© 2004 by The Society for Integrative and Comparative Biology
The Possible Roles of Ethanol in the Relationship Between Plants and Frugivores: First Experiments with Egyptian Fruit Bats1
1 Mitrani Department of Desert Ecology, Jacob Blaustein Institute for Desert Research, Ben-Gurion University of the Negev, 84990 Midreshet Ben-Gurion, Israel
2 Department of Integrative Biology, University of California, Berkeley, California 94720
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In this paper we discuss how yeast, fungi ubiquitously present in sugar-rich fruit, can influence the interaction between frugivores and fleshy-fruited plants via ethanol. We suggest that plants, the seeds of which are mostly dispersed by vertebrates, exploit the ethanol from alcoholic fermentation by yeast in their seed dispersal strategy. Moderate consumption of ethanol, i.e., at concentrations close to those in naturally ripening fruit, by frugivores may have beneficial short- and long-term effects for these potential dispersers, whereas consumption of larger quantities may have negative short- and long-term effects. Ethanol vapor emanating from palatable fruit may act as an odor cue, guiding bats and other frugivores to the fruit, and aiding them to assess its quality. In addition, we suggest that ingested ethanol may be an appetitive stimulant. We also evaluate the possibility that ethanol within fruit may be used as a source of energy by frugivorous vertebrates. Our preliminary data indicate that Egyptian fruit bats (Rousettus aegyptiacus) can use the odor of ethanol to assess food suitability, but also that it may not serve as an attractant over short distances (i.e., <1 m). Instead, ethanol is avoided at concentrations greater than 1%, a value which might typically characterize overripe and otherwise unpalatable fruit. Our initial results further indicate that Egyptian fruit bats significantly decrease their food consumption if it contains 1 or 2% ethanol. Overall, ethanol may play diverse roles in the nutritional ecology and behavior of fruit-eating bats, and in the interaction between frugivores and plants, in general.
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INTRODUCTION |
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Ethanol is a common molecule in biological systems, being the end product of anaerobic metabolism (i.e., alcoholic fermentation) in unicellular organisms and multicellular organisms including angiosperms, and some invertebrate and fish species (reviewed by van Waarde, 1991
). In plants, ethanol is produced in seeds with an oxygen-impermeable testa, root tips, and the deep tissues of ripening fruit where there is a high demand for oxygen (Cossins, 1978; Zemlianukhin and Ivanov, 1978; Knee, 1991). The ethanol content of ripening fruit is augmented by the action of microorganisms which use sugars present in fruit as a source of energy (Boekhout and Phaff, 2003). Therefore, animals that eat fruit as an important part of their diet may also consume significant amounts of ethanol. To date, the consequences of exposure to dietary ethanol have not been systematically investigated, and it is not clear whether ethanol emitted from fruit can affect the behavior of frugivorous animals.
Ethanol might have both negative and positive effects on fruit-eating animals. On the one hand, an animal cannot allow ethanol to reach high concentrations in its body, since it may have toxic effects (van Waarde, 1991) which would leave the animal vulnerable to predation (Janzen, 1977). Studies on alcohol consumption in humans have shown that short- and long-term exposure to high concentrations of ethanol have pathological effects on the central nervous system and digestive system (Taylor, 1989; Lieber, 2000). On the other hand, there are data suggesting that ingestion of moderate amounts of ethanol has long-term positive effects in Drosophila. Moreover, ethanol may be a hormetic substance for modern humans (see discussion in Dudley, 2000, 2002). Dudley (2000, 2002) hypothesized that ethanol may also have short-term positive effects on frugivores. Specifically, ethanol may be used as an odor cue to localize fruit crops, and may function as an appetitive stimulant, facilitating greater consumption of transient nutritional resources. For example, fruit flies (Drosophila spp.) fly upwind, tracking ethanol plumes to locate suitable oviposition sites (Hoffman and Parsons, 1984). In rats, odor manipulation and olfactectomy influence locomotor activity and preference for high concentrations of alcohol (Morrow et al., 1993; Myers et al., 1997). Human behavioral responses to ethanol can similarly be manipulated via olfactory stimulation before imbibition (Drummond and Glautier, 1994).
It has been suggested that fermentation by particular yeasts or bacteria does not necessarily decrease fruit palatability, but could even increase it (Whiting, 1975). For instance, in humans, alcoholic apéritifs can stimulate food intake (Westerterp-Plantenga and Verwegen, 1999; Caton et al., 2004). It is also known that alcohol ingestion in humans is intimately associated with feeding behavior, including extended meal duration and larger meal size (Poppitt et al., 1996). Ethanol may also be a source of energy. If Dudley's hypotheses (2000, 2002) are correct, the presence of ethanol in fruit may have important consequences not only for frugivores, but also for fruit-bearing plants (see also Levey, 2004).
The aim of this paper is to discuss how yeasts, via the ethanol they produce, may influence the interaction between frugivores and the plants they consume. We do this by considering the possible short-term effects of ethanol as suggested by Dudley (2000, 2002) for frugivorous mammals. In additions, we present initial data from two experiments designed to evaluate whether Egyptian fruit bats (Rousettus aegyptiacus) use ethanol emitted from fruit as an odor cue, and whether the quantity of food consumed by these bats is affected by the concentration of ethanol in the food; we present data on ethanol content in wild fruits consumed by Egyptian fruit bats and birds; and we assess the possibility that frugivorous vertebrates use ethanol as a source of energy.
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PLANT-FRUGIVORE INTERACTIONS MEDIATED BY YEAST VIA ETHANOL |
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In the reproductive cycle of angiosperms there are two crucial events: pollination and seed dispersal. Plants invest much energy in mechanisms to improve the success of these events. Indeed, many plants have conscripted the services of animals into their reproductive strategies. In this context, one of the evolutionary challenges for plants is to produce compounds that attract a group of animals to visit their reproductive structures in order to pollinate flowers or to disperse seeds, respectively. For example, some fruits have features in their shape, color and nutritional content that make them attractive to animals and can strongly influence their patterns of food choice (see Fleming, 1991
).
Additional traits are elicited when fruits interact with microorganisms. On the one hand, by metabolizing the nutrients in fruit pulp, microorganisms lower the nutritional quality of the fruit for other consumers. Accordingly, Janzen (1977) hypothesized that vertebrate fruit eaters compete with microorganisms for fruit pulp. However, because of the great variety of microorganisms present in fruit, the associated effects on the interactions between vertebrate frugivores and fruiting plants may also be highly variable. Cipollini and Stiles (1993) found that toxic fungi that grow on fruit, and that are deterrent to frugivores, are inhibited more strongly by chemical defenses produced by fruit than are non-toxic fungi (so-called latent fungi). These authors hypothesized that plants defend fruit less strongly against microorganisms that may have indirect positive effects by deterring other, more destructive microorganisms.
On the other hand, fermentative yeasts are ubiquitous both on and inside fleshy fruit (Spencer and Spencer, 1997). As discussed by Levey (2004), not all yeasts are capable of alcoholic fermentation; nevertheless, more than half of the known species present in fruit are fermentative (Deak, 2003). Moreover, these yeasts typically ferment sugars into ethanol, several other volatile alcohols, and carbon dioxide even in the presence of oxygen, which is curious given the unfavorable energetics of the reaction (De Deken, 1966; Lagunas, 1979, 1986; Barnett et al., 2000). The result is, that as fruit ripens and the concentration of sugars increases, the concentration of alcoholic fermentation products also increases (Dudley, 2002, 2004; Dominy, 2004). After the fruit is completely ripe, the increase of sugars ceases while fermentation continues, increasing until the sugars are depleted. We suggest that at least some species of latent yeasts may have positive effects stemming from their alcoholic fermentation products, which may possess both fungicidal and bactericidal activity (see also Fleet, 2003a, b). In this sense, yeast presence as manifested by the action of ethanol (and possibly other fermentation products) may benefit the interaction of the plant and its possible seed dispersers.
Apparently, since the beginning of vertebrate frugivory with the evolution of fleshy and large diaspores among the angiosperms in the Tertiary age (Collinson and Hooker, 1991), sugars in fruit pulp have been available as a substrate for alcoholic fermentation by fungi (see Ashburner, 1998). Hence, we posit that there is a long historical association between frugivory and ethanol ingestion in frugivorous animals which has led to complex interactions.
Mammalian frugivores generally select ripe fruit (Janzen, 1983, and references therein), implying that in nature frugivorous mammals encounter ethanol within a particular range of concentrations. Therefore, one might expect that frugivorous mammals experience beneficial effects of ethanol while consuming fruit with moderate concentrations of this substance, i.e., at concentrations close to those found in naturally ripening fruit. In contrast, frugivores would experience no effect or negative effects from food containing ethanol at concentrations below and above those present ripe fruit, respectively. Since it would be profitable to a frugivorous mammal to be able to detect ethanol emanating from fruit because this signal would inform about the location and quality of a nutritional reward, we predicted that odor plumes emanating from fruit with ethanol concentrations close to those in ripe fruit will attract frugivorous mammals, whereas odor plumes with ethanol concentrations close to those in unripe, overripe or otherwise unpalatable fruit, will not affect frugivorous mammals, or will be avoided by them. We also predicted that frugivorous vertebrates will have higher food intake when consuming food with ethanol concentrations close to those in ripe fruit relative to consumption of food with concentrations of ethanol below or above those concentrations. If ethanol can lead frugivorous mammals to sources of fruit, and if it can also increase the consumption of fruit (including seeds), then yeast, via ethanol, may be part of the seed dispersal strategy of some plants. Such a conclusion may help to explain, at least in part, why yeasts apparently occur in all fleshy fruit.
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TESTING PREDICTIONS: FIRST EXPERIMENTS WITH EGYPTIAN FRUIT BATS |
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We chose to test our predictions with Egyptian fruit bats (R. aegyptiacus) because fruit-eating bats of the Pteropodidae and Phyllostomidae can use odor cues to find and assess fruit condition (Heithaus et al., 1975
; Laska, 1990; Acharya et al., 1998; Thies et al., 1998; Luft et al., 2003). We expected that fruit-eating bats also use taste to evaluate the nutritional content of the fruit as implied by Thomas (1984), Korine et al. (1996), Courts (1998), Delorme and Thomas (1999), Eby (1998), Ruby et al. (2000) and Herrera et al. (2002).
In order to understand how ethanol may affect the foraging behavior of fruit-eating bats, we first looked at how they search for and select their food. While foraging, frugivorous bats go through various steps. First, they must reach a patch with fruiting plants, then choose a plant, pinpoint a fruit out of several available on a branch or infructescence, and finally handle and ingest or reject that fruit. Since sugars are less volatile than alcohols, frugivorous bats may be sensitive to volatile substances emitted from the fruit that are correlated with its sugar concentration. Odor plumes from ripe fruit, including such low-molecular mass volatile substances as ethanol and other alcohols (Nursten, 1970), possibly act as long-distance signals indicating availability to appropriate consumers. Thus, frugivorous bats could use products of fermentation such as ethanol to locate food patches, a fruiting plant, or a particular fruit, and also to assess fruit palatability. The information provided by the smell of the fruit, together with information concerning its hardness (Dumont, 1999, 2003), precedes a final step in which the animal bites into and tastes the fruit. Since ethanol can be part of the flavor of the fruit, its concentration may stimulate the bat to continue feeding or to reject the fruit, and it may also have a direct physiological effect by stimulating food ingestion.
Initially, we determined what concentrations of ethanol represent "low" or "high" to Egyptian fruit bats. In nature, concentrations of ethanol in fruit consumed by the Egyptian fruit bat range approximately from 0.02 to 0.2% in unripe fruit, and from 0.1 to 0.7% in ripe fruit (Table 1). Thus, we expected that food with ethanol concentrations between 0.1–0.7% will be perceived as attractive to Egyptian fruit bats.
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Ethanol as a short-distance attractant
To determine whether fruit bats perceive ethanol emitted from food as an odor cue, we performed trials in a flight cage. In the cage, we hung six feeders from the roof, placed 40 cm apart in a hexagonal configuration. In each trial, two feeders contained either ethanol in water or mango juice, and an individual bat was allowed to fly around and inspect the feeders. The first feeder selected by a bat was recorded. In total, fifteen fruit bats were used in experiments, although not all were used in all the treatments. This experiment was designed to ascertain whether the odor of ethanol affects the choice of fruits that are close together by fruit bats, i.e., fruit on the same branch of a fruiting plant, or in branches of different trees that are close to one another. Compared to mango juice alone, Egyptian fruit bats were not attracted by ethanol in water alone at any of the concentrations to which they were exposed (0.001%, 0.01%, 0.1% and 1%; Fig. 1). In addition, we found that when feeders contained either ethanol in water or ethanol in mango juice at concentrations exceeding those found in naturally ripe fruit (Table 1), the bats avoided the feeders entirely.
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Ethanol as an appetitive stimulant
We reasoned that the presence of ethanol in fleshy fruits may have a similar effect on the frugivores that eat them, as occurs in humans. We reasoned that if the presence of ethanol in fruit enhanced the fruit bat's appetite, they would eat more fruit, and therefore increase seed dispersal.
We placed eight Egyptian fruit bats in individual cages, and offered them an artificial liquid food, ad libitum. Each trial took two nights: one in which the bats were offered two feeders with artificial food, both without ethanol (control), and a second with food containing concentrations of ethanol bracketing those occurring in naturally ripe fruit (Table 1). The order of the nights and treatments was randomly assigned. Bats significantly decreased food consumption when it contained either 1% or 2% ethanol, from 122 ± 15 (Mean ± SD) g/day for the 0% control to 99 ± 8 g/day for food with 1% ethanol (t = 4.4, df = 7, P < 0.004), and from 93 ± 18 g/day (0% ethanol) to 35 ± 10 g/ day for food with 2% ethanol (t = 17.9, df = 7, P < 0.0001). Food intake at 0.001%, 0.01% ethanol (less than the concentration in ripe fruit, see Table 1) did not differ significantly from food with no ethanol.
These results are consistent with the preliminary results from the odor experiments, and they partially support our predictions. In both experiments, concentrations of ethanol below those characteristic of naturally ripe fruit did not affect the behavior of the bats. Also, in both experiments, concentrations of ethanol above those in ripe fruit were deterrent to the bats. We have yet to test the prediction that ethanol is attractive to fruit bats at concentrations close to those in ripe fruit.
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ETHANOL AS AN ENERGY SOURCE |
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The ethanol molecule itself yields a direct nutritional reward to consumers; the caloric value of ethanol (29.73 kJ/g) is nearly twice that for carbohydrates (17 kJ/g, on average). However, ethanol is probably not of quantitative significance in the total energy budget of frugivorous animals. For example, 100 g of ripe Ficus sycomorus fruit contains 0.7% ethanol (Table 1), and 85% of its dry mass is sugar (Korine et al., 1998
). This 0.7 g of ethanol, if completely metabolized, would release some 20.8 kJ, whereas metabolism of the 13 g of sugar would release about 210 kJ.
Unlike fat and carbohydrates, alcohol cannot be stored in the body, and the relative contribution of alcohol to overall energy balance in humans is still unclear (Jequier, 1999). Several studies suggest that alcohol consumption may increase the risk of positive energy balance and subsequent obesity (Kromhout, 1983). Conversely, epidemiological surveys show a negative association between alcohol consumption and adiposity in humans (Klatsky et al., 1977; Weissfeld et al., 1988). Conversion efficiency of ethanol to metabolizable energy is the same as that for carbohydrates (Westrate et al., 1990; Sonko et al., 1994). Light to moderate amounts of alcohol are efficiently metabolized by the alcohol dehydrogenase (ADH) pathway, whereby a large fraction of alcohol energy content is used for ATP production (Jequier, 1999). The extent to which low-concentration ethanol is used as an energy source by frugivorous animals is unknown.
In conclusion, we suggest that in light of its likely ubiquity at low concentrations in ripening and ripe fruit, ethanol might well serve as an odor cue for vertebrate frugivores in general, and for fruit bats in particular. We also suggest that, as in humans, ingestion of even small quantities of ethanol may enhance appetite in fruit bats, thus indirectly contributing to increased seed dispersal. Finally, and more obviously, the ingested ethanol will contribute to the animal's total energy budget, but not substantially relative to the caloric value of ingested carbohydrates.
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ACKNOWLEDGMENTS |
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We thank Amram Zabari and Anton Fennec for their assistance in capturing and maintaining the Egyptian fruit bats, Prigat International Ltd. for mango juice, and Sulbar Hazor Ltd. for soy protein. We also thank D. Levey for his helpful comments on this manuscript. Supported by US-Israel Binational Science Foundation grant number 2001038 to C.K., B.P. and R.D., and by a student research grant from the Mitrani Department of Desert Ecology to F.S. This is paper number 427 of the MDDE.
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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 Orleans, Louisiana.
2 E-mail: ckorine{at}bgumail.bgu.ac.il
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