Ethanol, Fruit Ripening, and the Historical Origins of Human Alcoholism in Primate Frugivory

ROBERT DUDLEY Department of Integrative Biology, University of California, Berkeley, Berkeley, California 94720 and Smithsonian Tropical Research Institute, P.O. Box 2072, Balboa, Republic of Panama

SYNOPSIS Ethanol is a naturally occurring substance resulting from the fermentation by yeast of fruit sugars. The association between yeasts and angiosperms dates to the Cretaceous, and dietary exposure of diverse frugivorous taxa to ethanol is similarly ancient. Ethanol plumes can potentially be used to localize ripe fruit, and consumption of low-concentration ethanol within fruit may act as a feeding stimulant. Ripe and over-ripe fruits of the Neotropical palm Astrocaryum standleyanum contained ethanol within the pulp at concentrations averaging 0.9% and 4.5%, respectively. Fruit ripening was associated with significant changes in color, puncture resistance, sugar, and ethanol content. Natural consumption rates of ethanol via frugivory and associated blood levels are not known for any animal taxon. However, behavioral responses to ethanol may have been the target of natural selection for all frugivorous species, including many primates and the hominoid lineages ancestral to modern humans. Pre-existing sensory biases associating this ancient psychoactive compound with nutritional reward might accordingly underlie contemporary patterns of al- cohol consumption and abuse

INTRODUCTION The widespread occurrence of fermentative yeasts in ripening and ripe fruits indicates potential co-option of associated ethanol for use as a behavioral cue by vertebrate frugivores (Dudley, 2000, 2002). In particular, ethanol plumes might serve in localization of these transient nutritional resources, whereas ethanol consumed during the course of frugivory could act as an appetitive stimulant. Because humans are ances-trally derived from frugivorous primates, preference for and excessive consumption of alcohol by modern humans might accordingly result from pre-existing sensory biases associating ethanol with nutritional reward. Little is known, however, about either the natural occurrence of ethanol within fruits or the behavioral responses of frugivorous animals to such cues. As agents of both microbial decay and fermentative activity, yeasts are widespread both on and inside fruits (see Last and Price, 1969; Cipollini and Stiles,1992, 1993b; Spencer and Spencer, 1997). Anaerobic fermentation of sugars by yeasts yields ethanol. This metabolic pathway emerged in yeasts concomitantly with the shift by angiosperms from small wind-dispersed seeds to larger and more fleshy vertebrate-dispersed fruits during the late Cretaceous into the Paleocene (see Erikssonet al., 2000; Benneret al., 2002). Ethanol expression by fermentative yeasts appears to have specifically evolved to inhibit activity of bacterial competitors within ripe fruit (Ingram and Buttke, 1984), and ethanol plumes emanating from ripe fruit might thus have provided useful sensory information, both diurnally and nocturnally, from the very inception of mammalian frugivory. Given this historical presence of yeasts that consume sugars, plants correspondingly express a diversity of antifungal compounds within developing and ripe fruit to impede decomposition (see Janzen, 1977; Borowicz, 1988b; Cipollini and Stiles, 1992; Cipollini and Levey, 1997ab,c).Because microbial decay reduces the likelihood of vertebrate dispersal (Herrera, 1982; Borowicz, 1988a; Cipollini and Stiles, 1993a), the evolutionary pressures for effective antifungal measures that prevent spoilage are substantial.

The phenomenon of ripening, however, involves relaxation of defenses against premature consumptionboth by potential dispersers and by microbial pathogens (Thompson and Willson, 1979; Herrera, 1982; Janzen, 1983). Fruit ripening involves a coordinated series of changes in color, texture, volatile expression, and the conversion of starch to sugars (Brady, 1987; Tucker, 1993). In aggregate, these changes indicate suitability for consumption and dispersal by a vertebrate frugivore. As a consequence, fully ripe fruits are susceptible to microbial decay, an outcome that can interfere with the plant’s evolutionary goal of consumption and dispersal by vertebrates (see Janzen, 1977; Borowicz, 1988a; Cipollini and Stiles, 1993a). Microbes, invertebrate fruit consumers (especially insect larvae), and vertebrate dispersers can thus be viewed as competitors for access to a rich but transient nutritional substrate. In spite of the possible significance of ethanol for frugivore behavior and ecology (Levey and Martı ́nezdel Rio, 2001), knowledge of fermentation for non-domesticated fruits in natural ecosystems is confined to only several examples. Eriksson and Nummi (1982; see also Forsander, 1978) determined fairly low ethanol contents (0.05–0.3% w/w) for rowan berries, rosehips, and hawthorn fruits in autumn and winter conditions in Finland. Such temperate-zone fruits are unlikely, for reasons of low ambient temperatures alone, to be characterized by particularly high ethanol concentrations. Fermentation of fruit crops is instead more pronounced in warm and humid environments that promote both yeast growth and rapid decomposition. Dudley (2002) presented ethanol data for three fruiting taxa in a Neotropical forest, and found that pulp of ripe and very ripe palm fruits (Astrocaryum standleyanum) contained ethanol at concentrations of about 0.5% and 0.6%, respectively. The present study extends existing data on A. standleyanum to include parallel measures of texture and color for quantitative assessment of fruit ripeness, and also compares larger sample sizes of fruits taken both directly from the infructescence and from the ground where a greater range of decompositional conditions is available. A. standleyanum is a common palm species in lowland Panamanian rainforest, and bears large crops of orange fruits that are consumed by red-tailed squirrels, spiny rats, kinkajou, Central American agoutis, collared peccaries, and white-faced capuchin monkeys (Hladik and Hladik, 1969; Croat, 1978; Smythe, 1978, 1989; Hoch and Adler, 1997; Kays, 1999). This palm therefore represents an appropriate target species for evaluating the potential role of ethanol in the sensory and nutritional ecology of mammalian frugivores.Moreover, palm fruits have been proposed (together with figs) to be keystone resources for Neotropical vertebrate frugivores (Terborgh, 1980). Broad biogeographic and taxonomic screening of angiosperm fruits for ethanol content is beyond the scope of the present paper, but demonstration of ethanol-associated ripeness cues in palms may nonetheless be of general relevance for those frugivorous primates predominantly associated with tropical rain forest.

MATERIALS AND METHODS Field collections and laboratory measurements were carried out on Barro Colorado Island (BCI), Republic of Panama, in May and June 2002 during the rainy season (ripe and over-ripe fruits), and in December 2002 (unripe fruits). Fruits were knocked down from infructescences using either a slingshot or thrown rocks (fruits thus obtained are hereafter referred to as hanging fruits), or were collected at the base of fruiting trees ( i.e., fallen fruits). Following transport of fruits within a closed plastic bag to the laboratory on BCI, measurements were made either immediately or within three hours of collection. In the latter case, individually bagged fruits were kept within a cold room at 108C. Fruits were visually categorized as being either ripe or over-ripe; obviously rotting fruits were not used for measurements. Over-ripe fruits were never obtained from infructescences, and thus were only collected from the ground. Spatial heterogeneity of ripeness within an individual fruit was sometimes pronounced, particularly for fallen fruits. In these cases, all measurements were confined to a visually homo geneous region of the fruit. Wet masses of the exocarp (skin), mesocarp (pulp), and endocarp (seed) were also measured on twenty ripe fallen fruits. Color reflectance spectra, puncture resistance, sugar content of the pulp, and ethanol concentration of the pulp were measured on all collected fruits. Reflectance spectra of the skins were determined using a portable spectroradiometer (Colortron II; Lightsource)

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