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      Taste Responsiveness of Spider Monkeys to Dietary Ethanol

      1 , 2 , 1
      Chemical Senses
      Oxford University Press (OUP)

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          Abstract

          Recent studies suggest that frugivorous primates might display a preference for the ethanol produced by microbia in overripe, fermenting fruit as an additional source of calories. We, therefore, assessed the taste responsiveness of 8 spider monkeys (Ateles geoffroyi) to the range of ethanol concentrations found in overripe, fermenting fruit (0.05–3.0%) and determined taste preference thresholds as well as relative taste preferences for ethanol presented in sucrose solutions and in fruit matrices, respectively. Using a 2-bottle preference test of short duration (1 min), we found that spider monkeys are able to detect ethanol concentrations as low as 0.5%, that they prefer ethanol concentrations up to 3% over water, and that they prefer sucrose solutions and pureed fruit spiked with ethanol over equimolar sucrose solutions and pureed fruit without ethanol. However, when presented with an ethanol-spiked sucrose solution and a higher-concentrated sucrose solution without ethanol, the animals clearly preferred the latter, even when the sucrose–ethanol mixture contained 3 times more calories. These results demonstrate that spider monkeys are more sensitive to the taste of ethanol than rats and humans and that they prefer ecologically relevant suprathreshold concentrations of ethanol over water. Tests with sucrose solutions and pureed fruits that were either spiked with ethanol or not suggest that sweetness may be more important for the preferences displayed by the spider monkeys than the calories provided by ethanol. The present results, therefore, do not support the notion that dietary ethanol might be used by frugivorous primates as a supplemental source of calories.

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          Most cited references50

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          Why Fruits Rot, Seeds Mold, and Meat Spoils

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            Voluntary ethanol consumption in 22 inbred mouse strains.

            Inbred strains are genetically stable across time and laboratories, allowing scientists to accumulate a record of phenotypes, including physiological characteristics and behaviors. To date, the C57/C58 family of inbred mouse strains has been identified as having the highest innate ethanol consumption, but some lineages have rarely or never been surveyed. Thus, the purpose of the present experiment was to measure ethanol preference and intake in 22 inbred mouse strains, some of which have never been tested for ethanol consumption. Male and female mice (A/J, BALB/cByJ, BTBR+T(tf/tf), BUB/BnJ, C57BL/6J, C57BLKS/J, C58/J, CZECH/Ei, DBA/2J, FVB/NJ, I/LnJ, LP/J, MA/MyJ, NOD/LtJ, NON/LtJ, NZB/B1NJ, NZW/LacJ, PERA/Ei, RIIIS/J, SEA/GnJ, SM/J, and 129S1/SvlmJ) were individually housed and given unlimited access in a two-bottle choice procedure to one bottle containing tap water and a second containing increasing concentrations of ethanol (3%, 6%, 10%), 0.2% saccharin, and then increasing concentrations of ethanol (3%, 6%, 10%) plus 0.2% saccharin. Mice were given access to each novel solution for a total of 4 days, with a bottle side change every other day. Consistent with previous studies, C57BL/6J (B6) mice consumed an ethanol dose of >10g/kg/day whereas DBA/2J (D2) mice consumed or =0.83) were determined between consumption of the unsweetened versus sweetened ethanol solutions. Consumption of saccharin alone was significantly positively correlated with the sweetened ethanol solutions (rs=0.62-0.81), but the correlation with unsweetened ethanol solutions was considerably lower (rs=0.37-0.45). These results add new strains to the strain mean database that will facilitate the identification of genetic relationships between voluntary ethanol consumption, saccharin preference, and other phenotypes.
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              Fruits, fingers, and fermentation: the sensory cues available to foraging primates.

              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.

                Author and article information

                Journal
                Chemical Senses
                Oxford University Press (OUP)
                0379-864X
                1464-3553
                August 11 2019
                August 11 2019
                Affiliations
                [1 ]IFM Biology, Linköping University, Linköping, Sweden
                [2 ]Instituto de Neuro-Etologia, Universidad Veracruzana, Xalapa, Veracruz, Mexico
                Article
                10.1093/chemse/bjz049
                31400282
                3fcbe9b2-0e00-4fec-b0a0-05b55e84873d
                © 2019

                https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model

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