© 2004 by The Society for Integrative and Comparative Biology
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Fruits, Fingers, and Fermentation: The Sensory Cues Available to Foraging Primates1
1 Department of Ecology and Evolution, University of Chicago, 1101 East 57th Street, Chicago, Illinois 60637
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Survival and reproductive success hinge on the perception of environmental stimuli. In this regard, foraging efficiency depends on discerning predictive signals in food. A widespread occurrence of ethanol in fruits indicates a sustained historical exposure of frugivores to this compound. Accordingly, Dudley (2000
, Quart. Rev. Biol. 75:3–15) proposed that ethanol could represent a prominent sensory cue to primates because of direct and indirectly associated caloric and physiological rewards. However, little is known regarding the extent to which ethanol correlates with such parameters. This information is essential to estimating the importance of detecting and detoxifying ethanol in fruits. Here I present a preliminary analysis of fruits from Southeast Asia; low levels of ethanol were present in fruits of all developmental stages (range: 0.005–0.48%). Moreover, ethanol correlated positively with concentrations of soluble sugars, suggesting that it could be a valuable foraging cue. Recent findings on the sensitivity of primate olfaction and gustation to ethanol are consistent with this notion. However, when primates smell fruits deliberately, it often occurs together with digital and/or dental evaluation of texture. Here I show that softening texture also characterizes the fruit ripening process, and that color is of ambiguous importance to primates possessing trichromatic vision. I discuss the relevance of these findings to the origins of primates and the ecology of key sensory systems and deduce that detecting and selecting fruits on the basis of cues other than color is a persistent theme in primate evolution. Ethanol has likely played a significant and underestimated role in the regulation of primate foraging behavior. |
INTRODUCTION |
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"From hour to hour, we ripe and ripe,And then from hour to hour, we rot and rot:
And thereby hangs a tale."
Shakespeare—As You Like It, I.vii.26
This tale hangs on the evolutionary triad of microbes, fruits, and frugivores (Levey, 2004). Competition between microorganisms and seed dispersers for fruit pulp raises the possibility that anaerobic yeast "discard [ethanol] as soldiers ‘discard’ bullets;" that is, "the primary reason why yeasts manufacture alcohol is to render ripe fruits distasteful or unacceptable to wild vertebrates" (Janzen, 1977, p. 60). Although frugivores tend to avoid rotting fruit (Levey, 1987; Borowicz, 1988; Buchholz and Levey, 1990; Valburg, 1992a, b), a repellent role for ethanol is unconvincing (Culberson and Culberson, 1981). In fact, ethanol is one of the less averse mycotoxins. In a study of fungi-laden fruits, those infected with yeast, Saccharomyces cerevisiae, were among the least objectionable to birds (Cipollini and Stiles, 1993a). Furthermore, birds are reported to consume fermenting fruits in natural contexts. Indeed, lethal intoxication has been inferred, with blood alcohol levels of 0.02%–0.10% being reported in perished individuals (Dennis, 1987; Fitzgerald et al., 1990; Stephen and Walley, 2000). Further instances of inebriation are few, and limited usually to animals consuming distilled spirits (e.g., Miller, 1997). In one notable case, a hedgehog that consumed egg-liqueur expired with a blood alcohol level of 0.04% (Schoon et al., 1992).
Positive effects of yeasts on frugivores or plant fitness are seldom considered (Cipollini and Stiles, 1993b). In this regard, Dudley (2000) suggested that low levels of ethanol in fruits might attract seed dispersers because of associated caloric and physiological benefits. Such benefits raise the possibility that frugivores have evolved adaptations to sense and detoxify low-levels of ethanol. On this basis, Dudley (2002) inferred that ethanol could be a foraging cue to anthropoid primates and that olfaction was a key sense for detecting and navigating towards edible fruits. He suggested, too, that the predilection evinced by contemporary humans to imbibe alcohol is rooted in this adaptive context. Accordingly, examining the sensory ecology of primate frugivory and determining the occurrence of ethanol in tropical fruits is an important issue in the study of human evolution. Here I have two aims: (1) to review recent information on the sensory adaptations of primates with respect to ethanol; and, (2) to present preliminary data on the ethanol content of fruits from Southeast Asia.
Recent experiments have demonstrated an exquisite sensitivity of primates to fruit-associated odors, such as aliphatic esters, aldehydes, and alcohols (Laska and Seibt, 2002a, b; Laska et al., 2003b). With respect to aliphatic alcohols, monkeys demonstrate olfactory thresholds lower than those of the rat (Laska and Seibt, 2002a), which is traditionally regarded as a macrosmatic animal (i.e., a species with an outstanding sense of smell). Humans are imbued with a similar olfactory sensitivity (Cometto-Muñiz and Cain, 1990; Laska and Freyer, 1997). Ethanol also elicits responses from nerves that convey taste and somatic sensations from the oral cavity. The responses of the chorda tympani, glossopharyngeal, and trigeminal nerves to ethanol are far stronger in rhesus macaques than in dogs, cats, and Norwegian rats (Hellekant et al., 1997; Danilova and Hellekant, 2000, 2002). The collective strength of these sensory responses is consistent with the notion that ethanol plays a significant and hitherto underestimated role in the regulation of primate foraging behavior (Dudley, 2000). However, few studies have examined the importance of ethanol as a foraging cue or the extent to which primates engage in chemotaxic navigation (Dominy et al., 2001).
Interestingly, elephants prefer ethanol solutions of 7% to concentrations of 0%, 10%, 14%, 25%, and 50% (Siegel and Brodie, 1984). Furthermore, captive and feral primates readily consume commercial spirits (Fitz-Gerald, 1972; Shoumatoff, 2003). However, the ethanol content in these reports lacks biological relevance. Mammals typically eschew rotten fruits, the ethanol content of which seldom exceeds 4% (Gibson et al., 1981; Merçot et al., 1994). Thus when consuming fruits in a natural context, primates are unlikely to exhibit signs of intoxication, making it difficult to infer ethanol-mediated foraging on the basis of behavior (Milton, 2004). However, anecdotes may be germane (Siegel, 1989). For example, van Roosmalen (personal communication) describes the tendency of spider monkeys (Ateles paniscus) to appear intoxicated when feeding on the fruits of Dicranostyles guianensis (Convolvulaceae) and hard-husked sapotaceous genera (i.e., Pouteria, Chrysophyllum, and Ecclinusa). He observed that only pulpy, but indehiscent, fruits with a juicy, sweet flesh produce ethanol when becoming overripe. During times of scarcity, such fruits are consumed before they ferment. Whitten (1982, p. 186) notes that Kloss gibbons (Hylobates klossii) avoid overripe fruits, but he is equivocal as to "whether the taste of ethanol... or other side products of microbial decay influence [gibbon food choice]." Accordingly, the hypothesized deterrence of ethanol to frugivorous vertebrates (Janzen, 1977), or specifically primates, is unsubstantiated. In fact, although evidence is scant, primates appear to ingest ethanol with few reservations.
Sensory cues and primate food selection
Primate feeding tends to involve a series of behavioral elements during which the individual responds to successive stimuli of different modalities. For example, spider monkeys "inspect fruits by sniffing or biting [them], since the external properties of the fruit (like colour) do not give a decisive answer on the stage of maturity" (van Roosmalen, 1985, p. 87). Similarly, Kappeler (1984, p.228) reported that, "food may be examined (by smell or taste) before it is ingested [by moloch gibbons]." Chimpanzees also "inspect individual food items by sight, touch, or smell" (Wrangham, 1977, p. 510). When the outcome of a sensory evaluation is to reject a particular food item, primates frequently select another, similar food item and repeat their evaluation process. The sequential nature of such behavioral elements is called a behavioral chain (van Loon and Dicke, 2001). Although modification of behavior can be observed as faster decision making or as changes in preference, the sequence is typically constant.
The chain of primate food selection behaviors can be divided into two consecutive phases: (1) searching and (2) contact-testing. The searching phase ends by establishing contact with a food item. Once a food is contacted, different forms of haptic behavior are exhibited. Such behaviors involve repeated contact with the digits, lips, or incisors, which are mechanically sensitive (Peleg, 1980). The contact-testing phase ends with food acceptance (deglutition). At this point mechanical and gustatory information have become available in the oral cavity in addition to olfactory information (Fig. 1). The final decision to accept or reject a food item is based not only on the sensory properties of the food itself, but also on the primate's physiological state (satiety, reproductive status) and information from previous experiences. All these factors are integrated in the central nervous system and in concert determine food acceptance and preference.
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Anteoral evaluations include close visual and olfactory assessment and digital contact or palpation. Fruit damage may include insect or fungal infestation and scarringThe existence of primate behavioral chains implies that diffuse, widespread correlations exist in the physicochemical attributes of fruits. Here I attempt to define these relationships and discuss their impact on the evolution of primate sensory systems. Attention is focused on the traits that may attract primates during searching (color and ethanol content) and the traits that may provide information during contact-testing (texture, sugar concentration, and ethanol content).
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METHODS |
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In August 2003, fruits were collected from the Bukit Timah Nature Reserve, central Singapore (1°21'N, 103°47'E). Approximately 225 ha in size, the reserve consists of primary lowland dipterocarp and secondary forest; rainfall is approximately 2,600 mm/year (Corlett, 1990
). Plant taxonomy follows Turner (1995a, b). Physicochemical measurements were made in the Department of Biological Sciences, National University of Singapore. The approximate developmental state of a fruit was characterized anthropogenically. Overripe and obviously decaying fruits from the ground were excluded on the basis that primates seldom consume them. The use of terms such as ripe and unripe are used solely for the purpose of vernacular convenience. Sensory measurements are not correlated with these terms, but with sugar concentrations. Sugars are viewed as the primary reward of vertebrate-dispersed fruits.
Physical measurements
Fruit reflectance spectra were measured with an Ocean Optics S2000 spectrometer (Dunedin, FL, USA) fitted with diffraction grating No. 2, admitting light from 200–850 nm. Within 4 hr of collection, fruit specimens were mounted in a custom-built chamber and illuminated with a 12 volt, 3100-Kelvin tungsten halogen lamp (LS-1; Ocean Optics; range: 350–700 nm; Lucas et al., 2001). Light was focused onto specimens through a 400-µm diameter patch fiber-optic cable and lens (Ocean Optics). Light was collected with a second lens and transmitted through a 200-µm fiber cable to the diffraction grating of the S2000. Specimens were placed 45° to the incident illumination with 20-degree axes separated the illuminating and recording lenses. All spectra were referenced to BaSO4.
A portable universal tester measured fruit mechanical properties (Darvell et al., 1996). Radial samples of fruit flesh were cut orthogonal to the outer surface and shaped with a 4-mm cork borer into right cylinders, about 5 mm high. The Young's modulus, E, of fruit flesh was determined from tests on short cylinders in compression. Fracture toughness, R, was determined with a 15° angle wedge driven into small rectangular specimens cut from the fruit wall. Toughness was calculated by dividing the area beneath the force-deformation curve by the product of crack depth (i.e., wedge displacement) and initial specimen width (Lucas et al., 2001). To account for anisotropic variation within a fruit, mechanical measurements were taken from both hemispheres and averaged. Lastly, the energetic equivalent of the critical stress intensity factor, KIC, was determined by calculating the square root of E x R (Agrawal and Lucas, 2003). KIC is a parameter related to the perception of hardness during initial incisory evaluation of a food item (Vincent et al., 2002).
Spectral modeling
Reconstructing the color of a primate food item requires spectral modeling. This is achieved by multiplying the reflectance spectrum of the object by an illuminant (Fig. 2). Attenuation of short-wavelengths by the lens and neural retina was not modeled here as in other studies (Regan et al., 2001). The quantum catch (Q) of S-, M-, and L-cone classes was calculated by multiplying the stimulus radiance and cone absorption spectra, and integrating the resulting spectrum over wavelength (Fig. 2). Chromaticity coordinates analogous to MacLeod-Boynton (1979) coordinates may be graphed by plotting a y value of QS/(QL + QM), which defines yellowblueness (yellow low, blue high), against an x value of QL/(QL + QM), which defines greenredness (green low, red high). Respectively, these coordinates correspond to the physiological ‘channels’ of catarrhine primates, the phylogenetically recent green-red channel (subserved by midget ganglion cells) and the S-cone mediated yellow-blue channel (subserved by small bistratified ganglion cells).
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Chemical measurements
High performance liquid chromatography (HPLC) was used to measure concentrations of sucrose, fructose, and glucose (Lee, 1990
). Extractions of 0.1 g fruit flesh in 5 ml 1:1 dH2O:CH3OH were made with a portable Tissue Tearor (BioSpec, Bartlesville, OK, USA). Ethanol concentrations were determined from vapor pressure measurements at 24°C using a modified electrochemical sensor (PAS Systems, Fredericksburg, VA, USA) calibrated against solutions of known concentration (Dudley, 2004). Fruit acidity was measured with a solid-state pH meter (model 1001, Sentron BV, Roden, the Netherlands). |
RESULTS |
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Ethanol as an olfactory cue
Depending on taxonomic identity and state of development, ethanol concentrations in fruits ranged from trace quantities to near 0.5% (Table 1). These results are consistent with reports of ripe fruits from Helsinki, Finland (n = 3 species; range: 0.01–0.3%; Eriksson and Nummi, 1982
), Barro Colorado Island, Panama (n = 3 species; range: 0.01–0.6%; Dudley, 2002), and varied localities in Israel (n = 5 species; range: 0.1–0.7%; Sanchez et al., 2004). Among the forest fruits analyzed here, a positive correlation exists between ethanol content and total sugar concentration (Fig. 3a), but not between ethanol content and pH (R2 = 0.001). With respect to mechanical properties, ethanol content is negatively correlated with both KIC (Fig. 3b) and Young's modulus (R2 = 0.31; P < 0.02).
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Color as a visual cue
Hues of collected fruits varied, with no single hue corresponding to the subjective evaluation of ripeness in all fruits (Table 1). Theoretical modeling of fruit spectra into the trichromatic color space of catarrhine primates yielded similar results. Although fruit chromaticities were collectively conspicuous when viewed against mature foliage (Fig. 4a), total sugar concentration could not be predicted from variation on either the green-red or yellow-blue axes (Fig. 4b). It is clear, however, that developmental color changes within a taxon, e.g., Fagrea fragrans and Ficus variegata (Table 1), can signal corresponding changes in nutritional status.
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Texture as a haptic cue
Observations that primates palpate fruits manually or bite fruits softly suggest that fruit texture is a cue that correlates with nutritional rewards. Among the fruits examined here, the critical stress intensity factor, KIC, correlated negatively with total sugar content (Fig. 5a). A similar relationship was observed with respect to Young's modulus (R2 = 0.23; P = 0.02). Compellingly, the relationship appears to extend to tropical fruits generally (Fig. 5b). The digital and dental perception of fruit texture appears to be a valuable sensory parameter. Finally, softer fruits also tended to be acidic (Young's modulus: R2 = 0.41; P = 0.001; KIC: R2 = 0.38; P = 0.002).
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DISCUSSION |
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Here it is shown that low levels of ethanol exist in ripening fruits. Moreover, it is shown that ethanol content correlates positively with concentrations of soluble sugars. Accordingly, olfaction of ethanol could represent a valuable sensory mechanism during foraging. However, when primates smell fruits deliberately, it often occurs together with digital and/or dental evaluation of texture. Here I have shown that softening texture is also a characteristic component of the fruit ripening process. Softening within a fruit taxon tends to progress more rapidly than external pigment accumulation (Brady, 1987
). In this regard, fruit texture may be a more accurate indicator of nutritional status than fruit color. Although fruit color is sometimes a conspicuous signal of edibility, I found no overall correlation between chromatic signals and sugar content (see also Dominy and Lucas, 2004). Because ethanol content and texture appear to be broadly informative fruit cues, it is inviting to speculate on the paleobiological importance these cues to the evolution of attendant sensory mechanisms in primates.
Fruits and the sensory ecology of basal primates
Cartmill (1974, 1992) hypothesized that basal primates were visually directed predators of fauna on slender branches, a milieu that favored a wide field of stereopsis and clawless, prehensile hands for visually tracking and grasping prey. The fine-branch niche model for primate origins has since enjoyed wide acceptance, although competing views have emphasized the importance of foraging on fruits, nectar, and/or cryptic prey (Rasmussen, 2002). Recently, reports on the grasping skill of tree shrews and an extinct plesiadapiform, Carpolestes simpsoni, indicate that fruit-foraging predated fauna capture during primate evolution (Sargis, 2001; Bloch and Boyer, 2002). Though it is unclear whether carpolestids should be included in Primates, it is generally deduced that primates have long been partially frugivorous (Ravosa and Savakova, 2004). In short, grasping food objects and small-diameter supports were probably key factors in the development of primate manual prehension (Lemelin, 1999; Kirk et al., 2003).
The nocturnal origins of primates imposed constraints on certain sensory systems, namely trichromatic vision (Heesy and Ross, 2001). Yet trichromatic vision is not essential to the successful acquisition of fruits. Despite possessing mono- or dichromatic vision, nearly every extant nocturnal primate is partially frugivorous. In fact, Aotus spends 50–80% of its foraging time feeding on fruit (Wright, 1989). If nocturnal primates rely on olfaction to detect fruiting trees, ethanol may be an important cue. It has been produced for 50– 60 Ma (Ashburner, 1998) and chemotaxis is aided by the tendency of low-weight molecules to plume farther at night, when air is cooler and the turbulence of solar convection is reduced (Janzen, 1983; Dusenbery, 1992). Thus basal primates might have used ethanol plumes to locate ripening fruits as well as associated fauna. Interestingly, "one of the best ways to see tarsiers is to wait quietly in the vicinity of [trees with fruit lying on the ground beneath them]. Tarsiers are not attracted to the fruit itself, but by insects and other animals attracted to the fruit. These include large numbers of cockroaches, crickets, other orthopterans and large moths, as well as geckos and other lizards" (Fogden, 1974, p. 161).
Fruits and the sensory ecology of anthropoids
Stem anthropoids are inferred to have been small, diurnal, gregarious, insectivore-frugivores (Ross, 1996, 2000; Kay et al., 1997; Kirk and Simons, 2001). Their adaptive radiation occurred in the Eocene when palms, figs, lipid-rich laurels, and other extant families were prominent (Collinson and Hooker, 1991; Morley, 2000). Although the colors and chemical attributes of Eocene fruits are unknown, gross morphological traits were as diverse as today (Willson and Whelan, 1990; Eriksson et al., 2000). Contemporary fruit variation has resulted in a tendency to describe diffuse dispersal assemblages or syndromes; i.e., fruits tend to be classed by a broad suite of characteristics corresponding to avian or mammalian consumption (e.g., Janson, 1983; Gautier-Hion et al., 1985; Kitamura et al., 2002). Extant anthropoids appear to be blithely insouciant to such syndromes. They consume a great diversity of fruits exhibiting a wide variety of hues (Dominy, 2004). This observation raises the possibility that primate fruit choice is driven not by the hues characterizing a particular dispersal assemblage, but by the universal cues that broadly correlate with sugar rewards. Ethanol and softening texture appear to be such cues.
Although early anthropoids appear to have retained some prominent olfactory adaptations (Rasmussen and Simons, 1992), the evolution of anthropoids is characterized by numerous changes to the visual system (Allman, 1999; Ross, 2000). Such changes indicate a shift of sensory emphasis during foraging. If ethanol continued to be a cue to anthropoids, its importance in the behavioral chain of fruit evaluation probably shifted to the anteoral contact-testing phase (Fig. 1). When an anthropoid smells a fruit deliberately, however, the behavior often coincides with digital and/or dental evaluation of texture. Spatulate incisors and independently controlled digits may have evolved to facilitate these haptic modalities. Indeed, the digital dexterity of anthropoids is unparalleled among vertebrates (Iwaniuk and Whishaw, 2000). Meissner corpuscles (MCs) in the digital skin of primates might also provide an enhanced sense of touch. MCs are rapidly adapting nerve endings that respond to skin deformation. They appear to provide primates with a perception of friction and/or elastic texture (Martin, 1990). Recently, a comparative analysis of MC density in nine anthropoids suggested that touch sensitivity correlates positively with the extent to which fruit is consumed, but locomotor and phylogentic effects could be discounted (Hoffmann et al., 2004).
The advantage to anthropoids of smelling ethanol and sensing the softening texture of fruits is clear—it lifts them from the constraints of feeding on fruits in any one dispersal syndrome. Such sensory modalities (in addition to spatial memory) expand the range of edible fruits and improve foraging efficiency. In this regard, selection may have also favored allelic variation of the M/L opsin gene because it permitted detection of a broad array of fruits; i.e., a diverse coterie of fruit colors may have favored foraging groups containing both di- and trichromatic individuals (Dominy et al., 2003; Smith et al., 2003). Of course, the color vision of Eocene anthropoids is unknown. It is inferred (see below) that they possessed a M/L cone opsin polymorphism similar to extant platyrrhines (New World monkeys), a clade with basal features subsequently lost in Old World monkeys and apes, the catarrhines (Fleagle, 1999).
The platyrrhine polymorphism exists at a single locus for the M/L opsin gene on the X-chromosome. All males possess dichromatic vision because the autosomal S-cone opsin is coupled with a single type of M/ L-cone opsin. Heterozygous females possess trichromatic vision because allelic variation yields differential expression of M/L-cone types (Surridge et al., 2003). Alouatta is an exception. Due to an M/L-opsin gene duplication similar to (but independent of) that of catarrhines, howling monkeys possess routine trichromacy, a condition in which every individual is trichromatic (Jacobs et al., 1996; Kainz et al., 1998). A resemblance of platyrrhine opsin alleles to the M/ L-opsin genes of Alouatta suggest that allelic divergence and fixation preceded gene duplication in the genus (Hunt et al., 1998). One scenario suggests that an unequal crossover event during DNA replication produced two opsin loci on each X-chromosome. Selective advantages conferred on such individuals lead to the spread of the mutation throughout the genus. A similar event in the evolution of catarrhines has been inferred (Surridge et al., 2003). Another view holds that the divergence of M/L-cone opsin genes occurred after an L-opsin gene duplication in a dichromatic ancestor (Nei et al., 1997). Although the small amount of sequence variation between catarrhine L- and M-opsin genes is consistent with this scenario (Hunt et al., 1998), gene conversion can reduce variation in X-chromosome opsin genes (Boissinot et al., 1998).
The selective advantages of trichromatic vision are disputed. Competing hypotheses stress the importance of detecting fruits or young leaves against a background of mature foliage (Lucas et al., 1998; Dominy and Lucas, 2001; Regan et al., 2001). The debate may be resolved by allowing for divergent selection in the evolution of allelic and routine trichromacy. Though speculative, climatic and floristic events during the Eocene-Oligocene transition may have favored regional specializations in anthropoid color vision. Dominy et al. (2003) suggested that anthropoids foraged in Paleogene forests characterized by figs and palms, the fruits of which played a keystone function. Anthropoids are inferred to have relied on such resources and dispersed the seeds. In turn, figs and palms lost or did not evolve conspicuous coloration, as this conferred little advantage for attracting mammals. The coloration might have offered a selective advantage to primates with an M/L cone opsin polymorphism. However, evidence supporting the notion that dichromats might be better suited to detecting color camouflaged fruits is scant or contradictory. Climatic cooling at the end of the Eocene and into the Neogene (ca. 35 Ma) attended widespread regional extinction or decimation of palms and (probably) figs (Morley, 2000). In regions of attrition, anthropoids may have evolved routine trichromacy to exploit proteinaceous young leaves as a fallback resource.
A survey of the color and biogeography of figs and palms provides some empirical support to this hypothesis. Where palms are infrequent, anthropoids are routinely trichromatic and consume young leaves during seasonal periods of fruit dearth (Dominy et al., 2003). Compellingly, the origins of catarrhine leaf consumption—as inferred from molar morphology and estimated body mass—appears between 36 and 33 Ma (Kay and Simons, 1980; Kirk and Simons, 2001). Furthermore, a global study of eight primate taxa showed that polymorphic species are constrained in the chromatic range of edible leaves, but not edible fruits (Lucas et al., 2003). Accordingly, the successful acquisition of fruits (or fruits of particular colors) cannot be strongly tied to the evolution of routine trichromatic vision. In fact, catarrhines and Alouatta possess more olfactory receptor pseudogenes than platyrrhines (Gilad et al., 2004), perhaps because a seasonal reliance on young leaves, which are less fragrant than fruits, resulted in a relaxed selective pressure on olfactory receptors. Indeed, spider monkeys outperform pig-tailed macaques in tasks related to food odor sensitivity (Laska et al., 2003a).
Although fruit color is sometimes or often a useful sensory cue, it cannot alone predict sugar levels in a broad range of edible fruits. Ethanol content and softening texture appear to be more universally informative characteristics. Discerning these cues has strong adaptive advantages to primates. Indeed, the detection and selection of fruits on the basis of cues other than color appears to be a long-standing trend in primate evolution. These findings are consistent with the hypothesis that low levels of ethanol in fruits has have exerted a strong selective pressure on the digestive kinetics (Cheung et al., 1999) and neurosensory physiology of primates (Dudley, 2000, 2002). However, few studies of primate foraging have examined the sensory basis of fruit selection. The existence of behavioral chains indicates that olfactory or haptic cues are important to primates, but such hypotheses must eventually be tested by careful direct observation in the field or laboratory.
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ACKNOWLEDGMENTS |
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I thank R. Dudley, M. Dickinson, and the participants of the In Vino Veritas Symposium. I also thank L. Alport, K.Y. Ang, E.C. Kirk, M. LaBarbera, P.W. Lucas, L. Ramsden, J.J. Socha, H.T.W. Tan, and one anonymous reviewer for their assistance and comments on this work. Lastly, I wish to thank the Raffles Museum of Biodiversity for financial support and the National Parks Board of Singapore for granting research permission (permit no. NP/RP328 A). Additional support was received from a National Institutes of Health National Service Research Award.
Pasoh Forest acknowledgements: Y. C. Chan, Y.-Y. Chen, S. Latif, I.-F. Sun, S. J. Wright, Forest Research Institute of Malaysia, and National Geographic Society grant 7179-01. Kibale forest acknowledgements: B. Balyeganira, C.A. Chapman, P. Kagoro, J. Magnay, M. Musana, D. Osorio, R.W. Wrangham, Makerere University Biological Field Station, Ugandan National Council for Science and Technology, Uganda Wildlife Authority, Croucher Foundation, Explorer's Club, National Geographic Society grant 6584-99, Research Grants Council of Hong Kong grant 7241/97M, and Sigma Xi.
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FOOTNOTES |
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1 From the Symposium In Vino Veritas: The Comparative Biology of Alcohol Consumption presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 5–9 January 2004, at New Orelans, Louisiana.
2 E-mail: njdominy{at}uchicago.edu
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