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.

Fruits, Fingers, and Fermentation: The Sensory Cues Available to Foraging Primates

In order to optimize foraging efficiency and avoid toxicosis, animals must be able to detect, discriminate, and learn about the predictive signals of potential food. Primates are typically regarded as animals that rely mainly on their highly developed visual systems, and little is known about the role that the other senses may play in food selection. It was therefore the aim of the present study to assess which senses are involved in the evaluation of food by two species of New World primates: the squirrel monkey and the spider monkey. To this end, six animals per species were repeatedly presented with both familiar and novel food items, and their behavior was videotaped and analyzed. To obtain a further indication of the relative importance of visual and chemosensory cues, the animals were also presented with familiar food items that were experimentally modified in color, odor, or both color and odor. The results demonstrate that squirrel monkeys and spider monkeys use olfactory, gustatory, and tactile cues in addition to visual information to evaluate novel food, whereas they mainly inspect familiar food items visually prior to consumption. Our findings also show that in both species the use of nonvisual cues decreased rapidly with repeated presentations of novel food, suggesting a fast multimodal learning process. Further, the two species clearly differ in their relative use of nonvisual cues when evaluating novel or modified food, with spider monkeys relying more on olfactory cues than squirrel monkeys, and squirrel monkeys relying more on tactile cues compared to spider monkeys.

Which senses play a role in nonhuman primate food selection? A comparison between squirrel monkeys and spider monkeys

CT imaging was undertaken on the skull of approximately 20-Myr-old Miocene Tremacebus harringtoni. Here we report our observations on the relative size of the olfactory fossa and its implications for the behavior of Tremacebus. The endocranial surface of Tremacebus is incomplete, making precise estimate of brain size and olfactory fossa size imprecise. However, olfactory fossa breadth and maximum endocranial breadth measured from CT images of one catarrhine species and eight platyrrhine species for which volumes of the olfactory bulb and brain are known show that the osteological proxies give a reasonably accurate indication of relative olfactory bulb size. Nocturnal Aotus has the largest relative olfactory fossa breadth and the largest olfactory bulb volume compared to brain volume among extant anthropoids. Tremacebus had a much smaller olfactory fossa breadth and, by inference, bulb volume--within the range of our sample of diurnal anthropoids. Variations in the relative size of the olfactory bulbs in platyrrhines appear to relate to the importance of olfaction in daily behaviors. Aotus has the largest olfactory bulbs among platyrrhines and relies more on olfactory cues when foraging than Cebus, Callicebus, or Saguinus. As in other examples of nocturnal versus diurnal primates, nocturnality may have been the environmental factor that selected for this difference in Aotus, although communication and other behaviors are also likely to select for olfactory variation in diurnal anthropoids. Considering the olfactory fossa size of Tremacebus, olfactory ability of this Miocene monkey was probably not as sensitive as in Aotus and counts against the hypothesis that Tremacebus was nocturnal. This finding accords well with previous observations that the orbits of Tremacebus are not as large as nocturnal Aotus.

https://onlinelibrary.wiley.com/doi/pdf/10.1002/ar.a.20121

Olfactory fossa of Tremacebus harringtoni (platyrrhini, early Miocene, Sacanana, Argentina): implications for activity pattern.

Using a conditioning paradigm, the olfactory sensitivity of three squirrel monkeys and three pigtail macaques for homologous series of aliphatic 2-ketones (2-butanone to 2-nonanone), symmetrical ketones (3-pentanone to 6-undecanone), and C7-ketones (2-heptanone to 4-heptanone) was assessed. In the majority of cases, the animals of both species significantly discriminated concentrations below 1 ppm from the odorless solvent, and with 2-nonanone and 5-nonanone the monkeys even demonstrated thresholds below 1 ppb. The results showed both primate species have a well-developed olfactory sensitivity for aliphatic ketones, and pigtail macaques generally perform better than squirrel monkeys in detecting members of this class of odorants. Further, in both species tested, we found a significant negative correlation between perceptibility in terms of olfactory detection thresholds and carbon-chain length of both the 2-ketones and the symmetrical ketones, but not between detection thresholds and position of the functional group with the C7-ketones. These findings lend further support to the growing body of evidence suggesting that between-species comparisons of the number of functional olfactory receptor genes or of neuroanatomical features are poor predictors of olfactory performance.

Olfactory sensitivity for aliphatic alcohols in squirrel monkeys and pigtail macaques.

For omnivorous primates, as for other selective omnivores, the array of potential foods in their home ranges present a twofold problem: not all nutrients are present in any food in the requisite amounts or proportions and not all toxins and other costs are absent. Costs and benefits are inextricably linked. This so-called packaging problem is particularly acute during periods, often seasonal, when the benefit-to-cost ratios of available foods are especially low and animals must subsist on fallback foods. Thus, fallback foods represent the packaging problem in extreme form. The use of fallback foods by omnivorous primates is part of a suite of interconnected adaptations to the packaging problem, the commingling of costs and benefits in accessing food and other vital resources. These adaptations occur at every level of biological organization. This article surveys 16 types of potential adaptations of omnivorous primates to fallback foods and the packaging problem. Behavioral adaptations, in addition to finding and feeding on fallback foods, include minimizing costs and requirements, exploiting food outbreaks, living in social groups and learning from others, and shifting the home range. Adaptive anatomical and physiological traits include unspecialized guts and dentition, binocular color vision, agile bodies and limbs, Meissner's corpuscles in finger tips, enlargement of the neocortex, internal storage of foods and nutrients, and ability internally to synthesize compounds not readily available in the habitat. Finally, during periods requiring prolonged use of fallback foods, life history components may undergo changes, including reduction of parental investment, extended interbirth intervals, seasonal breeding or, in the extreme, aborted fetuses.

/pdf/fallback-foods-eclectic-omnivores-and-the-packaging-problem-1hdyvrjizs.pdf

Fallback foods, eclectic omnivores, and the packaging problem.

Using a conditioning paradigm, the olfactory sensitivity of three squirrel monkeys and three pigtail macaques for a homologous series of aliphatic aldehydes (n-butanal to n-nonanal) was assessed. With only few exceptions, the animals of both species significantly discriminated concentrations below 1 ppm from the odorless solvent, and with n-butanal and n-hexanal individual pigtail macaques even demonstrated thresholds below 1 ppb. The results showed (1) both primate species to have a well-developed olfactory sensitivity for aliphatic aldehydes, (2) pigtail macaques to generally perform better than squirrel monkeys in detecting members of this class of odorants, and (3) no significant correlation between perceptibility in terms of olfactory detection thresholds and carbon chain length of the aliphatic aldehydes in both species tested. These findings lend further support to the growing body of evidence suggesting that between-species comparisons of the number of functional olfactory receptor genes or of neuroanatomical features are poor predictors of olfactory performance. Further, our findings suggest that olfaction may play an important and hitherto underestimated role in the regulation of behavior in the species tested.

Y. Simon

Papers

Olfactory sensitivity for aliphatic aldehydes in squirrel monkeys and pigtail macaques.