yellow-blue and red-green colour signals
Where a description of colour of an object is needed and not just a colour
difference, it is convenient to assume that colour is coded by
blueyellow (BY) and redgreen (RG) opponent
mechanisms (Regan et al.,
1998). The responses of the L (562 nm), M (535 nm) and S (430 nm)
cones, relative to an achromatic standard, are respectively given by the
quantum catches of the receptor QL, QM
and QS:
![]() | (6) |
Using these parameters the colour of a fruit can be defined as either bluer
or yellower, and either redder or greener than the leaf background
(Regan et al., 1998;
Lucas et al., 2004
). We used
MannWhitney tests to: (a) determine if the difference between the
colour of the fruit species and the background was significantly different
between the yellowblue or redgreen channels, (b) to determine if
consumed fruits signal more at the yellow or blue section of the
yellowblue channel, and (c) to determine if consumed fruits signal more
at the red or green section of the redgreen channel.
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Results |
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The difference between fruit colour and background was significantly different for blueyellow and redgreen signals (MannWhitney test, U=418.5, P=0.04, d.f.=1), with greater differences between fruit and background being observed for the blueyellow signal (Fig. 1). Differences in blueyellowness were distributed approximately equally on both sides of the mean background chromaticity with no tendency for a blue or yellow bias (MannWhitney test, U=189, P=0.38, d.f.=1). For the redgreen signal, all but two species were redder than the background (U=0, P=0.02, d.f.=1).
Fruit detection performance by phenotype
We have predicted that nearly all the fruit species could be detected by
all six phenotypes, in that the fruit differed from leaves by at least 1 jnd.
It is also interesting to ask if performance differed between
phenotypes by at least 1 jnd (Table
1). The performance of the regular trichromat was better than the
three dichromatic phenotypes (Table
1A) as well as the two anomalous trichromats
(Table 1B). The two anomalous
trichromats were very similar in performance; for only 15% of the species did
colour signals for the 535/550 phenotype exceed those for the 550/562
phenotype by >1 jnd (Table
1B). The anomalous trichromats did not perform better than the
regular trichromat for any of the species
(Table 1B). Within the
dichromatic phenotypes, the 562 nm allele performed better than 535 nm in 33%
of the species and better than 550 nm in 25% of species.
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Discussion |
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Our results support the hypothesis that trichromacy is advantageous for
frugivory in platyrrhine monkeys. Phenotypes with the 535 nm and 562 nm
alleles are best, and these are the genes found in routinely trichromatic Old
World and howling monkeys. Furthermore, our observations of spider monkey
behaviour provide some support for the notion that social interactions are
important in foraging for this species. Foraging subgroups of the study
population in our study site most frequently consisted of 23 adult
females with their associated offspring. Although all male subgroups were
common, as has been described by other studies
(Symington, 1988;
Chapman, 1990
), these subgroups
frequently met with subgroups containing females throughout the day. Although
agonistic interactions occurred more often in feeding trees than under other
circumstances and usually resulted in low-ranking females being pushed out of
feedings trees, the entire subgroup benefited from the discovery of
the feeding tree, as all individuals eventually fed in the tree. In such
cases, fruit foraging in spider monkeys does not appear to be an individual
task but rather more of a group task. Under these conditions, the heterozygote
advantage of trichromacy may be the most plausible explanation for maintaining
the X-polymorphism in A. geoffroyi. Nevertheless, more studies need
to evaluate social foraging behaviour and the performance of different
phenotypes of other New World monkeys to determine if this is a global
explanation for this phenomena or more specific to A. geoffroyi.
According to our model, dichromacy appears to be adequate for the detection
of most of the fruit species in the diet of A. geoffroyi (3738
species of the 39 consumed) including the five most important species in the
fruit diet of this primate. Interestingly, Snodderly
(1979) put forward an opposite
suggestion (prior to the discovery of M/L polymorphism) that trichromacy would
be of little benefit to platyrrhine monkeys because most of the fruits they
consume are cryptically coloured and hence could not be located by any
type of colour vision. In practice, whilst there are a number of cryptic (i.e.
green) fruit, Snodderly's suggestion does not seem to hold for many species
eaten by primates, and overall our results agree with previous studies that
have shown dichromacy to be useful in fruit detection in studies with Old
World monkeys (Dominy and Lucas,
2001
; Sumner and Mollon,
2000a
).
Several conclusions can be made from our study. First, when fruit colour is
considered separate from other fruit traits, it can play an important role in
fruit selection by platyrrhine monkeys. Since dichromatic phenotypes were able
to detect 9497% of all the fruit species that were detected by
trichromatic phenotypes, including the five most important species in their
diet, the performance of dichromats in detecting fruit is not as poor as
previously suggested by Jacobs
(1998). Second, although
trichromacy always has an advantage for fruit detection at long distances for
the individuals with this trait, factors such as social interactions and
sub-group composition while foraging may also provide an advantage for other
individuals in the group that are not trichromatic. Thus in the population of
A. geoffroyi studied, the polymorphic alleles for colour vision may
be maintained due to a heterozygote advantage. However, our conclusions should
be taken with caution, since we lack information on the genotype of the
population studied, and our model does not include the effect of illumination
intensity on performance.
Three issues need to be clarified to better understand the advantage of
trichromatic colour vision for frugivory, and hence the evolution of colour
vision in platyrrhine primates. First, the actual frequencies of alleles in
natural populations need to be determined. Second, the antiquity of opsin
alleles in Atelid monkeys (Surridge and
Mundy, 2002) must be defined. And third, experimental evidence
that primates actually use colour as a cue to select fruits needs to be
demonstrated. Finally future studies should incorporate these elements, along
with social relationships among individuals and the actual fitness increase of
trichromats (Surridge et al.,
2003
), in order to understand the evolution of trichromacy in
primates.
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Acknowledgments |
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