Comparative use of color vision for frugivory by sympatric species of platyrrhines

Ateles spp. and Alouatta spp. are often sympatric, and although they are mainly frugivorous and folivorous, respectively, they consume some of the same fruit species. However, they differ in terms of color vision, which is thought to be important for fruit detection. Alouatta spp. have routine trichromatic color vision, while Ateles spp. presents the classic polymorphism of platyrrhines: heterozygous females have trichromatic color vision, and males and homozygous females have dichromatic vision. Given these perceptual differences, one might expect Alouatta spp. to consume more reddish fruits than Ateles spp., since trichromats have an advantage for detecting fruits of that hue. Furthermore, since Ateles spp. have up to six different color vision phenotypes, as do most other platyrrhines, they might be expected to include fruits with a wider variety of hues in their diet than Alouatta spp. To test these hypotheses we studied the fruit foraging behavior of sympatric Alouatta palliata and Ateles geoffroyi in Costa Rica, and modeled the detectability of fruit via the various color vision phenotypes in these primates. We found little similarity in fruit diet between these two species (Morisita = 0.086). Furthermore, despite its polymorphism, A. geoffroyi consumed more reddish fruits than A. palliata, which consumed more greenish fruits. Our modeling results suggest that most fruit species included in the diet of A. geoffroyi can be discriminated by most color vision phenotypes present in the population. These findings show that the effect of polymorphism in platyrrhines on fruit detection may not be a disadvantage for frugivory. We suggest that routine trichromacy may be advantageous for other foraging tasks, such as feeding on young leaves.     

Sugar concentration of fruits and their detection via color in the Central American spider monkey (Ateles geoffroyi)

Although most arguments explaining the predominance of polymorphic color vision in platyrrhine monkeys are linked to the advantage of trichromacy over dichromacy for foraging for ripe fruits, little information exists on the relationship between nutritional reward and performance in fruit detection with different types of color vision. The principal reward of most fruits is sugar, and thus it seems logical to investigate whether fruit coloration provides a long-distance sensory cue to primates that correlates with sugar content. Here we test the hypothesis that fruit detection performance via trichromatic color vision phenotypes provides better information regarding sugar concentration than dichromatic phenotypes (i.e., is a color vision phenotype with sufficient red-green (RG) differentiation necessary to "reveal" the concentration of major sugars in fruits?). Accordingly, we studied the fruit foraging behavior of Ateles geoffroyi by measuring both the reflectance spectra and the concentrations of major sugars in the consumed fruits. We modeled detection performance with different color phenotypes. Our results provide some support for the hypothesis. The yellow-blue (YB) color signal, which is the only one available to dichromats, was not significantly related to sugar concentration. The RG color vision signal, which is present only in trichromats, was significantly correlated with sugar content, but only when the latter was defined by glucose. There was in fact a consistent negative relationship between fruit detection performance and sucrose concentration, although this was not significant for the 430 nm and 550 nm phenotypes. The regular trichromatic phenotypes (430 nm, 533 nm, and 565 nm) showed higher correlations between fruit performance and glucose concentration than the other two trichromatic phenotypes. Our study documents a trichromatic foraging advantage in terms of fruit quality, and suggests that trichromatic color vision is advantageous over dichromatic color vision for detecting sugar-rich fruits.     

Evolution and function of routine trichromatic vision in primates

Evolution of the red-green visual subsystem in trichromatic primates has been linked to foraging advantages, namely the detection of either ripe fruits or young leaves amid mature foliage. We tested competing hypotheses globally for eight primate taxa: five with routine trichromatic vision, three without. Routinely trichromatic species ingested leaves that were "red shifted" compared to background foliage more frequently than species lacking this trait. Observed choices were not the reddest possible, suggesting a preference for optimal nutritive gain. There were no similar differences for fruits although red-greenness may sometimes be important in close-range fruit selection. These results suggest that routine trichromacy evolved in a context in which leaf consumption was critical.     

Howler monkey foraging ecology suggests convergent evolution of routine trichromacy as an adaptation for folivory

Primates possess remarkably variable color vision, and the ecological and social factors shaping this variation remain heavily debated. Here, we test whether central tenants of the folivory hypothesis of routine trichromacy hold for the foraging ecology of howler monkeys. Howler monkeys (genus Alouatta) and paleotropical primates (Parvorder: Catarrhini) have independently acquired routine trichromacy through fixation of distinct mid‐ to long‐wavelength‐sensitive (M/LWS) opsin genes on the X‐chromosome. The presence of routine trichromacy in howlers, while other diurnal neotropical monkeys (Platyrrhini) possess polymorphic trichromacy, is poorly understood. A selective force proposed to explain the evolution of routine trichromacy in catarrhines—reliance on young, red leaves—has received scant attention in howlers, a gap we fill in this study. We recorded diet, sequenced M/LWS opsin genes in four social groups of Alouatta palliata, and conducted colorimetric analysis of leaves consumed in Sector Santa Rosa, Costa Rica. For a majority of food species, including Ficus trees, an important resource year‐round, young leaves were more chromatically conspicuous from mature leaves to trichromatic than to hypothetical dichromatic phenotypes. We found that 18% of opsin genes were MWS/LWS hybrids; when combined with previous research, the incidence of hybrid M/LWS opsins in this species is 13%. In visual models of food discrimination ability, the hybrid trichromatic phenotype performed slightly poorer than normal trichromacy, but substantially better than dichromacy. Our results provide support for the folivory hypothesis of routine trichromacy. Similar ecological pressures, that is, the search for young, reddish leaves, may have driven the independent evolution of routine trichromacy in primates on separate continents. We discuss our results in the context of balancing selection acting on New World monkey opsin genes and hypothesize that howlers experience stronger selection against dichromatic phenotypes than other sympatric species, which rely more heavily on cryptic foods.     

Fig Foraging by Dichromatic and Trichromatic <Emphasis Type="Italic">Cebus capucinus</Emphasis> in a Tropical Dry Forest

Figs are important resources for frugivores, and Ficus is an ideal taxon for evaluating patterns of primate foraging related to food color. Ficus spp. can be classified as conspicuous (color change from greenish to reddish during ripening) or cryptic (green throughout ripening). To investigate the effect on foraging of color vision phenotype variation for these 2 types of figs, we conducted a 20-mo study on 4 groups of white-faced capuchins (Cebus capucinus) in the Santa Rosa Sector of the ACG, Costa Rica between May 2004 and September 2008. We genotyped all individuals and collected behavioral data on feeding rates, acceptance indices, and foraging sequences. We found a significant effect of fig type; feeding rates and acceptance indices were higher for conspicuous figs than for cryptic figs, and subjects sniffed cryptic figs more often than conspicuous figs. We also found that dichromats sniffed more figs and had longer foraging sequences than trichromats, especially for cryptic figs. Among 6 subtypes of dichromats and trichromats, monkeys possessing the trichromat phenotype with the most spectrally separated L-M opsin alleles showed the highest acceptance index for conspicuous figs, though there were no differences in feeding rates among phenotypes. We conclude: 1) conspicuous figs are visually salient not only for trichromats but also for dichromats, 2) olfaction is important for evaluating edibility of cryptic figs, and 3) the reliance on olfaction for selecting fruit is greater in dichromats. These results indicate divergent foraging strategies among color vision phenotypes for assessing food items.     

Historical contingency in the evolution of primate color vision

Primates are unique among eutherian mammals for possessing three types of retinal cone. Curiously, catarrhines, platyrrhines, and strepsirhines share this anatomy to different extents, and no hypothesis has hitherto accounted for this variability. Here we propose that the historical biogeography of figs and arborescent palms accounts for the global variation in primate color vision. Specifically, we suggest that primates invaded Paleogene forests characterized by figs and palms, the fruits of which played a keystone function. Primates not only relied on such resources, but also provided high-quality seed dispersal. In turn, figs and palms lost or simply did not evolve conspicuous coloration, as this conferred little advantage for attracting mammals. We suggest that the abundance and coloration of figs and palms offered a selective advantage to foraging groups with mixed capabilities for chromatic distinction. Climatic cooling at the end of the Eocene and into the Neogene resulted in widespread regional extinction or decimation of palms and (probably) figs. In regions where figs and palms became scarce, we suggest primates evolved routine trichromatic vision in order to exploit proteinaceous young leaves as a replacement resource. A survey of the hue and biogeography of extant figs and palms provides some empirical support. Where these resources are infrequent, primates are routinely trichromatic and consume young leaves during seasonal periods of fruit dearth. These results imply a link between the differential evolution of primate color vision and climatic changes during the Eocene-Oligocene transition.     

The Behavioral Ecology of Color Vision: Considering Fruit Conspicuity,Detection Distance and Dietary Importance

Primate color vision is well suited for investigating the genetic basis of foraging behavior owing to a clear genotype–phenotype linkage. Finding fruits amid tropical foliage has long been proffered as an adaptive explanation for primate trichromacy, yet there is a dearth of systematic evaluations of frugivory as an ecological selective force. We studied the behavioral ecology of wild capuchins (Cebus capucinus) in northwestern Costa Rica across the annual cycle and modeled the ability of three dichromatic and three trichromatic phenotypes to discriminate fruits from leaves, a task that represents long-distance search for food patches in a tropical forest. Models of the trichromatic phenotypes could correctly discriminate approximately three-quarters of the total capuchin dietary fruits from leaves, including some fruits subjectively classified as having “cryptic” (greenish-brownish) hues. In contrast, models of dichromatic phenotypes could discriminate fewer than one-third of the fruits. This pattern held when we restricted our analysis to only the most heavily consumed diet items, preferred foods, or seasonally critical species. We in addition highlight the potential of fruit species with small patch sizes to confer an advantage to trichromats, as these resources are anticipated to provide a high finder’s reward. Our results are consistent with the hypothesis that long-distance detection of fruit patches exerts a selective pressure on trichromacy in neotropical primates, and suggest that greenish-brownish fruits might have played an underappreciated role in the evolution of primate color vision.     

Significance of color, calories, and climate to the visual ecology of catarrhines

Here we describe correlations among visual ecology and the physiochemical properties of fruits and leaves consumed by four species of catarrhine primate: Cercopithecus ascanius, Colobus guereza, Pan troglodytes, and Piliocolobus badius. Collectively, their diet was diverse, with each species relying on fruits and leaves to different extents. The mean chromaticity of both foods, as perceived by the green-red and yellow-blue signals that catarrhines decode, was distinct from background foliage. However, selection on the basis of color was evident only for leaves. Primates consumed leaves with higher green-red values than the leaves they avoided-sensory mechanism that correlated with key nutritional variables, such as increased protein and reduced toughness. Moreover, the monkeys ingested leaves near dusk, when reddish targets may be more salient. Similar patterns were never observed with respect to edible fruits, the chromaticities of which did not differ from unconsumed fruits or correlate with nutritional properties. We also found that primate biomass is higher in seasonal sites. We conclude that these findings are consistent with the notion that routine trichromatic vision evolved in a context where seasonal folivory was pivotal to survival.     

Non-visual senses in fruit selection by the mantled howler monkey (Alouatta palliata)

Primates - There is extensive knowledge about the visual system and the implications of the evolution of trichromatic color vision in howler monkeys (genus Alouatta) related to food selection;...     

Do female tamarins use visual cues to detect fruit rewards more successfully than do males?

Primates are unique among eutherian mammals for possessing trichromatic colour vision. It is generally proposed that trichromacy evolved to aid detection of ripe fruits against mature foliage. However, while trichromacy is routine in all Old World monkeys and apes (the catarrhines), a cone opsin polymorphism in New World monkeys (the platyrrhines) results in foraging groups with mixed capacities for chromatic distinction. Although 50-66% of female platyrrhines are trichromatic, all males are dichromatic. Here, we test the hypothesis that trichromatic platyrrhines use visual cues to detect fruit rewards more successfully than do males. Specifically, we ask whether female emperor tamarins, Saguinus imperator imperator, and saddleback tamarins, S. fuscicollis weddelli, are the first members of their foraging group to locate food patches; and, furthermore, whether they are more successful than males in using colour, shape and size cues to discriminate between sham and reward feeding sites. Our results show that females and males do not differ in their ability to locate or discriminate between feeding sites. We conclude that trichromatic vision in female tamarins does not confer an advantage for detecting yellow fruit rewards against mature foliage. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Fruit choice by red howler monkeys (Alouatta seniculus) in a tropical rain forest

This paper presents and discusses aspects of fruit selectivity by red howler monkeys (Alouatta seniculus) in relation with morphological characteristics of fruits. These data are used to provide an answer to the following questions: which are the fruit characteristics that lead fruit choice of howler monkeys and to what extent fruit characteristics play a role in seed dispersal by monkeys? The frugivorous diet of a troop of red howler monkeys was determined during a 2-year field study in French Guiana. The selection of fruit by howler monkeys was analyzed in relation to the fruit availability. Results showed that, although consumption followed availability, fruit species could be classified in three categories according to their selection ratio (percentage of consumption/percentage of abundance) as “high ranking,” “middle ranking,” and “low ranking” species. Also, the 97 species of fruit eaten by the monkeys were grouped according to the morphological characteristics thought to influence the monkeys' choice. This showed that howler monkeys consumed essentially fruits with juicy pulp, bright color, and a small number of well-protected seeds. Most of high ranking species had medium-sized fruits with yellow color, and low ranking species often had small fruits. However, howler monkeys are associated with the dispersal of seeds from fruit with a hard and indehiscent pericarp and/or large seeds, like those of the Sapotaceae family. Consequently, they can be considered as “specialized” frugivores for this fruit syndrome. © l996 Wiley-Liss, Inc.     

Genetic evidence for the coexistence of pheromone perception and full trichromatic vision in howler monkeys

Vertebrate pheromones are water-soluble chemicals perceived mainly by the vomeronasal organ (VNO) for intraspecific communications. Humans, apes, and Old World (OW) monkeys lack functional genes responsible for the pheromone signal transduction and are generally insensitive to vomeronasal pheromones. It has been hypothesized that the evolutionary deterioration of pheromone sensitivity occurred because pheromone communication became redundant after the emergence of full trichromatic color vision via the duplication of the X-chromosome-linked red/green opsin gene in the common ancestor of hominoids and OW monkeys. Interestingly, full trichromacy also evolved in the New World (NW) howler monkeys via an independent duplication of the same gene. Here we sequenced from three species of howler monkeys an essential component of the VNO pheromone transduction pathway, the gene encoding the ion channel TRP2. In contrast to those of hominoids and OW monkeys, the howler TRP2 sequences have none of the characteristics of pseudogenes. This and other observations indicate that howler monkeys have maintained both their systems of pheromone communication and full trichromatic vision, suggesting that the presence of full trichromacy alone does not lead to the loss of pheromone communication. We suggest that the ecological differences between OW and NW primates, particularly in habitat selection, may have also affected the evolution of pheromone perception.     

Importance of achromatic contrast in short-range fruit foraging of primates

Trichromatic primates have a 'red-green' chromatic channel in addition to luminance and 'blue-yellow' channels. It has been argued that the red-green channel evolved in primates as an adaptation for detecting reddish or yellowish objects, such as ripe fruits, against a background of foliage. However, foraging advantages to trichromatic primates remain unverified by behavioral observation of primates in their natural habitats. New World monkeys (platyrrhines) are an excellent model for this evaluation because of the highly polymorphic nature of their color vision due to allelic variation of the L-M opsin gene on the X chromosome. In this study we carried out field observations of a group of wild, frugivorous black-handed spider monkeys (Ateles geoffroyi frontatus, Gray 1842, Platyrrhini), consisting of both dichromats (n = 12) and trichromats (n = 9) in Santa Rosa National Park, Costa Rica. We determined the color vision types of individuals in this group by genotyping their L-M opsin and measured foraging efficiency of each individual for fruits located at a grasping distance. Contrary to the predicted advantage for trichromats, there was no significant difference between dichromats and trichromats in foraging efficiency and we found that the luminance contrast was the main determinant of the variation of foraging efficiency among red-green, blue-yellow and luminance contrasts. Our results suggest that luminance contrast can serve as an important cue in short-range foraging attempts despite other sensory cues that could be available. Additionally, the advantage of red-green color vision in primates may not be as salient as previously thought and needs to be evaluated in further field observations.     

Color vision of ancestral organisms of higher primates

The color vision of mammals is controlled by photosensitive proteins called opsins. Most mammals have dichromatic color vision, but hominoids and Old World (OW) monkeys enjoy trichromatic vision, having the blue-, green-, and red-sensitive opsin genes. Most New World (NW) monkeys are either dichromatic or trichromatic, depending on the sex and genotype. Trichromacy in higher primates is believed to have evolved to facilitate the detection of yellow and red fruits against dappled foliage, but the process of evolutionary change from dichromacy to trichromacy is not well understood. Using the parsimony and the newly developed Bayesian methods, we inferred the amino acid sequences of opsins of ancestral organisms of higher primates. The results suggest that the ancestors of OW and NW monkeys lacked the green gene and that the green gene later evolved from the red gene. The fact that the red/green opsin gene has survived the long nocturnal stage of mammalian evolution and that it is under strong purifying selection in organisms that live in dark environments suggests that this gene has another important function in addition to color vision, probably the control of circadian rhythms.      

Effect of color vision phenotype on the foraging of wild white-faced capuchins, Cebus capucinus

New World monkeys exhibit a color vision polymorphism. It resultsfrom allelic variation of the single-locus middle-to-long wavelengthopsin gene on the X chromosome. Females that are heterozygousfor the gene possess trichromatic vision. All other individualspossess dichromatic vision. The prevailing hypothesis for themaintenance of the color vision polymorphism is through a consistentfitness advantage to heterozygous trichromatic females. Suchfemales are predicted to be more efficient than dichromats whendetecting and selecting fruit. Recent experiments with captivecallitrichid primates provided support for this hypothesis bydemonstrating that color vision phenotype affects behavioralresponses to contrived food targets. Yet, the assumptions thattrichromatic females acquire more calories from fruit, or thatnumber of offspring is linked to caloric intake, remain untested.Here, we assess if, in the wild, heterozygous trichromatic individualsin a group of white-faced capuchins (Cebus capucinus) enjoyan energetic advantage over dichromats when foraging on fruit.Contrary to the assumptions of previous theoretical and experimentalstudies, our analysis of C. capucinus foraging behavior showsthat trichromats do not differ from dichromats in their fruitor energy acquisition rates. For white-faced capuchins, theadvantage of trichromatic vision may be related to the detectionof predators, animal prey, or fruit under mesopic conditions.This result demonstrates the importance of using a fitness currencythat is relevant to individual animals to test evolutionaryhypotheses.     

Spectral sensitivity of vervet monkeys (Cercopithecus aethiops sabaeus) and the issue of catarrhine trichromacy

Several genera of platyrrhine monkeys show significant polymorphism of color vision. By contrast, catarrhine monkeys have usually been assumed to have uniform trichromatic color vision. However, the evidential basis for this assumption is quite limited. To study this issue further, spectral sensitivity functions were obtained from vervet monkeys (Cercopithecus aethiops sabaeus) using the technique of electroretinographic flicker photometry. Results from a chromatic adaptation experiment indicated that each of the twelve subjects had two classes of cone pigment in the 540/640 nm portion of the spectrum. That result strongly suggests that this species has routine trichromatic color vision. Comparison of the spectral sensitivity functions obtained from vervets and from similarly-tested humans further indicates that the cone complements of the two species are very similar. Results from this investigation add further support to the idea that there are fundamental differences in the genetic mechanisms underlying color vision in platyrrhine and catarrhine monkeys.     

Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates

Olfactory receptor (OR) genes constitute the molecular basis for the sense of smell and are encoded by the largest gene family in mammalian genomes. Previous studies suggested that the proportion of pseudogenes in the OR gene family is significantly larger in humans than in other apes and significantly larger in apes than in the mouse. To investigate the process of degeneration of the olfactory repertoire in primates, we estimated the proportion of OR pseudogenes in 19 primate species by surveying randomly chosen subsets of 100 OR genes from each species. We find that apes, Old World monkeys and one New World monkey, the howler monkey, have a significantly higher proportion of OR pseudogenes than do other New World monkeys or the lemur (a prosimian). Strikingly, the howler monkey is also the only New World monkey to possess full trichromatic vision, along with Old World monkeys and apes. Our findings suggest that the deterioration of the olfactory repertoire occurred concomitant with the acquisition of full trichromatic color vision in primates.     

Color vision pigment frequencies in wild tamarins (Saguinus spp.)

The adaptive importance of polymorphic color vision found in many New World and some prosimian primates has been discussed for many years. Polymorphism is probably maintained in part through a heterozygote advantage for trichromatic females, as such individuals are observed to have greater foraging success when selecting ripe fruits against a background of forest leaves. However, recent work also suggests there are some situations in which dichromatic individuals may have an advantage, and that variation in color vision among individuals possessing different alleles may also be significant. Alleles that confer a selective advantage to individuals are expected to occur at a higher frequency in populations than those that do not. Therefore, analyzing the frequencies of color vision alleles in wild populations can add to our understanding of the selective advantages of some color vision phenotypes over others. With this aim, we used molecular techniques to determine the frequencies of color vision alleles in 12 wild tamarin groups representing three species of the genus Saguinus. Our results show that allele frequencies are not equal, possibly reflecting different selective regimes operating on different color vision phenotypes.     

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.     

Diet and Feeding Ecology of Woolly Monkeys in a Western Amazonian Rain Forest

I investigated the diet and feeding ecology of two social groups of woolly monkeys (Lagothrix lagotricha poeppigii) in Yasuní National Park, Ecuador between April 1995 and March 1996. Woolly monkeys in Yasuní were predominantly frugivorous, with fruits comprising ca. 77% of the yearly diet; the next most common food type in the diet was insect and other animal prey. The fruit diet of woolly monkeys in Yasuní is the most diverse yet recorded for any ateline primate, including spider monkeys (Ateles), which are often regarded as ripe fruit specialists: 208 distinct morphospecies of fruits were consumed by woolly monkeys either during the study or during several preceding months of pilot work. Nonetheless, close to one-third of the yearly diet came from just 3 plant genera—Inga, Ficus, and Spondias—and only 20 genera each contributed to 1% of the diet. For one study group, the proportion of ripe fruit in the diet each month was correlated with the habitat-wide availability of this resource, a pattern evidenced by several other ateline species. However, the relationship was not apparent in the second study group. The modal party size for feeding bouts on all food types was a single monkey, and, contrary to reports for other atelines, neither feeding party size nor the total number of feeding minutes that groups spent in food patches was well predicted by patch size. Both results highlight the independent nature of woolly monkey foraging. Given that woolly monkeys and closely-related spider monkeys focus so heavily on ripe fruits, their very different patterns of social organization are intriguing and raise the question of just how their ecological strategies differ. Two important differences appear to be in the use of animal prey and in the phytochemical composition of the ripe fruits that they consume: spider monkeys rarely forage for animal prey, and woolly monkeys seldom consume the lipid-rich fruits that are an important part of spider monkey diets.